Role of Pin1 in neointima formation: Down-regulation of Nrf2-dependent heme oxygenase-1 expression by Pin1

Free Radical Biology and Medicine

Volumn 48, Issue 12, 2010, Pages 1644-1653

  Kim, Sang Eun ^a   Lee, Moo Yeol ^b   Lim, Sung Chul ^a   Hien, Tran Thi ^a   Kim, Jung Woo ^a   Ahn, Sang Gun ^a   Yoon, Jung Hoon ^a   Kim, Sang Kyum ^c   Choi, Hong Seok ^a   Kang, Keon Wook ^a  

^a Chosun University   (South Korea)

^b Chonnam National University   (South Korea)

^c Chungnam National University   (South Korea)

Author keywords

Free radicals; HO 1; Neointima; Nrf2; Pin1; Vascular smooth muscle cells

Indexed keywords

CYCLIN D1; HEME OXYGENASE 1; PEPTIDYLPROLYL ISOMERASE PIN1; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; ATHEROSCLEROSIS; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE OVEREXPRESSION; GROWTH RATE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE FIBER; UBIQUITINATION;

ANIMALS; CELL PROLIFERATION; DOWN-REGULATION; FEMORAL ARTERY; GENE EXPRESSION; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MICE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NF-E2-RELATED FACTOR 2; PEPTIDYLPROLYL ISOMERASE; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; TUNICA INTIMA;

EID: 77952674474     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.03.013     Document Type: Article

References (45)

