Circulation, Vol 89, 1943-1950, Copyright © 1994 by American Heart Association
RH Karas, BL Patterson and ME Mendelsohn
BACKGROUND: The decreased incidence of coronary artery disease observed in
postmenopausal women given estrogen (E2) replacement demonstrates an
atheroprotective effect of E2 that is generally believed to be mediated by
indirect, E2-induced changes in cardiovascular risk factor profiles. We
hypothesized that the atheroprotective effect of E2 may be in part mediated
by a direct effect of E2 on vascular smooth muscle cells (VSMCs).
Therefore, a series of experiments was performed to determine whether human
VSMCs contain a competent E2 receptor, a ligand-activated transcription
factor known to mediate E2-induced effects in nonvascular cells. METHODS
AND RESULTS: Ribonuclease protection assays, with a probe derived from the
human E2 receptor, were used to demonstrate E2- receptor mRNA in human
saphenous vein VSMCs. To show that VSMCs contain E2-receptor protein as
well as message, immunoblotting and immunofluorescence studies with a
monoclonal anti-E2-receptor antibody were performed, and E2-receptor
protein was detected by both methods. Transient transfection assays using a
specific E2-responsive reporter system were used next to determine whether
the VSMC E2 receptor is capable of E2-induced transcriptional
transactivation. Initial studies using mammary artery-derived VSMCs
resulted in a 2.4-fold increase in reporter activity in response to 10(-7)
mol/L E2. Subsequent studies using saphenous vein VSMCs demonstrated
increasing levels of reporter activation as the concentration of E2 was
increased from 10(-9) mol/L (1.3-fold increase; SEM, 0.07; P = .05, n = 3)
to 10(-7) mol/L (1.6- fold increase; SEM, 0.04; P = .002, n = 6). The
specificity of the E2- induced transactivation of the reporter gene was
shown by dose- dependent inhibition of transactivation by the pure E2
antagonist ICI 164,384 and by enhancement of the transactivation by
simultaneous overexpression of the E2 receptor. CONCLUSIONS: We have
demonstrated for the first time that human VSMCs express E2-receptor mRNA
and protein and that the E2 receptor in VSMCs is capable of estrogen-
dependent gene activation. These data suggest a mechanism by which estrogen
may directly alter VSMC function.
ARTICLES
Human vascular smooth muscle cells contain functional estrogen receptor
Molecular Cardiology Research Center, New England Medical Center, Tufts University School of Medicine, Boston, Mass. 02111.
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M. E. Mendelsohn and R. H. Karas The Protective Effects of Estrogen on the Cardiovascular System N. Engl. J. Med., June 10, 1999; 340(23): 1801 - 1811. [Full Text] [PDF]
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S. Makela, H. Savolainen, E. Aavik, M. Myllarniemi, L. Strauss, E. Taskinen, J.-A. Gustafsson, and P. Hayry Differentiation between vasculoprotective and uterotrophic effects of ligands with different binding affinities to estrogen receptors alpha and beta PNAS, June 8, 1999; 96(12): 7077 - 7082. [Abstract] [Full Text] [PDF]
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Y. K. Hodges, J. K. Richer, K. B. Horwitz, and L. D. Horwitz Variant Estrogen and Progesterone Receptor Messages in Human Vascular Smooth Muscle Circulation, May 25, 1999; 99(20): 2688 - 2693. [Abstract] [Full Text] [PDF]
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V. Zancan, S. Santagati, C. Bolego, E. Vegeto, A. Maggi, and L. Puglisi 17{beta}-Estradiol Decreases Nitric Oxide Synthase II Synthesis in Vascular Smooth Muscle Cells Endocrinology, May 1, 1999; 140(5): 2004 - 2009. [Abstract] [Full Text]
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H. Teoh, S. W.S. Leung, and R. Y.K. Man Short-term exposure to physiological levels of 17{beta}-estradiol enhances endothelium-independent relaxation in porcine coronary artery Cardiovasc Res, April 1, 1999; 42(1): 224 - 231. [Abstract] [Full Text] [PDF]
