© 1996 American Heart Association, Inc.
Articles |
Vasoactive Substances Regulate Vascular Smooth Muscle Cell Apoptosis
Countervailing Influences of Nitric Oxide and Angiotensin II
the Falk Cardiovascular Research Center, Stanford (Calif) University.
Correspondence to Gary H. Gibbons, MD, Falk CVRC, Division of Cardiovascular Medicine, Stanford University, Stanford, CA 94305. E-mail mL.ghg@forsythe.stanford.edu.
This study tests the hypothesis that the control of vascular smooth muscle cell (VSMC) apoptosis is regulated by the antagonistic balance between vasoactive substances such as NO and angiotensin II (Ang II). Moreover, it is postulated that the cellular signaling pathways involved in regulating vessel tone are also coupled to the regulation of programmed cell death. Using an in vitro model system, we documented that the addition of NO donor molecules S-nitroso-N-acetylpenicillamine or sodium nitroprusside to VSMC dose-dependently induced apoptosis as documented by DNA laddering and quantified by analysis of cellular chromatin morphology. The mediator role of the guanylate cyclase signaling pathway in NO-induced apoptosis was evidenced by (1) induction of apoptosis by the 8-bromo-cGMP analogue, (2) potentiation of NO-induced apoptosis by cGMP-specific phosphodiesterase inhibition, and (3) the prevention of NO-induced apoptosis by the inhibition of the cGMP-dependent protein kinase I
. In contrast, Ang II directly antagonized NO donor– and cGMP analogue–induced apoptosis via activation of the type I Ang II receptor. These findings suggest that the countervailing balance between NO and Ang II may determine the overall cell population within the vessel wall by regulating genetic programs determining cell death as well as cell growth.
Key Words: programmed cell death • vascular remodeling • vasoactive substances • cGMP • guanylate cyclase
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M. J. Pollman, L. Naumovski, and G. H. Gibbons Vascular Cell Apoptosis : Cell Type–Specific Modulation by Transforming Growth Factor-ß1 in Endothelial Cells Versus Smooth Muscle Cells Circulation, April 20, 1999; 99(15): 2019 - 2026. [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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D. Li, B. Yang, M. I. Philips, and J. L. Mehta Proapoptotic effects of ANG II in human coronary artery endothelial cells: role of AT1 receptor and PKC activation Am J Physiol Heart Circ Physiol, March 1, 1999; 276(3): H786 - H792. [Abstract] [Full Text] [PDF]
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M.-J. Champagne, P. Dumas, S. N. Orlov, M. R. Bennett, P. Hamet, and J. Tremblay Protection Against Necrosis but Not Apoptosis by Heat-Stress Proteins in Vascular Smooth Muscle Cells : Evidence for Distinct Modes of Cell Death Hypertension, March 1, 1999; 33(3): 906 - 913. [Abstract] [Full Text] [PDF]
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M. Horiuchi, M. Akishita, and V. J. Dzau Recent Progress in Angiotensin II Type 2 Receptor Research in the Cardiovascular System Hypertension, February 1, 1999; 33(2): 613 - 621. [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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D. J. Ing, J. Zang, V. J. Dzau, K. A. Webster, and N. H. Bishopric Modulation of Cytokine-Induced Cardiac Myocyte Apoptosis by Nitric Oxide, Bak, and Bcl-x Circ. Res., January 22, 1999; 84(1): 21 - 33. [Abstract] [Full Text] [PDF]
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M. J. Pollman, J. L. Hall, and G. H. Gibbons Determinants of Vascular Smooth Muscle Cell Apoptosis After Balloon Angioplasty Injury : Influence of Redox State and Cell Phenotype Circ. Res., January 22, 1999; 84(1): 113 - 121. [Abstract] [Full Text] [PDF]
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 S. K. Sharma, D. Chapman, R. Temsah, T. Netticadan, D. P. Brasil, and N. S. Dhalla Prevention of Vascular Apoptosis in Myocardial Infarction by Losartan Journal of Cardiovascular Pharmacology and Therapeutics, January 1, 1999; 4(2): 77 - 84. [Abstract] [PDF]
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P. J. M. Best, D. Hasdai, G. Sangiorgi, R. S. Schwartz, D. R. Holmes Jr, R. D. Simari, and A. Lerman Apoptosis : Basic Concepts and Implications in Coronary Artery Disease Arterioscler Thromb Vasc Biol, January 1, 1999; 19(1): 14 - 22. [Abstract] [Full Text] [PDF]
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N. Suenobu, M. Shichiri, M. Iwashina, F. Marumo, and Y. Hirata Natriuretic Peptides and Nitric Oxide Induce Endothelial Apoptosis via a cGMP–Dependent Mechanism Arterioscler Thromb Vasc Biol, January 1, 1999; 19(1): 140 - 146. [Abstract] [Full Text] [PDF]
