The role of the renin-angiotensin system and oxidative stress in spontaneously hypertensive rat mesenteric collateral growth impairment

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 292, Issue 5, 2007, Pages

  Miller, Steven J ^a,b   Norton, Laura E ^a   Murphy, Michael P ^a,b   Dalsing, Michael C ^a   Unthank, Joseph L ^a,b  

^a INDIANA UNIVERSITY MEDICAL CENTER   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiotensin converting enzyme inhibitor; Antioxidant; Arteriogenesis; Captopril; Collateral growth; Hypertension

Indexed keywords

1 (4 DIMETHYLAMINO 3 METHYLBENZYL) 5 DIPHENYLACETYL 4,5,6,7 TETRAHYDRO 1H IMIDAZO[4,5 C]PYRIDINE 6 CARBOXYLIC ACID; APOCYNIN; CAPTOPRIL; ENALAPRIL; LOSARTAN; TEMPOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTERIAL PRESSURE; ARTERY LIGATION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HYPERTENSION; ILIAC ARTERY; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; ANIMAL; GROWTH DISORDER; GROWTH, DEVELOPMENT AND AGING; MESENTERIC ARTERY; PATHOPHYSIOLOGY; SPONTANEOUSLY HYPERTENSIVE RAT;

ANIMALS; GROWTH DISORDERS; HYPERTENSION; MALE; MESENTERIC ARTERIES; OXIDATIVE STRESS; RATS; RATS, INBRED SHR; RENIN-ANGIOTENSIN SYSTEM;

EID: 34250837960     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01296.2006     Document Type: Article

References (74)

