Apoptosis in inflammatory-fibroproliferative disorders of the vessel wall

Cardiovascular Research

Volumn 45, Issue 3, 2000, Pages 756-765

  Walsh, Kenneth ^a,b   Isner, Jeffrey M ^a  

^a ST ELIZABETH'S MEDICAL CENTER   (United States)

^b Program in Cell   (United States)

Author keywords

Apoptosis; Arteries; Atherosclerosis; Infection inflammation; Smooth muscle

Indexed keywords

CELL SURFACE RECEPTOR; FAS ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2; PROTEIN P53; TUMOR NECROSIS FACTOR RECEPTOR;

APOPTOSIS; ATHEROSCLEROSIS; BLOOD VESSEL INJURY; CELL VIABILITY; HUMAN; INFLAMMATION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; RESTENOSIS; REVIEW; VASCULAR DISEASE;

ANTIGENS, CD95; APOPTOSIS; ARTERIOSCLEROSIS; FAS LIGAND PROTEIN; MEMBRANE GLYCOPROTEINS; MUSCLE, SMOOTH, VASCULAR; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0033972856     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0008-6363(99)00270-9     Document Type: Review

References (126)

1. Bennett M.R., Evan G.I., Schwartz S.M. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atheroschlerotic plaques. J Clin Invest. 95:1995;2266-2274.
2. Geng J.Y., Libby P. Evidence for apoptosis in advanced human atheroma: colocalization with interleukin-1β converting enzyme. Am J Pathol. 147:1995;251-266.
3. Isner J.M., Kearney M., Bortman S., Passeri J. Apoptosis in human atherosclerosis and restenosis. Circulation. 91:1995;2703-2711.
4. Mallat Z., Ohan J., Leseche G., Tedugi A. Colocalization of CPP-32 with apoptotic cells in human atherosclerotic plaques. Circulation. 96:1997;424-428.
5. Bjorkerud S., Bjorkerud B. Apoptosis is abundant in human atherosclerotic lesions, especially in inflammatory cells (macrophages and T cells), and may contribute to the accumulation of gruel and plaque instability. Am J Pathol. 149:1996;367-380.
6. Kockx M., De Meyer G., Muhring J., et al. Apoptosis and related proteins in different stages of human atherosclerotic plaques. Circulation. 97:1998;2307-2315.
7. Bennett M., Macdonald K., Chan S., Boyle J., Weissberg P. Cooperative interactions between RB and p53 regulate cell proliferation, cell senescence, and apoptosis in human vascular smooth muscle cells from atherosclerotic plaques. Circ Res. 82:1998;704-712.
8. Crisby M., Kallin B., Thyberg J., et al. Cell death in human atherosclerotic plaques involves both oncosis and apoptosis. Atherosclerosis. 130:1997;17-27.
9. Kearney M., Pieczek A., Haley L., et al. Histopathology of in-stent restenosis in patients with peripheral artery disease. Circulation. 95:1997;1998-2002.
10. Kockx M.M., DeMeyer G.R.Y., Muhring J., et al. Distribution of cell replication and apoptosis in atherosclerotic plaques of cholesterol-fed rabbits. Atherosclerosis. 120:1996;115-124.
11. Kockx M., De Meyer G., Buyssens N., et al. Cell composition, replication, and apoptosis in atherosclerotic plaques after 6 months of cholesterol withdrawal. Circ Res. 83:1998;378-387.
12. Shindo J., Ishibashi T., Yokoyama K., et al. Granulocyte-macrophage colony-stimulating factor prevents the progression of atherosclerosis via changes in the cellular and extracellular composition of atherosclerotic lesions in watanabe heritable hyperlipidemic rabbits. Circulation. 99:1999;2150-2156.
13. Wang B., Ho H., Lin P., et al. Regression of atherosclerosis: role of nitric oxide and apoptosis. Circulation. 99:1999;1236-1241.
14. Lutgens E., Daemen M., Kockx M., et al. Atherosclerosis in APOE*3-Leiden transgenic mice: from proliferative to atheromatous stage. Circulation. 99:1999;276-283.
15. Harada K., Chen Z., Ishibashi S., et al. Apoptotic cell death in atherosclerotic plaques of hyperlipidemic knockout mice. Atherosclerosis. 135:1997;235-239.
