Dynamic microrna-101a and fosab expression controls zebrafish heart regeneration

Development (Cambridge)

Volumn 142, Issue 23, 2015, Pages 4029-4037

  Beauchemin, Megan ^a,b   Smith, Ashley ^a   Yin, Viravuth P ^a,b  

^a MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

^b UNIVERSITY OF MAINE   (United States)

Author keywords

Cardiomyocyte proliferation; Fosab; Heart regeneration; MicroRNA 101a; Scarring; Zebrafish

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; MICRORNA 101; MICRORNA 101A; PROTEIN C FOS; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN; MICRORNA; MIRN101A, ZEBRAFISH; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; HEART; HEART INJURY; HEART MUSCLE CELL; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCAR; TISSUE REGENERATION; UPREGULATION; ZEBRA FISH; ANIMAL; CARDIAC MUSCLE CELL; CARDIOVASCULAR SYSTEM; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NECROSIS; PATHOLOGY; PHYSIOLOGY; REGENERATION; TIME FACTOR; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARDIOVASCULAR SYSTEM; CELL PROLIFERATION; CICATRIX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HEART; MICRORNAS; MYOCYTES, CARDIAC; NECROSIS; OLIGONUCLEOTIDES, ANTISENSE; PROTO-ONCOGENE PROTEINS C-FOS; REGENERATION; TIME FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84949425787     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.126649     Document Type: Article

References (56)

