Vascular cell apoptosis in remodeling, restenosis, and plaque rupture.

This Review is part of a thematic series on Apoptosis in the Cardiovascular System , which includes the following articles: Apoptosis and Heart Failure: A Critical Review of the Literature Vascular Cell Apoptosis in Remodeling, Restenosis, and Plaque Rupture Apoptosis During Cardiovascular Development Myocyte Apoptosis in Ischemic Heart Disease Endothelial Cell Apoptosis in Angiogenesis and Vessel Regression Richard Kitsis, Guest Editor Apoptotic death of vascular cells is a prominent feature of blood vessel remodeling that occurs during normal development and fibroproliferative disorders of the vessel wall. This review summarizes a large number of studies that have provided evidence for apoptotic cell death in the vasculature. We also describe reports that shed light on the molecular mechanisms that may control this process. Finally, we highlight the relatively small number of studies that suggest a function for vascular cell apoptosis in controlling the morphology and cellular composition of the blood vessel wall. A number of studies have demonstrated apoptotic death of vascular cells in vessels that remodel postnatally. Regionalized apoptosis has been found in vascular smooth muscle cells (VSMCs) during the regression and closure of the human ductus arteriosus before birth1 and in VSMCs and endothelial cells of the arteries and veins of the umbilical cord, which are subject to dramatic hemodynamic changes at birth.2 Evidence of VSMC apoptosis in the human neonate has also been found at the branch points of the great arteries arising from the aortic arch when they are exposed to a disturbed blood flow, whereas VSMC apoptosis was not observed in the aorta when a normal flow pattern is maintained.2 Finally, VSMC apoptosis has been observed during the remodeling of the abdominal aorta in lambs, resulting from the large decrease in blood flow that occurs after the loss of the placenta at birth.3 …

[1]  N. Jenkins,et al.  Generalized lymphoproliferative disease in mice, caused by a point mutation in the fas ligand , 1994, Cell.

[2]  G. Evan,et al.  Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. , 1995, The Journal of clinical investigation.

[3]  Young‐Bae Park,et al.  Apoptosis and regulation of Bax and Bcl-X proteins during human neonatal vascular remodeling. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[4]  R. Kinscherf,et al.  Apoptosis after stent implantation compared with balloon angioplasty in rabbits. Role of macrophages. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[5]  P. Doevendans,et al.  Atherosclerosis in APOE*3-Leiden transgenic mice: from proliferative to atheromatous stage. , 1999, Circulation.

[6]  G. Gibbons,et al.  Determinants of vascular smooth muscle cell apoptosis after balloon angioplasty injury. Influence of redox state and cell phenotype. , 1999, Circulation research.

[7]  P. M. Davis,et al.  Differential Induction of Apoptosis by Fas–Fas Ligand Interactions in Human Monocytes and Macrophages , 1997, The Journal of experimental medicine.

[8]  B. L. Langille,et al.  Atrophic remodeling of the artery-cuffed artery. , 1999, Arteriosclerosis, thrombosis, and vascular biology.

[9]  H. Perlman,et al.  Flice-Inhibitory Protein Expression during Macrophage Differentiation Confers Resistance to FAS-Mediated Apoptosis , 1999, The Journal of experimental medicine.

[10]  J. Isner,et al.  Apoptosis in human atherosclerosis and restenosis. , 1995, Circulation.

[11]  M. Bennett,et al.  Cooperative interactions between RB and p53 regulate cell proliferation, cell senescence, and apoptosis in human vascular smooth muscle cells from atherosclerotic plaques. , 1998, Circulation research.

[12]  MacdonaldK ChanSW BoyleJJ WeissbergPL BennettMR Cooperative interactions between RB and p53 regulate cell proliferation, cell senescence, and apoptosis in human vascular smooth muscle cells from atherosclerotic plaques. , 1998 .

[13]  T. Ogihara,et al.  Possible participation of Fas-mediated apoptosis in the mechanism of atherosclerosis. , 1997, Gerontology.

[14]  K. Walsh,et al.  Fas ligand-deficient mice display enhanced leukocyte infiltration and intima hyperplasia in flow-restricted vessels. , 2000, Journal of molecular and cellular cardiology.

