Nox2 and p47phox modulate compensatory growth of primary collateral arteries

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 306, Issue 10, 2014, Pages

  DiStasi, Matthew R ^a   Unthank, Joseph L ^a   Miller, Steven J ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Collateral artery; Hydrogen peroxide; NADPH oxidase; Nox2

Indexed keywords

ANTIOXIDANT; APOCYNIN; HYDROGEN PEROXIDE; MESSENGER RNA; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY LIGATION; ARTICLE; COLLATERAL CIRCULATION; CONTROLLED STUDY; FEMORAL ARTERY; GROWTH; HINDLIMB; MALE; MESENTERY; MOUSE; NONHUMAN; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION;

COLLATERAL ARTERY; HYDROGEN PEROXIDE; NADPH OXIDASE; NOX2; P47PHOX;

ACETOPHENONES; ANIMALS; ANTIOXIDANTS; ARTERIES; COLLATERAL CIRCULATION; HYDROGEN PEROXIDE; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; NADPH OXIDASE; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; RATS, INBRED WKY; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING;

EID: 84900536918     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00828.2013     Document Type: Article

References (78)

1. Abaci A, Oguzhan A, Kahraman S, Eryol NK, Unal S, Arinc H, Ergin A. Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation 99: 2239-2242, 1999.
2. Antoniucci D, Valenti R, Moschi G, Migliorini A, Trapani M, Santoro GM, Bolognese L, Cerisano G, Buonamici P, Dovellini EV. Relation between preintervention angiographic evidence of coronary collateral circulation and clinical and angiographic outcomes after primary angioplasty or stenting for acute myocardial infarction. Am J Cardiol 89: 121-125, 2002.
3. Belin de Chantemele EJ, Vessieres E, Dumont O, Guihot AL, Toutain B, Loufrani L, Henrion D. Reactive oxygen species are necessary for high flow (shear stress)-induced diameter enlargement of rat resistance arteries. Microcirculation 16: 391-402, 2009.
4. Belin de Chantemele EJ, Vessieres E, Guihot AL, Toutain B, Maquignau M, Loufrani L, Henrion D. Type 2 diabetes severely impairs structural and functional adaptation of rat resistance arteries to chronic changes in blood flow. Cardiovasc Res 81: 788-796, 2009.
5. Brandes RP, Kreuzer J. Vascular NADPH oxidases: molecular mechanisms of activation. Cardiovasc Res 65: 16-27, 2005.
6. Cai H, Li Z, Dikalov S, Holland SM, Hwang J, Jo H, Dudley SC Jr, Harrison DG. NAD(P)H oxidase-derived hydrogen peroxide mediates endothelial nitric oxide production in response to angiotensin II. J Biol Chem 277: 48311-48317, 2002.
7. Castier Y, Brandes RP, Leseche G, Tedgui A, Lehoux S. p47phoxdependent NADPH oxidase regulates flow-induced vascular remodeling. Circ Res 97: 533-540, 2005.
8. Castier Y, Ramkhelawon B, Riou S, Tedgui A, Lehoux S. Role of NF-kappaB in flow-induced vascular remodeling. Antioxid Redox Signal 11: 1641-1649, 2009.
9. Chalothorn D, Zhang H, Clayton JA, Thomas SA, Faber JE. Catecholamines augment collateral vessel growth and angiogenesis in hindlimb ischemia. Am J Physiol Heart Circ Physiol 289: H947-H959, 2005.
10. Conrad MC, Green HD. Hemodynamics of large and small vessels in peripheral vascular disease. Circulation 29: 847-853, 1964.
11. Csanyi G, Cifuentes-Pagano E, Al Ghouleh I, Ranayhossaini DJ, Egana L, Lopes LR, Jackson HM, Kelley EE, Pagano PJ. Nox2 B-loop peptide, Nox2ds, specifically inhibits the NADPH oxidase Nox2. Free Radic Biol Med 51: 1116-1125, 2011.
12. Dai X, Faber JE. Endothelial nitric oxide synthase deficiency causes collateral vessel rarefaction and impairs activation of a cell cycle gene network during arteriogenesis. Circ Res 106: 1870-1881, 2010.
13. Datla SR, Peshavariya H, Dusting GJ, Mahadev K, Goldstein BJ, Jiang F. Important role of Nox4 type NADPH oxidase in angiogenic responses in human microvascular endothelial cells in vitro. Arterioscler Thromb Vasc Biol 27: 2319-2324, 2007.
14. DeBakey ME, Lawrie GM, Glaeser DH. Patterns of atherosclerosis and their surgical significance. Ann Surg 201: 115-131, 1985.
15. Dikalov S. Cross talk between mitochondria and NADPH oxidases. Free Radic Biol Med 51: 1289-1301, 2011.
