© 1997 American Heart Association, Inc.
Articles |
17ß-Estradiol Regulation of Human Endothelial Cell Basal Nitric Oxide Release, Independent of Cytosolic Ca2+ Mobilization
From the Division of Cardiovascular Medicine and the Raymond and Beverly Sackler Foundation Laboratory (T.C.-G., J.R.B.), the Department of Pharmacology (G.G.-C., W.C.S.), the Departments of Obstetrics and Gynecology and Psychiatry (P.S.), and the Molecular Cardiobiology Program, Boyer Center for Molecular Medicine (T.C.-G., G.G.-C., W.C.S., J.R.B.), Yale University School of Medicine, New Haven, Conn.
Correspondence to Jeffrey R. Bender, MD, Yale University School Medicine, Boyer Center for Molecular Medicine, 295 Congress Ave, Room 454, New Haven, CT 06536-0812. E-mail jeffrey_bender{at}quickmail.yale.edu.
Abstract Estradiol retards the development of atherosclerosis. Animal models have suggested that NO may be a critical effector molecule in this cardiovascular protection. In this study, female human umbilical vein endothelial cells (HUVECs) were propagated in phenol red–free gonadal hormone–free medium and pretreated with 17ß-estradiol (E2). Reduced NO2- and NO3- (NOX) concentration, determined by chemiluminescence, demonstrated a rapid increase in basal HUVEC NO release in response to physiological concentrations of E2. The estrogen receptor (ER) antagonist ICI 164,384 inhibited the augmented NO release, demonstrating an ER-mediated component of this response. Because endothelial NO synthase (eNOS) activity is largely regulated by cytosolic Ca2+, relative [Ca2+]i in response to E2 was determined in a fluorometric assay. E2 did not promote HUVEC Ca2+ fluxes. Furthermore, eNOS activity in E2-pretreated endothelial whole-cell lysates was not dependent on additional Ca2+. Despite involving the ER, this is a nongenomic effect of E2, as demonstrated by maintained responses in transcriptionally inhibited cells and by the rapidity (10 minutes) of cGMP formation in an NO bioassay. We demonstrate, for the first time, that independent of cytosolic Ca2+ mobilization, there is augmentation of eNOS activity with a resultant increase in HUVEC basal NO release in response to short-term estradiol exposure. Implications for the cardiovascular protective role of estrogen are discussed.
Key Words: atherosclerosis • estrogen • vascular endothelium • nitric oxide • nitric oxide synthase
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N. N. Chan, R. J. MacAllister, H. M. Colhoun, P. Vallance, and A. D. Hingorani Changes in Endothelium-Dependent Vasodilatation and {{alpha}}-Adrenergic Responses in Resistance Vessels during the Menstrual Cycle in Healthy Women J. Clin. Endocrinol. Metab., June 1, 2001; 86(6): 2499 - 2504. [Abstract] [Full Text] [PDF]
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K. K. Koh, D. K. Jin, S. H. Yang, S.-K. Lee, H. Y. Hwang, M. H. Kang, W. Kim, D. S. Kim, I. S. Choi, and E. K. Shin Vascular Effects of Synthetic or Natural Progestagen Combined With Conjugated Equine Estrogen in Healthy Postmenopausal Women Circulation, April 17, 2001; 103(15): 1961 - 1966. [Abstract] [Full Text] [PDF]
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R. K. Dubey and E. K. Jackson Estrogen-induced cardiorenal protection: potential cellular, biochemical, and molecular mechanisms Am J Physiol Renal Physiol, March 1, 2001; 280(3): F365 - F388. [Abstract] [Full Text] [PDF]
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S. Wassmann, A. T. Baumer, K. Strehlow, M. van Eickels, C. Grohe, K. Ahlbory, R. Rosen, M. Bohm, and G. Nickenig Endothelial Dysfunction and Oxidative Stress During Estrogen Deficiency in Spontaneously Hypertensive Rats Circulation, January 23, 2001; 103(3): 435 - 441. [Abstract] [Full Text] [PDF]
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 D. W. Losordo and J. M. Isner Estrogen and Angiogenesis : A Review Arterioscler. Thromb. Vasc. Biol., January 1, 2001; 21(1): 6 - 12. [Abstract] [Full Text] [PDF]
