Citations of papers with Morpholinos blocking miRNA activity are here.
Morpholino oligos can block the activity of microRNAs. Morpholinos complementary to the miRNA guide strand can block activity of the miRNA. Morpholinos can also block the Drosha or Dicer nucleolytic processing sites of primary miRNA or pre-miRNA. Morpholinos can interfere with miRNA activity when targeted to the miRNA's target site (MRE) on mRNA. Gene Tools assists in targeting 25-base Morpholino oligos to miRNAs, ideally using sequence information from the Sanger Institute's miRBase.
Morpholinos are usually targeted to one of these sites (shown on the lower part of figure below):
Note that Dicer activity is not requred for maturation of all miRNAs. Here is a known case where miRNA maturation is independent of Dicer activity:
Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, Ma E, Mane S, Hannon GJ, Lawson ND, Wolfe SA, Giraldez AJ. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science. 2010 Jun 25;328(5986):1694-8. Epub 2010 May 6.
Morpholinos can also be targeted to the site on an mRNA where a miRNA binds, called the miRNA response element (MRE). Usually these are found in the 3'-UTR of an mRNA. A Morpholino that binds across an MRE is called a target protector. To design target protector Morpholinos, we need about 60 bases of mRNA sequence centered on the MRE, written mostly in upper case but with the bases complementary to the miRNA seed sequence shown in lower case.
References
González-Martínez I, Cerro-Herreros E, Moreno N, García-Rey A, Espinosa-Espinosa J, Carrascosa-Sàez M, Piqueras-Losilla D, Arzumanov A, Seoane-Miraz D, Jad Y, Raz R, Wood MJ, Varela MA, Llamusí B, Artero R. Peptide-conjugated antimiRs improve myotonic dystrophy type 1 phenotypes by promoting endogenous MBNL1 expression. Mol Ther Nucleic Acids. 2023 Sep 5;34:102024. doi: 10.1016/j.omtn.2023.09.001. eCollection 2023 Dec 12.
"Here, we report the design and testing of six CPP-conjugated PMO antimiRs (three against miR-23b and three against miR-218) in DM1 patient-derived myotubes and a DM1 mouse model." Fridrich A, Salinas-Saaverda M, Kozlolvski I, Surm JM, Chrysostomou E, Tripathi AM, Frank U, Moran Y. An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis. Cell Rep. 2023 Sep 5;42(9):113072. doi: 10.1016/j.celrep.2023.113072. Online ahead of print.
"Male adults of the Ncol3::memOrange2 transgenic line ... were spawned and crossed with WT eggs. The gelatinous sack surrounding the eggs was removed using 4% L-Cysteine (Merck Milipore, USA) and followed by microinjecting the zygotes with antisense MOs." Ghersi JJ, Baldissera G, Hintzen J, Luff SA, Cheng S, Xia IF, Sturgeon CM, Nicoli S. Haematopoietic stem and progenitor cell heterogeneity is inherited from the embryonic endothelium. Nat Cell Biol. 2023 Jul 17. doi: 10.1038/s41556-023-01187-9. Online ahead of print.
"To test this hypothesis, we induced transient downregulation of miR-128 in embryos by injecting 0.75 ng of morpholino, which was sufficient to recapitulate the biased expansion of erythroid and lymphoid progenitor cells that we detected in miR-128Δ/Δ" Oda H, Sato Y, Kawashima SA, Fujiwara Y, Pálfy M, Wu E, Vastenhouw NL, Kanai M, Kimura H. Actin filaments accumulated in the nucleus remain in the vicinity of condensing chromosomes in the zebrafish early embryo. Biol Open. 2023 May 15;12(5):bio059783. doi: 10.1242/bio.059783. Epub 2023 May 17.
Fluorochrome-labeled Morpholino used as a diagnostic probe in a zebrafish to visualize transcription of the miRNA mir-430 Qaryoute AA, Fallatah W, Dhinoja S, Raman R, Jagadeeswaran P. Role of MicroRNAs and their Downstream Target Transcription Factors in Zebrafish Thrombopoiesis. Res Sq. 2023 Apr 24:rs.3.rs-2807790. doi: 10.21203/rs.3.rs-2807790/v1. Preprint.
DNA oligos targeting miRNA delivered by Vivo-Morpholino piggyback Wan Y, Slevin E, Koyama S, Huang CK, Shetty AK, Li X, Harrison K, Li T, Zhou B, Lorenzo SR, Zhang Y, Salinas JM, Xu W, Klaunig JE, Wu C, Tsukamoto H, Meng F. miR-34a regulates macrophage-associated inflammation and angiogenesis in alcohol-induced liver injury. Hepatol Commun. 2023 Apr 4;7(4):e0089. doi: 10.1097/HC9.0000000000000089. eCollection 2023 Apr
miR-34a targeted in mouse Slevin E, Wan Y, Harrison K, Zhang Y, Li X, Li T, Lorenzo SR, Xu W, Klaunig JE, Shetty AK, Meng F. microRNA-34a modulates the senescence of activated hepatic stellate cells in alcohol-associated liver injury. FASEB J. 2022;[Epub] doi:10.1096/fasebj.2022.36.S1.R4231
Blocking mmu-miR-34a Holm A, Possovre M-L, Bandarabadi M, Moseholm KF, Justinussen JL, Bozic I, Lemcke R, Arribat Y, Amati F, Silahtaroglu A, Juventin M, Adamantidis A, Tafti M, Kornum BR. The evolutionarily conserved miRNA-137 targets the neuropeptide hypocretin/orexin and modulates the wake to sleep ratio. Proc Nat Acad Sci USA. 2022;117(17):e2112225119 [Epub] doi:10.1073/pnas.2112225119
Blocking dre-miR-137 Sheng J, Gong J, Shi Y, Wang X, Liu D. MicroRNA-22 coordinates vascular and motor neuronal pathfinding via sema4 during zebrafish development. Open Biol. 2022 Apr;12(4):210315. doi: 10.1098/rsob.210315. Epub 2022 Apr 6.
Blocking dre-miR-22a Huang Y, Wang W-F, Huang C-X, Li X-H, Liu H, Wang H-L. miR-731 modulates the zebrafish heart morphogenesis via targeting Calcineurin/Nfatc3a pathway. Biochim Biophys Acta Gen Subj. 2022;1866(6):130133. doi:10.1016/j.bbagen.2022.130133
Blocking dre-miR-731 Magner E, Sandoval-Sanchez P, Kramer AC, Thummel R, Hitchcock PF, Taylor SM. Disruption of miR-18a Alters Proliferation, Photoreceptor Replacement Kinetics, Inflammatory Signaling, and Microglia/Macrophage Numbers During Retinal Regeneration in Zebrafish. Mol Neurobiol. 2022 Mar 4. doi: 10.1007/s12035-022-02783-w. Online ahead of print.
Blocking dre-miR-18a Konrad KD, Song JL. miR-124 regulates Notch and NeuroD1 to mediate transition states of neuronal development. bioRxiv. 2021;[preprint]. doi:10.1101/2021.12.10.471989 Blocking miRNA-124 in a sea urchin Meng L, Yuan L, Ni J, Fang M, Guo S, Cai H, Qin J, Cai Q, Zhang M, Hu F, Ma J, Zhang Y. Mir24-2-5p suppresses the osteogenic differentiation with Gnai3 inhibition presenting a direct target via inactivating JNK-p38 MAPK signaling axis. Int J Biol Sci. 2021 Oct 17;17(15):4238-4253. doi: 10.7150/ijbs.60536. eCollection 2021.
Mir24-2-5p knockdown with a Morpholino. Magner E, Sandoval-Sanchez P, Kramer AC, Thummel R, Hitchcock PF, Taylor SM. The microRNA miR-18a links proliferation and inflammation during photoreceptor regeneration in the injured zebrafish retina. bioRxiv. 2021;[preprint] doi:10.1101/2021.04.25.441353
Dre-miR-18a knockdown with a Morpholino. Falcao MAP, Walker COB, Disner GR, Batista-Filho J, Soares ABS, Balan-Lima L, Lima C, Lopes-Ferreira M. Knockdown of miR-26a in Zebrafish Leads to Impairment of the Anti-Inflammatory Function of TnP in the Control of Neutrophilia. Fish Shellfish Immunol. 2021;[Epub] doi:10.1016/j.fsi.2021.04.029 Sheng J, Gong J, Shi Y, Wang X, Liu D. Blood vessels regulate primary motor neuronal pathfinding in zebrafish via exosome contained microRNA-22. bioRxiv. 2021;[preprint] doi:10.1101/2021.04.29.441918 Zhang H-Y, Liang H-X, Wu S-H, Jiang H-Q, Wang Q, Yu Z-J. Overexpressed Tumor Suppressor Exosomal miR-15a-5p in Cancer Cells Inhibits PD1 Expression in CD8+T Cells and Suppresses the Hepatocellular Carcinoma Progression. Front Oncol. 2021;11:440. doi:10.3389/fonc.2021.622263 Li X, Gao Y, Tian F, Du R, Yuan Y, Li P, Liu F, Wang C. miR-31 promotes neural stem cell proliferation and restores motor function after spinal cord injury. Exp Biol Med (Maywood). 2021 Mar 9:1535370221997071. doi: 10.1177/1535370221997071. Online ahead of print. miR-31 in zebrafish Sengupta K, Loro E, Khurana TS. PMO-based let-7c site blocking oligonucleotide (SBO) mediated utrophin upregulation in mdx mice, a therapeutic approach for Duchenne muscular dystrophy (DMD). Sci Rep. 2020;10(1):21492. doi:10.1038/s41598-020-76338-1
Target protectors for utrophin Kang T, Quarton T, Nowak CM, Ehrhardt K, Singh A, Li Y, Bleris L. Robust Filtering and Noise Suppression in Intragenic miRNA-Mediated Host Regulation. iScience. 2020 Sep 21;23(10):101595. doi: 10.1016/j.isci.2020.101595. eCollection 2020 Oct 23.
synthetic miRNA FF3 suppressed in HEK293 reporter cells Vazquez‐Armendariz AI, Heiner M, El Agha E, Salwig I, Hoek A, Hessler MC, Shalashova I, Shrestha A, Carraro G, Mengel JP, Günther A, Morty RE, Vadász I, Schwemmle M, Kummer W, Hain T, Goesmann A, Bellusci S, Seeger W, Braun T, Herold S. Multilineage murine stem cells generate complex organoids to model distal lung development and disease. EMBO J. 2020;e103476 [Epub] doi:10.15252/embj.2019103476
Targeting mmu-miR‐142-3p in murine bronchioalveolar lung organoid culture Adusumilli L, Facchinello N, Teh C, Busolin G, Le TM, Yang H, Beffagna G, Campanaro S, Tam LW, Argenton F, Lim B, Korzh V, Tiso N. miR-7 Controls the Dopaminergic/Oligodendroglial Fate through Wnt/β-catenin Signaling Regulation. Cells. 2020;9(3):2073-4409 doi:10.3390/cells9030711
Morpholinos targeting miR-7a Huang Y, Huang C-X, Wang W-F, Liu H, Wang H-L. Zebrafish miR-462-731 is required for digestive organs development. Comp Biochem Physiol Part D Genomics Proteomics. 2020;[Epub] doi:10.1016/j.cbd.2020.100679.
Morpholino knockdown of miR-462/miR-731 Corradi E, Dalla Costa I, Gavoci A, Iyer A, Roccuzzo M, Otto TA, Oliani E, Bridi S, Strohbuecker S, Santos-Rodriguez G, Valdembri D, Serini G, Abreu-Goodger C, Baudet ML. Axonal precursor miRNAs hitchhike on endosomes and locally regulate the development of neural circuits. EMBO J. 2020 Feb 19:e102513. doi: 10.15252/embj.2019102513. [Epub ahead of print]
Morpholinos blocking pre‐miR‐181a‐1, pre‐miR‐181a‐2, pre‐miR‐181b processing Hoelscher CS, Stich T, Diehm A, Lahm H, Dreßen M, Zhang Z, Neb I, Aherrahrou Z, Erdmann J, Schunkert H, Santamaria G, Cuda G, Gilsbach R, Hein L, Lange R, Hassel D, Krane M, Doppler AS. miR-128a Acts as a Regulator in Cardiac Development by Modulating Differentiation of Cardiac Progenitor Cell Populations. Int J Molec Sci. 2020;21(3);1158. doi:10.3390/ijms21031158
MO-20b, MO-30b, MO-128a morphants Hackett EE, Charles-Messance H, O’Leary SM, Gleeson LE, Muñoz-Wolf N, Case S, Wedderburn A, Johnston DGW, Williams MA, Smyth A, Ouimet M, Moore KJ, Lavelle EC, Corr SC, Gordon SV, Keane J, Sheedy FJ. Mycobacterium tuberculosis Limits Host Glycolysis and IL-1β by Restriction of PFK-M via MicroRNA-21. Cell Rep. 2020;30(1):124-36.e4. doi:10.1016/j.celrep.2019.12.015.
Target protector Wang D, Weng Y, Guo S, Qin W, Ni J, Yu L, Zhang Y, Zhao Q, Ben J, Ma J. microRNA-1 Regulates NCC Migration and Differentiation by Targeting sec63. Int J Biol Sci. 2019;15(12):2538-2547. doi:10.7150/ijbs.35357
Morpholino targeting dre-miR-1 de Morree A, Klein JDD, Gan Q, Farup J, Urtasun A, Kanugovi A, Bilen B, van Velthoven CTJ, Quarta M, Rando TA. Alternative polyadenylation of Pax3 controls muscle stem cell fate and muscle function. Science. 2019 Nov 8;366(6466):734-738. doi: 10.1126/science.aax1694.
Morpholino targeting miR-206 Guzzolino E, Pellegrino M, Ahuja N, Garrity D, D'Aurizio R, Groth M, Baumgart M, Hatcher CJ, Mercatanti A, Evangelista M, Ippolito C, Tognoni E, Fukuda R, Lionetti V, Pellegrini M, Cremisi F, Pitto L. miR-182-5p is an evolutionarily conserved Tbx5 effector that impacts cardiac development and electrical activity in zebrafish. Cell Mol Life Sci. 2019 Nov 4. doi: 10.1007/s00018-019-03343-7. [Epub ahead of print]
Morpholino targeting miR-182 Duan F-G, Wang M-F, Cao Y-B, Li D, Li R-Z, Fan X-X, Khan I, Lai H-L, Zhang Y-Z, Hsiao WW-L, Yao X-J, Wu Q-B, Liu L, Tang I-J, Leung EL-H. MicroRNA-421 confers paclitaxel resistance by binding to the KEAP1 3′UTR and predicts poor survival in non-small cell lung cancer. Cell Death Dis. 2019;10:821. doi:10.1038/s41419-019-2031-1
miR-421 in mouse xenografts, intratumoral injection Sharma P, Gupta S, Chaudhary M, Mitra S, Chawla B, Khursheed MA, Ramachandran R. Oct4 mediates Müller glia reprogramming and cell cycle exit during retina regeneration in zebrafish. Life Sci Alliance. 2019 Oct 8;2(5). pii: e201900548. doi: 10.26508/lsa.201900548. Print 2019 Oct.
zebrafish ocular injection then electroporation:
dre-miR-200A, dre-miR-200b, dre-miR-143, dre-miR-145 Jung HM, Hu CT, Fister AM, Davis AE, Castranova D, Pham VN, Price LM, Weinstein BM. MicroRNA-mediated control of developmental lymphangiogenesis. eLife. 2019;8:e46007. doi: 10.7554/eLife.46007
dre-mir-204 Wade SM, Ohnesorge N, McLoughlin H, Biniecka M, Carter SP, Trenkman M, Cunningham CC, McGarry T, Canavan M, Kennedy BN, Veale DJ, Fearon U. Dysregulated miR-125a promotes angiogenesis through enhanced glycolysis. EBioMedicine. 2019;[Epub ahead of print] doi:10.1016/j.ebiom.2019.08.043
targeting dre-miR-125a Mukherjee S, Akbar I, Kumari B, Vrati S, Basu A, Banerjee A. Japanese Encephalitis Virus-induced let-7a/b interacted with the NOTCH-TLR7 pathway in microglia and facilitated neuronal death via caspase activation. J Neurochem. 2018 Dec 17. doi: 10.1111/jnc.14645. [Epub ahead of print]
Let7 miRNA knockdown with Vivo-Morpholino in mouse brain Watterston C, Zeng L, Onabadejo A, Childs SJ. MicroRNA26 attenuates vascular smooth muscle maturation via endothelial BMP signalling. PLoS Genet. 2019 May 15;15(5):e1008163. doi: 10.1371/journal.pgen.1008163. [Epub ahead of print]
dre-miR-26a knockdown Indrieri A, Carrella S, Romano A, Spaziano A, Marrocco E, Fernandez‐Vizarra E, Barbato S, Pizzo M, Ezhova Y, Golia FM, Ciampi L, Tammaro R, Henao‐Mejia J, Williams A, Flavell RA, De Leonibus E, Zeviani M, Surace EM, Banfi S, Franco B. miR‐181a/b downregulation exerts a protective action on mitochondrial disease models. EMBO Molec Med. 2019;e8734 [Epub ahead of print] doi:10.15252/emmm.201708734
dre-miR-181 knockdown Remsburg C, Konrad K, Sampilo NF, Song JL. Analysis of microRNA functions. Methods Cell Biol. 2019;151:323-334. doi: 10.1016/bs.mcb.2018.10.005. Epub 2018 Dec 11.
