Molecular Mechanisms of Hypertension-Reactive Oxygen Species and Antioxidants: A Basic Science Update for the Clinician

Canadian Journal of Cardiology

Volumn 28, Issue 3, 2012, Pages 288-295

  Montezano, Augusto C ^a   Touyz, Rhian M ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ANTIOXIDANT; ASCORBIC ACID; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; BETA CAROTENE; BILIRUBIN; CALCIUM CHANNEL BLOCKING AGENT; CANDESARTAN; CAPTOPRIL; CARVEDILOL; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; NEBIVOLOL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDOREDUCTASE INHIBITOR; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 5; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE INHIBITOR; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; XANTHINE OXIDASE; ZINC;

ANGIOGENESIS; ANTIOXIDANT ACTIVITY; APOPTOSIS; BLOOD PRESSURE REGULATION; BLOOD VESSEL TONE; BODY MASS; CARDIOVASCULAR RISK; CARDIOVASCULAR SYSTEM; CELL METABOLISM; CELL MIGRATION; CELL PROLIFERATION; ENDOTHELIUM CELL; ENZYME ACTIVITY; HEART FUNCTION; HEART MUSCLE FIBROSIS; HUMAN; HYPERTENSION; HYPERTROPHY; INFLAMMATION; INSULIN SENSITIVITY; KIDNEY INJURY; LIPID PEROXIDATION; MOLECULAR MECHANICS; NERVOUS SYSTEM; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PROTEINURIA; RENAL SYSTEM PARAMETERS; REVIEW; VASCULAR RESISTANCE; WATER RETENTION;

ANIMALS; ANTIHYPERTENSIVE AGENTS; ANTIOXIDANTS; CARDIOVASCULAR DISEASES; DISEASE MODELS, ANIMAL; HUMANS; HYPERTENSION; MOLECULAR BIOLOGY; OXIDATIVE STRESS; PROGNOSIS; REACTIVE OXYGEN SPECIES; RISK ASSESSMENT; TREATMENT OUTCOME;

EID: 84860918905     PISSN: 0828282X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cjca.2012.01.017     Document Type: Review

References (99)

1. Wilkins K., Campbell N.R.C., Joffres M.R., et al. Blood pressure in Canadian adults. Statistics Canada 2010, 21.
2. Chobanian A.V. Mixed messages on blood pressure goals. Hypertension 2011, 57:1039-1040.
3. Savoia C., Burger D., Nishigaki N., Montezano A., Touyz R.M. Angiotensin II and the vascular phenotype in hypertension. Expert Rev Mol Med 2011, 13:e11.
4. Belmonte S.L., Blaxall B.C. G protein coupled receptor kinases as therapeutic targets in cardiovascular disease. Circ Res 2011, 109:309-319.
5. Zubcevic J., Waki H., Raizada M.K., Paton J.F. Autonomic-immune-vascular interaction: an emerging concept for neurogenic hypertension. Hypertension 2011, 57:1026-1033.
6. Muller D.N., Kvakan H., Luft F.C. Immune-related effects in hypertension and target-organ damage. Curr Opin Nephrol Hypertens 2011, 20:113-117.
7. Sugamura K., Keaney J.F. Reactive oxygen species in cardiovascular disease. Free Radic Biol Med 2011, 51:978-992.
8. Puddu P., Puddu G.M., Cravero E., Rosati M., Muscari A. The molecular sources of reactive oxygen species in hypertension. Blood Press 2008, 17:70-77.
9. Forman H.J., Fukuto J.M., Miller T., et al. The chemistry of cell signaling by reactive oxygen and nitrogen species and 4-hydroxynonenal. Arch Biochem Biophys 2008, 477:183-195.
10. Jacob C., Jamier V., Ba L.A. Redox active secondary metabolites. Curr Opin Chem Biol 2011, 15:149-155.
11. Förstermann U. Oxidative stress in vascular disease: causes, defense mechanisms and potential therapies. Nat Clin Pract Cardiovasc Med 2008, 5:338-349.
12. Touyz R.M. Reactive oxygen species as mediators of calcium signaling by angiotensin II: implications in vascular physiology and pathophysiology. Antioxid Redox Signal 2005, 7:1302-1314.