1. Aguirre, A., Montserrat, N., Zacchigna, S., Nivet, E., Hishida, T., Krause, M. N., Kurian, L., Ocampo, A., Vazquez-Ferrer, E., Rodriguez-Esteban, C. et al. (2014). In vivo activation of a conserved microRNA program induces mammalian heart regeneration. Cell Stem Cell 15, 589-604
2. Aurora, A. B., Porrello, E. R., Tan, W., Mahmoud, A. I., Hill, J. A., Bassel-Duby, R., Sadek, H. A. and Olson, E. N. (2014). Macrophages are required for neonatal heart regeneration. J. Clin. Invest. 124, 1382-1392
3. Bergmann, O., Bhardwaj, R. D., Bernard, S., Zdunek, S., Barnabe-Heider, F., Walsh, S., Zupicich, J., Alkass, K., Buchholz, B. A., Druid, H. et al. (2009). Evidence for cardiomyocyte renewal in humans. Science 324, 98-102
4. Bernstein, E., Kim, S. Y., Carmell, M. A., Murchison, E. P., Alcorn, H., Li, M. Z., Mills, A. A., Elledge, S. J., Anderson, K. V. and Hannon, G. J. (2003). Dicer is essential for mouse development. Nat. Genet. 35, 215-217
5. Carvalho, J., van Grieken, N. C., Pereira, P. M., Sousa, S., Tijssen, M., Buffart, T. E., Diosdado, B., Grabsch, H., Santos, M. A. S., Meijer, G. et al. (2012). Lack of microRNA-101 causes E-cadherin functional deregulation through EZH2 upregulation in intestinal gastric cancer. J. Pathol. 228, 31-44
6. Chablais, F. and Jazwinska, A. (2012). The regenerative capacity of the zebrafish heart is dependent on TGFbeta signaling. Development 139, 1921-1930
7. Chablais, F., Veit, J., Rainer, G. and Jaźwińska, A. (2011). The zebrafish heart regenerates after cryoinjury-induced myocardial infarction. BMC Dev. Biol. 11, 21
8. Elmén, J, Lindow, M., Schütz, S., Lawrence, M., Petri, A., Obad, S., Lindholm, M., Hedtjärn, M., Hansen, H. F., Berger, U.. (2008). LNA-mediated microRNA silencing in non-human primates. Nature 452, 896-899
9. Eulalio, A., Mano, M., Dal Ferro, M., Zentilin, L., Sinagra, G., Zacchigna, S. and Giacca, M. (2012). Functional screening identifies miRNAs inducing cardiac regeneration. Nature 492, 376-381
10. Fang, Y., Gupta, V., Karra, R., Holdway, J. E., Kikuchi, K. and Poss, K. D. (2013). Translational profiling of cardiomyocytes identifies an early Jak1/Stat3 injury response required for zebrafish heart regeneration. Proc. Natl. Acad. Sci. USA 110, 13416-13421
11. Gemberling, M., Karra, R., Dickson, A. L. and Poss, K. D. (2015). Nrg1 is an injury-induced cardiomyocyte mitogen for the endogenous heart regeneration program in zebrafish. eLife 4, e05871
12. Giraldez, A. J., Cinalli, R. M., Glasner, M. E., Enright, A. J., Thomson, J. M., Baskerville, S., Hammond, S. M., Bartel, D. P. and Schier, A. F. (2005). MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833-838
13. Godwin, J. W., Pinto, A. R. and Rosenthal, N. A. (2013). Macrophages are required for adult salamander limb regeneration. Proc. Natl. Acad. Sci. USA 110, 9415-9420
14. Gonzalez-Rosa, J. M., Martin, V., Peralta, M., Torres, M. and Mercader, N. (2011). Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 138, 1663-1674
15. Gupta, V., Gemberling, M., Karra, R., Rosenfeld, G. E., Evans, T. and Poss, K. D. (2013). An injury-responsive gata4 program shapes the zebrafish cardiac ventricle. Curr. Biol. 23, 1221-1227
16. Ha, M. and Kim, V. N. (2014). Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15, 509-524
17. Hatfield, S. D., Shcherbata, H. R., Fischer, K. A., Nakahara, K., Carthew, R. W. and Ruohola-Baker, H. (2005). Stem cell division is regulated by the microRNA pathway. Nature 435, 974-978
18. Haubner, B. J., Adamowicz-Brice, M., Khadayate, S., Tiefenthaler, V., Metzler, B., Aitman, T. and Penninger, J. M. (2012). Complete cardiac regeneration in a mouse model of myocardial infarction. Aging 4, 966-977
19. Hodgkinson, C. P., Kang, M. H., Dal-Pra, S., Mirotsou, M. and Dzau, V. J. (2015). MicroRNAs and cardiac regeneration. Circ. Res. 116, 1700-1711
20. Huang, Y., Harrison, M. R., Osorio, A., Kim, J., Baugh, A., Duan, C., Sucov, H. M. and Lien, C.-L. (2013). Igf signaling is required for cardiomyocyte proliferation during zebrafish heart development and regeneration. PLoS ONE 8, e67266
21. Jepsen, J. S., Sørensen, M. D. and Wengel, J. (2004). Locked nucleic acid: a potent nucleic acid analog in therapeutics and biotechnology. Oligonucleotides 14, 130-146
22. Jopling, C., Sleep, E., Raya, M., Martí, M., Raya, A. and Izpisua Belmonte, J. C. (2010). Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464, 606-609
23. Jopling, C., Suñé, G., Morera, C. and Izpisua Belmonte, J. C. (2012). p38alpha MAPK regulates myocardial regeneration in zebrafish. Cell Cycle 11, 1195-1201
24. Kikuchi, K. (2014). Advances in understanding the mechanism of zebrafish heart regeneration. Stem Cell Res. 13, 542-555
25. Kikuchi, K., Holdway, J. E., Werdich, A. A., Anderson, R. M., Fang, Y., Egnaczyk, G. F., Evans, T., MacRae, C. A., Stainier, D. Y. R. and Poss, K. D. (2010). Primary contribution to zebrafish heart regeneration by gata4+ cardiomyocytes. Nature 464, 601-605
26. Kikuchi, K., Holdway, J. E., Major, R. J., Blum, N., Dahn, R. D., Begemann, G. and Poss, K. D. (2011). Retinoic acid production by endocardiumand epicardium is an injury response essential for zebrafish heart regeneration. Dev. Cell 20, 397-404
27. Kim, V. N. (2005). Small RNAs: classification, biogenesis, and function. Mol. Cells 19, 1-15
28. Kim, J., Wu, Q., Zhang, Y., Wiens, K. M., Huang, Y., Rubin, N., Shimada, H., Handin, R. I., Chao, M. Y., Tuan, T.-L. et al. (2010). PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc. Natl. Acad. Sci. USA 107, 17206-17210
