Regulation of zebrafish heart regeneration by miR-133

Developmental Biology

Volumn 365, Issue 2, 2012, Pages 319-327

  Yin, Viravuth P ^a,b   Lepilina, Alexandra ^a   Smith, Ashley ^b   Poss, Kenneth D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

Author keywords

Heart; MicroRNAs; MiR 133; Regeneration; Zebrafish

Indexed keywords

CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 37; CLAUDIN 5; CONNEXIN 43; MEMBRANE PROTEIN; MICRORNA; PROTEIN MPS1; PROTEIN PA2G4; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; HEART; HEART MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; TISSUE REGENERATION; ZEBRA FISH;

DANIO RERIO;

EID: 84859989029     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.02.018     Document Type: Article

References (45)

1. Bergmann O., Bhardwaj R.D., Bernard S., Zdunek S., Barnabe-Heider F., Walsh S., Zupicich J., Alkass K., Buchholz B.A., Druid H., Jovinge S., Frisen J. Evidence for cardiomyocyte renewal in humans. Science 2009, 324:98-102.
2. Bruce A.F., Rothery S., Dupont E., Severs N.J. Gap junction remodelling in human heart failure is associated with increased interaction of connexin43 with ZO-1. Cardiovasc. Res. 2008, 77:757-765.
3. Care A., Catalucci D., Felicetti F., Bonci D., Addario A., Gallo P., Bang M.L., Segnalini P., Gu Y., Dalton N.D., Elia L., Latronico M.V., Hoydal M., Autore C., Russo M.A., Dorn G.W., Ellingsen O., Ruiz-Lozano P., Peterson K.L., Croce C.M., Peschle C., Condorelli G. MicroRNA-133 controls cardiac hypertrophy. Nat. Med. 2007, 13:613-618.
4. Chablais F., Veit J., Rainer G., Jazwinska A. The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC Dev. Biol. 2011, 11:21.
5. Ebert M.S., Neilson J.R., Sharp P.A. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 2007, 4:721-726.
6. Flynt A.S., Li N., Thatcher E.J., Solnica-Krezel L., Patton J.G. Zebrafish miR-214 modulates Hedgehog signaling to specify muscle cell fate. Nat. Genet. 2007, 39:259-263.
7. Formigli L., Ibba-Manneschi L., Perna A.M., Pacini A., Polidori L., Nediani C., Modesti P.A., Nosi D., Tani A., Celli A., Neri-Serneri G.G., Quercioli F., Zecchi-Orlandini S. Altered Cx43 expression during myocardial adaptation to acute and chronic volume overloading. Histol. Histopathol. 2003, 18:359-369.
8. Giraldez A.J., Cinalli R.M., Glasner M.E., Enright A.J., Thomson J.M., Baskerville S., Hammond S.M., Bartel D.P., Schier A.F. MicroRNAs regulate brain morphogenesis in zebrafish. Science 2005, 308:833-838.
9. Gonzalez-Rosa J.M., Martin V., Peralta M., Torres M., Mercader N. Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 2011, 138:1663-1674.
10. He L., Hannon G.J. MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 2004, 5:522-531.
11. Jopling C., Sleep E., Raya M., Marti M., Raya A., Belmonte J.C. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010, 464:606-609.
12. Kedersha N., Stoecklin G., Ayodele M., Yacono P., Lykke-Andersen J., Fritzler M.J., Scheuner D., Kaufman R.J., Golan D.E., Anderson P. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 2005, 169:871-884.
13. Kikuchi K., Holdway J.E., Werdich A.A., Anderson R.M., Fang Y., Egnaczyk G.F., Evans T., Macrae C.A., Stainier D.Y., Poss K.D. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 2010, 464:601-605.
14. + epicardial cells adopt non-myocardial fates during zebrafish heart development and regeneration. Development 2011, 138:2895-2902.
15. Kikuchi K., Holdway J.E., Major R.J., Blum N., Dahn R.D., Begemann G., Poss K.D. Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev. Cell 2011, 20:397-404.
16. Kim J., Wu Q., Zhang Y., Wiens K.M., Huang Y., Rubin N., Shimada H., Handin R.I., Chao M.Y., Tuan T.L., Starnes V.A., Lien C.L. PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17206-17210.
17. Kloosterman W.P., Wienholds E., de Bruijn E., Kauppinen S., Plasterk R.H. In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nat. Methods 2006, 3:27-29.
18. Kostin S., Dammer S., Hein S., Klovekorn W.P., Bauer E.P., Schaper J. Connexin 43 expression and distribution in compensated and decompensated cardiac hypertrophy in patients with aortic stenosis. Cardiovasc. Res. 2004, 62:426-436.
19. Lepilina A., Coon A.N., Kikuchi K., Holdway J.E., Roberts R.W., Burns C.G., Poss K.D. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 2006, 127:607-619.
20. Leung A.K., Sharp P.A. microRNAs: a safeguard against turmoil?. Cell 2007, 130:581-585.
21. Leung A.K., Calabrese J.M., Sharp P.A. Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18125-18130.
22. Lin N., Friedlander R.M. Regeneration of neuromuscular synapses: action of microRNA-206. Neurosurgery 2010, 66:N19-N20.
