The primary microRNA-208b interacts with Polycomb-group protein, Ezh2, to regulate gene expression in the heart

Nucleic Acids Research

Volumn 42, Issue 2, 2014, Pages 790-803

  Mathiyalagan, Prabhu ^a   Okabe, Jun ^a   Chang, Lisa ^a   Su, Yidan ^b   Du, Xiao Jun ^b,d   El Osta, Assam ^a,c,d  

^a Alfred Medical Research and Education Precinct   (Australia)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; MICRORNA; MICRORNA 208B; MYOSIN HEAVY CHAIN; TRANSCRIPTION FACTOR EZH2; TRICHOSTATIN A; UNCLASSIFIED DRUG;

ALPHA MHC GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; BETA MHC GENE; CELL FRACTIONATION; CELL ISOLATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; HEART; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSVERSE AORTIC CONSTRICTION;

ANIMALS; CARDIOMEGALY; CELLS, CULTURED; CHROMATIN; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; HYDROXAMIC ACIDS; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; MYOCARDIUM; MYOCYTES, CARDIAC; MYOSIN HEAVY CHAINS; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; RNA, ANTISENSE; RNA, UNTRANSLATED;

EID: 84893302190     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt896     Document Type: Article

References (45)

1. Kook, H., Lepore, J.J., Gitler, A.D., Lu, M.M., Wing-Man Yung, W., Mackay, J., Zhou, R., Ferrari, V., Gruber, P. and Epstein, J.A. (2003) Cardiac hypertrophy and histone deacetylasedependent transcriptional repression mediated by the atypical homeodomain protein Hop. J. Clin. Invest., 112, 863-871.
2. Frey, N. and Olson, E.N. (2003) Cardiac hypertrophy: the good, the bad, and the ugly. Annu. Rev. Physiol., 65, 45-79.
3. Gupta, M.P. (2007) Factors controlling cardiac myosin-isoform shift during hypertrophy and heart failure. J. Mol. Cell Cardiol., 43, 388-403.
4. Luther, H.P. (2005) Role of endogenous antisense RNA in cardiac gene regulation. J. Mol. Med. (Berl.), 83, 26-32.
5. Han, P., Hang, C.T., Yang, J. and Chang, C.P. (2011) Chromatin remodeling in cardiovascular development and physiology. Circ. Res., 108, 378-396.
6. Hang, C.T., Yang, J., Han, P., Cheng, H.L., Shang, C., Ashley, E., Zhou, B. and Chang, C.P. (2010) Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature, 466, 62-67.
7. Haddad, F., Qin, A.X., Bodell, P.W., Zhang, L.Y., Guo, H., Giger, J.M. and Baldwin, K.M. (2006) Regulation of antisense RNA expression during cardiac MHC gene switching in response to pressure overload. Am. J. Physiol. Heart Circ. Physiol., 290, H2351-H2361.
8. Giger, J., Qin, A.X., Bodell, P.W., Baldwin, K.M. and Haddad, F. (2007) Activity of the beta-myosin heavy chain antisense promoter responds to diabetes and hypothyroidism. Am. J. Physiol. Heart Circ. Physiol., 292, H3065-H3071.
9. Callis, T.E., Pandya, K., Seok, H.Y., Tang, R.H., Tatsuguchi, M., Huang, Z.P., Chen, J.F., Deng, Z., Gunn, B., Shumate, J. et al. (2009) MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J. Clin. Invest., 119, 2772-2786.
10. van Rooij, E., Quiat, D., Johnson, B.A., Sutherland, L.B., Qi, X., Richardson, J.A., Kelm, R.J. Jr and Olson, E.N. (2009) A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev. Cell, 17, 662-673.
11. He, A., Ma, Q., Cao, J., von Gise, A., Zhou, P., Xie, H., Zhang, B., Hsing, M., Christodoulou, D.C., Cahan, P. et al. (2012) Polycomb repressive complex 2 regulates normal development of the mouse heart. Circ. Res., 110, 406-415.
12. Delgado-Olguin, P., Huang, Y., Li, X., Christodoulou, D., Seidman, C.E., Seidman, J.G., Tarakhovsky, A. and Bruneau, B.G. (2012) Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis. Nat. Genet., 44, 343-347.
