Role of Fas/Fas-L in vascular cell apoptosis

Journal of Cardiovascular Pharmacology

Volumn 53, Issue 2, 2009, Pages 100-108

  Stoneman, Victoria E A ^a   Bennett, Martin R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Caspases; Endothelial cells; Fas L; Hemodynamic forces; Macrophages; Vascular smooth muscle

Indexed keywords

CASPASE 8; CD28 ANTIGEN; CD69 ANTIGEN; DEATH RECEPTOR; DECOY RECEPTOR 3; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FAS LIGAND; FLICE INHIBITORY PROTEIN; PROTEIN BCL 2; PROTEIN KINASE B; ZINC FINGER PROTEIN;

APOPTOSIS; ATHEROSCLEROSIS; BLOOD VESSEL; BLOOD VESSEL WALL; CD4+ T LYMPHOCYTE; CELL INTERACTION; ENDOTHELIUM CELL; HUMAN; IMMUNE SYSTEM; IN VIVO STUDY; INFLAMMATORY CELL; MACROPHAGE; MECHANICAL STRESS; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; T LYMPHOCYTE; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE; ANIMAL; CARDIOVASCULAR DISEASE; CELL COMMUNICATION; CYTOLOGY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; BLOOD VESSELS; CARDIOVASCULAR DISEASES; CELL COMMUNICATION; ENDOTHELIUM, VASCULAR; FAS LIGAND PROTEIN; HUMANS; MACROPHAGES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 65549143999     PISSN: 01602446     EISSN: None     Source Type: Journal    
DOI: 10.1097/FJC.0b013e318198fe60     Document Type: Review

References (123)

1. Degterev A, Boyce M, Yuan J. A decade of caspases. Oncogene. 2003; 22:8543-8567.
2. Nagata S. Apoptotic DNA fragmentation. Exp Cell Res. 2000;256: 12-18.
3. Strasser A, O'Connor L, Dixit VM. Apoptosis signaling. Annu Rev Biochem. 2000;69:217-245.
4. Leist M, Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol. 2001;2:589-598. (Pubitemid 33674010)
5. Wen LP, Fahrni JA, Troie S, et al. Cleavage of focal adhesion kinase by caspases during apoptosis. J Biol Chem. 1997;272:26056-26061. (Pubitemid 27438936)
6. Brown SB, Bailey K, Savill J. Actin is cleaved during constitutive apoptosis. Biochem J. 1997;323(Pt 1):233-237.
7. Bauriedel G, Hutter R,Welsch U, et al. Role of smooth muscle cell death in advanced coronary primary lesions: implications for plaque instability. Cardiovasc Res. 1999;41:480-488. (Pubitemid 29087345)
8. Henderson EL, Gang YJ, Sukhova GK, et al. Death of smooth muscle cells and expression of mediators of apoptosis by T lymphocytes in human abdominal aortic aneurysms. Circulation. 1999;99:96-104. (Pubitemid 29035963)
9. Isner J, Kearney M, Bortman S, et al. Apoptosis in human atherosclerosis and restenosis. Circulation. 1995;91:2703-2711.
10. Okura T, Watanabe S, Jiang Y, et al. Soluble Fas ligand and atherosclerosis in hypertensive patients. J Hypertens. 2002;20:895-898. (Pubitemid 34913670)
11. Slomp J, Gittenberger de Groot AC, Glukhova MA, et al. Differentiation, dedifferentiation, and apoptosis of smooth muscle cells during the development of the human ductus arteriosus. Arterioscler Thromb Vasc Biol. 1997;17:1003-1009. (Pubitemid 27209281)
12. Kim HS, Hwang KK, Seo JW, et al. Apoptosis and regulation of Bax and Bcl-X proteins during human neonatal vascular remodeling. Arterioscler Thromb Vasc Biol. 2000;20:957-963.
13. Ashton SV, Whitley GS, Dash PR, et al. Uterine spiral artery remodeling involves endothelial apoptosis induced by extravillous trophoblasts through Fas/FasL interactions. Arterioscler Thromb Vasc Biol. 2005;25: 102-108.
