A novel function of FoxO transcription factors in thrombin-stimulated vascular smooth muscle cell proliferation

Thrombosis and Haemostasis

Volumn 108, Issue 1, 2012, Pages 148-158

  Mahajan, Shailaja G ^a   Fender, Anke C ^a   Meyer Kirchrath, Jutta ^a   Kurt, Muhammed ^b   Barth, Mareike ^a   Sagban, Tolga Atilla ^b   Fischer, Jens W ^a   Schrör, Karsten ^a   Hohlfeld, Thomas ^a   Rauch, Bernhard H ^c  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^c UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

FoxO transcription factors; Proliferation; Smooth muscle cells; Thrombin; Vein grafts

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL) CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL) IMIDAZOLE; MESSENGER RNA; PROTEIN KINASE B; PROTEIN P21; PROTEIN P27; PROTEINASE ACTIVATED RECEPTOR 1; SMALL INTERFERING RNA; THROMBIN; THROMBIN RECEPTOR ACTIVATING PEPTIDE; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE REGULATION; CELL PROLIFERATION; DNA SYNTHESIS; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MITOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SAPHENOUS VEIN GRAFT; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE;

CELL PROLIFERATION; CELLS, CULTURED; CHROMONES; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; ENDOTHELIUM, VASCULAR; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; IMIDAZOLES; MORPHOLINES; MYOCYTES, SMOOTH MUSCLE; OLIGOPEPTIDES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PYRIDINES; PYRROLES; QUINAZOLINES; RNA, SMALL INTERFERING; SAPHENOUS VEIN; THROMBIN;

EID: 84863658455     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH11-11-0756     Document Type: Article

References (50)

