Nox4 Is a protective reactive oxygen species generating vascular NADPH oxidase

Circulation Research

Volumn 110, Issue 9, 2012, Pages 1217-1225

  Schröder, Katrin ^a   Zhang, Min ^b   Benkhoff, Sebastian ^a   Mieth, Anja ^a   Pliquett, Rainer ^a   Kosowski, Judith ^a   Kruse, Christoph ^a   Luedike, Peter ^c   Michaelis, U Ruth ^a   Weissmann, Norbert ^d   Dimmeler, Stefanie ^a   Shah, Ajay M ^b   Brandes, Ralf P ^a  

^a GOETHE UNIVERSITY   (Germany)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Angiogenesis; Carbon monoxide; Hypertension; Nitric oxide; Redox regulation

Indexed keywords

ANGIOTENSIN II; CARBON MONOXIDE; CATALASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEME OXYGENASE 1; HEMIN; HYDROGEN PEROXIDE; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; TAMOXIFEN; TRANSCRIPTION FACTOR NRF2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTITIS; APOPTOSIS; ARTERY LIGATION; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; FEMORAL ARTERY; GENE DELETION; HUMAN; HUMAN CELL; HYPERTROPHY; IN VIVO STUDY; ISCHEMIA; LUNG ENDOTHELIUM; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; REPORTER GENE; TRANSCRIPTION REGULATION; VASCULAR ENDOTHELIUM;

ANGIOTENSIN II; ANIMALS; ANTIOXIDANTS; APOPTOSIS; BORANES; CARBON DIOXIDE; CARBONATES; CATALASE; CELLS, CULTURED; CYTOPROTECTION; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HEME OXYGENASE-1; HEMIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; HYPERTENSION; HYPERTROPHY; ISCHEMIA; LUNG; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SKELETAL; NADH, NADPH OXIDOREDUCTASES; NADPH OXIDASE; NEOVASCULARIZATION, PHYSIOLOGIC; NF-E2-RELATED FACTOR 2; NITRIC OXIDE SYNTHASE TYPE III; ORGANOMETALLIC COMPOUNDS; OXIDATIVE STRESS; POLYETHYLENE GLYCOLS; RNA, MESSENGER; TIME FACTORS; TRANSFECTION;

EID: 84862776938     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.112.267054     Document Type: Article

References (40)