Target protector discussion Shrestha A, Carraro G, Nottet N, Vazquez-Armendariz AI, Susanne Herold S, Cordero J, Singh I, Jochen Wilhelm J, Barreto G, Morty R, El Agha E, Mari B, Chen C, Jin-San Zhang J-S, Chao C-M, Bellusci S. A critical role for miR-142 in alveolar epithelial lineage formation in mouse lung development. Cell Molec Life Sci. 2019;[Epub] doi:10.1007/s00018-019-03067-8 Jung HM, Hu C, Fister AM, Davis AE, Castranova D, Pham VN, Price LM, Weinstein BM. MicroRNA-mediated control of developmental lymphangiogenesis. bioRxiv. 2019;[preprint] doi:10.1101/555664
Morpholinos blocking dre-miR-204 Yin Y, Xu L, Chang Y, Zeng T, Chen X, Wang A, Groth J, Foo WC, Liang C, Hu H, Huang J. N-Myc promotes therapeutic resistance development of neuroendocrine prostate cancer by differentially regulating miR-421/ATM pathway. Mol Cancer. 2019 Jan 18;18(1):11. doi: 10.1186/s12943-019-0941-2.
Vivo-Morpholino targeting miR-421 Corradi E, Gavoci A, Strohbuecker S, Roccuzzo M, Costa ID, Iyer A, Bridi S, Rodriguez GS, Abreu-Goodger C, Baudet M-L. Precursor miRNAs are trafficked along axons associated with vesicles and locally processed to regulate growth cone steering. bioRxive. 2018;[Preprint] doi:10.1101/470393
xla-miR-181a-1, xla-miR-181a-2 Sampilo NF, Stepicheva NA, Zaidi SAM, Wang L, Wu W, Wikramanayake A, Song JL. Inhibition of microRNA suppression of Dishevelled results in Wnt pathway associated developmental defects. Development. 2018 Nov 2. pii: dev.167130. doi: 10.1242/dev.167130. [Epub ahead of print]
Target protectors Huang C-X, Huang Y, Duan X-K, Zhang M, Tu J-P, Liu J-X, Liu H, Chen T-S, Wang W-M, Wang H-L. Zebrafish miR-462-731 regulates hematopoietic specification and pu.1-dependent primitive myelopoiesis. Cell Death Differ. 2018; doi:10.1038/s41418-018-0234-0
dre-miR-462, dre-miR-731 knockdown Lin CY, Zhang PH, Chen YJ, Wu CL, Tsai HJ. Conditional Overexpression of rtn4al in Muscle of Adult Zebrafish Displays Defects Similar to Human Amyotrophic Lateral Sclerosis. Mar Biotechnol (NY). 2018 Nov 15. doi: 10.1007/s10126-018-9857-x. [Epub ahead of print]
dre-miR-206, dre-miR-1 Taylor SM, Giuffre E, Moseley P, Hitchcock PF. The microRNA, miR-18a, regulates NeuroD and photoreceptor differentiation in the retina of the zebrafish. bioRXive. 2018;[Epub] doi:10.1101/440263
dre-miR-18 family knockdowns Du X-f, Xu B, Zhang Y, Chen M-j, Du J-l. A transgenic zebrafish model for in vivo long-term imaging of retinotectal synaptogenesis. Sci Rep. 2018;8:14077. doi:10.1038/s41598-018-32409-y
dre-miR-132 knockdown Leinonen JT, Chen YC, Tukiainen T, Panula P, Widén E. Transient modification of lin28b expression - Permanent effects on zebrafish growth. Mol Cell Endocrinol. 2018 Sep 6. pii: S0303-7207(18)30263-6. doi: 10.1016/j.mce.2018.09.001. [Epub ahead of print]
zebrafish lin28b target Romney ALT, Podrabsky JE. Small noncoding RNA profiles along alternative developmental trajectories in an annual killifish. Sci Rep. 2018;8:13364. doi:10.1038/s41598-018-31466-7
alim-miR-430a knockdown Vergara HM, Ramirez J, Rosing T, Nave C, Blandino R, Saw D, Saraf P, Piexoto G, Coombes C, Adams M, Domingo CR. miR-206 is required for changes in cell adhesion that drive muscle cell morphogenesis in Xenopus laevis. Dev Biol. 2018;[Epub ahead of print] doi:10.1016/j.ydbio.2018.03.021 Cao H, Shi J, Du J, Chen K, Dong C, Jiang D, Jiang H. MicroRNA-194 Regulates the Development and Differentiation of Sensory Patches and Statoacoustic Ganglion of Inner Ear by Fgf4. Med Sci Monit. 2018 Mar 23;24:1712-1723. Kontarakis Z, Rossi A, Ramas S, Dellinger MT, Stainier DYR. Mir-126 is a conserved modulator of lymphatic development. Dev Biol. 2018 Mar 14. pii: S0012-1606(18)30138-6. doi: 10.1016/j.ydbio.2018.03.006. [Epub ahead of print] Madelaine R, Notwell JH, Skariah G, Halluin C, Chen CC, Bejerano G, Mourrain P. A screen for deeply conserved non-coding GWAS SNPs uncovers a MIR-9-2 functional mutation associated to retinal vasculature defects in human. Nucl Acids Res. 2018;[Epub ahead of print] doi:10.1093/nar/gky166
Targeting dre-miR-9 Kim CW, Han JH, Wu L, Choi JY. microRNA-183 is Essential for Hair Cell Regeneration after Neomycin Injury in Zebrafish. Yonsei Med J. 2018 Jan;59(1):141-147. doi: 10.3349/ymj.2018.59.1.141.
Targeting dre-miR-183 Lin CY, He JY, Zeng CW, Loo MR, Chang WY, Zhang PH, Tsai HJ. microRNA-206 modulates an Rtn4a/Cxcr4a/Thbs3a axis in newly forming somites to maintain and stabilize the somite boundary formation of zebrafish embryos. Open Biol. 2017 Jul;7(7). pii: 170009. doi: 10.1098/rsob.170009. Wu Y, Lou QY, Ge F, Xiong Q. Quantitative Proteomics Analysis Reveals Novel Targets of miR-21 in Zebrafish Embryos. Sci Rep. 2017 Jun 22;7(1):4022. doi: 10.1038/s41598-017-04166-x.
Blocking miR-21 in zebrafish Kara N, Wei C, Commanday AC, Patton JG. miR-27 regulates chondrogenesis by suppressing focal adhesion kinase during pharyngeal arch development. Dev Biol. 2017 Jun 16. pii: S0012-1606(16)30850-8. doi: 10.1016/j.ydbio.2017.06.013. [Epub ahead of print]
Blocking miR-132 in zebrafish Hall C, Ehrlich L, Meng F, Invernizzi P, Bernuzzi F, Lairmore TC, Alpini G, Glaser S. Inhibition of microRNA-24 increases liver fibrosis by enhanced menin expression in Mdr2-/- mice. J Surg Res. 2017 May 11. pii: S0022-4804(17)30273-1. doi: 10.1016/j.jss.2017.05.020. [Epub ahead of print]
Vivo-Morpholino inhibiting mmu-miR-24 Xu B, Zhang Y, Du XF, Li J, Zi HX, Bu JW, Yan Y, Han H, Du JL. Neurons secrete miR-132-containing exosomes to regulate brain vascular integrity. Cell Res. 2017 Apr 21. doi: 10.1038/cr.2017.62. [Epub ahead of print]
Blocking miR-132 in zebrafish Flynt AS, Rao M, Patton JG. Blocking Zebrafish MicroRNAs with Morpholinos. Methods Mol Biol. 2017;1565:59-78. doi: 10.1007/978-1-4939-6817-6_6. Hazra B, Kumawat KL, Basu A. The host microRNA miR-301a blocks the IRF1-mediated neuronal innate immune response to Japanese encephalitis virus infection. Sci Signal. 2017;10(466):eaaf5185. doi:10.1126/scisignal.aaf5185
BALB/c mice, intracranially treated with a Vivo-Morpholino targeting miR-301a Bellon A, Iyer A, Bridi S, Lee FC, Ovando-Vázquez C, Corradi E, Longhi S, Roccuzzo M, Strohbuecker S, Naik S, Sarkies P, Miska E, Abreu-Goodger C, Holt CE, Baudet ML. miR-182 Regulates Slit2-Mediated Axon Guidance by Modulating the Local Translation of a Specific mRNA. Cell Rep. 2017 Jan 31;18(5):1171-1186. doi: 10.1016/j.celrep.2016.12.093.
Targeting mir-182 in Xenopus laevis. Hung IC, Hsiao YC, Sun HS, Chen TM, Lee SJ. MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae. BMC Genomics. 2016 Nov 15;17(1):922.
Targeting dre-mir-29b. Chang RM, Xiao S, Lei X, Yang H, Fang F, Yang LY. miRNA-487a Promotes Proliferation and Metastasis in Hepatocellular Carcinoma. Clin Cancer Res. 2016 Nov 8. pii: clincanres.0851.2016. [Epub ahead of print]
miRNA-487a targeted with a Vivo-Morpholino in mice. Katz S, Cussigh D, Urbán N, Blomfield I, Guillemot F, Bally-Cuif L, Coolen M. A Nuclear Role for miR-9 and Argonaute Proteins in Balancing Quiescent and Activated Neural Stem Cell States. Cell Rep. 2016 Oct 25;17(5):1383-1398. doi: 10.1016/j.celrep.2016.09.088. Benz A, Kossack M, Auth D, Seyler C, Zitron E, Juergensen L, Katus HA, Hassel D. miR-19b Regulates Ventricular Action Potential Duration in Zebrafish. Sci Rep. 2016 Nov 2;6:36033. doi: 10.1038/srep36033. Presslauer C, Bizuayehu TT, Razmi K, Fernandes JM, Babiak I. See-Thru-Gonad zebrafish line: developmental and functional validation. Reproduction. 2016 Nov;152(5):507-17. doi: 10.1530/REP-16-0328.
Vivo-Morpholino injection into developing zebrafish ovaries to block miR-92a-3p Li Y, Huang C, Feng P, Jiang Y, Wang W, Zhou D, Chen L. Aberrant expression of miR-153 is associated with overexpression of hypoxia-inducible factor-1α in refractory epilepsy. Sci Rep. 2016 Aug 24;6:32091. doi: 10.1038/srep32091. Targeting miR-153 in rat astrocytes Hildyard JC, Wells DJ. Investigating Synthetic Oligonucleotide Targeting of Mir31 in Duchenne Muscular Dystrophy. PLoS Curr. 2016 Jun 16;8. pii: ecurrents.md.99d88e72634387639707601b237467d7. doi: 10.1371/currents.md.99d88e72634387639707601b237467d7.
sponges, star sequence targets, target protectors Giacomotto J, Carroll AP, Rinkwitz S, Mowry B, Cairns MJ, Becker TS. Developmental suppression of schizophrenia-associated miR-137 alters sensorimotor function in zebrafish. Transl Psychiatry. 2016 May 24;6:e818. doi: 10.1038/tp.2016.88. Wang X, Ling CC, Li L, Qin Y, Qi J, Liu X, You B, Shi Y, Zhang J, Jiang Q, Xu H, Sun C, You Y, Chai R, Liu D. MicroRNA-10a/10b represses a novel target gene mib1 to regulate angiogenesis. Cardiovasc Res. 2016 Jan 29. pii: cvw023. [Epub ahead of print] Chiavacci E, D'Aurizio R, Guzzolino E, Russo F, Baumgart M, Groth M, Mariani L, D'Onofrio M, Arisi I, Pellegrini M, Cellerino A, Cremisi F, Pitto L. MicroRNA 19a replacement partially rescues fin and cardiac defects in zebrafish model of Holt Oram syndrome. Sci Rep. 2015 Dec 14;5:18240. doi: 10.1038/srep18240. Liu C, Lou CH, Shah V, Ritter R, Talley J, Soibam B, Benham A, Zhu H, Perez E, Shieh YE, Gunaratne PH, Sater AK. Identification of microRNAs and microRNA Targets in Xenopus gastrulae: The role of miR-26 in the regulation of Smad1. Dev Biol. 2015 Nov 5. pii: S0012-1606(15)30277-3. doi: 10.1016/j.ydbio.2015.11.005. [Epub ahead of print] Target protector Morpholino Singh BN, Kawakami Y, Akiyama R, Rasmussen TL, Garry MG, Gong W, Das S, Shi X, Koyano-Nakagawa N, Garry DJ. The Etv2-miR-130a Network Regulates Mesodermal Specification. Cell Rep. 2015 Nov 3;13(5):915-23. doi: 10.1016/j.celrep.2015.09.060. Epub 2015 Oct 22. Stepicheva NA, Song JL. microRNA-31 modulates skeletal patterning in the sea urchin embryo. Development. 2015 Nov 1;142(21):3769-80. doi: 10.1242/dev.127969. Epub 2015 Sep 23.
Target protector Morpholinos Kiesow K, Bennewitz K, Miranda LG, Stoll SJ, Hartenstein B, Angel P, Kroll J, Schorpp-Kistner M. Junb controls lymphatic vascular development in zebrafish via miR-182. Sci Rep. 2015 Oct 13;5:15007. doi: 10.1038/srep15007. Chevalier B, Adamiok A, Mercey O, Revinski DR, Zaragosi LE, Pasini A, Kodjabachian L, Barbry P, Marcet B. miR-34/449 control apical actin network formation during multiciliogenesis through small GTPase pathways. Nat Commun. 2015 Sep 18;6:8386. doi: 10.1038/ncomms9386.