14. Harris LK, Keogh RJ, Wareing M, et al. Invasive trophoblasts stimulate vascular smooth muscle cell apoptosis by a Fas ligand-dependent mechanism. Am J Pathol. 2006;169:1863-1874. (Pubitemid 351182015)
15. Feinberg RN, Latker CH, Beebe DC. Localized vascular regression during limb morphogenesis in the chicken embryo. I. Spatial and temporal changes in the vascular pattern. Anat Rec. 1986;214:405-409.
16. Cho A, Mitchell L, Koopmans D, et al. Effects of changes in blood flow rate on cell death and cell proliferation in carotid arteries of immature rabbits. Circ Res. 1997;81:328-337. (Pubitemid 27362519)
17. Isner JM, Asahara T. Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest. 1999;103: 1231-1236. (Pubitemid 29218292)
18. Djonov V, Schmid M, Tschanz SA, et al. Intussusceptive angiogenesis: its role in embryonic vascular network formation. Circ Res. 2000;86: 286-292. (Pubitemid 30108822)
19. Meeson A, Palmer M, Calfon M, et al. A relationship between apoptosis and flow during programmed capillary regression is revealed by vital analysis. Development. 1996;122:3929-3938. (Pubitemid 27033887)
20. Kockx MM. Apoptosis in the atherosclerotic plaque-quantitative and qualitative aspects. Arterioscler Thromb Vasc Biol. 1998;18:1519-1522.
21. Dimmeler S, Hermann C, Zeiher AM. Apoptosis of endothelial cells. Contribution to the pathophysiology of atherosclerosis? Eur Cytokine Netw. 1998;9:697-698.
22. Kearney M, Pieczek A, Haley L, et al. Histopathology of in-stent restenosis in patients with peripheral artery disease. Circulation. 1997; 95:1998-2002. (Pubitemid 27184264)
23. Malik N, Francis SE, Holt CM, et al. Apoptosis and cell proliferation after porcine coronary angioplasty. Circulation. 1998;98:1657-1665. (Pubitemid 28500389)
24. Sata M, Perlman HR, Muruve DA, et al. Fas ligand gene transfer to the vessel wall inhibits neointima formation and overrides the adenovirusmediated T cell response. Proc Natl Acad Sci U S A. 1998;95: 1213-1217. (Pubitemid 28124938)
25. Perlman H, Maillard L, Krasinski K, et al. Evidence for the rapid onset of apoptosis in medial smooth muscle cells after balloon injury. Circulation. 1997;95:981-987. (Pubitemid 27091544)
26. Jiang C, Yang YF, Cheng SH. Fas ligand gene therapy for vascular intimal hyperplasia. Curr Gene Ther. 2004;4:33-39. (Pubitemid 38854944)
27. Diez J, Panizo A, Hernandez M, et al. Is the regulation of apoptosis altered in smooth muscle cells of adult spontaneously hypertensive rats? Hypertension. 1997;29:776-780.
28. Sharifi AM, Schiffrin EL, Iwashina M, et al. Apoptosis in vasculature of spontaneously hypertensive rats-effect of an angiotensin converting enzyme inhibitor and a calcium channel antagonist. Am J Hypertens. 1998;11:1108-1116. (Pubitemid 28451916)
29. Lopez-Candales A, Holmes DR, Liao SX, et al. Decreased vascular smooth muscle cell density in medial degeneration of human abdominal aortic aneurysms. Am J Pathol. 1997;150:993-1007. (Pubitemid 27106171)
30. He R, Guo DC, Estrera AL, et al. Characterization of the inflammatory and apoptotic cells in the aortas of patients with ascending thoracic aortic aneurysms and dissections. J Thorac Cardiovasc Surg. 2006;131: 671-678. (Pubitemid 43312897)
31. Moldovan NI, Qian Z, Chen Y, et al. Fas-mediated apoptosis in accelerated graft arteriosclerosis. Angiogenesis. 1998;2:245-254. (Pubitemid 128513124)
32. Trauth BC, Klas C, Peters AM, et al. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science. 1989;245:301-305. (Pubitemid 19196649)
33. Yonehara S, Ishii A, Yonehara M. A cell killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J Exp Med. 1989;169:1747-1756. (Pubitemid 19126830)
34. Nagata S, Golstein P. The Fas death factor. Science. 1995;267: 1449-1456.
35. Kayagaki N, Kawasaki A, Ebata T, et al. Metalloproteinase-mediated release of human Fas ligand. J Exp Med. 1995;182:1777-1783.
