Myocardin sumoylation transactivates cardiogenic genes in pluripotent 10T1/2 fibroblasts

Molecular and Cellular Biology

Volumn 27, Issue 2, 2007, Pages 622-632

  Wang, Jun ^a,b   Li, AnKang ^a,b   Wang, ZhiGao ^c   Feng, XinHua ^a   Olson, Eric N ^c   Schwartz, Robert J ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTIN; ARGININE; LYSINE; MYOCARDIN; MYOSIN HEAVY CHAIN ALPHA; PROTEIN INHIBITOR OF ACTIVATED STAT; SERUM RESPONSE FACTOR; SUMO 1 PROTEIN; TRANSCRIPTION FACTOR GATA 4; UBIQUITIN PROTEIN LIGASE E3;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROBLAST; GENE EXPRESSION; HEART DEVELOPMENT; HEART MUSCLE CELL; HUMAN; HUMAN CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SUMOYLATION; TRANSACTIVATION;

ACTINS; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CERCOPITHECUS AETHIOPS; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; MUTATION; MYOCYTES, CARDIAC; NUCLEAR PROTEINS; PLURIPOTENT STEM CELLS; PROTEIN INHIBITORS OF ACTIVATED STAT; SUMO-1 PROTEIN; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; UBIQUITIN-PROTEIN LIGASES; VENTRICULAR MYOSINS;

EID: 33846182262     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01160-06     Document Type: Article

References (59)

