Oxidative stress and endothelial dysfunction

G. Muller; C. Goettsch; H. Morawietz

doi:10.1055/s-0037-1616894

Hämostaseologie, Table of Contents

Hamostaseologie 2007; 27(01): 5-12
DOI: 10.1055/s-0037-1616894

Orginal Articles

Schattauer GmbH

Oxidative stress and endothelial dysfunction

Oxidative stress und endotheliale Dysfunckion

G. Muller

¹Department of Vascular Endothelium and Microcirculation (Head: Prof. Henning Morawietz), University of Technology Dresden, Germany

,

C. Goettsch

¹Department of Vascular Endothelium and Microcirculation (Head: Prof. Henning Morawietz), University of Technology Dresden, Germany

,

H. Morawietz

¹Department of Vascular Endothelium and Microcirculation (Head: Prof. Henning Morawietz), University of Technology Dresden, Germany

› Author Affiliations

Abstract

Summary

This review focuses on the role of vascular oxidative stress in the development and progression of endothelial dysfunction. We discuss different sources of oxidative stress in the vessel wall, oxidative stress and coagulation, the role of oxidative stress and vascular function in arteries and veins, the flow-dependent regulation of reactive oxygen species, the putative impact of oxidative stress on atherosclerosis, the interaction of angiotensin II, oxidative stress and endothelial dysfunction, and clinical implications.

Zusammenfassung

Diese Übersichtsarbeit fokussiert auf die Rolle von vaskulärem oxidativen Stress in der Entwicklung und Progression von endothelialer Dysfunktion. Wir diskutieren unterschiedliche Quellen reaktiver Sauerstoffspezies in der Gefäßwand, oxidativen Stress und Koagulation, die Rolle von oxidativem Stress und Gefäßfunktion in Arterien und Venen, die flussabhängige Regulation von reaktiven Sauerstoffspezies, den möglichen Einfluss von oxidativem Stress auf die Atherosklerose, die Interaktion von Angiotensin II, oxidativem Stress und endothelialer Dysfunktion und klinische Implikationen.

