Inhibition of neointimal formation by trans-resveratrol: Role of phosphatidyl inositol 3-kinase-dependent nrf2 activation in heme oxygenase-1 induction

Molecular Nutrition and Food Research

Volumn 54, Issue 10, 2010, Pages 1497-1505

  Kim, Jung Woo ^a   Lim, Sung Chul ^a   Lee, Moo Yeol ^b   Lee, Jeong Woon ^a   Oh, Won Keun ^a   Kim, Sang Kyum ^c   Kang, Keon Wook ^a  

^a Chosun University   (South Korea)

^b Chonnam National University   (South Korea)

^c Chungnam National University   (South Korea)

Author keywords

Heme oxygenase 1; Neointima; Nrf2; Phosphatidyl inositol 3 kinase Trans resveratrol

Indexed keywords

CYCLIN D; ENZYME INHIBITOR; HEME OXYGENASE 1; HMOX1 PROTEIN, MOUSE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NFE2L2 PROTEIN, MOUSE; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; RESVERATROL; RETINOBLASTOMA PROTEIN; STILBENE DERIVATIVE; TRANSCRIPTION FACTOR NRF2;

ANIMAL; ARTICLE; CELL CULTURE; CELL LINE; CELL NUCLEUS; CELL PROLIFERATION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FEMORAL ARTERY; HYPERPLASIA; INJURY; METABOLISM; MOUSE; NEOINTIMA; PATHOLOGY; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PROTEIN TRANSPORT; RAT; THORACIC AORTA; VASCULAR SMOOTH MUSCLE;

ANIMALS; AORTA, THORACIC; ARTERIAL OCCLUSIVE DISEASES; CELL LINE; CELL NUCLEUS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN D; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMORAL ARTERY; HEME OXYGENASE-1; HYPERPLASIA; MEMBRANE PROTEINS; MICE; MUSCLE, SMOOTH, VASCULAR; NEOINTIMA; NF-E2-RELATED FACTOR 2; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN TRANSPORT; RATS; REACTIVE OXYGEN SPECIES; RETINOBLASTOMA PROTEIN; STILBENES;

EID: 78751500727     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201000016     Document Type: Article

References (49)