1. Aravind, L., and E. V. Koonin. 2000. SAP-a putative DNA-binding motif involved in chromosomal organization. Trends Biochem. Sci. 25:112-114.
2. Arora, T., B. Liu, H. He, J. Kim, T. L. Murphy, K. M. Murphy, R. L. Modlin, and K. Shuai. 2003. PIASx is a transcriptional co-repressor of signal transducer and activator of transcription 4. J. Biol. Chem. 278:21327-21330.
3. Belaguli, N. S., J. L. Sepulveda, V. Nigam, F. Charron, M. Nemer, and R. J. Schwartz. 2000. Cardiac tissue enriched factors serum response factor and GATA-4 are mutual coregulators. Mol. Cell. Biol. 20:7550-7558.
4. Cao, D., Z. Wang, C. L. Zhang, J. Oh, W. Xing, S. Li, J. A. Richardson, D. Z. Wang, and E. N. Olson. 2005. Modulation of smooth muscle gene expression by association of histone acetyltransferases and deacetylases with myocardin. Mol. Cell. Biol. 25:364-376.
5. Chang, D. F., N. S. Belaguli, D. Iyer, W. B. Roberts, S. P. Wu, X. R. Dong, J. G. Marx, M. S. Moore, M. C. Beckerle, M. W. Majesky, and R. J. Schwartz. 2003. Cysteine-rich LIM-only proteins CRP1 and CRP2 are potent smooth muscle differentiation cofactors. Dev. Cell 4:107-118.
6. Chang, J., L. Wei, T. Otani, K. A. Youker, M. L. Entman, and R. J. Schwartz. 2003. Inhibitory cardiac transcription factor, SRF-N, is generated by caspase 3 cleavage in human heart failure and attenuated by ventricular unloading. Circulation 108:407-413.
7. Chen, A., H. Mannen, and S. S. Li. 1998. Characterization of mouse ubiquitin-like SMT3A and SMT3B cDNAs and gene/pseudogenes. Biochem. Mol. Biol. Int. 46:1161-1174.
8. Chen, J., C. M. Kitchen, J. W. Streb, and J. M. Miano. 2002. Myocardin: a component of a molecular switch for smooth muscle differentiation. J. Mol. Cell. Cardiol. 34:1345-1356.
9. Chi, N. C., and J. S. Karliner. 2004. Molecular determinants of responses to myocardial ischemia/reperfusion injury: focus on hypoxia-inducible and heat shock factors. Cardiovasc. Res. 61:437-447.
10. Chung, C. D., J. Liao, B. Liu, X. Rao, P. Jay, P. Berta, and K. Shuai. 1997. Specific inhibition of Stat3 signal transduction by PIAS3. Science 278:1803-1805.
11. Collavin, L., M. Gostissa, F. Avolio, P. Secco, A. Ronchi, C. Santoro, and G. Del Sal. 2004. Modification of the erythroid transcription factor GATA-1 by SUMO-1. Proc. Natl. Acad. Sci. USA 101:8870-8875.
12. Du, K. L., H. S. Ip, J. Li, M. Chen, F. Dandre, W. Yu, M. M. Lu, G. K. Owens, and M. S. Parmacek. 2003. Myocardin is a critical serum response factor cofactor in the transcriptional program regulating smooth muscle cell differentiation. Mol. Cell. Biol. 23:2425-2437.
13. Gill, G. 2004. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18:2046-2059.
14. Girdwood, D., D. Bumpass, O. A. Vaughan, A. Thain, L. A. Anderson, A. W. Snowden, E. Garcia-Wilson, N. D. Perkins, and R. T. Hay. 2003. P300 transcriptional repression is mediated by SUMO modification. Mol. Cell 11:1043-1054.
15. Gross, M., R. Yang, I. Top, C. Gasper, and K. Shuai. 2004. PIASy-mediated repression of the androgen receptor is independent of sumoylation. Oncogene 23:3059-3066.
16. Guo, D., M. Li, Y. Zhang, P. Yang, S. Eckenrode, D. Hopkins, W. Zheng, S. Purohit, R. H. Podolsky, A. Muir, J. Wang, Z. Dong, T. Brusko, M. Atkinson, P. Pozzilli, A. Zeidler, L. J. Raffel, C. O. Jacob, Y. Park, M. Serrano-Rios, M. T. Larrad, Z. Zhang, H. J. Garchon, J. F. Bach, J. I. Rotter, J. X. She, and C. Y. Wang. 2004. A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat. Genet. 36:837-841.
17. Hay, R. T. 2005. SUMO: a history of modification. Mol. Cell 18:1-12.
18. Hayashi, T., M. Seki, D. Maeda, W. Wang, Y. Kawabe, T. Seki, H. Saitoh, T. Fukagawa, H. Yagi, and T. Enomoto. 2002. Ubc9 is essential for viability of higher eukaryotic cells. Exp. Cell Res. 280:212-221.
19. Jackson, P. K. 2001. A new RING for SUMO: wrestling transcriptional responses into nuclear bodies with PIAS family E3 SUMO ligases. Genes Dev. 15:3053-3058.