1. Conte MS. Molecular engineering of vein bypass grafts. J Vasc Surg 2007; 45 (Suppl A): A74-81.
2. Motwani JG, Topol EJ. Aortocoronary saphenous vein graft disease: pathogenesis, predisposition, and prevention. Circulation 1998; 97: 916-931.
3. Schrö K, Bretschneider E, Fischer K, et al. Thrombin receptors in vascular smooth muscle cells - function and regulation by vasodilatory prostaglandins. Thromb Haemost 2010; 103: 884-890.
4. Yang Z, Oemar BS, Carrel T, et al. Different proliferative properties of smooth muscle cells of human arterial and venous bypass vessels: role of PDGF receptors, mitogen-activated protein kinase, and cyclin-dependent kinase inhibitors. Circulation 1998; 97: 181-187.
5. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000; 407: 258-264.
6. Macfarlane SR, Seatter MJ, Kanke T, et al. Proteinase-activated receptors. Pharmacol Rev 2001; 53: 245-282.
7. McNamara CA, Sarembock IJ, Gimple LW, et al. Thrombin stimulates proliferation of cultured rat aortic smooth muscle cells by a proteolytically activated receptor. J Clin Invest 1993; 91: 94-98.
8. Bretschneider E, Spanbroek R, Lotzer K, et al. Evidence for functionally active protease- activated receptor-3 (PAR-3) in human vascular smooth muscle cells. Thromb Haemost 2003; 90: 704-709.
9. Bretschneider E, Kaufmann R, Braun M, et al. Evidence for functionally active protease-activated receptor-4 (PAR-4) in human vascular smooth muscle cells. Br J Pharmacol 2001; 132: 1441-1446.
10. Abid MR, Yano K, Guo S, et al. Forkhead transcription factors inhibit vascular smooth muscle cell proliferation and neointimal hyperplasia. J Biol Chem 2005; 280: 29864-29773.
11. Yang XF, Fang P, Meng S, et al. The forkhead transcription factors play important roles in vascular pathology and immunology. Adv Exp Med Biol 2009; 665: 90-105.
12. van der Vos KE, Coffer PJ. FOXO-binding partners: it takes two to tango. Oncogene 2008; 27: 2289-2299.
13. Maiese K, Chong ZZ, Shang YC, et al. FoxO proteins: cunning concepts and considerations for the cardiovascular system. Clin Sci (Lond) 2009; 116: 191-203.
14. Brunet A, Bonni A, Zigmond MJ, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999; 96: 857-868.
15. Huang H, Tindall DJ. Dynamic FoxO transcription factors. J Cell Sci 2007; 120: 2479-2487.
16. Asada S, Daitoku H, Matsuzaki H, et al. Mitogen-activated protein kinases, Erk and p38, phosphorylate and regulate Foxo1. Cell Signal 2007; 19: 519-527.
17. Flynn AN, Buret AG. Proteinase-activated receptor 1 (PAR-1) and cell apoptosis. Apoptosis 2004; 9: 729-737.
18. Zania P, Papaconstantinou M, Flordellis CS, et al. Thrombin mediates mitogenesis and survival of human endothelial cells through distinct mechanisms. Am J Physiol Cell Physiol 2008; 294: C1215-1226.
19. Isenovic ER, Soskic S, Trpkovic A, et al. Insulin, thrombine, ERK1/2 kinase and vascular smooth muscle cells proliferation. Curr Pharm Des 2010; 16: 3895-3902.
20. Walker TR, Moore SM, Lawson MF, et al. Platelet-derived growth factor-BB and thrombin activate phosphoinositide 3-kinase and protein kinase B: role in mediating airway smooth muscle proliferation. Mol Pharmacol 1998; 54: 1007-1015.
21. Fallier-Becker P, Rupp J, Fingerle J, et al. Smooth muscle cells from rabbit aorta. In: Cell Culture Techniques in Heart and Vessel Research. Berlin/Heidelberg/New York: Springer Verlag; 1990. pp. 247-270.
22. Rauch BH, Bretschneider E, Braun M, et al. Factor Xa releases matrix metalloproteinase- 2 (MMP-2) from human vascular smooth muscle cells and stimulates the conversion of pro-MMP-2 to MMP-2: role of MMP-2 in factor Xa-induced DNA synthesis and matrix invasion. Circ Res 2002; 90: 1122-1127.
23. Rauch BH, Weber A-A, Braun M, et al. PDGF-induced Akt phosphorylation does not activate NF-κB in human vascular smooth muscle cells and fibroblasts. FEBS Lett 2000; 481: 3-7.
24. Rauch BH, Rosenkranz AC, Ermler S, et al. Regulation of functionally active P2Y12 ADP receptors by thrombin in human smooth muscle cells and the presence of P2Y12 in carotid artery lesions. Arterioscler Thromb Vasc Biol 2010; 30: 2434-2442.
25. Winer J, Jung CK, Shackel I, et al. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 1999; 270: 41-49.
26. Rosenkranz AC, Schrö K, Rauch BH. Direct inhibitors of thrombin and factor Xa attenuate clot-induced mitogenesis and inflammatory gene expression in human vascular smooth muscle cells. Thromb Haemost 2011; 106: 561-562.
