G9a promotes proliferation and inhibits cell cycle exit during myogenic differentiation

Nucleic Acids Research

Volumn 44, Issue 17, 2016, Pages 8129-8143

  Rao, Vinay Kumar ^a   Ow, Jin Rong ^a   Shankar, Shilpa Rani ^a   Bharathy, Narendra ^a   Manikandan, Jayapal ^b   Wang, Yaju ^a   Taneja, Reshma ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NANOSTRING TECHNOLOGIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; G9A PROTEIN; HISTONE ACETYLTRANSFERASE PCAF; METHYLTRANSFERASE; MYOD PROTEIN; RB1 PROTEIN; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTOME; UNCLASSIFIED DRUG; G9A PROTEIN, MOUSE; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; LYSINE; P300-CBP-ASSOCIATED FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; GENE ACTIVATION; GENE TARGETING; HISTONE ACETYLATION; HISTONE METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATOR GENE; RNA ANALYSIS; SKELETAL MUSCLE CELL; TRANSCRIPTION REGULATION; ANIMAL; C57BL MOUSE; CELL CYCLE; CELL LINE; CYTOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; METHYLATION; MUSCLE DEVELOPMENT; MYOBLAST;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; E2F1 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LYSINE; METHYLATION; MICE, INBRED C57BL; MUSCLE DEVELOPMENT; MYOBLASTS; MYOD PROTEIN; P300-CBP TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC;

EID: 84991294853     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw483     Document Type: Article

References (57)

1. Tapscott, S.J. (2005) The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development, 132, 2685-2695.
2. Wang, J., Helin, K., Jin, P. and Nadal-Ginard, B. (1995) Inhibition of in vitro myogenic differentiation by cellular transcription factor E2F1. Cell Growth Differ., 6, 1299-1306.
3. Puri, P.L., Iezzi, S., Stiegler, P., Chen, T.T., Schiltz, R.L., Muscat, G.E., Giordano, A., Kedes, L., Wang, J.Y. and Sartorelli, V. (2001) Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis. Mol. Cell, 8, 885-897.
4. Mal, A., Sturniolo, M., Schiltz, R.L., Ghosh, M.K. and Harter, M.L. (2001) A role for histone deacetylase HDAC1 in modulating the transcriptional activity of MyoD: inhibition of the myogenic program. EMBO J., 20, 1739-1753.
5. Ling, B.M.T., Bharathy, N., Chung, T.-K., Kok, W.K., Li, S., Tan, Y.H., Rao, V.K., Gopinadhan, S., Sartorelli, V., Walsh, M.J. et al. (2012) Lysine methyltransferase G9a methylates the transcription factor MyoD and regulates skeletal muscle differentiation. Proc. Natl. Acad. Sci. U.S.A., 109, 841-846.
6. Jung, E.-S., Sim, Y.-J., Jeong, H.-S., Kim, S.-J., Yun, Y.-J., Song, J.-H., Jeon, S.-H., Choe, C., Park, K.-T., Kim, C.-H. et al. (2015) Jmjd2C increases MyoD transcriptional activity through inhibiting G9a-dependent MyoD degradation. Biochim. Biophys. Acta, 1849, 1081-1094.
7. Mal, A.K. (2006) Histone methyltransferase Suv39h1 represses MyoD-stimulated myogenic differentiation. EMBO J., 25, 3323-3334.
8. De Falco, G., Comes, F. and Simone, C. (2006) pRb: master of differentiation. Coupling irreversible cell cycle withdrawal with induction of muscle-specific transcription. Oncogene, 25, 5244-5249.
9. Martínez-Balbás, M.A., Bauer, U.-M., Nielsen, S.J., Brehm, A. and Kouzarides, T. (2000) Regulation of E2F1 activity by acetylation. EMBO J., 19, 662-671.
10. Puri, P.L., Sartorelli, V., Yang, X.-J., Hamamori, Y., Ogryzko, V.V., Howard, B.H., Kedes, L., Wang, J.Y.J., Graessmann, A., Nakatani, Y. et al. (1997) Differential roles of p300 and PCAF acetyltransferases in muscle differentiation. Mol. Cell, 1, 35-45.
11. Robertson, K.D., Ait-Si-Ali, S., Yokochi, T., Wade, P.A., Jones, P.L. and Wolffe, A.P. (2000) DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet., 25, 338-342.
