Arteriosclerosis, Thrombosis, and Vascular Biology. 1996;16:19-27
© 1996 American Heart Association, Inc.
Articles |
Apoptosis of Vascular Smooth Muscle Cells Induced by In Vitro Stimulation With Interferon-
, Tumor Necrosis Factor–
, and Interleukin-1ß
From the Vascular Medicine and Atherosclerosis Unit, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Mass, and the King Gustaf V Research Institute (G.K.H.), Karolinska Institute, Karolinska Hospital, Stockholm, Sweden.
Correspondence to Dr Peter Libby, Vascular Medicine and Atherosclerosis Unit, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, 221 Longwood Ave, Boston, MA 02115.
Abstract Recent studies have documented evidence for the
death of smooth muscle cells (SMCs) within advanced human
atheroma. These lesions contain macrophages and T
lymphocytes in addition to SMCs. We therefore investigated whether
interferon-
(IFN-), a cytokine secreted by T lymphocytes,
or interleukin-1ß (IL-1ß) and tumor necrosis factor–
(TNF-),
two cytokines characteristically produced by activated
macrophages, can trigger apoptosis of vascular SMCs.
Simultaneous treatment with IFN- and TNF- and/or
IL-1ß but not with each cytokine alone promoted death of
human and rat SMCs. Exposure for 48 hours to a combination of IFN-
(400 U/mL), TNF- (400 U/mL), and IL-1ß (100 U/mL) significantly
(P<.001) increased the accumulation of oligonucleosomes
comprising DNA fragments and histones in human SMCs. Electrophoresis of
genomic DNA showed internucleosomal fragments of genomic DNA isolated
from the cytokine-cotreated SMCs of both humans and rats.
These cells exhibited morphological changes typical of
apoptosis, including cell shrinkage, membrane blebbing,
chromatin condensation, and nuclear fragmentation. In situ 3' end
labeling of DNA fragments with terminal transferase confirmed the
fragmentation of genomic DNA in these cells. Simultaneous
treatment with IFN- and TNF- or IL-1ß induced elaboration of
nitrite, an end product of nitric oxide, in rat but not human SMCs.
NG-monomethyl-L-arginine
inhibited nitrite accumulation and also partly blocked
cytokine-induced apoptosis of rat SMCs but had
little effect on human SMCs, suggesting operation of both nitric
oxide–dependent and –independent mechanisms for
cytokine-induced apoptosis in vascular SMCs.
Production of immune cytokines by vascular cells and/or
infiltrating leukocytes may regulate apoptotic death of SMCs
during atherogenesis.
Key Words: smooth muscle cells • cell death • nitric oxide • cytokines • atherosclerosis
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 T. Imanishi, J. McBride, Q. Ho, K. D. O達rien, S. M. Schwartz, and D. K. M. Han Expression of Cellular FLICE-Inhibitory Protein in Human Coronary Arteries and in a Rat Vascular Injury Model Am. J. Pathol., January 1, 2000; 156(1): 125 - 137. [Abstract] [Full Text] [PDF]
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J. Niebauer, S. P. Schwarzacher, M. Hayase, B. Wang, R. S. Kernoff, J. P. Cooke, and A. C. Yeung Local L-Arginine Delivery After Balloon Angioplasty Reduces Monocyte Binding and Induces Apoptosis Circulation, October 26, 1999; 100(17): 1830 - 1835. [Abstract] [Full Text] [PDF]
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J. Heckenkamp, D. Leszczynski, J. Schiereck, J. Kung, and G. M. LaMuraglia Different Effects of Photodynamic Therapy and {gamma}-Irradiation on Vascular Smooth Muscle Cells and Matrix : Implications for Inhibiting Restenosis Arterioscler Thromb Vasc Biol, September 1, 1999; 19(9): 2154 - 2161. [Abstract] [Full Text] [PDF]
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J. Ruef, A. S. Meshel, Z. Hu, C. Horaist, C. A. Ballinger, L. J. Thompson, V. D. Subbarao, J. A. Dumont, and C. Patterson Flavopiridol Inhibits Smooth Muscle Cell Proliferation In Vitro and Neointimal Formation In Vivo After Carotid Injury in the Rat Circulation, August 10, 1999; 100(6): 659 - 665. [Abstract] [Full Text] [PDF]