16. Clowes A.W., Reidy M.A., Clowes M.M. Mechanisms of stenosis after arterial injury. Lab Invest. 49:1983;208-215.
17. Clowes A.W., Reidy M.A., Clowes M.M. Kinetics of cellular proliferation after arterial injury. I. smooth muscle cell growth in the absence of endothelium. Lab Invest. 49:1983;327-333.
18. Bochaton-Piallat M., Gabbiani F., Redard M., Desmouliere A., Gabbiani G. Apoptosis participates in cellularity regulation during rat aortic intimal thickening. Am J Pathol. 146:1995;1059-1064.
19. Han D.K.M., Haudenschild C.C., Hong M.K., et al. Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. Am J Pathol. 147:1995;267-277.
20. Perlman H., Maillard L., Krasinski K., Walsh K. Evidence for the rapid onset of apoptosis in medial smooth muscle cells following balloon injury. Circulation. 95:1997;981-987.
21. Pollman M.J., Hall Z.L., Mann M.J., Zhang L., Gibbons G.H. Inhibition of neointimal cell bcl-x expression induces apoptosis and regression of vascular disease. Nat Med. 4:1998;222-227.
22. Rivard A., Luo Z., Perlman H., et al. Early cell loss after angioplasty results in a disproportionate decrease in percutaneous gene transfer to the vessel wall. Hum Gene Ther. 10:1999;711-721.
23. Pollman M.J., Hall J.L., Gibbons G.H. Determinants of vascular smooth muscle cell apoptosis after balloon angioplasty injury. Circ Res. 84:1999;113-121.
24. Malik N., Francis S.E., Holt C.M., et al. Apoptosis and cell proliferation after porcine coronary angioplasty. Circulation. 98:1998;1657-1665.
25. Ashkenazi A., Dixit V. Death receptors: signaling and modulation. Science. 281:1998;1305-1308.
26. Nagata S., Golstein P. The Fas death factor. Science. 267:1995;1449-1456.
27. Dockrell D., Badley A., Villacian J., et al. The expression of Fas ligand by macrophages and its upregulation by human immunodeficiency virus infection. J Clin Invest. 101:1998;2394-2405.
28. Oshimi Y., Oda S., Honda Y., Nagata S., Miyazaki S. Involvement of Fas ligand and Fas-mediated pathway in the cytotoxicity of human natural killer cells. J Immunol. 157:1996;2909-2915.
29. Nagata S. Apoptosis by death factor. Cell. 88:1997;355-365.
30. Kiener P.A., Davis P.M., Starling G.C., et al. Differential induction of apoptosis by Fas-Fas ligand interactions in human monocytes and macrophages. J Exp Med. 185:1997;1511-1516.
31. Kiener P., Davis P., Rankin B., et al. Human monocytic cells contain high levels of intracellular Fas ligand: rapid release following cellular activation. J Immunol. 159:1997;1594-1598.
32. Griffith T.S., Brunner T., Fletcher S.M., Green D.R., Ferguson T.A. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science. 270:1995;1189-1192.
33. Bellgrau D., Gold D., Selawry H., et al. A role of CD95 ligand in preventing graft rejection. Nature. 377:1995;630-632.
34. Hahne M., Rimoldi D., Schröter M., et al. Melanoma cell expression of Fas (Apo-1/CD95) ligand: Implications for tumor immune escape. Science. 274:1996;1363-1366.
35. Strand S., Hofman W.J., Hug H., et al. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand expressing tumor cells-A mechanism of immune evasion? Nat Med. 2:1996;1361-1366.
36. Niehans G.A., Brunner T., Frizelle S.P., et al. Human lung carcinomas express Fas ligand. Cancer Res. 57:1997;1007-1012.
37. Sata M., Walsh K. TNF regulation of Fas ligand expression on the vascular endothelium modulates leukocyte extravasation. Nat Med. 4:1998;415-420.
38. Takahashi T., Tanaka M., Brannan C., et al. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell. 76:1994;969-976.
39. Watanabe-Fukunaga R., Brannan C., Copeland N., Jenkins N., Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature. 356:1992;314-317.
