The NADPH oxidase Nox4 has anti-atherosclerotic functions

European Heart Journal

Volumn 36, Issue 48, 2015, Pages 3447-3456

  Schürmann, Christoph ^a,b   Rezende, Flavia ^a,b   Kruse, Christoph ^a,b   Yasar, Yakub ^a,b   Löwe, Oliver ^a,b   Fork, Christian ^a,b   Van De Sluis, Bart ^c   Bremer, Rolf ^d   Weissmann, Norbert ^e   Shah, Ajay M ^f   Jo, Hanjoong ^g   Brandes, Ralf P ^a,b   Schröder, Katrin ^a,b  

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d HBB Datenkommunikation and Abrechnungssysteme   (Germany)

^e JUSTUS LIEBIG UNIVERSITY   (Germany)

^f KING'S COLLEGE LONDON   (United Kingdom)

^g GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

ApoE; Arteriosclerosis; Inflammation; Lipids; NADPH oxidase; Reactive oxygen species; Remodelling

Indexed keywords

APOLIPOPROTEIN; CHOLESTEROL; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; TAMOXIFEN; TRIACYLGLYCEROL; APOLIPOPROTEIN E; HYDROGEN PEROXIDE; NOX4 PROTEIN, MOUSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; CAROTID ARTERY LIGATION; CELL CULTURE; CLINICAL ASSESSMENT; CLINICAL EVALUATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENE EXPRESSION; KNOCKOUT MOUSE; LEUKOCYTE ADHERENCE; LIPID DIET; MACROPHAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; CAROTID ARTERY; CELL ADHESION; LEUKOCYTE; LIGATION; METABOLISM; MICROARRAY ANALYSIS; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CAROTID ARTERIES; CELL ADHESION; HYDROGEN PEROXIDE; LEUKOCYTES; LIGATION; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; NADPH OXIDASE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84952042542     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehv460     Document Type: Article

References (30)

