STAT3 protein regulates vascular smooth muscle cell phenotypic switch by interaction with myocardin

Journal of Biological Chemistry

Volumn 290, Issue 32, 2015, Pages 19641-19652

  Liao, Xing Hua ^a,b   Wang, Nan ^b   Zhao, Dong Wei ^b   Zheng, De Liang ^b   Zheng, Li ^b   Xing, Wen Jing ^b   Ma, Wen Jian ^b   Bao, Le Yuan ^a   Dong, Jian ^a   Zhang, Tong Cun ^a,b  

^a WUHAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b TIANJIN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BODY FLUIDS; CELL DEATH; CELL PROLIFERATION; CELLS; GENE EXPRESSION; GENES; MUSCLE; TRANSCRIPTION;

ACTIVATION PROCESS; GENE REGULATION PATHWAYS; MOLECULAR MECHANISM; OVER-EXPRESSION; SERUM RESPONSE FACTORS; SIGNALING PATHWAYS; TRANSCRIPTION ACTIVITY; VASCULAR SMOOTH MUSCLE CELLS;

CELL SIGNALING;

MYOCARDIN; SERUM RESPONSE FACTOR; STAT3 PROTEIN; JANUS KINASE; MAPK1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NUCLEAR PROTEIN; SRF PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ARTICLE; CARG BOX; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION; VASCULAR SMOOTH MUSCLE CELL; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; DRUG EFFECTS; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MUSCLE CONTRACTION; PHENOTYPE; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; HUMANS; JANUS KINASES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NUCLEAR PROTEINS; PHENOTYPE; SERUM RESPONSE FACTOR; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84939123705     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.630111     Document Type: Article

References (58)