Direct miRNA binding Morpholinos and target protectors. Morris JF, Chomyk A, Song P, Parker N, Deckard S, Trapp BD, Pimplikar SW, Dutta R. Decrease in levels of the evolutionarily conserved microRNA miR-124 affects oligodendrocyte numbers in Zebrafish, Danio rerio. Invert Neurosci. 2015;15:4 doi:10.1007/s10158-015-0180-1 Conte I, Hadfield KD, Barbato S, Carrella S, Pizzo M, Bhat RS, Carissimo A, Karali M, Porter LF, Urquhart J, Hateley S, O'Sullivan J, Manson FD, Neuhauss SC, Banfi S, Black GC. MiR-204 is responsible for inherited retinal dystrophy associated with ocular coloboma. Proc Natl Acad Sci U S A. 2015 Jun 8. pii: 201401464. [Epub ahead of print] Wang K, Liu CY, Zhou LY, Wang JX, Wang M, Zhao B, Zhao WK, Xu SJ, Fan LH, Zhang XJ, Feng C, Wang CQ, Zhao YF, Li PF. APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p. Nat Commun. 2015 Apr 10;6:6779. doi: 10.1038/ncomms7779. Geiger SS, Hokamp K, Reilly MP, Coogan AN, Vigorito E, FitzGerald GA, O'Neill LA. Circadian control of innate immunity in macrophages by miR-155 targeting Bmal1. Proc Natl Acad Sci U S A. 2015 May 20. pii: 201501327. [Epub ahead of print]
two target protectors for mmu-miR-155 binding sites in Bmal1 Carrella S, D'Agostino Y, Barbato S, Huber-Reggi SP, Salierno FG, Manfredi A, Neuhauss SC, Banfi S, Conte I. miR-181a/b control the assembly of visual circuitry by regulating retinal axon specification and growth. Dev Neurobiol. 2015 Feb 27. doi: 10.1002/dneu.22282. [Epub ahead of print]
Target protector Makino S, Mishima Y, Inoue K, Inada T. Roles of mRNA fate modulators Dhh1 and Pat1 in TNRC6-dependent gene silencing recapitulated in yeast. J Biol Chem. 2015 Mar 27;290(13):8331-47. doi: 10.1074/jbc.M114.615088. Epub 2015 Feb 5. Ristori E, Lopez-Ramirez MA, Narayanan A, Hill-Teran G, Moro A, Calvo C-F, Thomas J-L, Nicoli S. A Dicer-miR-107 Interaction Regulates Biogenesis of Specific miRNAs Crucial for Neurogenesis. Dev Cell. 2015;[Epub ahead of print] doi:10.1016/j.devcel.2014.12.013 Olena AF, Rao MB, Thatcher EJ, Wu SY, Patton JG. miR-216a regulates snx5, a novel notch signaling pathway component, during zebrafish retinal development. Dev Biol. 2015 Apr 1;400(1):72-81. doi: 10.1016/j.ydbio.2015.01.016. Epub 2015 Jan 31. Song B, Zhang Q, Zhang Z, Wan Y, Jia Q, Wang X, Zhu X, Leung A Y-H, Cheng T, Fang X, Yuan W, Jia H. Systematic transcriptome analysis of the zebrafish model of diamond-blackfan anemia induced by RPS24 deficiency. BMC Genomics. 2014;15:759. doi:10.1186/1471-2164-15-759 Feng Y, Gross S, Wolf NM, Butenschön VM, Qiu Y, Devraj K, Liebner S, Kroll J, Skolnik EY, Hammes H-P, Wieland T. Nucleoside Diphosphate Kinase B Regulates Angiogenesis Through Modulation of Vascular Endothelial Growth Factor Receptor Type 2 and Endothelial Adherens Junction Proteins. Arterioscler Thromb Vasc Biol. 2014;[Epub ahead of print] doi:10.1161/ATVBAHA.114.304239 Salta E, Lau P, Frigerio CS, Coolen M, Bally-Cuif L, De Strooperemail B. A Self-Organizing miR-132/Ctbp2 Circuit Regulates Bimodal Notch Signals and Glial Progenitor Fate Choice during Spinal Cord Maturation. Dev Cell. 2014;[Epub ahead of print] doi:10.1016/j.devcel.2014.07.006 Francis H, McDaniel K, Han Y, Liu X, Kennedy L, Yang F, McCarra J, Zhou T, Glaser S, Venter J, Huang L, Levine P, Lai J-M, Liu C-G, Alpini G, Meng F. Regulation of the extrinsic apoptotic pathway by microRNA-21 in alcoholic liver injury. J Biol Chem. 2014;[Epub ahead of print] doi:10.1074/jbc.M114.602383 Tsai P-C, Bake S, Balaraman S, Rawlings J, Holgate RR, Dubois D, Miranda RC. MiR-153 targets the nuclear factor-1 family and protects against teratogenic effects of ethanol exposure in fetal neural stem cells. Biology Open. 2014;[Epub] doi:10.1242/bio.20147765
miRNA target protectors Conte I, Merella S, Garcia-Manteiga JM, Migliore C, Lazarevic D, Carrella S, Marco-Ferreres R, Avellino R, Davidson NP, Emmett W, Sanges R, Bockett N, Van Heel D, Meroni G, Bovolenta P, Stupka E, Banfi S. The combination of transcriptomics and informatics identifies pathways targeted by miR-204 during neurogenesis and axon guidance. Nucleic Acids Res. 2014 Aug 1;42(12):7793-806. doi: 10.1093/nar/gku498. Epub 2014 Jun 3. Rajaram K, Harding RL, Hyde DR, Patton JG. miR-203 regulates progenitor cell proliferation during adult zebrafish retina regeneration. Dev Biol. 2014 May 20. pii: S0012-1606(14)00260-7. doi: 10.1016/j.ydbio.2014.05.005. [Epub ahead of print] Song R, Walentek P, Sponer N, Klimke A, Lee JS, Dixon G, Harland R, Wan Y, Lishko P, Lize M, Kessel M, He L. miR-34/449 miRNAs are required for motile ciliogenesis by repressing cp110. Nature. 2014;510:115-20 doi:10.1038/nature13413
knockdowns of miR-34b, miR-449a in Xenopus laevis Conte I, Merella S, Garcia-Manteiga JM, Migliore C, Lazarevic D, Carrella S, Marco-Ferreres R, Avellino R, Davidson NP, Emmett W, Sanges R, Bockett N, Van Heel D, Meroni G, Bovolenta P, Stupka E, Banfi S. The combination of transcriptomics and informatics identifies pathways targeted by miR-204 during neurogenesis and axon guidance. Nucl Acids Res. 2014;[Epub ahead of print] doi:10.1093/nar/gku498
miR-204 knockdown in Medaka Joshi HP, Subramanian IV, Schnettler EK, Ghosh G, Rupaimoole R, Evans C, Saluja M, Jing Y, Cristina I, Roy S, Zeng Y, Shah VH, Sood AK, Ramakrishnan S. Dynamin 2 along with microRNA-199a reciprocally regulate hypoxia-inducible factors and ovarian cancer metastasis. PNAS. 2014;[Epub ahead of print] doi:10.1073/pnas.1317242111 Targeting miR-199a in cultured cells Carraro G, Shrestha A, Rostkovius J, Contreras A, Chao CM, El Agha E, Mackenzie B, Dilai S, Guidolin D, Taketo MM, Günther A, Kumar ME, Seeger W, De Langhe S, Barreto G, Bellusci S. miR-142-3p balances proliferation and differentiation of mesenchymal cells during lung development. Development. 2014 Feb 19. [Epub ahead of print]
Vivo-Morpholinos targeting mmu-miR-126,mmu-miR-miR-142-3p, and mmu-miR-144 in mouse lung explants. Glaser S, Meng F, Han Y, Onori P, Chow BK, Francis H, Venter J, McDaniel K, Marzioni M, Invernizzi P, Ueno Y, Lai JM, Huang L, Standeford H, Alvaro D, Gaudio E, Franchitto A, Alpini G. Secretin Stimulates Biliary Cell Proliferation by Regulating Expression of MicroRNA 125b and MicroRNA let7a in Mice. Gastroenterology. 2014 Feb 25. pii: S0016-5085(14)00241-8. doi: 10.1053/j.gastro.2014.02.030. [Epub ahead of print]
Vivo-Morpholino tail-vein injections into mice, oligos targeting microRNAs mmu-miR-125b or mmu-miR-let7 Lou CH, Shao A, Shum EY, Espinoza JL, Huang L, Karam R, Wilkinson MF. Posttranscriptional Control of the Stem Cell and Neurogenic Programs by the Nonsense-Mediated RNA Decay Pathway. Cell Rep. 2014;[Epub ahead of print] doi:10.1016/j.celrep.2014.01.028
miR-128 target protectors on Upf1 transcript Ben-Moshe Z, Alon S, Mracek P, Faigenbloom L, Tovin A, Vatine GD, Eisenberg E, Foulkes NS, Gothilf Y. The light-induced transcriptome of the zebrafish pineal gland reveals complex regulation of the circadian clockwork by light. Nucl Acids Res. 2014;[Epub ahead of print] doi:10.1093/nar/gkt1359
Targeting dre-miR-183. Velu CS, Chaubey A, Phelan JD, Horman SR, Wunderlich M, Guzman ML, Jegga AG, Zeleznik-Le NJ, Chen J, Mulloy JC, Cancelas JA, Jordan CT, Aronow BJ, Marcucci G, Bhat B, Gebelein B, Grimes HL. Therapeutic antagonists of microRNAs deplete leukemia-initiating cell activity. J Clin Invest. 2014 Jan 2;124(1):222-36. doi: 10.1172/JCI66005. Epub 2013 Dec 16. Lu X, Li X, He Q, Gao J, Gao Y, Liu B, Liu F. miR-142-3p regulates the formation and differentiation of hematopoietic stem cells in vertebrates. Cell Res. 2013 Dec;23(12):1356-68. doi: 10.1038/cr.2013.145. Epub 2013 Oct 29. Lin CY, Lee HC, Fu CY, Ding YY, Chen JS, Lee MH, Huang WJ, Tsai HJ. miR-1 and miR-206 target different genes to have opposing roles during angiogenesis in zebrafish embryos. Nat Commun. 2013 Nov 22;4:2829. doi: 10.1038/ncomms3829.
Targeting miRNA and a target protector in zebrafish Anton L, Olarerin-George AO, Schwartz N, Srinivas S, Bastek J, Hogenesch JB, Elovitz MA. miR-210 inhibits trophoblast invasion and is a serum biomarker for preeclampsia. Am J Pathol. 2013 Nov;183(5):1437-45. doi: 10.1016/j.ajpath.2013.07.021. Epub 2013 Sep 10. Ordas A, Kanwal Z, Lindenberg V, Rougeot J, Mink M, Spaink HP, Meijer AH. MicroRNA-146 function in the innate immune transcriptome response of zebrafish embryos to Salmonella typhimurium infection. BMC Genomics. 2013;14:696 doi:10.1186/1471-2164-14-696 Targeting dre-miR-146a, dre-miR-146b Franzosa JA, Bugel SM, Tal TL, La Du JK, Tilton SC, Waters KM, Tanguay RL. Retinoic acid-dependent regulation of miR-19 expression elicits vertebrate axis defects. FASEB J. 2013 Aug 23. [Epub ahead of print] Nimmo R, Ciau-Uitz A, Ruiz-Herguido C, Soneji S, Bigas A, Patient R, Enver T. MiR-142-3p controls the specification of definitive hemangioblasts during ontogeny. Dev Cell. 2013 Aug 12;26(3):237-49. doi: 10.1016/j.devcel.2013.06.023. Epub 2013 Aug 1. Wang K, Liu F, Zhou LY, Ding SL, Long B, Liu CY, Sun T, Fan YY, Sun L, Li PF. miR-874 regulates myocardial necrosis by targeting caspase-8. Cell Death Dis. 2013 Jul 4;4:e709. doi: 10.1038/cddis.2013.233.
Target protectors delivered in mouse primary cardiomyocytes using Endo-Porter Lin C-Y, Chen J-S, Loo M-R, Hsiao C-C, Chang W-Y, Tsai H-J. MicroRNA-3906 Regulates Fast Muscle Differentiation through Modulating the Target Gene homer-1b in Zebrafish Embryos. PLoS ONE. 2013;8(7):e70187. doi:10.1371/journal.pone.0070187 McCarthy N, Wetherill L, Lovely CB, Swartz ME, Foroud TM, Eberhart JK. Pdgfra protects against ethanol-induced craniofacial defects in a zebrafish model of FASD. Development 2013 140:3254-3265; doi:10.1242/dev.094938
Knockdown of dre-miR-140 by microinjection in zebrafish. Jiang Q, Lagos-Quintana M, Liu D, Shi Y, Helker C, Herzog W, le Noble F. miR-30a Regulates Endothelial Tip Cell Formation and Arteriolar Branching. Hypertension. 2013 Jul 1. [Epub ahead of print] Pappalardo-Carter DL, Balaraman S, Sathyan P, Carter ES, Chen WJ, Miranda RC. Suppression and Epigenetic Regulation of MiR-9 Contributes to Ethanol Teratology: Evidence from Zebrafish and Murine Fetal Neural Stem Cell Models. Alcohol Clin Exp Res. 2013 Jun 25. doi: 10.1111/acer.12139. [Epub ahead of print] Banjo T, Grajcarek J, Yoshino D, Osada H, Miyasaka KY, Kida YS, Ueki Y, Nagayama K, Kawakami K, Matsumoto T, Sato M, Ogura T. Haemodynamically dependent valvulogenesis of zebrafish heart is mediated by flow-dependent expression of miR-21. Nature Comm. 2013;4:article1978 doi:10.1038/ncomms2978
Includes Morpholinos against miR-21-1, miR-21-2, and a target protector. Coinjections of miR-21-1 & miR-21-2 oligos. Ketley A, Warren A, Holmes E, Gering M, Aboobaker AA, Brook JD. The miR-30 MicroRNA Family Targets smoothened to Regulate Hedgehog Signalling in Zebrafish Early Muscle Development. PLoS ONE. 2013;8(6):e65170. doi:10.1371/journal.pone.0065170
dre-miR-30 oligo and a target protector for miR-30 MRE on smoothened Wang L, Fu C, Fan H, Du T, Dong M, Chen Y, Jin Y, Zhou Y, Deng M, Gu A, Jing Q, Liu T, Zhou Y. miR-34b regulates multiciliogenesis during organ formation in zebrafish. Development. 2013 May 22. [Epub ahead of print] Martin NT, Nakamura K, Davies R, Nahas SA, Brown C, Tunuguntla R, Gatti RA, Hu H. ATM-Dependent MiR-335 Targets CtIP and Modulates the DNA Damage Response. PLoS Genet. 2013;9(5):e1003505. doi:10.1371/journal.pgen.1003505
Xu RR, Zhang CW, Cao Y, Wang Q. [mir122 deficiency inhibits differentiation of zebrafish hepatoblast into hepatocyte]. Yi Chuan. 2013 Apr;35(4):488-94. Chinese. Kolpa HJ, Peal DS, Lynch SN, Giokas AC, Ghatak S, Misra S, Norris RA, Macrae CA, Markwald RR, Ellinor P, Bischoff J, Milan DJ. miR-21 represses Pdcd4 during cardiac valvulogenesis. Development. 2013 May;140(10):2172-80. doi: 10.1242/dev.084475. Epub 2013 Apr 11. Riley MF, Bochter MS, Wahi K, Nuovo GJ, Cole SE. Mir-125a-5p-mediated regulation of Lfng is essential for the avian segmentation clock. Dev Cell. 2013 Mar 11;24(5):554-61. doi: 10.1016/j.devcel.2013.01.024.
mir-125a oligo and Lfng 3’UTR target protector. Avellino R, Carrella S, Pirozzi M, Risolino M, Salierno FG, Franco P, Stoppelli P, Verde P, Banfi S, Conte I. miR-204 Targeting of Ankrd13A Controls Both Mesenchymal Neural Crest and Lens Cell Migration. PLoS ONE. 2013;8(4):e61099. doi:10.1371/journal.pone.0061099 Shaham O, Gueta K, Mor E, Oren-Giladi P, Grinberg D, Xie Q, Cvekl A, Shomron N, Davis N, Keydar-Prizant M, Raviv S, Pasmanik-Chor M, Bell RE, Levy C, Avellino R, Banfi S, Conte I, Ashery-Padan R. Pax6 Regulates Gene Expression in the Vertebrate Lens through miR-204. PLoS Genet. 2013;9(3):e1003357. doi:10.1371/journal.pgen.1003357 Wei C, Thatcher EJ, Olena AF, Cha DJ, Perdigoto AL, Marshall AF, Carter BD, Broadie K, Patton JG. miR-153 Regulates SNAP-25, Synaptic Transmission, and Neuronal Development. PLoS One. 2013;8(2):e57080. doi: 10.1371/journal.pone.0057080. Epub 2013 Feb 25. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013 Feb 27. doi: 10.1038/nature11928. [Epub ahead of print]
Knockdown of dre-miR-7 Zhu Y, Wang D, Wang F, Li T, Dong L, Liu H, Ma Y, Jiang F, Yin H, Yan W, Luo M, Tang Z, Zhang G, Wang Q, Zhang J, Zhou J, Yu J. A comprehensive analysis of GATA-1-regulated miRNAs reveals miR-23a to be a positive modulator of erythropoiesis. Nucleic Acids Res. 2013 Feb 17. [Epub ahead of print] Kaluza D, Kroll J, Gesierich S, Manavski Y, Boeckel JN, Doebele C, Zelent A, Rössig L, Zeiher AM, Augustin HG, Urbich C, Dimmeler S. Histone Deacetylase 9 Promotes Angiogenesis by Targeting the Antiangiogenic MicroRNA 17-92 Cluster in Endothelial Cells. Arterioscler Thromb Vasc Biol. 2013 Jan 3. [Epub ahead of print] Chang SH, Lu YC, Li X, Hsieh WY, Xiong Y, Ghosh M, Evans T, Elemento O, Hla T. Antagonistic function of the RNA-binding protein HuR and miR-200b in post-transcriptional regulation of VEGF-A expression and angiogenesis. J Biol Chem. 2012;[Epub ahead of print]doi:10.1074/jbc.M112.423871 Lalwani MK, Sharma M, Singh AR, Chauhan RK, Patowary A, Singh N, Scaria V, Sivasubbu S. Reverse Genetics Screen in Zebrafish Identifies a Role of miR-142a-3p in Vascular Development and Integrity. PLoS ONE. 2012;7(12):e52588. doi:10.1371/journal.pone.0052588 Bridge G, Monteiro R, Henderson S, Emuss V, Lagos D, Georgopoulou D, Patient R, Boshoff C. The microRNA-30 family targets DLL4 to modulate endothelial cell behavior during angiogenesis. Blood 2012;[Epub ahead of print] doi:10.1182/blood-2012-04-423004
Target protector against the miR-30 site within the dll4 3′UTR. Chiavacci E, Dolfi L, Verduci L, Meghini F, Gestri G, Evangelista AMM, Wilson SW, Cremisi F, Pitto L. MicroRNA 218 Mediates the Effects of Tbx5a Over-Expression on Zebrafish Heart Development. PLoS ONE. 2012;7(11):e50536. doi:10.1371/journal.pone.0050536 Stahlhut C, Suárez Y, Lu J, Mishima Y, Giraldez AJ. miR-1 and miR-206 regulate angiogenesis by modulating VegfA expression in zebrafish. Development. 2012;139:4356-4365. doi:10.1242/dev.083774 Inui M, Montagner M, Ben-Zvi D, Martello G, Soligo S, Manfrin A, Aragona M, Enzo E, Zacchigna L, Zanconato F, Azzolin L, Dupont S, Cordenonsi M, Piccolo S. Self-regulation of the head-inducing properties of the Spemann organizer. Proc Natl Acad Sci U S A. 2012 Sep 4. [Epub ahead of print]
Xla-miR-15/16 Morpholinos in Xenopus laevis. Hassel D, Cheng P, White MP, Ivey KN, Kroll J, Augustin HG, Katus HA, Stainier DY, Srivastava D. miR-10 Regulates the Angiogenic Behavior of Zebrafish and Human Endothelial Cells by Promoting VEGF Signaling. Circ Res. 2012 Sep 5. [Epub ahead of print] Domínguez-Bendala J, Álvarez-Cubela S, Nieto M, Vargas N, Espino-Grosso P, Sacher VY, Pileggi A, García E, Ricordi C, Inverardi L, Pastori RL. Intracardial Embryonic Delivery of Developmental Modifiers In Utero. Cold Spring Harb Protoc. 2012;doi:10.1101/pdb.prot069427
Vivo-Morpholino targeting miRNA in mouse embryos. Nishiyama T, Kaneda R, Ono T, Tohyama S, Hashimoto H, Endo J, Tsuruta H, Yuasa S, Ieda M, Makino S, Fukuda K. miR-142-3p is essential for hematopoiesis and affects cardiac cell fate in zebrafish. Biochem Biophys Res Commun. 2012 Aug 2. [Epub ahead of print] Sessa R, Seano G, di Blasio L, Gagliardi PA, Isella C, Medico E, Cotelli F, Bussolino F, Primo L. The miR-126 regulates Angiopoietin-1 signaling and vessel maturation by targeting p85β. Biochim Biophys Acta. 2012 Jul 31. [Epub ahead of print] Liu X, Ning G, Meng A, Wang Q. MicroRNA-206 regulates cell movements during zebrafish gastrulation by targeting prickle1a and regulating JNK2 phosphorylation. Mol Cell Biol. 2012 May 21. [Epub ahead of print] Coolen M, Thieffry D, Drivenes Ø, Becker TS, Bally-Cuif L. miR-9 controls the timing of neurogenesis through the direct inhibition of antagonistic factors. Dev Cell. 2012 May 15;22(5):1052-64. doi: 10.1016/j.devcel.2012.03.003.
Target protector Furlong F, Fitzpatrick P, O'Toole S, Phelan S, McGrogan B, Maguire A, O'Grady A, Gallagher M, Prencipe M, McGoldrick A, McGettigan P, Brennan D, Sheils O, Martin C, W Kay E, O'Leary J, McCann A. Low MAD2 expression levels associate with reduced progression-free survival in patients with high-grade serous epithelial ovarian cancer. J Pathol. 2012 Apr;226(5):746-55. doi: 10.1002/path.3035. Epub 2012 Jan 17.