27. Roy SK, Srivastava RK, Shankar S. Inhibition of PI3K/AKT and MAPK/ERK pathways causes activation of FOXO transcription factor, leading to cell cycle arrest and apoptosis in pancreatic cancer. J Mol Signal 2010; 5: 10.
28. Yang Z, Ruschitzka F, Rabelink TJ, et al. Different effects of thrombin receptor activation on endothelium and smooth muscle cells of human coronary bypass vessels. Implications for venous bypass graft failure. Circulation 1997; 95: 1870-1876.
29. Abid MR, Guo S, Minami T, et al. Vascular endothelial growth factor activates PI3K/Akt/forkhead signaling in endothelial cells. Arterioscler Thromb Vasc Biol 2004; 24: 294-300.
30. Nakamura N, Ramaswamy S, Vazquez F, et al. Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol Cell Biol 2000; 20: 8969-8982.
31. Paik JH. FOXOs in the maintenance of vascular homoeostasis. Biochem Soc Trans 2006; 34: 731-734.
32. Castro C, Diez-Juan A, Cortes MJ, et al. Distinct regulation of mitogen-activated protein kinases and p27Kip1 in smooth muscle cells from different vascular beds. A potential role in establishing regional phenotypic variance. J Biol Chem 2003; 278: 4482-4490.
33. Dangwal S, Rauch BH, Gensch T, et al. High glucose enhances thrombin responses via protease-activated receptor-4 in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2011; 31: 624-633.
34. Rosenkranz AC, Rauch BH, Doller A, et al. Regulation of Human Vascular Protease- Activated Receptor-3 through mRNA Stabilization and the Transcription Factor Nuclear Factor of Activated T Cells (NFAT). Mol Pharmacol 2011; 80: 337-344.
35. Ahn HS, Chackalamannil S, Boykow G, et al. Development of proteinase-activated receptor 1 antagonists as therapeutic agents for thrombosis, restenosis and inflammatory diseases. Curr Pharm Des 2003; 9: 2349-2365.
36. Braun-Dullaeus RC, Mann MJ, Seay U, et al. Cell cycle protein expression in vascular smooth muscle cells in vitro and in vivo is regulated through phosphatidylinositol 3-kinase and mammalian target of rapamycin. Arterioscler Thromb Vasc Biol 2001; 21: 1152-1158.
37. Shigematsu K, Koyama H, Olson NE, et al. Phosphatidylinositol 3-kinase signaling is important for smooth muscle cell replication after arterial injury. Arterios Thromb Vasc Biol 2000; 20: 2373-2378.
38. Yang JY, Xia W, Hu MC. Ionizing radiation activates expression of FOXO3a, Fas ligand, and Bim, and induces cell apoptosis. Int J Oncol 2006; 29: 643-648.
39. Zuckerbraun BS, McCloskey CA, Mahidhara RS, et al. Overexpression of mutated IkappaBalpha inhibits vascular smooth muscle cell proliferation and intimal hyperplasia formation. J Vasc Surg 2003; 38: 812-819.
40. Sherr CJ, Roberts JM. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 1995; 9: 1149-1163.
41. Green D, Karpatkin S. Role of thrombin as a tumor growth factor. Cell Cycle 2010; 9: 656-661.
42. Hu L, Ibrahim S, Liu C, et al. Thrombin induces tumor cell cycle activation and spontaneous growth by down-regulation of p27Kip1, in association with the upregulation of Skp2 and MiR-222. Cancer Res 2009; 69: 3374-3381.
43. Naldini A, Carney DH, Pucci A, et al. Human alpha-thrombin stimulates proliferation of interferon-gamma differentiated, growth-arrested U937 cells, overcoming differentiation-related changes in expression of p21CIP1/WAF1 and cyclin D1. J Cell Physiol 2002; 191: 290-297.
44. Bogatkevich GS, Gustilo E, Oates JC, et al. Distinct PKC isoforms mediate cell survival and DNA synthesis in thrombin-induced myofibroblasts. Am J Physiol Lung Cell Mol Physiol 2005; 288: L190-201.
45. Balmanno K, Cook SJ. Sustained MAP kinase activation is required for the expression of cyclin D1, p21Cip1 and a subset of AP-1 proteins in CCL39 cells. Oncogene 1999; 18: 3085-3097.
46. Fernandes DJ, Ravenhall CE, Harris T, et al. Contribution of the p38MAPK signaling pathway to proliferation in human cultured airway smooth muscle cells is mitogen- specific. Br J Pharmacol 2004; 142: 1182-1190.
47. Hindnavis V, Cho SH, Goldberg S. Saphenous vein graft intervention: a review. J Invasive Cardiol 2012; 24: 64-71.
48. Poston RS, Gu J, Brown JM, et al. Endothelial injury and acquired aspirin resistance as promoters of regional thrombin formation and early vein graft failure after coronary artery bypass grafting. J Thoracic Cardiovasc Surg 2006; 131: 122-130.
49. Park K-W, Kim D-H, You H-J, et al. Activated forkhead transcription factor inhibits neointimal hyperplasia after angioplasty through induction of p27. Arterioscler Thromb Vasc Biol 2005; 25: 742-747.
50. Berk BC. Vascular smooth muscle growth: autocrine growth mechanisms. Physiol Rev 2001; 81: 999-1030.