Redox signaling, Nox5 and vascular remodeling in hypertension

Current Opinion in Nephrology and Hypertension

Volumn 24, Issue 5, 2015, Pages 425-433

  Montezano, Augusto C ^a   Tsiropoulou, Sofia ^a   Dulak Lis, Maria ^a   Harvey, Adam ^a   De Lucca Camargo, Livia ^a   Touyz, Rhian M ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

NADPH oxidase; Oxidative post translational modification; Reactive oxygen species; Vascular smooth muscle cells

Indexed keywords

ANTIOXIDANT; NOX5 PROTEIN; OXIDOREDUCTASE INHIBITOR; PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; NOX5 PROTEIN, HUMAN;

ANTIOXIDANT ACTIVITY; BIOAVAILABILITY; BLOOD VESSEL TONE; BLOOD VESSEL WALL; CARDIOVASCULAR SYSTEM; CELL FUNCTION; CELL GROWTH; CLINICAL TRIAL (TOPIC); GLUTATHIONYLATION; HUMAN; HYPERTENSION; NITROSYLATION; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SULFENYLATION; SULFYDRATION; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; DRUG EFFECTS; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANIMALS; HUMANS; HYPERTENSION; MEMBRANE PROTEINS; NADPH OXIDASE; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; VASCULAR REMODELING;

EID: 84942599150     PISSN: 10624821     EISSN: 14736543     Source Type: Journal    
DOI: 10.1097/MNH.0000000000000153     Document Type: Review

References (92)