36. Geng YJ, Henderson LE, Levesque EB, et al. Fas is expressed in human atherosclerotic intima and promotes apoptosis of cytokine-primed human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 1997;17:2200-2208. (Pubitemid 28057122)
37. Grivennikov SI, Kuprash DV, Liu ZG, et al. Intracellular signals and events activated by cytokines of the tumor necrosis factor superfamily: from simple paradigms to complex mechanisms. Int Rev Cytol. 2006; 252:129-161.
38. Chinnaiyan A, O'Rourke K, Tewari M, et al. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell. 1995;81:505.
39. Peter ME, Krammer PH. The CD 95(APO-1/Fas) DISC and beyond. Cell Death Differ. 2003;10:26-35.
40. Suhara T, Mano T, Oliveira BE, et al. Phosphatidylinositol 3-kinase/Akt signaling controls endothelial cell sensitivity to Fas-mediated apoptosis via regulation of FLICE-inhibitory protein (FLIP). Circ Res. 2001;89: 13-19. (Pubitemid 34135486)
41. Aschkenazi S, Straszewski S, Verwer KM, et al. Differential regulation and function of the Fas/Fas ligand system in human trophoblast cells. Biol Reprod. 2002;66:1853-1861. (Pubitemid 34547287)
42. Pitti RM, Marsters SA, Lawrence DA, et al. Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature. 1998; 396:699-703.
43. Jenkins M, Keir M, McCune JM. A membrane-bound Fas decoy receptor expressed by human thymocytes. J Biol Chem. 2000;275:7988-7993. (Pubitemid 30159709)
44. Li W, Zhang C, Chen C, et al. Correlation between expression of DcR3 on tumor cells and sensitivity to FasL. Cell Mol Immunol. 2007;4: 455-460.
45. Bennett M, Evan G, Schwartz S. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest. 1995;95:2266-2274.
46. Clarke MC, Figg N, Maguire JJ, et al. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12:1075-1080. (Pubitemid 44353389)
47. Stoneman V, Braganza D, Figg N, et al. Monocyte/macrophage suppression in CD11b diphtheria toxin receptor transgenic mice differentially affects atherogenesis and established plaques. Circ Res. 2007;100:884-893. (Pubitemid 46555694)
48. Kleemann R, Zadelaar S, Kooistra T. Cytokines and atherosclerosis: a comprehensive review of studies in mice. Cardiovasc Res. 2008;79: 360-376.
49. Dimmeler S, Haendeler J, Galle J, et al. Oxidized low-density lipoprotein induces apoptosis of human endothelial cells by activation of CPP32-like proteases. A mechanistic clue to the 'response to injury' hypothesis. Circulation. 1997;95:1760-1763.
50. Tricot O, Mallat Z, Heymes C, et al. Relation between endothelial cell apoptosis and blood flow direction in human atherosclerotic plaques. Circulation. 2000;101:2450-2453. (Pubitemid 30366245)
51. Choy JC, Granville DJ, Hunt DW, et al. Endothelial cell apoptosis: biochemical characteristics and potential implications for atherosclerosis. J Mol Cell Cardiol. 2001;33:1673-1690. (Pubitemid 32844225)
52. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
53. Richardson B, Lalwani N, Johnson K, et al. Fas ligation triggers apoptosis in macrophages but not endothelial cells. Eur J Immunol. 1994;24:2640-2645. (Pubitemid 24342177)
54. Askenasy N, Yolcu ES, Wang Z, et al. Display of Fas ligand protein on cardiac vasculature as a novel means of regulating allograft rejection. Circulation. 2003;107:1525-1531. (Pubitemid 36378492)
55. Yang J, Sato K, Aprahamian T, et al. Endothelial overexpression of Fas ligand decreases atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2004;24:1466-1473. (Pubitemid 39050442)
56. Yang J, Jones SP, Suhara T, et al. Endothelial cell overexpression of Fas ligand attenuates ischemia-reperfusion injury in the heart. J Biol Chem. 2003;278:15185-15191. (Pubitemid 36799853)
57. Mano T, Luo Z, Suhara T, et al. Expression of wild-type and noncleavable Fas ligand by tetracycline-regulated adenoviral vectors to limit intimal hyperplasia in vascular lesions. Hum Gene Ther. 2000;11:1625-1635.