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L. J. Walton, I. J. Franklin, T. Bayston, L. C. Brown, R. M. Greenhalgh, G. W. Taylor, and J. T. Powell Inhibition of Prostaglandin E2 Synthesis in Abdominal Aortic Aneurysms : Implications for Smooth Muscle Cell Viability, Inflammatory Processes, and the Expansion of Abdominal Aortic Aneurysms Circulation, July 6, 1999; 100(1): 48 - 54. [Abstract] [Full Text] [PDF]
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J. Alcouffe, S. Caspar-Bauguil, V. Garcia, R. Salvayre, M. Thomsen, and H. Benoist Oxidized low density lipoproteins induce apoptosis in PHA-activated peripheral blood mononuclear cells and in the Jurkat T-cell line J. Lipid Res., July 1, 1999; 40(7): 1200 - 1210. [Abstract] [Full Text]
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G. K. Sukhova, U. Schonbeck, E. Rabkin, F. J. Schoen, A. R. Poole, R. C. Billinghurst, and P. Libby Evidence for Increased Collagenolysis by Interstitial Collagenases-1 and -3 in Vulnerable Human Atheromatous Plaques Circulation, May 18, 1999; 99(19): 2503 - 2509. [Abstract] [Full Text] [PDF]
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C. H. Selzman, B. D. Shames, L. L. Reznikov, S. A. Miller, X. Meng, H. A. Barton, A. Werman, A. H. Harken, C. A. Dinarello, and A. Banerjee Liposomal Delivery of Purified Inhibitory-{kappa}B{alpha} Inhibits Tumor Necrosis Factor-{alpha}蜂nduced Human Vascular Smooth Muscle Proliferation Circ. Res., April 30, 1999; 84(8): 867 - 875. [Abstract] [Full Text] [PDF]
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D. Bonderman, E. Gharehbaghi-Schnell, G. Wollenek, G. Maurer, H. Baumgartner, and I. M. Lang Mechanisms Underlying Aortic Dilatation in Congenital Aortic Valve Malformation Circulation, April 27, 1999; 99(16): 2138 - 2143. [Abstract] [Full Text] [PDF]
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J. Shindo, T. Ishibashi, K. Yokoyama, K. Nakazato, T. Ohwada, M. Shiomi, and Y. Maruyama Granulocyte-Macrophage Colony亡timulating Factor Prevents the Progression of Atherosclerosis via Changes in the Cellular and Extracellular Composition of Atherosclerotic Lesions in Watanabe Heritable Hyperlipidemic Rabbits Circulation, April 27, 1999; 99(16): 2150 - 2156. [Abstract] [Full Text] [PDF]
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W. Erl, G. K. Hansson, R. de Martin, G. Draude, K. S. C. Weber, and C. Weber Nuclear Factor-{kappa}B Regulates Induction of Apoptosis and Inhibitor of Apoptosis Protein-1 Expression in Vascular Smooth Muscle Cells Circ. Res., April 2, 1999; 84(6): 668 - 677. [Abstract] [Full Text] [PDF]
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B.-Y. Wang, H.-K. V. Ho, P. S. Lin, S. P. Schwarzacher, M. J. Pollman, G. H. Gibbons, P. S. Tsao, and J. P. Cooke Regression of Atherosclerosis : Role of Nitric Oxide and Apoptosis Circulation, March 9, 1999; 99(9): 1236 - 1241. [Abstract] [Full Text] [PDF]
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Z. Mallat, C. Heymes, J. Ohan, E. Faggin, G. Leseche, and A. Tedgui Expression of Interleukin-10 in Advanced Human Atherosclerotic Plaques : Relation to Inducible Nitric Oxide Synthase Expression and Cell Death Arterioscler Thromb Vasc Biol, March 1, 1999; 19(3): 611 - 616. [Abstract] [Full Text] [PDF]
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D. E. Gutstein and V. Fuster Pathophysiology and clinical significance of atherosclerotic plaque rupture Cardiovasc Res, February 1, 1999; 41(2): 323 - 333. [Abstract] [Full Text] [PDF]
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M. R Bennett Apoptosis of vascular smooth muscle cells in vascular remodelling and atherosclerotic plaque rupture Cardiovasc Res, February 1, 1999; 41(2): 361 - 368. [Abstract] [Full Text] [PDF]