Target protector Biyashev D, Veliceasa D, Topczewski J, Topczewska JM, Mizgirev I, Vinokour E, Reddi AL, Licht JD, Revskoy SY, Volpert OV. miR-27b controls venous specification and tip cell fate. Blood. 2012 Mar 15;119(11):2679-87. doi: 10.1182/blood-2011-07-370635. Epub 2011 Dec 29. Zeng L, Childs SJ. The smooth muscle microRNA miR-145 regulates gut epithelial development via a paracrine mechanism. Dev Biol. 2012;[Epub ahead of print] doi:10.1016/j.ydbio.2012.05.009. Nicoli S, Knyphausen CP, Zhu LJ, Lakshmanan A, Lawson ND. miR-221 Is Required for Endothelial Tip Cell Behaviors during Vascular Development. Dev Cell. 2012 Feb 14;22(2):418-29.
dre-miR-221 Morpholino Mishima Y, Fukao A, Kishimoto T, Sakamoto H, Fujiwara T, Inoue K. Translational inhibition by deadenylation-independent mechanisms is central to microRNA-mediated silencing in zebrafish. Proc Natl Acad Sci U S A. 2012 Jan 24;109(4):1104-9. Epub 2012 Jan 9.
dre-miR-1/206 Morpholino. Urbich C, Kaluza D, Frömel T, Knau A, Bennewitz K, Boon RA, Bonauer A, Doebele C, Boeckel JN, Hergenreider E, Zeiher AM, Kroll J, Fleming I, Dimmeler S. MicroRNA-27a/b controls endothelial cell repulsion and angiogenesis by targeting semaphorin 6A. Blood. 2011 Dec 19. [Epub ahead of print]
miRNA knockdown in zebrafish embryos. Tal TL, Franzosa JA, Tilton SC, Philbrick KA, Iwaniec UT, Turner RT, Waters KM, Tanguay RL. MicroRNAs control neurobehavioral development and function in zebrafish. FASEB J. 2012 Jan 17. [Epub ahead of print] Dill H, Linder B, Fehr A, Fischer U. Intronic miR-26b controls neuronal differentiation by repressing its host transcript, ctdsp2. Genes Dev. 2012;26:25-30 doi:10.1101/gad.177774.111
Knockdown of miR-26b in zebrafish embryos. Baudet ML, Zivraj KH, Abreu-Goodger C, Muldal A, Armisen J, Blenkiron C, Goldstein LD, Miska EA, Holt CE. miR-124 acts through CoREST to control onset of Sema3A sensitivity in navigating retinal growth cones. Nat Neurosci. 2011 Dec 4;15(1):29-38. doi: 10.1038/nn.2979.
Electroporation in Xenopus laevis cells. Nieto M, Hevia P, Garcia E, Klein D, Alvarez-Cubela S, Bravo-Egana V, Rosero S, Molano RD, Vargas N, Ricordi C, Pileggi A, Diez J, Domínguez-Bendala J, Pastori RL. Anti sense miR-7 impairs insulin expression in developing pancreas and in cultured pancreatic buds. Cell Transplant. 2011 Dec 20. [Epub ahead of print] Laudadio I, Manfroid I, Achouri Y, Schmidt D, Wilson MD, Cordi S, Thorrez L, Knoops L, Jacquemin P, Schuit F, Pierreux CE, Odom DT, Peers B, Lemaigre FP. A feedback loop between the liver-enriched transcription factor network and miR-122 controls hepatocyte differentiation. Gastroenterology. 2012 Jan;142(1):119-29. doi: 10.1053/j.gastro.2011.09.001. Epub 2011 Sep 12. Le MTN, Shyh-Chang N, Khaw SL, Chin L, Teh C, Tay J, O'Day E, Korzh V, Yang H, Lal A, Lieberman J, Lodish HF, Lim B. Conserved Regulation of p53 Network Dosage by MicroRNA–125b Occurs through Evolving miRNA–Target Gene Pairs. PLoS Genet. 2011;7(9): e1002242. doi:10.1371/journal.pgen.1002242 Lagendijk AK, Goumans MJ, Burkhard SB, Bakkers J. MicroRNA-23 Restricts Cardiac Valve Formation by Inhibiting Has2 and Extracellular Hyaluronic Acid Production. Circ Res. 2011 Sep 2;109(6):649-57. Epub 2011 Jul 21. He X, Yan YL, Eberhart JK, Herpin A, Wagner TU, Schartl M, Postlethwait JH. miR-196 regulates axial patterning and pectoral appendage initiation. Dev Biol. 2011 Jul 20. [Epub ahead of print] Kapsimali M, Kaushik A-L, Gibon G, Dirian L, Ernest S, Rosa FM. Fgf signaling controls pharyngeal taste bud formation through miR-200 and Delta-Notch activity. Development. 2011;138:3473-84. doi:10.1242/dev.058669
Knockdowns of miR-200a, miR-200b and/or miR-429. Marcet B, Chevalier B, Luxardi G, Coraux C, Zaragosi LE, Cibois M, Robbe-Sermesant K, Jolly T, Cardinaud B, Moreilhon C, Giovannini-Chami L, Nawrocki-Raby B, Birembaut P, Waldmann R, Kodjabachian L, Barbry P. Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat Cell Biol. 2011 May 22. [Epub ahead of print]
Morpholino targeting miR-499 and a Dll1 target protector. Miyasaka KY, Kida YS, Banjo T, Ueki Y, Nagayama K, Matsumoto T, Sato M, Ogura T. Heartbeat regulates cardiogenesis by suppressing retinoic acid signaling via expression of miR-143. Mech Dev. 2011 Jan-Feb;128(1-2):18-28. Epub 2010 Sep 30. Shieh JTC, Huang Y, Gilmore J, Srivastava D. Elevated miR-499 Levels Blunt the Cardiac Stress Response. PLoS ONE. 2011;6(5):e19481. doi:10.1371/journal.pone.0019481
Oligo targeting miR-499 electroporated into ventricular cardiomyocyte line H9c2. Gilligan PC, Kumari P, Lim S, Cheong A, Chang A, Sampath K. Conservation defines functional motifs in the squint/nodal-related 1 RNA dorsal localization element. Nucleic Acids Res. 2011 Apr 1;39(8):3340-9. Epub 2010 Dec 10.
Target protector Li N, Wei C, Olena AF, Patton JG. Regulation of endoderm formation and left-right asymmetry by miR-92 during early zebrafish development. Development. 2011 May;138(9):1817-26. Epub 2011 Mar 29. Yu YM, Gibbs KM, Davila J, Campbell N, Sung S, Todorova TI, Otsuka S, Sabaawy HE, Hart RP, Schachner M. MicroRNA miR-133b is essential for functional recovery after spinal cord injury in adult zebrafish. Eur J Neurosci. 2011 May;33(9):1587-97. doi: 10.1111/j.1460-9568.2011.07643.x. Epub 2011 Mar 30.
Morpholino solution soaked on Gelfoam and applied to lesion. Fish JE, Wythe JD, Xiao T, Bruneau BG, Stainier DY, Srivastava D, Woo S. A Slit/miR-218/Robo regulatory loop is required during heart tube formation in zebrafish. Development. 2011 Apr;138(7):1409-19. Hwang-Verslues WW, Chang PH, Wei PC, Yang CY, Huang CK, Kuo WH, Shew JY, Chang KJ, Lee EY, Lee WH. miR-495 is upregulated by E12/E47 in breast cancer stem cells, and promotes oncogenesis and hypoxia resistance via downregulation of E-cadherin and REDD1. Oncogene. 2011 Jan 24. [Epub ahead of print] Staton AA, Knaut H, Giraldez AJ. miRNA regulation of Sdf1 chemokine signaling provides genetic robustness to germ cell migration. Nat Genet. 2011 Jan 23. [Epub ahead of print]
Target protectors Bonev B, Pisco A, Papalopulu N. MicroRNA-9 Reveals Regional Diversity of Neural Progenitors along the Anterior-Posterior Axis. Dev Cell. 2011 Jan 18;20(1):19-32.
Targeting Xtr-miR-9 and target protecting hairy1. Zou J, Li WQ, Li Q, Li XQ, Zhang JT, Liu GQ, Chen J, Qiu XX, Tian FJ, Wang ZZ, Zhu N, Qin YW, Shen B, Liu TX, Jing Q. Two Functional MicroRNA-126s Repress a Novel Target Gene p21-Activated Kinase 1 to Regulate Vascular Integrity in Zebrafish. Circ Res. 2010 Dec 9. [Epub ahead of print] Ghosh G, Subramanian IV, Adhikari N, Zhang X, Joshi HP, Basi D, Chandrashekhar YS, Hall JL, Roy S, Zeng Y, Ramakrishnan S. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-α isoforms and promotes angiogenesis. J Clin Invest. 2010 Oct 25. pii: 42980. doi: 10.1172/JCI42980. [Epub ahead of print] Conte I, Carrella S, Avellino R, Karali M, Marco-Ferreres R, Bovolenta P, Banfi S. miR-204 is required for lens and retinal development via Meis2 targeting. Proc Natl Acad Sci U S A. 2010 Aug 16. [Epub ahead of print] Yu D, dos Santos CO, Zhao G, Jiang J, Amigo JD, Khandros E, Dore LC, Yao Y, D'Souza J, Zhang Z, Ghaffari S, Choi J, Friend S, Tong W, Orange JS, Paw BH, Weiss MJ. miR-451 protects against erythroid oxidant stress by repressing 14-3-3zeta. Genes Dev. 2010 Aug 1;24(15):1620-33. Pedrioli DM, Karpanen T, Dabouras V, Jurisic G, van de Hoek G, Shin JW, Marino D, Kälin RE, Leidel S, Cinelli P, Schulte-Merker S, Brändli AW, Detmar M. miR-31 functions as a negative regulator of lymphatic vascular lineage-specific differentiation in vitro and vascular development in vivo. Mol Cell Biol. 2010 Jul;30(14):3620-34. Epub 2010 May 17. Deacon DC, Nevis KR, Cashman TJ, Zhou Y, Zhao L, Washko D, Guner-Ataman B, Burns CG, Burns CE. The miR-143-adducin3 pathway is essential for cardiac chamber morphogenesis. Development. 2010 Jun;137(11):1887-96.
See supplemental online information for comparison figure of various Morpholino oligos targeting dre-miR-143 on guide or star strands. Long J, Wang Y, Wang W, Chang BH, Danesh FR. Identification of MicroRNA-93 as a novel regulator of vascular endothelial growth factor (VEGF) in hyperglycemic conditions. J Biol Chem. 2010 May 25. [Epub ahead of print]
Delivery note: abstract mentions peptide-conjugated Morpholino oligomers, but mat'l and methods describes Endo-Porter. Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND. MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature. 2010 Apr 4. [Epub ahead of print] Hsu RJ, Lin CY, Hoi HS, Zheng SK, Lin CC, Tsai HJ. Novel intronic microRNA represses zebrafish myf5 promoter activity through silencing dickkopf-3 gene. Nucleic Acids Res. 2010 Mar 17. [Epub ahead of print] Zhao X, He X, Han X, Yu Y, Ye F, Chen Y, Hoang T, Xu X, Mi QS, Xin M, Wang F, Appel B, Lu QR. MicroRNA-Mediated Control of Oligodendrocyte Differentiation. Neuron. 2010 Mar 11;65(5):612-626. Li H, Kloosterman W, Fekete DM. MicroRNA-183 Family Members Regulate Sensorineural Fates in the Inner Ear. J Neurosci. 2010 Mar 3;30(9):3254-63. Hu H, Du L, Nagabayashi G, Seeger RC, Gatti RA. ATM is down-regulated by N-Myc-regulated microRNA-421. Proc Natl Acad Sci U S A. 2010 Jan 4. [Epub ahead of print] Sheedy FJ, Palsson-McDermott E, Hennessy EJ, Martin C, O'Leary J, Ruan Q, Johnson DP, Chen Y, O'Neill LA. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol. 2009 Nov 29. [Epub ahead of print]
NOTE: Target protector for miR-21 Agrawal R, Tran U, Wessely O. The miR-30 miRNA family regulates Xenopus pronephros development and targets the transcription factor Xlim1/Lhx1. Development. 2009 Dec;136(23):3927-36. Zeng L, Carter AD, Childs SJ. miR-145 directs intestinal maturation in zebrafish. Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17793-8. Epub 2009 Oct 5. Weiss FU, Marques IJ, Woltering JM, Vlecken DH, Aghdassi A, Partecke LI, Heidecke CD, Lerch MM, Bagowski CP. Retinoic acid receptor (RAR) antagonists inhibit miR-10a expression and block metastatic behaviour of pancreatic cancer. Gastroenterology. 2009 Sep 9. [Epub ahead of print] Lin Z, Murtaza I, Wang K, Jiao J, Gao J, Li PF. miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proc Natl Acad Sci U S A. 2009 Jul 2. [Epub ahead of print]
NOTE: target protector strategy used Walker JC, Harland RM. microRNA-24a is required to repress apoptosis in the developing neural retina. Genes Dev. 2009 May 1;23(9):1046-51. Epub 2009 Apr 16. Le MT, Teh C, Shyh-Chang N, Xie H, Zhou B, Korzh V, Lodish HF, Lim B. MicroRNA-125b is a novel negative regulator of p53. Genes Dev. 2009 Apr 1;23(7):862-76. Epub 2009 Mar 17. Flynt AS, Thatcher EJ, Burkewitz K, Li N, Liu Y, Patton JG. miR-8 microRNAs regulate the response to osmotic stress in zebrafish embryos. J Cell Biol. 2009 Mar 30. [Epub ahead of print] Mishima Y, Abreu-Goodger C, Staton AA, Stahlhut C, Shou C, Cheng C, Gerstein M, Enright AJ, Giraldez AJ. Zebrafish miR-1 and miR-133 shape muscle gene expression and regulate sarcomeric actin organization. Genes Dev. 2009 Feb 24. [Epub ahead of print] Du TT, Fu YF, Dong M, Wang L, Fan HB, Chen Y, Jin Y, Chen SJ, Chen Z, Deng M, Huang QH, Liu TX. Experimental validation and complexity of miRNA-mRNA target interaction during zebrafish primitive erythropoiesis. Biochem Biophys Res Commun. 2009 Apr 17;381(4):688-93. Epub 2009 Feb 28. Thatcher EJ, Paydar I, Anderson KK, Patton JG. Regulation of zebrafish fin regeneration by microRNAs. Proc Natl Acad Sci U S A. 2008 Nov 25;105(47):18384-9. Epub 2008 Nov 17.
NOTE: Electroporation of Morpholinos into fins Zhang MC, Lv Y, Qi YT, Zhang Z, Fu XN, Yuan CG, Lai LH. [Knockdown and overexpression of miR-219 lead to embryonic defects in zebrafish development] Fen Zi Xi Bao Sheng Wu Xue Bao. 2008 Oct;41(5):341-8. Chinese. Pase L, Layton JE, Kloosterman WP, Carradice D, Waterhouse PM, Lieschke GJ. miR-451 regulates zebrafish erythroid maturation in vivo via its target gata2. Blood. 2008 Oct 10. [Epub ahead of print] Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, Ivey KN, Bruneau BG, Stainier DY, Srivastava D. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008 Aug;15(2):272-84. Li N, Flynt AS, Kim HR, Solnica-Krezel L, Patton JG. Dispatched Homolog 2 is targeted by miR-214 through a combination of three weak microRNA recognition sites. Nucleic Acids Res. 2008 Jun 26. [Epub ahead of print]
NOTE: target protector strategy used Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L. MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci. 2008 Jun;11(6):641-648. Epub 2008 May 4. Yin VP, Thomson JM, Thummel R, Hyde DR, Hammond SM, Poss KD. Fgf-dependent depletion of microRNA-133 promotes appendage regeneration in zebrafish. Genes Dev. 2008 Mar 15;22(6):728-33.
NOTE: Electroporation of Morpholinos into fins Dore LC, Amigo JD, Dos Santos CO, Zhang Z, Gai X, Tobias JW, Yu D, Klein AM, Dorman C, Wu W, Hardison RC, Paw BH, Weiss MJ. A GATA-1-regulated microRNA locus essential for erythropoiesis. Proc Natl Acad Sci U S A. 2008 Feb 26; [Epub ahead of print] Eberhart JK, He X, Swartz ME, Yan YL, Song H, Boling TC, Kunerth AK, Walker MB, Kimmel CB, Postlethwait JH. MicroRNA Mirn140 modulates Pdgf signaling during palatogenesis. Nat Genet. 2008 Feb 10; [Epub ahead of print] Choi PS, Zakhary L, Choi WY, Caron S, Alvarez-Saavedra E, Miska EA, McManus M, Harfe B, Giraldez AJ, Horvitz RH, Schier AF, Dulac C. Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron. 2008 Jan 10;57(1):41-55. Woltering JM, Durston AJ. MiR-10 represses HoxB1a and HoxB3a in zebrafish. PLoS ONE. 2008 Jan 2;3(1):e1396. Lin YC, Hsieh LC, Kuo MW, Yu J, Kuo HH, Lo WL, Lin RJ, Yu AL, Li WH. Human TRIM71 and Its Nematode Homologue are Targets of let-7 MicroRNA and Its Zebrafish Orthologue is Essential for Development. Mol Biol Evol. 2007 Sep 21; [Epub ahead of print] An miRNA's target site on an mRNA can be protected by a complementary Morpholino oligo.
Choi WY, Giraldez AJ, Schier AF. Target Protectors Reveal Dampening and Balancing of Nodal Agonist and Antagonist by miR-430. Science. 2007 Oct 12;318(5848):271-4. Epub 2007 Aug 30. Martello G, Zacchigna L, Inui M, Montagner M, Adorno M, Mamidi A, Morsut L, Soligo S, Tran U, Dupont S, Cordenonsi M, Wessely O & Piccolo S. MicroRNA control of Nodal signalling. Nature 2007 Sep 13;449(7159):183-8. Epub 2007 Aug 29 A Gene Tools collaboration with Wigard Kloosterman, first of Ronald Plasterk's lab then Rene Ketting's lab at the Hubrecht Institute in the Netherlands, has shown that Morpholino oligos can strongly inhibit the activity of miRNAs in zebrafish so that, after Morphoino treatment, the miRNA signal from in-situ hybridization and Northern blots is decreased or absent. Knockdowns of miRNA activity have generally used oligos targeting the miRNA guide strand. A Morpholino oligo targeting an miRNA guide strand can interfere with the activity of the miRNA. It is difficult to control for the specificity of the knockdown when using this technique alone. However, Morpholinos targeting the nucleolytic processing sites of an immature miRNA can prevent maturation of the miRNA. This allows sets of nonoverlapping Morpholino oligos targeting a primary miRNA to be used as specificity controls; if two non-overlapping oligos targeting the same miRNA (typically targeting the 5p and 3p sites) produce the same phenotype, this supports the hypothesis that the phenotype is due to knocking down the activity of the targeted miRNA and not due to an off-target effect. These techniques are explored in the following paper:
Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RHA. Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol. 2007;5(8): e203.
