Resveratrol induces p53 and suppresses myocardin-mediated vascular smooth muscle cell differentiation

Toxicology Letters

Volumn 199, Issue 2, 2010, Pages 115-122

  Zheng, Jian Pu ^a   Ju, Donghong ^a   Jiang, Hong ^a   Shen, Jianbin ^a   Yang, Maozhou ^b   Li, Li ^a,c  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HENRY FORD HOSPITAL   (United States)

^c WAYNE STATE UNIVERSITY   (United States)

Author keywords

Myocardin; P53; Resveratrol; Smooth muscle cells; SRF; Tagln

Indexed keywords

MYOCARDIN; PROTEIN P53; RESVERATROL; NUCLEAR PROTEIN; SERUM RESPONSE FACTOR; STILBENE DERIVATIVE; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; EMBRYO; GENE EXPRESSION REGULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INDUCTION; RAT; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION; VASCULAR SMOOTH MUSCLE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NUCLEAR PROTEINS; RATS; SERUM RESPONSE FACTOR; SIGNAL TRANSDUCTION; STILBENES; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77957970296     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2010.08.010     Document Type: Article

References (47)

1. Ailawadi G., Moehle C.W., Pei H., Walton S.P., Yang Z., Kron I.L., Lau C.L., Owens G.K. Smooth muscle phenotypic modulation is an early event in aortic aneurysms. J. Thorac. Cardiovasc. Surg. 2009, 138:1392-1399.
2. Athar M., Back J.H., Kopelovich L., Bickers D.R., Kim A.L. Multiple molecular targets of resveratrol: anti-carcinogenic mechanisms. Arch. Biochem. Biophys. 2009, 486:95-102.
3. Chao H.H., Juan S.H., Liu J.C., Yang H.Y., Yang E., Cheng T.H., Shyu K.G. Resveratrol inhibits angiotensin II-induced endothelin-1 gene expression and subsequent proliferation in rat aortic smooth muscle cells. Eur. J. Pharmacol. 2005, 515:1-9.
4. Creemers E.E., Sutherland L.B., McAnally J., Richardson J.A., Olson E.N. Myocardin is a direct transcriptional target of Mef2, Tead and Foxo proteins during cardiovascular development. Development 2006, 133:4245-4256.
5. Crowell J.A., Korytko P.J., Morrissey R.L., Booth T.D., Levine B.S. Resveratrol-associated renal toxicity. Toxicol. Sci. 2004, 82:614-619.
6. Das S., Das D.K. Resveratrol: a therapeutic promise for cardiovascular diseases. Recent Pat. Cardiovasc. Drug Discov. 2007, 2:133-138.
7. Deaton R.A., Gan Q., Owens G.K. Sp1-dependent activation of KLF4 is required for PDGF-BB-induced phenotypic modulation of smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 2009, 296:H1027-1037.
8. El-Mowafy A.M., Alkhalaf M., El-Kashef H.A. Resveratrol reverses hydrogen peroxide-induced proliferative effects in human coronary smooth muscle cells: a novel signaling mechanism. Arch. Med. Res. 2008, 39:155-161.
9. Feil S., Hofmann F., Feil R. SM22alpha modulates vascular smooth muscle cell phenotype during atherogenesis. Circ. Res. 2004, 94:863-865.
10. Frankel E.N., Kanner J., German J.B., Parks E., Kinsella J.E. Inhibition of oxidation of human low-density lipoprotein by phenolic substances in red wine. Lancet 1993, 341:454-457.
11. Garvey S.M., Sinden D.S., Schoppee Bortz P.D., Wamhoff B.R. Cyclosporine up-regulates Kruppel-like factor-4 (KLF4) in vascular smooth muscle cells and drives phenotypic modulation in vivo. J. Pharmacol. Exp. Ther. 2010, 333:34-42.
12. Gerthoffer W.T. Mechanisms of vascular smooth muscle cell migration. Circ. Res. 2007, 100:607-621.
13. Gracia-Sancho J., Villarreal G., Zhang Y., Garcia-Cardena G. Activation of SIRT1 by resveratrol induces KLF2 expression conferring an endothelial vasoprotective phenotype. Cardiovasc. Res. 2010, 85:514-519.
14. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., Zipkin R.E., Chung P., Kisielewski A., Zhang L.L., Scherer B., Sinclair D.A. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 425:191-196.
15. Iyemere V.P., Proudfoot D., Weissberg P.L., Shanahan C.M. Vascular smooth muscle cell phenotypic plasticity and the regulation of vascular calcification. J. Intern. Med. 2006, 260:192-210.
16. Lee B., Moon S.K. Resveratrol inhibits TNF-alpha-induced proliferation and matrix metalloproteinase expression in human vascular smooth muscle cells. J. Nutr. 2005, 135:2767-2773.
17. Lee J.E., Safe S. Involvement of a post-transcriptional mechanism in the inhibition of CYP1A1 expression by resveratrol in breast cancer cells. Biochem. Pharmacol. 2001, 62:1113-1124.
18. Lekli I., Szabo G., Juhasz B., Das S., Das M., Varga E., Szendrei L., Gesztelyi R., Varadi J., Bak I., Das D.K., Tosaki A. Protective mechanisms of resveratrol against ischemia-reperfusion-induced damage in hearts obtained from Zucker obese rats: the role of GLUT-4 and endothelin. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H859-866.
19. Lenk G.M., Tromp G., Weinsheimer S., Gatalica Z., Berguer R., Kuivaniemi H. Whole genome expression profiling reveals a significant role for immune function in human abdominal aortic aneurysms. BMC Genom. 2007, 8:237.
20. Li L., Liu Z., Mercer B., Overbeek P., Olson E.N. Evidence for serum response factor-mediated regulatory networks governing SM22alpha transcription in smooth, skeletal, and cardiac muscle cells. Dev. Biol. 1997, 187:311-321.
21. Li L., Miano J.M., Mercer B., Olson E.N. Expression of the SM22alpha promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J. Cell Biol. 1996, 132:849-859.
22. Liu N., Olson E.N. MicroRNA regulatory networks in cardiovascular development. Dev. Cell 2010, 18:510-525.
23. Liu Y., Liu G. Isorhapontigenin and resveratrol suppress oxLDL-induced proliferation and activation of ERK1/2 mitogen-activated protein kinases of bovine aortic smooth muscle cells. Biochem. Pharmacol. 2004, 67:777-785.
24. Liu Y., Sinha S., McDonald O.G., Shang Y., Hoofnagle M.H., Owens G.K. Kruppel-like factor 4 abrogates myocardin-induced activation of smooth muscle gene expression. J. Biol. Chem. 2005, 280:9719-9727.
25. Manna S.K., Mukhopadhyay A., Aggarwal B.B. Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-kappa B, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation. J. Immunol. 2000, 164:6509-6519.
26. Martinez J., Moreno J.J. Effect of resveratrol, a natural polyphenolic compound, on reactive oxygen species and prostaglandin production. Biochem. Pharmacol. 2000, 59:865-870.
27. Miano J.M., Long X., Fujiwara K. Serum response factor: master regulator of the actin cytoskeleton and contractile apparatus. Am. J. Physiol. Cell Physiol. 2007, 292:C70-81.
28. Miyazaki R., Ichiki T., Hashimoto T., Inanaga K., Imayama I., Sadoshima J., Sunagawa K. SIRT1, a longevity gene, downregulates angiotensin II type 1 receptor expression in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1263-1269.
29. Mizutani K., Ikeda K., Yamori Y. Resveratrol inhibits AGEs-induced proliferation and collagen synthesis activity in vascular smooth muscle cells from stroke-prone spontaneously hypertensive rats. Biochem. Biophys. Res. Commun. 2000, 274:61-67.
30. Mnjoyan Z.H., Fujise K. Profound negative regulatory effects by resveratrol on vascular smooth muscle cells: a role of p53-p21 (WAF1/CIP1) pathway. Biochem. Biophys. Res. Commun. 2003, 311:546-552.