1. Owens, G. K., Kumar, M. S., and Wamhoff, B. R. (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801
2. Majesky, M. W. (2007) Developmental basis of vascular smooth muscle diversity. Arterioscler. Thromb. Vasc. Biol. 27, 1248-1258
3. Xie, C., Ritchie, R. P., Huang, H., Zhang, J., and Chen, Y. E. (2011) Smooth muscle cell differentiation in vitro: models and underlying molecular mechanisms. Arterioscler. Thromb. Vasc. Biol. 31, 1485-1494
4. Wang, Z., Wang, D. Z., Hockemeyer, D., McAnally, J., Nordheim, A., and Olson, E. N. (2004) Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature 428, 185-189
5. Miano, J. M. (2003) Serum response factor: toggling between disparate programs of gene expression. J. Mol. Cell. Cardiol. 35, 577-593
6. Sun, Q., Chen, G., Streb, J. W., Long, X., Yang, Y., Stoeckert, C. J., Jr., and Miano, J. M. (2006) Defining the mammalian CArGome. Genome Res. 16, 197-207
7. Wang, D., Chang, P. S., Wang, Z., Sutherland, L., Richardson, J. A., Small, E., Krieg, P. A., and Olson, E. N. (2001) Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105, 851-862
8. Chen, J., Kitchen, C. M., Streb, J. W., and Miano, J. M. (2002) Myocardin: a component of a molecular switch for smooth muscle differentiation. J. Mol. Cell. Cardiol. 34, 1345-1356
9. Du, K. L., Ip, H. S., Li, J., Chen, M., Dandre, F., Yu, W., Lu, M. M., Owens, G. K., and Parmacek, M. S. (2003) Myocardin is a critical serum response factor cofactor in the transcriptional program regulating smooth muscle cell differentiation. Mol. Cell. Biol. 23, 2425-2437
10. Wang, Z., Wang, D. Z., Pipes, G. C., and Olson, E. N. (2003) Myocardin is a master regulator of smooth muscle gene expression. Proc. Natl. Acad. Sci. U.S.A. 100, 7129-7134
11. Yoshida, T., Sinha, S., Dandré, F., Wamhoff, B. R., Hoofnagle, M. H., Kremer, B. E., Wang, D. Z., Olson, E. N., and Owens, G. K. (2003) Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ. Res. 92, 856-864
12. Yoshida, T., Kawai-Kowase, K., and Owens, G. K. (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
13. Long, X., Bell, R. D., Gerthoffer, W. T., Zlokovic, B. V., and Miano, J. M. (2008) Myocardin is sufficient for a smooth muscle-like contractile phenotype. Arterioscler. Thromb. Vasc. Biol. 28, 1505-1510
14. Kimura, Y., Morita, T., Hayashi, K., Miki, T., and Sobue, K. (2010) Myocardin functions as an effective inducer of growth arrest and differentiation in human uterine leiomyosarcoma cells. Cancer Res. 70, 501-511
15. Tang, R. H., Zheng, X. L., Callis, T. E., Stansfield, W. E., He, J., Baldwin, A. S., Wang, D. Z., and Selzman, C. H. (2008) Myocardin inhibits cellular proliferation by inhibiting NF-κB(p65)-dependent cell cycle progression. Proc. Natl. Acad. Sci. U.S.A. 105, 3362-3367
16. Chiu, C. Z., Wang, B. W., Chung, T. H., and Shyu, K. G. (2010) Angiotensin II and the ERK pathway mediate the induction of myocardin by hypoxia in cultured rat neonatal cardiomyocytes. Clin. Sci. 119, 273-282
17. Xie, C., Guo, Y., Zhu, T., Zhang, J., Ma, P. X., and Chen, Y. E. (2012) Yap1 protein regulates vascular smooth muscle cell phenotypic switch by interaction with myocardin. J. Biol. Chem. 287, 14598-14605
18. Badorff, C., Seeger, F. H., Zeiher, A. M., and Dimmeler, S. (2005) Glycogen synthase kinase 3β inhibits myocardin-dependent transcription and hypertrophy induction through site-specific phosphorylation. Circ. Res. 97, 645-654
19. Taurin, S., Sandbo, N., Yau, D. M., Sethakorn, N., Kach, J., and Dulin, N. O. (2009) Phosphorylation of myocardin by extracellular signal-regulated kinase. J. Biol. Chem. 284, 33789-33794
20. Xie, P., Fan, Y., Zhang, H., Zhang, Y., She, M., Gu, D., Patterson, C., and Li, H. (2009) ChIP represses myocardin-induced smooth muscle cell differentiation via ubiquitin-mediated proteasomal degradation. Mol. Cell. Biol. 29, 2398-2408
21. Grote, K., Luchtefeld, M., and Schieffer, B. (2005) JANUS under stress-role of JAK/STAT signaling pathway in vascular diseases. Vascul. Pharmacol. 43, 357-363
22. Neeli, I., Liu, Z., Dronadula, N., Ma, Z. A., and Rao, G. N. (2004) An essential role of the Jak-2/STAT-3/cytosolic phospholipase A(2) axis in platelet-derived growth factor BB-induced vascular smooth muscle cell motility. J. Biol. Chem. 279, 46122-46128