Keywords

Endothelial dysfunction - lipoproteins - nitric oxide - oxidative stress

Schlüsselwörter

Endotheliale Dysfunktion - Lipoproteine - oxidativer Stress - Stickstoffmonoxid

Full Text

References

References
1 Adams V, Linke A, Krankel N. et al. Impact of regular physical activity on the NAD(P)H oxidase and angiotensin receptor system in patients with coronary artery disease. Circulation 2005; 111: 555-62.
2 Ago T, Kitazono T, Ooboshi H. et al. Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation 2004; 109: 227-33.
3 Ahamed J, Versteeg HH, Kerver M. et al. Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc Natl Acad Sci USA 2006; 103: 13932-7.
4 Al-Benna S, Hamilton CA, McClure JD. et al. Low-density lipoprotein cholesterol determines oxidative stress and endothelial dysfunction in saphenous veins from patients with coronary artery disease. Arterioscler Thromb Vasc Biol 2006; 26: 218-23.
5 Ambasta RK, Kumar P, Griendling KK. et al. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J Biol Chem 2004; 279: 45935-41.
6 Arbogast HP. Antithrombogenicity of human endothelial cells. Hämostaseologie 2005; 25: 394-400.
7 Ayajiki K, Kindermann M, Hecker M. et al. Intracellular pH and tyrosine phosphorylation but not calcium determine shear stress-induced nitric oxide production in native endothelial cells. Circ Res 1996; 78: 750-8.
8 Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 2000; 87: 840-4.
9 Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 2004; 24: 816-23.
10 Chatterjee S, Ghosh N. Oxidized low density lipoprotein stimulates aortic smooth muscle cell proliferation. Glycobiology 1996; 6: 303-11.
11 Chlopicki S, Olszanecki R, Janiszewski M. et al. Functional role of NADPH oxidase in activation of platelets. Antioxid Redox Signal. 2004; 6: 691-8.
12 Cifuentes ME, Pagano PJ. Targeting reactive oxygen species in hypertension. Curr Opin Nephrol Hypertens 2006; 15: 179-86.
13 Cushing SD, Berliner JA, Valente AJ. et al. Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells. Proc Natl Acad Sci USA 1990; 87: 5134-8.
14 Darley-Usmar VM, Hogg N, O’Leary VJ. et al. The simultaneous generation of superoxide and nitric oxide can initiate lipid peroxidation in human low density lipoprotein. Free Radic Res Commun 1992; 17: 9-20.
15 De Keulenaer GW, Chappell DC, Ishizaka N. et al. Oscillatory and steady laminar shear stress differentially affect human endothelial redox state: role of a superoxide-producing NADH oxidase. Circ Res 1998; 82: 1094-101.
16 Dimmeler S, Hermann C, Galle J. et al. Upregulation of superoxide dismutase and nitric oxide synthase mediates the apoptosis-suppressive effects of shear stress on endothelial cells. Arterioscler Thromb Vasc Biol 1999; 19: 656-64.
17 Djordjevic T, Hess J, Herkert O. et al. Rac regulates thrombin-induced tissue factor expression in pulmonary artery smooth muscle cells involving the nuclear factor-kappaB pathway. Antioxid Redox Signal 2004; 6: 713-20.
18 Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2002; 82: 47-95.
19 Duerrschmidt N, Wippich N, Goettsch W. et al. Endothelin-1 induces NAD(P)H oxidase in human endothelial cells. Biochem Biophys Res Commun 2000; 269: 713-7.
20 Duerrschmidt N, Stielow C, Muller G. et al. NOmediated regulation of NAD(P)H oxidase by laminar shear stress in human endothelial cells. J Physiol 2006; 576: 557-67.
21 Endemann DH, Schiffrin EL. Endothelial dysfunction. J Am Soc Nephrol 2004; 15: 1983-92.
22 Esper RJ, Nordaby RA, Vilarino JO. et al. Endothelial dysfunction: a comprehensive appraisal. Cardiovasc Diabetol 2006; 5: 4.
23 Fink GD, Johnson RJ, Galligan JJ. Mechanisms of increased venous smooth muscle tone in desoxycorticosterone acetate-salt hypertension. Hypertension 2000; 35: 464-9.
24 Fleming I, Busse R. Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol 2003; 284: R1-12.
25 Forstermann U, Mugge A, Alheid U. et al. Selective attenuation of endothelium-mediated vasodilation in atherosclerotic human coronary arteries. Circ Res 1988; 62: 185-90.
