Oxidative stress and vascular damage in hypertension

Correspondence and requests for reprints to David G. Harrison MD, Division of Cardiology, Emory University School of Medicine, 1639 Pierce Drive, 319 WMB, Atlanta, GA 30322, USA. Tel: +1 404 727 3710; fax: +1 404 727 3585; e-mail: dharr02@emory.edu Introduction Increased vascular superoxide production has now been demonstrated in many different experimental models of hypertension, including spontaneous hypertensive rats Ž . SHRs 1 , rats with angiotensin II-induced hypertension 2 , rats with aortic banding-induced or renovascuŽ . lar hypertension two kidney one clip model 3,4 and recently also in rats with deoxycorticosterone acetate-salt Ž . DOCA-salt -induced hypertension, that have no systemic activation of the renin angiotensin system 5 . In addition, in cultured endothelial and vascular smooth muscle cells a twoto three-fold increase in superoxide production is observed after cyclic stretch 6 10 .

[1]  T. Poulos,et al.  Crystal Structure of Constitutive Endothelial Nitric Oxide Synthase A Paradigm for Pterin Function Involving a Novel Metal Center , 1998, Cell.

[2]  M. Moskowitz,et al.  Hypertension in mice lacking the gene for endothelial nitric oxide synthase , 1995, Nature.

[3]  K. Hirata,et al.  Stretch force on vascular smooth muscle cells enhances oxidation of LDL via superoxide production. , 1998, The American journal of physiology.

[4]  K. Irani.  Oxidant signaling in vascular cell growth, death, and survival : a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling. , 2000, Circulation research.

[5]  R. Alexander,et al.  Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. , 1993, The Journal of clinical investigation.

[6]  D. Sorescu,et al.  Modulation of Protein Kinase Activity and Gene Expression by Reactive Oxygen Species and Their Role in Vascular Physiology and Pathophysiology , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[7]  J. Tainer,et al.  Structure of nitric oxide synthase oxygenase dimer with pterin and substrate. , 1998, Science.

[8]  T. Lüscher,et al.  Pulsatile Stretch Stimulates Superoxide Production and Activates Nuclear Factor-κB in Human Coronary Smooth Muscle , 1997 .

[9]  A. Tessitore,et al.  Angiotensin II stimulates intercellular adhesion molecule-1 (ICAM-1) expression by human vascular endothelial cells and increases soluble ICAM-1 release in vivo. , 1999, Circulation.

[10]  D. Harrison,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. , 1996, The Journal of clinical investigation.

[11]  E. Werner,et al.  Tetrahydrobiopterin alters superoxide and nitric oxide release in prehypertensive rats. , 1998, The Journal of clinical investigation.

[12]  B. Berk.  Redox Signals that Regulate the Vascular Response to Injury , 1999, Thrombosis and Haemostasis.

[13]  N. Holbrook,et al.  Oxidants, oxidative stress and the biology of ageing , 2000, Nature.

[14]  E. Ferrannini,et al.  Effect of Vitamin C on Forearm Blood Flow and Glucose Metabolism in Essential Hypertension , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[15]  A. Takeshita,et al.  Important role of local angiotensin II activity mediated via type 1 receptor in the pathogenesis of cardiovascular inflammatory changes induced by chronic blockade of nitric oxide synthesis in rats. , 2000, Circulation.

[16]  H. Maegawa,et al.  Oral Administration of Tetrahydrobiopterin Prevents Endothelial Dysfunction and Vascular Oxidative Stress in the Aortas of Insulin-Resistant Rats , 2000, Circulation research.

[17]  J. Sasaki,et al.  Does superoxide underlie the pathogenesis of hypertension? , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[18]  A. Nishiyama,et al.  Systemic and Regional Hemodynamic Responses to Tempol in Angiotensin II–Infused Hypertensive Rats , 2001, Hypertension.

[19]  G. Schmid-Schönbein,et al.  In vivo evidence for microvascular oxidative stress in spontaneously hypertensive rats. Hydroethidine microfluorography. , 1995, Hypertension.

[20]  N. Vaziri,et al.  Effect of Antioxidant Therapy on Blood Pressure and NO Synthase Expression in Hypertensive Rats , 2000, Hypertension.