13. Kee, H.J., Sohn, I.S., Nam, K.I., Park, J.E., Qian, Y.R., Yin, Z., Ahn, Y., Jeong, M.H., Bang, Y.J., Kim, N. et al. (2006) Inhibition of histone deacetylation blocks cardiac hypertrophy induced by angiotensin II infusion and aortic banding. Circulation, 113, 51-59.
14. Glenn, D.J., Wang, F., Chen, S., Nishimoto, M. and Gardner, D.G. (2009) Endothelin-stimulated human B-type natriuretic peptide gene expression is mediated by Yin Yang 1 in association with histone deacetylase 2. Hypertension, 53, 549-555.
15. Trivedi, C.M., Luo, Y., Yin, Z., Zhang, M., Zhu, W., Wang, T., Floss, T., Goettlicher, M., Noppinger, P.R., Wurst, W. et al. (2007) Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity. Nat. Med., 13, 324-331.
16. Davis, F.J., Pillai, J.B., Gupta, M. and Gupta, M.P. (2005) Concurrent opposite effects of trichostatin A, an inhibitor of histone deacetylases, on expression of alpha-MHC and cardiac tubulins: implication for gain in cardiac muscle contractility. Am. J. Physiol. Heart Circ. Physiol., 288, H1477-H1490.
17. Chang, L., Kiriazis, H., Gao, X.M., Du, X.J. and El-Osta, A. (2011) Cardiac genes show contextual SWI/SNF interactions with distinguishable gene activities. Epigenetics, 6, 760-768.
18. Gao, X.M., Kiriazis, H., Moore, X.L., Feng, X.H., Sheppard, K., Dart, A. and Du, X.J. (2005) Regression of pressure overload-induced left ventricular hypertrophy in mice. Am. J. Physiol. Heart Circ. Physiol., 288, H2702-H2707.
19. Xiao, Q., Zeng, L., Zhang, Z., Margariti, A., Ali, Z.A., Channon, K.M., Xu, Q. and Hu, Y. (2006) Sca-1+progenitors derived from embryonic stem cells differentiate into endothelial cells capable of vascular repair after arterial injury. Arterioscler Thromb. Vasc. Biol., 26, 2244-2251.
20. Mathiyalagan, P., Chang, L., Du, X.J. and El-Osta, A. (2010) Cardiac ventricular chambers are epigenetically distinguishable. Cell Cycle, 9, 612-617.
21. Okabe, J., Orlowski, C., Balcerczyk, A., Tikellis, C., Thomas, M.C., Cooper, M.E. and El-Osta, A. (2012) Distinguishing hyperglycemic changes by Set7 in vascular endothelial cells. Circ. Res., 110, 1067-1076.
22. Corsten, M.F., Dennert, R., Jochems, S., Kuznetsova, T., Devaux, Y., Hofstra, L., Wagner, D.R., Staessen, J.A., Heymans, S. and Schroen, B. (2010) Circulating MicroRNA-208b and MicroRNA-499 reflect myocardial damage in cardiovascular disease. Circ. Cardiovasc. Genet., 3, 499-506.
23. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R.S. and Zhang, Y. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science, 298, 1039-1043.
24. Varambally, S., Dhanasekaran, S.M., Zhou, M., Barrette, T.R., Kumar-Sinha, C., Sanda, M.G., Ghosh, D., Pienta, K.J., Sewalt, R.G., Otte, A.P. et al. (2002) The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature, 419, 624-629.
25. Chng, K.R., Chang, C.W., Tan, S.K., Yang, C., Hong, S.Z., Sng, N.Y. and Cheung, E. (2012) A transcriptional repressor co-regulatory network governing androgen response in prostate cancers. EMBO J., 31, 2810-2823.
26. Rinn, J.L. and Chang, H.Y. (2012) Genome regulation by long noncoding RNAs. Annu. Rev. Biochem., 81, 145-166.
27. Margueron, R. and Reinberg, D. (2011) The Polycomb complex PRC2 and its mark in life. Nature, 469, 343-349.
28. Yang, F., Zhang, L., Huo, X.S., Yuan, J.H., Xu, D., Yuan, S.X., Zhu, N., Zhou, W.P., Yang, G.S., Wang, Y.Z. et al. (2011) Long noncoding RNA high expression in hepatocellular carcinoma facilitates tumor growth through enhancer of zeste homolog 2 in humans. Hepatology, 54, 1679-1689.