[15]  R. Virmani,et al.  Expression of Fas ligand in arteries of hypercholesterolemic rabbits accelerates atherosclerotic lesion formation. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[16]  K. Walsh,et al.  Temporally and spatially coordinated expression of cell cycle regulatory factors after angioplasty. , 1997, Circulation research.

[17]  K. Walsh,et al.  TNFalpha regulation of Fas ligand expression on the vascular endothelium modulates leukocyte extravasation. , 1998, Nature medicine.

[18]  K Walsh,et al.  Evidence for the rapid onset of apoptosis in medial smooth muscle cells after balloon injury. , 1997, Circulation.

[19]  S. Nagata,et al.  The Fas death factor , 1995, Science.

[20]  J P Luzio,et al.  Cell surface trafficking of Fas: a rapid mechanism of p53-mediated apoptosis. , 1998, Science.

[21]  M. Lee,et al.  Effect of hypercholesterolemia on the sequential changes of apoptosis and proliferation after balloon injury to rabbit iliac artery. , 2000, Atherosclerosis.

[22]  J. Gunn,et al.  Apoptosis and cell proliferation after porcine coronary angioplasty. , 1998, Circulation.

[23]  Margot Thome,et al.  Inhibition of death receptor signals by cellular FLIP , 1997, Nature.

[24]  P. M. Davis,et al.  Human monocytic cells contain high levels of intracellular Fas ligand: rapid release following cellular activation. , 1997, Journal of immunology.

[25]  K. Walsh,et al.  Oxidized LDL activates fas-mediated endothelial cell apoptosis. , 1998, The Journal of clinical investigation.

[26]  J. Isner,et al.  Histopathology of in-stent restenosis in patients with peripheral artery disease. , 1997, Circulation.

[27]  W. Jacob,et al.  Apoptosis and related proteins in different stages of human atherosclerotic plaques. , 1998, Circulation.

[28]  John Calvin Reed,et al.  Identification of a p53-dependent negative response element in the bcl-2 gene. , 1994, Cancer research.

[29]  D. Green,et al.  Fas Ligand-Induced Apoptosis as a Mechanism of Immune Privilege , 1995, Science.

[30]  M. Hecker,et al.  Elevated perfusion pressure upregulates endothelin-1 and endothelin B receptor expression in the rabbit carotid artery. , 2000, Hypertension.

[31]  S. Mori,et al.  Role of macrophages in the development of arteritis in MRL strains of mice with a deficit in Fas‐mediated apoptosis , 1996, Clinical and experimental immunology.

[32]  A. Cho,et al.  Effects of changes in blood flow rate on cell death and cell proliferation in carotid arteries of immature rabbits. , 1997, Circulation research.

[33]  H. Perlman,et al.  Adenovirus-encoded hammerhead ribozyme to Bcl-2 inhibits neointimal hyperplasia and induces vascular smooth muscle cell apoptosis. , 2000, Cardiovascular research.

[34]  P. Libby,et al.  Evidence for apoptosis in advanced human atheroma. Colocalization with interleukin-1 beta-converting enzyme. , 1995, The American journal of pathology.

[35]  J. Trent,et al.  WAF1, a potential mediator of p53 tumor suppression , 1993, Cell.

[36]  Y. Yazaki,et al.  Apoptotic cell death in atherosclerotic plaques of hyperlipidemic knockout mice. , 1997, Atherosclerosis.

[37]  T. Libermann,et al.  Fas ligand gene transfer to the vessel wall inhibits neointima formation and overrides the adenovirus-mediated T cell response. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[38]  S. Nagata,et al.  Downregulation of Fas ligand by shedding , 1998, Nature Medicine.

[39]  J. Bultinck,et al.  Distribution of cell replication and apoptosis in atherosclerotic plaques of cholesterol-fed rabbits. , 1996, Atherosclerosis.

[40]  Y. Kaneda,et al.  Transfer of wild-type p53 gene effectively inhibits vascular smooth muscle cell proliferation in vitro and in vivo. , 1998, Circulation research.

[41]  Jennifer L Hall,et al.  Inhibition of neointimal cell bcl-x expression induces apoptosis and regression of vascular disease , 1998, Nature Medicine.

[42]  G. Fraedrich,et al.  Co‐expression of p53 and MDM2 in human atherosclerosis: implications for the regulation of cellularity of atherosclerotic lesions , 1998, The Journal of pathology.

[43]  B. Björkerud,et al.  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. , 1996, The American journal of pathology.