[21]  G. Zalba,et al.  Polymorphisms and Promoter Overactivity of the p22 phox Gene in Vascular Smooth Muscle Cells From Spontaneously Hypertensive Rats , 2001, Circulation research.

[22]  J. Keaney,et al.  Pharmacological concentrations of ascorbic acid are required for the beneficial effect on endothelial vasomotor function in hypertension. , 2000, Hypertension.

[23]  K. Williams,et al.  Atherosclerosis--an inflammatory disease. , 1999, The New England journal of medicine.

[24]  A. Zeiher,et al.  Reactive oxygen species and vascular cell apoptosis in response to angiotensin II and pro-atherosclerotic factors , 2000, Regulatory Peptides.

[25]  W R Taylor,et al.  Role of NADH/NADPH oxidase-derived H2O2 in angiotensin II-induced vascular hypertrophy. , 1998, Hypertension.

[26]  G. Kojda,et al.  Protein expression, vascular reactivity and soluble guanylate cyclase activity in mice lacking the endothelial cell nitric oxide synthase: contributions of NOS isoforms to blood pressure and heart rate control. , 1999, Cardiovascular research.

[27]  A. Zeiher,et al.  Angiotensin II induces apoptosis of human endothelial cells. Protective effect of nitric oxide. , 1997, Circulation research.

[28]  R. Busse,et al.  Endothelial dysfunction coincides with an enhanced nitric oxide synthase expression and superoxide anion production. , 1997, Hypertension.

[29]  K. Pritchard,et al.  Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[30]  N. Vaziri,et al.  Induction of oxidative stress by glutathione depletion causes severe hypertension in normal rats. , 2000, Hypertension.

[31]  H. Drexler,et al.  Role of NAD(P)H Oxidase in Angiotensin II–Induced JAK/STAT Signaling and Cytokine Induction , 2000, Circulation research.

[32]  D. Ganten,et al.  Hypertension-induced end-organ damage : A new transgenic approach to an old problem. , 1999, Hypertension.

[33]  R. Nerem,et al.  Cyclic strain induces an oxidative stress in endothelial cells. , 1997, The American journal of physiology.

[34]  R. Alexander,et al.  Angiotensin II induces monocyte chemoattractant protein-1 gene expression in rat vascular smooth muscle cells. , 1998, Circulation research.

[35]  J. Díez,et al.  Vascular NADH/NADPH oxidase is involved in enhanced superoxide production in spontaneously hypertensive rats. , 2000, Hypertension.

[36]  D. Harrison,et al.  Nitric oxide regulates vascular cell adhesion molecule 1 gene expression and redox-sensitive transcriptional events in human vascular endothelial cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  D. Weiss,et al.  Angiotensin II–Induced Hypertension Accelerates the Development of Atherosclerosis in ApoE-Deficient Mice , 2001, Circulation.

[38]  T. Meinertz,et al.  Increased NAD(P)H oxidase-mediated superoxide production in renovascular hypertension: evidence for an involvement of protein kinase C. , 1999, Kidney international.

[39]  J. Keaney,et al.  Ascorbic Acid Enhances Endothelial Nitric-oxide Synthase Activity by Increasing Intracellular Tetrahydrobiopterin* , 2000, The Journal of Biological Chemistry.

[40]  T. Rabelink,et al.  Tetrahydrobiopterin regulates superoxide and nitric oxide generation by recombinant endothelial nitric oxide synthase. , 1997, Biochemical and biophysical research communications.

[41]  H Ishii,et al.  Xanthine oxidase activity associated with arterial blood pressure in spontaneously hypertensive rats. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  R W Alexander,et al.  Angiotensin II induces vascular cell adhesion molecule-1 expression in rat vasculature: A potential link between the renin-angiotensin system and atherosclerosis. , 1999, Circulation.

[43]  M. Ushio-Fukai,et al.  p22phox Is a Critical Component of the Superoxide-generating NADH/NADPH Oxidase System and Regulates Angiotensin IIinduced Hypertrophy in Vascular Smooth Muscle Cells* , 1996, The Journal of Biological Chemistry.

[44]  J. Mehta,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. , 1999, Circulation research.

[45]  S. Rajagopalan,et al.  p22phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. , 1997, Circulation research.

