© 1998 American Heart Association, Inc.
Original Contributions |
Oscillatory and Steady Laminar Shear Stress Differentially Affect Human Endothelial Redox State
Role of a Superoxide-Producing NADH Oxidase
From the Division of Cardiology, Emory University School of Medicine (G.W. De K., D.C.C., N.I., R.W.A., K.K.G.), and Georgia Institute of Technology, School of Mechanical Engineering (R.M.N.), Atlanta, Ga.
Correspondence to Kathy K. Griendling, PhD, Emory University, Division of Cardiology, 1639 Pierce Dr, 319 WMB, Atlanta, GA 30322. E-mail kgriend{at}emory.edu
Abstract—Atherosclerotic lesions are found opposite vascular flow dividers at sites of low shear stress and oscillatory flow. Since endothelial proinflammatory genes prominent in lesions are regulated by oxidation-sensitive transcriptional control mechanisms, we examined the redox state of cultured human umbilical vein endothelial cells after either oscillatory or steady laminar fluid shear stress. Endothelial oxidative stress was assessed by measuring activity of the superoxide (O2·-)–producing NADH oxidase (a major source of reactive oxygen species in vascular cells), intracellular O2·- levels, induction of the redox-sensitive gene heme oxygenase-1 (HO-1), and abundance of Cu/Zn superoxide dismutase (Cu/Zn SOD), an antioxidant defense enzyme whose level of expression adapts to changes in oxidative stress. When cells were exposed to oscillatory shear (±5 dyne/cm2, 1 Hz) for 1, 5, and 24 hours, NADH oxidase activity and the amount of HO-1 progressively increased up to 174±16% (P<0.05) and 505±111% (P<0.05) versus static conditions, respectively, whereas levels of Cu/Zn SOD remained unchanged. This upregulation of HO-1 was completely blocked by the antioxidant N-acetylcysteine (NAC, 20 mmol/L). In contrast, steady laminar shear (5 dyne/cm2) induced NADH oxidase activity and NAC-sensitive HO-1 mRNA expression only at 1 and 5 hours, a transient response that returned toward baseline at 24 hours. Levels of Cu/Zn SOD mRNA and protein were increased after 24 hours of steady laminar shear. Furthermore, intracellular O2·-, as measured by dihydroethidium fluorescence, was higher in cells exposed to oscillatory than to laminar shear. These data are consistent with the hypothesis that continuous oscillatory shear causes a sustained activation of pro-oxidant processes resulting in redox-sensitive gene expression in human endothelial cells. Steady laminar shear stress initially activates these processes but appears to induce compensatory antioxidant defenses. We speculate that differences in endothelial redox state, orchestrated by different regimens of shear stress, may contribute to the focal nature of atherosclerosis.
Key Words: shear stress • endothelium • NADH/NADPH oxidase • oxygen-derived free radical • heme oxygenase-1
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J. A. Vita and G. F. Mitchell Effects of shear stress and flow pulsatility on endothelial function: Insights gleaned from external counterpulsation therapy J. Am. Coll. Cardiol., December 17, 2003; 42(12): 2096 - 2098. [Full Text] [PDF]
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J. Hwang, M. H. Ing, A. Salazar, B. Lassegue, K. Griendling, M. Navab, A. Sevanian, and T. K. Hsiai Pulsatile Versus Oscillatory Shear Stress Regulates NADPH Oxidase Subunit Expression: Implication for Native LDL Oxidation Circ. Res., December 12, 2003; 93(12): 1225 - 1232. [Abstract] [Full Text] [PDF]
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J. S. McNally, M. E. Davis, D. P. Giddens, A. Saha, J. Hwang, S. Dikalov, H. Jo, and D. G. Harrison Role of xanthine oxidoreductase and NAD(P)H oxidase in endothelial superoxide production in response to oscillatory shear stress Am J Physiol Heart Circ Physiol, December 1, 2003; 285(6): H2290 - H2297. [Abstract] [Full Text] [PDF]
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Y. Taniyama and K. K. Griendling Reactive Oxygen Species in the Vasculature: Molecular and Cellular Mechanisms Hypertension, December 1, 2003; 42(6): 1075 - 1081. [Abstract] [Full Text] [PDF]
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J. Hwang, A. Saha, Y. C. Boo, G. P. Sorescu, J. S. McNally, S. M. Holland, S. Dikalov, D. P. Giddens, K. K. Griendling, D. G. Harrison, et al. Oscillatory Shear Stress Stimulates Endothelial Production of O2- from p47phox-dependent NAD(P)H Oxidases, Leading to Monocyte Adhesion J. Biol. Chem., November 21, 2003; 278(47): 47291 - 47298. [Abstract] [Full Text] [PDF]
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 M. Kitada, D. Koya, T. Sugimoto, M. Isono, S.-i. Araki, A. Kashiwagi, and M. Haneda Translocation of Glomerular p47phox and p67phox by Protein Kinase C-{beta} Activation Is Required for Oxidative Stress in Diabetic Nephropathy Diabetes, October 1, 2003; 52(10): 2603 - 2614. [Abstract] [Full Text] [PDF]
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Y. Liu, H. Zhao, H. Li, B. Kalyanaraman, A. C. Nicolosi, and D. D. Gutterman Mitochondrial Sources of H2O2 Generation Play a Key Role in Flow-Mediated Dilation in Human Coronary Resistance Arteries Circ. Res., September 19, 2003; 93(6): 573 - 580. [Abstract] [Full Text] [PDF]
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T. K. HSIAI, S. K. CHO, P. K. WONG, M. ING, A. SALAZAR, A. SEVANIAN, M. NAVAB, L. L. DEMER, and C.-M. HO Monocyte recruitment to endothelial cells in response to oscillatory shear stress FASEB J, September 1, 2003; 17(12): 1648 - 1657. [Abstract] [Full Text] [PDF]