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M. Horiuchi, H. Yamada, M. Akishita, M. Ito, K. Tamura, and V. J. Dzau Interferon Regulatory Factors Regulate Interleukin-1ß–Converting Enzyme Expression and Apoptosis in Vascular Smooth Muscle Cells Hypertension, January 1, 1999; 33(1): 162 - 166. [Abstract] [Full Text] [PDF]
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D. Li, K. Tomson, B. Yang, P. Mehta, B. P. Croker, and J. L. Mehta Modulation of constitutive nitric oxide synthase, bcl-2 and Fas expression in cultured human coronary endothelial cells exposed to anoxia-reoxygenation and angiotensin II: role of AT1 receptor activation Cardiovasc Res, January 1, 1999; 41(1): 109 - 115. [Abstract] [Full Text] [PDF]
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J.-D. Chiche, S. M. Schlutsmeyer, D. B. Bloch, S. M. de la Monte, J. D. Roberts Jr., G. Filippov, S. P. Janssens, A. Rosenzweig, and K. D. Bloch Adenovirus-mediated Gene Transfer of cGMP-dependent Protein Kinase Increases the Sensitivity of Cultured Vascular Smooth Muscle Cells to the Antiproliferative and Pro-apoptotic Effects of Nitric Oxide/cGMP J. Biol. Chem., December 18, 1998; 273(51): 34263 - 34271. [Abstract] [Full Text] [PDF]
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M. Iwashina, M. Shichiri, F. Marumo, and Y. Hirata Transfection of Inducible Nitric Oxide Synthase Gene Causes Apoptosis in Vascular Smooth Muscle Cells Circulation, September 22, 1998; 98(12): 1212 - 1218. [Abstract] [Full Text] [PDF]
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C. J. McKenna, S. E. Burke, T. J. Opgenorth, R. J. Padley, L. J. Camrud, A. R. Camrud, J. Johnson, P. J. Carlson, A. Lerman, D. R. Holmes Jr, et al. Selective ETA Receptor Antagonism Reduces Neointimal Hyperplasia in a Porcine Coronary Stent Model Circulation, June 30, 1998; 97(25): 2551 - 2556. [Abstract] [Full Text] [PDF]
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U. Schmitz, T. Ishida, M. Ishida, J. Surapisitchat, M. I. Hasham, S. Pelech, and B. C. Berk Angiotensin II Stimulates p21-Activated Kinase in Vascular Smooth Muscle Cells : Role in Activation of JNK Circ. Res., June 29, 1998; 82(12): 1272 - 1278. [Abstract] [Full Text] [PDF]
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L. Chen, G. Daum, R. Forough, M. Clowes, U. Walter, and A. W. Clowes Overexpression of Human Endothelial Nitric Oxide Synthase in Rat Vascular Smooth Muscle Cells and in Balloon-Injured Carotid Artery Circ. Res., May 4, 1998; 82(8): 862 - 870. [Abstract] [Full Text] [PDF]
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 B. Yang, D. Li, M I. Phillips, P. Mehta, and J. L Mehta Myocardial angiotensin II receptor expression and ischemia-reperfusion injury Vascular Medicine, May 1, 1998; 3(2): 121 - 130. [Abstract] [PDF]
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H. Wang and J. A. Keiser Molecular characterization of rabbit CPP32 and its function in vascular smooth muscle cell apoptosis Am J Physiol Heart Circ Physiol, April 1, 1998; 274(4): H1132 - H1140. [Abstract] [Full Text] [PDF]
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 B. L. Tepperman, T. D. Abrahamson, and B. D. Soper The Role of Cyclic Guanylate Monophosphate in Nitric Oxide-Induced Injury to Rat Small Intestinal Epithelial Cells J. Pharmacol. Exp. Ther., March 1, 1998; 284(3): 929 - 933. [Abstract] [Full Text]
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A. M. Devlin, M. J. Brosnan, D. Graham, J. J. Morton, A. R. McPhaden, M. McIntyre, C. A. Hamilton, J. L. Reid, and A. F. Dominiczak Vascular smooth muscle cell polyploidy and cardiomyocyte hypertrophy due to chronic NOS inhibition in vivo Am J Physiol Heart Circ Physiol, January 1, 1998; 274(1): H52 - H59. [Abstract] [Full Text] [PDF]
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H. Matsushita, R. Morishita, I. Kida, M. Aoki, S.-i. Hayashi, N. Tomita, K. Yamamoto, A. Moriguchi, A. Noda, Y. Kaneda, et al. Inhibition of Growth of Human Vascular Smooth Muscle Cells by Overexpression of p21 Gene Through Induction of Apoptosis Hypertension, January 1, 1998; 31(1): 493 - 498. [Abstract] [Full Text] [PDF]
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S. Dimmeler, V. Rippmann, U. Weiland, J. Haendeler, and A. M. Zeiher Angiotensin II Induces Apoptosis of Human Endothelial Cells : Protective Effect of Nitric Oxide Circ. Res., December 19, 1997; 81(6): 970 - 976. [Abstract] [Full Text]
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M. Weis and W. von Scheidt Cardiac Allograft Vasculopathy : A Review Circulation, September 16, 1997; 96(6): 2069 - 2077. [Abstract] [Full Text]
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C.-F. Wu, N. H. Bishopric, and R. E. Pratt Atrial Natriuretic Peptide Induces Apoptosis in Neonatal Rat Cardiac Myocytes J. Biol. Chem., June 6, 1997; 272(23): 14860 - 14866. [Abstract] [Full Text] [PDF]
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