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I. C. D. Westendorp, M. L. Bots, D. E. Grobbee, R. S. Reneman, A. P. G. Hoeks, N. M. Van Popele, A. Hofman, and J. C. M. Witteman Menopausal Status and Distensibility of the Common Carotid Artery Arterioscler Thromb Vasc Biol, March 1, 1999; 19(3): 713 - 717. [Abstract] [Full Text] [PDF]
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H. Lou, M. B. Martin, A. Stoica, P. W. Ramwell, and M. L. Foegh Upregulation of Estrogen Receptor-{alpha} Expression in Rabbit Cardiac Allograft Circ. Res., November 2, 1998; 83(9): 947 - 951. [Abstract] [Full Text] [PDF]
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 R. D. Minshall, K. Miyagawa, C. C. Chadwick, M. J. Novy, and K. Hermsmeyer In vitro modulation of primate coronary vascular muscle cell reactivity by ovarian steroid hormones FASEB J, October 1, 1998; 12(13): 1419 - 1429. [Abstract] [Full Text]
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M. Christ and M. Wehling Cardiovascular steroid actions: swift swallows or sluggish snails? Cardiovasc Res, October 1, 1998; 40(1): 34 - 44. [Abstract] [Full Text] [PDF]
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S. Kim-Schulze, W. L. Lowe Jr, and H. W. Schnaper Estrogen Stimulates Delayed Mitogen-Activated Protein Kinase Activity in Human Endothelial Cells via an Autocrine Loop That Involves Basic Fibroblast Growth Factor Circulation, August 4, 1998; 98(5): 413 - 421. [Abstract] [Full Text] [PDF]
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V. Lindner, S. K. Kim, R. H. Karas, G. G. J. M. Kuiper, J.-A. Gustafsson, and M. E. Mendelsohn Increased Expression of Estrogen Receptor-ß mRNA in Male Blood Vessels After Vascular Injury Circ. Res., July 27, 1998; 83(2): 224 - 229. [Abstract] [Full Text] [PDF]
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G. Nickenig, A. T. Baumer, C. Grohe, S. Kahlert, K. Strehlow, S. Rosenkranz, A. Stablein, F. Beckers, J. F. M. Smits, M. J. A. P. Daemen, et al. Estrogen Modulates AT1 Receptor Gene Expression In Vitro and In Vivo Circulation, June 9, 1998; 97(22): 2197 - 2201. [Abstract] [Full Text] [PDF]
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D. A. Edouard, B. M. Pannier, G. M. London, J. L. Cuche, and M. E. Safar Venous and arterial behavior during normal pregnancy Am J Physiol Heart Circ Physiol, May 1, 1998; 274(5): H1605 - H1612. [Abstract] [Full Text] [PDF]
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J. Binko and H. Majewski 17beta -Estradiol reduces vasoconstriction in endothelium-denuded rat aortas through inducible NOS Am J Physiol Heart Circ Physiol, March 1, 1998; 274(3): H853 - H859. [Abstract] [Full Text] [PDF]
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R. D. Minshall, F. Z. Stanczyk, K. Miyagawa, B. Uchida, M. Axthelm, M. Novy, and K. Hermsmeyer Ovarian Steroid Protection against Coronary Artery Hyperreactivity in Rhesus Monkeys J. Clin. Endocrinol. Metab., February 1, 1998; 83(2): 649 - 659. [Abstract] [Full Text]
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D. F. Skafar, R. Xu, J. Morales, J. Ram, and J. R. Sowers Female Sex Hormones and Cardiovascular Disease in Women J. Clin. Endocrinol. Metab., December 1, 1997; 82(12): 3913 - 3918. [Abstract] [Full Text] [PDF]
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K. Sudhir, E. Ko, C. Zellner, H. E. Wong, S. J. Hutchison, T. M. Chou, and K. Chatterjee Physiological Concentrations of Estradiol Attenuate Endothelin 1–Induced Coronary Vasoconstriction In Vivo Circulation, November 18, 1997; 96(10): 3626 - 3632. [Abstract] [Full Text]