Wigard Kloosterman also describes targeting miRNAs with Morpholinos in his dissertation, The expression and function of microRNAs in vertebrate embryonic development This is the first published report we've found of data from miRNA knockdown using Morpholinos.
Flynt AS, Li N, Thatcher EJ, Solnica-Krezel L, Patton JG. Zebrafish miR-214 modulates Hedgehog signaling to specify muscle cell fate. Nature Genetics 2007; 39: 259 - 263. The following paper primarily reports experiments with 2'-O-methyl oligos but the authors also report that Morpholinos are effective in this application, though no data for the Morpholino knockdowns is shown.
Kloosterman WP, Wienholds E, Ketting RF, Plasterk RH. Substrate requirements for let-7 function in the developing zebrafish embryo. Nucleic Acids Res. 2004 Dec 07;32(21):6284-91.
Morpholino oligos can block the activity of microRNAs. Morpholinos complementary to the miRNA guide strand can block activity of the miRNA. Morpholinos can also block the Drosha or Dicer nucleolytic processing sites of primary miRNA or pre-miRNA. Morpholinos can interfere with miRNA activity when targeted to the miRNA's target site (MRE) on mRNA. Gene Tools assists in targeting 25-base Morpholino oligos to miRNAs, ideally using sequence information from the Sanger Institute's miRBase.
Morpholinos are usually targeted to one of these sites (shown on the lower part of figure below):
- Guide
- Star
- Guide Drosha
- Guide Dicer
- Star Drosha
- Star Dicer
Note that Dicer activity is not requred for maturation of all miRNAs. Here is a known case where miRNA maturation is independent of Dicer activity:
Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, Ma E, Mane S, Hannon GJ, Lawson ND, Wolfe SA, Giraldez AJ. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science. 2010 Jun 25;328(5986):1694-8. Epub 2010 May 6.
Morpholinos can also be targeted to the site on an mRNA where a miRNA binds, called the miRNA response element (MRE). Usually these are found in the 3'-UTR of an mRNA. A Morpholino that binds across an MRE is called a target protector. To design target protector Morpholinos, we need about 60 bases of mRNA sequence centered on the MRE, written mostly in upper case but with the bases complementary to the miRNA seed sequence shown in lower case.
References
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"Here, we report the design and testing of six CPP-conjugated PMO antimiRs (three against miR-23b and three against miR-218) in DM1 patient-derived myotubes and a DM1 mouse model." Fridrich A, Salinas-Saaverda M, Kozlolvski I, Surm JM, Chrysostomou E, Tripathi AM, Frank U, Moran Y. An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis. Cell Rep. 2023 Sep 5;42(9):113072. doi: 10.1016/j.celrep.2023.113072. Online ahead of print.
"Male adults of the Ncol3::memOrange2 transgenic line ... were spawned and crossed with WT eggs. The gelatinous sack surrounding the eggs was removed using 4% L-Cysteine (Merck Milipore, USA) and followed by microinjecting the zygotes with antisense MOs." Ghersi JJ, Baldissera G, Hintzen J, Luff SA, Cheng S, Xia IF, Sturgeon CM, Nicoli S. Haematopoietic stem and progenitor cell heterogeneity is inherited from the embryonic endothelium. Nat Cell Biol. 2023 Jul 17. doi: 10.1038/s41556-023-01187-9. Online ahead of print.
"To test this hypothesis, we induced transient downregulation of miR-128 in embryos by injecting 0.75 ng of morpholino, which was sufficient to recapitulate the biased expansion of erythroid and lymphoid progenitor cells that we detected in miR-128Δ/Δ" Oda H, Sato Y, Kawashima SA, Fujiwara Y, Pálfy M, Wu E, Vastenhouw NL, Kanai M, Kimura H. Actin filaments accumulated in the nucleus remain in the vicinity of condensing chromosomes in the zebrafish early embryo. Biol Open. 2023 May 15;12(5):bio059783. doi: 10.1242/bio.059783. Epub 2023 May 17.
Fluorochrome-labeled Morpholino used as a diagnostic probe in a zebrafish to visualize transcription of the miRNA mir-430 Qaryoute AA, Fallatah W, Dhinoja S, Raman R, Jagadeeswaran P. Role of MicroRNAs and their Downstream Target Transcription Factors in Zebrafish Thrombopoiesis. Res Sq. 2023 Apr 24:rs.3.rs-2807790. doi: 10.21203/rs.3.rs-2807790/v1. Preprint.
DNA oligos targeting miRNA delivered by Vivo-Morpholino piggyback Wan Y, Slevin E, Koyama S, Huang CK, Shetty AK, Li X, Harrison K, Li T, Zhou B, Lorenzo SR, Zhang Y, Salinas JM, Xu W, Klaunig JE, Wu C, Tsukamoto H, Meng F. miR-34a regulates macrophage-associated inflammation and angiogenesis in alcohol-induced liver injury. Hepatol Commun. 2023 Apr 4;7(4):e0089. doi: 10.1097/HC9.0000000000000089. eCollection 2023 Apr
miR-34a targeted in mouse Slevin E, Wan Y, Harrison K, Zhang Y, Li X, Li T, Lorenzo SR, Xu W, Klaunig JE, Shetty AK, Meng F. microRNA-34a modulates the senescence of activated hepatic stellate cells in alcohol-associated liver injury. FASEB J. 2022;[Epub] doi:10.1096/fasebj.2022.36.S1.R4231
Blocking mmu-miR-34a Holm A, Possovre M-L, Bandarabadi M, Moseholm KF, Justinussen JL, Bozic I, Lemcke R, Arribat Y, Amati F, Silahtaroglu A, Juventin M, Adamantidis A, Tafti M, Kornum BR. The evolutionarily conserved miRNA-137 targets the neuropeptide hypocretin/orexin and modulates the wake to sleep ratio. Proc Nat Acad Sci USA. 2022;117(17):e2112225119 [Epub] doi:10.1073/pnas.2112225119
Blocking dre-miR-137 Sheng J, Gong J, Shi Y, Wang X, Liu D. MicroRNA-22 coordinates vascular and motor neuronal pathfinding via sema4 during zebrafish development. Open Biol. 2022 Apr;12(4):210315. doi: 10.1098/rsob.210315. Epub 2022 Apr 6.
Blocking dre-miR-22a Huang Y, Wang W-F, Huang C-X, Li X-H, Liu H, Wang H-L. miR-731 modulates the zebrafish heart morphogenesis via targeting Calcineurin/Nfatc3a pathway. Biochim Biophys Acta Gen Subj. 2022;1866(6):130133. doi:10.1016/j.bbagen.2022.130133
Blocking dre-miR-731 Magner E, Sandoval-Sanchez P, Kramer AC, Thummel R, Hitchcock PF, Taylor SM. Disruption of miR-18a Alters Proliferation, Photoreceptor Replacement Kinetics, Inflammatory Signaling, and Microglia/Macrophage Numbers During Retinal Regeneration in Zebrafish. Mol Neurobiol. 2022 Mar 4. doi: 10.1007/s12035-022-02783-w. Online ahead of print.
Blocking dre-miR-18a Konrad KD, Song JL. miR-124 regulates Notch and NeuroD1 to mediate transition states of neuronal development. bioRxiv. 2021;[preprint]. doi:10.1101/2021.12.10.471989 Blocking miRNA-124 in a sea urchin Meng L, Yuan L, Ni J, Fang M, Guo S, Cai H, Qin J, Cai Q, Zhang M, Hu F, Ma J, Zhang Y. Mir24-2-5p suppresses the osteogenic differentiation with Gnai3 inhibition presenting a direct target via inactivating JNK-p38 MAPK signaling axis. Int J Biol Sci. 2021 Oct 17;17(15):4238-4253. doi: 10.7150/ijbs.60536. eCollection 2021.
Mir24-2-5p knockdown with a Morpholino. Magner E, Sandoval-Sanchez P, Kramer AC, Thummel R, Hitchcock PF, Taylor SM. The microRNA miR-18a links proliferation and inflammation during photoreceptor regeneration in the injured zebrafish retina. bioRxiv. 2021;[preprint] doi:10.1101/2021.04.25.441353
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synthetic miRNA FF3 suppressed in HEK293 reporter cells Vazquez‐Armendariz AI, Heiner M, El Agha E, Salwig I, Hoek A, Hessler MC, Shalashova I, Shrestha A, Carraro G, Mengel JP, Günther A, Morty RE, Vadász I, Schwemmle M, Kummer W, Hain T, Goesmann A, Bellusci S, Seeger W, Braun T, Herold S. Multilineage murine stem cells generate complex organoids to model distal lung development and disease. EMBO J. 2020;e103476 [Epub] doi:10.15252/embj.2019103476
Targeting mmu-miR‐142-3p in murine bronchioalveolar lung organoid culture Adusumilli L, Facchinello N, Teh C, Busolin G, Le TM, Yang H, Beffagna G, Campanaro S, Tam LW, Argenton F, Lim B, Korzh V, Tiso N. miR-7 Controls the Dopaminergic/Oligodendroglial Fate through Wnt/β-catenin Signaling Regulation. Cells. 2020;9(3):2073-4409 doi:10.3390/cells9030711
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Morpholino knockdown of miR-462/miR-731 Corradi E, Dalla Costa I, Gavoci A, Iyer A, Roccuzzo M, Otto TA, Oliani E, Bridi S, Strohbuecker S, Santos-Rodriguez G, Valdembri D, Serini G, Abreu-Goodger C, Baudet ML. Axonal precursor miRNAs hitchhike on endosomes and locally regulate the development of neural circuits. EMBO J. 2020 Feb 19:e102513. doi: 10.15252/embj.2019102513. [Epub ahead of print]
Morpholinos blocking pre‐miR‐181a‐1, pre‐miR‐181a‐2, pre‐miR‐181b processing Hoelscher CS, Stich T, Diehm A, Lahm H, Dreßen M, Zhang Z, Neb I, Aherrahrou Z, Erdmann J, Schunkert H, Santamaria G, Cuda G, Gilsbach R, Hein L, Lange R, Hassel D, Krane M, Doppler AS. miR-128a Acts as a Regulator in Cardiac Development by Modulating Differentiation of Cardiac Progenitor Cell Populations. Int J Molec Sci. 2020;21(3);1158. doi:10.3390/ijms21031158
MO-20b, MO-30b, MO-128a morphants Hackett EE, Charles-Messance H, O’Leary SM, Gleeson LE, Muñoz-Wolf N, Case S, Wedderburn A, Johnston DGW, Williams MA, Smyth A, Ouimet M, Moore KJ, Lavelle EC, Corr SC, Gordon SV, Keane J, Sheedy FJ. Mycobacterium tuberculosis Limits Host Glycolysis and IL-1β by Restriction of PFK-M via MicroRNA-21. Cell Rep. 2020;30(1):124-36.e4. doi:10.1016/j.celrep.2019.12.015.
Target protector Wang D, Weng Y, Guo S, Qin W, Ni J, Yu L, Zhang Y, Zhao Q, Ben J, Ma J. microRNA-1 Regulates NCC Migration and Differentiation by Targeting sec63. Int J Biol Sci. 2019;15(12):2538-2547. doi:10.7150/ijbs.35357
Morpholino targeting dre-miR-1 de Morree A, Klein JDD, Gan Q, Farup J, Urtasun A, Kanugovi A, Bilen B, van Velthoven CTJ, Quarta M, Rando TA. Alternative polyadenylation of Pax3 controls muscle stem cell fate and muscle function. Science. 2019 Nov 8;366(6466):734-738. doi: 10.1126/science.aax1694.
Morpholino targeting miR-206 Guzzolino E, Pellegrino M, Ahuja N, Garrity D, D'Aurizio R, Groth M, Baumgart M, Hatcher CJ, Mercatanti A, Evangelista M, Ippolito C, Tognoni E, Fukuda R, Lionetti V, Pellegrini M, Cremisi F, Pitto L. miR-182-5p is an evolutionarily conserved Tbx5 effector that impacts cardiac development and electrical activity in zebrafish. Cell Mol Life Sci. 2019 Nov 4. doi: 10.1007/s00018-019-03343-7. [Epub ahead of print]
Morpholino targeting miR-182 Duan F-G, Wang M-F, Cao Y-B, Li D, Li R-Z, Fan X-X, Khan I, Lai H-L, Zhang Y-Z, Hsiao WW-L, Yao X-J, Wu Q-B, Liu L, Tang I-J, Leung EL-H. MicroRNA-421 confers paclitaxel resistance by binding to the KEAP1 3′UTR and predicts poor survival in non-small cell lung cancer. Cell Death Dis. 2019;10:821. doi:10.1038/s41419-019-2031-1
miR-421 in mouse xenografts, intratumoral injection Sharma P, Gupta S, Chaudhary M, Mitra S, Chawla B, Khursheed MA, Ramachandran R. Oct4 mediates Müller glia reprogramming and cell cycle exit during retina regeneration in zebrafish. Life Sci Alliance. 2019 Oct 8;2(5). pii: e201900548. doi: 10.26508/lsa.201900548. Print 2019 Oct.
zebrafish ocular injection then electroporation:
dre-miR-200A, dre-miR-200b, dre-miR-143, dre-miR-145 Jung HM, Hu CT, Fister AM, Davis AE, Castranova D, Pham VN, Price LM, Weinstein BM. MicroRNA-mediated control of developmental lymphangiogenesis. eLife. 2019;8:e46007. doi: 10.7554/eLife.46007
dre-mir-204 Wade SM, Ohnesorge N, McLoughlin H, Biniecka M, Carter SP, Trenkman M, Cunningham CC, McGarry T, Canavan M, Kennedy BN, Veale DJ, Fearon U. Dysregulated miR-125a promotes angiogenesis through enhanced glycolysis. EBioMedicine. 2019;[Epub ahead of print] doi:10.1016/j.ebiom.2019.08.043
targeting dre-miR-125a Mukherjee S, Akbar I, Kumari B, Vrati S, Basu A, Banerjee A. Japanese Encephalitis Virus-induced let-7a/b interacted with the NOTCH-TLR7 pathway in microglia and facilitated neuronal death via caspase activation. J Neurochem. 2018 Dec 17. doi: 10.1111/jnc.14645. [Epub ahead of print]
Let7 miRNA knockdown with Vivo-Morpholino in mouse brain Watterston C, Zeng L, Onabadejo A, Childs SJ. MicroRNA26 attenuates vascular smooth muscle maturation via endothelial BMP signalling. PLoS Genet. 2019 May 15;15(5):e1008163. doi: 10.1371/journal.pgen.1008163. [Epub ahead of print]
dre-miR-26a knockdown Indrieri A, Carrella S, Romano A, Spaziano A, Marrocco E, Fernandez‐Vizarra E, Barbato S, Pizzo M, Ezhova Y, Golia FM, Ciampi L, Tammaro R, Henao‐Mejia J, Williams A, Flavell RA, De Leonibus E, Zeviani M, Surace EM, Banfi S, Franco B. miR‐181a/b downregulation exerts a protective action on mitochondrial disease models. EMBO Molec Med. 2019;e8734 [Epub ahead of print] doi:10.15252/emmm.201708734
dre-miR-181 knockdown Remsburg C, Konrad K, Sampilo NF, Song JL. Analysis of microRNA functions. Methods Cell Biol. 2019;151:323-334. doi: 10.1016/bs.mcb.2018.10.005. Epub 2018 Dec 11.
Target protector discussion Shrestha A, Carraro G, Nottet N, Vazquez-Armendariz AI, Susanne Herold S, Cordero J, Singh I, Jochen Wilhelm J, Barreto G, Morty R, El Agha E, Mari B, Chen C, Jin-San Zhang J-S, Chao C-M, Bellusci S. A critical role for miR-142 in alveolar epithelial lineage formation in mouse lung development. Cell Molec Life Sci. 2019;[Epub] doi:10.1007/s00018-019-03067-8 Jung HM, Hu C, Fister AM, Davis AE, Castranova D, Pham VN, Price LM, Weinstein BM. MicroRNA-mediated control of developmental lymphangiogenesis. bioRxiv. 2019;[preprint] doi:10.1101/555664
Morpholinos blocking dre-miR-204 Yin Y, Xu L, Chang Y, Zeng T, Chen X, Wang A, Groth J, Foo WC, Liang C, Hu H, Huang J. N-Myc promotes therapeutic resistance development of neuroendocrine prostate cancer by differentially regulating miR-421/ATM pathway. Mol Cancer. 2019 Jan 18;18(1):11. doi: 10.1186/s12943-019-0941-2.