16. 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 45: 1340-1351, 2008.
17. -/- mice does not result from impaired collateral growth. Am J Physiol Heart Circ Physiol 296: H877-H886, 2009.
18. Drummond GR, Cai H, Davis ME, Ramasamy S, Harrison DG. Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression by hydrogen peroxide. Circ Res 86: 347-354, 2000.
19. Duerrschmidt N, Stielow C, Muller G, Pagano PJ, Morawietz H. NO-mediated regulation of NAD(P)H oxidase by laminar shear stress in human endothelial cells. J Physiol 576: 557-567, 2006.
20. 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 169: 719-728, 2006.
21. Eitenmuller I, Volger O, Kluge A, Troidl K, Barancik M, Cai WJ, Heil M, Pipp F, Fischer S, Horrevoets AJ, Schmitz-Rixen T, Schaper W. The range of adaptation by collateral vessels after femoral artery occlusion. Circ Res 99: 656-662, 2006.
22. Fath SW, Burkhart HM, Miller SC, Dalsing MC, Unthank JL. Wall remodeling after wall shear rate normalization in rat mesenteric arterial collaterals. J Vasc Res 35: 257-264, 1998.
23. Girerd X, London G, Boutouyrie P, Mourad JJ, Safar M, Laurent S. Remodeling of the radial artery in response to a chronic increase in shear stress. Hypertension 27: 799-803, 1996.
24. Gu W, Weihrauch D, Tanaka K, Tessmer JP, Pagel PS, Kersten JR, Chilian WM, Warltier DC. Reactive oxygen species are critical mediators of coronary collateral development in a canine model. Am J Physiol Heart Circ Physiol 285: H1582-H1589, 2003.
25. Haddad P, Dussault S, Groleau J, Turgeon J, Michaud SE, Menard C, Perez G, Maingrette F, Rivard A. Nox2-containing NADPH oxidase deficiency confers protection from hindlimb ischemia in conditions of increased oxidative stress. Arterioscler Thromb Vasc Biol 29: 1522-1528, 2009.
26. Hedera P, Bujdakova J, Traubner P, Pancak J. Stroke risk factors and development of collateral flow in carotid occlusive disease. Acta Neurol Scand 98: 182-186, 1998.
27. Herrmann LG, Cranley JJ, Preuninger RM. Importance of collateral circulation in obliterative arterial disease of the lower extremities. Geriatrics 9: 1-7, 1954.
28. Heumuller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schroder K, Brandes RP. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51: 211-217, 2008.
29. Johnson DK, Schillinger KJ, Kwait DM, Hughes CV, McNamara EJ, Ishmael F, O'Donnell RW, Chang MM, Hogg MG, Dordick JS, Santhanam L, Ziegler LM, Holland JA. Inhibition of NADPH oxidase activation in endothelial cells by ortho-methoxy-substituted catechols. Endothelium 9: 191-203, 2002.
30. Kamiya A, Togawa T. Adaptive regulation of wall shear stress to flow change in the canine carotid artery. Am J Physiol Heart Circ Physiol 239: H14-H21, 1980.
31. Kang LS, Reyes RA, Muller-Delp JM. Aging impairs flow-induced dilation in coronary arterioles: role of NO and H2O2. Am J Physiol Heart Circ Physiol 297: H1087-H1095, 2009.
32. Khatri JJ, Johnson C, Magid R, Lessner SM, Laude KM, Dikalov SI, Harrison DG, Sung HJ, Rong Y, Galis ZS. Vascular oxidant stress enhances progression and angiogenesis of experimental atheroma. Circulation 109: 520-525, 2004.
33. Kilian JG, Keech A, Adams MR, Celermajer DS. Coronary collateralization: determinants of adequate distal vessel filling after arterial occlusion. Coron Artery Dis 13: 155-159, 2002.
34. Kumar S, Sud N, Fonseca FV, Hou Y, Black SM. Shear stress stimulates nitric oxide signaling in pulmonary arterial endothelial cells via a reduction in catalase activity: role of protein kinase C delta. Am J Physiol Lung Cell Mol Physiol 298: L105-L116, 2010.
35. Kunsch C, Medford RM. Oxidative stress as a regulator of gene expression in the vasculature. Circ Res 85: 753-766, 1999.
36. Lamblin N, Cuilleret FJ, Helbecque N, Dallongeville J, Lablanche JM, Amouyel P, Bauters C, Van Belle E. A common variant of endothelial nitric oxide synthase (Glu298Asp) is associated with collateral development in patients with chronic coronary occlusions. BMC Cardiovasc Disord 5: 27 (Sept 15, 2005). doi:10.1186/1471-2261-5-27.