29. Kloosterman, W. P. and Plasterk, R. H. A. (2006). The diverse functions of microRNAs in animal development and disease. Dev. Cell 11, 441-450
30. Kohlhapp, F. J., Mitra, A. K., Lengyel, E. and Peter, M. E. (2015). MicroRNAs as mediators and communicators between cancer cells and the tumor microenvironment. Oncogene, doi:10.1038/onc.2015.89
31. Kumar, R., Singh, S. K., Koshkin, A. A., Rajwanshi, V. K., Meldgaard, M. and Wengel, J. (1998). The first analogues of LNA (locked nucleic acids): phosphorothioate-LNA and 2′-thio-LNA. Bioorg. Med. Chem. Lett. 8, 2219-2222
32. Lee, R. C., Feinbaum, R. L. and Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 Cell 75, 843-854
33. Lepilina, A., Coon, A. N., Kikuchi, K., Holdway, J. E., Roberts, R. W., Burns, C. G. and Poss, K. D. (2006). A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127, 607-619
34. Liu, N., Bezprozvannaya, S., Williams, A. H., Qi, X., Richardson, J. A., Bassel- Duby, R. and Olson, E. N. (2008). microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev. 22, 3242-3254
35. Liu, J.-J., Lin, X.-J., Yang, X.-J., Zhou, L., He, S., Zhuang, S.-M. and Yang, J. (2014). A novel AP-1/miR-101 regulatory feedback loop and its implication in the migration and invasion of hepatoma cells. Nucleic Acids Res. 42, 12041-12051
36. Naqvi, N., Li, M., Calvert, J.W., Tejada, T., Lambert, J. P., Wu, J., Kesteven, S. H., Holman, S. R., Matsuda, T., Lovelock, J. D. et al. (2014). A proliferative burst during preadolescence establishes the final cardiomyocyte number. Cell 157, 795-807
37. Odden, M. C., Coxson, P. G., Moran, A., Lightwood, J. M., Goldman, L. and Bibbins-Domingo, K. (2011). The impact of the aging population on coronary heart disease in the U.S. Am. J. Med. 124, 827-833
38. Pan, Z., Sun, X., Shan, H., Wang, N., Wang, J., Ren, J., Feng, S., Xie, L., Lu, C., Yuan, Y. et al. (2012). MicroRNA-101 inhibited postinfarct cardiac fibrosis and improved left ventricular compliance via the FBJ osteosarcoma oncogene/ transforming growth factor-beta1 pathway. Circulation 126, 840-850
39. Petrie, T. A., Strand, N. S., Tsung-Yang, C., Rabinowitz, J. S. and Moon, R. T. (2014). Macrophages modulate adult zebrafish tail fin regeneration. Development 141, 2581-2591
40. Porrello, E. R., Johnson, B. A., Aurora, A. B., Simpson, E., Nam, Y.-J., Matkovich, S. J., Dorn, G.W., II, van Rooij, E. and Olson, E. N. (2011a). MiR-15 family regulates postnatal mitotic arrest of cardiomyocytes. Circ. Res. 109, 670-679
41. Porrello, E. R., Mahmoud, A. I., Simpson, E., Hill, J. A., Richardson, J. A., Olson, E. N. and Sadek, H. A. (2011b). Transient regenerative potential of the neonatal mouse heart. Science 331, 1078-1080
42. Porrello, E. R., Mahmoud, A. I., Simpson, E., Johnson, B. A., Grinsfelder, D., Canseco, D., Mammen, P. P., Rothermel, B. A., Olson, E. N. and Sadek, H. A. (2013). Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc. Natl. Acad. Sci. USA 110, 187-192
43. Poss, K. D., Wilson, L. G. and Keating, M. T. (2002). Heart regeneration in zebrafish. Science 298, 2188-2190
44. Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., Rougvie, A. E., Horvitz, H. R. and Ruvkun, G. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906
45. Schnabel, K., Wu, C.-C., Kurth, T. and Weidinger, G. (2011). Regeneration of cryoinjury induced necrotic heart lesions in zebrafish is associated with epicardial activation and cardiomyocyte proliferation. PLoS ONE 6, e18503.
46. van Rooij, E., Sutherland, L. B., Liu, N., Williams, A. H., McAnally, J., Gerard, R. D., Richardson, J. A. and Olson, E. N. (2006). A signature pattern of stressresponsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc. Natl. Acad. Sci. USA 103, 18255-18260.
47. van Rooij, E., Sutherland, L. B., Qi, X., Richardson, J. A., Hill, J. and Olson, E. N. (2007). Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316, 575-579
48. Varambally, S., Cao, Q., Mani, R.-S., Shankar, S., Wang, X., Ateeq, B., Laxman, B., Cao, X., Jing, X., Ramnarayanan, K. et al. (2008). Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 322, 1695-1699
49. Vester, B. and Wengel, J. (2004). LNA (locked nucleic acid): high-affinity targeting of complementary RNA and DNA. Biochemistry 43, 13233-13241
50. Wang, H.-J., Ruan, H.-J., He, X.-J., Ma, Y.-Y., Jiang, X.-T., Xia, Y.-J., Ye, Z.-Y. and Tao, H.-Q. (2010). MicroRNA-101 is down-regulated in gastric cancer and involved in cell migration and invasion. Eur. J. Cancer 46, 2295-2303
51. 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. et al. (2011). The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 138, 3421-3430
52. Wang, J., Cao, J., Dickson, A. L. and Poss, K. D. (2015). Epicardial regeneration is guided by cardiac outflow tract and Hedgehog signalling. Nature 522, 226-230
53. Yin, V. P., Thomson, J. M., Thummel, R., Hyde, D. R., Hammond, S. M., Poss, K. D. (2008). Fgf-dependent depletion of microRNA-133 promotes appendage regeneration in zebrafish. Genes Dev. 22, 728-733
54. Yin, V. P., Lepilina, A., Smith, A. and Poss, K. D. (2012). Regulation of zebrafish heart regeneration by miR-133 Dev. Biol. 365, 319-327
55. Zhao, Y., Samal, E. and Srivastava, D. (2005). Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436, 214-220
56. Zhao, L., Borikova, A. L., Ben-Yair, R., Guner-Ataman, B., MacRae, C. A., Lee, R. T., Burns, C. G. and Burns, C. E. (2014). Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc. Natl. Acad. Sci. USA 111, 1403-1408.