1. Serruys P.W., de Jaegere P., Kiemeneij F., Macaya C., Rutsch W., Heyndrickx G., Emanuelsson H., et al. A comparison of balloon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease: Benestent Study Group. N. Engl. J. Med. 1994, 331:489-495.
2. Fischman L., Leon M.B., Baim D.S., Schatz R.A., Savage M.P., Penn I., Detre K., 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.
3. 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.
4. Chandrasekar B., Tanguay J.F. Local delivery of 17-beta-estradiol decreases neointimal hyperplasia after coronary angioplasty in a porcine model. J. Am. Coll. Cardiol. 2000, 35:555-562.
5. Siess W. Athero- and thrombogenic actions of lysophosphatidic acid and sphingosine-1-phosphate. Biochim. Biophys. Acta 2002, 1582:204-215.
6. Lu K.P., Hanes S.D., Hunter T. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 1996, 380:544-547.
7. Bayer E., Goettsch S., Mueller J.W., Griewel B., Guiberman E., Mayr L.M., Bayer P. Structural analysis of the mitotic regulator hPin1 in solution: insights into domain architecture and substrate binding. J. Biol. Chem. 2003, 278:26183-26193.
8. Weiwad M., Kullertz G., Schutkowski M., Fischer G. Evidence that the substrate backbone conformation is critical to phosphorylation by p42 MAP kinase. FEBS Lett. 2000, 478:39-42.
9. Bao L., Sauter G., Sowadski J., Lu K.P., Wang D. Prevalent overexpression of prolyl isomerase Pin1 in human cancers. Am. J. Pathol. 2004, 164:1727-1737.
10. Balastik M., Lim J., Pastorino L., Lu K.P. Pin1 in Alzheimer's disease: multiple substrates, one regulatory mechanism?. Biochim. Biophys. Acta 2007, 1772:422-429.
11. Pang R., Lee T.K., Poon R.T., Fan S.T., Wong K.B., Kwong Y.L., Tse E. Pin1 interacts with a specific serine-proline motif of hepatitis B virus X-protein to enhance hepatocarcinogenesis. Gastroenterology 2007, 132:1088-1103.
12. Kuramochi J., Arai T., Ikeda S., Kumagai J., Uetake H., Sugihara K. High Pin1 expression is associated with tumor progression in colorectal cancer. J. Surg. Oncol. 2006, 94:155-160.
13. 2+ exchange in primary cultured arterial myocytes. Am. J. Physiol. 1995, 269:C1340-C1345.
14. Lee M.Y., San Martin A., Mehta P.K., Dikalova A.E., Garrido A.M., Datla S.R., Lyons E., Krause K.H., Banfi B., Lambeth J.D., Lassègue B., Griendling K.K. Mechanisms of vascular smooth muscle NADPH oxidase 1 (Nox1) contribution to injury-induced neointimal formation. Arterioscler. Thromb. Vasc. Biol. 2009, 29:480-487.
15. Kim S.K., Yang J.W., Kim M.R., Roh S.H., Kim H.G., Lee K.Y., Jeong H.G., Kang K.W. Increased expression of Nrf2/ARE-dependent anti-oxidant proteins in tamoxifen-resistant breast cancer cells. Free Radic. Biol. Med. 2008, 45:537-546.
16. Son D.J., Lee H.W., Shin H.W., Lee J.J., Yoo H.S., Kim T.J., Yun Y.P., Hong J.T. Enhanced release of sphingosine-1-phosphate from hypercholesterolemic platelets: role in development of hypercholesterolemic atherosclerosis. Prostaglandins Leukot. Essent. Fatty Acids 2008, 78:383-390.
17. Wulf G.M., Ryo A., Wulf G.G., Lee S.W., Niu T., Petkova V., Lu K.P. Pin1 is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1. EMBO J. 2001, 20:3459-3472.
18. Ryo A., Uemura H., Ishiguro H., Saitoh T., Yamaguchi A., Perrem K., Kubota Y., Lu K.P., Aoki I. Stable suppression of tumorigenicity by Pin1-targeted RNA interference in prostate cancer. Clin. Cancer Res. 2005, 11:7523-7531.
19. 2 for platelet-derived growth factor signal transduction. Science 1995, 270:296-299.
20. 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.
21. Lin S.J., Shyue S.K., Shih M.C., Chu T.H., Chen Y.H., Ku H.H., Chen J.W., Tam K.B., Chen Y.L. Superoxide dismutase and catalase inhibit oxidized low-density lipoprotein-induced human aortic smooth muscle cell proliferation: role of cell-cycle regulation, mitogen-activated protein kinases, and transcription factors. Atherosclerosis 2007, 190:124-134.
22. 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.
23. Hartsfield C.L., Alam J., Cook J.L., Choi A.M. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am. J. Physiol. 1997, 273:L980-L988.
24. Duckers H.J., Boehm M., True A.L., Yet S.F., San H., Park J.L., Clinton Webb R., Lee M.E., Nabel G.J., Nabel E.G. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat. Med. 2001, 7:693-698.