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G. Mancia, G. Parati, P. Castiglioni, R. Tordi, E. Tortorici, F. Glavina, and M. Di Rienzo Daily Life Blood Pressure Changes Are Steeper in Hypertensive Than in Normotensive Subjects Hypertension, September 1, 2003; 42(3): 277 - 282. [Abstract] [Full Text] [PDF]
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R. Magid, T. J. Murphy, and Z. S. Galis Expression of Matrix Metalloproteinase-9 in Endothelial Cells Is Differentially Regulated by Shear Stress: ROLE OF c-Myc J. Biol. Chem., August 29, 2003; 278(35): 32994 - 32999. [Abstract] [Full Text] [PDF]
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B. Lassegue and R. E. Clempus Vascular NAD(P)H oxidases: specific features, expression, and regulation Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2003; 285(2): R277 - R297. [Abstract] [Full Text] [PDF]
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O. Sorop, J. A.E. Spaan, T. E. Sweeney, and E. VanBavel Effect of Steady Versus Oscillating Flow on Porcine Coronary Arterioles: Involvement of NO and Superoxide Anion Circ. Res., June 27, 2003; 92(12): 1344 - 1351. [Abstract] [Full Text] [PDF]
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 D. G Harrison, Hua Cai, U. Landmesser, and K. K Griendling The Pickering Lecture British Hypertension Society, 10th September 2002: Interactions of angiotensin II with NAD(P)H oxidase, oxidant stress and cardiovascular disease Journal of Renin-Angiotensin-Aldosterone System, June 1, 2003; 4(2): 51 - 61. [Abstract] [PDF]
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 B.A. Kelly, B.C. Bond, and L. Poston Gestational profile of matrix metalloproteinases in rat uterine artery Mol. Hum. Reprod., June 1, 2003; 9(6): 351 - 358. [Abstract] [Full Text] [PDF]
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C.-W. Ni, H.-J. Hsieh, Y.-J. Chao, and D. L. Wang Shear Flow Attenuates Serum-induced STAT3 Activation in Endothelial Cells J. Biol. Chem., May 23, 2003; 278(22): 19702 - 19708. [Abstract] [Full Text] [PDF]
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R. Ceravolo, R. Maio, A. Pujia, A. Sciacqua, G. Ventura, M. C. Costa, G. Sesti, and F. Perticone Pulse pressure and endothelial dysfunction in never-treated hypertensive patients J. Am. Coll. Cardiol., May 21, 2003; 41(10): 1753 - 1758. [Abstract] [Full Text] [PDF]
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A. Lerman and J. Herrmann Endothelial function under pressure J. Am. Coll. Cardiol., May 21, 2003; 41(10): 1759 - 1760. [Full Text] [PDF]
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E. R. Gross, J. F. LaDisa Jr., D. Weihrauch, L. E. Olson, T. T. Kress, D. A. Hettrick, P. S. Pagel, D. C. Warltier, and J. R. Kersten Reactive oxygen species modulate coronary wall shear stress and endothelial function during hyperglycemia Am J Physiol Heart Circ Physiol, May 1, 2003; 284(5): H1552 - H1559. [Abstract] [Full Text] [PDF]
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L. Belhassen, G. Pelle, J.-L. Dubois-Rande, and S. Adnot Improved endothelial function by the thromboxane a2 receptor antagonist s 18886 in patients with coronary artery disease treated with aspirin J. Am. Coll. Cardiol., April 2, 2003; 41(7): 1198 - 1204. [Abstract] [Full Text] [PDF]
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J. W. E. Rush, J. R. Turk, and M. H. Laughlin Exercise training regulates SOD-1 and oxidative stress in porcine aortic endothelium Am J Physiol Heart Circ Physiol, April 1, 2003; 284(4): H1378 - H1387. [Abstract] [Full Text] [PDF]
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H. Miura, J. J. Bosnjak, G. Ning, T. Saito, M. Miura, and D. D. Gutterman Role for Hydrogen Peroxide in Flow-Induced Dilation of Human Coronary Arterioles Circ. Res., February 7, 2003; 92 (2): e31 - e40. [Abstract] [Full Text] [PDF]
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D. X. Zhang, A.-P. Zou, and P.-L. Li Ceramide-induced activation of NADPH oxidase and endothelial dysfunction in small coronary arteries Am J Physiol Heart Circ Physiol, February 1, 2003; 284(2): H605 - H612. [Abstract] [Full Text] [PDF]
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X. Peng, S. Haldar, S. Deshpande, K. Irani, and D. A. Kass Wall Stiffness Suppresses Akt/eNOS and Cytoprotection in Pulse-Perfused Endothelium Hypertension, February 1, 2003; 41(2): 378 - 381. [Abstract] [Full Text] [PDF]
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X.-L. Chen, S. E. Varner, A. S. Rao, J. Y. Grey, S. Thomas, C. K. Cook, M. A. Wasserman, R. M. Medford, A. K. Jaiswal, and C. Kunsch Laminar Flow Induction of Antioxidant Response Element-mediated Genes in Endothelial Cells. A NOVEL ANTI-INFLAMMATORY MECHANISM J. Biol. Chem., January 3, 2003; 278(2): 703 - 711. [Abstract] [Full Text] [PDF]
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S. M. Wasserman, F. Mehraban, L. G. Komuves, R.-B. Yang, J. E. Tomlinson, Y. Zhang, F. Spriggs, and J. N. Topper Gene expression profile of human endothelial cells exposed to sustained fluid shear stress Physiol Genomics, December 26, 2002; 12(1): 13 - 23. [Abstract] [Full Text] [PDF]
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