Nox-derived ROS are acutely activated in pressure overload pulmonary hypertension: Indications for a seminal role for mitochondrial Nox4

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 306, Issue 2, 2014, Pages

  Frazziano, Giovanna ^a,c   Al Ghouleh, Imad ^a,b   Baust, Jeff ^a   Shiva, Sruti ^a,b   Champion, Hunter C ^a,b   Pagano, Patrick J ^a,b  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c Fondazione RiMED   (Italy)

Author keywords

NADPH oxidase; Pulmonary artery banding; Reactive oxygen species; Right ventricle

Indexed keywords

CATALASE; COMPLEMENTARY DNA; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION ASSAY; HEART LEFT VENTRICLE; HEART MITOCHONDRION; HEART RIGHT VENTRICLE; HEART RIGHT VENTRICLE FAILURE; HEART RIGHT VENTRICLE OVERLOAD; LUNG ARTERY BANDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PULMONARY ARTERY; PULMONARY HYPERTENSION; WESTERN BLOTTING;

NADPH OXIDASE; PULMONARY ARTERY BANDING; REACTIVE OXYGEN SPECIES; RIGHT VENTRICLE;

ANIMALS; CATALASE; GLUTATHIONE PEROXIDASE; HEART VENTRICLES; HYPERTENSION, PULMONARY; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MITOCHONDRIA; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SUPEROXIDE DISMUTASE; UP-REGULATION; VENTRICULAR DYSFUNCTION;

EID: 84892584303     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00977.2012     Document Type: Article

References (42)