58. Schlag G, Redl H, Hallstrom S. The cell in shock: the origin of multiple organ failure. Resuscitation. 1991;21:137-180.
59. Koide N, Morikawa A, Tumurkhuu G, et al. Lipopolysaccharide and interferon-gamma enhance Fas-mediated cell death in mouse vascular endothelial cells via augmentation of Fas expression. Clin Exp Immunol. 2007;150:553-560. (Pubitemid 350098727)
60. Bielawska-Pohl A, Crola C, Caignard A, et al. Human NK cells lyse organ-specific endothelial cells: analysis of adhesion and cytotoxic mechanisms. J Immunol. 2005;174:5573-5582. (Pubitemid 40593198)
61. Schneider DB, Vassalli G, Wen S, et al. Expression of Fas ligand in arteries of hypercholesterolemic rabbits accelerates atherosclerotic lesion formation. Arterioscler Thromb Vasc Biol. 2000;20:298-308. (Pubitemid 30086084)
62. Kockx MM, Herman AG. Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc Res. 2000;45:736-746.
63. Clarke MC, Littlewood TD, Figg N, et al. Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res. 2008;102:1529-1538.
64. Fukuo K, Nakahashi T, Nomura S, et al. Possible participation of Fasmediated apoptosis in the mechanism of atherosclerosis. Gerontology. 1997;43 (Suppl 1):35-42. (Pubitemid 27230646)
65. Chan S-W, Hegyi L, Scott S, et al. Sensitivity to Fas-mediated apoptosis is determined below receptor level in vascular smooth muscle cells. Circ Res. 2000;86:1038-1046. (Pubitemid 30367862)
66. Peduto Eberl L, Guillou L, Saraga E, et al. Fas and Fas ligand expression in tumor cells and in vascular smooth-muscle cells of colonic and renal carcinomas. Int J Cancer. 1999;81:772-778. (Pubitemid 29214389)
67. Sata M, Suhara T, Walsh K. Vascular endothelial cells and smooth muscle cells differ in expression of Fas and Fas ligand and in sensitivity to Fas ligand-induced cell death: implications for vascular disease and therapy. Arterioscler Thromb Vasc Biol. 2000;20:309-316. (Pubitemid 30086085)
68. Kim K. Proteasome inhibitors sensitize human vascular smooth muscle cells to Fas (CD95)-mediated death. Biochem Biophys Res Commun. 2001;281:305-310. (Pubitemid 32928154)
69. Geng YJ. Regulation of programmed cell death or apoptosis in atherosclerosis. Heart Vessels. 1997(Suppl 12):76-80.
70. Bennett M, Macdonald K, Chan S-W, et al. Cell surface trafficking of Fas: a rapid mechanism of p53-mediated apoptosis. Science. 1998;282: 290-293. (Pubitemid 28487200)
71. Rosner D, Stoneman V, Littlewood T, et al. Interferon-gamma induces Fas trafficking and sensitization to apoptosis in vascular smooth muscle cells via a PI3K- and Akt-dependent mechanism. Am J Pathol. 2006;168: 2054-2063. (Pubitemid 43825323)
72. van der Wal AC, Becker AE, van der Loos CM, et al. Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation. 1994;89:36-44.