13. Romanowskia A., Murray J.R., Huston M.J. Effects of hydrogen peroxide on normal and hypertensive rats. Pharm Acta Helv 1960, 35:354-357.
14. Nakazono K., Watanabe N., Matsuno K., et al. Does superoxide underlie the pathogenesis of hypertension?. Proc Natl Acad Sci U S A 1991, 88:10045-10048.
15. Rajagopalan S., Kurz S., Münzel 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, 97:1916-1923.
16. Bhatia K., Elmarakby A.A., El-Remessey A., Sullivan J.C. Oxidative stress contributes to sex differences in angiotensin II-mediated hypertension in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 2012, 302:R274-R282.
17. Jia Z., Aoyagi T., Yang T. mPGES-1 protects against DOCA-salt hypertension via inhibition of oxidative stress or stimulation of NO/cGMP. Hypertension 2010, 55:539-546.
18. Grande M.T., Pascual G., Riolobos A.S., et al. Increased oxidative stress, the renin-angiotensin system, and sympathetic overactivation induce hypertension in kidney androgen-regulated protein transgenic mice. Free Radic Biol Med 2011, 51:1831-1841.
19. Haque M.Z., Majid D.S. High salt intake delayed angiotensin II-induced hypertension in mice with a genetic variant of NADPH oxidase. Am J Hypertens 2011, 24:114-118.
20. Grote K., Ortmann M., Salguero G., et al. Critical role for p47phox in renin-angiotensin system activation and blood pressure regulation. Cardiovasc Res 2006, 71:596-605.
21. Lob H.E., Vinh A., Li L., et al. Role of vascular extracellular superoxide dismutase in hypertension. Hypertension 2011, 58:232-237.
22. Franco M.C., Kawamoto E.M., Gorjão R., et al. Biomarkers of oxidative stress and antioxidant status in children born small for gestational age: evidence of lipid peroxidation. Pediatr Res 2007, 62:204-208.
23. Cottone S., Mulè G., Guarneri M., et al. Endothelin-1 and F2- isoprostane relate to and predict renal dysfunction in hypertensive patients. Nephrol Dial Transplant 2009, 24:497-503.
24. Nishino T., Okamoto K., Eger B.T., Pai E.F., Nishino T. Mammalian xanthine oxidoreductase - mechanism of transition from xanthine dehydrogenase to xanthine oxidase. FEBS J 2008, 275:3278-3289.
25. Adlam D., Bendall J.K., De Bono J.P., et al. Relationships between nitric oxide-mediated endothelial function, eNOS coupling and blood pressure revealed by eNOS-GTP cyclohydrolase 1 double transgenic mice. Exp Physiol 2007, 92:119-126.
26. Sedeek M., Hébert R.L., Kennedy C.R., Burns K.D., Touyz R.M. Molecular mechanisms of hypertension: role of Nox family NADPH oxidases. Curr Opin Nephrol Hypertens 2009, 18:122-127.
27. Geiszt M. NADPH oxidases: new kids on the block. Cardiovasc Res 2006, 71:289-299.
28. Bedard K., Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007, 87:245-313.
29. Touyz R.M., Chen X., Tabet F., et al. Expression of a functionally active gp91phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ Res 2002, 90:1205-1213.
30. Briones A.M., Tabet F., Callera G.E., et al. Differential regulation of Nox1, Nox2 and Nox4 in vascular smooth muscle cells from WKY and SHR. J Am Soc Hypertens 2011, 5. 137-5.
31. Xue B., Beltz T.G., Yu Y., et al. Central interactions of aldosterone and angiotensin II in aldosterone- and angiotensin II- induced hypertension. Am J Physiol Heart Circ Physiol 2011, 300:H555-H564.
32. Montezano A.C., Burger D., Ceravolo G.S., et al. Novel Nox homologues in the vasculature: focusing on Nox4 and Nox5. Clin Sci (Lond) 2011, 120:131-141.
33. Katsuyama M. NOX/NADPH oxidase, the superoxide-generating enzyme: its transcriptional regulation and physiological roles. J Pharmacol Sci 2010, 114:134-146.