40. Hewicker M., Trautwein G. Sequential study of vasculitis in MRL mice. Lab Anim. 21:1987;335-341.
41. Berden J.H., Hang L., McConahey P.J., Dixon F.J. Analysis of vascular lesions in murine SLE. Association with serologic abnormalities. J Immunol. 130:1983;1699-1705.
42. Moyer C.F., Reinisch C.L. The role of vascular smooth muscle cells in experimental autoimmune vasculitis. The initiation of delayed type hypersensitivity angitis. Am J Pathol. 117:1984;380-390.
43. Miwa K., Asano M., Horai R., et al. Caspase 1-independent IL-1β release and inflammation induced by the apoptosis inducer Fas ligand. Nat Med. 4:1998;1287-1292.
44. Itoh N., Nagata S. A novel protein domain required for apoptosis: Mutational analysis of human Fas antigen. J Biol Chem. 268:1993;10932-10937.
45. Boldin M.P., Goncharov T.M., Goltsev Y.V., Wallach D. Involvement of Mach, a novel MORT1/FADD-interacting protease, in FAS/Apo-1 and TNF receptor-induced cell death. Cell. 85:1996;803-815.
46. Muzio M., Chinnaiyan A.M., Kischkel F.C., et al. FLICE, a novel, FADD-homologous ICE/CED-3-like protease is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell. 85:1996;817-827.
47. Juo P., Kuo C., Yuan J., Blenis J. Essential requirement for caspase-8/FLICE in the initiation of the Fas-induced apoptotic cascade. Curr Biol. 8:1998;1001-1008.
48. Irmler M., Thome M., Hahne M., et al. Inhibition of death receptor signals by cellular FLIP. Nature. 388:1997;190-195.
49. Hu S., Vincenz C., Ni J., Gentz R., Dixit V.M. I-FLICE, a novel inhibitor of tumor necrosis factor receptor-1 and CD-95-induced apoptosis. J Biol Chem. 272:1997;17255-17257.
50. Srinivasula S.M., Ahmad M., Otilie S., et al. FLAME-1, a novel FADD-like anti-apoptotic molecules that regulates Fas/TNFR1-induced apoptosis. J Biol Chem. 272:1997;18542-18545.
51. Shu H.B., Halpin D.R., Goeddel D.V. Casper is a FADD- and caspase-related inducer of apoptosis. Immunity. 6:1997;751-763.
52. Han D.K.M., Chaudhary P.M., Wright M.E., et al. MRIT, a novel death-effector domain-containing protein, interacts with caspases and BclXL and initiates cell death. Proc Natl Acad Sci USA. 94:1997;11333-11338.
53. Rasper D., Vaillancourt J., Hadano S., et al. Cell death attenuation by 'Usurpin', a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex. Cell Death Differ. 5:1998;271-288.
54. Scaffidi C., Fulda S., Srinivasan A., et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:1998;1675-1687.
55. Li H., Zhu H., Xu C.-J., Yuan J. Cleavage of BID by caspase8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:1998;491-501.
56. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:1998;481-490.
57. Enari M., Sakahira H., Yokoyama H., et al. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature. 391:1998;43-50.
58. Beg A.A., Baltimore D. An essential role for NF-κB in preventing TNF-α-induced cell death. Science. 274:1996;782-784.
59. Wu M., Ao Z., Prasad K., Wu R., Schlossman S. IEX-1L, an apoptosis inhibitor involved in NF-κB-mediated cell survival. Science. 281:1998;998-1001.
60. Erl W., Hansson G., de Martin R., et al. Nuclear factor-kappa B regulates induction of apoptosis and inhibitor of apoptosis protein-1 expression in vascular smooth muscle cells. Circ Res. 84:1999;668-677.
61. Wang C.-Y., Mayo M., Korneluk R., Goeddel D., Baldwin A. Jr. NF-κB antiapoptosis: Induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science. 281:1998;1680-1683.
62. Zong W., Edelstein L., Chen C., Bash J., Gelinas C. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-κB that blocks TNFα-induced apoptosis. Genes Dev. 13:1999;382-387.
