© 1996 American Heart Association, Inc.
Articles |
Phosphorylation of Endothelial Nitric Oxide Synthase in Response to Fluid Shear Stress
the Cardiology Divisions of the University of Washington School of Medicine (M.A.C., B.C.B.), Seattle, Wa; Emory University School of Medicine (S.E.L., D.G.H.), Atlanta, Ga; and the School of Mechanical Engineering (N.L.J., R.M.N.), Georgia Institute of Technology, Atlanta, Ga.
Correspondence to Marshall A. Corson, MD, Cardiology Division, Box 357710, University of Washington, Seattle, WA 98195. E-mail mcorson@u.washington.edu.
Endothelial cells release nitric oxide (NO) more potently in response to increased shear stress than to agonists which elevate intracellular free calcium concentration ([Ca2+]i). To determine mechanistic differences in the regulation of endothelial constitutive NO synthase (ecNOS), we measured NO production by bovine aortic endothelial cells exposed to shear stress in a laminar flow chamber or treated with Ca2+ ionophores in static culture. The kinetics of cumulative NO production varied strikingly: shear stress (25 dyne/cm2) stimulated a biphasic increase over control that was 13-fold at 60 minutes, whereas raising [Ca2+]i caused a monophasic 6-fold increase. We hypothesized that activation of a protein kinase cascade mediates the early phase of flow-dependent NO production. Immunoprecipitation of ecNOS showed a 210% increase in phosphorylation 1 minute after flow initiation, whereas there was no significant increase after Ca2+ ionophore treatment. Although ecNOS was not tyrosine-phosphorylated, the early phase of flow-dependent NO production was blocked by genistein, an inhibitor of tyrosine kinases. To determine the Ca2+ requirement for flow-dependent NO production, we measured [Ca2+]i with a novel flow-step protocol. [Ca2+]i increased with the onset of shear stress, but not after a step increase. However, the step increase in shear stress was associated with a potent biphasic increase in NO production rate and ecNOS phosphorylation. These studies demonstrate that shear stress can increase NO production in the absence of increased [Ca2+]i, and they suggest that phosphorylation of ecNOS may importantly modulate its activity during the imposition of increased shear stress.
Key Words: mechanotransduction • endothelium-derived relaxing factor • vasorelaxation • Ca2+ • tyrosine kinase
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Y.-M. Go, Y. C. Boo, H. Park, M. C. Maland, R. Patel, K. A. Pritchard Jr., Y. Fujio, K. Walsh, V. Darley-Usmar, and H. Jo Protein kinase B/Akt activates c-Jun NH2-terminal kinase by increasing NO production in response to shear stress J Appl Physiol, October 1, 2001; 91(4): 1574 - 1581. [Abstract] [Full Text] [PDF]
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C. Knauf, S. Ferreira, M. Hamdane, C. Mailliot, V. Prevot, J.-C. Beauvillain, and D. Croix Variation of Endothelial Nitric Oxide Synthase Synthesis in the Median Eminence during the Rat Estrous Cycle: An Additional Argument for the Implication of Vascular Blood Vessel in the Control of GnRH Release Endocrinology, October 1, 2001; 142(10): 4288 - 4294. [Abstract] [Full Text] [PDF]
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H. Cai, M. E. Davis, G. R. Drummond, and D. G. Harrison Induction of Endothelial NO Synthase by Hydrogen Peroxide via a Ca2+/Calmodulin-Dependent Protein Kinase II/Janus Kinase 2-Dependent Pathway Arterioscler Thromb Vasc Biol, October 1, 2001; 21(10): 1571 - 1576. [Abstract] [Full Text] [PDF]
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T. Nakano, R. Tominaga, S. Morita, M. Masuda, I. Nagano, K.-i. Imasaka, and H. Yasui Impacts of pulsatile systemic circulation on endothelium-derived nitric oxide release in anesthetized dogs Ann. Thorac. Surg., July 1, 2001; 72(1): 156 - 162. [Abstract] [Full Text] [PDF]