73. Hosono M, de Boer OJ, van der Wal AC, et al. Increased expression of T cell activation markers (CD25, CD26, CD40L and CD69) in atherectomy specimens of patients with unstable angina and acute myocardial infarction. Atherosclerosis. 2003;168:73-80. (Pubitemid 36555813)
74. Yao PM, Tabas I. Free cholesterol loading of macrophages induces apoptosis involving the Fas pathway. J Biol Chem. 2000;275: 23807-23813. (Pubitemid 30624666)
75. Luo ZY, Sata M, Nguyen T, et al. Adenovirus-mediated delivery of Fas ligand inhibits intimal hyperplasia after balloon injury in immunologically primed animals. Circulation. 1999;99:1776-1779. (Pubitemid 29181403)
76. Luo Z, Garron T, Palasis M, et al. Enhancement of Fas ligand-induced inhibition of neointimal formation in rabbit femoral and iliac arteries by coexpression of p35. Hum Gene Ther. 2001;12:2191-2202. (Pubitemid 34075183)
77. Zadelaar AS, von der Thusen JH, Boesten LS, et al. Increased vulnerability of pre-existing atherosclerosis in ApoE-deficient mice following adenovirus-mediated Fas ligand gene transfer. Atherosclerosis. 2005;183:244-250.
78. Feng X, Li H, Rumbin AA, et al. ApoE2/2Fas2/2 C57BL/6 mice: a novel murine model simultaneously exhibits lupus nephritis, atherosclerosis, and osteopenia. J Lipid Res. 2007;48:794-805. (Pubitemid 46557884)
79. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol. 2006;6:508-519. (Pubitemid 43980523)
80. Goronzy JJ, Weyand CM. Immunosuppression in atherosclerosis: mobilizing the opposition within. Circulation. 2006;114:1901-1904.
81. O'Connell J, Bennett MW, Nally K, et al. Interferon-gamma sensitizes colonic epithelial cell lines to physiological and therapeutic inducers of colonocyte apoptosis. J Cell Physiol. 2000;185:331-338. (Pubitemid 30824238)
82. Shin EC, Shin WC, Choi Y, et al. Effect of interferon-gamma on the susceptibility to Fas (CD95/APO-1)-mediated cell death in human hepatoma cells. Cancer Immunol Immunother. 2001;50:23-30. (Pubitemid 32250043)
83. Assis MC, Freitas C, Saliba AM, et al. Up-regulation of Fas expression by Pseudomonas aeruginosa-infected endothelial cells depends on modulation of iNOS and enhanced production of NO induced by bacterial type III secreted proteins. Int J Mol Med. 2006;18:355-363.
84. Millet A, Bettaieb A, Renaud F, et al. Influence of the nitric oxide donor glyceryl trinitrate on apoptotic pathways in human colon cancer cells. Gastroenterology. 2002;123:235-246. (Pubitemid 34747544)
85. Li CQ, Robles AI, Hanigan CL, et al. Apoptotic signaling pathways induced by nitric oxide in human lymphoblastoid cells expressing wildtype or mutant p53. Cancer Res. 2004;64:3022-3029.
86. Imanishi T, Han DK, Hofstra L, et al. Apoptosis of vascular smooth muscle cells is induced by Fas ligand derived from monocytes/ macrophage. Atherosclerosis. 2002;161:143-151. (Pubitemid 34214830)
87. Seshiah PN, Kereiakes DJ, Vasudevan SS, et al. Activated monocytes induce smooth muscle cell death: role of macrophage colony-stimulating factor and cell contact. Circulation. 2002;105:174-180.
88. Vasudevan SS, Lopes NH, Seshiah PN, et al. Mac-1 and Fas activities are concurrently required for execution of smooth muscle cell death by M-CSF-stimulated macrophages. Cardiovasc Res. 2003;59:723-733.
89. Boyle JJ, Weissberg PL, Bennett MR. Human macrophage-induced vascular smooth muscle cell apoptosis requires NO enhancement of Fas/ Fas-L interactions. Arterioscler Thromb Vasc Biol. 2002;22:1624-1630.