63. Horrevoets A., Fontijn R., van Zonneveld A., et al. Vascular endothelial genes that are responsive to tumor necrosis factor-alpha in vitro are expressed in atherosclerotic lesions, including inhibitor of apoptosis protein-1, stannin, and two novel genes. Blood. 93:1999;3418-3431.
64. Read M., Whitley M., Williams A., Collins T. NF-κB and IκB-α: an inducible regulatory system in endothelial activation. J Exp Med. 179:1994;503-512.
65. Tanaka H., Swanson S.J., Sukhova G., Schoen F.J., Libby P. Smooth muscle cells of the coronary arterial tunica media express tumor necrosis factor-α and proliferate during acute rejection of rabbit cardiac allografts. Am J Pathol. 147:1995;617-626.
66. Libby P., Hansson G.K. Involvement of the immune system in human atherogenesis: Current knowledge and unanswered questions. Lab Invest. 64:1991;5-15.
67. Dimmeler S., Breitschopf K., Haendeler H., Zeiher A. Dephosphorylation targets Bcl-2 for ubiquitin-dependent degradation: a link between the apoptosome and the proteasome pathway. J Exp Med. 189:1999;1815-1822.
68. Spyridopoulos I., Sullivan A.B., Kearney M., Isner J.M., Losordo D.W. Estrogen-receptor-mediated inhibition of human endothelial cell apoptosis: Estradiol as a survival factor. Circulation. 95:1997;1505-1514.
69. Spyridopoulos I., Brogi E., Kearney M., et al. Vascular endothelial growth factor inhibits endothelial cell apoptosis induced by tumor necrosis factor-α: Balance between growth and death signals. J Mol Cell Cardiol. 29:1997;1321-1330.
70. Clausell N., Milossi S., Sett S., Rabinovitch M. In vivo blockade of tumor necrosis factor-α in cholesterol-fed rabbits after cardiac transplant inhibits acute coronary artery neoinimal formation. Circulation. 89:1994;2768-2779.
71. Schreyer S.A., Peschon J.J., LeBoeuf R.C. Accelerated atherosclerosis in mice lacking tumor necrosis factor receptor p55. J Biol Chem. 271:1996;26174-26178.
72. Sata M., Walsh K. Oxidized LDL activates Fas-mediated endothelial cell apoptosis. J Clin Invest. 102:1998;1682-1689.
73. Fukuo K., Nakahashi T., Nomura S., et al. Possible participation of Fas-mediated apoptosis in the mechanism of atherosclerosis. Gerontology. 43:1997;35-42.
74. Cai W., Devaux B., Schaper W., Schaper J. The role of Fas/APO 1 and apoptosis in the development of human atherosclerotic lesions. Atherosclerosis. 131:1997;177-186.
75. Geng Y.-J., Henderson L.E., Levesque E.B., Muszynzki M., Libby P. Fas is expressed in human atherosclerotic intima and promotes apoptosis of cytokine-primed human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 17:1997;2200-2208.
76. Dong C., Wilson J.E., Winters G.L., McManus B.M. Human transplant coronary artery disease: pathological evidence for Fas-mediated apoptotic cytotoxicity in allograft arteriopathy. Lab Invest. 74:1996;921-931.
77. Sata M., Perlman H., Muruve D.A., et al. Fas ligand gene transfer to the vessel wall inhibits neointima formation and overrides the adenovirus-mediated T cell response. Proc Natl Acad Sci USA. 95:1998;1213-1217.
78. Luo Z., Sata M., Nguyen T., et al. Adenovirus-mediated delivery of Fas ligand inhibits intimal hyperplasia after balloon injury in immunologically primed animals. Circulation. 99:1999;1776-1779.
79. Suda T., Hashimoto H., Tanaka M., Ochi T., Nagata S. Membrane Fas ligand kills human peripheral blood T lymphocytes, and soluble Fas ligand blocks the killing. J Exp Med. 186:1997;2045-2050.
80. Tanaka M., Itai T., Adachi M., Nagata S. Downregulation of Fas ligand by shedding. Nature Med. 4:1998;31-36.
81. Fukuo K., Suhara T., Nakahashi T., et al. Activated T cells induce up-regulation of Fas antigen in cultured endothelial cells. Heart Vessels. 12:(Suppl):1997;81-83.