1. Savouret, J. F., Quesne, M., Resveratrol and cancer: a review. Biomed. Pharmacother. 2002, 56, 84–87.
2. Orallo, F., Comparative studies of the antioxidant effects of cis-and trans-resveratrol. Curr. Med. Chem. 2006, 13, 87–98.
3. Kannel, W. B., Ellison, R. C., Alcohol and coronary heart disease: the evidence for a protective effect. Clin. Chim. Acta. 1996, 246, 59–76.
4. Baur, J. A., Sinclair, D. A., Therapeutic potential of resveratrol: the in vivo evidence, Nat. Rev. Drug Discov. 2006, 5, 493–506.
5. Dolinsky, V. W., Chan, A. Y., Robillard, F. I., Light, P. E. et al., Resveratrol prevents the prohypertrophic effects of oxidative stress on LKB1. Circulation 2009, 119, 1643–1652.
6. Mizutani, K., Ikeda, K., Kawai, Y., Yamori, Y., Resveratrol attenuates ovariectomy-induced hypertension and bone loss in stroke-prone spontaneously hypertensive rats. J. Nutr. Sci. Vitaminol. 2000, 46, 78–83.
7. Yoshida, Y., Shioi, T., Izumi, T., Resveratrol ameliorates experimental autoimmune myocarditis. Circ. J. 2007, 71, 397–404.
8. Do, G. M., Kwon, E. Y., Kim, H. J., Jeon, S. M. et al., Long-term effects of resveratrol supplementation on suppression of atherogenic lesion formation and cholesterol synthesis in apo E-deficient mice. Biochem. Biophys. Res. Commun. 2008, 374, 55–59.
9. Fischman, L., Leon, M. B., Baim, D. S., Schatz, R. A. et al., A randomized comparison of coronary-stent placement and balloon angioplasty in the treatment of coronary artery disease. Stent Restenosis Study Investigators. N. Engl. J. Med. 1994, 331, 496–501.
10. Zou, J., Huang, Y., Chen, Q., Wang, N. et al., Suppression of mitogenesis and regulation of cell cycle traverse by resveratrol in cultured smooth muscle cells. Int. J. Oncol. 1999, 15, 647–651.
11. Araim, O., Ballantyne, J., Waterhouse, A. L., Sumpio, B. E., Inhibition of vascular smooth muscle cell proliferation with red wine and red wine polyphenols. J. Vasc. Surg. 2002, 35, 1226–1232.
12. Harikumar, K. B., Aggarwal, B. B., Resveratrol: a multi-targeted agent for age-associated chronic diseases. Cell Cycle 2008, 7, 1020–1035.
13. Athar, M., Back, J. H., Kopelovich, L., Bickers, D. R., Kim, A. L., Multiple molecular targets of resveratrol: Anti-carcino-genic mechanisms. Arch. Biochem. Biophys. 2009, 486, 95–102.
14. Jaschke, B., Milz, S., Vogeser, M., Michaelis, C. et al., Local cyclin-dependent kinase inhibition by flavopiridol inhibits coronary artery smooth muscle cell proliferation and migration: Implications for the applicability on drug-eluting stents to prevent neointima formation following vascular injury. FASEB J. 2004, 18, 1285–1287.
15. Morita, T., Kourembanas, S., Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J. Clin. Invest. 1995, 96, 2676–2682.
16. Yet, S. F., Layne, M. D., Liu, X., Chen, Y. H. et al., Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 2003, 17, 1759–1761.
17. Liu, X., Wei, J., Peng, D. H., Layne, M. D., Yet, S. F., Absence of heme oxygenase-1 exacerbates myocardial ischemia/ reperfusion injury in diabetic mice. Diabetes 2005, 54, 778–784.
18. Lee, M. Y., San, Martin, A., Mehta, P. K., Dikalova, A. E. et al., Mechanisms of vascular smooth muscle NADPH oxidase 1 (Nox1) contribution to injury-induced neointimal formation. Arterioscler. Thromb. Vasc. Biol. 2009, 29, 480–487.
19. Kim, M. R., Choi, H. S., Yang, J. W., Park, B. C. et al., Enhancement of vascular endothelial growth factor-medi-ated angiogenesis in tamoxifen-resistant breast cancer cells: role of Pin1 overexpression. Mol. Cancer Ther. 2009, 8, 2163–2171.
20. Kang, K. W., Ryu, J. H., Kim, S. G., The essential role of phosphatidylinositol 3-kinase and of p38 mitogen-activated protein kinase activation in the antioxidant response element-mediated rGSTA2 induction by decreased glutathione in H4IIE hepatoma cells. Mol. Pharmacol. 2000, 58, 1017–1025.
21. Uchida, K., Sasahara, M., Morigami, N., Hazama, F., Kinoshita, M., Expression of platelet-derived growth factor B-chain in neointimal smooth muscle cells of balloon injured rabbit femoral arteries. Atherosclerosis 1996, 124, 9–23.
22. Finkel, T., Redox-dependent signal transduction. FEBS Lett. 2000, 476, 52–54.
23. Juan, S. H., Lee, T. S., Tseng, K. W., Liou, J. Y. et al., Adenovirus-mediated heme oxygenase-1 gene transfer inhibits the development of atherosclerosis in apolipopro-tein E-deficient mice. Circulation 2001, 104, 1519–1525.
24. Schillinger, M., Exner, M., Minar, E., Mlekusch, W. et al., Heme oxygenase-1 genotype and restenosis after balloon angioplasty: a novel vascular protective factor. J. Am. Coll. Cardiol. 2004, 43, 950–957.
25. Lee, I. T., Wang, S. W., Lee, C. W., Chang, C. C. et al., Lipoteichoic acid induces HO-1 expression via the TLR2/ MyD88/c-Src/NADPH oxidase pathway and Nrf2 in human tracheal smooth muscle cells. J. Immunol. 2008, 181, 5098–5110.
26. Juan, S. H., Cheng, T. H., Lin, H. C., Chu, Y. L., Lee, W. S., Mechanism of concentration-dependent induction of heme oxygenase-1 by resveratrol in human aortic smooth muscle cells. Biochem. Pharmacol. 2005, 69, 41–48.