26 Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980; 288: 373-6.
27 Galle J, Hansen-Hagge T, Wanner C. et al. Impact of oxidized low density lipoprotein on vascular cells. Atherosclerosis 2006; 185: 219-26.
28 Garg UC, Hassid A. Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 1989; 83: 1774-7.
29 Geiszt M, Kopp JB, Varnai P. et al. Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci USA 2000; 97: 8010-4.
30 Gerlach M, Keh D, Bezold G. et al. Nitric oxide inhibits tissue factor synthesis, expression and activity in human monocytes by prior formation of peroxynitrite. Intensive Care Med 1998; 24: 1199-208.
31 Ghiadoni L, Virdis A, Magagna A. et al. Effect of the angiotensin II type 1 receptor blocker candesartan on endothelial function in patients with essential hypertension. Hypertension 2000; 35: 501-6.
32 Golino P, Ragni M, Cirillo P. et al. Effects of tissue factor induced by oxygen free radicals on coronary flow during reperfusion. Nat Med 1996; 2: 35-40.
33 Gorlach A. Redox control of blood coagulation. Antioxid Redox Signal 2004; 6: 687-90.
34 Gorlach A, Brandes RP, Nguyen K. et al. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ Res 2000; 87: 26-32.
35 Gregg D, de Carvalho DD, Kovacic H. Integrins and coagulation: a role for ROS/redox signaling?. Antioxid Redox Signal 2004; 6: 757-64.
36 Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 2000; 86: 494-501.
37 Gryglewski RJ, Palmer RM, Moncada S. Superoxide anion is involved in the breakdown of endothelium- derived vascular relaxing factor. Nature 1986; 320: 454-6.
38 Guzik TJ, West NE, Black E. et al. Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors. Circ Res 2000; 86: E85-90.
39 Guzik TJ, Sadowski J, Kapelak B. et al. Systemic regulation of vascular NAD(P)H oxidase activity and nox isoform expression in human arteries and veins. Arterioscler Thromb Vasc Biol 2004; 24: 1614-20.
40 Harrison D, Griendling KK, Landmesser U. et al. Role of oxidative stress in atherosclerosis. Am J Cardiol 2003; 91: 7A-11A.
41 Herkert O, Djordjevic T, BelAiba RS. et al. Insights into the redox control of blood coagulation: role of vascular NADPH oxidase-derived reactive oxygen species in the thrombogenic cycle. Antioxid Redox Signal 2004; 6: 765-76.
42 Hwang J, Ing MH, Salazar A. et al. Pulsatile versus oscillatory shear stress regulates NADPH oxidase subunit expression: implication for native LDL oxidation. Circ Res 2003; 93: 1225-32.
43 Hwang J, Saha A, Boo YC. et al. Oscillatory shear stress stimulates endothelial production of O2 - from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion. J Biol Chem 2003; 278: 47291-8.
44 Jacobi J, Kristal B, Chezar J. et al. Exogenous superoxide mediates pro-oxidative, proinflammatory, and procoagulatory changes in primary endothelial cell cultures. Free Radic Biol Med 2005; 39: 1238-48.
45 Jialal I, Devaraj S. Antioxidants and atherosclerosis: don’t throw out the baby with the bath water. Circulation 2003; 107: 926-8.
46 Jones SA, O’Donnell VB, Wood JD. et al. Expression of phagocyte NADPH oxidase components in human endothelial cells. Am J Physiol 1996; 271: H1626-34.
47 Kelm M. The L-arginine-nitric oxide pathway in hypertension. Curr Hypertens Rep 2003; 5: 80-6.
48 Khan BV, Harrison DG, Olbrych MT. et al. Nitric oxide regulates vascular cell adhesion molecule 1 gene expression and redox-sensitive transcriptional events in human vascular endothelial cells. Proc Natl Acad Sci USA 1996; 93: 9114-9.
49 Khan Q, Mehta JL. Relevance of platelet-independent effects of aspirin to its salutary effect in atherosclerosis- related events. J Atheroscler Thromb 2005; 12: 185-90.
50 Kim S, Iwao H. Molecular and cellular mechanisms of angiotensin II-mediated cardiovascular and renal diseases. Pharmacol Rev 2000; 52: 11-34.
51 Kume N, Cybulsky MI, Gimbrone Jr MA. Lysophosphatidylcholine, a component of atherogenic lipoproteins, induces mononuclear leukocyte adhesion molecules in cultured human and rabbit arterial endothelial cells. J Clin Invest 1992; 90: 1138-44.