37. Lash JM, Nixon JC, Unthank JL. Exercise training effects on collateral and microvascular resistances in rat model of arterial insufficiency. Am J Physiol Heart Circ Physiol 268: H125-H137, 1995.
38. Lassegue B, Clempus RE. Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285: R277-R297, 2003.
39. Lassegue B, San Martin A, Griendling KK. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res 110: 1364-1390, 2012.
40. Laurindo FR, Pedro Mde A, Barbeiro HV, Pileggi F, Carvalho MH, Augusto O, da Luz PL. Vascular free radical release Ex vivo and in vivo evidence for a flow-dependent endothelial mechanism. Circ Res 74: 700-709, 1994.
41. Liu J, Yang F, Yang XP, Jankowski M, Pagano PJ. NAD(P)H oxidase mediates angiotensin II-induced vascular macrophage infiltration and medial hypertrophy. Arterioscler Thromb Vasc Biol 23: 776-782, 2003.
42. Longland CJ. The collateral circulation of the limb; Arris and Gale lecture delivered at the Royal College of Surgeons of England on 4th February, 1953. Ann R Coll Surg Engl 13: 161-176, 1953.
43. Ludbrook J. Collateral artery resistance in the human lower limb. J Surg Res 6: 423-434, 1966.
44. Martin-Garrido A, Gonzalez-Ramos M, Griera M, Guijarro B, Cannata-Andia J, Rodriguez-Puyol D, Rodriguez-Puyol M, Saura M. H2O2 regulation of vascular function through sGC mRNA stabilization by HuR. Arterioscler Thromb Vasc Biol 31: 567-573, 2011.
45. Menard MT, Belkin M. Femoropopliteal and tibial occlusive disease. In: Greenfield's Surgery: Scientific Principles and Practice, edited by Mulholland MW, Lillemoe KD, Doherty GM, Maier RV, and Upchurch GR. Philadelphia, PA: Lippincott Williams & Wilkins, p. 1649-1661, 2006.
46. Miller SJ, Coppinger BJ, Zhou X, Unthank JL. Antioxidants reverse age-related collateral growth impairment. J Vasc Res 47: 108-114, 2010.
47. Miller SJ, Norton LE, Murphy MP, Dalsing MC, Unthank JL. The role of the renin-angiotensin system and oxidative stress in spontaneously hypertensive rat mesenteric collateral growth impairment. Am J Physiol Heart Circ Physiol 292: H2523-H2531, 2007.
48. Nakae I, Fujita M, Miwa K, Hasegawa K, Kihara Y, Nohara R, Miyamoto S, Ueda K, Tamaki S, Sasayama S. Age-dependent impairment of coronary collateral development in humans. Heart Vessels 15: 176-180, 2000.
49. Paliege A, Pasumarthy A, Mizel D, Yang T, Schnermann J, Bachmann S. Effect of apocynin treatment on renal expression of COX-2, NOS1, and renin in Wistar-Kyoto and spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 290: R694-R700, 2006.
50. Patel VB, Wang Z, Fan D, Zhabyeyev P, Basu R, Das SK, Wang W, Desaulniers J, Holland SM, Kassiri Z, Oudit GY. Loss of p47phox subunit enhances susceptibility to biomechanical stress and heart failure because of dysregulation of cortactin and actin filaments. Circ Res 112: 1542-1556, 2013.
51. 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 31: 1368-1376, 2011.
52. Reed R, Kolz C, Potter B, Rocic P. The mechanistic basis for the disparate effects of angiotensin II on coronary collateral growth. Arterioscler Thromb Vasc Biol 28: 61-67, 2008.
53. Rey FE, Cifuentes ME, Kiarash A, Quinn MT, Pagano PJ. Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O2 and systolic blood pressure in mice. Circ Res 89: 408-414, 2001.
54. Rocic P, Kolz C, Reed R, Potter B, Chilian WM. Optimal reactive oxygen species concentration and p38 MAP kinase are required for coronary collateral growth. Am J Physiol Heart Circ Physiol 292: H2729-H2736, 2007.
55. 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 110: 1217-1225, 2012.
56. Shaw JH, Lloyd PG. Post-transcriptional regulation of placenta growth factor mRNA by hydrogen peroxide. Microvasc Res 84: 155-160, 2012.
57. Sousa T, Pinho D, Morato M, Marques-Lopes J, Fernandes E, Afonso J, Oliveira S, Carvalho F, Albino-Teixeira A. Role of superoxide and hydrogen peroxide in hypertension induced by an antagonist of adenosine receptors. Eur J Pharmacol 588: 267-276, 2008.
58. Thomas SR, Chen K, Keaney JF Jr. Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J Biol Chem 277: 6017-6024, 2002.
59. 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 111: 2347-2355, 2005.