12. Frolov, M.V. and Dyson, N.J. (2004) Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J. Cell Sci., 117, 2173-2181.
13. Ait-Si-Ali, S., Guasconi, V., Fritsch, L., Yahi, H., Sekhri, R., Naguibneva, I., Robin, P., Cabon, F., Polesskaya, A. and Harel-Bellan, A. (2004) A Suv39h-dependent mechanism for silencing S-phase genes in differentiating but not in cycling cells. EMBO J., 23, 605-615.
14. Ling, B.M.T., Gopinadhan, S., Kok, W.K., Shankar, S.R., Gopal, P., Bharathy, N., Wang, Y. and Taneja, R. (2012) G9a mediates Sharp-1-dependent inhibition of skeletal muscle differentiation. Mol. Biol. Cell, 23, 4778-4785.
15. Caretti, G., Di Padova, M., Micales, B., Lyons, G.E. and Sartorelli, V. (2004) The polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev., 18, 2627-2638.
16. Guasconi, V., Pritchard, L.-L., Fritsch, L., Mesner, L.D., Francastel, C., Harel-Bellan, A. and Ait-Si-Ali, S. (2010) Preferential association of irreversibly silenced E2F-target genes with pericentromeric heterochromatin in differentiated muscle cells. Epigenetics, 5, 704-709.
17. Blais, A., van Oevelen, C.J.C., Margueron, R., Acosta-Alvear, D. and Dynlacht, B.D. (2007) Retinoblastoma tumor suppressor protein-dependent methylation of histone H3 lysine 27 is associated with irreversible cell cycle exit. J. Cell Biol., 179, 1399-1412.
18. Halevy, O., Novitch, B.G., Spicer, D.B., Skapek, S.X., Rhee, J., Hannon, G.J., Beach, D. and Lassar, A.B. (1995) Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science, 267, 1018-1021.
19. Parker, S.B., Eichele, G., Zhang, P., Rawls, A., Sands, A.T., Bradley, A., Olson, E.N., Harper, J.W. and Elledge, S.J. (1995) p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science, 267, 1024-1027.
20. Martelli, F., Cenciarelli, C., Santarelli, G., Polikar, B., Felsani, A. and Caruso, M. (1994) MyoD induces retinoblastoma gene expression during myogenic differentiation. Oncogene, 9, 3579-3590.
21. Mal, A., Chattopadhyay, D., Ghosh, M.K., Poon, R.Y., Hunter, T. and Harter, M.L. (2000) p21 and retinoblastoma protein control the absence of DNA replication in terminally differentiated muscle cells. J. Cell Biol., 149, 281-292.
22. Guo, K., Wang, J., Andrés, V., Smith, R.C. and Walsh, K. (1995) MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol. Cell. Biol., 15, 3823-3829.
23. Gu, W., Schneider, J.W., Condorelli, G., Kaushal, S., Mahdavi, V. and Nadal-Ginard, B. (1993) Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell, 72, 309-324.
24. Novitch, B.G., Mulligan, G.J., Jacks, T. and Lassar, A.B. (1996) Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle. J. Cell Biol., 135, 441-456.
25. Zacksenhaus, E., Jiang, Z., Chung, D., Marth, J.D., Phillips, R.A. and Gallie, B.L. (1996) pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev., 10, 3051-3064.
26. Wang, J. and Abate-Shen, C. (2012) The MSX1 homeoprotein recruits G9a methyltransferase to repressed target genes in myoblast cells. PLoS One, 7, e37647.
27. Choi, J., Jang, H., Kim, H., Lee, J.-H., Kim, S.-T., Cho, E.-J. and Youn, H.-D. (2014) Modulation of lysine methylation in myocyte enhancer factor 2 during skeletal muscle cell differentiation. Nucleic Acids Res., 42, 224-234.
28. Sun, H., Li, L., Vercherat, C., Gulbagci, N.T., Acharjee, S., Li, J., Chung, T.-K., Thin, T.H. and Taneja, R. (2007) Stra13 regulates satellite cell activation by antagonizing Notch signaling. J. Cell Biol., 177, 647-657.
29. Yang, X.J., Ogryzko, V.V., Nishikawa, J., Howard, B.H. and Nakatani, Y. (1996) A p300/CBP-associated factor that competes with the adenoviral oncoprotein E1A. Nature, 382, 319-324.