34. Lassègue B., Griendling K.K. NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb Vasc Biol 2010, 30:653-661.
35. Gongora M.C., Qin Z., Laude K., et al. Role of extracellular superoxide dismutase in hypertension. Hypertension 2006, 48:473-481.
36. Chen X., Touyz R.M., Park J.B., Schiffrin E.L. Antioxidant effects of vitamins C and E are associated with altered activation of vascular NADPH oxidase and superoxide dismutase in stroke-prone SHR. Hypertension 2001, 38:606-611.
37. Redon J., Oliva M.R., Tormos C., et al. Antioxidant activities and oxidative stress byproducts in human hypertension. Hypertension 2003, 41:1096-1101.
38. Fridovich I. Superoxide anion radical (O2-.), superoxide dismutases, and related matters. J Biol Chem 1997, 272:18515-18517.
39. Fukai T., Ushio-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 2011, 15:1583-1606.
40. Goyal M.M., Basak A. Human catalase: looking for complete identity. Protein Cell 2010, 1:888-897.
41. Traber M.G., Stevens J.F. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic Biol Med 2011, 51:1000-1013.
42. Nagao A. Absorption and metabolism of dietary carotenoids. Biofactors 2011, 37:83-87.
43. Lin J.P., Vitek L., Schwertner H.A. Serum bilirubin and genes controlling bilirubin concentrations as biomarkers for cardiovascular disease. Clin Chem 2010, 56:1535-1543.
44. Schwertner H.A., Vítek L. Gilbert syndrome, UGT1A1*28 allele, and cardiovascular disease risk: possible protective effects and therapeutic applications of bilirubin. Atherosclerosis 2008, 198:1-11.
45. Kizhakekuttu T.J., Widlansky M.E. Natural antioxidants and hypertension: promise and challenges. Cardiovasc Ther 2010, 28:e20-e32.
46. Al Ghouleh I., Khoo N.K., Knaus U.G., et al. Oxidases and peroxidases in cardiovascular and lung disease: new concepts in reactive oxygen species signaling. Free Radic Biol Med 2011, 51:1271-1288.
47. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2002, 82:47-95.
48. Zinkevich N.S., Gutterman D.D. ROS-induced ROS release in vascular biology: redox-redox signaling. Am J Physiol Heart Circ Physiol 2011, 301:H647-H653.
49. Touyz R.M., Briones A.M. Reactive oxygen species and vascular biology: implications in human hypertension. Hypertens Res 2011, 34:5-14.
50. Lee M.Y., Griendling K.K. Redox signaling, vascular function, and hypertension. Antioxid Redox Signal 2008, 10:1045-1059.
51. Wilcox C.S. Oxidative stress and nitric oxide deficiency in the kidney: a critical link to hypertension?. Am J Physiol Regul Integr Comp Physiol 2005, 289:R913-R935.
52. Purushothaman S., Renuka Nair R., Harikrishnan V.S., Fernandez A.C. Temporal relation of cardiac hypertrophy, oxidative stress, and fatty acid metabolism in spontaneously hypertensive rat. Mol Cell Biochem 2011, 351:59-64.
53. Viel E.C., Benkirane K., Javeshghani D., Touyz R.M., Schiffrin E.L. Xanthine oxidase and mitochondria contribute to vascular superoxide anion generation in DOCA-salt hypertensive rats. Am J Physiol Heart Circ Physiol 2008, 295:H281-H288.
54. Virdis A., Neves M.F., Amiri F., Touyz R.M., Schiffrin E.L. Role of NADPH oxidase on vascular alterations in angiotensin II-infused mice. J Hypertens 2004, 22:535-542.
55. Harrison D.G., Gongora M.C. Oxidative stress and hypertension. Med Clin North Am 2009, 93:621-635.
56. Rivera J., Sobey C.G., Walduck A.K., Drummond G.R. Nox isoforms in vascular pathophysiology: insights from transgenic and knockout mouse models. Redox Rep 2010, 15:50-63.
57. Murdoch C.E., Alom-Ruiz S.P., Wang M., et al. Role of endothelial Nox2 NADPH oxidase in angiotensin II-induced hypertension and vasomotor dysfunction. Basic Res Cardiol 2011, 106:527-538.
58. Rey F.E., Cifuentes M.E., Kiarash A., Quinn M.T., Pagano P.J. Novel competitive inhibitor of NADPH oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice. Circ Res 2001, 89:408-414.