1. Li H, Horke S, Forstermann U. Vascular oxidative stress, nitric oxide and atherosclerosis. Atherosclerosis 2014;237:208-219.
2. Lonn ME, Dennis JM, Stocker R. Actions of "antioxidants" in the protection against atherosclerosis. Free Radic Biol Med 2012;53:863-884.
3. Drummond GR, Selemidis S, Griendling KK, Sobey CG. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat Rev Drug Discov 2011;10:453-471.
4. Brandes RP, Weissmann N, Schroder K. NADPH oxidases in cardiovascular disease. Free Radic Biol Med 2010;49:687-706.
5. Violi F, Sanguigni V, Carnevale R, Plebani A, Rossi P, Finocchi A, Pignata C, De MD, Martire B, Pietrogrande MC, Martino S, Gambineri E, Soresina AR, Pignatelli P, Martino F, Basili S, Loffredo L. Hereditary deficiency of gp91(phox) is associated with enhanced arterial dilatation: results of a multicenter study. Circulation 2009; 120:1616-1622.
6. Gray SP, Di ME, Okabe J, Szyndralewiez C, Heitz F, Montezano AC, de Haan JB, Koulis C, El-Osta A, Andrews KL, Chin-Dusting JP, Touyz RM, Wingler K, Cooper ME, Schmidt HH, Jandeleit-Dahm KA. NADPH oxidase 1 plays a key role in diabetes mellitus-accelerated atherosclerosis. Circulation 2013;127: 1888-1902.
7. Sobey CG, Judkins CP, Rivera J, Lewis CV, Diep H, Lee HW, Kemp-Harper BK, Broughton BR, Selemidis S, Gaspari TA, Samuel CS, Drummond GR. NOX1 deficiency in apolipoprotein E-knockout mice is associated with elevated plasma lipids and enhanced atherosclerosis. Free Radic Res 2015;49:186-198.
8. Barry-Lane PA, Patterson C, van der Merwe M, Hu Z, Holland SM, Yeh ET, Runge MS. p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J Clin Invest 2001;108:1513-1522.
9. Judkins CP, Diep H, Broughton BR, Mast AE, Hooker EU, Miller AA, Selemidis S, Dusting GJ, Sobey CG, Drummond GR. Direct evidence of a role for Nox2 in superoxide production, reduced nitric oxide bioavailability, and early atherosclerotic plaque formation in ApoE-/-mice. Am J Physiol Heart Circ Physiol 2010;298: H24-H32.
10. Kirk EA, Dinauer MC, Rosen H, Chait A, Heinecke JW, LeBoeuf RC. Impaired superoxide production due to a deficiency in phagocyte NADPH oxidase fails to inhibit atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2000;20:1529-1535.
11. Sibley CT, Estwick T, Zavodni A, Huang CY, Kwan AC, Soule BP, Long Priel DA, Remaley AT, Rudman Spergel AK, Turkbey EB, Kuhns DB, Holland SM, Malech HL, Zarember KA, Bluemke DA, Gallin JI. Assessment of atherosclerosis in chronic granulomatous disease. Circulation 2014;130:2031-2039.
12. Violi F, Pignatelli P, Pignata C, Plebani A, Rossi P, Sanguigni V, Carnevale R, Soresina A, Finocchi A, Cirillo E, Catasca E, Angelico F, Loffredo L. Reduced atherosclerotic burden in subjects with genetically determined low oxidative stress. Arterioscler Thromb Vasc Biol 2013;33:406-412.
13. Montezano AC, Burger D, Ceravolo GS, Yusuf H, Montero M, Touyz RM. Novel Nox homologues in the vasculature: focusing on Nox4 and Nox5. Clin Sci (Lond) 2011;120:131-141.
14. Schroder K, Zhang M, Benkhoff S, Mieth A, Pliquett R, Kosowski J, Kruse C, Luedike P, Michaelis UR, Weissmann N, Dimmeler S, Shah AM, Brandes RP. Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ Res 2012;110:1217-1225.
15. Craige SM, Chen K, Pei Y, Li C, Huang X, Chen C, Shibata R, Sato K, Walsh K, Keaney JF Jr. NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation 2011;124:731-740.
16. Indra AK, Warot X, Brocard J, Bornert JM, Xiao JH, Chambon P, Metzger D. Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res 1999;27:4324-4327.
17. Nam D, NiCW, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H. Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol 2009;297: H1535-H1543.
18. Brewer AC, Murray TV, Arno M, Zhang M, Anilkumar NP, Mann GE, Shah AM. Nox4 regulates Nrf2 and glutathione redox in cardiomyocytes in vivo. Free Radic Biol Med 2011;51:205-215.
19. Babelova A, Avaniadi D, Jung O, Fork C, Beckmann J, Kosowski J, Weissmann N, Anilkumar N, Shah AM, Schaefer L, Schroder K, Brandes RP. Role of Nox4 in murine models of kidney disease. Free Radic Biol Med 2012;53:842-853.
20. Goettsch C, Babelova A, Trummer O, Erben RG, Rauner M, Rammelt S, Weissmann N, Weinberger V, Benkhoff S, Kampschulte M, Obermayer-Pietsch B, Hofbauer LC, Brandes RP, Schroder K. NADPH oxidase 4 limits bone mass by promoting osteoclastogenesis. J Clin Invest 2013;123:4731-4738.
21. Clempus RE, Sorescu D, Dikalova AE, Pounkova L, Jo P, Sorescu GP, Schmidt HH, Lassegue B, Griendling KK. Nox4 is required for maintenance of the differentiated vascular smooth muscle cell phenotype. Arterioscler Thromb Vasc Biol 2007;27: 42-48.
22. 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 2010;107:18121-18126.
23. Lener B, Koziel R, Pircher H, Hutter E, Greussing R, Herndler-Brandstetter D, Hermann M, Unterluggauer H, Jansen-Durr P. The NADPH oxidase Nox4 restricts the replicative lifespan of human endothelial cells. Biochem J 2009;423: 363-374.
24. Wu RF, Ma Z, Liu Z, Terada LS. Nox4-derived H2O2 mediates endoplasmic reticulum signaling through local Ras activation. Mol Cell Biol 2010;30:3553-3568.
25. Szocs K, Lassegue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, Wilcox JN, Quinn MT, Lambeth JD, Griendling KK. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol 2002;22:21-27.
26. Xu S, Chamseddine AH, Carrell S, Miller FJ Jr. Nox4 NADPH oxidase contributes to smooth muscle cell phenotypes associated with unstable atherosclerotic plaques. Redox Biol 2014;2:642-650.
27. Sorescu D, Weiss D, Lassegue B, Clempus RE, Szocs K, Sorescu GP, Valppu L, Quinn MT, Lambeth JD, Vega JD, Taylor WR, Griendling KK. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 2002;105:1429-1435.
28. Stanic B, Pandey D, Fulton DJ, Miller FJ Jr. Increased epidermal growth factor-like ligands are associated with elevated vascular nicotinamide adenine dinucleotide phosphate oxidase in a primate model of atherosclerosis. Arterioscler Thromb Vasc Biol 2012;32:2452-2460.
29. Pleskova M, Beck KF, Behrens MH, Huwiler A, Fichtlscherer B, Wingerter O, Brandes RP, Mulsch A, Pfeilschifter J. Nitric oxide down-regulates the expression of the catalytic NADPH oxidase subunit Nox1 in rat renal mesangial cells. FASEB J 2006;20:139-141.
30. Lee CF, Qiao M, Schroder K, Zhao Q, Asmis R. Nox4 is a novel inducible source of reactive oxygen species in monocytes and macrophages and mediates oxidized low density lipoprotein-induced macrophage death. Circ Res 2010;106:1489-1497.