23. Wang, D., Liu, Z., Li, Q., Karpurapu, M., Kundumani-Sridharan, V., Cao, H., Dronadula, N., Rizvi, F., Bajpai, A. K., Zhang, C., Müller-Newen, G., Harris, K. W., and Rao, G. N. (2007) An essential role for gp130 in neointima formation following arterial injury. Circ. Res. 100, 807-816
24. Wang, H., Byfield, G., Jiang, Y., Smith, G. W., McCloskey, M., and Hartnett, M. E. (2012) VEGF-mediated STAT3 activation inhibits retinal vascularization by down-regulating local erythropoietin expression. Am. J. Pathol. 180, 1243-1253
25. Devarajan, E., and Huang, S. (2009) STAT3 as a central regulator of tumor metastases. Curr. Mol. Med. 9, 626-633
26. Daniel, J. M., Dutzmann, J., Bielenberg, W., Widmer-Teske, R., Gündüz, D., Hamm, C. W., and Sedding, D. G. (2012) Inhibition of STAT3 signaling prevents vascular smooth muscle cell proliferation and neointima formation. Basic Res. Cardiol. 107, 261
27. Bartoli, M., Platt, D., Lemtalsi, T., Gu, X., Brooks, S. E., Marrero, M. B., and Caldwell, R. B. (2003) VEGF differentially activates STAT3 in microvascular endothelial cells. FASEB J. 17, 1562-1564
28. Yahata, Y., Shirakata, Y., Tokumaru, S., Yamasaki, K., Sayama, K., Hanakawa, Y., Detmar, M., and Hashimoto, K. (2003) Nuclear translocation of phosphorylated STAT3 is essential for vascular endothelial growth factor-induced human dermal microvascular endothelial cell migration and tube formation. J. Biol. Chem. 278, 40026-40031
29. Chen, S. H., Murphy, D. A., Lassoued, W., Thurston, G., Feldman, M. D., and Lee, W. M. (2008) Activated STAT3 is a mediator and biomarker of VEGF endothelial activation. Cancer Biol. Ther. 7, 1994-2003
30. Chen, K. H., Guo, X., Ma, D., Guo, Y., Li, Q., Yang, D., Li, P., Qiu, X., Wen, S., Xiao, R. P., and Tang, J. (2004) Dysregulation of HSG triggers vascular proliferative disorders. Nat. Cell Biol. 6, 872-883
31. Liao, X. H., Wang, N., Liu, Q. X., Qin, T., Cao, B., Cao, D. S., and Zhang, T. C. (2011) Myocardin-related transcription factor-A induces cardiomyocyte hypertrophy. IUBMB Life 63, 54-61
32. Liao, X. H., Li, Y. Q., Wang, N., Zheng, L., Xing, W. J., Zhao, D. W., Yan, T. B., Wang, Y., Liu, L. Y., Sun, X. G., Hu, P., Zhou, H., and Zhang, T. C. (2014) Re-expression and epigenetic modification of maspin induced apoptosis in MCF-7 cells mediated by myocardin. Cell. Signal. 26, 1335-1346
33. Liao, X. H., Wang, N., Liu, L. Y., Zheng, L., Xing, W. J., Zhao, D. W., Sun, X. G., Hu, P., Dong, J., and Zhang, T. C. (2014) MRTF-A and STAT3 synergistically promote breast cancer cell migration. Cell. Signal. 26, 2370-2380
34. Shi, X., Guo, L. W., Seedial, S. M., Si, Y., Wang, B., Takayama, T., Suwanabol, P. A., Ghosh, S., DiRenzo, D., Liu, B., and Kent, K. C. (2014) TGF-β/Smad3 inhibit vascular smooth muscle cell apoptosis through an autocrine signaling mechanism involving VEGF-A. Cell Death Dis. 5, e1317
35. Demyanets, S., Kaun, C., Rychli, K., Pfaffenberger, S., Kastl, S. P., Hohensinner, P. J., Rega, G., Katsaros, K. M., Afonyushkin, T., Bochkov, V. N., Paireder, M., Huk, I., Maurer, G., Huber, K., and Wojta, J. (2011) Oncostatin M-enhanced vascular endothelial growth factor expression in human vascular smooth muscle cells involvesPI3K-, p38 MAPK-, Erk1/2- and STAT1/STAT3-dependent pathways and is attenuated by interferon-γ. Basic Res. Cardiol. 106, 217-231
36. Fukada, T., Ohtani, T., Yoshida, Y., Shirogane, T., Nishida, K., Nakajima, K., Hibi, M., and Hirano, T. (1998) STAT3 orchestrates contradictory signals in cytokine-induced G1 to S cell-cycle transition. EMBO J. 17, 6670-6677
37. Carmeliet, P., and Jain, R. K. (2000) Angiogenesis in cancer and other diseases. Nature 407, 249-257
38. Ferrara, N. (2009) Vascular endothelial growth factor. Arterioscler. Thromb. Vasc. Biol. 29, 789-791
39. Ferrara, N. (2009) VEGF-A: a critical regulator of blood vessel growth. Eur. Cytokine Netw. 20, 158-163
40. Lamalice, L., Houle, F., and Huot, J. (2006) Phosphorylation of Tyr1214 within VEGFR-2 triggers the recruitment of Nck and activation of Fyn leading to SAPK2/p38 activation and endothelial cell migration in response to VEGF. J. Biol. Chem. 281, 34009-34020