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T. Di, J. A. Sullivan, R. R. Magness, L. Zhang, and I. M. Bird Pregnancy-Specific Enhancement of Agonist-Stimulated ERK-1/2 Signaling in Uterine Artery Endothelial Cells Increases Ca2+ Sensitivity of Endothelial Nitric Oxide Synthase as well as Cytosolic Phospholipase A2 Endocrinology, July 1, 2001; 142(7): 3014 - 3026. [Abstract] [Full Text] [PDF]
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D. Xiao, W. J. Pearce, and L. Zhang Pregnancy enhances endothelium-dependent relaxation of ovine uterine artery: role of NO and intracellular Ca2+ Am J Physiol Heart Circ Physiol, July 1, 2001; 281(1): H183 - H190. [Abstract] [Full Text] [PDF]
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I. Fleming, B. Fisslthaler, S. Dimmeler, B. E. Kemp, and R. Busse Phosphorylation of Thr495 Regulates Ca2+/Calmodulin-Dependent Endothelial Nitric Oxide Synthase Activity Circ. Res., June 8, 2001; 88 (11): e68 - e75. [Abstract] [Full Text] [PDF]
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I. Zachary Signaling mechanisms mediating vascular protective actions of vascular endothelial growth factor Am J Physiol Cell Physiol, June 1, 2001; 280(6): C1375 - C1386. [Abstract] [Full Text] [PDF]
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F. Kim, B. Gallis, and M. A. Corson TNF-{alpha} inhibits flow and insulin signaling leading to NO production in aortic endothelial cells Am J Physiol Cell Physiol, May 1, 2001; 280(5): C1057 - C1065. [Abstract] [Full Text] [PDF]
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D. Sun, A. Huang, S. Sharma, A. Koller, and G. Kaley Endothelial microtubule disruption blocks flow-dependent dilation of arterioles Am J Physiol Heart Circ Physiol, May 1, 2001; 280(5): H2087 - H2093. [Abstract] [Full Text] [PDF]
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 R. Govers and T. J. Rabelink Cellular regulation of endothelial nitric oxide synthase Am J Physiol Renal Physiol, February 1, 2001; 280(2): F193 - F206. [Abstract] [Full Text] [PDF]
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S. Gielen, G. Schuler, and R. Hambrecht Exercise Training in Coronary Artery Disease and Coronary Vasomotion Circulation, January 2, 2001; 103 (1): e1 - e6. [Abstract] [Full Text] [PDF]
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N. Paolocci, P. Pagliaro, T. Isoda, F. W. Saavedra, and D. A. Kass Role of Calcium-Sensitive K+ Channels and Nitric Oxide in In Vivo Coronary Vasodilation From Enhanced Perfusion Pulsatility Circulation, January 2, 2001; 103(1): 119 - 124. [Abstract] [Full Text] [PDF]
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K. M. Reber, G. M. Mager, C. E. Miller, and P. T. Nowicki Relationship between flow rate and NO production in postnatal mesenteric arteries Am J Physiol Gastrointest Liver Physiol, January 1, 2001; 280(1): G43 - G50. [Abstract] [Full Text] [PDF]
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F. T. Ruschitzka, R. H. Wenger, T. Stallmach, T. Quaschning, C. de Wit, K. Wagner, R. Labugger, M. Kelm, G. Noll, T. Rulicke, et al. Nitric oxide prevents cardiovascular disease and determines survival in polyglobulic mice overexpressing erythropoietin PNAS, October 10, 2000; 97(21): 11609 - 11613. [Abstract] [Full Text] [PDF]
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V. Hampl and J. Herget Role of Nitric Oxide in the Pathogenesis of Chronic Pulmonary Hypertension Physiol Rev, October 1, 2000; 80(4): 1337 - 1372. [Abstract] [Full Text] [PDF]
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J. Kitayama, T. Kitazono, S. Ibayashi, M. Wakisaka, Y. Watanabe, M. Kamouchi, T. Nagao, M. Fujishima, and F. M. Faraci Role of Phosphatidylinositol 3-Kinase in Acetylcholine-Induced Dilatation of Rat Basilar Artery Editorial Comment Stroke, October 1, 2000; 31(10): 2487 - 2493. [Abstract] [Full Text] [PDF]