30. Wang, S., Fusaro, G., Padmanabhan, J. and Chellappan, S.P. (2002) Prohibitin co-localizes with Rb in the nucleus and recruits N-CoR and HDAC1 for transcriptional repression. Oncogene, 21, 8388-8396.
31. Müller, H., Lukas, J., Schneider, A., Warthoe, P., Bartek, J., Eilers, M. and Strauss, M. (1994) Cyclin D1 expression is regulated by the retinoblastoma protein. Proc. Natl. Acad. Sci. U.S.A., 91, 2945-2949.
32. Wang, Y., Rao, V.K., Kok, W.K., Roy, D.N., Sethi, S., Ling, B.M.T., Lee, M.B.H. and Taneja, R. (2012) SUMO modification of Stra13 is required for repression of cyclin D1 expression and cellular growth arrest. PLoS One, 7, e43137.
33. Cheedipudi, S., Puri, D., Saleh, A., Gala, H.P., Rumman, M., Pillai, M.S., Sreenivas, P., Arora, R., Sellathurai, J., Schroeder, H.D. et al. (2015) A fine balance: epigenetic control of cellular quiescence by the tumor suppressor PRDM2/RIZ at a bivalent domain in the cyclin a gene. Nucleic Acids Res.,43, 6236-6256.
34. Vandromme, M., Chailleux, C., Escaffit, F. and Trouche, D. (2008) Binding of the retinoblastoma protein is not the determinant for stable repression of some E2F-regulated promoters in muscle cells. Mol. Cancer Res., 6, 418-425.
35. Azmi, S., Ozog, A. and Taneja, R. (2004) Sharp-1/DEC2 inhibits skeletal muscle differentiation through repression of myogenic transcription factors. J. Biol. Chem., 279, 52643-52652.
36. Dignam, J.D., Lebovitz, R.M. and Roeder, R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1489.
37. Ferreira, R., Naguibneva, I., Mathieu, M., Ait-Si-Ali, S., Robin, P., Pritchard, L.L. and Harel-Bellan, A. (2001) Cell cycle-dependent recruitment of HDAC-1 correlates with deacetylation of histone H4 on an Rb-E2F target promoter. EMBO Rep., 2, 794-799.
38. Berkes, C.A., Bergstrom, D.A., Penn, B.H., Seaver, K.J., Knoepfler, P.S. and Tapscott, S.J. (2004) Pbx marks genes for activation by MyoD indicating a role for a homeodomain protein in establishing myogenic potential. Mol. Cell, 14, 465-477.
39. Vedadi, M., Barsyte-Lovejoy, D., Liu, F., Rival-Gervier, S., Allali-Hassani, A., Labrie, V., Wigle, T.J., Dimaggio, P.A., Wasney, G.A., Siarheyeva, A. et al. (2011) A chemical probe selectively inhibits G9a and GLP methyltransferase activity in cells. Nat. Chem. Biol., 7, 566-574.
40. Bittencourt, D., Wu, D.-Y., Jeong, K.W., Gerke, D.S., Herviou, L., Ianculescu, I., Chodankar, R., Siegmund, K.D. and Stallcup, M.R. (2012) G9a functions as a molecular scaffold for assembly of transcriptional coactivators on a subset of glucocorticoid receptor target genes. Proc. Natl. Acad. Sci. U.S.A., 109, 19673-19678.
41. Chaturvedi, C.-P., Hosey, A.M., Palii, C., Perez-Iratxeta, C., Nakatani, Y., Ranish, J.A., Dilworth, F.J. and Brand, M. (2009) Dual role for the methyltransferase G9a in the maintenance of beta-globin gene transcription in adult erythroid cells. Proc. Natl. Acad. Sci. U.S.A., 106, 18303-18308.
42. Shankar, S.R., Bahirvani, A.G., Rao, V.K., Bharathy, N., Ow, J.R. and Taneja, R. (2013) G9a, a multipotent regulator of gene expression. Epigenetics 8, 16-22.
43. Ait-Si-Ali, S., Polesskaya, A., Filleur, S., Ferreira, R., Duquet, A., Robin, P., Vervish, A., Trouche, D., Cabon, F. and Harel-Bellan, A. (2000) CBP/p300 histone acetyl-transferase activity is important for the G1/S transition. Oncogene, 19, 2430-2437.