1. Brown DI, Griendling KK. Regulation of signal transduction by reactive oxygen species in the cardiovascular system. Circ Res 2015; 116:531-549.
2. Montezano AC, Touyz RM. Reactive oxygen species, vascular Noxs, and hypertension: focus on translational and clinical research. Antioxid Redox Signal 2014; 20:164-182.
3. Al Ghouleh I, Khoo NK, Knaus UG, et al. Oxidases and peroxidases in cardiovascular and lung d isease: new concepts in reactive oxygen species signalling. Free Radic Biol Med 2011; 51:1271-1288.
4. Salabei JK, Hill BG. Autophagic regulation of smooth muscle cell biology. Redox Biol 2015; 4:97-103. 5.
5. MacKay CE, Knock GA. Control of vascular smooth muscle function by Srcfamily kinases and reactive oxygen species in health and disease. J Physiol 2014. An excellent overview linking molecular mechanism w hereby ROS and redox signaling network with the Src family kinases.
6. Lee SE, Park-S. Role of lipid peroxidation-derived a, b-unsaturated aldehydes in vascular dysfunction. Oxid Med Cell Longev 2013; 2013:629028.
7. Sinha N, Dabla PK. Oxidative stress and antioxidants in hypertension: a current review. Curr Hypertens Rev 2015; May 29. [Epub ahead of print]
8. Lee MY, Griendling KK. Redox s ignaling, vascular function, and hypertension. Antioxid Redox Signal 2008; 10:1045-1059.
9. Fridovich I. Superoxide anion radical, superoxide dismutases, and related matters. J Biol Chem 1997; 272:18515-18517.
10. Fukai T,Ushio-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases Antioxid Redox Signal 2011 15 1583-1606.
11. Cantu-Medellin N, Kelley EE. Xanthine oxidoreductase-catalyzed reactive species generation: a process in critical need of reevaluation. Redox Biol 2013; 1:353-358.
12. Montezano AC, Touyz RM. R eactive oxygen species and endothelial function: role of nitric oxide synthase uncoupling and Nox family nicotinamide adenine dinucleotide phosphate oxidases. Basic Clin Pharmacol Toxicol 2012; 110:87-94.
13. Dikalov SI, Ungvari Z. Role of mitochondrial oxidative stress in hypertension. Am J Physiol Heart Circ Physiol 2013; 305:H1417-H1422.
14. Laurindo FR, Araujo TL, Abrahão TB. Nox NADPH oxidases and the endoplasmic reticulum. Antioxid Redox Signal 2014; 20:2755-2775.
15. Brandes RP, Weissmann N, Schröder K. Nox family NADPH oxidases in mechano-transduction: mechanisms and consequences. Antioxid Redox Signal 2014; 20:887-898.
16. Montezano AC, Nguyen Dinh Cat A, Rios FJ, Touyz RM. Angiotensin II and vascular injury. Curr Hypertens Rep 2014; 16:431.
17. Raaz U, Toh R, Maegdefessel L, et al. Hemodynamic regulation of reactive oxygen species: implications for vascular diseases. Antioxid Redox Signal 2014; 20:914-928.
18. Briones AM, Tabet F, Callera GE, et al. Differential regulation of Nox1, Nox2 and Nox4 in vascular smooth muscle cells from WKY and SHR. J Am Soc Hypertens 2011; 5:137-153.
19. Konior A, Schramm A, Czesnikiewicz-Guzik M, Guzik TJ. NADPH oxidases in vascular pathology. Antioxid Redox Signal 2014; 20:2794-2814.
20. Montezano AC, Dulak-Lis M, Tsiropoulou S, et al. Oxidative stress and human hypertension: vascular mechanisms, biomarkers, and novel therapies. Can J Cardiol 2015; 31:631-641.
21. . Kaludercic N, Deshwal S, Di Lisa F. Reactive oxygen species and redox compartmentalization. Front Physiol 2014; 5:285.
22. Barman SA, Chen F, Su Y, et al. NADPH oxidase 4 is e xpressed in pulmonary artery adventitia and contributes to hypertensive vascular remodeling. Arterioscler Thromb Vasc Biol 2014; 34:1704-1715.
23. Montezano AC, Burger D, Paravicini TM, et al. N icotinamide adenine dinucleotide phosphate reduced oxidase 5 (Nox5) regulation by angiotensin II and endothelin-1 is mediated via calcium/calmodulin-dependent, rac-1-independent pathways in human endothelial cells. Circ Res 2010; 106:1363-1373.
24. Montezano AC, Touyz RM. Oxidative stress, Noxs, and hypertension: experimental evidence and clinical controversies. Ann Med 2012; 44:S2-S16.
25. Rivera J, Sobey CG, Walduck AK, Drummond GR. Nox isoforms in vascular pathophysiology: insights from transgenic and knockout mouse models. Redox Rep 2010; 15:50-63.