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G. R. Hellermann, B. R. Flam, D. C. Eichler, and L. P. Solomonson Stimulation of Receptor-Mediated Nitric Oxide Production by Vanadate Arterioscler Thromb Vasc Biol, September 1, 2000; 20(9): 2045 - 2050. [Abstract] [Full Text] [PDF]
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 T. Matsuo Basal nitric oxide production is enhanced by hydraulic pressure in cultured human trabecular cells Br J Ophthalmol, June 1, 2000; 84(6): 631 - 635. [Abstract] [Full Text]
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E. N. Mbaku, L. Zhang, S. P. Duckles, and J. Buchholz Nitric-Oxide Synthase-Containing Nerves Facilitate Adrenergic Transmitter Release in Sheep Middle Cerebral Arteries J. Pharmacol. Exp. Ther., May 1, 2000; 293(2): 397 - 402. [Abstract] [Full Text]
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T. Nakano, R. Tominaga, I. Nagano, H. Okabe, and H. Yasui Pulsatile flow enhances endothelium-derived nitric oxide release in the peripheral vasculature Am J Physiol Heart Circ Physiol, April 1, 2000; 278(4): H1098 - H1104. [Abstract] [Full Text] [PDF]
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I. M. Bird, J. A. Sullivan, T. Di, J. M. Cale, L. Zhang, J. Zheng, and R. R. Magness Pregnancy-Dependent Changes in Cell Signaling Underlie Changes in Differential Control of Vasodilator Production in Uterine Artery Endothelial Cells Endocrinology, March 1, 2000; 141(3): 1107 - 1117. [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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E. Butt, M. Bernhardt, A. Smolenski, P. Kotsonis, L. G. Frohlich, A. Sickmann, H. E. Meyer, S. M. Lohmann, and H. H. H. W. Schmidt Endothelial Nitric-oxide Synthase (Type III) Is Activated and Becomes Calcium Independent upon Phosphorylation by Cyclic Nucleotide-dependent Protein Kinases J. Biol. Chem., February 18, 2000; 275(7): 5179 - 5187. [Abstract] [Full Text] [PDF]
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R. VEELKEN, K. F. HILGERS, A. HARTNER, A. HAAS, K. P. BÖHMER, and R. B. STERZEL Nitric Oxide Synthase Isoforms and Glomerular Hyperfiltration in Early Diabetic Nephropathy J. Am. Soc. Nephrol., January 1, 2000; 11(1): 71 - 79. [Abstract] [Full Text]
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B. Gallis, G. L. Corthals, D. R. Goodlett, H. Ueba, F. Kim, S. R. Presnell, D. Figeys, D. G. Harrison, B. C. Berk, R. Aebersold, et al. Identification of Flow-dependent Endothelial Nitric-oxide Synthase Phosphorylation Sites by Mass Spectrometry and Regulation of Phosphorylation and Nitric Oxide Production by the Phosphatidylinositol 3-Kinase Inhibitor LY294002 J. Biol. Chem., October 15, 1999; 274(42): 30101 - 30108. [Abstract] [Full Text] [PDF]
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M. P. Boric, X. F. Figueroa, M. V. Donoso, A. Paredes, I. Poblete, and J. P. Huidobro-Toro Rise in endothelium-derived NO after stimulation of rat perivascular sympathetic mesenteric nerves Am J Physiol Heart Circ Physiol, September 1, 1999; 277(3): H1027 - H1035. [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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I. Fleming and R. Busse Signal transduction of eNOS activation Cardiovasc Res, August 15, 1999; 43(3): 532 - 541. [Abstract] [Full Text] [PDF]
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T. E. Peterson, V. Poppa, H. Ueba, A. Wu, C. Yan, and B. C. Berk Opposing Effects of Reactive Oxygen Species and Cholesterol on Endothelial Nitric Oxide Synthase and Endothelial Cell Caveolae Circ. Res., July 9, 1999; 85(1): 29 - 37. [Abstract] [Full Text] [PDF]
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