23. Liu N., Bezprozvannaya S., Williams A.H., Qi X., Richardson J.A., Bassel-Duby R., Olson E.N. microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev. 2008, 22:3242-3254.
24. Loya C.M., Lu C.S., Van Vactor D., Fulga T.A. Transgenic microRNA inhibition with spatiotemporal specificity in intact organisms. Nat. Methods 2009, 6:897-903.
25. Marquez R.T., Wendlandt E., Galle C.S., Keck K., McCaffrey A.P. MicroRNA-21 is upregulated during the proliferative phase of liver regeneration, targets Pellino-1, and inhibits NF-kappaB signaling. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298:G535-G541.
26. Matkovich S.J., Wang W., Tu Y., Eschenbacher W.H., Dorn L.E., Condorelli G., Diwan A., Nerbonne J.M., Dorn G.W. MicroRNA-133a protects against myocardial fibrosis and modulates electrical repolarization without affecting hypertrophy in pressure-overloaded adult hearts. Circ. Res. 2010, 106:166-175.
27. Mays T.A., Binkley P.F., Lesinski A., Doshi A.A., Quaile M.P., Margulies K.B., Janssen P.M., Rafael-Fortney J.A. Claudin-5 levels are reduced in human end-stage cardiomyopathy. J. Mol. Cell. Cardiol. 2008, 45:81-87.
28. Oviedo N.J., Levin M. smedinx-11 is a planarian stem cell gap junction gene required for regeneration and homeostasis. Development 2007, 134:3121-3131.
29. Oviedo N.J., Morokuma J., Walentek P., Kema I.P., Gu M.B., Ahn J.M., Hwang J.S., Gojobori T., Levin M. Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration. Dev. Biol. 2010, 339:188-199.
30. Poss K.D., Nechiporuk A., Hillam A.M., Johnson S.L., Keating M.T. Mps1 defines a proximal blastemal proliferative compartment essential for zebrafish fin regeneration. Development 2002, 129:5141-5149.
31. Poss K.D., Wilson L.G., Keating M.T. Heart regeneration in zebrafish. Science 2002, 298:2188-2190.
32. Sanford J.L., Edwards J.D., Mays T.A., Gong B., Merriam A.P., Rafael-Fortney J.A. Claudin-5 localizes to the lateral membranes of cardiomyocytes and is altered in utrophin/dystrophin-deficient cardiomyopathic mice. J. Mol. Cell. Cardiol. 2005, 38:323-332.
33. Sayed D., Hong C., Chen I.Y., Lypowy J., Abdellatif M. MicroRNAs play an essential role in the development of cardiac hypertrophy. Circ. Res. 2007, 100:416-424.
34. Schnabel K., Wu C.C., Kurth T., Weidinger G. Regeneration of cryoinjury induced necrotic heart lesions in zebrafish is associated with epicardial activation and cardiomyocyte proliferation. PLoS One 2011, 6:e18503.
35. Sehm T., Sachse C., Frenzel C., Echeverri K. miR-196 is an essential early-stage regulator of tail regeneration, upstream of key spinal cord patterning events. Dev. Biol. 2009, 334:468-480.
36. Small E.M., Frost R.J., Olson E.N. MicroRNAs add a new dimension to cardiovascular disease. Circulation 2010, 121:1022-1032.
37. Song M., Yu X., Cui X., Zhu G., Zhao G., Chen J., Huang L. Blockade of connexin 43 hemichannels reduces neointima formation after vascular injury by inhibiting proliferation and phenotypic modulation of smooth muscle cells. Exp. Biol. Med. (Maywood) 2009, 234:1192-1200.
38. Thatcher E.J., Paydar I., Anderson K.K., Patton J.G. Regulation of zebrafish fin regeneration by microRNAs. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:18384-18389.
39. Thum T., Gross C., Fiedler J., Fischer T., Kissler S., Bussen M., Galuppo P., Just S., Rottbauer W., Frantz S., Castoldi M., Soutschek J., Koteliansky V., Rosenwald A., Basson M.A., Licht J.D., Pena J.T., Rouhanifard S.H., Muckenthaler M.U., Tuschl T., Martin G.R., Bauersachs J., Engelhardt S. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008, 456:980-984.
40. Tseng A.S., Beane W.S., Lemire J.M., Masi A., Levin M. Induction of vertebrate regeneration by a transient sodium current. J. Neurosci. 2010, 30:13192-13200.
41. van Rooij E., Sutherland L.B., Qi X., Richardson J.A., Hill J., Olson E.N. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 2007, 316:575-579.
42. Wang J., Panakova D., Kikuchi K., Holdway J.E., Gemberling M., Burris J.S., Singh S.P., Dickson A.L., Lin Y.F., Sabeh M.K., Werdich A.A., Yelon D., Macrae C.A., Poss K.D. The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 2011, 138:3421-3430.
43. Wills A.A., Holdway J.E., Major R.J., Poss K.D. Regulated addition of new myocardial and epicardial cells fosters homeostatic cardiac growth and maintenance in adult zebrafish. Development 2008, 135:183-192.
44. Yin V.P., Thomson J.M., Thummel R., Hyde D.R., Hammond S.M., Poss K.D. Fgf-dependent depletion of microRNA-133 promotes appendage regeneration in zebrafish. Genes Dev. 2008, 22:728-733.
45. Yu S., Li G. MicroRNA expression and function in cardiac ischemic injury. J. Cardiovasc. Transl. Res. 2010, 3:241-245.