20. Kagey, M. H., T. A. Melhuish, and D. Wotton. 2003. The polycomb protein Pc2 is a SUMO E3. Cell 113:127-137.
21. Kahyo, T., T. Nishida, and H. Yasuda. 2001. Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol. Cell 8:713-718.
22. Kawai-Kowase, K., M. S. Kumar, M. H. Hoofnagle, T. Yoshida, and G. K. Owens. 2005. PIAS1 activates the expression of smooth muscle cell differentiation marker genes by interacting with serum response factor and class I basic helix-loop-helix proteins. Mol. Cell. Biol. 25:8009-8023.
23. Kirsh, O., J. S. Seeler, A. Pichler, A. Gast, S. Muller, E. Miska, M. Mathieu, A. Harel-Bellan, T. Kouzarides, F. Melchior, and A. Dejean. 2002. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 21:2682-2691.
24. Kotaja, N., U. Karvonen, O. A. Janne, and J. J. Palvimo. 2002. FIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol. Cell. Biol. 22:5222-5234.
25. Lapenta, V., P. Chiurazzi, P. van der Spek, A. Pizzuti, F. Hanaoka, and C. Brahe. 1997. SMT3A, a human homologue of the S. cerevisiae SMT3 gene, maps to chromosome 21qter and defines a novel gene family. Genomics 40:362-366.
26. Lee, H., J. C. Quinn, K. V. Prasanth, V. A. Swiss, K. D. Economides, M. M. Camacho, D. L. Spector, and C. Abate-Shen. 2006. PIAS1 confers DNA-binding specificity on the Msx1 homeoprotein. Genes Dev. 20:784-794.
27. Lee, Y. S., M. S. Jang, J. S. Lee, E. J. Choi, and E. Kim. 2005. SUMO-1 represses apoptosis signal-regulating kinase 1 activation through physical interaction and not through covalent modification. EMBO Rep. 6:949-955.
28. Li, S., D. Z. Wang, Z. Wang, J. A. Richardson, and E. N. Olson. 2003. The serum response factor coactivator myocardin is required for vascular smooth muscle development. Proc. Natl. Acad. Sci. USA 100:9366-9370.
29. Liang, M., F. Melchior, X. H. Feng, and X. Lin. 2004. Regulation of Smad4 sumoylation and transforming growth factor-beta signaling by protein inhibitor of activated STAT1. J. Biol. Chem. 279:22857-22865.
30. Liang, Q., L. J. De Windt, S. A. Witt, T. R. Kimball, B. E. Markham, and J. D. Molkentin. 2001. The transcription factors GATA4 and GATA6 regulate cardiomyocyte hypertrophy in vitro and in vivo. J. Biol. Chem. 276: 30245-30253.
31. Lin, X., M. Liang, Y. Y. Liang, F. C. Brunicardi, F. Melchior, and X. H. Feng. 2003. Activation of transforming growth factor-beta signaling by SUMO-1 modification of tumor suppressor Smad4/DPC4. J. Biol. Chem. 278:18714-18719.
32. Lin, X., B. Sun, M. Liang, Y. Y. Liang, A. Gast, J. Hildebrand, F. C. Brunicardi, F. Melchior, and X. H. Feng. 2003. Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding. Mol. Cell 11:1389-1396.
33. Lin, B., M. Gross, J. ten Hoeve, and K. Shuai. 2001. A transcriptional corepressor of Stat1 with an essential LXXLL signature motif. Proc. Natl. Acad. Sci. USA 98:3203-3207.
34. Liu, B., J. Liao, X. Rao, S. A. Kushner, C. D. Chung, D. D. Chang, and K. Shuai. 1998. Inhibition of Stat1-mediated gene activalion by PIAS1. Proc. Natl. Acad. Sci. USA 95:10626-10631.
35. Long, J., I. Matsuura, D. He, G. Wang, K. Shuai, and F. Liu. 2003. Repression of Smad transcriptional activity by PIASy, an inhibitor of activated STAT. Proc. Natl. Acad. Sci. USA 100:9791-9796.
36. Matsuzaki, K., T. Minami, M. Tojo, Y. Honda, Y. Uchimura, H. Saitoh, H. Yasuda, S. Nagahiro, H. Saya, and M. Nakao. 2003. Serum response factor is modulated by the SUMO-1 conjugation system. Biochem. Biophys. Res. Commun. 306:32-38.
37. Melchior, F. 2000. SUMO-nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 16:591-626.
38. Muller, S., C. Hoege, G. Pyrowolakis, and S. Jentsch. 2001. SUMO, ubiquitin's mysterious cousin. Nat. Rev. Mol. Cell Biol. 2:202-210.
39. Nacerddine, K., F. Lehembre, M. Bhaumik, J. Artus, M. Cohen-Tannoudji, C. Babinet, P. P. Pandolfi, and A. Dejean. 2005. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev. Cell 9:769-779.