90. Chan WL, Pejnovic N, Hamilton H, et al. Atherosclerotic abdominal aortic aneurysm and the interaction between autologous human plaquederived vascular smooth muscle cells, type 1 NKT, and helper T cells. Circ Res. 2005;96:675-683. (Pubitemid 40478335)
91. Murray AG, Libby P, Pober JS. Human vascular smooth muscle cells poorly co-stimulate and actively inhibit allogeneic CD4+ T cell proliferation in vitro. J Immunol. 1995;154:151-161.
92. Liuzzo G, Goronzy JJ, Yang H, et al. Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes. Circulation. 2000;101: 2883-2888. (Pubitemid 30415876)
93. Nakajima T, Schulte S, Warrington KJ, et al. T-cell-mediated lysis of endothelial cells in acute coronary syndromes. Circulation. 2002;105: 570-575. (Pubitemid 34123430)
94. Pryshchep S, Sato K, Goronzy JJ, et al. T cell recognition and killing of vascular smooth muscle cells in acute coronary syndrome. Circ Res. 2006;98:1168-1176. (Pubitemid 43948103)
95. Sato K, Niessner A, Kopecky SL, et al. TRAIL-expressing T cells induce apoptosis of vascular smooth muscle cells in the atherosclerotic plaque. J Exp Med. 2006;203:239-250. (Pubitemid 43139661)
96. Meier P, Spertini F, Blanc E, et al. Oxidized low-density lipoproteins activate CD4+ T cell apoptosis in patients with end-stage renal disease through Fas engagement. J Am Soc Nephrol. 2007;18:331-342. (Pubitemid 46053445)
97. Tanemura M, Saga A, Kawamoto K, et al. In vitro and in vivo prevention of human CD8+ CTL-mediated xenocytotoxicity by pig c-FLIP expression in porcine endothelial cells. Am J Transplant. 2008;8: 288-297.
98. Martin S, Tesse A, Hugel B, et al. Shed membrane particles from T lymphocytes impair endothelial function and regulate endothelial protein expression. Circulation. 2004;109:1653-1659. (Pubitemid 38451723)
99. Tesse A, Martinez MC, Hugel B, et al. Upregulation of proinflammatory proteins through NF-kappaB pathway by shed membrane microparticles results in vascular hyporeactivity. Arterioscler Thromb Vasc Biol. 2005; 25:2522-2527. (Pubitemid 43732273)
100. Ruemmele FM, Beaulieu JF, O'Connell J, et al. The susceptibility to Fasinduced apoptosis in normal enterocytes is regulated on the level of cIAP1 and 2. Biochem Biophys Res Commun. 2002;290:1308-1314. (Pubitemid 34694448)
101. Qin Y, Auh S, Blokh L, et al. TNF-alpha induces transient resistance to Fas-induced apoptosis in eosinophilic acute myeloid leukemia cells. Cell Mol Immunol. 2007;4:43-52.
102. Daniel S, Arvelo MB, Patel VI, et al. A20 protects endothelial cells from TNF-, Fas-, and NK-mediated cell death by inhibiting caspase 8 activation. Blood. 2004;104:2376-2384.
103. Patel VI, Daniel S, Longo CR, et al. A20, a modulator of smooth muscle cell proliferation and apoptosis, prevents and induces regression of neointimal hyperplasia. FASEB J. 2006;20:1418-1430.
104. Gagarin D, Yang Z, Butler J, et al. Genomic profiling of acquired resistance to apoptosis in cells derived from human atherosclerotic lesions: potential role of STATs, cyclinD1, BAD, and Bcl-XL. J Mol Cell Cardiol. 2005;39:453-465. (Pubitemid 41133731)
105. Yang Z, Gagarin D, Ramezani A, et al. Resistance to Fas-induced apoptosis in cells from human atherosclerotic lesions: elevated Bcl-XL inhibits apoptosis and caspase activation. J Vasc Res. 2007;44:483-494. (Pubitemid 350022322)
106. Stegh AH, Barnhart BC, Volkland J, et al. Inactivation of caspase-8 on mitochondria of Bcl-xL-expressing MCF7-Fas cells: role for the bifunctional apoptosis regulator protein. J Biol Chem. 2002;277:4351-4360. (Pubitemid 34968701)
107. Pollman MJ, Hall JL, Mann MJ, et al. Inhibition of neointimal cell bcl-x expression induces apoptosis and regression of vascular disease. Nat Med. 1998;4:222-227.