82. Richardson B.C., Lalwani N.D., Johnson K.J., Marks R.M. Fas ligation triggers apoptosis in macrophages but not endothelial cells. Eur J Immunol. 24:1994;2640-2645.
83. Sata M., Walsh K. Endothelial cell apoptosis induced by oxidized LDL is associated with the downregulation of the cellular caspase inhibitor FLIP. J Biol Chem. 273:1998;33103-33106.
84. Rodriguez I., Matsuura K., Khatib K., et al. A bcl-2 transgene expressed in hepatocytes protects mice from fulminant liver destruction but not from rapid death induced by anti-Fas antibody injection. J Exp Med. 183:1996;1031-1036.
85. Lacronique V., Mignon A., Fabre M., et al. Bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nat Med. 2:1996;80-86.
86. Itoh N., Tsujimoto Y., Nagata S. Effect of bcl-2 on Fas antigen-mediated cell death. J Immunol. 151:1993;621-627.
87. Strasser A., Harris A.W., Huang D.C.S., Krammer P.H., Cory S. Bcl-2 and Fas/APO-1 regulates distinct pathways to lymphocyte apoptosis. EMBO J. 14:1995;6136-6147.
88. Okura T., Gong L., Kamitani T., et al. Protection against Fas/APO-1 and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J Immunol. 157:1996;4277-4281.
89. Maria R.D., Lenti L., Malisan F., et al. Requirement for GD3 ganglioside in CD95- and ceramide-induced apoptosis. Science. 1997:1997;1652-1655.
90. Melino G., Bernassola F., Knight R.A., et al. S-nitrosylation regulates apoptosis. Nature. 388:1997;432-433.
91. Mannick J.B., Miao X.Q., Stamler J.S. Nitric oxide inhibits Fas-induced apoptosis. J Biol Chem. 272:1997;24125-24128.
92. Mannick J.B., Hausladen A., Liu L., et al. Fas-induced caspase denitrosylation. Science. 284:1999;651-654.
93. Escargueil-Blanc I., Meilhac O., Pieraggi M.-T., Arnal J.-F., Salvayre R., Negre-Salvayre A. Oxidized LDLs induce massive apoptosis of cultured human endothelial cells through a calcium-dependent pathway. Arterioscler Thromb Vasc Biol. 17:1997;331-339.
94. Dimmeler S., Haendeler J., Galle J., Zeiher A.M. Oxidized low-density lipoprotein induces apoptosis of human endothelial cells by activation of CPP32-like proteases. Circulation. 95:1997;1760-1763.
95. Juckett M.B., Balla J., Balla G., et al. Ferritin protects endothelial cells from oxidized low density lipoprotein in vitro. Am J Pathol. 147:1995;782-789.
96. Harada-Shiba M., Kinoshita M., Kamido H., Shimokado K. Oxidized low density lipoprotein induces apoptosis in cultured human umbilical vein endothelial cells by common and unique mechanisms. J Biol Chem. 273:1998;9681-9687.
97. Lemaire S., Lizard G., Monier S., et al. Different patterns of IL-1beta secretion, adhesion molecule expression and apoptosis induction in human endothelial cells treated with 7alpha-, 7beta-hycroxycholesterol, or 7-ketocholesterol. FEBS Lett. 440:1998;434-439.
98. Steinberg D. Low density lipoprotein oxidation and its pathological significance. J Biol Chem. 272:1997;20963-20966.
99. Ylä-Herttuala S., Palinski W., Rosenfeld M.E., et al. Evidence for the presence of oxidatively modified LDL in atherosclerotic lesions of rabbit and man. J Clin Invest. 84:1989;1086-1095.
100. Haberland M.E., Fong D., Cheng L. Malondialdehyde altered protein occurs in atheroma of Watanabe heritable hyperlipidemic rabbits. Science. 241:1988;215-218.
101. Li D., Yang B., Mehta J. Ox-LDL induces apoptosis in human coronary artery endothelial cells: role of PKC, PTK, bcl-2, and Fas. Am J Physiol. 275:1998;H568-H576.
102. Suhara T., Fukuo K., Sugimoto T., et al. Hydrogen peroxide induces up-regulation of Fas in human endothelial cells. J Immunol. 160:1998;4042-4047.
103. L, and inhibitor of programmed cell death. Nature. 381:1996;335-341.
104. L forms an ion channel in synthetic lipid membranes. Nature. 385:1997;353-357.