[44]  B. McManus,et al.  Human transplant coronary artery disease: pathological evidence for Fas-mediated apoptotic cytotoxicity in allograft arteriopathy. , 1996, Laboratory investigation; a journal of technical methods and pathology.

[45]  W. Schaper,et al.  The role of Fas/APO 1 and apoptosis in the development of human atherosclerotic lesions. , 1997, Atherosclerosis.

[46]  P. Jones,et al.  Regulation of Tenascin-C, a Vascular Smooth Muscle Cell Survival Factor that Interacts with the αvβ3 Integrin to Promote Epidermal Growth Factor Receptor Phosphorylation and Growth , 1997, The Journal of cell biology.

[47]  B L Langille,et al.  Apoptosis (programmed cell death) in arteries of the neonatal lamb. , 1995, Circulation research.

[48]  H. Perlman,et al.  Early cell loss after angioplasty results in a disproportionate decrease in percutaneous gene transfer to the vessel wall. , 1999, Human gene therapy.

[49]  N. Copeland,et al.  Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis , 1992, Nature.

[50]  John Calvin Reed,et al.  Tumor suppressor p53 is a direct transcriptional activator of the human bax gene , 1995, Cell.

[51]  M. Reidy,et al.  Kinetics of cellular proliferation after arterial injury. I. Smooth muscle growth in the absence of endothelium. , 1983, Laboratory investigation; a journal of technical methods and pathology.

[52]  J. Thyberg,et al.  Cell death in human atherosclerotic plaques involves both oncosis and apoptosis. , 1997, Atherosclerosis.

[53]  S. Nagata,et al.  Caspase 1-independent IL-1β release and inflammation induced by the apoptosis inducer Fas ligand , 1998, Nature Medicine.

[54]  A. Tedgui,et al.  Colocalization of CPP-32 with apoptotic cells in human atherosclerotic plaques. , 1997, Circulation.

[55]  G. Trautwein,et al.  Sequential study of vasculitis in MRL mice , 1987, Laboratory animals.

[56]  P. Libby,et al.  Fas is expressed in human atherosclerotic intima and promotes apoptosis of cytokine-primed human vascular smooth muscle cells. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[57]  D. Bellgrau,et al.  A role for CD95 ligand in preventing graft rejection , 1995, Nature.

[58]  K. Walsh,et al.  Adenovirus-mediated delivery of fas ligand inhibits intimal hyperplasia after balloon injury in immunologically primed animals. , 1999, Circulation.

[59]  A. Desmoulière,et al.  Apoptosis participates in cellularity regulation during rat aortic intimal thickening. , 1995, The American journal of pathology.

[60]  E. I. Antonova,et al.  The absence of p53 accelerates atherosclerosis by increasing cell proliferation in vivo , 1999, Nature Medicine.

[61]  T. Ogihara,et al.  Activated T cells induce up-regulation of Fas antigen in cultured endothelial cells. , 1997, Heart and vessels.

[62]  K. Walsh,et al.  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. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[63]  B. Trask,et al.  MRIT, a novel death-effector domain-containing protein, interacts with caspases and BclXL and initiates cell death. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[64]  A. Baker,et al.  Divergent effects of tissue inhibitor of metalloproteinase-1, -2, or -3 overexpression on rat vascular smooth muscle cell invasion, proliferation, and death in vitro. TIMP-3 promotes apoptosis. , 1998, The Journal of clinical investigation.

[65]  M. Sata,et al.  Endothelial Cell Apoptosis Induced by Oxidized LDL Is Associated with the Down-regulation of the Cellular Caspase Inhibitor FLIP* , 1998, The Journal of Biological Chemistry.

[66]  S. Schwartz,et al.  Expression of cellular FLICE-inhibitory protein in human coronary arteries and in a rat vascular injury model. , 2000, American Journal of Pathology.

[67]  A. G. Gittenberger-de Groot,et al.  Differentiation, dedifferentiation, and apoptosis of smooth muscle cells during the development of the human ductus arteriosus. , 1997, Arteriosclerosis, thrombosis, and vascular biology.

[68]  M. Leon,et al.  Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. , 1995, The American journal of pathology.

[69]  N. Lalwani,et al.  Fas ligation triggers apoptosis in macrophages but not endothelial cells , 1994, European journal of immunology.