25. 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.
26. Rubiolo J.A., Mithieux G., Vega F.V. Resveratrol protects primary rat hepatocytes against oxidative stress damage: activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes. Eur. J. Pharmacol. 2008, 591:66-72.
27. Zhang D.D., Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol. Cell. Biol. 2003, 23:8137-8151.
28. Nakano A., Koinuma D., Miyazawa K., Uchida T., Saitoh M., Kawabata M., Hanai J., Akiyama H., Abe M., Miyazono K., Matsumoto T., Imamura T. Pin1 down-regulates transforming growth factor-beta (TGF-beta) signaling by inducing degradation of Smad proteins. J. Biol. Chem. 2009, 284:6109-6115.
29. Ryo A., Hirai A., Nishi M., Liou Y.C., Perrem K., Lin S.C., Hirano H., Lee S.W., Aoki I. A suppressive role of the prolyl isomerase Pin1 in cellular apoptosis mediated by the death-associated protein Daxx. J. Biol. Chem. 2007, 282:36671-36681.
30. Hennig L., Christner C., Kipping M., Schelbert B., Rücknagel K.P., Grabley S., Küllertz G., Fischer G. Selective inactivation of parvulin-like peptidyl-prolyl cis/trans isomerases by juglone. Biochemistry 1998, 37:5953-5960.
31. Chen Z., Lee F.Y., Bhalla K.N., Wu J. Potent inhibition of platelet-derived growth factor-induced responses in vascular smooth muscle cells by BMS-354825 (dasatinib). Mol. Pharmacol. 2006, 69:1527-1533.
32. Ryo A., Liou Y.C., Lu K.P., Wulf G. Prolyl isomerase Pin1: a catalyst for oncogenesis and a potential therapeutic target in cancer. J. Cell Sci. 2003, 116:773-783.
33. Takahashi K., Uchida C., Shin R.W., Shimazaki K., Uchida T. Prolyl isomerase, Pin1: new findings of post-translational modifications and physiological substrates in cancer, asthma and Alzheimer's disease. Cell. Mol. Life Sci. 2008, 65:359-375.
34. Liou Y.C., Ryo A., Huang H.K., Lu P.J., Bronson R., Fujimori F., Uchida T., Hunter T., Lu K.P. Loss of Pin1 function in the mouse resembles the cyclin D1-null phenotypes. Proc. Natl. Acad. Sci. USA 2002, 99:1335-1340.
35. Brenkman A.B., de Keizer P.L., van den Broek N.J., van der Groep P., van Diest P.J., van der Horst A., Smits A.M., Burgering B.M. The peptidyl-isomerase Pin1 regulates p27kip1 expression through inhibition of Forkhead box O tumor suppressors. Cancer Res. 2008, 68:7597-7605.
36. Yet S.F., Layne M.D., Liu X., Chen Y.H., Ith B., Sibinga N.E., Perrella M.A. Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 2003, 17:1759-1761.
37. Finkel T. Redox-dependent signal transduction. FEBS Lett. 2000, 476:52-54.
38. Nakao A., Murase N., Ho C., Toyokawa H., Billiar T.R., Kanno S. Biliverdin administration prevents the formation of intimal hyperplasia induced by vascular injury. Circulation 2005, 112:587-591.
39. Ollinger R., Bilban M., Erat A., Froio A., McDaid J., Tyagi S., Csizmadia E., Graça-Souza A.V., Liloia A., Soares M.P., Otterbein L.E., Usheva A., Yamashita K., Bach F.H. Bilirubin: a natural inhibitor of vascular smooth muscle cell proliferation. Circulation 2005, 112:1030-1039.
40. Ryo A., Liou Y.C., Wulf G., Nakamura M., Lee S.W., Lu K.P. PIN1 is an E2F target gene essential for Neu/Ras-induced transformation of mammary epithelial cells. Mol. Cell. Biol. 2002, 22:5281-5295.
41. Itoh K., Ishii T., Wakabayashi N., Yamamoto M. Regulatory mechanisms of cellular response to oxidative stress. Free Radic. Res. 1999, 31:319-324.
42. Levonen A.L., Inkala M., Heikura T., Jauhiainen S., Jyrkkänen H.K., Kansanen E., Määttä K., Romppanen E., Turunen P., Rutanen J., Ylä-Herttuala S. Nrf2 gene transfer induces antioxidant enzymes and suppresses smooth muscle cell growth in vitro and reduces oxidative stress in rabbit aorta in vivo. Arterioscler. Thromb. Vasc. Biol. 2007, 27:741-747.
43. Cullinan S.B., Gordan J.D., Jin J., Harper J.W., Diehl J.A. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol. Cell. Biol. 2004, 24:8477-8486.
44. Cho M.K., Kim W.D., Ki S.H., Hwang J.I., Choi S., Lee C.H., Kim S.G. Role of Galpha12 and Galpha13 as novel switches for the activity of Nrf2, a key antioxidative transcription factor. Mol. Cell. Biol. 2007, 27:6195-6208.
45. Brondani V., Schefer Q., Hamy F., Klimkait T. The peptidyl-prolyl isomerase Pin1 regulates phospho-Ser77 retinoic acid receptor ? stability. Biochem. Biophys. Res. Commun. 2005, 328:6-13.