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K. Sudhir, T. M. Chou, K. Chatterjee, E. P. Smith, T. C. Williams, J. P. Kane, M. J. Malloy, K. S. Korach, and G. M. Rubanyi Premature Coronary Artery Disease Associated With a Disruptive Mutation in the Estrogen Receptor Gene in a Man Circulation, November 18, 1997; 96(10): 3774 - 3777. [Abstract] [Full Text]
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V. L. Baker, V. A. Chao, J. T. Murai, C. J. Zaloudek, and R. N. Taylor Human Umbilical Vessels and Cultured Umbilical Vein Endothelial and Smooth Muscle Cells Lack Detectable Protein and mRNA Endocing Estrogen Receptors Reproductive Sciences, November 1, 1997; 4(6): 316 - 324. [Abstract] [PDF]
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Y. Matsubara, M. Murata, K. Kawano, T. Zama, N. Aoki, H. Yoshino, G. Watanabe, K. Ishikawa, and Y. Ikeda Genotype Distribution of Estrogen Receptor Polymorphisms in Men and Postmenopausal Women From Healthy and Coronary Populations and Its Relation to Serum Lipid Levels Arterioscler Thromb Vasc Biol, November 1, 1997; 17(11): 3006 - 3012. [Abstract] [Full Text]
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A. N. MacRitchie, S. S. Jun, Z. Chen, Z. German, I. S. Yuhanna, T. S. Sherman, and P. W. Shaul Estrogen Upregulates Endothelial Nitric Oxide Synthase Gene Expression in Fetal Pulmonary Artery Endothelium Circ. Res., September 19, 1997; 81(3): 355 - 362. [Abstract] [Full Text]
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A. K. Morey, A. Pedram, M. Razandi, B. A. Prins, R.-M. Hu, E. Biesiada, and E. R. Levin Estrogen and Progesterone Inhibit Vascular Smooth Muscle Proliferation Endocrinology, August 1, 1997; 138(8): 3330 - 3339. [Abstract] [Full Text] [PDF]
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K. Krasinski, I. Spyridopoulos, T. Asahara, R. van der Zee, J. M. Isner, and D. W. Losordo Estradiol Accelerates Functional Endothelial Recovery After Arterial Injury Circulation, April 1, 1997; 95(7): 1768 - 1772. [Abstract] [Full Text]
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M. Balica, K. Bostrom, V. Shin, K. Tillisch, and L. L. Demer Calcifying Subpopulation of Bovine Aortic Smooth Muscle Cells Is Responsive to 17ß-Estradiol Circulation, April 1, 1997; 95(7): 1954 - 1960. [Abstract] [Full Text]
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I. Spyridopoulos, A. B. Sullivan, M. Kearney, J. M. Isner, and D. W. Losordo Estrogen-Receptor–Mediated Inhibition of Human Endothelial Cell Apoptosis : Estradiol as a Survival Factor Circulation, March 18, 1997; 95(6): 1505 - 1514. [Abstract] [Full Text]
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S. Kim-Schulze, K. A. McGowan, S. C. Hubchak, M. C. Cid, M. B. Martin, H. K. Kleinman, G. L. Greene, and H. W. Schnaper Expression of an Estrogen Receptor by Human Coronary Artery and Umbilical Vein Endothelial Cells Circulation, September 15, 1996; 94(6): 1402 - 1407. [Abstract] [Full Text]
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C. D. Venkov, A. B. Rankin, and D. E. Vaughan Identification of Authentic Estrogen Receptor in Cultured Endothelial Cells: A Potential Mechanism for Steroid Hormone Regulation of Endothelial Function Circulation, August 15, 1996; 94(4): 727 - 733. [Abstract] [Full Text]
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H. Hanke, S. Hanke, G. Finking, A. Muhic-Lohrer, A. O. Muck, F. W. Schmahl, R. Haasis, and V. Hombach Different Effects of Estrogen and Progesterone on Experimental Atherosclerosis inFemale Versus Male Rabbits: Quantification of Cellular Proliferation by Bromodeoxyuridine Circulation, July 15, 1996; 94(2): 175 - 181. [Abstract] [Full Text]
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S.-J. Chen, H. Li, J. Durand, S. Oparil, and Y.-F. Chen Estrogen Reduces Myointimal Proliferation After Balloon Injury of Rat Carotid Artery Circulation, February 1, 1996; 93(3): 577 - 584. [Abstract] [Full Text]
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