31. Molchadsky A., Shats I., Goldfinger N., Pevsner-Fischer M., Olson M., Rinon A., Tzahor E., Lozano G., Zipori D., Sarig R., Rotter V. p53 plays a role in mesenchymal differentiation programs, in a cell fate dependent manner. PLoS One 2008, 3:e3707.
32. Olas B., Wachowicz B., Saluk-Juszczak J., Zielinski T. Effect of resveratrol, a natural polyphenolic compound, on platelet activation induced by endotoxin or thrombin. Thromb. Res. 2002, 107:141-145.
33. Orr A.W., Hastings N.E., Blackman B.R., Wamhoff B.R. Complex regulation and function of the inflammatory smooth muscle cell phenotype in atherosclerosis. J. Vasc. Res. 2010, 47:168-180.
34. Poussier B., Cordova A.C., Becquemin J.P., Sumpio B.E. Resveratrol inhibits vascular smooth muscle cell proliferation and induces apoptosis. J. Vasc. Surg. 2005, 42:1190-1197.
35. Regan C.P., Adam P.J., Madsen C.S., Owens G.K. Molecular mechanisms of decreased smooth muscle differentiation marker expression after vascular injury. J. Clin. Invest. 2000, 106:1139-1147.
36. Rothman A., Kulik T.J., Taubman M.B., Berk B.C., Smith C.W., Nadal-Ginard B. Development and characterization of a cloned rat pulmonary arterial smooth muscle cell line that maintains differentiated properties through multiple subcultures. Circulation 1992, 86:1977-1986.
37. Shanahan C.M., Cary N.R., Metcalfe J.C., Weissberg P.L. High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J. Clin. Invest. 1994, 93:2393-2402.
38. Shen J., Yang M., Ju D., Jiang H., Zheng J.P., Xu Z., Li L. Disruption of SM22 promotes inflammation upon artery injury via NF-kappaB activation. Circ. Res. 2010, Published online before print March 11, 2010, 10.1161/CIRCRESAHA.109.213900.
39. Wallerath T., Deckert G., Ternes T., Anderson H., Li H., Witte K., Forstermann U. Resveratrol, a polyphenolic phytoalexin present in red wine, enhances expression and activity of endothelial nitric oxide synthase. Circulation 2002, 106:1652-1658.
40. Wang D., Chang P.S., Wang Z., Sutherland L., Richardson J.A., Small E., Krieg P.A., Olson E.N. Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 2001, 105:851-862.
41. Wang D.Z., Olson E.N. Control of smooth muscle development by the myocardin family of transcriptional coactivators. Curr. Opin. Genet. Dev. 2004, 14:558-566.
42. Wang Z., Chen Y., Labinskyy N., Hsieh T.C., Ungvari Z., Wu J.M. Regulation of proliferation and gene expression in cultured human aortic smooth muscle cells by resveratrol and standardized grape extracts. Biochem. Biophys. Res. Commun. 2006, 346:367-376.
43. Yoshida T., Owens G.K. Molecular determinants of vascular smooth muscle cell diversity. Circ. Res. 2005, 96:280-291.
44. Yoshida T., Sinha S., Dandre F., Wamhoff B.R., Hoofnagle M.H., Kremer B.E., Wang D.Z., Olson E.N., Owens G.K. Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ. Res. 2003, 92:856-864.
45. Zhang H., Zhang J., Ungvari Z., Zhang C. Resveratrol improves endothelial function: role of TNF{alpha} and vascular oxidative stress. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1164-1171.
46. Zheng J.P., Ju D., Shen J., Yang M., Li L. Disruption of actin cytoskeleton mediates loss of tensile stress induced early phenotypic modulation of vascular smooth muscle cells in organ culture. Exp. Mol. Pathol. 2010, 88:52-57.
47. Zhou H., Shang L., Li X., Zhang X., Gao G., Guo C., Chen B., Liu Q., Gong Y., Shao C. Resveratrol augments the canonical Wnt signaling pathway in promoting osteoblastic differentiation of multipotent mesenchymal cells. Exp. Cell Res. 2009, 315:2953-2962.