41. Zhang, M. X., Zhao, X., Wang, Z. G., Zhao, W. M., and Wang, Y. S. (2010) Constitutive activation of signal transducer and activator of transcription 3 regulates expression of vascular endothelial growth factor in human meningioma differentiation. J. Cancer Res. Clin. Oncol. 136, 981-988
42. Wang, M., Zhang, W., Crisostomo, P., Markel, T., Meldrum, K. K., Fu, X. Y., and Meldrum, D. R. (2007) STAT3 mediates bone marrow mesenchymal stem cell VEGF production. J. Mol. Cell. Cardiol. 42, 1009-1015
43. Dale-Nagle, E. A., Satriotomo, I., and Mitchell, G. S. (2011) Spinal vascular endothelial growth factor induces phrenic motor facilitation via extracellular signal-regulated kinase and Akt signaling. J. Neurosci. 31, 7682-7690
44. Narasimhan, P., Liu, J., Song, Y. S., Massengale, J. L., and Chan, P. H. (2009) VEGF stimulates the ERK1/2 signaling pathway and apoptosis in cerebral endothelial cells after ischemic conditions. Stroke 40, 1467-1473
45. Fournier, N. M., Lee, B., Banasr, M., Elsayed, M., and Duman, R. S. (2012) Vascular endothelial growth factor regulates adult hippocampal cell proliferation through MEK/ERK- and PI3K/Akt-dependent signaling. Neuropharmacology 63, 642-652
46. Niwa, Y., Kanda, H., Shikauchi, Y., Saiura, A., Matsubara, K., Kitagawa, T., Yamamoto, J., Kubo, T., and Yoshikawa, H. (2005) Methylation silencing of SOCS-3 promotes cell growth and migration by enhancing JAK/STAT and FAK signalings in human hepatocellular carcinoma. Oncogene 24, 6406-6417
47. Xu, Q., Briggs, J., Park, S., Niu, G., Kortylewski, M., Zhang, S., Gritsko, T., Turkson, J., Kay, H., Semenza, G. L., Cheng, J. Q., Jove, R., and Yu, H. (2005) Targeting Stat3 blocks both HIF-1 and VEGF expression induced by multiple oncogenic growth signaling pathways. Oncogene 24, 5552-5560
48. Haridas, V., Nishimura, G., Xu, Z. X., Connolly, F., Hanausek, M., Walaszek, Z., Zoltaszek, R., and Gutterman, J. U. (2009) Avicin D: a protein reactive plant isoprenoid dephosphorylates Stat 3 by regulating both kinase and phosphatase activities. PLoS One 4, e5578
49. Belgore, F., Blann, A., Neil, D., Ahmed, A. S., and Lip, G. Y. (2004) Localisation of members of the vascular endothelial growth factor (VEGF) family and their receptors in human atherosclerotic arteries. J. Clin. Pathol. 57, 266-272
50. Jin, J., Yuan, F., Shen, M. Q., Feng, Y. F., and He, Q. L. (2013) Vascular endothelial growth factor regulates primate choroid-retinal endothelial cell proliferation and tube formation through PI3K/Akt and MEK/ERK dependent signaling. Mol. Cell. Biochem. 381, 267-272
51. Tallquist, M. D., Soriano, P., and Klinghoffer, R. A. (1999) Growth factor signaling pathways in vascular development. Oncogene 18, 7917-7932
52. Watanabe, Y., and Dvorak, H. F. (1997) Vascular permeability factor/vascularendothelialgrowthfactorinhibitsanchorage-disruption-inducedapoptosis in microvessel endothelial cells by inducing scaffold formation. Exp. Cell Res. 233, 340-349
53. Alon, T., Hemo, I., Itin, A., Pe'er, J., Stone, J., and Keshet, E. (1995) Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat. Med. 1, 1024-1028
54. Chai, J., Jones, M. K., and Tarnawski, A. S. (2004) Serum response factor is a critical requirement for VEGF signaling in endothelial cells and VEGF-induced angiogenesis. FASEB J. 18, 1264-1266
55. Franco, C. A., Mericskay, M., Parlakian, A., Gary-Bobo, G., Gao-Li, J., Paulin, D., Gustafsson, E., and Li, Z. (2008) Serum response factor is required for sprouting angiogenesis and vascular integrity. Dev. Cell 15, 448-461
56. Weinl, C., Riehle, H., Park, D., Stritt, C., Beck, S., Huber, G., Wolburg, H., Olson, E. N., Seeliger, M. W., Adams, R. H., and Nordheim, A. (2013) Endothelial SRF/MRTF ablation causes vascular disease phenotypes in murine retinae. J. Clin. Invest. 123, 2193-2206
57. Mack, C. P., Thompson, M. M., Lawrenz-Smith, S., and Owens, G. K. (2000) Smooth muscle oα-actin CArG elements coordinate formation of a smooth muscle cell-selective, serum response factor-containing activation complex. Circ. Res. 86, 221-232
58. Richard, D. E., Berra, E., Gothié, E., Roux, D., and Pouysségur, J. (1999) p42/p44 mitogen activated protein kinases phosphorylate hypoxia-inducible factor 1α (HIF-1α) and enhance the transcriptional activity of HIF-1. J. Biol. Chem. 274, 32631-32637