52 Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 2004; 4: 181-9.
53 Lambeth JD, Cheng G, Arnold RS. et al. Novel homologs of gp91phox. Trends Biochem Sci 2000; 25: 459-61.
54 Landmesser U, Hornig B, Drexler H. Endothelial function: a critical determinant in atherosclerosis?. Circulation 2004; 109: II27-33.
55 Laufs U, La Fata V, Plutzky J. et al. Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation 1998; 97: 1129-35.
56 Laufs U, Wassmann S, Czech T. et al. Physical inactivity increases oxidative stress, endothelial dysfunction, and atherosclerosis. Arterioscler Thromb Vasc Biol 2005; 25: 809-14.
57 Li DY, Zhang YC, Philips MI. et al. Upregulation of endothelial receptor for oxidized low-density lipoprotein (LOX-1) in cultured human coronary artery endothelial cells by angiotensin II type 1 receptor activation. Circ Res 1999; 84: 1043-9.
58 Lonn E, Yusuf S, Dzavik V. et al. Effects of ramipril and vitamin E on atherosclerosis: the study to evaluate carotid ultrasound changes in patients treated with ramipril and vitamin E (SECURE). Circulation 2001; 103: 919-25.
59 Marbet GA. Quantification of coagulation factors and inhibitors. Hämostaseologie 2006; 26: 38-41.
60 Matsuzaki I, Chatterjee S, Debolt K. et al. Membrane depolarization and NADPH oxidase activation in aortic endothelium during ischemia reflect altered mechanotransduction. Am J Physiol Heart Circ Physiol 2005; 288: H336-43.
61 McGorisk GM, Treasure CB. Endothelial dysfunction in coronary heart disease. Curr Opin Cardiol 1996; 11: 341-50.
62 McNally JS, Davis ME, Giddens DP. et al. 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 2003; 285: H2290-7.
63 Mehta P. Aspirin in the prophylaxis of coronary artery disease. Curr Opin Cardiol 2002; 17: 552-8.
64 Morawietz H, Duerrschmidt N, Niemann B. et al. Induction of the oxLDL receptor LOX-1 by endothelin-1 in human endothelial cells. Biochem Biophys Res Commun 2001; 284: 961-5.
65 Morawietz H, Rueckschloss U, Niemann B. et al. Angiotensin II induces LOX-1, the human endothelial receptor for oxidized low-density lipoprotein. Circulation 1999; 100: 899-902.
66 Morawietz H, Erbs S, Holtz J. et al. Endothelial Protection, AT1 blockade and Cholesterol-Dependent Oxidative Stress: the EPAS trial. Circulation 2006; 114: I296-301.
67 Muller G, Catar RA, Niemann B. et al. Upregulation of endothelin receptor B in human endothelial cells by low-density lipoproteins. Exp Biol Med (Maywood) 2006; 231: 766-71.
68 Napoli C, Ackah E, De Nigris F. et al. Chronic treatment with nitric oxide-releasing aspirin reduces plasma low-density lipoprotein oxidation and oxidative stress, arterial oxidation-specific epitopes, and atherogenesis in hypercholesterolemic mice. Proc Natl Acad Sci USA 2002; 99: 12467-70.
69 Nickenig G, Sachinidis A, Michaelsen F. et al. Upregulation of vascular angiotensin II receptor gene expression by low- density lipoprotein in vascular smooth muscle cells. Circulation 1997; 95: 473-8.
70 Nickenig G, Baumer AT, Temur Y. et al. Statin-sensitive dysregulated AT1 receptor function and density in hypercholesterolemic men. Circulation 1999; 100: 2131-4.
71 Niemann B, Rohrbach S, Catar RA. et al. Native and oxidized low-density lipoproteins stimulate endothelin-converting enzyme-1 expression in human endothelial cells. Biochem Biophys Res Commun 2005; 334: 747-53.
72 Nishida K, Harrison DG, Navas JP. et al. Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. J Clin Invest 1992; 90: 2092-6.
73 Ohkura N, Hiraishi S, Itabe H. et al. Oxidized phospholipids in oxidized low-density lipoprotein reduce the activity of tissue factor pathway inhibitor through association with its carboxy-terminal region. Antioxid Redox Signal 2004; 6: 705-12.
74 Packer M, Poole-Wilson PA, Armstrong PW. et al. Comparative effects of low and high doses of the angiotensin-converting enzyme inhibitor, lisinopril, on morbidity and mortality in chronic heart failure. ATLAS Study Group. Circulation 1999; 100: 2312-8.