40. Nakagawa, K., and N. Kuzumaki. 2005. Transcriptional activity of megakaryoblastic leukemia 1 (MKL1) is repressed by SUMO modification. Genes Cells 10:835-850.
41. Narita, N., M. Bielinska, and D. B. Wilson. 1997. Wild-type endoderm abrogates the ventral developmental defects associated with GATA-4 deficiency in the mouse. Dev. Biol. 189:270-274.
42. Niu, Z., W. Yu, S. X. Zhang, M. Barron, N. S. Belaguli, M. D. Schneider, M. Parmacek, A. Nordheim, and R. J. Schwartz. 2005. Conditional mutagenesis of the murine serum response factor gene blocks cardiogenesis and the transcription of downstream gene targets. J. Biol. Chem. 280:32531-32538.
43. Oh, J., Z. Wang, D. Z. Wang, C. L. Lien, W. Xing, and E. N. Olson. 2004. Target gene-specific modulation of myocardin activity by GATA transcription factors. Mol. Cell. Biol. 24:8519-8528.
44. Pichler, A., A. Gast, J. S. Seeler, A. Dejean, and F. Melchior. 2002. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108:109-120.
45. Prigge, J. R., and E. E. Schmidt. 2006. Interaction of protein inhibitor of activated STAT (PIAS) proteins with the TATA-binding protein, TBP. J. Biol. Chem. 281:12260-12269.
46. Riquelme, C., K. K. Barthel, X. F. Qin, and X. Liu. 2006. Ubc9 expression is essential for myotube formation in C2C12. Exp. Cell Res. 312:2132-2141.
47. Rodriguez, M. S., C. Dargemont, and R. T. Hay. 2001. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276:12654-12659.
48. Roy Chowdhuri, S., T. Crum, A. Woollard, S. Aslam, and P. G. Okkema. 2006. The T-box factor TBX-2 and the SUMO conjugating enzyme UBC-9 are required for ABa-derived pharyngeal muscle in C. elegans. Dev. Biol. 295:664-677.
49. Saitoh, H., and J. Hinchey. 2000. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275:6252-6258.
50. Sepulveda, J. L., S. Vlahopoulos, D. Iyer, N. Belaguli, and R. J. Schwartz. 2002. Combinatorial expression of GATA4, Nkx2-5, and serum response factor directs early cardiac gene activity. J. Biol. Chem. 277:25775-25782.
51. Shao, R., F. P. Zhang, F. Tian, P. Anders Friberg, X. Wang, H. Sjoland, and H. Billig. 2004. Increase of SUMO-1 expression in response to hypoxia: direct interaction with HIF1alpha in adult mouse brain and heart in vivo. FEBS Lett. 569:293-300.
52. Tashiro, K., M. P. Pando, Y. Kanegae, P. M. Wamsley, S. Inoue, and I. M. Verma. 1997. Direct involvement of the ubiquitin-conjugating enzyme Ubc9/Hus5 in the degradation of IkappaBalpha. Proc. Natl. Acad. Sci. USA 94: 7862-7867.
53. Ueyama, T., H. Kasahara, T. Ishiwata, Q. Nie, and S. Izumo. 2003. Myocardin expression is regulated by Nkx2.5, and its function is required for cardiomyogenesis. Mol. Cell. Biol. 23:9222-9232.
54. van Tuyn, J., S. Knaan-Shanzer, M. J. van de Watering, M. de Graaf, A. van der Laarse, M. J. Schalij, E. E. van der Wall, A. A. de Vries, and D. E. Atsma. 2005. Activation of cardiac and smooth muscle-specific genes in primary human cells after forced expression of human myocardin. Cardiovasc. Res. 67:245-255.
55. Wang, D., P. S. Chang, Z. Wang, L. Sutherland, J. A. Richardson, E. Small, P. A. Krieg, and E. N. Olson. 2001. Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105: 851-862.
56. Wang, D. Z., S. Li, D. Hockemeyer, L. Sutherland, Z. Wang, G. Schratt, J. A. Richardson, A. Nordheim, and E. N. Olson. 2002. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc. Natl. Acad. Sci. USA 99:14855-14860.
57. Wang, J., X. H. Feng, and R. J. Schwartz. 2004. SUMO-1 modification activated GATA4-dependent cardiogenic gene activity. J. Biol. Chem. 279: 49091-49098.
58. Wang, Z., D. Z. Wang, G. C. Pipes, and E. N. Olson. 2003. Myocardin is a master regulator of smooth muscle gene expression. Proc. Natl. Acad. Sci. USA 100:7129-7134.
59. Yoshida, T., K. Kawai-Kowase, and G. K. Owens. 2004. Forced expression of myocardin is not sufficient for induction of smooth muscle differentiation in multipotential embryonic cells. Arterioscler. Thromb. Vasc. Biol. 24:1596-1601.