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. Adams V, Linke A, Krankel N, Erbs S, Gielen S, Mobius-Winkler S, Gummert JF, Mohr FW, Schuler G, Hambrecht R. Impact of regular physical activity on the NAD(P)H oxidase and angiotensin receptor system in patients with coronary artery disease. Circulation 111: 555-562, 2005.
3. Agoudemos MM, Greene AS. Localization of the renin-angiotensin system components to the skeletal muscle microcirculation. Microcirculation 12: 627-636, 2005.
4. Anderson TJ, Elstein E, Haber H, Charbonneau F. Comparative study of ACE-inhibition, angiotensin II antagonism, and calcium channel blockade on flow-mediated vasodilation in patients with coronary disease (BANFF study). J Am Coll Cardiol 35: 60-66, 2000.
5. 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.
6. Bolterman RJ, Manriquez MC, Ruiz MCO, Juncos LA, Romero JC. Effects of captopril on the renin angiotensin system, oxidative stress, and endothelin in normal and hypertensive rats. Hypertension 46: 943-947, 2005.
7. Brooks WW, Bing OHL, Robinson KG, Slawsky MT, Chaletsky DM, Conrad CH. Effect of angiotensin-converting enzyme inhibition on myocardial fibrosis and function in hypertrophied and failing myocardium from the spontaneously hypertensive rat. Circulation 96: 4002-4010, 1997.
8. Brown NJ, Vaughan DE. Angiotensin-converting enzyme inhibitors. Circulation 97: 1411-1420, 1998.
9. Cai WJ, Kocsis E, Luo X, Schaper W, Schaper J. Expression of endothelial nitric oxide synthase in the vascular wall during arteriogenesis. Mol Cell Biochem 264: 193-200, 2004.
10. Dantas AP, Franco MC, Silva-Antonialli MM, Tostes RCA, Fortes ZB, Nigro D, Carvalho MH. Gender differences in superoxide generation in microvessels of hypertensive rats: role of NAD(P)H-oxidase. Cardiovasc Res 61: 22-29, 2004.
11. Duan J, Murohara T, Ikeda H, Katoh A, Shintani S, Sasaki K, Kawata H, Yamamoto N, Imaizumi T. Hypercholesterolemia inhibits angiogenesis in response to hindlimb ischemia : nitric oxide-dependent mechanism. Circulation 102: III370-III376, 2000.
12. Ebrahimian TG, Tamarat R, Clergue M, Duriez M, Levy BI, Silvestre JS. Dual effect of angiotensin-converting enzyme inhibition on angiogenesis in type 1 diabetic mice. Arterioscler Thromb Vasc Biol 25: 65-70, 2005.
13. Egami K, Murohara T, Shimada T, Sasaki K, Shintani S, Sugaya T, Ishii M, Akagi T, Ikeda H, Matsuishi T, Imaizumi T. Role of host angiotensin II type 1 receptor in tumor angiogenesis and growth. J Clin Invest 112: 67-75, 2003.
14. Ellenby MI, Ernst CB, Carretero OA, Scicli AG. Role of nitric oxide in the effect of blood flow on neointima formation. J Vasc Surg 23: 314-322, 1996.
15. Emanueli C, Salis MB, Figueroa C, Chao J, Chao L, Gaspa L, Capogrossi MC, Madeddu P. Participation of kinins in the captopril-induced inhibition of intimal hyperplasia caused by interruption of carotid blood flow in the mouse. Br J Pharmacol 130: 1076-1082, 2000.
16. Emanueli C, Salis MB, Stacca T, Gaspa L, Chao J, Chao L, Piana A, Madeddu P. Rescue of impaired angiogenesis in spontaneously hypertensive rats by intramuscular human tissue kallikrein gene transfer. Hypertension 38: 136-141, 2001.
17. Emanueli C, Salis MB, Stacca T, Pinna A, Gaspa L, Spano A, Madeddu P. Ramipril improves hemodynamic recovery but not microvascular response to ischemia in spontaneously hypertensive rats. Am J Hypertens 15: 410-415, 2002.
18. Fabre JE, Rivard A, Magner M, Silver M, Isner JM. Tissue inhibition of angiotensin-converting enzyme activity stimulates angiogenesis in vivo. Circulation 99: 3043-3049, 1999.
19. Ferrario CM, Trask AJ, Jessup JA. Advances in biochemical and functional roles of angiotensin-converting enzyme 2 and angiotensin-(1-7) in regulation of cardiovascular function. Am J Physiol Heart Circ Physiol 289: H2281-H2290, 2005.
20. Gagnon C, Legault F, Geraldes P, Tanguay JF, Lambert C. Diverse effects of Ace inhibitors and angiotensin II receptor antagonists on prevention of cardiac hypertrophy and collagen distribution in spontaneously hypertensive rats. Int J Cardiol 97: 373-381, 2004.
21. Griendling KK, FitzGerald GA. Oxidative stress and cardiovascular injury. II. Animal and human studies. Circulation 108: 2034-2040, 2003.
22. Hamilton CA, Brosnan MJ, McIntyre M, Graham D, Dominiczak AF. Superoxide excess in hypertension and aging: a common cause of endothelial dysfunction. Hypertension 37: 529-534, 2001.
23. 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.
24. Ichiki T. Role of renin angiotensin system in angiogenesis: it is still elusive. Arterioscler Thromb Vasc Biol 24: 622-624, 2004.