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 E. Falkenstein, H.-C. Tillmann, M. Christ, M. Feuring, and M. Wehling Multiple Actions of Steroid Hormones---A Focus on Rapid, Nongenomic Effects Pharmacol. Rev., December 1, 2000; 52(4): 513 - 556. [Abstract] [Full Text] [PDF]
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M. E. Mendelsohn Nongenomic, ER-Mediated Activation of Endothelial Nitric Oxide Synthase: : How Does It Work? What Does It Mean? Circ. Res., November 24, 2000; 87(11): 956 - 960. [Abstract] [Full Text] [PDF]
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K. L. Chambliss, I. S. Yuhanna, C. Mineo, P. Liu, Z. German, T. S. Sherman, M. E. Mendelsohn, R. G. W. Anderson, and P. W. Shaul Estrogen Receptor {alpha} and Endothelial Nitric Oxide Synthase Are Organized Into a Functional Signaling Module in Caveolae Circ. Res., November 24, 2000; 87 (11): e44 - e52. [Abstract] [Full Text] [PDF]
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M. P. Haynes, D. Sinha, K. S. Russell, M. Collinge, D. Fulton, M. Morales-Ruiz, W. C. Sessa, and J. R. Bender Membrane Estrogen Receptor Engagement Activates Endothelial Nitric Oxide Synthase via the PI3-Kinase-Akt Pathway in Human Endothelial Cells Circ. Res., October 13, 2000; 87(8): 677 - 682. [Abstract] [Full Text] [PDF]
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G. Nickenig, K. Strehlow, S. Wassmann, A. T. Baumer, K. Albory, H. Sauer, and M. Bohm Differential Effects of Estrogen and Progesterone on AT1 Receptor Gene Expression in Vascular Smooth Muscle Cells Circulation, October 10, 2000; 102(15): 1828 - 1833. [Abstract] [Full Text] [PDF]
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M. Noris, M. Todeschini, S. Zappella, S. Bonazzola, C. Zoja, D. Corna, F. Gaspari, F. Marchetti, S. Aiello, and G. Remuzzi 17beta -Estradiol corrects hemostasis in uremic rats by limiting vascular expression of nitric oxide synthases Am J Physiol Renal Physiol, October 1, 2000; 279(4): F626 - F635. [Abstract] [Full Text] [PDF]
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M. T. Littleton-Kearney, D. M. Agnew, R. J. Traystman, and P. D. Hurn Effects of estrogen on cerebral blood flow and pial microvasculature in rabbits Am J Physiol Heart Circ Physiol, September 1, 2000; 279(3): H1208 - H1214. [Abstract] [Full Text] [PDF]
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G. G. Geary, D. N. Krause, and S. P. Duckles Estrogen reduces mouse cerebral artery tone through endothelial NOS- and cyclooxygenase-dependent mechanisms Am J Physiol Heart Circ Physiol, August 1, 2000; 279(2): H511 - H519. [Abstract] [Full Text] [PDF]
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G. G. Geary, D. N. Krause, and S. P. Duckles Gonadal hormones affect diameter of male rat cerebral arteries through endothelium-dependent mechanisms Am J Physiol Heart Circ Physiol, August 1, 2000; 279(2): H610 - H618. [Abstract] [Full Text] [PDF]
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C. R. Rosenfeld, R. E. White, T. Roy, and B. E. Cox Calcium-activated potassium channels and nitric oxide coregulate estrogen-induced vasodilation Am J Physiol Heart Circ Physiol, July 1, 2000; 279(1): H319 - H328. [Abstract] [Full Text] [PDF]
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D. M. Herrington, B. E. Pusser, W. A. Riley, T. Y. Thuren, K. B. Brosnihan, E. A. Brinton, and D. B. MacLean Cardiovascular Effects of Droloxifene, a New Selective Estrogen Receptor Modulator, in Healthy Postmenopausal Women Arterioscler. Thromb. Vasc. Biol., June 1, 2000; 20(6): 1606 - 1612. [Abstract] [Full Text] [PDF]
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K. S. Russell, M. P. Haynes, D. Sinha, E. Clerisme, and J. R. Bender Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling PNAS, May 23, 2000; 97(11): 5930 - 5935. [Abstract] [Full Text] [PDF]
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 M. W. Knoferl, M. D. Diodato, M. K. Angele, A. Ayala, W. G. Cioffi, K. I. Bland, and I. H. Chaudry Do Female Sex Steroids Adversely or Beneficially Affect the Depressed Immune Responses in Males After Trauma-Hemorrhage? Arch Surg, April 1, 2000; 135(4): 425 - 433. [Abstract] [Full Text] [PDF]