[46]  S. Rajagopalan,et al.  Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. , 1997, Circulation.

[47]  D. O'Connor,et al.  Plasma hydrogen peroxide production in hypertensives and normotensive subjects at genetic risk of hypertension , 1998, Journal of hypertension.

[48]  A. Takeshita,et al.  Pathogenic role of oxidative stress in vascular angiotensin-converting enzyme activation in long-term blockade of nitric oxide synthesis in rats. , 1999, Hypertension.

[49]  D. Harrison,et al.  Vascular superoxide production and vasomotor function in hypertension induced by deoxycorticosterone acetate-salt. , 2000, Circulation.

[50]  G. Ferns,et al.  Effect of vitamin C on ambulatory blood pressure and plasma lipids in older persons , 2000, Journal of hypertension.

[51]  W. Welch,et al.  Normalization of blood pressure and renal vascular resistance in SHR with a membrane-permeable superoxide dismutase mimetic: role of nitric oxide. , 1998, Hypertension.

[52]  M. Runge,et al.  Angiotensin II induces interleukin-6 transcription in vascular smooth muscle cells through pleiotropic activation of nuclear factor-kappa B transcription factors. , 1999, Circulation research.

[53]  A. Dominiczak,et al.  Investigation into the sources of superoxide in human blood vessels: angiotensin II increases superoxide production in human internal mammary arteries. , 2000, Circulation.

[54]  C. Kunsch,et al.  Oxidative stress as a regulator of gene expression in the vasculature. , 1999, Circulation research.

[55]  L. Ghiadoni,et al.  Vitamin C improves endothelium-dependent vasodilation by restoring nitric oxide activity in essential hypertension. , 1998, Circulation.

[56]  A. Dominiczak,et al.  Superoxide anion production is increased in a model of genetic hypertension: role of the endothelium. , 1999, Hypertension.

[57]  J. Keaney,et al.  Treatment of hypertension with ascorbic acid , 1999, The Lancet.

[58]  D. Harrison,et al.  Endothelial Regulation of Vasomotion in ApoE-Deficient Mice: Implications for Interactions Between Peroxynitrite and Tetrahydrobiopterin , 2001, Circulation.

[59]  D. L. Wang,et al.  Cyclic strain-induced reactive oxygen species involved in ICAM-1 gene induction in endothelial cells. , 1998, Hypertension.

[60]  D. Webb,et al.  Inhibition of nitric oxide synthesis increases blood pressure in healthy humans , 1993, Journal of hypertension.

[61]  W. Gonzalez,et al.  Angiotensin II stimulates endothelial vascular cell adhesion molecule-1 via nuclear factor-kappaB activation induced by intracellular oxidative stress. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[62]  T. Lüscher,et al.  Pulsatile stretch stimulates superoxide production in human aortic endothelial cells. , 1997, Circulation.

[63]  B. Hornig,et al.  Vitamin C improves endothelial dysfunction of epicardial coronary arteries in hypertensive patients. , 1997, Circulation.

[64]  O. Griffith,et al.  Mammalian nitric oxide synthases. , 1999, Advances in enzymology and related areas of molecular biology.

[65]  A. Deng,et al.  Chronic blockade of nitric oxide synthesis in the rat produces systemic hypertension and glomerular damage. , 1992, The Journal of clinical investigation.

[66]  A. Kashiwagi,et al.  Abnormal biopterin metabolism is a major cause of impaired endothelium-dependent relaxation through nitric oxide/O2- imbalance in insulin-resistant rat aorta. , 1999, Diabetes.

[67]  J. Holtz,et al.  Angiotensin II induces LOX-1, the human endothelial receptor for oxidized low-density lipoprotein. , 1999, Circulation.

[68]  D. O'Connor,et al.  Plasma Hydrogen Peroxide Production in Human Essential Hypertension: Role of Heredity, Gender, and Ethnicity , 2000, Hypertension.

[69]  E. Werner,et al.  l-Ascorbic Acid Potentiates Endothelial Nitric Oxide Synthesis via a Chemical Stabilization of Tetrahydrobiopterin* , 2001, The Journal of Biological Chemistry.

[70]  S. Snyder,et al.  Generation of superoxide by purified brain nitric oxide synthase. , 1992, The Journal of biological chemistry.