26. San Martin A, Griendling KK. NADPH oxidases: progress and opportunities. Antioxid Redox Signal 2014; 20:2692-2694.
27. Santos CX, Nabeebaccus AA, Shah AM, et al. Endoplasmic reticulum stress and Nox-mediated reactive oxygen species signaling in the peripheral vasculature: potential role in hypertension. Antioxid Redox Signal 2 014; 20:121-134.
28. Pandey D, Fulton DJ. Molecular regulation of NADPH oxidase 5 via the MAPK pathway. Am J Physiol Heart Circ Physiol 2011; 300:H1336-H1344.
29. Qian J, Chen F, Kovalenkov Y, et al. Nitric oxide reduces NADPH oxidase 5 (Nox5) activity by reversible S-nitrosylation. Free Radic Biol Med 2012; 52:1806-1819.
30. Hahn NE, Meischl C, K awahara T, et al. NOX5 expression is increased in intramyocardial blood vessels and cardiomyocytes after acute myocardial infarction in humans. Am J Pathol 2012; 180:2222-2229.
31. Guzik TJ,Chen W,Gongora MC,et al. Calcium dependent NOX5 nicotinamide adenine dinucleotide phosphate oxidase contributes to vascular oxidative stress in human coronary artery disease J Am Coll Cardiol 2008, 52, 1803-1809.
32. Chen F, Yu Y, Haigh S, et al. Regulation of NADPH oxidase 5 by protein kinase C isoforms. Plos One 2014; 9:e88405. This study advances the field of Nox5 biology by demonstrating mechanisms whereby kin ases, specifically PKC, regulate activity of Nox5.
33. El Jamali A, Valente AJ, Lechleiter JD, et al. Novel redox-dependent regulation of NOX5 by the tyrosine kinase c-Abl. Free Radic Biol Med 2008; 44:868-881.
34. Chen F, Pandey D, Chadli A, et al. Hsp90 regulates NADPH oxidase activity and is necessary for superoxide but not hydrogen peroxide production. Antioxid Redox Signal 2011; 14:2107-2119.
35. Bedard K, Jaquet V, Krause KH. NOX5: from basic biology to signaling and disease. Free Radic Biol Med 2012; 52:725-734.
36. Serrander L, Jaquet V, Beda rd K, et al. NOX5 is expressed at the plasma membrane and generates superoxide in response to protein kinase C activation. Biochimie 2007; 89:1159-1167.
37. Greco TM, Hodara R, Parastatidis I, et al. Identification of S-nitrosylation motifs by site specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells. Proc Natl Acad Sci USA 2006; 103:7420-7425.
38. Pandey D, Patel A, Patel V, et al. Expression and functional significance of NADPH oxidase 5 (Nox5) and its splice variants in human blood vessels. Am J Physiol Heart Circ Physiol 2012; 302:H1919-H1928.
39. Gole Hope K A, Tharp Darla L, Bowles Douglas K. Upregulation of intermediate-conductance Ca2+-Activated K+ channels (KCNN4) in porcine coronary smooth muscle requires NADPH oxidase 5 (NOX5). Plos One 2014; 9:e105337.
40. Fulton DJ. Nox5 and the regulation of cellular function. Antioxid Redox Signal 2009; 11:2443-2452.
41. Yu P, Han W, Villar VA, et al. Unique role of NADPH oxidase 5 in oxidative stress in human renal proximal tubule cells. Redox Biol 2014; 2:570-579.
42. Manea A, Manea SA, Gan AM, et al. Human monocytes and macrophages express NADPH oxidase 5; a potential s ource of reactive oxygen species in atherosclerosis. Biochem Biophys Res Commun 2015; 461:172-179.
43. Holterman CE, Thibodeau JF, Towaij C, et al. Nephropathy and elevated BP in mice with podocyte-sp ecific NADPH oxidase 5 expression. J Am Soc Nephrol 2014; 25:784-797. The first study to show that renal (podocyte) Nox5 plays an important role in renal dysfunction and hypertension. This study was performed in mice expressing human Nox5 in a podocyte-specific manner.
44. Madamanchi NR, Runge MS. Redox signaling in cardiovascular health and disease. Free Radic Biol Med 2013; 61:473-501.
45. Chatterjee S, Fujiwara K, Perez NG, et al. Mechanosignaling in the vasculature: emerging concepts in sensing, transduction and physiological responses. Am J Physiol Heart Circ Physiol 2015; 308: (in press).
46. T homas SR, Witting PK, Drummond GR. Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities. Antioxid Redox Signal 2008; 10:1713-1765.
47. Androwiki A C, Camargo Lde L, Sartoretto S, et al. Protein disulfide isomerase expression increases in resistance arteries during hypertension development. Effects on Nox1 NADPH oxidase signaling. Front Chem 2015; 3:24-28.