1. Touyz RM, Briones AM. Reactive oxygen species and vascular biology: implications in human hypertension. Hypertens Res. 2011;34:5-14.
2. Loot AE, Schreiber JG, Fisslthaler B, Fleming I. Angiotensin II impairs endothelial function via tyrosine phosphorylation of the endothelial nitric oxide synthase. J Exp Med. 2009;206:2889-2896.
3. Burgoyne JR, Madhani M, Cuello F, Charles RL, Brennan JP, Schroder E, Browning DD, Eaton P. Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science. 2007;317:1393-1397.
4. Cai H. Hydrogen peroxide regulation of endothelial function: origins, mechanisms, and consequences. Cardiovasc Res. 2005;68:26-36.
5. Brandes RP, Weissmann N, Schroder K. NADPH oxidases in cardiovascular disease. Free Radic Biol Med. 2010;49:687-706.
6. 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.
7. Lassegue B, Sorescu D, Szocs K, Yin Q, Akers M, Zhang Y, Grant SL, Lambeth JD, Griendling KK. Novel gp91(phox) homologues in vascular smooth muscle cells : nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ Res. 2001;88: 888-894.
8. 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.
9. 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.
10. Geiszt M, Kopp JB, Varnai P, Leto TL. Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci USA. 2000;97: 8010-8014.
11. 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. 2006;18:69-82.
12. Helmcke I, Heumuller S, Tikkanen R, Schroder K, Brandes RP. Identification of structural elements in Nox1 and Nox4 controlling localization and activity. Antioxid Redox Signal. 2009;11:1279-1287.
13. Lyle AN, Deshpande NN, Taniyama Y, Seidel-Rogol B, Pounkova L, Du P, Papaharalambus C, Lassegue B, Griendling KK. Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells. Circ Res. 2009;105:249-259.
14. 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. 2007;406:105-114.
15. Takac I, Schroder K, Zhang L, Lardy B, Anilkumar N, Lambeth JD, Shah AM, Morel F, Brandes RP. The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4. J Biol Chem. 2011;286: 13304-13313.
16. Ray R, Murdoch CE, Wang M, Santos CX, Zhang M, Alom-Ruiz S, Anilkumar N, Ouattara A, Cave AC, Walker SJ, Grieve DJ, Charles RL, Eaton P, Brewer AC, Shah AM. Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo. Arterioscler Thromb Vasc Biol. 2011;31:1368-1376.
17. Rey FE, Cifuentes ME, Kiarash A, Quinn MT, Pagano PJ. Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(r) and systolic blood pressure in mice. Circ Res. 2001;89:408-414.
18. Dikalov SI, Dikalova AE, Bikineyeva AT, Schmidt HH, Harrison DG, Griendling KK. Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production. Free Radic Biol Med. 2008;45:1340-1351.
19. 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.
20. 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.
21. Sturrock A, Cahill B, Norman K, Huecksteadt TP, Hill K, Sanders K, Karwande SV, Stringham JC, Bull DA, Gleich M, Kennedy TP, Hoidal JR. Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen species-dependent proliferation in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2006; 290:L661-L673.
22. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev. 2008;60:79-127.
23. Srisook K, Kim C, Cha YN. Molecular mechanisms involved in enhancing HO-1 expression: de-repression by heme and activation by Nrf2, the "one-two" punch. Antioxid Redox Signal. 2005;7:1674-1687.
24. Shuvaev VV, Christofidou-Solomidou M, Bhora F, Laude K, Cai H, Dikalov S, Arguiri E, Solomides CC, Albelda SM, Harrison DG, Muzy-kantov VR. Targeted detoxification of selected reactive oxygen species in the vascular endothelium. J Pharmacol Exp Ther. 2009;331:404-411.
25. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest. 2003;111:1201-1209.
26. Idriss NK, Blann AD, Lip GY. Hemoxygenase-1 in cardiovascular disease. J Am Coll Cardiol. 2008;52:971-978.
27. Winn RK, Harlan JM. The role of endothelial cell apoptosis in inflammatory and immune diseases. J Thromb Haemost. 2005;3:1815-1824.
28. 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.
29. Zafari AM, Ushio-Fukai M, Akers M, Yin Q, Shah A, Harrison DG, Taylor WR, Griendling KK. Role of NADH/NADPH oxidase-derived H2O2 in angiotensin II-induced vascular hypertrophy. Hypertension. 1998;32:488-495.
30. Zhang Y, Griendling KK, Dikalova A, Owens GK, Taylor WR. Vascular hypertrophy in angiotensin II-induced hypertension is mediated by vascular smooth muscle cell-derived H2O2. Hypertension. 2005;46:732-737.
31. Lauer N, Suvorava T, Ruther U, Jacob R, Meyer W, Harrison DG, Kojda G. Critical involvement of hydrogen peroxide in exercise-induced up-regulation of endothelial NO synthase. Cardiovasc Res. 2005;65:254-262.
32. Urano N, Kim S-J, Varadarajan S, Chen G-F, McKinney RD, Kojda G, Fukai T, Ushio-Fukai M. Critical role of endogenous vascular hydrogen peroxide in post-ischemic neovascularization: Studies using Tie2-driven endothelial specific catalase transgenic mice. Ciruclation. 2011;21S:124.
33. Garrido-Urbani S, Jemelin S, Deffert C, Carnesecchi S, Basset O, Szyndralewiez C, Heitz F, Page P, Montet X, Michalik L, Arbiser J, Ruegg C, Krause KH, Imhof BA. Targeting vascular NADPH oxidase 1 blocks tumor angiogenesis through a PPARalpha mediated mechanism. PLoS One. 2011;6:e14665.
34. Ushio-Fukai M, Tang Y, Fukai T, Dikalov SI, Ma Y, Fujimoto M, Quinn MT, Pagano PJ, Johnson C, Alexander RW. Novel role of gp91(phox)-containing NAD(P)H oxidase in vascular endothelial growth factorinduced signaling and angiogenesis. Circ Res. 2002;91:1160-1167.
35. Tojo T, Ushio-Fukai M, Yamaoka-Tojo M, Ikeda S, Patrushev N, Alexander RW. Role of gp91phox (Nox2)-containing NAD(P)H oxidase in angiogenesis in response to hindlimb ischemia. Circulation. 2005;111: 2347-2355.
36. Ebrahimian TG, Heymes C, You D, Blanc-Brude O, Mees B, Waeckel L, Duriez M, Vilar J, Brandes RP, Levy BI, Shah AM, Silvestre JS. NADPH oxidase-derived overproduction of reactive oxygen species impairs postischemic neovascularization in mice with type 1 diabetes. Am J Pathol. 2006;169:719-728.
37. Carnesecchi S, Deffert C, Donati Y, Basset O, Hinz B, Preynat-Seauve O, Guichard C, Arbiser JL, Banfi B, Pache JC, Barazzone-Argiroffo C, Krause KH. A key role for NOX4 in epithelial cell death during development of lung fibrosis. Antioxid Redox Signal. 2011;15:607-619.
38. Winterbourn CC. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol. 2008;4:278-286.
39. Winterbourn CC, Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med. 2008;45:549-561.
40. Ushio-Fukai M. Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal. 2009;11:1289-1299.