TGF-ß/Smad3 inhibit vascular smooth muscle cell apoptosis through an autocrine signaling mechanism involving VEGF-A

Cell Death and Disease

Volumn 5, Issue 7, 2014, Pages

  Shi, X ^a   Guo, L W ^a   Seedial, S M ^a   Si, Y ^a   Wang, B ^a   Takayama, T ^a   Suwanabol, P A ^a   Ghosh, S ^a   DiRenzo, D ^a   Liu, B ^a   Kent, K C ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; AXITINIB; CASPASE 3; CYCLOHEXIMIDE; FIBROBLAST GROWTH FACTOR 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; NEUTRALIZING ANTIBODY; PLATELET DERIVED GROWTH FACTOR BB; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA; RECOMBINANT VASCULOTROPIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN 164; VASCULOTROPIN A; VASCULOTROPIN A NEUTRALIZING ANTIBODY; VASCULOTROPIN ANTIBODY; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTERY INTIMA PROLIFERATION; ARTICLE; AUTOCRINE EFFECT; CAROTID ANGIOPLASTY; CAROTID ARTERY INJURY; CHROMATIN IMMUNOPRECIPITATION; COMMON CAROTID ARTERY; CONTROLLED STUDY; DISEASE EXACERBATION; DNA FRAGMENTATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; GENE TRANSFER; GENETIC TRANSCRIPTION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO GENE TRANSFER; LIMIT OF QUANTITATION; MALE; MICROARRAY ANALYSIS; NICK END LABELING; NONHUMAN; PERCUTANEOUS TRANSLUMINAL ANGIOPLASTY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHAM PROCEDURE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; ULTRAVIOLET RADIATION; UPREGULATION; VASCULAR SMOOTH MUSCLE; VIRUS EXPRESSION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CYTOLOGY; GENETICS; HUMAN; HYPERPLASIA; INTIMA; METABOLISM; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; AUTOCRINE COMMUNICATION; CELLS, CULTURED; HUMANS; HYPERPLASIA; MALE; MYOCYTES, SMOOTH MUSCLE; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUNICA INTIMA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84905442416     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.282     Document Type: Article

References (46)