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L. H Arroyo and R. T Lee Mechanisms of plaque rupture: mechanical and biologic interactions Cardiovasc Res, February 1, 1999; 41(2): 369 - 375. [Abstract] [Full Text] [PDF]
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R. Rabbani and E. J. Topol Strategies to achieve coronary arterial plaque stabilization Cardiovasc Res, February 1, 1999; 41(2): 402 - 417. [Abstract] [Full Text] [PDF]
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G. Bauriedel, R. Hutter, U. Welsch, R. Bach, H. Sievert, and B. Luderitz Role of smooth muscle cell death in advanced coronary primary lesions: implications for plaque instability Cardiovasc Res, February 1, 1999; 41(2): 480 - 488. [Abstract] [Full Text] [PDF]
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Z. Mallat, B. Hugel, J. Ohan, G. Leseche, J.-M. Freyssinet, and A. Tedgui Shed Membrane Microparticles With Procoagulant Potential in Human Atherosclerotic Plaques : A Role for Apoptosis in Plaque Thrombogenicity Circulation, January 26, 1999; 99(3): 348 - 353. [Abstract] [Full Text] [PDF]
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Y.-J. Geng, Y. Ishikawa, D. E. Vatner, T. E. Wagner, S. P. Bishop, S. F. Vatner, and C. J. Homcy Apoptosis of Cardiac Myocytes in Gs{alpha} Transgenic Mice Circ. Res., January 22, 1999; 84(1): 34 - 42. [Abstract] [Full Text] [PDF]
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 T. K. Tarrant, P. B. Silver, J. L. Wahlsten, L. V. Rizzo, C.-C. Chan, B. Wiggert, and R. R. Caspi Interleukin 12 Protects from a T Helper Type 1-mediated Autoimmune Disease, Experimental Autoimmune Uveitis, through a Mechanism Involving Interferon {gamma}, Nitric Oxide, and Apoptosis J. Exp. Med., January 18, 1999; 189(2): 219 - 230. [Abstract] [Full Text] [PDF]
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E. L. Henderson, Y.-J. Geng, G. K. Sukhova, A. D. Whittemore, J. Knox, and P. Libby Death of Smooth Muscle Cells and Expression of Mediators of Apoptosis by T Lymphocytes in Human Abdominal Aortic Aneurysms Circulation, January 12, 1999; 99(1): 96 - 104. [Abstract] [Full Text] [PDF]
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A. Raisanen-Sokolowski, T. Glysing-Jensen, and M. E. Russell Leukocyte-Suppressing Influences of Interleukin (IL)-10 in Cardiac Allografts : Insights from IL-10 Knockout Mice Am. J. Pathol., November 1, 1998; 153(5): 1491 - 1500. [Abstract] [Full Text] [PDF]
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P. Libby The interface of atherosclerosis and thrombosis: basic mechanisms Vascular Medicine, August 1, 1998; 3(3): 225 - 229. [Abstract] [PDF]
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V. Poppa, J. K. Miyashiro, M. A. Corson, and B. C. Berk Endothelial NO Synthase Is Increased in Regenerating Endothelium After Denuding Injury of the Rat Aorta Arterioscler Thromb Vasc Biol, August 1, 1998; 18(8): 1312 - 1321. [Abstract] [Full Text] [PDF]
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 J. K. Liao Endothelium and acute coronary syndromes Clin. Chem., August 1, 1998; 44(8): 1799 - 1808. [Abstract] [Full Text] [PDF]
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G. Bauriedel, S. Schluckebier, R. Hutter, U. Welsch, R. Kandolf, B. Luderitz, and M. F. Prescott Apoptosis in Restenosis Versus Stable-Angina Atherosclerosis : Implications for the Pathogenesis of Restenosis Arterioscler Thromb Vasc Biol, July 1, 1998; 18(7): 1132 - 1139. [Abstract] [Full Text] [PDF]
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M. D. Rekhter, R. D. Simari, C. W. Work, G. J. Nabel, E. G. Nabel, and D. Gordon Gene Transfer Into Normal and Atherosclerotic Human Blood Vessels Circ. Res., June 29, 1998; 82(12): 1243 - 1252. [Abstract] [Full Text] [PDF]
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