105. Yang J., Liu X., Bhalla K., et al. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 275:1997;1129-1132.
106. Miyashita T., Reed J.D. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 80:1995;293-299.
107. Miyashita T., Harigal M., Hanada M., Reed J.C. Identification of a p53-dependent negative response element in the bcl-2 gene. Cancer Res. 54:1994;3131-3135.
108. El-Deiry W.S., Tokino T., Velculescu V.E., et al. WAF1, a potential mediator of p53 tumor suppression. Cell. 75:1993;817-825.
109. Yonemitsu Y., Kaneda Y., Tanaka S., et al. Transfer of wild-type p53 gene effectively inhibits vascular smooth muscle cell proliferation in vitro and in vivo. Circ Res. 82:1998;147-156.
110. Ihling C., Haendeler J., Menzel G., et al. Co-expression of p53 and MDM2 in human atherosclerosis: implications for the regulation of cellularity of atherosclerotic lesions. J Pathol. 185:1998;303-312.
111. Haupt Y., Maya R., Kazaz A., Oren M. Mdm2 promotes the rapid degradation of p53. Nature. 387:1997;296-299.
112. Tanaka K., Zou J., Takeda K., et al. Effects of human cytomegalovirus immediate-early proteins on p53-mediated apoptosis in coronary artery smooth muscle cells. Circulation. 99:1999;1656-1659.
113. Guevara N., Kim H., Antonova E., Chan L. The absence of p53 accelerates atherosclerosis by increasing cell proliferation in vivo. Nat Med. 5:1999;335-339.
114. Bennett M.R., Evan G.I., Schwartz S.M. Apoptosis in rat vascular smooth muscle cells is regulated by p53-dependent and -independent pathways. Circ Res. 77:1995;266-273.
115. Guo K., Andrés V., Walsh K. Nitric oxide-induced downregulation of cdk2 activity and cyclin A gene transcription in vascular smooth muscle cells. Circulation. 20:1998;2066-2072.
116. Pollman M.J., Yamada T., Horiuchi M., Gibbons G.H. Vasoactive substances regulate vascular smooth muscle apoptosis. Countervailing influences of nitric oxide and angiotensin II. Circ Res. 79:1996;748-756.
117. Fukuo K., Hata S., Suhara T., et al. Nitric oxide induces upregulation of Fas and apoptosis in vascular smooth muscle. Hypertension. 27:1996;823-826.
118. 1 transition in vascular smooth muscle cells. Mol Cell Biol. 13:1993;3722-3733.
119. Weir L., Chen D., Pastore C., Isner J.M., Walsh K. Expression of GAX, a growth-arrest homeobox gene, is rapidly down-regulated in the rat carotid artery during the proliferative response to balloon injury. J Biol Chem. 270:1995;5457-5461.
120. Perlman H., Sata M., Le Roux A., et al. Bax-mediated cell death by the Gax homeoprotein requires mitogen activation but is independent of cell cycle activity. EMBO J. 17:1998;3576-3586.
121. Perlman H., Luo Z., Krasinski K., et al. Adenoviral-mediated delivery of the Gax transcription factor to rat carotid arteries inhibits smooth muscle proliferation and induces apoptosis. Gene Ther. 6:1999;758-763.
122. Corjay M., Kearney M., Munzer D., Diamond S., Stoltenborg J. Antiproliferative gene BTG1 is highly expressed in apoptotic cells in macrophage-rich areas of advanced lesions in Watanabe heritable hyperlipidemic rabbit and human. Lab Invest. 78:1998;847-858.
123. Gerber H.-P., Dixit V., Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J Biol Chem. 273:1998;13313-13316.
124. Fujio F., Walsh K. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem. 274:1999;16349-16354.
125. Gerber H.-P., McMurtrey A., Kowalski J., et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway: Requirement for Flk-1/KDR activation. J Biol Chem. 273:1998;30336-30343.
126. Bennett M., Macdonald K., Chan S.-W., Luzio J.P., Simari R., Weissberg P. Cell surface trafficking of Fas: a rapid mechanism of p53-mediated apoptosis. Science. 282:1998;290-293.