1. Suwanabol PA, Kent KC, Liu B. TGF-beta and restenosis revisited: a Smad link. J Surg Res 2011; 167: 287-297
2. Tsai S, Hollenbeck ST, Ryer EJ, Edlin R, Yamanouchi D, Kundi R et al. TGF-beta through Smad3 signaling stimulates vascular smooth muscle cell proliferation and neointimal formation. Am J Physiol Heart Circ Physiol 2009; 297: H540-H549
3. McCaffrey TA, Consigli S, Du B, Falcone DJ, Sanborn TA, Spokojny AM et al. Decreased type II/type I TGF-beta receptor ratio in cells derived from human atherosclerotic lesions. Conversion from an antiproliferative to profibrotic response to TGF-beta1. J Clin Invest 1995; 96: 2667-2675
4. Perlman H, Sata M, Krasinski K, Dorai T, Buttyan R, Walsh K. Adenovirus-encoded hammerhead ribozyme to Bcl-2 inhibits neointimal hyperplasia and induces vascular smooth muscle cell apoptosis. Cardiovasc Res 2000; 45: 570-578
5. Pollman MJ, Hall JL, Mann MJ, Zhang L, Gibbons GH. Inhibition of neointimal cell bcl-x expression induces apoptosis and regression of vascular disease. Nat Med 1998; 4: 222-227
6. Si Y, Ren J,Wang P, Rateri DL, Daugherty A, Shi XD et al. Protein kinase C-delta mediates adventitial cell migration through regulation of monocyte chemoattractant protein-1 expression in a rat angioplasty model. Arterioscler Thromb Vasc Biol 2012; 32: 943-954
7. Sata M, Perlman H, Muruve DA, Silver M, Ikebe M, Libermann TA et al. Fas ligand gene transfer to the vessel wall inhibits neointima formation and overrides the adenovirusmediated T cell response. Proc Natl Acad Sci USA 1998; 95: 1213-1217
8. Han DK, Haudenschild CC, Hong MK, Tinkle BT, Leon MB, Liau G. Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. Am J Pathol 1995; 147: 267-277
9. Bochaton-Piallat ML, Gabbiani F, Redard M, Desmouliere A, Gabbiani G. Apoptosis participates in cellularity regulation during rat aortic intimal thickening. Am J Pathol 1995; 146: 1059-1064
10. Hanke H, Strohschneider T, Oberhoff M, Betz E, Karsch KR. Time course of smooth muscle cell proliferation in the intima and media of arteries following experimental angioplasty. Circ Res 1990; 67: 651-659
11. Kulms D, Schwarz T. Molecular mechanisms of UV-induced apoptosis. Photodermatol Photoimmunol Photomed 2000; 16: 195-201
12. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003; 113: 685-700
13. Hneino M, Bouazza L, Bricca G, Li JY, Langlois D. Density-dependent shift of transforming growth factor-beta-1 from inhibition to stimulation of vascular smooth muscle cell growth is based on unconventional regulation of proliferation, apoptosis and contact inhibition. J Vasc Res 2009; 46: 85-97
14. Orlandi A, Ropraz P, Gabbiani G. Proliferative activity and alpha-smooth muscle actin expression in cultured rat aortic smooth muscle cells are differently modulated by transforming growth factor-beta 1 and heparin. Exp Cell Res 1994; 214: 528-536
15. Markowitz SD, Roberts AB. Tumor suppressor activity of the TGF-beta pathway in human cancers. Cytokine Growth Factor Rev 1996; 7: 93-102
16. Bjorkerud S. Effects of transforming growth factor-beta 1 on human arterial smooth muscle cells in vitro. Arterioscler Thromb 1991; 11: 892-902
17. Christen T, Bochaton-Piallat ML, Neuville P, Rensen S, Redard M, van Eys G et al. Cultured porcine coronary artery smooth muscle cells. A new model with advanced differentiation. Circ Res 1999; 85: 99-107
18. Grainger DJ, Kirschenlohr HL, Metcalfe JC, Weissberg PL, Wade DP, Lawn RM. Proliferation of human smooth muscle cells promoted by lipoprotein(a). Science 1993; 260: 1655-1658
19. Majesky MW, Lindner V, Twardzik DR, Schwartz SM, Reidy MA. Production of transforming growth factor beta 1 during repair of arterial injury. J Clin Invest 1991; 88: 904-910
20. Nabel EG, Shum L, Pompili VJ, Yang ZY, San H, Shu HB et al. Direct transfer of transforming growth factor beta 1 gene into arteries stimulates fibrocellular hyperplasia. Proc Natl Acad Sci USA 1993; 90: 10759-10763
21. Suwanabol PA, Seedial SM, Shi X, Zhang F, Yamanouchi D, Roenneburg D et al. Transforming growth factor-beta increases vascular smooth muscle cell proliferation through the Smad3 and extracellular signal-regulated kinase mitogen-activated protein kinases pathways. J Vasc Surg 2012; 56: e441
22. Roskoski Jr R. Vascular endothelial growth factor (VEGF) signaling in tumor progression. Crit Rev Oncol Hematol 2007; 62: 179-213
23. Khurana R, Moons L, Shafi S, Luttun A, Collen D, Martin JF et al. Placental growth factor promotes atherosclerotic intimal thickening and macrophage accumulation. Circulation 2005; 111: 2828-2836
24. Ferlosio A, Arcuri G, Doldo E, Scioli MG, De Falco S, Spagnoli LG et al. Age-related increase of stem marker expression influences vascular smooth muscle cell properties. Atherosclerosis 2012; 224: 51-57
