Nox2-containing NADPH oxidase deficiency confers protection from hindlimb ischemia in conditions of increased oxidative stress

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 29, Issue 10, 2009, Pages 1522-1528

  Haddad, Paola ^a   Dussault, Sylvie ^a   Groleau, Jessika ^a   Turgeon, Julie ^a   Michaud, Sophie Elise ^a   Ménard, Catherine ^a   Perez, Gemma ^a   Maingrette, Fritz ^a   Rivard, Alain ^a  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Cigarette smoking; Endothelial progenitor cells; NADPH oxidase; Neovascularization; Nitric oxide

Indexed keywords

ANTIOXIDANT; CIGARETTE SMOKE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; NITRITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE; VASCULOTROPIN; CYBB PROTEIN, MOUSE; MEMBRANE PROTEIN; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD FLOW; CAPILLARY DENSITY; CIGARETTE SMOKING; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME DEFICIENCY; HINDLIMB; KNOCKOUT MOUSE; LIMB ISCHEMIA; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE; ANIMAL; C57BL MOUSE; ISCHEMIA; METABOLISM; PHYSIOLOGY; SMOKE; STEM CELL; TOBACCO; VASCULARIZATION;

ANIMALS; ENDOTHELIAL CELLS; HINDLIMB; ISCHEMIA; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; NADPH OXIDASE; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SMOKE; STEM CELLS; TOBACCO;

EID: 70349579202     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.109.191437     Document Type: Article

References (33)

1. Losordo DW, Dimmeler S. Therapeutic angiogenesis and vasculogenesis for ischemic disease. Part I: angiogenic cytokines. Circulation. 2004;109: 2487-2491. (Pubitemid 38720544)
2. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005; 438:932-936.
3. Heil M, Schaper W. Insights into pathways of arteriogenesis. Curr Pharm Biotechnol. 2007;8:35-42.
4. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967.
5. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221-228.
6. Urbich C, Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res. 2004;95:343-353. (Pubitemid 39100452)
7. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. Faseb J. 1999;13:9-22.
8. Papapetropoulos A, Garcia-Cardena G, Madri JA, Sessa WC. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest. 1997;100: 3131-3139.
9. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kearney M, Chen D, Symes JF, Fishman MC, Huang PL, Isner JM. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest. 1998;101:2567-2578.
10. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, Dimmeler S. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med. 2003;9:1370-1376.
11. Rivard A, Fabre JE, Silver M, Chen D, Murohara T, Kearney M, Magner M, Asahara T, Isner JM. Age-dependent impairment of angiogenesis. Circulation. 1999;99:111-120.
12. Rivard A, Silver M, Chen D, Kearney M, Magner M, Annex B, Peters K, Isner JM. Rescue of diabetes-related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am J Pathol. 1999;154: 355-363.
13. Couffinhal T, Silver M, Kearney M, Sullivan A, Witzenbichler B, Magner M, Annex B, Peters K, Isner JM. Impaired collateral vessel development associated with reduced expression of vascular endothelial growth factor in ApoE-/- mice. Circulation. 1999;99:3188-3198.
14. Michaud SE, Menard C, Guy LG, Gennaro G, Rivard A. Inhibition of hypoxia-induced angiogenesis by cigarette smoke exposure: impairment of the HIF-1alpha/VEGF pathway. Faseb J. 2003;17:1150-1152.
15. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999; 340:115-126.
16. Ushio-Fukai M, Alexander RW. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol Cell Biochem. 2004;264:85-97.
17. Urbich C, Dernbach E, Aicher A, Zeiher AM, Dimmeler S. CD40 ligand inhibits endothelial cell migration by increasing production of endothelial reactive oxygen species. Circulation. 2002;106:981-986.
18. Michaud SE, Dussault S, Groleau J, Haddad P, Rivard A. Cigarette smoke exposure impairs VEGF-induced endothelial cell migration: role of NO and reactive oxygen species. J Mol Cell Cardiol. 2006;41:275-284.
19. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res. 2000;86:494-501.
20. Cave AC, Brewer AC, Narayanapanicker A, Ray R, Grieve DJ, Walker S, Shah AM. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal. 2006;8:691-728.
21. Babior BM. The NADPH oxidase of endothelial cells. IUBMB Life. 2000;50:267-269.
22. 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 factor-induced signaling and angiogenesis. Circ Res. 2002;91:1160-1167.
23. 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.
24. Villablanca AC, McDonald JM, Rutledge JC. Smoking and cardiovascular disease. Clin Chest Med. 2000;21:159-172.
25. Lefevre J, Michaud SE, Haddad P, Dussault S, Menard C, Groleau J, Turgeon J, Rivard A. Moderate consumption of red wine (cabernet sauvignon) improves ischemia-induced neovascularization in ApoE-deficient mice: effect on endothelial progenitor cells and nitric oxide. Faseb J. 2007;21:3845-3852.
26. Michaud SE, Dussault S, Haddad P, Groleau J, Rivard A. Circulating endothelial progenitor cells from healthy smokers exhibit impaired functional activities. Atherosclerosis. 2006;187:423-432.
27. Al-Shabrawey M, Bartoli M, El-Remessy AB, Platt DH, Matragoon S, Behzadian MA, Caldwell RW, Caldwell RB. Inhibition of NAD(P)H oxidase activity blocks vascular endothelial growth factor overexpression and neovascularization during ischemic retinopathy. Am J Pathol. 2005; 167:599-607.
28. Barua RS, Ambrose JA, Srivastava S, DeVoe MC, Eales-Reynolds LJ. Reactive oxygen species are involved in smoking-induced dysfunction of nitric oxide biosynthesis and upregulation of endothelial nitric oxide synthase: an in vitro demonstration in human coronary artery endothelial cells. Circulation. 2003;107:2342-2347.
29. Jaimes EA, DeMaster EG, Tian RX, Raij L. Stable compounds of cigarette smoke induce endothelial superoxide anion production via NADPH oxidase activation. Arterioscler Thromb Vasc Biol. 2004;24:1031-1036.
30. 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 post-ischemic neovascularization in mice with type 1 diabetes. Am J Pathol. 2006;169:719-728.
31. Dernbach E, Urbich C, Brandes RP, Hofmann WK, Zeiher AM, Dimmeler S. Antioxidative stress-associated genes in circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood. 2004;104:3591-3597.
32. Ingram DA, Krier TR, Mead LE, McGuire C, Prater DN, Bhavsar J, Saadatzadeh MR, Bijangi-Vishehsaraei K, Li F, Yoder MC, Haneline LS. Clonogenic endothelial progenitor cells are sensitive to oxidative stress. Stem Cells. 2007;25:297-304.
33. Kondo T, Hayashi M, Takeshita K, Numaguchi Y, Kobayashi K, Iino S, Inden Y, Murohara T. Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers. Arterioscler Thromb Vasc Biol. 2004;24:1442-1447.