25. Iyer SN, Ferrario CM, Chappell MC. Angiotensin-(1-7) contributes to the antihypertensive effects of blockade of the renin-angiotensin system. Hypertension 31: 356-361, 1998.
26. Junot C, Menard J, Gonzales MF, Michaud A, Corvol P, Ezan E. In vivo assessment of captopril selectivity of angiotensin I-converting enzyme inhibition: differential inhibition of Acetyl-Ser-Asp-Lys-Pro and angiotensin I hydrolysis. J Pharmacol Exp Ther 289: 1257-1261, 1999.
27. 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.
28. Kobayashi N, DeLano FA, and Schmid-Schonbein GW. Oxidative stress promotes endothelial cell apoptosis loss of microvessels in the spontaneously hypertensive rats. Arterioscler Thromb Vasc Biol 25: 2114-2121, 2005.
29. 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.
30. Lassegue B, Griendling KK. Reactive oxygen species in hypertension: an update. Am J Hypertens 17: 852-860, 2004.
31. Levy BI. How to explain the differences between renin angiotensin system modulators. Am J Hypertens 18: 134-141, 2005.
32. Levy BI, Benessiano J, Henrion D, Caputo L, Heymes C, Duriez M, Poitevin P, Samuel JL. Chronic blockade of AT2-subtype receptors prevents the effect of angiotensin II on the rat vascular structure. J Clin Invest 98: 418-425, 1996.
33. Lewis SJ, Hashmi-Hill MP, Owen JR, Sandock K, Robertson TP, Bates JN. ACE inhibition restores the vasodilator potency of the endothelium-derived relaxing factor, L-S-nitrosocysteine, in conscious spontaneously hypertensive rats. Vascul Pharmacol 44: 491-507, 2006.
34. Matsunaga T, Warltier DC, Weihrauch DW, Moniz M, Tessmer J, Chilian WM. Ischemia-induced coronary collateral growth is dependent on vascular endothelial growth factor and nitric oxide. Circulation 102: 3098-3103, 2000.
35. Miura S, Nishikawa H, Zhang B, Matsuo Y, Kawamura A, Tsuchiya Y, Matsuo K, Saku K. Angiotensin-converting enzyme inhibitor promotes coronary collateral circulation in patients with coronary artery disease. Circ J 67: 535-538, 2003.
36. Miyakawa AA, de Lourdes Junqueira M, Krieger JE. Identification of two novel shear stress responsive elements in rat angiotensin I converting enzyme promoter. Physiol Genomics 17: 107-113, 2004.
37. 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.
38. Napoli C, Sica V, de Nigris F, Pignalosa O, Condorelli M, Ignarro LJ, Liguori A. Sulfhydryl angiotensin-converting enzyme inhibition induces sustained reduction of systemic oxidative stress and improves the nitric oxide pathway in patients with essential hypertension. Am Heart J 148: 172-178, 2004.
39. Nowicki PT, Flavahan S, Hassanain H, Mitra S, Holland S, Goldschmidt-Clermont PJ, Flavahan NA. Redox signaling of the arteriolar myogenic response. Circ Res 89: 114-116, 2001.
40. Otsuka S, Sugano M, Makino N, Sawada S, Hata T, Niho Y. Interaction of mRNAs for angiotensin II type 1 and type 2 receptors to vascular remodeling in spontaneously hypertensive rats. Hypertension 32: 467-472, 1998.
41. Paliege A, Parsumathy 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.
42. Park YM, Park MY, Suh YL, Park JB. NAD(P)H oxidase inhibitor prevents blood pressure elevation and cardiovascular hypertrophy in aldosterone-infused rats. Biochem Biophys Res Commun 313: 812-817, 2004.
43. Rieder MJ, Carmona R, Krieger JE, Pritchard KA Jr, Greene AS. Suppression of angiotensin-converting enzyme expression and activity by shear stress. Circ Res 80: 312-319, 1997.
44. Rivard A, Fabre JE, Silver M, Chen D, Murohara T, Kearney M, Magner M, Asahara T, Isner JM. Age-dependent impairment of angiogenesis. Circulation 99: 111-120, 1999.
45. 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 154: 355-363, 1999.
46. Rizzoni D, Porteri E, Piccoli A, Castellano M, Bettoni G, Muiesan ML, Pasini G, Guelfi D, Mulvany MJ, Rosei EA. Effects of losartan and enalapril on small artery structure in hypertensive rats. Hypertension 32: 305-310, 1998.
47. Sanchez M, Galisteo M, Vera R, Villar IC, Zarzuelo A, Tamargo J, Perez-Vizcaino F, Duarte J. Quercetin downregulates NADPH oxidase, increases eNOS activity and prevents endothelial dysfunction in spontaneously hypertensive rats. J Hypertens 24: 75-84, 2006.
48. Sasaki K, Murohara T, Ikeda H, Sugaya T, Shimada T, Shintani S, Imaizumi T. Evidence for the importance of angiotensin II type 1 receptor in ischemia-induced angiogenesis. J Clin Invest 109: 603-611, 2002.
49. Schiekofer S, Galasso G, Sato K, Kraus BJ, Walsh K. Impaired revascularization in a mouse model of type 2 diabetes is associated with dysregulation of a complex angiogenic-regulatory network. Arterioscler Thromb Vasc Biol 25: 1603-1609, 2005.