1. Aebi H. Catalase in vitro. Methods Enzymol 105: 121-126, 1984.
2. Ago T, Matsushima S, Kuroda J, Zablocki D, Kitazono T, Sadoshima J. The NADPH oxidase Nox4 and aging in the heart. Aging (Albany NY) 2: 1012-1016, 2010.
3. Al Ghouleh I, Frazziano G, Rodriguez AI, Csanyi G, Maniar S, St Croix CM, Kelley EE, Egana LA, Song GJ, Bisello A, Lee YJ, Pagano PJ. Aquaporin 1, Nox1, and Ask1 mediate oxidant-induced smooth muscle cell hypertrophy. Cardiovasc Res 97: 134-142, 2013.
4. Al Ghouleh I, Khoo NK, Knaus UG, Griendling KK, Touyz RM, Thannickal VJ, Barchowsky A, Nauseef WM, Kelley EE, Bauer PM, Darley-Usmar V, Shiva S, Cifuentes-Pagano E, Freeman BA, Gladwin MT, Pagano PJ. Oxidases and peroxidases in cardiovascular and lung disease: new concepts in reactive oxygen species signaling. Free Radic Biol Med 51: 1271-1288, 2011.
5. Ambasta RK, Kumar P, Griendling KK, Schmidt HH, Busse R, Brandes RP. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J Biol Chem 279: 45935-45941, 2004.
6. Anilkumar N, Jose GS, Sawyer I, Santos CX, Sand C, Brewer AC, Warren D, Shah AM. A 28-kDa splice variant of NADPH oxidase-4 is nuclear-localized and involved in redox signaling in vascular cells. Arterioscler Thromb Vasc Biol 33: 104-112, 2013.
7. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313, 2007.
8. Bendall JK, Cave AC, Heymes C, Gall N, Shah AM. Pivotal role of a gp91(phox)-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation 105: 293-296, 2002.
9. Block K, Gorin Y, Abboud HE. Subcellular localization of Nox4 and regulation in diabetes. Proc Natl Acad Sci USA 106: 14385-14390, 2009.
10. Brandes RP, Weissmann N, Schroder K. NADPH oxidases in cardiovascular disease. Free Radic Biol Med 49: 687-706, 2010.
11. Brown DI, Griendling KK. Nox proteins in signal transduction. Free Radic Biol Med 47: 1239-1253, 2009.
12. Byrne JA, Grieve DJ, Bendall JK, Li JM, Gove C, Lambeth JD, Cave AC, Shah AM. Contrasting roles of NADPH oxidase isoforms in pressure-overload versus angiotensin II-induced cardiac hypertrophy. Circ Res 93: 802-805, 2003.
13. Champion HC, Michelakis ED, Hassoun PM. Comprehensive invasive and noninvasive approach to the right ventricle-pulmonary circulation unit: state of the art and clinical and research implications. Circulation 120: 992-1007, 2009.
14. Chen K, Kirber MT, Xiao H, Yang Y, Keaney JF Jr. Regulation of ROS signal transduction by NADPH oxidase 4 localization. J Cell Biol 181: 1129-1139, 2008.
15. Datla SR, Griendling KK. Reactive oxygen species, NADPH oxidases, and hypertension. Hypertension 56: 325-330, 2010.
16. Ecarnot-Laubriet A, Rochette L, Vergely C, Sicard P, Teyssier JR. The activation pattern of the antioxidant enzymes in the right ventricle of rat in response to pressure overload is of heart failure type. Heart Dis 5: 308-312, 2003.
17. Forfia PR, Fisher MR, Mathai SC, Housten-Harris T, Hemnes AR, Borlaug BA, Chamera E, Corretti MC, Champion HC, Abraham TP, Girgis RE, Hassoun PM. Tricuspid annular displacement predicts survival in pulmonary hypertension. Am J Respir Crit Care Med 174: 1034-1041, 2006.
18. Govindarajan B, Sligh JE, Vincent BJ, Li M, Canter JA, Nickoloff BJ, Rodenburg RJ, Smeitink JA, Oberley L, Zhang Y, Slingerland J, Arnold RS, Lambeth JD, Cohen C, Hilenski L, Griendling K, Martinez-Diez M, Cuezva JM, Arbiser JL. Overexpression of Akt converts radial growth melanoma to vertical growth melanoma. J Clin Invest 117: 719-729, 2007.
19. Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H. Role of oxidative stress in atherosclerosis. Am J Cardiol 91: 7A-11A, 2003.
20. Hemnes AR, Maynard KB, Champion HC, Gleaves L, Penner N, West J, Newman JH. Testosterone negatively regulates right ventricular load stress responses in mice. Pulm Circ 2: 352-358, 2012.
21. Heymes C, Bendall JK, Ratajczak P, Cave AC, Samuel JL, Hasenfuss G, Shah AM. Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 41: 2164-2171, 2003.
22. Hilenski LL, Clempus RE, Quinn MT, Lambeth JD, Griendling KK. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 24: 677-683, 2004.
23. Kim SM, Kim YG, Jeong KH, Lee SH, Lee TW, Ihm CG, Moon JY. Angiotensin II-induced mitochondrial Nox4 is a major endogenous source of oxidative stress in kidney tubular cells. PLos One 7: e39739, 2012.
24. Kuroda J, Ago T, Matsushima S, Zhai P, Schneider MD, Sadoshima J. NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci USA 107: 15565-15570, 2010.
25. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4: 181-189, 2004.
26. Laufs U, Wassmann S, Czech T, Munzel T, Eisenhauer M, Bohm M, Nickenig G. Physical inactivity increases oxidative stress, endothelial dysfunction, and atherosclerosis. Arterioscler Thromb Vasc Biol 25: 809-814, 2005.
27. Lee YM, Kim BJ, Chun YS, So I, Choi H, Kim MS, Park JW. NOX4 as an oxygen sensor to regulate TASK-1 activity. Cell Signal 18: 499-507, 2006.
28. Li J, Stouffs M, Serrander L, Banfi B, Bettiol E, Charnay Y, Steger K, Krause KH, Jaconi ME. The NADPH oxidase NOX4 drives cardiac differentiation: role in regulating cardiac transcription factors and MAP kinase activation. Mol Biol Cell 17: 3978-3988, 2006.
29. Li JM, Gall NP, Grieve DJ, Chen M, Shah AM. Activation of NADPH oxidase during progression of cardiac hypertrophy to failure. Hypertension 40: 477-484, 2002.
30. Li S, Tabar SS, Malec V, Eul BG, Klepetko W, Weissmann N, Grimminger F, Seeger W, Rose F, Hanze J. NOX4 regulates ROS levels under normoxic and hypoxic conditions, triggers proliferation, and inhibits apoptosis in pulmonary artery adventitial fibroblasts. Antioxid Redox Signal 10: 1687-1698, 2008.
31. Looi YH, Grieve DJ, Siva A, Walker SJ, Anilkumar N, Cave AC, Marber M, Monaghan MJ, Shah AM. Involvement of Nox2 NADPH oxidase in adverse cardiac remodeling after myocardial infarction. Hypertension 51: 319-325, 2008.
32. Lu Z, Xu X, Hu X, Zhu G, Zhang P, van Deel ED, French JP, Fassett JT, Oury TD, Bache RJ, Chen Y. Extracellular superoxide dismutase deficiency exacerbates pressure overload-induced left ventricular hypertrophy and dysfunction. Hypertension 51: 19-25, 2008.
33. Maejima Y, Kuroda J, Matsushima S, Ago T, Sadoshima J. Regulation of myocardial growth and death by NADPH oxidase. J Mol Cell Cardiol 50: 408-416, 2011.
34. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 18: 69-82, 2006.
35. Molshanski-Mor S, Mizrahi A, Ugolev Y, Dahan I, Berdichevsky Y, Pick E. Cell-free assays: the reductionist approach to the study of NADPH oxidase assembly, or "all you wanted to know about cell-free assays but did not dare to ask". Methods Mol Biol 412: 385-428, 2007.
36. Nabeebaccus A, Zhang M, Shah AM. NADPH oxidases and cardiac remodelling. Heart Fail Rev 16: 5-12, 2011.
37. Pagano PJ, Clark JK, Cifuentes-Pagano ME, Clark SM, Callis GM, Quinn MT. Localization of a constitutively active, phagocyte-like NADPH oxidase in rabbit aortic adventitia: enhancement by angiotensin II. Proc Natl Acad Sci USA 94: 14483-14488, 1997.
38. Peluffo G, Calcerrada P, Piacenza L, Pizzano N, Radi R. Superoxide-mediated inactivation of nitric oxide and peroxynitrite formation by tobacco smoke in vascular endothelium: studies in cultured cells and smokers. Am J Physiol Heart Circ Physiol 296: H1781-H1792, 2009.
39. Santos CX, Anilkumar N, Zhang M, Brewer AC, Shah AM. Redox signaling in cardiac myocytes. Free Radic Biol Med 50: 777-793, 2011.
40. Serrander L, Cartier L, Bedard K, Banfi B, Lardy B, Plastre O, Sienkiewicz A, Forro L, Schlegel W, Krause KH. NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem J 406: 105-114, 2007.
41. Wosniak J Jr, Santos CX, Kowaltowski AJ, Laurindo FR. Cross-talk between mitochondria and NADPH oxidase: effects of mild mitochondrial dysfunction on angiotensin II-mediated increase in Nox isoform expression and activity in vascular smooth muscle cells. Antioxid Redox Signal 11: 1265-1278, 2009.
42. Zhang M, Brewer AC, Schroder K, Santos CX, Grieve DJ, Wang M, Anilkumar N, Yu B, Dong X, Walker SJ, Brandes RP, Shah AM. NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci USA 107: 18121-18126, 2010.