44. Skapek, S.X., Rhee, J., Spicer, D.B. and Lassar, A.B. (1995) Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science, 267, 1022-1024.
45. Tachibana, M., Sugimoto, K., Fukushima, T. and Shinkai, Y. (2001) Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J. Biol. Chem., 276, 25309-25317.
46. Casciello, F., Windloch, K., Gannon, F. and Lee, J.S. (2015) Functional role of G9a histone methyltransferase in cancer. Front. Immunol., 6, 487.
47. Lehnertz, B., Pabst, C., Su, L., Miller, M., Liu, F., Yi, L., Zhang, R., Krosl, J., Yung, E., Kirschner, J. et al. (2014) The methyltransferase G9a regulates HoxA9-dependent transcription in AML. Genes Dev., 28, 317-327.
48. Dong, C., Wu, Y., Yao, J., Wang, Y., Yu, Y., Rychahou, P.G., Evers, B.M. and Zhou, B.P. (2012) G9a interacts with Snail and is critical for Snail-mediated E-cadherin repression in human breast cancer. J. Clin. Invest., 122, 1469-1486.
49. Ueda, J., Ho, J.C., Lee, K.L., Kitajima, S., Yang, H., Sun, W., Fukuhara, N., Zaiden, N., Chan, S.L., Tachibana, M. et al. (2014) The hypoxia-inducible epigenetic regulators Jmjd1a and G9a provide a mechanistic link between angiogenesis and tumor growth. Mol. Cell. Biol., 34, 3702-3720.
50. Ding, J., Li, T., Wang, X., Zhao, E., Choi, J.-H., Yang, L., Zha, Y., Dong, Z., Huang, S., Asara, J.M. et al. (2013) The histone H3 methyltransferase G9A epigenetically activates the serine-glycine synthesis pathway to sustain cancer cell survival and proliferation. Cell Metab., 18, 896-907.
51. Nishio, H. and Walsh, M.J. (2004) CCAAT displacement protein/cut homolog recruits G9a histone lysine methyltransferase to repress transcription. Proc. Natl. Acad. Sci. U.S.A., 101, 11257-11262.
52. Kim, J.K., Estève, P.-O., Jacobsen, S.E. and Pradhan, S. (2009) UHRF1 binds G9a and participates in p21 transcriptional regulation in mammalian cells. Nucleic Acids Res., 37, 493-505.
53. Kim, K.-B., Son, H.-J., Choi, S., Hahm, J.Y., Jung, H., Baek, H.J., Kook, H., Hahn, Y., Kook, H. and Seo, S.-B. (2015) H3K9 methyltransferase G9a negatively regulates UHRF1 transcription during leukemia cell differentiation. Nucleic Acids Res., 43, 3509-3523.
54. Kitzmann, M., Carnac, G., Vandromme, M., Primig, M., Lamb, N.J. and Fernandez, A. (1998) The muscle regulatory factors MyoD and myf-5 undergo distinct cell cycle-specific expression in muscle cells. J. Cell Biol., 142, 1447-1459.
55. Hua, K.-T., Wang, M.-Y., Chen, M.-W., Wei, L.-H., Chen, C.-K., Ko, C.-H., Jeng, Y.-M., Sung, P.-L., Jan, Y.-H., Hsiao, M. et al. (2014) The H3K9 methyltransferase G9a is a marker of aggressive ovarian cancer that promotes peritoneal metastasis. Mol. Cancer, 13, 189.
56. Chen, M.-W., Hua, K.-T., Kao, H.-J., Chi, C.-C., Wei, L.-H., Johansson, G., Shiah, S.-G., Chen, P.-S., Jeng, Y.-M., Cheng, T.-Y. et al. (2010) H3K9 histone methyltransferase G9a promotes lung cancer invasion and metastasis by silencing the cell adhesion molecule Ep-CAM. Cancer Res., 70, 7830-7840.
57. Yuan, Y., Wang, Q., Paulk, J., Kubicek, S., Kemp, M.M., Adams, D.J., Shamji, A.F., Wagner, B.K. and Schreiber, S.L. (2012) A small-molecule probe of the histone methyltransferase G9a induces cellular senescence in pancreatic adenocarcinoma. ACS Chem. Biol., 7, 1152-1157.