Vivo-Morpholino targeting miR-421 Corradi E, Gavoci A, Strohbuecker S, Roccuzzo M, Costa ID, Iyer A, Bridi S, Rodriguez GS, Abreu-Goodger C, Baudet M-L. Precursor miRNAs are trafficked along axons associated with vesicles and locally processed to regulate growth cone steering. bioRxive. 2018;[Preprint] doi:10.1101/470393
xla-miR-181a-1, xla-miR-181a-2 Sampilo NF, Stepicheva NA, Zaidi SAM, Wang L, Wu W, Wikramanayake A, Song JL. Inhibition of microRNA suppression of Dishevelled results in Wnt pathway associated developmental defects. Development. 2018 Nov 2. pii: dev.167130. doi: 10.1242/dev.167130. [Epub ahead of print]
Target protectors Huang C-X, Huang Y, Duan X-K, Zhang M, Tu J-P, Liu J-X, Liu H, Chen T-S, Wang W-M, Wang H-L. Zebrafish miR-462-731 regulates hematopoietic specification and pu.1-dependent primitive myelopoiesis. Cell Death Differ. 2018; doi:10.1038/s41418-018-0234-0
dre-miR-462, dre-miR-731 knockdown Lin CY, Zhang PH, Chen YJ, Wu CL, Tsai HJ. Conditional Overexpression of rtn4al in Muscle of Adult Zebrafish Displays Defects Similar to Human Amyotrophic Lateral Sclerosis. Mar Biotechnol (NY). 2018 Nov 15. doi: 10.1007/s10126-018-9857-x. [Epub ahead of print]
dre-miR-206, dre-miR-1 Taylor SM, Giuffre E, Moseley P, Hitchcock PF. The microRNA, miR-18a, regulates NeuroD and photoreceptor differentiation in the retina of the zebrafish. bioRXive. 2018;[Epub] doi:10.1101/440263
dre-miR-18 family knockdowns Du X-f, Xu B, Zhang Y, Chen M-j, Du J-l. A transgenic zebrafish model for in vivo long-term imaging of retinotectal synaptogenesis. Sci Rep. 2018;8:14077. doi:10.1038/s41598-018-32409-y
dre-miR-132 knockdown Leinonen JT, Chen YC, Tukiainen T, Panula P, Widén E. Transient modification of lin28b expression - Permanent effects on zebrafish growth. Mol Cell Endocrinol. 2018 Sep 6. pii: S0303-7207(18)30263-6. doi: 10.1016/j.mce.2018.09.001. [Epub ahead of print]
zebrafish lin28b target Romney ALT, Podrabsky JE. Small noncoding RNA profiles along alternative developmental trajectories in an annual killifish. Sci Rep. 2018;8:13364. doi:10.1038/s41598-018-31466-7
alim-miR-430a knockdown Vergara HM, Ramirez J, Rosing T, Nave C, Blandino R, Saw D, Saraf P, Piexoto G, Coombes C, Adams M, Domingo CR. miR-206 is required for changes in cell adhesion that drive muscle cell morphogenesis in Xenopus laevis. Dev Biol. 2018;[Epub ahead of print] doi:10.1016/j.ydbio.2018.03.021 Cao H, Shi J, Du J, Chen K, Dong C, Jiang D, Jiang H. MicroRNA-194 Regulates the Development and Differentiation of Sensory Patches and Statoacoustic Ganglion of Inner Ear by Fgf4. Med Sci Monit. 2018 Mar 23;24:1712-1723. Kontarakis Z, Rossi A, Ramas S, Dellinger MT, Stainier DYR. Mir-126 is a conserved modulator of lymphatic development. Dev Biol. 2018 Mar 14. pii: S0012-1606(18)30138-6. doi: 10.1016/j.ydbio.2018.03.006. [Epub ahead of print] Madelaine R, Notwell JH, Skariah G, Halluin C, Chen CC, Bejerano G, Mourrain P. A screen for deeply conserved non-coding GWAS SNPs uncovers a MIR-9-2 functional mutation associated to retinal vasculature defects in human. Nucl Acids Res. 2018;[Epub ahead of print] doi:10.1093/nar/gky166
Targeting dre-miR-9 Kim CW, Han JH, Wu L, Choi JY. microRNA-183 is Essential for Hair Cell Regeneration after Neomycin Injury in Zebrafish. Yonsei Med J. 2018 Jan;59(1):141-147. doi: 10.3349/ymj.2018.59.1.141.
Targeting dre-miR-183 Lin CY, He JY, Zeng CW, Loo MR, Chang WY, Zhang PH, Tsai HJ. microRNA-206 modulates an Rtn4a/Cxcr4a/Thbs3a axis in newly forming somites to maintain and stabilize the somite boundary formation of zebrafish embryos. Open Biol. 2017 Jul;7(7). pii: 170009. doi: 10.1098/rsob.170009. Wu Y, Lou QY, Ge F, Xiong Q. Quantitative Proteomics Analysis Reveals Novel Targets of miR-21 in Zebrafish Embryos. Sci Rep. 2017 Jun 22;7(1):4022. doi: 10.1038/s41598-017-04166-x.
Blocking miR-21 in zebrafish Kara N, Wei C, Commanday AC, Patton JG. miR-27 regulates chondrogenesis by suppressing focal adhesion kinase during pharyngeal arch development. Dev Biol. 2017 Jun 16. pii: S0012-1606(16)30850-8. doi: 10.1016/j.ydbio.2017.06.013. [Epub ahead of print]
Blocking miR-132 in zebrafish Hall C, Ehrlich L, Meng F, Invernizzi P, Bernuzzi F, Lairmore TC, Alpini G, Glaser S. Inhibition of microRNA-24 increases liver fibrosis by enhanced menin expression in Mdr2-/- mice. J Surg Res. 2017 May 11. pii: S0022-4804(17)30273-1. doi: 10.1016/j.jss.2017.05.020. [Epub ahead of print]
Vivo-Morpholino inhibiting mmu-miR-24 Xu B, Zhang Y, Du XF, Li J, Zi HX, Bu JW, Yan Y, Han H, Du JL. Neurons secrete miR-132-containing exosomes to regulate brain vascular integrity. Cell Res. 2017 Apr 21. doi: 10.1038/cr.2017.62. [Epub ahead of print]
Blocking miR-132 in zebrafish Flynt AS, Rao M, Patton JG. Blocking Zebrafish MicroRNAs with Morpholinos. Methods Mol Biol. 2017;1565:59-78. doi: 10.1007/978-1-4939-6817-6_6. Hazra B, Kumawat KL, Basu A. The host microRNA miR-301a blocks the IRF1-mediated neuronal innate immune response to Japanese encephalitis virus infection. Sci Signal. 2017;10(466):eaaf5185. doi:10.1126/scisignal.aaf5185
BALB/c mice, intracranially treated with a Vivo-Morpholino targeting miR-301a Bellon A, Iyer A, Bridi S, Lee FC, Ovando-Vázquez C, Corradi E, Longhi S, Roccuzzo M, Strohbuecker S, Naik S, Sarkies P, Miska E, Abreu-Goodger C, Holt CE, Baudet ML. miR-182 Regulates Slit2-Mediated Axon Guidance by Modulating the Local Translation of a Specific mRNA. Cell Rep. 2017 Jan 31;18(5):1171-1186. doi: 10.1016/j.celrep.2016.12.093.
Targeting mir-182 in Xenopus laevis. Hung IC, Hsiao YC, Sun HS, Chen TM, Lee SJ. MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae. BMC Genomics. 2016 Nov 15;17(1):922.
Targeting dre-mir-29b. Chang RM, Xiao S, Lei X, Yang H, Fang F, Yang LY. miRNA-487a Promotes Proliferation and Metastasis in Hepatocellular Carcinoma. Clin Cancer Res. 2016 Nov 8. pii: clincanres.0851.2016. [Epub ahead of print]
miRNA-487a targeted with a Vivo-Morpholino in mice. Katz S, Cussigh D, Urbán N, Blomfield I, Guillemot F, Bally-Cuif L, Coolen M. A Nuclear Role for miR-9 and Argonaute Proteins in Balancing Quiescent and Activated Neural Stem Cell States. Cell Rep. 2016 Oct 25;17(5):1383-1398. doi: 10.1016/j.celrep.2016.09.088. Benz A, Kossack M, Auth D, Seyler C, Zitron E, Juergensen L, Katus HA, Hassel D. miR-19b Regulates Ventricular Action Potential Duration in Zebrafish. Sci Rep. 2016 Nov 2;6:36033. doi: 10.1038/srep36033. Presslauer C, Bizuayehu TT, Razmi K, Fernandes JM, Babiak I. See-Thru-Gonad zebrafish line: developmental and functional validation. Reproduction. 2016 Nov;152(5):507-17. doi: 10.1530/REP-16-0328.
Vivo-Morpholino injection into developing zebrafish ovaries to block miR-92a-3p Li Y, Huang C, Feng P, Jiang Y, Wang W, Zhou D, Chen L. Aberrant expression of miR-153 is associated with overexpression of hypoxia-inducible factor-1α in refractory epilepsy. Sci Rep. 2016 Aug 24;6:32091. doi: 10.1038/srep32091. Targeting miR-153 in rat astrocytes Hildyard JC, Wells DJ. Investigating Synthetic Oligonucleotide Targeting of Mir31 in Duchenne Muscular Dystrophy. PLoS Curr. 2016 Jun 16;8. pii: ecurrents.md.99d88e72634387639707601b237467d7. doi: 10.1371/currents.md.99d88e72634387639707601b237467d7.
sponges, star sequence targets, target protectors Giacomotto J, Carroll AP, Rinkwitz S, Mowry B, Cairns MJ, Becker TS. Developmental suppression of schizophrenia-associated miR-137 alters sensorimotor function in zebrafish. Transl Psychiatry. 2016 May 24;6:e818. doi: 10.1038/tp.2016.88. Wang X, Ling CC, Li L, Qin Y, Qi J, Liu X, You B, Shi Y, Zhang J, Jiang Q, Xu H, Sun C, You Y, Chai R, Liu D. MicroRNA-10a/10b represses a novel target gene mib1 to regulate angiogenesis. Cardiovasc Res. 2016 Jan 29. pii: cvw023. [Epub ahead of print] Chiavacci E, D'Aurizio R, Guzzolino E, Russo F, Baumgart M, Groth M, Mariani L, D'Onofrio M, Arisi I, Pellegrini M, Cellerino A, Cremisi F, Pitto L. MicroRNA 19a replacement partially rescues fin and cardiac defects in zebrafish model of Holt Oram syndrome. Sci Rep. 2015 Dec 14;5:18240. doi: 10.1038/srep18240. Liu C, Lou CH, Shah V, Ritter R, Talley J, Soibam B, Benham A, Zhu H, Perez E, Shieh YE, Gunaratne PH, Sater AK. Identification of microRNAs and microRNA Targets in Xenopus gastrulae: The role of miR-26 in the regulation of Smad1. Dev Biol. 2015 Nov 5. pii: S0012-1606(15)30277-3. doi: 10.1016/j.ydbio.2015.11.005. [Epub ahead of print] Target protector Morpholino Singh BN, Kawakami Y, Akiyama R, Rasmussen TL, Garry MG, Gong W, Das S, Shi X, Koyano-Nakagawa N, Garry DJ. The Etv2-miR-130a Network Regulates Mesodermal Specification. Cell Rep. 2015 Nov 3;13(5):915-23. doi: 10.1016/j.celrep.2015.09.060. Epub 2015 Oct 22. Stepicheva NA, Song JL. microRNA-31 modulates skeletal patterning in the sea urchin embryo. Development. 2015 Nov 1;142(21):3769-80. doi: 10.1242/dev.127969. Epub 2015 Sep 23.
Target protector Morpholinos Kiesow K, Bennewitz K, Miranda LG, Stoll SJ, Hartenstein B, Angel P, Kroll J, Schorpp-Kistner M. Junb controls lymphatic vascular development in zebrafish via miR-182. Sci Rep. 2015 Oct 13;5:15007. doi: 10.1038/srep15007. Chevalier B, Adamiok A, Mercey O, Revinski DR, Zaragosi LE, Pasini A, Kodjabachian L, Barbry P, Marcet B. miR-34/449 control apical actin network formation during multiciliogenesis through small GTPase pathways. Nat Commun. 2015 Sep 18;6:8386. doi: 10.1038/ncomms9386.
Direct miRNA binding Morpholinos and target protectors. Morris JF, Chomyk A, Song P, Parker N, Deckard S, Trapp BD, Pimplikar SW, Dutta R. Decrease in levels of the evolutionarily conserved microRNA miR-124 affects oligodendrocyte numbers in Zebrafish, Danio rerio. Invert Neurosci. 2015;15:4 doi:10.1007/s10158-015-0180-1 Conte I, Hadfield KD, Barbato S, Carrella S, Pizzo M, Bhat RS, Carissimo A, Karali M, Porter LF, Urquhart J, Hateley S, O'Sullivan J, Manson FD, Neuhauss SC, Banfi S, Black GC. MiR-204 is responsible for inherited retinal dystrophy associated with ocular coloboma. Proc Natl Acad Sci U S A. 2015 Jun 8. pii: 201401464. [Epub ahead of print] Wang K, Liu CY, Zhou LY, Wang JX, Wang M, Zhao B, Zhao WK, Xu SJ, Fan LH, Zhang XJ, Feng C, Wang CQ, Zhao YF, Li PF. APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p. Nat Commun. 2015 Apr 10;6:6779. doi: 10.1038/ncomms7779. Geiger SS, Hokamp K, Reilly MP, Coogan AN, Vigorito E, FitzGerald GA, O'Neill LA. Circadian control of innate immunity in macrophages by miR-155 targeting Bmal1. Proc Natl Acad Sci U S A. 2015 May 20. pii: 201501327. [Epub ahead of print]
two target protectors for mmu-miR-155 binding sites in Bmal1 Carrella S, D'Agostino Y, Barbato S, Huber-Reggi SP, Salierno FG, Manfredi A, Neuhauss SC, Banfi S, Conte I. miR-181a/b control the assembly of visual circuitry by regulating retinal axon specification and growth. Dev Neurobiol. 2015 Feb 27. doi: 10.1002/dneu.22282. [Epub ahead of print]
Target protector Makino S, Mishima Y, Inoue K, Inada T. Roles of mRNA fate modulators Dhh1 and Pat1 in TNRC6-dependent gene silencing recapitulated in yeast. J Biol Chem. 2015 Mar 27;290(13):8331-47. doi: 10.1074/jbc.M114.615088. Epub 2015 Feb 5. Ristori E, Lopez-Ramirez MA, Narayanan A, Hill-Teran G, Moro A, Calvo C-F, Thomas J-L, Nicoli S. A Dicer-miR-107 Interaction Regulates Biogenesis of Specific miRNAs Crucial for Neurogenesis. Dev Cell. 2015;[Epub ahead of print] doi:10.1016/j.devcel.2014.12.013 Olena AF, Rao MB, Thatcher EJ, Wu SY, Patton JG. miR-216a regulates snx5, a novel notch signaling pathway component, during zebrafish retinal development. Dev Biol. 2015 Apr 1;400(1):72-81. doi: 10.1016/j.ydbio.2015.01.016. Epub 2015 Jan 31. Song B, Zhang Q, Zhang Z, Wan Y, Jia Q, Wang X, Zhu X, Leung A Y-H, Cheng T, Fang X, Yuan W, Jia H. Systematic transcriptome analysis of the zebrafish model of diamond-blackfan anemia induced by RPS24 deficiency. BMC Genomics. 2014;15:759. doi:10.1186/1471-2164-15-759 Feng Y, Gross S, Wolf NM, Butenschön VM, Qiu Y, Devraj K, Liebner S, Kroll J, Skolnik EY, Hammes H-P, Wieland T. Nucleoside Diphosphate Kinase B Regulates Angiogenesis Through Modulation of Vascular Endothelial Growth Factor Receptor Type 2 and Endothelial Adherens Junction Proteins. Arterioscler Thromb Vasc Biol. 2014;[Epub ahead of print] doi:10.1161/ATVBAHA.114.304239 Salta E, Lau P, Frigerio CS, Coolen M, Bally-Cuif L, De Strooperemail B. A Self-Organizing miR-132/Ctbp2 Circuit Regulates Bimodal Notch Signals and Glial Progenitor Fate Choice during Spinal Cord Maturation. Dev Cell. 2014;[Epub ahead of print] doi:10.1016/j.devcel.2014.07.006 Francis H, McDaniel K, Han Y, Liu X, Kennedy L, Yang F, McCarra J, Zhou T, Glaser S, Venter J, Huang L, Levine P, Lai J-M, Liu C-G, Alpini G, Meng F. Regulation of the extrinsic apoptotic pathway by microRNA-21 in alcoholic liver injury. J Biol Chem. 2014;[Epub ahead of print] doi:10.1074/jbc.M114.602383 Tsai P-C, Bake S, Balaraman S, Rawlings J, Holgate RR, Dubois D, Miranda RC. MiR-153 targets the nuclear factor-1 family and protects against teratogenic effects of ethanol exposure in fetal neural stem cells. Biology Open. 2014;[Epub] doi:10.1242/bio.20147765
miRNA target protectors Conte I, Merella S, Garcia-Manteiga JM, Migliore C, Lazarevic D, Carrella S, Marco-Ferreres R, Avellino R, Davidson NP, Emmett W, Sanges R, Bockett N, Van Heel D, Meroni G, Bovolenta P, Stupka E, Banfi S. The combination of transcriptomics and informatics identifies pathways targeted by miR-204 during neurogenesis and axon guidance. Nucleic Acids Res. 2014 Aug 1;42(12):7793-806. doi: 10.1093/nar/gku498. Epub 2014 Jun 3. Rajaram K, Harding RL, Hyde DR, Patton JG. miR-203 regulates progenitor cell proliferation during adult zebrafish retina regeneration. Dev Biol. 2014 May 20. pii: S0012-1606(14)00260-7. doi: 10.1016/j.ydbio.2014.05.005. [Epub ahead of print] Song R, Walentek P, Sponer N, Klimke A, Lee JS, Dixon G, Harland R, Wan Y, Lishko P, Lize M, Kessel M, He L. miR-34/449 miRNAs are required for motile ciliogenesis by repressing cp110. Nature. 2014;510:115-20 doi:10.1038/nature13413
knockdowns of miR-34b, miR-449a in Xenopus laevis Conte I, Merella S, Garcia-Manteiga JM, Migliore C, Lazarevic D, Carrella S, Marco-Ferreres R, Avellino R, Davidson NP, Emmett W, Sanges R, Bockett N, Van Heel D, Meroni G, Bovolenta P, Stupka E, Banfi S. The combination of transcriptomics and informatics identifies pathways targeted by miR-204 during neurogenesis and axon guidance. Nucl Acids Res. 2014;[Epub ahead of print] doi:10.1093/nar/gku498
miR-204 knockdown in Medaka Joshi HP, Subramanian IV, Schnettler EK, Ghosh G, Rupaimoole R, Evans C, Saluja M, Jing Y, Cristina I, Roy S, Zeng Y, Shah VH, Sood AK, Ramakrishnan S. Dynamin 2 along with microRNA-199a reciprocally regulate hypoxia-inducible factors and ovarian cancer metastasis. PNAS. 2014;[Epub ahead of print] doi:10.1073/pnas.1317242111 Targeting miR-199a in cultured cells Carraro G, Shrestha A, Rostkovius J, Contreras A, Chao CM, El Agha E, Mackenzie B, Dilai S, Guidolin D, Taketo MM, Günther A, Kumar ME, Seeger W, De Langhe S, Barreto G, Bellusci S. miR-142-3p balances proliferation and differentiation of mesenchymal cells during lung development. Development. 2014 Feb 19. [Epub ahead of print]
Vivo-Morpholinos targeting mmu-miR-126,mmu-miR-miR-142-3p, and mmu-miR-144 in mouse lung explants. Glaser S, Meng F, Han Y, Onori P, Chow BK, Francis H, Venter J, McDaniel K, Marzioni M, Invernizzi P, Ueno Y, Lai JM, Huang L, Standeford H, Alvaro D, Gaudio E, Franchitto A, Alpini G. Secretin Stimulates Biliary Cell Proliferation by Regulating Expression of MicroRNA 125b and MicroRNA let7a in Mice. Gastroenterology. 2014 Feb 25. pii: S0016-5085(14)00241-8. doi: 10.1053/j.gastro.2014.02.030. [Epub ahead of print]
Vivo-Morpholino tail-vein injections into mice, oligos targeting microRNAs mmu-miR-125b or mmu-miR-let7 Lou CH, Shao A, Shum EY, Espinoza JL, Huang L, Karam R, Wilkinson MF. Posttranscriptional Control of the Stem Cell and Neurogenic Programs by the Nonsense-Mediated RNA Decay Pathway. Cell Rep. 2014;[Epub ahead of print] doi:10.1016/j.celrep.2014.01.028
miR-128 target protectors on Upf1 transcript Ben-Moshe Z, Alon S, Mracek P, Faigenbloom L, Tovin A, Vatine GD, Eisenberg E, Foulkes NS, Gothilf Y. The light-induced transcriptome of the zebrafish pineal gland reveals complex regulation of the circadian clockwork by light. Nucl Acids Res. 2014;[Epub ahead of print] doi:10.1093/nar/gkt1359
Targeting dre-miR-183. Velu CS, Chaubey A, Phelan JD, Horman SR, Wunderlich M, Guzman ML, Jegga AG, Zeleznik-Le NJ, Chen J, Mulloy JC, Cancelas JA, Jordan CT, Aronow BJ, Marcucci G, Bhat B, Gebelein B, Grimes HL. Therapeutic antagonists of microRNAs deplete leukemia-initiating cell activity. J Clin Invest. 2014 Jan 2;124(1):222-36. doi: 10.1172/JCI66005. Epub 2013 Dec 16. Lu X, Li X, He Q, Gao J, Gao Y, Liu B, Liu F. miR-142-3p regulates the formation and differentiation of hematopoietic stem cells in vertebrates. Cell Res. 2013 Dec;23(12):1356-68. doi: 10.1038/cr.2013.145. Epub 2013 Oct 29. Lin CY, Lee HC, Fu CY, Ding YY, Chen JS, Lee MH, Huang WJ, Tsai HJ. miR-1 and miR-206 target different genes to have opposing roles during angiogenesis in zebrafish embryos. Nat Commun. 2013 Nov 22;4:2829. doi: 10.1038/ncomms3829.