59. Dorfmüller P., Chaumais M.C., Giannakouli M., et al. Increased oxidative stress and severe arterial remodeling induced by permanent high-flow challenge in experimental pulmonary hypertension. Respir Res 2011, 12:119.
60. Nuyt A.M. Mechanisms underlying developmental programming of elevated blood pressure and vascular dysfunction: evidence from human studies and experimental animal models. Clin Sci (Lond) 2008, 114:1-17.
61. Török J. Participation of nitric oxide in different models of hypertension. Physiol Res 2008, 57:813-825.
62. Wilcox C.S. Effects of tempol and redox-cycling nitroxides in models of oxidative stress. Pharmacol Ther 2010, 126:119-145.
63. Rodrigo R., Prat H., Passalacqua W., et al. Relationship between oxidative stress and essential hypertension. Hypertens Res 2007, 30:1159-1167.
64. Ward N.C., Hodgson J.M., Puddey I.B., et al. Oxidative stress in human hypertension: association with antihypertensive treatment, gender, nutrition, and lifestyle. Free Radic Biol Med 2004, 36:226-232.
65. Raijmakers M.T., Dechend R., Poston L. Oxidative stress and preeclampsia: rationale for antioxidant clinical trials. Hypertension 2004, 44:374-380.
66. Chen K., Xie F., Liu S., et al. Plasma reactive carbonyl species: potential risk factor for hypertension. Free Radic Res 2011, 45:568-574.
67. Murphey L.J., Morrow J.D., Sawathiparnich P., et al. Acute angiotensin II increases plasma F2-isoprostanes in salt-replete human hypertensives. Free Radic Biol Med 2003, 35:711-718.
68. Yasunari K., Maeda K., Nakamura M., Yoshikawa J. Oxidative stress in leukocytes is a possible link between blood pressure, blood glucose, and C-reactive protein. Hypertension 2002, 39:777-780.
69. Lacy F., O'Connor D.T., Schmid-Schönbein G.W. Plasma hydrogen peroxide production in hypertensives and normotensive subjects at genetic risk of hypertension. J Hypertens 1998, 16:291-303.
70. Lacy F., Kailasam M.T., O'Connor D.T., Schmid-Schonbein G.W., Parmer R.J. Plasma hydrogen peroxide production in human essential hypertension: role of heredity, gender, and ethnicity. Hypertension 2000, 36:878-884.
71. Wang D., Strandgaard S., Iversen J., Wilcox C.S. Asymmetric dimethylarginine, oxidative stress, and vascular nitric oxide synthase in essential hypertension. Am J Physiol Regul Integr Comp Physiol 2009, 296:R195-R200.
72. Touyz R.M., Schiffrin E.L. Increased generation of superoxide by angiotensin II in smooth muscle cells from resistance arteries of hypertensive patients: role of phospholipase D-dependent NADPH oxidase-sensitive pathways. J Hypertens 2001, 19:1245-1254.
73. San José G., Fortuño A., Beloqui O., Díez J., Zalba G. NADPH oxidase CYBA polymorphisms, oxidative stress and cardiovascular diseases. Clin Sci (Lond) 2008, 114:173-182.
74. Sugiura T., Dohi Y., Takase H., et al. Increased reactive oxygen metabolites is associated with cardiovascular risk factors and vascular endothelial damage in middle-aged Japanese subjects. Vasc Health Risk Manag 2011, 7:475-482.
75. Patel R.S., Al Mheid I., Morris A.A., et al. Oxidative stress is associated with impaired arterial elasticity. Atherosclerosis 2011, 218:90-96.
76. Simic D.V., Mimic-Oka J., Pljesa-Ercegovac M., et al. Byproducts of oxidative protein damage and antioxidant enzyme activities in plasma of patients with different degrees of essential hypertension. J Hum Hypertens 2006, 20:149-155.
77. Caner M., Karter Y., Uzun H., et al. Oxidative stress in human sustained and white coat hypertension. Int J Clin Pract 2006, 60:1565-1571.