25. Orlandi A, Ferlosio A, Arcuri G, Scioli MG, De Falco S, Spagnoli LG. Flt-1 expression influences apoptotic susceptibility of vascular smooth muscle cells through the NF-kappaB/IAP-1 pathway. Cardiovasc Res 2010; 85: 214-223
26. Edlin RS, Tsai S, Yamanouchi D, Wang C, Liu B, Kent KC. Characterization of primary and restenotic atherosclerotic plaque from the superficial femoral artery: potential role of Smad3 in regulation of SMC proliferation. J Vasc Surg 2009; 49: 1289-1295
27. Jeon SH, Chae BC, Kim HA, Seo GY, Seo DW, Chun GT et al. Mechanisms underlying TGF-beta1-induced expression of VEGF and Flk-1 in mouse macrophages and their implications for angiogenesis. J Leukoc Biol 2007; 81: 557-566
28. Hishikawa K, Oemar BS, Tanner FC, Nakaki T, Fujii T, Luscher TF. Overexpression of connective tissue growth factor gene induces apoptosis in human aortic smooth muscle cells. Circulation 1999; 100: 2108-2112
29. McCaffrey TA, Du B, Fu C, Bray PJ, Sanborn TA, Deutsch E et al. The expression of TGF-beta receptors in human atherosclerosis: evidence for acquired resistance to apoptosis due to receptor imbalance. J Mol Cell Cardiol 1999; 31: 1627-1642
30. Nataatmadja M, West J, West M. Overexpression of transforming growth factor-beta is associated with increased hyaluronan content and impairment of repair in Marfan syndrome aortic aneurysm. Circulation 2006; 114: I371-I377
31. Ferns GA, Avades TY. The mechanisms of coronary restenosis: insights from experimental models. Int J Exp Pathol 2000; 81: 63-88
32. Walsh K, Smith RC, Kim HS. Vascular cell apoptosis in remodeling, restenosis, and plaque rupture. Circ Res 2000; 87: 184-188
33. Wolff RA, Ryomoto M, Stark VE, Malinowski R, Tomas JJ, Stinauer MA et al. Antisense to transforming growth factor-beta1 messenger RNA reduces vein graft intimal hyperplasia and monocyte chemotactic protein 1. J Vasc Surg 2005; 41: 498-508
34. Lu P, Wang S, Cai W, Sheng J. TGF-beta 1/Smad3 expression and its effects on carotid intimal hyperplasia. Front Biosci (Elite Ed) 2012; 4: 2022-2028
35. Kundi R, Hollenbeck ST, Yamanouchi D, Herman BC, Edlin R, Ryer EJ et al. Arterial gene transfer of the TGF-beta signalling protein Smad3 induces adaptive remodelling following angioplasty: a role for CTGF. Cardiovasc Res 2009; 84: 326-335
36. Reis ED, Roque M, Cordon-Cardo C, Drobnjak M, Fuster V, Badimon JJ. Apoptosis, proliferation, and p27 expression during vessel wall healing: time course study in a mouse model of transluminal femoral artery injury. J Vasc Surg 2000; 32: 1022-1029
37. Reddy MK, Vasir JK, Sahoo SK, Jain TK, Yallapu MM, Labhasetwar V. Inhibition of apoptosis through localized delivery of rapamycin-loaded nanoparticles prevented neointimal hyperplasia and reendothelialized injured artery. Circ Cardiovasc Interv 2008; 1: 209-216
38. Asahara T, Chen D, Tsurumi Y, Kearney M, Rossow S, Passeri J et al. Accelerated restitution of endothelial integrity and endothelium-dependent function after phVEGF165 gene transfer. Circulation 1996; 94: 3291-3302
39. ardwaj S, Roy H, Heikura T, Yla-Herttuala S. VEGF-A, VEGF-D and VEGFD( DeltaNDeltaC) induced intimal hyperplasia in carotid arteries. Eur J Clin Invest 2005; 35: 669-676
40. Shiojima I, Walsh K. The role of vascular endothelial growth factor in restenosis: the controversy continues. Circulation 2004; 110: 2283-2286
41. Ohtani K, Egashira K, Hiasa K, Zhao Q, Kitamoto S, Ishibashi M et al. Blockade of vascular endothelial growth factor suppresses experimental restenosis after intraluminal injury by inhibiting recruitment of monocyte lineage cells. Circulation 2004; 110: 2444-2452
42. Koga J, Matoba T, Egashira K, Kubo M, Miyagawa M, Iwata E et al. Soluble Flt-1 gene transfer ameliorates neointima formation after wire injury in flt-1 tyrosine kinase-deficient mice. Arterioscler Thromb Vasc Biol 2009; 29: 458-464
43. Hedman M, Hartikainen J, Syvanne M, Stjernvall J, Hedman A, Kivela A et al. Safety and feasibility of catheter-based local intracoronary vascular endothelial growth factor gene transfer in the prevention of postangioplasty and in-stent restenosis and in the treatment of chronic myocardial ischemia: phase II results of the Kuopio Angiogenesis Trial (KAT). Circulation 2003; 107: 2677-2683
44. Ferrari G, Pintucci G, Seghezzi G, Hyman K, Galloway AC, Mignatti P. VEGF, a prosurvival factor, acts in concert with TGF-beta1 to induce endothelial cell apoptosis. Proc Natl Acad Sci USA 2006; 103: 17260-17265
45. Sanchez-Elsner T, Botella LM, Velasco B, Corbi A, Attisano L, Bernabeu C. Synergistic cooperation between hypoxia and transforming growth factor-beta pathways on human vascular endothelial growth factor gene expression. J Biol Chem 2001; 276: 38527-38535
46. Leitges M, Mayr M, Braun U, Mayr U, Li C, Pfister G et al. Exacerbated vein graft arteriosclerosis in protein kinase C σ - null mice. J Clin Invest 2001; 108: 1505-1512