27. Krönke, G., Kadl, A., Ikonomu, E., Bl uml, S. et al., Expression of heme oxygenase-1 in human vascular cells is regulated by peroxisome proliferator-activated receptors. Arterioscler. Thromb. Vasc. Biol. 2007, 27, 1276–1282.
28. Thuong, P. T., Pokharel, Y. R., Lee, M. Y., Kim, S. K. et al., Dual anti-oxidative effects of fraxetin isolated from Fraxinus rhinchophylla. Biol. Pharm. Bull. 2009, 32, 1527–1532.
29. Anwar, A. A., Li, F. Y., Leake, D. S., Ishii, T. et al., Induction of heme oxygenase 1 by moderately oxidized low-density lipoproteins in human vascular smooth muscle cells: role of mitogen-activated protein kinases and Nrf2. Free Radic. Biol. Med. 2005, 39, 227–236.
30. Liu, X. M., Peyton, K. J., Ensenat, D., Wang, H. et al., Nitric oxide stimulates heme oxygenase-1 gene transcription via the Nrf2/ARE complex to promote vascular smooth muscle cell survival. Cardiovasc. Res. 2007, 75, 381–389.
31. Kim, S. K., Yang, J. W., Kim, M. R., Roh, S. H. et al., Increased expression of Nrf2/ARE-dependent anti-oxidant proteins in tamoxifen-resistant breast cancer cells. Free Radic. Biol. Med. 2008, 45, 537–546.
32. Ferguson, H. E., Thatcher, T. H., Olsen, K. C., Garcia-Bates, T. M. et al., Peroxisome proliferator-activated receptor-gamma ligands induce heme oxygenase-1 in lung fibroblasts by a PPAR-gamma-independent, glutathione-dependent mechanism. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297, L912–L919.
33. Gupta, S., Campbell, D., Derijard, B., Davis, R. J., Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 1995, 267, 389–393.
34. Geraldes, P., Yagi, K., Ohshiro, Y., He, Z. et al., Selective regulation of heme oxygenase-1 expression and function by insulin through IRS1/phosphoinositide 3-kinase/Akt-2 pathway. J. Biol. Chem. 2008, 283, 34327–34336.
35. Kim, J. W., Li, M. H., Jang, J. H., Na, H. K. et al., 15-Deoxy-Delta(12,14)-prostaglandin J(2) rescues PC12 cells from H2O2-induced apoptosis through Nrf2-mediated upregula-tion of heme oxygenase-1: potential roles of Akt and ERK1/ 2. Biochem. Pharmacol. 2008, 76, 1577–1589.
36. Guan, J., Wu, X., Arons, E., Christou, H., The p38 mitogen-activated protein kinase pathway is involved in the regulation of heme oxygenase-1 by acidic extracellular pH in aortic smooth muscle cells. J. Cell. Biochem. 2008, 105, 1298–1306.
37. Bhat, K. P. L., Kosmeder, J. W., II, Pezzuto, J. M., Biological effects of resveratrol. Antioxid. Redox Signal. 2001, 3, 1041–1064.
38. Cherubini, A., Ruggiero, C., Morand, C., Lattanzio, F. et al., Dietary antioxidants as potential pharmacological agents for ischemic stroke. Curr. Med. Chem. 2008, 15, 1236–1248.
39. Benitez, D. A., Pozo-Guisado, E., Alvarez-Barrientos, A., Fernandez-Salguero, P. M., Castellón, E. A., Mechanisms involved in resveratrol-induced apoptosis and cell cycle arrest in prostate cancer-derived cell lines. J. Androl. 2007, 28, 282–293.
40. 2 for platelet-derived growth factor signal transduction. Science 1995, 270, 296–299.
41. Sekharam, M., Trotti, A., Cunnick, J. M., Wu, J., Suppression of fibroblast cell cycle progression in G1 phase by N-acetylcysteine. Toxicol. Appl. Pharmacol. 1998, 149, 210–216.
42. Chen, C. Y., Jang, J. H., Li, M. H., Surh, Y. J., Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells. Biochem. Biophys. Res. Commun. 2005, 331, 993–1000.
43. Kang, K. W., Cho, M. K., Lee, C. H., Kim, S. G., Activation of phosphatidylinositol 3-kinase and Akt by tert-butylhy-droquinone is responsible for antioxidant response element-mediated rGSTA2 induction in H4IIE cells. Mol. Pharmacol. 2001, 59.1147–1156.
44. Lee, J. Y., Han, C. Y., Yang, J. W., Smith, C. et al., Induction of glutathione transferase in insulin-like growth factor type I receptor-overexpressed hepatoma cells. Mol. Pharmacol. 2007, 72, 1082–1093.
45. Kang, K. A., Lee, K. H., Park, J. W., Lee, N. H. et al., Tri-phlorethol-A induces heme oxygenase-1 via activation of ERK and NF-E2 related factor 2 transcription factor. FEBS Lett. 2007, 581, 2000–2008.
46. Ahanchi, S. S., Tsihlis, N. D., Kibbe, M. R., The role of nitric oxide in the pathophysiology of intimal hyperplasia. J. Vasc. Surg. 2007, 45, A64–A73.
47. Klinge, C. M., Wickramasinghe, N. S., Ivanova, M. M., Dougherty, S. M., Resveratrol stimulates nitric oxide production by increasing estrogen receptor alpha-Src-caveolin-1 interaction and phosphorylation in human umbilical vein endothelial cells. FASEB J. 2008, 22, 2185–2197.
48. Bi, X. L., Yang, J. Y., Dong, Y. X., Wang, J. M. et al., Resveratrol inhibits nitric oxide and TNF-alpha production by lipopolysaccharide-activated microglia. Int. Immunopharmacol. 2005, 5, 185–193.
49. Hsieh, T. C., Juan, G., Darzynkiewicz, Z., Wu, J. M., Resveratrol increases nitric oxide synthase, induces accumulation of p53 and p21(WAF1/CIP1), and suppresses cultured bovine pulmonary artery endothelial cell proliferation by perturbing progression through S and G2. Cancer Res. 1999, 59, 2596–2601.