78. Schiffrin E.L. Antioxidants in hypertension and cardiovascular disease. Mol Interv 2010, 10:354-362.
79. Hasnain B.I., Mooradian A.D. Recent trials of antioxidant therapy: what should we be telling our patients?. Cleve Clin J Med 2004, 71:327-334.
80. Houston M.C. The role of cellular micronutrient analysis, nutraceuticals, vitamins, antioxidants and minerals in the prevention and treatment of hypertension and cardiovascular disease. Ther Adv Cardiovasc Dis 2010, 4:165-183.
81. Duffy S.J., Gokce N., Holbrook M., et al. Treatment of hypertension with ascorbic acid. Lancet 1999, 354:2048-2049.
82. Ward N.C., Hodgson J.M., Croft K.D., et al. The combination of vitamin C and grape seed polyphenols increases blood pressure: a randomized, double-blind, placebo-controlled trial. J Hypertens 2005, 23:427-434.
83. Barbagallo M., Dominguez L.J., Tagliamonte M.R., Resnick L.M., Paolisso G. Effects of vitamin E and glutathione on glucose metabolism: role of magnesium. Hypertension 1999, 34:1002-1006.
84. Rossi A.C., Mullin P.M. Prevention of pre-eclampsia with low-dose aspirin or vitamins C and E in women at high or low risk: a systematic review with meta- analysis. Eur J Obstet Gynecol Reprod Biol 2011, 158:9-16.
85. Kizhakekuttu T.J., Widlansky M.E. Natural antioxidants and hypertension: promise and challenges. Cardiovasc Ther 2010, 28:e20-e32.
86. Gori T., Münzel T. Oxidative stress and endothelial dysfunction: therapeutic implications. Ann Med 2011, 43:259-272.
87. Talaulikar V.S., Manyonda I.T. Vitamin C as an antioxidant supplement in women's health: a myth in need of urgent burial. Eur J Obstet Gynecol Reprod Biol 2011, 157:10-13.
88. Farbstein D., Kozak-Blickstein A., Levy A.P. Antioxidant vitamins and their use in preventing cardiovascular disease. Molecules 2010, 15:8098-8110.
89. Drummond G.R., Selemidis S., Griendling K.K., Sobey C.G. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat Rev Drug Discov 2011, 10:453-471.
90. Kim J.A., Neupane G.P., Lee E.S., et al. NADPH oxidase inhibitors: a patent review. Expert Opin Ther Pat 2011, 21:1147-1158.
91. Gupte S.A. Targeting the pentose phosphate pathway in Syndrome X-related cardiovascular complications. Drug Dev Res 2010, 71:161-167.
92. Van Assche T., Huygelen V., Crabtree M.J. Targeting vascular redox biology through antioxidant gene delivery: a historical view and current perspectives. Recent Pat Cardiovasc Drug Discov 2011, 6:89-102.
93. Rabi D.M., Daskalopoulou S.S., Padwal R.S., et al. The 2011 Canadian Hypertension Education Program recommendations for the management of hypertension: blood pressure measurement, diagnosis, assessment of risk, and therapy. Can J Cardiol 2011, 27:415-433.
94. Lopes H.F., Martin K.L., Nashar K., et al. DASH diet lowers blood pressure and lipid-induced oxidative stress in obesity. Hypertension 2003, 41:422-430.
95. Agarwal D., Welsch M.A., Keller J.N., Francis J. Chronic exercise modulates RAS components and improves balance between pro- and anti-inflammatory cytokines in the brain of SHR. Basic Res Cardiol 2011, 106:1069-1085.
96. Adams V., Linke A., Krankel N., et al. Impact of regular physical activity on the NADPH oxidase and angiotensin receptor system in patients with coronary artery disease. Circulation 2005, 111:555-560.
97. Whaley-Connell A., Habibi J., Johnson M., et al. Nebivolol reduces proteinuria and renal NADPH oxidase-generated reactive oxygen species in the transgenic Ren2 rat. Am J Nephrol 2009, 30:354-360.
98. Chen S., Ge Y., Si J., et al. Candesartan suppresses chronic renal inflammation by a novel antioxidant action independent of AT1R blockade. Kidney Int 2008, 74:1128-1138.
99. Weseler A.R., Bast A. Oxidative stress and vascular function: implications for pharmacologic treatments. Curr Hypertens Rep 2010, 12:154-161.