Targeting miRNA and a target protector in zebrafish Anton L, Olarerin-George AO, Schwartz N, Srinivas S, Bastek J, Hogenesch JB, Elovitz MA. miR-210 inhibits trophoblast invasion and is a serum biomarker for preeclampsia. Am J Pathol. 2013 Nov;183(5):1437-45. doi: 10.1016/j.ajpath.2013.07.021. Epub 2013 Sep 10. Ordas A, Kanwal Z, Lindenberg V, Rougeot J, Mink M, Spaink HP, Meijer AH. MicroRNA-146 function in the innate immune transcriptome response of zebrafish embryos to Salmonella typhimurium infection. BMC Genomics. 2013;14:696 doi:10.1186/1471-2164-14-696 Targeting dre-miR-146a, dre-miR-146b Franzosa JA, Bugel SM, Tal TL, La Du JK, Tilton SC, Waters KM, Tanguay RL. Retinoic acid-dependent regulation of miR-19 expression elicits vertebrate axis defects. FASEB J. 2013 Aug 23. [Epub ahead of print] Nimmo R, Ciau-Uitz A, Ruiz-Herguido C, Soneji S, Bigas A, Patient R, Enver T. MiR-142-3p controls the specification of definitive hemangioblasts during ontogeny. Dev Cell. 2013 Aug 12;26(3):237-49. doi: 10.1016/j.devcel.2013.06.023. Epub 2013 Aug 1. Wang K, Liu F, Zhou LY, Ding SL, Long B, Liu CY, Sun T, Fan YY, Sun L, Li PF. miR-874 regulates myocardial necrosis by targeting caspase-8. Cell Death Dis. 2013 Jul 4;4:e709. doi: 10.1038/cddis.2013.233.
Target protectors delivered in mouse primary cardiomyocytes using Endo-Porter Lin C-Y, Chen J-S, Loo M-R, Hsiao C-C, Chang W-Y, Tsai H-J. MicroRNA-3906 Regulates Fast Muscle Differentiation through Modulating the Target Gene homer-1b in Zebrafish Embryos. PLoS ONE. 2013;8(7):e70187. doi:10.1371/journal.pone.0070187 McCarthy N, Wetherill L, Lovely CB, Swartz ME, Foroud TM, Eberhart JK. Pdgfra protects against ethanol-induced craniofacial defects in a zebrafish model of FASD. Development 2013 140:3254-3265; doi:10.1242/dev.094938
Knockdown of dre-miR-140 by microinjection in zebrafish. Jiang Q, Lagos-Quintana M, Liu D, Shi Y, Helker C, Herzog W, le Noble F. miR-30a Regulates Endothelial Tip Cell Formation and Arteriolar Branching. Hypertension. 2013 Jul 1. [Epub ahead of print] Pappalardo-Carter DL, Balaraman S, Sathyan P, Carter ES, Chen WJ, Miranda RC. Suppression and Epigenetic Regulation of MiR-9 Contributes to Ethanol Teratology: Evidence from Zebrafish and Murine Fetal Neural Stem Cell Models. Alcohol Clin Exp Res. 2013 Jun 25. doi: 10.1111/acer.12139. [Epub ahead of print] Banjo T, Grajcarek J, Yoshino D, Osada H, Miyasaka KY, Kida YS, Ueki Y, Nagayama K, Kawakami K, Matsumoto T, Sato M, Ogura T. Haemodynamically dependent valvulogenesis of zebrafish heart is mediated by flow-dependent expression of miR-21. Nature Comm. 2013;4:article1978 doi:10.1038/ncomms2978
Includes Morpholinos against miR-21-1, miR-21-2, and a target protector. Coinjections of miR-21-1 & miR-21-2 oligos. Ketley A, Warren A, Holmes E, Gering M, Aboobaker AA, Brook JD. The miR-30 MicroRNA Family Targets smoothened to Regulate Hedgehog Signalling in Zebrafish Early Muscle Development. PLoS ONE. 2013;8(6):e65170. doi:10.1371/journal.pone.0065170
dre-miR-30 oligo and a target protector for miR-30 MRE on smoothened Wang L, Fu C, Fan H, Du T, Dong M, Chen Y, Jin Y, Zhou Y, Deng M, Gu A, Jing Q, Liu T, Zhou Y. miR-34b regulates multiciliogenesis during organ formation in zebrafish. Development. 2013 May 22. [Epub ahead of print] Martin NT, Nakamura K, Davies R, Nahas SA, Brown C, Tunuguntla R, Gatti RA, Hu H. ATM-Dependent MiR-335 Targets CtIP and Modulates the DNA Damage Response. PLoS Genet. 2013;9(5):e1003505. doi:10.1371/journal.pgen.1003505
Xu RR, Zhang CW, Cao Y, Wang Q. [mir122 deficiency inhibits differentiation of zebrafish hepatoblast into hepatocyte]. Yi Chuan. 2013 Apr;35(4):488-94. Chinese. Kolpa HJ, Peal DS, Lynch SN, Giokas AC, Ghatak S, Misra S, Norris RA, Macrae CA, Markwald RR, Ellinor P, Bischoff J, Milan DJ. miR-21 represses Pdcd4 during cardiac valvulogenesis. Development. 2013 May;140(10):2172-80. doi: 10.1242/dev.084475. Epub 2013 Apr 11. Riley MF, Bochter MS, Wahi K, Nuovo GJ, Cole SE. Mir-125a-5p-mediated regulation of Lfng is essential for the avian segmentation clock. Dev Cell. 2013 Mar 11;24(5):554-61. doi: 10.1016/j.devcel.2013.01.024.
mir-125a oligo and Lfng 3’UTR target protector. Avellino R, Carrella S, Pirozzi M, Risolino M, Salierno FG, Franco P, Stoppelli P, Verde P, Banfi S, Conte I. miR-204 Targeting of Ankrd13A Controls Both Mesenchymal Neural Crest and Lens Cell Migration. PLoS ONE. 2013;8(4):e61099. doi:10.1371/journal.pone.0061099 Shaham O, Gueta K, Mor E, Oren-Giladi P, Grinberg D, Xie Q, Cvekl A, Shomron N, Davis N, Keydar-Prizant M, Raviv S, Pasmanik-Chor M, Bell RE, Levy C, Avellino R, Banfi S, Conte I, Ashery-Padan R. Pax6 Regulates Gene Expression in the Vertebrate Lens through miR-204. PLoS Genet. 2013;9(3):e1003357. doi:10.1371/journal.pgen.1003357 Wei C, Thatcher EJ, Olena AF, Cha DJ, Perdigoto AL, Marshall AF, Carter BD, Broadie K, Patton JG. miR-153 Regulates SNAP-25, Synaptic Transmission, and Neuronal Development. PLoS One. 2013;8(2):e57080. doi: 10.1371/journal.pone.0057080. Epub 2013 Feb 25. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013 Feb 27. doi: 10.1038/nature11928. [Epub ahead of print]
Knockdown of dre-miR-7 Zhu Y, Wang D, Wang F, Li T, Dong L, Liu H, Ma Y, Jiang F, Yin H, Yan W, Luo M, Tang Z, Zhang G, Wang Q, Zhang J, Zhou J, Yu J. A comprehensive analysis of GATA-1-regulated miRNAs reveals miR-23a to be a positive modulator of erythropoiesis. Nucleic Acids Res. 2013 Feb 17. [Epub ahead of print] Kaluza D, Kroll J, Gesierich S, Manavski Y, Boeckel JN, Doebele C, Zelent A, Rössig L, Zeiher AM, Augustin HG, Urbich C, Dimmeler S. Histone Deacetylase 9 Promotes Angiogenesis by Targeting the Antiangiogenic MicroRNA 17-92 Cluster in Endothelial Cells. Arterioscler Thromb Vasc Biol. 2013 Jan 3. [Epub ahead of print] Chang SH, Lu YC, Li X, Hsieh WY, Xiong Y, Ghosh M, Evans T, Elemento O, Hla T. Antagonistic function of the RNA-binding protein HuR and miR-200b in post-transcriptional regulation of VEGF-A expression and angiogenesis. J Biol Chem. 2012;[Epub ahead of print]doi:10.1074/jbc.M112.423871 Lalwani MK, Sharma M, Singh AR, Chauhan RK, Patowary A, Singh N, Scaria V, Sivasubbu S. Reverse Genetics Screen in Zebrafish Identifies a Role of miR-142a-3p in Vascular Development and Integrity. PLoS ONE. 2012;7(12):e52588. doi:10.1371/journal.pone.0052588 Bridge G, Monteiro R, Henderson S, Emuss V, Lagos D, Georgopoulou D, Patient R, Boshoff C. The microRNA-30 family targets DLL4 to modulate endothelial cell behavior during angiogenesis. Blood 2012;[Epub ahead of print] doi:10.1182/blood-2012-04-423004
Target protector against the miR-30 site within the dll4 3′UTR. Chiavacci E, Dolfi L, Verduci L, Meghini F, Gestri G, Evangelista AMM, Wilson SW, Cremisi F, Pitto L. MicroRNA 218 Mediates the Effects of Tbx5a Over-Expression on Zebrafish Heart Development. PLoS ONE. 2012;7(11):e50536. doi:10.1371/journal.pone.0050536 Stahlhut C, Suárez Y, Lu J, Mishima Y, Giraldez AJ. miR-1 and miR-206 regulate angiogenesis by modulating VegfA expression in zebrafish. Development. 2012;139:4356-4365. doi:10.1242/dev.083774 Inui M, Montagner M, Ben-Zvi D, Martello G, Soligo S, Manfrin A, Aragona M, Enzo E, Zacchigna L, Zanconato F, Azzolin L, Dupont S, Cordenonsi M, Piccolo S. Self-regulation of the head-inducing properties of the Spemann organizer. Proc Natl Acad Sci U S A. 2012 Sep 4. [Epub ahead of print]
Xla-miR-15/16 Morpholinos in Xenopus laevis. Hassel D, Cheng P, White MP, Ivey KN, Kroll J, Augustin HG, Katus HA, Stainier DY, Srivastava D. miR-10 Regulates the Angiogenic Behavior of Zebrafish and Human Endothelial Cells by Promoting VEGF Signaling. Circ Res. 2012 Sep 5. [Epub ahead of print] Domínguez-Bendala J, Álvarez-Cubela S, Nieto M, Vargas N, Espino-Grosso P, Sacher VY, Pileggi A, García E, Ricordi C, Inverardi L, Pastori RL. Intracardial Embryonic Delivery of Developmental Modifiers In Utero. Cold Spring Harb Protoc. 2012;doi:10.1101/pdb.prot069427
Vivo-Morpholino targeting miRNA in mouse embryos. Nishiyama T, Kaneda R, Ono T, Tohyama S, Hashimoto H, Endo J, Tsuruta H, Yuasa S, Ieda M, Makino S, Fukuda K. miR-142-3p is essential for hematopoiesis and affects cardiac cell fate in zebrafish. Biochem Biophys Res Commun. 2012 Aug 2. [Epub ahead of print] Sessa R, Seano G, di Blasio L, Gagliardi PA, Isella C, Medico E, Cotelli F, Bussolino F, Primo L. The miR-126 regulates Angiopoietin-1 signaling and vessel maturation by targeting p85β. Biochim Biophys Acta. 2012 Jul 31. [Epub ahead of print] Liu X, Ning G, Meng A, Wang Q. MicroRNA-206 regulates cell movements during zebrafish gastrulation by targeting prickle1a and regulating JNK2 phosphorylation. Mol Cell Biol. 2012 May 21. [Epub ahead of print] Coolen M, Thieffry D, Drivenes Ø, Becker TS, Bally-Cuif L. miR-9 controls the timing of neurogenesis through the direct inhibition of antagonistic factors. Dev Cell. 2012 May 15;22(5):1052-64. doi: 10.1016/j.devcel.2012.03.003.
Target protector Furlong F, Fitzpatrick P, O'Toole S, Phelan S, McGrogan B, Maguire A, O'Grady A, Gallagher M, Prencipe M, McGoldrick A, McGettigan P, Brennan D, Sheils O, Martin C, W Kay E, O'Leary J, McCann A. Low MAD2 expression levels associate with reduced progression-free survival in patients with high-grade serous epithelial ovarian cancer. J Pathol. 2012 Apr;226(5):746-55. doi: 10.1002/path.3035. Epub 2012 Jan 17.
Target protector Biyashev D, Veliceasa D, Topczewski J, Topczewska JM, Mizgirev I, Vinokour E, Reddi AL, Licht JD, Revskoy SY, Volpert OV. miR-27b controls venous specification and tip cell fate. Blood. 2012 Mar 15;119(11):2679-87. doi: 10.1182/blood-2011-07-370635. Epub 2011 Dec 29. Zeng L, Childs SJ. The smooth muscle microRNA miR-145 regulates gut epithelial development via a paracrine mechanism. Dev Biol. 2012;[Epub ahead of print] doi:10.1016/j.ydbio.2012.05.009. Nicoli S, Knyphausen CP, Zhu LJ, Lakshmanan A, Lawson ND. miR-221 Is Required for Endothelial Tip Cell Behaviors during Vascular Development. Dev Cell. 2012 Feb 14;22(2):418-29.
dre-miR-221 Morpholino Mishima Y, Fukao A, Kishimoto T, Sakamoto H, Fujiwara T, Inoue K. Translational inhibition by deadenylation-independent mechanisms is central to microRNA-mediated silencing in zebrafish. Proc Natl Acad Sci U S A. 2012 Jan 24;109(4):1104-9. Epub 2012 Jan 9.
dre-miR-1/206 Morpholino. Urbich C, Kaluza D, Frömel T, Knau A, Bennewitz K, Boon RA, Bonauer A, Doebele C, Boeckel JN, Hergenreider E, Zeiher AM, Kroll J, Fleming I, Dimmeler S. MicroRNA-27a/b controls endothelial cell repulsion and angiogenesis by targeting semaphorin 6A. Blood. 2011 Dec 19. [Epub ahead of print]
miRNA knockdown in zebrafish embryos. Tal TL, Franzosa JA, Tilton SC, Philbrick KA, Iwaniec UT, Turner RT, Waters KM, Tanguay RL. MicroRNAs control neurobehavioral development and function in zebrafish. FASEB J. 2012 Jan 17. [Epub ahead of print] Dill H, Linder B, Fehr A, Fischer U. Intronic miR-26b controls neuronal differentiation by repressing its host transcript, ctdsp2. Genes Dev. 2012;26:25-30 doi:10.1101/gad.177774.111
Knockdown of miR-26b in zebrafish embryos. Baudet ML, Zivraj KH, Abreu-Goodger C, Muldal A, Armisen J, Blenkiron C, Goldstein LD, Miska EA, Holt CE. miR-124 acts through CoREST to control onset of Sema3A sensitivity in navigating retinal growth cones. Nat Neurosci. 2011 Dec 4;15(1):29-38. doi: 10.1038/nn.2979.