48. Chung HS, Wang S-B, Venkatraman V, et al. Cysteine oxidative posttranslational modifications emerging regulation in the cardiovascular system. Circ Res 2013; 112:382-392.
49. Wang SB, Foster DB, Rucker J, et al. Redox regulation of mitochondrial ATP synthase: implications for cardiac resynchronization therapy. Circ Res 2011; 109:750-757.
50. Choi H, Allahdadi K J, Tostes RC, Webb RC. Augmented S-nitrosylation contributes to impaired relaxation in angiotensin II hypertensive mouse aorta: role of thioredoxinreductase. J Hypertens 2011; 29:2359-2368.
51. Yang G, Wu L, Jiang B, et al. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 2008; 322:587-590.
52. Murray CI, Kane LA, Uhrigshard t H, et al. Site mapping of in vitro S-nitrosation in cardiac mitochondria: implications for cardioprotection. Mol Cell Proteomics 2011; 10.
53. Wang X, Ling S, Zhao D, et al. Redox regulati on of actin by thioredoxin-1 is mediated by the interaction of the proteins via cysteine 62. Antioxid Redox Signal 2010; 13:565-573.
54. Krishnan N,Fu C,Pappin DJ,Tonks NK. H2S-induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response Sci Signal 2011 4:ra86.
55. Dalle-Donne I, Giustarini D, Colombo R, et al. S-glutathionylation in human platelets by a thiol-disulfide exchange independent mechanism. Free Radic Biol Med 2005; 38:1501-1510.
56. Oelze M, Kröller-Schön S, Steven S, et al. Glutathione peroxidase-1 deficiency potentiates dysregulatory modifications of endothelial nitric oxide synthase and vascular dysfunction in aging. Hypertension 2014; 63:390-396.
57. Zweier JL, Chen CA, Druhan LJ. S-glutathionylation reshapes our understanding of endothelial nitric oxide synthase uncoupling and nitric oxide/reactive oxygen species-mediated signaling. Antioxid Redox Sign al 2011; 14:1769-1775.
58. Mieyal JJ, Gallogly MM, Qanungo S, et al. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal 2008; 10:1941-1988.
59. Dalle-Donne I, Rossi R, Milzani A, et al. The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radic Biol Med 2001; 31:1624-1632.
60. Canton M, Menazza S, Sheeran FL, et al. Oxidation of myofibrillar proteins in human heart failure. J Am Coll Cardiol 2011; 57:300-309.
61. Bansal G, Das D, Hsieh CY, et al. IL-22 activates oxidant signaling in pulmonary vascular smooth muscle cells. Cell Signal 2013; 25:2727-2733.
62. Savoia C, Burger D, Nishigaki N, et al. Angiotensin II and the vascular phenotype in hypertension. Expert Rev Mol Med 2011; 13:e11.
63. Rao GN, Berk BC. Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression. Circ Res 1992; 70:593-599.
64. Tabet F, Schiffrin EL, Touyz RM. Mitogen-Activated protein kinase activation by hydrogen peroxide is mediated through tyrosine kinase-dependent, protein kinase C-independent pathways in vascular smooth muscle cells: upregulation in spontaneously hypertensive rats. J Hypert ens 2005; 23:2005-2012.
65. Knock GA, Ward JP. Redox regulation of protein kinases as a modulator of vascular function. Antioxid Redox Signal 2011; 15:1531-1547.
66. Touyz RM, Yao G, Viel E, et al. Angiotensin II and endothelin-1 regulate MAP kinases through different redox-dependent mechanisms in human vascular smooth muscle cells. J Hypertens 2004; 22:1141-1149.
67. Touyz RM, Cruzado M, Tabet F, et al. Redox-dependent MAP kinase signaling by Ang II in vascular smooth muscle cells: role of receptor tyrosine kinase transactivation. Can J Physiol Pharmacol 2003; 81:159-16 7.
68. Zhang X, Liu L, Chen C, et al. Interferon regulatory factor-1 together with reactive oxygen species promotes the acceleration of cell cycle progression by up-regulating the cyclin E and CDK2 genes during high glucose-induced proliferation of vascular smooth muscle cells. Cardiovasc Diabetol 2013; 12:147.
69. Kim TH, Oh S, Kim SS. Recombinant human prothrombin kringle-2 induces bovine capillary endothelial cell cycle arrest at G0-G1 phase through inhibition of cyclin D1/CDK4 complex: modulation of reactive oxygen species generat ion and up-regulation of cyclin-dependent kinase inhibitors. Angiogenesis 2005; 8:307-314.