60. Touyz RM, Montezano AC. Vascular Nox4: a multifarious NADPH oxidase. Circ Res 110: 1159-1161, 2012.
61. Traupe T, Ortmann J, Stoller M, Baumgartner I, de Marchi SF, Seiler C. Direct quantitative assessment of the peripheral artery collateral circulation in patients undergoing angiography. Circulation 128: 737-744, 2013.
62. Tuttle JL, Hahn TL, Sanders BM, Witzmann FA, Miller SJ, Dalsing MC, Unthank JL. Impaired collateral development in mature rats. Am J Physiol Heart Circ Physiol 283: H146-H155, 2002.
63. Tuttle JL, Nachreiner RD, Bhuller AS, Condict KW, Connors BA, Herring BP, Dalsing MC, Unthank JL. Shear level influences resistance artery remodeling: wall dimensions, cell density, and eNOS expression. Am J Physiol Heart Circ Physiol 281: H1380-H1389, 2001.
64. Tuttle JL, Sanders BM, Burkhart HM, Fath SW, Kerr KA, Watson WC, Herring BP, Dalsing MC, Unthank JL. Impaired collateral artery development in spontaneously hypertensive rats. Microcirculation 9: 343-351, 2002.
65. Unthank JL, Fath SW, Burkhart HM, Miller SC, Dalsing MC. Wall remodeling during luminal expansion of mesenteric arterial collaterals in the rat. Circ Res 79: 1015-1023, 1996.
66. Unthank JL, McClintick JN, Labarrere CA, Li L, Distasi MR, Miller SJ. Molecular basis for impaired collateral artery growth in the spontaneously hypertensive rat: insight from microarray analysis. Physiol Rep 1: (June 26, 2013). doi:10.1002/phy2.5.00005.2013.
67. Unthank JL, Nixon JC, Burkhart HM, Fath SW, Dalsing MC. Early collateral and microvascular adaptations to intestinal artery occlusion in rat. Am J Physiol Heart Circ Physiol 271: H914-H923, 1996.
68. Unthank JL, Nixon JC, Lash JM. Early adaptations in collateral and microvascular resistances after ligation of the rat femoral artery. J Appl Physiol 79: 73-82, 1995.
69. Urao N, Inomata H, Razvi M, Kim HW, Wary K, McKinney R, Fukai T, Ushio-Fukai M. Role of Nox2-based NADPH oxidase in bone marrow and progenitor cell function involved in neovascularization induced by hindlimb ischemia. Circ Res 103: 212-220, 2008.
70. Urao N, Sudhahar V, Kim SJ, Chen GF, McKinney RD, Kojda G, Fukai T, Ushio-Fukai M. Critical role of endothelial hydrogen peroxide in post-ischemic neovascularization. PLoS One 8 (March 5, 2013): doi: 10.1371/journal.pone.0057618.
71. Walden R, Adar R, Rubinstein ZJ, Bass A. Distribution and symmetry of arteriosclerotic lesions of the lower extremities: an arteriographic study of 200 limbs. Cardiovasc Intervent Radiol 8: 180-182, 1985.
72. Wang D, Gill PS, Chabrashvili T, Onozato ML, Raggio J, Mendonca M, Dennehy K, Li M, Modlinger P, Leiper J, Vallance P, Adler O, Leone A, Tojo A, Welch WJ, Wilcox CS. Isoform-specific regulation by N(G), N(G)-dimethylarginine dimethylaminohydrolase of rat serum asymmetric dimethylarginine and vascular endothelium-derived relaxing factor/ NO. Circ Res 101: 627-635, 2007.
73. Yang H, Roberts LJ, Shi MJ, Zhou LC, Ballard BR, Richardson A, Guo ZM. Retardation of atherosclerosis by overexpression of catalase or both Cu/Zn-superoxide dismutase and catalase in mice lacking apolipoprotein E. Circ Res 95: 1075-1081, 2004.
74. Yang HT, Ren J, Laughlin MH, Terjung RL. Prior exercise training produces NO-dependent increases in collateral blood flow after acute arterial occlusion. Am J Physiol Heart Circ Physiol 282: H301-H310, 2002.
75. 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.
76. Zhou X, Bohlen HG, Miller SJ, Unthank JL. NAD(P)H oxidase-derived peroxide mediates elevated basal and impaired flow-induced NO production in SHR mesenteric arteries in vivo. Am J Physiol Heart Circ Physiol 295: H1008-H1016, 2008.
77. Zhou X, Bohlen HG, Unthank JL, Miller SJ. Abnormal nitric oxide production in aged rat mesenteric arteries is mediated by NAD(P)H oxidase-derived peroxide. Am J Physiol Heart Circ Physiol 297: H2227-H2233, 2009.
78. Ziegler MA, Distasi MR, Bills RG, Miller SJ, Alloosh M, Murphy MP, George Akingba A, Sturek M, Dalsing MC, Unthank JL. Marvels, mysteries, and misconceptions of vascular compensation to peripheral artery occlusion. Microcirculation 17: 3-20, 2010.