75 Panza JA, Quyyumi AA, Brush Jr JE. et al. Abnormal endothelium-dependent vascular relaxation in patients with essential hypertension. N Engl J Med 1990; 323: 22-7.
76 Prasad A, Tupas-Habib T, Schenke WH. et al. Acute and chronic angiotensin-1 receptor antagonism reverses endothelial dysfunction in atherosclerosis. Circulation 2000; 101: 2349-54.
77 Radomski MW, Palmer RM, Moncada S. The role of nitric oxide and cGMP in platelet adhesion to vascular endothelium. Biochem Biophys Res Commun 1987; 148: 1482-9.
78 Rajagopalan S, Kurz S, Munzel T. et al. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest 1996; 97: 1916-23.
79 Rueckschloss U, Duerrschmidt N, Morawietz H. NADPH oxidase in endothelial cells: impact on atherosclerosis. Antioxid Redox Signal 2003; 5: 171-80.
80 Rueckschloss U, Quinn MT, Holtz J. et al. Dosedependent regulation of NAD(P)H oxidase expression by angiotensin II in human endothelial cells: protective effect of angiotensin II type 1 receptor blockade in patients with coronary artery disease. Arterioscler Thromb Vasc Biol 2002; 22: 1845-51.
81 Rueckschloss U, Galle J, Holtz J. et al. Induction of NAD(P)H oxidase by oxidized low-density lipoprotein in human endothelial cells: antioxidative potential of hydroxymethylglutaryl coenzyme A reductase inhibitor therapy. Circulation 2001; 104: 1767-72.
82 Schiffrin EL, Park JB, Intengan HD. et al. Correction of arterial structure and endothelial dysfunction in human essential hypertension by the angiotensin receptor antagonist losartan. Circulation 2000; 101: 1653-9.
83 Shaul PW. Regulation of endothelial nitric oxide synthase: location, location, location. Ann Rev Physiol 2002; 64: 749-74.
84 Sorescu D, Weiss D, Lassegue B. et al. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 2002; 105: 1429-35.
85 Sorop O, Spaan JAE, Sweeney TE. et al. Effect of steady versus oscillatory flow on porcine coronary arterioles: involvement of NO and superoxide anion. Circ Res 2003; 92: 1344-51.
86 Stielow C, Müller G, Morawietz H. Nox4-mediated superoxide anion formation in human endothelial cells. J Vasc Res 2005; 43: 28-9.
87 Stielow C, Catar RA, Muller G. et al. Novel Nox inhibitor of oxLDL-induced reactive oxygen species formation in human endothelial cells. Biochem Biophys Res Commun 2006; 344: 200-5.
88 Strawn WB, Chappell MC, Dean RH. et al. Inhibition of early atherogenesis by losartan in monkeys with diet- induced hypercholesterolemia. Circulation 2000; 101: 1586-93.
89 Thakali KM, Lau Y, Fink GD. et al. Mechanisms of hypertension induced by nitric oxide (NO) deficiency: focus on venous function. J Cardiovasc Pharmacol 2006; 47: 742-50.
90 Usui M, Ichiki T, Katoh M. et al. Regulation of angiotensin II receptor expression by nitric oxide in rat adrenal gland. Hypertension 1998; 32: 527-33.
91 Vergnani L, Hatrik S, Ricci F. et al. Effect of native and oxidized low-density lipoprotein on endothelial nitric oxide and superoxide production: key role of L-arginine availability. Circulation 2000; 101: 1261-6.
92 Wang HD, Xu S, Johns DG. et al. Role of NADPH oxidase in the vascular hypertrophic and oxidative stress response to angiotensin II in mice. Circ Res 2001; 88: 947-53.
93 Witztum JL, Steinberg D. Role of oxidized low density lipoprotein in atherogenesis. J Clin Invest 1991; 88: 1785-92.
94 Yoshida H, Quehenberger O, Kondratenko N. et al. Minimally oxidized low-density lipoprotein increases expression of scavenger receptor A, CD36, and macrosialin in resident mouse peritoneal macrophages. Arterioscler Thromb Vasc Biol 1998; 18: 794-802.
95 Yusuf S, Sleight P, Pogue J. et al. Effects of an angiotensin- converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med 2000; 342: 145-53.
96 Zou M, Martin C, Ullrich V. Tyrosine nitration as a mechanism of selective inactivation of prostacyclin synthase by peroxynitrite. Biol Chem 1997; 378: 707-13.