29. Bolli, P., Vardabasso, C., Bernstein, E. and Chaudhry, H.W. (2013) Chromatin immunoprecipitation of adult murine cardiomyocytes. In: Bonifacino, J.S. et al. (eds), Current Protocols in Cell Biology/Editorial Board. Wiley, Hoboken, New Jersey, Chapter 17, Unit17 14.
30. Winter, J., Jung, S., Keller, S., Gregory, R.I. and Diederichs, S. (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell. Biol., 11, 228-234.
31. Juan, A.H., Derfoul, A., Feng, X., Ryall, J.G., Dell'Orso, S., Pasut, A., Zare, H., Simone, J.M., Rudnicki, M.A. and Sartorelli, V. (2011) Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Genes Dev., 25, 789-794.
32. Sher, F., Boddeke, E., Olah, M. and Copray, S. (2012) Dynamic changes in Ezh2 gene occupancy underlie its involvement in neural stem cell self-renewal and differentiation towards oligodendrocytes. PLoS One, 7, e40399.
33. Grote, P., Wittler, L., Hendrix, D., Koch, F., Wahrisch, S., Beisaw, A., Macura, K., Blass, G., Kellis, M., Werber, M. et al. (2013) The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev. Cell, 24, 206-214.
34. Rinn, J.L., Kertesz, M., Wang, J.K., Squazzo, S.L., Xu, X., Brugmann, S.A., Goodnough, L.H., Helms, J.A., Farnham, P.J., Segal, E. et al. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell, 129, 1311-1323.
35. Tsai, M.C., Manor, O., Wan, Y., Mosammaparast, N., Wang, J.K., Lan, F., Shi, Y., Segal, E. and Chang, H.Y. (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science, 329, 689-693.
36. Mattick, J.S. (2010) RNA as the substrate for epigenomeenvironment interactions: RNA guidance of epigenetic processes and the expansion of RNA editing in animals underpins development, phenotypic plasticity, learning, and cognition. Bioessays, 32, 548-552.
37. Pandey, R.R., Mondal, T., Mohammad, F., Enroth, S., Redrup, L., Komorowski, J., Nagano, T., Mancini-Dinardo, D. and Kanduri, C. (2008) Kcnq1ot1 antisense noncoding RNA mediates lineagespecific transcriptional silencing through chromatin-level regulation. Mol. Cell, 32, 232-246.
38. Gupta, R.A., Shah, N., Wang, K.C., Kim, J., Horlings, H.M., Wong, D.J., Tsai, M.C., Hung, T., Argani, P., Rinn, J.L. et al. (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature, 464, 1071-1076.
39. Schorderet, P. and Duboule, D. (2011) Structural and functional differences in the long non-coding RNA hotair in mouse and human. PLoS Genet., 7, e1002071.
40. Mercer, T.R., Dinger, M.E. and Mattick, J.S. (2009) Long non-coding RNAs: insights into functions. Nat. Rev. Genet., 10, 155-159.
41. Schonrock, N., Harvey, R.P. and Mattick, J.S. (2012) Long noncoding RNAs in cardiac development and pathophysiology. Circ. Res., 111, 1349-1362.
42. Yu, W., Gius, D., Onyango, P., Muldoon-Jacobs, K., Karp, J., Feinberg, A.P. and Cui, H. (2008) Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature, 451, 202-206.
43. 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.
44. Hsieh, P.C., Segers, V.F., Davis, M.E., MacGillivray, C., Gannon, J., Molkentin, J.D., Robbins, J. and Lee, R.T. (2007) Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat. Med., 13, 970-974.
45. Urbanek, K., Quaini, F., Tasca, G., Torella, D., Castaldo, C., Nadal-Ginard, B., Leri, A., Kajstura, J., Quaini, E. and Anversa, P. (2003) Intense myocyte formation from cardiac stem cells in human cardiac hypertrophy. Proc. Natl Acad. Sci. USA, 100, 10440-10445.