Electroporation in Xenopus laevis cells. Nieto M, Hevia P, Garcia E, Klein D, Alvarez-Cubela S, Bravo-Egana V, Rosero S, Molano RD, Vargas N, Ricordi C, Pileggi A, Diez J, Domínguez-Bendala J, Pastori RL. Anti sense miR-7 impairs insulin expression in developing pancreas and in cultured pancreatic buds. Cell Transplant. 2011 Dec 20. [Epub ahead of print] Laudadio I, Manfroid I, Achouri Y, Schmidt D, Wilson MD, Cordi S, Thorrez L, Knoops L, Jacquemin P, Schuit F, Pierreux CE, Odom DT, Peers B, Lemaigre FP. A feedback loop between the liver-enriched transcription factor network and miR-122 controls hepatocyte differentiation. Gastroenterology. 2012 Jan;142(1):119-29. doi: 10.1053/j.gastro.2011.09.001. Epub 2011 Sep 12. Le MTN, Shyh-Chang N, Khaw SL, Chin L, Teh C, Tay J, O'Day E, Korzh V, Yang H, Lal A, Lieberman J, Lodish HF, Lim B. Conserved Regulation of p53 Network Dosage by MicroRNA–125b Occurs through Evolving miRNA–Target Gene Pairs. PLoS Genet. 2011;7(9): e1002242. doi:10.1371/journal.pgen.1002242 Lagendijk AK, Goumans MJ, Burkhard SB, Bakkers J. MicroRNA-23 Restricts Cardiac Valve Formation by Inhibiting Has2 and Extracellular Hyaluronic Acid Production. Circ Res. 2011 Sep 2;109(6):649-57. Epub 2011 Jul 21. He X, Yan YL, Eberhart JK, Herpin A, Wagner TU, Schartl M, Postlethwait JH. miR-196 regulates axial patterning and pectoral appendage initiation. Dev Biol. 2011 Jul 20. [Epub ahead of print] Kapsimali M, Kaushik A-L, Gibon G, Dirian L, Ernest S, Rosa FM. Fgf signaling controls pharyngeal taste bud formation through miR-200 and Delta-Notch activity. Development. 2011;138:3473-84. doi:10.1242/dev.058669
Knockdowns of miR-200a, miR-200b and/or miR-429. Marcet B, Chevalier B, Luxardi G, Coraux C, Zaragosi LE, Cibois M, Robbe-Sermesant K, Jolly T, Cardinaud B, Moreilhon C, Giovannini-Chami L, Nawrocki-Raby B, Birembaut P, Waldmann R, Kodjabachian L, Barbry P. Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat Cell Biol. 2011 May 22. [Epub ahead of print]
Morpholino targeting miR-499 and a Dll1 target protector. Miyasaka KY, Kida YS, Banjo T, Ueki Y, Nagayama K, Matsumoto T, Sato M, Ogura T. Heartbeat regulates cardiogenesis by suppressing retinoic acid signaling via expression of miR-143. Mech Dev. 2011 Jan-Feb;128(1-2):18-28. Epub 2010 Sep 30. Shieh JTC, Huang Y, Gilmore J, Srivastava D. Elevated miR-499 Levels Blunt the Cardiac Stress Response. PLoS ONE. 2011;6(5):e19481. doi:10.1371/journal.pone.0019481
Oligo targeting miR-499 electroporated into ventricular cardiomyocyte line H9c2. Gilligan PC, Kumari P, Lim S, Cheong A, Chang A, Sampath K. Conservation defines functional motifs in the squint/nodal-related 1 RNA dorsal localization element. Nucleic Acids Res. 2011 Apr 1;39(8):3340-9. Epub 2010 Dec 10.
Target protector Li N, Wei C, Olena AF, Patton JG. Regulation of endoderm formation and left-right asymmetry by miR-92 during early zebrafish development. Development. 2011 May;138(9):1817-26. Epub 2011 Mar 29. Yu YM, Gibbs KM, Davila J, Campbell N, Sung S, Todorova TI, Otsuka S, Sabaawy HE, Hart RP, Schachner M. MicroRNA miR-133b is essential for functional recovery after spinal cord injury in adult zebrafish. Eur J Neurosci. 2011 May;33(9):1587-97. doi: 10.1111/j.1460-9568.2011.07643.x. Epub 2011 Mar 30.
Morpholino solution soaked on Gelfoam and applied to lesion. Fish JE, Wythe JD, Xiao T, Bruneau BG, Stainier DY, Srivastava D, Woo S. A Slit/miR-218/Robo regulatory loop is required during heart tube formation in zebrafish. Development. 2011 Apr;138(7):1409-19. Hwang-Verslues WW, Chang PH, Wei PC, Yang CY, Huang CK, Kuo WH, Shew JY, Chang KJ, Lee EY, Lee WH. miR-495 is upregulated by E12/E47 in breast cancer stem cells, and promotes oncogenesis and hypoxia resistance via downregulation of E-cadherin and REDD1. Oncogene. 2011 Jan 24. [Epub ahead of print] Staton AA, Knaut H, Giraldez AJ. miRNA regulation of Sdf1 chemokine signaling provides genetic robustness to germ cell migration. Nat Genet. 2011 Jan 23. [Epub ahead of print]
Target protectors Bonev B, Pisco A, Papalopulu N. MicroRNA-9 Reveals Regional Diversity of Neural Progenitors along the Anterior-Posterior Axis. Dev Cell. 2011 Jan 18;20(1):19-32.
Targeting Xtr-miR-9 and target protecting hairy1. Zou J, Li WQ, Li Q, Li XQ, Zhang JT, Liu GQ, Chen J, Qiu XX, Tian FJ, Wang ZZ, Zhu N, Qin YW, Shen B, Liu TX, Jing Q. Two Functional MicroRNA-126s Repress a Novel Target Gene p21-Activated Kinase 1 to Regulate Vascular Integrity in Zebrafish. Circ Res. 2010 Dec 9. [Epub ahead of print] Ghosh G, Subramanian IV, Adhikari N, Zhang X, Joshi HP, Basi D, Chandrashekhar YS, Hall JL, Roy S, Zeng Y, Ramakrishnan S. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-α isoforms and promotes angiogenesis. J Clin Invest. 2010 Oct 25. pii: 42980. doi: 10.1172/JCI42980. [Epub ahead of print] Conte I, Carrella S, Avellino R, Karali M, Marco-Ferreres R, Bovolenta P, Banfi S. miR-204 is required for lens and retinal development via Meis2 targeting. Proc Natl Acad Sci U S A. 2010 Aug 16. [Epub ahead of print] Yu D, dos Santos CO, Zhao G, Jiang J, Amigo JD, Khandros E, Dore LC, Yao Y, D'Souza J, Zhang Z, Ghaffari S, Choi J, Friend S, Tong W, Orange JS, Paw BH, Weiss MJ. miR-451 protects against erythroid oxidant stress by repressing 14-3-3zeta. Genes Dev. 2010 Aug 1;24(15):1620-33. Pedrioli DM, Karpanen T, Dabouras V, Jurisic G, van de Hoek G, Shin JW, Marino D, Kälin RE, Leidel S, Cinelli P, Schulte-Merker S, Brändli AW, Detmar M. miR-31 functions as a negative regulator of lymphatic vascular lineage-specific differentiation in vitro and vascular development in vivo. Mol Cell Biol. 2010 Jul;30(14):3620-34. Epub 2010 May 17. Deacon DC, Nevis KR, Cashman TJ, Zhou Y, Zhao L, Washko D, Guner-Ataman B, Burns CG, Burns CE. The miR-143-adducin3 pathway is essential for cardiac chamber morphogenesis. Development. 2010 Jun;137(11):1887-96.
See supplemental online information for comparison figure of various Morpholino oligos targeting dre-miR-143 on guide or star strands. Long J, Wang Y, Wang W, Chang BH, Danesh FR. Identification of MicroRNA-93 as a novel regulator of vascular endothelial growth factor (VEGF) in hyperglycemic conditions. J Biol Chem. 2010 May 25. [Epub ahead of print]
Delivery note: abstract mentions peptide-conjugated Morpholino oligomers, but mat'l and methods describes Endo-Porter. Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND. MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature. 2010 Apr 4. [Epub ahead of print] Hsu RJ, Lin CY, Hoi HS, Zheng SK, Lin CC, Tsai HJ. Novel intronic microRNA represses zebrafish myf5 promoter activity through silencing dickkopf-3 gene. Nucleic Acids Res. 2010 Mar 17. [Epub ahead of print] Zhao X, He X, Han X, Yu Y, Ye F, Chen Y, Hoang T, Xu X, Mi QS, Xin M, Wang F, Appel B, Lu QR. MicroRNA-Mediated Control of Oligodendrocyte Differentiation. Neuron. 2010 Mar 11;65(5):612-626. Li H, Kloosterman W, Fekete DM. MicroRNA-183 Family Members Regulate Sensorineural Fates in the Inner Ear. J Neurosci. 2010 Mar 3;30(9):3254-63. Hu H, Du L, Nagabayashi G, Seeger RC, Gatti RA. ATM is down-regulated by N-Myc-regulated microRNA-421. Proc Natl Acad Sci U S A. 2010 Jan 4. [Epub ahead of print] Sheedy FJ, Palsson-McDermott E, Hennessy EJ, Martin C, O'Leary J, Ruan Q, Johnson DP, Chen Y, O'Neill LA. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol. 2009 Nov 29. [Epub ahead of print]
NOTE: Target protector for miR-21 Agrawal R, Tran U, Wessely O. The miR-30 miRNA family regulates Xenopus pronephros development and targets the transcription factor Xlim1/Lhx1. Development. 2009 Dec;136(23):3927-36. Zeng L, Carter AD, Childs SJ. miR-145 directs intestinal maturation in zebrafish. Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17793-8. Epub 2009 Oct 5. Weiss FU, Marques IJ, Woltering JM, Vlecken DH, Aghdassi A, Partecke LI, Heidecke CD, Lerch MM, Bagowski CP. Retinoic acid receptor (RAR) antagonists inhibit miR-10a expression and block metastatic behaviour of pancreatic cancer. Gastroenterology. 2009 Sep 9. [Epub ahead of print] Lin Z, Murtaza I, Wang K, Jiao J, Gao J, Li PF. miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proc Natl Acad Sci U S A. 2009 Jul 2. [Epub ahead of print]
NOTE: target protector strategy used Walker JC, Harland RM. microRNA-24a is required to repress apoptosis in the developing neural retina. Genes Dev. 2009 May 1;23(9):1046-51. Epub 2009 Apr 16. Le MT, Teh C, Shyh-Chang N, Xie H, Zhou B, Korzh V, Lodish HF, Lim B. MicroRNA-125b is a novel negative regulator of p53. Genes Dev. 2009 Apr 1;23(7):862-76. Epub 2009 Mar 17. Flynt AS, Thatcher EJ, Burkewitz K, Li N, Liu Y, Patton JG. miR-8 microRNAs regulate the response to osmotic stress in zebrafish embryos. J Cell Biol. 2009 Mar 30. [Epub ahead of print] Mishima Y, Abreu-Goodger C, Staton AA, Stahlhut C, Shou C, Cheng C, Gerstein M, Enright AJ, Giraldez AJ. Zebrafish miR-1 and miR-133 shape muscle gene expression and regulate sarcomeric actin organization. Genes Dev. 2009 Feb 24. [Epub ahead of print] Du TT, Fu YF, Dong M, Wang L, Fan HB, Chen Y, Jin Y, Chen SJ, Chen Z, Deng M, Huang QH, Liu TX. Experimental validation and complexity of miRNA-mRNA target interaction during zebrafish primitive erythropoiesis. Biochem Biophys Res Commun. 2009 Apr 17;381(4):688-93. Epub 2009 Feb 28. Thatcher EJ, Paydar I, Anderson KK, Patton JG. Regulation of zebrafish fin regeneration by microRNAs. Proc Natl Acad Sci U S A. 2008 Nov 25;105(47):18384-9. Epub 2008 Nov 17.
NOTE: Electroporation of Morpholinos into fins Zhang MC, Lv Y, Qi YT, Zhang Z, Fu XN, Yuan CG, Lai LH. [Knockdown and overexpression of miR-219 lead to embryonic defects in zebrafish development] Fen Zi Xi Bao Sheng Wu Xue Bao. 2008 Oct;41(5):341-8. Chinese. Pase L, Layton JE, Kloosterman WP, Carradice D, Waterhouse PM, Lieschke GJ. miR-451 regulates zebrafish erythroid maturation in vivo via its target gata2. Blood. 2008 Oct 10. [Epub ahead of print] Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, Ivey KN, Bruneau BG, Stainier DY, Srivastava D. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008 Aug;15(2):272-84. Li N, Flynt AS, Kim HR, Solnica-Krezel L, Patton JG. Dispatched Homolog 2 is targeted by miR-214 through a combination of three weak microRNA recognition sites. Nucleic Acids Res. 2008 Jun 26. [Epub ahead of print]
NOTE: target protector strategy used Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L. MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci. 2008 Jun;11(6):641-648. Epub 2008 May 4. Yin VP, Thomson JM, Thummel R, Hyde DR, Hammond SM, Poss KD. Fgf-dependent depletion of microRNA-133 promotes appendage regeneration in zebrafish. Genes Dev. 2008 Mar 15;22(6):728-33.
NOTE: Electroporation of Morpholinos into fins Dore LC, Amigo JD, Dos Santos CO, Zhang Z, Gai X, Tobias JW, Yu D, Klein AM, Dorman C, Wu W, Hardison RC, Paw BH, Weiss MJ. A GATA-1-regulated microRNA locus essential for erythropoiesis. Proc Natl Acad Sci U S A. 2008 Feb 26; [Epub ahead of print] Eberhart JK, He X, Swartz ME, Yan YL, Song H, Boling TC, Kunerth AK, Walker MB, Kimmel CB, Postlethwait JH. MicroRNA Mirn140 modulates Pdgf signaling during palatogenesis. Nat Genet. 2008 Feb 10; [Epub ahead of print] Choi PS, Zakhary L, Choi WY, Caron S, Alvarez-Saavedra E, Miska EA, McManus M, Harfe B, Giraldez AJ, Horvitz RH, Schier AF, Dulac C. Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron. 2008 Jan 10;57(1):41-55. Woltering JM, Durston AJ. MiR-10 represses HoxB1a and HoxB3a in zebrafish. PLoS ONE. 2008 Jan 2;3(1):e1396. Lin YC, Hsieh LC, Kuo MW, Yu J, Kuo HH, Lo WL, Lin RJ, Yu AL, Li WH. Human TRIM71 and Its Nematode Homologue are Targets of let-7 MicroRNA and Its Zebrafish Orthologue is Essential for Development. Mol Biol Evol. 2007 Sep 21; [Epub ahead of print] An miRNA's target site on an mRNA can be protected by a complementary Morpholino oligo.
Choi WY, Giraldez AJ, Schier AF. Target Protectors Reveal Dampening and Balancing of Nodal Agonist and Antagonist by miR-430. Science. 2007 Oct 12;318(5848):271-4. Epub 2007 Aug 30. Martello G, Zacchigna L, Inui M, Montagner M, Adorno M, Mamidi A, Morsut L, Soligo S, Tran U, Dupont S, Cordenonsi M, Wessely O & Piccolo S. MicroRNA control of Nodal signalling. Nature 2007 Sep 13;449(7159):183-8. Epub 2007 Aug 29 A Gene Tools collaboration with Wigard Kloosterman, first of Ronald Plasterk's lab then Rene Ketting's lab at the Hubrecht Institute in the Netherlands, has shown that Morpholino oligos can strongly inhibit the activity of miRNAs in zebrafish so that, after Morphoino treatment, the miRNA signal from in-situ hybridization and Northern blots is decreased or absent. Knockdowns of miRNA activity have generally used oligos targeting the miRNA guide strand. A Morpholino oligo targeting an miRNA guide strand can interfere with the activity of the miRNA. It is difficult to control for the specificity of the knockdown when using this technique alone. However, Morpholinos targeting the nucleolytic processing sites of an immature miRNA can prevent maturation of the miRNA. This allows sets of nonoverlapping Morpholino oligos targeting a primary miRNA to be used as specificity controls; if two non-overlapping oligos targeting the same miRNA (typically targeting the 5p and 3p sites) produce the same phenotype, this supports the hypothesis that the phenotype is due to knocking down the activity of the targeted miRNA and not due to an off-target effect. These techniques are explored in the following paper:
Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RHA. Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol. 2007;5(8): e203.
Wigard Kloosterman also describes targeting miRNAs with Morpholinos in his dissertation, The expression and function of microRNAs in vertebrate embryonic development This is the first published report we've found of data from miRNA knockdown using Morpholinos.
Flynt AS, Li N, Thatcher EJ, Solnica-Krezel L, Patton JG. Zebrafish miR-214 modulates Hedgehog signaling to specify muscle cell fate. Nature Genetics 2007; 39: 259 - 263. The following paper primarily reports experiments with 2'-O-methyl oligos but the authors also report that Morpholinos are effective in this application, though no data for the Morpholino knockdowns is shown.
Kloosterman WP, Wienholds E, Ketting RF, Plasterk RH. Substrate requirements for let-7 function in the developing zebrafish embryo. Nucleic Acids Res. 2004 Dec 07;32(21):6284-91.