108. Dimmeler S, Rippmann V, Weiland U, et al. Angiotensin II induces apoptosis of human endothelial cells. Protective effect of nitric oxide. Circ Res. 1997;81:970-976.
109. Schmidt-Ott KM, Kagiyama S, Phillips MI. The multiple actions of angiotensin II in atherosclerosis. Regul Pept. 2000;93:65-77.
110. Li Y, Song YH, Mohler J, et al. ANG II induces apoptosis of human vascular smooth muscle via extrinsic pathway involving inhibition of Akt phosphorylation and increased FasL expression. Am J Physiol Heart Circ Physiol. 2006;290:H2116-H2123.
111. Upchurch GR Jr, Loscalzo J, Banes AJ. Changes in the amplitude of cyclic load biphasically modulate endothelial cell DNA synthesis and division. Vasc Med. 1997;2:19-24. (Pubitemid 27298538)
112. Kaiser D, Freyberg MA, Friedl P. Lack of hemodynamic forces triggers apoptosis in vascular endothelial cells. Biochem Biophys Res Commun. 1997;231:586-590. (Pubitemid 27217558)
113. Intengan HD, Schiffrin EL. Vascular remodeling in hypertension: roles of apoptosis, inflammation, and fibrosis. Hypertension. 2001;38(Pt 2): 581-587.
114. Hasel C, Durr S, Bauer A, et al. Pathologically elevated cyclic hydrostatic pressure induces CD95-mediated apoptotic cell death in vascular endothelial cells. Am J Physiol Cell Physiol. 2005;289:C312-C322. (Pubitemid 41008878)
115. Janin A, Deschaumes C, Daneshpouy M, et al. CD95 engagement induces disseminated endothelial cell apoptosis in vivo: immunopathologic implications. Blood. 2002;99:2940-2947. (Pubitemid 34525384)
116. Freyberg MA, Kaiser D, Graf R, et al. Vascular endothelial cells express a functional Fas-receptor due to lack of hemodynamic forces. Apoptosis. 2001;6:339-343. (Pubitemid 32910874)
117. Apenberg S, Freyberg MA, Friedl P. Shear stress induces apoptosis in vascular smooth muscle cells via an autocrine Fas/FasL pathway. Biochem Biophys Res Commun. 2003;310:355-359. (Pubitemid 37163671)
118. Imanishi T, Hano T, Nishio I, et al. Apoptosis of vascular smooth muscle cells is induced by Fas ligand derived from endothelial cells. Jpn Circ J. 2001;65:556-560. (Pubitemid 32531551)
119. Vouyouka AG, Jiang Y, Basson MD. Pressure alters endothelial effects upon vascular smooth muscle cells by decreasing smooth muscle cell proliferation and increasing smooth muscle cell apoptosis. Surgery. 2004;136:282-290. (Pubitemid 39037666)
120. Azuma H, Hamasaki H, Sato J, et al. Different localization of ETA and ETB receptors in the hyperplastic vascular wall. J Cardiovasc Pharmacol. 1995;25:802-809.
121. Uckan D, Steele A, Wang BY, et al. Trophoblasts express Fas ligand: a proposed mechanism for immune privilege in placenta and maternal invasion. Mol Hum Reprod. 1997;3:655-662. (Pubitemid 127509722)
122. Mor G, Gutierrez LS, Eliza M, et al. Fas-fas ligand system-induced apoptosis in human placenta and gestational trophoblastic disease. Am J Reprod Immunol. 1998;40:89-94. (Pubitemid 28380063)
123. Abrahams VM, Straszewski-Chavez SL, Guller S, et al. First trimester trophoblast cells secrete Fas ligand which induces immune cell apoptosis. Mol Hum Reprod. 2004;10:55-63. (Pubitemid 38195966)