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T. J. McCabe, D. Fulton, L. J. Roman, and W. C. Sessa Enhanced Electron Flux and Reduced Calmodulin Dissociation May Explain "Calcium-independent" eNOS Activation by Phosphorylation J. Biol. Chem., February 25, 2000; 275(9): 6123 - 6128. [Abstract] [Full Text] [PDF]
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K. S. Russell, M. P. Haynes, T. Caulin-Glaser, J. Rosneck, W. C. Sessa, and J. R. Bender Estrogen Stimulates Heat Shock Protein 90 Binding to Endothelial Nitric Oxide Synthase in Human Vascular Endothelial Cells. EFFECTS ON CALCIUM SENSITIVITY AND NO RELEASE J. Biol. Chem., February 18, 2000; 275(7): 5026 - 5030. [Abstract] [Full Text] [PDF]
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 T. A. Parker, D. Dunbar Ivy, H. L. Galan, T. R. Grover, J. P. Kinsella, and S. H. Abman Estradiol improves pulmonary hemodynamics and vascular remodeling in perinatal pulmonary hypertension Am J Physiol Lung Cell Mol Physiol, February 1, 2000; 278(2): L374 - L381. [Abstract] [Full Text] [PDF]
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A. Huang, D. Sun, A. Koller, and G. Kaley 17{beta}-Estradiol Restores Endothelial Nitric Oxide Release to Shear Stress in Arterioles of Male Hypertensive Rats Circulation, January 4, 2000; 101(1): 94 - 100. [Abstract] [Full Text] [PDF]
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R. H. Karas, J. B. Hodgin, M. Kwoun, J. H. Krege, M. Aronovitz, W. Mackey, J. A. Gustafsson, K. S. Korach, O. Smithies, and M. E. Mendelsohn Estrogen inhibits the vascular injury response in estrogen receptor beta -deficient female mice PNAS, December 21, 1999; 96(26): 15133 - 15136. [Abstract] [Full Text] [PDF]
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 X. Zhu, B. Bonet, H. Gillenwater, and R. H. Knopp Opposing Effects of Estrogen and Progestins on LDL Oxidation and Vascular Wall Cytotoxicity: Implications for Atherogenesis Experimental Biology and Medicine, December 1, 1999; 222(3): 214 - 221. [Abstract] [Full Text]
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V. M. Miller Gender, Estrogen, and NOS : Cautions About Generalizations Circ. Res., November 26, 1999; 85(11): 979 - 981. [Full Text] [PDF]
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M. Garcia-Duran, T. de Frutos, J. Diaz-Recasens, G. Garcia-Galvez, A. Jimenez, M. Monton, J. Farre, L. S. de Miguel, F. Gonzalez-Fernandez, M. d. M. Arriero, et al. Estrogen Stimulates Neuronal Nitric Oxide Synthase Protein Expression in Human Neutrophils Circ. Res., November 26, 1999; 85(11): 1020 - 1026. [Abstract] [Full Text] [PDF]
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K. K. Koh, A. Blum, L. Hathaway, R. Mincemoyer, G. Csako, M. A. Waclawiw, J. A. Panza, and R. O. Cannon III Vascular Effects of Estrogen and Vitamin E Therapies in Postmenopausal Women Circulation, November 2, 1999; 100(18): 1851 - 1857. [Abstract] [Full Text] [PDF]
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 K. G. Stewart, Y. Zhang, and S. T. Davidge Estrogen Decreases Prostaglandin H Synthase Products From Endothelial Cells Reproductive Sciences, November 1, 1999; 6(6): 322 - 327. [Abstract] [PDF]
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 J. Case and C. A. Davison Estrogen Alters Relative Contributions of Nitric Oxide and Cyclooxygenase Products to Endothelium-Dependent Vasodilation J. Pharmacol. Exp. Ther., November 1, 1999; 291(2): 524 - 530. [Abstract] [Full Text]
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 A. M. McNeill, N. Kim, S. P. Duckles, D. N. Krause, and H. A. Kontos Chronic Estrogen Treatment Increases Levels of Endothelial Nitric Oxide Synthase Protein in Rat Cerebral Microvessels • Editorial Comment Stroke, October 1, 1999; 30(10): 2186 - 2190. [Abstract] [Full Text] [PDF]
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A. Papapetropoulos, R. D. Rudic, and W. C Sessa Molecular control of nitric oxide synthases in the cardiovascular system Cardiovasc Res, August 15, 1999; 43(3): 509 - 520. [Abstract] [Full Text] [PDF]
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