50. Schiffrin EL, Thome FS, Genest J. Vascular angiotensin II receptors in SHR. Hypertension 6: 682-688, 1984.
51. Schnackenberg CG, Wilcox CS. Two-week administration of tempol attenuates both hypertension and renal excretion of 8-Iso prostaglandin f2alpha. Hypertension 33: 424-428, 1999.
52. Scribner AW, Loscalzo J, Napoli C. The effect of angiotensin-converting enzyme inhibition on endothelial function and oxidant stress. Eur J Pharmacol 482: 95-99, 2003.
53. Suzuki H, DeLano FA, Parks DA, Jamshidi N, Granger DN, Ishii H, Suematsu M, Zweifach BW, Schmid-Schonbein GW. Xanthine oxidase activity associated with arterial blood pressure in spontaneously hypertensive rats. Proc Natl Acad Sci USA 95: 4754-4759, 1998.
54. Toko H, Zou Y, Minamino T, Sakamoto M, Sano M, Harada M, Nagai T, Sugaya T, Terasaki F, Kitaura Y, Komuro I. Angiotensin II type 1a receptor is involved in cell infiltration, cytokine production, and neovascularization in infarcted myocardium. Arterioscler Thromb Vasc Biol 24: 664-670, 2004.
55. Touyz RM, Schiffrin EL. Reactive oxygen species in vascular biology: implications in hypertension. Histochem Cell Biol 122: 339-352, 2004.
56. Tronc F, Mallat Z, Lehoux S, Wassef M, Esposito B, Tedgui A. Role of matrix metalloproteinases in blood flow-induced arterial enlargement: interaction with NO. Arterioscler Thromb Vasc Biol 20: E120-E126, 2000.
57. Tuttle JL, Condict KW, Bhuller AS, Nachreiner RD, 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.
58. 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.
59. Tuttle JL, Sanders BM, Burkhart HM, Fath SW, Herring BP, Dalsing MC, Unthank JL. Impaired collateral artery development in spontaneously hypertensive rats. Microcirculation 9: 343-351, 2002.
60. Ulker S, McKeown PP, Bayraktutan U. Vitamins reverse endothelial dysfunction through regulation of eNOS and NAD(P)H oxidase activities. Hypertension 41: 534-539, 2003.
61. Unthank JL, Nixon JC, Burkhart HM, Fath SW, Dalsing MC. Early collateral and microvascular adaptations to intestinal artery occlusion in the rat. Am J Physiol Heart Circ Physiol 271: H914-H923, 1996.
62. 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.
63. van Weel V, de Vries M, Voshol PJ, Verloop RE, Eilers PHC, van Hinsbergh VWM, van Bockel JH, Quax PHA. Hypercholesterolemia reduces collateral artery growth more dominantly than hyperglycemia or insulin resistance in mice. Arterioscler Thromb Vasc Biol 26: 1383-1390, 2006.
64. Vicaut E, Hou X. Local renin-angiotensin system in the microcirculation of spontaneously hypertensive rats. Hypertension 24: 70-76, 1994.
65. Volpert OV, Ward WF, Lingen MW, Chesler L, Solt DB, Johnson MD, Molteni A, Polverini PJ, Bouck NP. Captopril inhibits angiogenesis and slows the growth of experimental tumors in rats. J Clin Invest 98: 671-679, 1996.
66. Wang D, Carretero OA, Yang XY, Rhaleb NE, Liu YH, Liao TD, Yang XP. N-acetyl-seryl-aspartyl-lysyl-proline stimulates angiogenesis in vitro and in vivo. Am J Physiol Heart Circ Physiol 287: H2099-H2105, 2004.
67. Welch WJ, Mendonca M, Blau J, Karber A, Dennehy K, Patel K, Lao YS, Jose PA, Wilcox CS. Antihypertensive response to prolonged tempol in the spontaneously hypertensive rat. Kidney Int 68: 179-187, 2005.
68. Yan C, Kim D, Aizawa T, Berk BC. Functional interplay between angiotensin II and nitric oxide: cyclic GMP as a key mediator. Arterioscler Thromb Vasc Biol 23: 26-36, 2003.
69. Yanes L, Romero D, Iliescu R, Cucchiarelli VE, Fortepiani LA, Santacruz F, Bell W, Zhang H, Reckelhoff JF. Systemic arterial pressure response to two weeks of Tempol therapy in SHR: involvement of NO, the RAS, and oxidative stress. Am J Physiol Regul Integr Comp Physiol 288: R903-R908, 2005.
70. 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.
71. Yang HT, Terjung RL. Angiotensin-converting enzyme inhibition increases collateral-dependent muscle blood flow. J Appl Physiol 75: 452-457, 1993.
72. Yu J, deMuinck ED, Zhuang Z, Drinane M, Kauser K, Rubanyi GM, Qian HS, Murata T, Escalante B, Sessa WC. Endothelial nitric oxide synthase is critical for ischemic remodeling, mural cell recruitment, and blood flow reserve. Proc Natl Acad Sci USA 102: 10999-11004, 2005.
73. Zalba G, Beaumont FJ, San Jose G, Fortuno A, Fortuno MA, Etayo JC, Diez J. Vascular NADH/NADPH oxidase is involved in enhanced superoxide production in spontaneously hypertensive rats. Hypertension 35: 1055-1061, 2000.
74. Zhou MS, Jaimes EA, Raij L. Vascular but not cardiac remodeling is associated with superoxide production in angiotensin II hypertension. J Hypertens 23: 1737-1743, 2005.