70. Kim MH, Ham O, Lee SY, et al. MicroRNA-365 inhibits the proliferation of vascular smooth muscle cells by targeting cyclin D1. J Cell Biochem 2014; 115:1752-1761.
71. Barnouin K, Dubuisson ML, Child ES, et al. H2O2 induces a transient multiphase cell cycle arrest in mouse fibroblasts through mo dulating cyclin D and p21Cip1 expression. J Biol Chem 2002; 277:13761-13770.
72. Rizzoni D, Agabiti Rosei E. Small artery remodeling in hypertension and diabetes. Curr Hypertens Rep 2006; 8:90-95.
73. Schiffrin EL. Remodeling of resistance arteries in essential hypertension and effects of antihypertensive treatment. Am J Hypertens 2004; 17 (12 Pt 1): 1192-1200.
74. Liu B, Luo XJ, Yang ZB, et al. Inhibition of NOX/VPO1 pathway and inflammatory reaction by trimethoxystilbene in prevention of cardiovascular remodeling in hypoxia-induced pulmonary hypertensive rats. J Cardiovasc Pharmacol 20 14; 63:567-576.
75. Altenhöfer S, Radermacher KA, Kleikers PW, et al. Evolution of NADPH oxidase inhibitors: selectivity and mechanisms for target engagement. Antioxid Redox Signal 2014; Feb 26. [Epub ahead of print]
76. Drummond GR,Sobey CG Endothelial NADPH oxidases: which NOX to target in vascular disease Trends Endocrinol Metab 2014 25 452-463.
77. Sorce S, Krause KH, Jaquet V. Targeting NOX enzymes in the central nervous system: therapeutic opportunities. Cell Mol Life Sci 2012; 69:2387-2407.
78. Sato Y, Ikeda M, Ito T, et al. Ascorbic acid levels and neutrop hil superoxide production in blood of pre, early and late hypertensive stroke-prone spontaneously hypertensive rats. Clin Exp Hypertens 2011; 33:397-403.
79. Chen X, Touyz RM, Park JB, Schiffrin EL. 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 (3 Pt 2): 606-611.
80. Scioli MG, Bielli A, Agostinelli S, et al. Antioxidant treatment prevents serum deprivation-And TNF-A-induced endothelial dysfunction through the inhibition of NADPH oxidase 4 and the restoration of b-oxidation. J Vasc Res 2014; 51: 327-337; Kyaw M.
81. Yoshizumi M, Tsuchiya K, Izawa Y, et al. Atheroprotective effects of antioxidants through inhibition of mitogen-Activated protein kinases. Acta Pharmacol Sin 2004; 25:977-985.
82. Ashor AW, Siervo M, Lara J, et al. Effect of vitamin C and vitamin E supplementation on endothelial function: a systematic review and metaanalysis of randomised controlled trials. Br J Nutr 2015; 113:1182-1194.
83. Desai CK, Huang J, Lokhandwala A, et al. Antioxidants, inflammation and cardiovascular disease. World J Cardiol 2014; 6:462-477.
84. Tousoulis D, Psaltopoulou T, Androulakis E, et al. Oxidative stress and early atherosclerosis: novel antioxidant treatment. Cardiovasc Drugs Ther 2015; 29:75-88.
85. Mangge H , Becker K, Fuchs D, Gostner JM. The role of vitamin supplementation in the prevention of cardiovascular disease events. Clin Cardiol 2014; 37:576-578.
86. Paganini-Hill A, Kawas CH, Cor rada MM. Antioxidant vitamin intake and mortality: the Leisure World Cohort Study. Am J Epidemiol 2015; 181:120-126.
87. Bruder-Nascimento T, Callera GE, Montezano AC, et al. Vascular injur y in diabetic db/db mice is ameliorated by atorvastatin: role of Rac1/2-sensitive Nox-dependent pathways. Clin Sci (Lond) 2015; 128:411-423.
88. Sabuhi R, Asghar M, Hussain T. Inhibition of NAD(P)H oxidase potentiates AT2 receptor agonist-induced natriuresis in Sprague-Dawley rats. Am J Physiol Renal Physiol 2010; 299:F815-F820.
89. Heumüller S, Wind S, Barbosa-Sicard E, et al. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 2008; 51:211-217.
90. Cifuentes-Pagano E, Meijles DN, Pagano PJ. The quest for selective Nox inhibitors and therapeutics: challenge s, triumphs and pitfalls. Antioxid Redox Signal 2014; 20:2741-2754. A comprehensive update and critical review of Nox inhibitors, with a discussion about novel approaches to inhibit Nox isoforms.
91. Cifuentes-P agano E, Csanyi G, Pagano PJ. NADPH oxidase inhibitors: a decade of discovery from Nox2ds to HTS. Cell Mol Life Sci 2012; 69:2315-2325.
92. Go YM, Chandler JD, Jones DP. The cysteine proteome. Free Radic Biol Med 2015; 84:227-245.