Aging impairs flow-induced dilation in coronary arterioles: Role of NO and H2O2

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 297, Issue 3, 2009, Pages

  Kang, Lori S ^a,b   Reyes, Rafael A ^c   Muller Delp, Judy M ^c  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Center for Interdisciplinary Research in Cardiovascular Sciences   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Deferoxamine; Hydrogen peroxide; Hydroxyl radical; Nitric oxide; Reactive oxygen species; Superoxide dismutase

Indexed keywords

DEFEROXAMINE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TEMPOL;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; CORONARY ARTERY; CORONARY ARTERY BLOOD FLOW; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; IMMUNOBLOTTING; ISCHEMIC HEART DISEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; VASODILATATION;

AGING; ANIMALS; ANTIOXIDANTS; ARTERIOLES; CATALASE; CORONARY CIRCULATION; CYCLIC N-OXIDES; DEFEROXAMINE; HYDROGEN PEROXIDE; MALE; MICROSCOPY, FLUORESCENCE; NITRIC OXIDE; RATS; RATS, INBRED F344; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SIDEROPHORES; SPIN LABELS; SUPEROXIDE DISMUTASE; TYROSINE; VASODILATION;

EID: 69249106918     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00356.2009     Document Type: Article

References (51)

1. Blackwell KA, Sorenson JP, Richardson DM, Smith LA, Suda O, Nath K, Katusic ZS. Mechanisms of aging-induced impairment of endothelium-dependent relaxation: role of tetrahydrobiopterin. Am J Physiol Heart Circ Physiol 287: H2448-H2453, 2004.
2. Bulvik B, Grinberg L, Eliashar R, Berenshtein E, Chevion MM. Iron, ferritin and proteins of the methionine-centered redox cycle in young and old rat hearts. Mech Ageing Dev 130: 139-144, 2009.
3. Carroll RT, Galatsis P, Borosky S, Kopec KK, Kumar V, Althaus JS, Hall ED. 4-Hydroxy-2,2,6,6-tetramethylpiperidine-1-oxyl (Tempol) inhibits peroxynitrite-mediated phenol nitration. Chem Res Toxicol 13: 294-300, 2000.
4. Celermajer DS, Sorensen KE, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Deanfield JE. Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 24: 471-476, 1994.
5. Chilian WM, Eastham CL, Marcus ML. Microvascular distribution of coronary vascular resistance in beating left ventricle. Am J Physiol Heart Circ Physiol 251: H779-H788, 1986.
6. Cooke CL, Davidge ST. Endothelial-dependent vasodilation is reduced in mesenteric arteries from superoxide dismutase knockout mice. Cardiovasc Res 60: 635-642, 2003.
7. Csiszar A, Ungvari Z, Edwards JG, Kaminski P, Wolin MS, Koller A, Kaley G. Aging-induced phenotypic changes and oxidative stress impair coronary arteriolar function. Circ Res 90: 1159-1166, 2002.
8. Delp MD, Evans MV, Duan C. Effects of aging on cardiac output, regional blood flow, and body composition in Fischer-344 rats. J Appl Physiol 85: 1813-1822, 1998.
9. Didion SP, Ryan MJ, Baumbach GL, Sigmund CD, Faraci FM. Superoxide contributes to vascular dysfunction in mice that express human renin and angiotensinogen. Am J Physiol Heart Circ Physiol 283: H1569-H1576, 2002.
10. Donato AJ, Eskurza I, Silver AE, Levy AS, Pierce GL, Gates PE, Seals DR. Direct evidence of endothelial oxidative stress with aging in humans: relation to impaired endothelium-dependent dilation and upregulation of nuclear factor-kappaB. Circ Res 100: 1659-1666, 2007.
11. Emsley AM, Jeremy JY, Gomes GN, Angelini GD, Plane F. Investigation of the inhibitory effects of homocysteine and copper on nitric oxide-mediated relaxation of rat isolated aorta. Br J Pharmacol 126: 1034-1040, 1999.
12. Feng MG, Dukacz SA, Kline RL. Selective effect of tempol on renal medullary hemodynamics in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 281: R1420-R1425, 2001.
13. Fleming DJ, Jacques PF, Tucker KL, Massaro JM, D'Agostino RB Sr, Wilson PW, Wood RJ. Iron status of the free-living, elderly Framingham Heart Study cohort: an iron-replete population with a high prevalence of elevated iron stores. Am J Clin Nutr 73: 638-646, 2001.
14. Gao X, Belmadani S, Picchi A, Xu X, Potter BJ, Tewari-Singh N, Capobianco S, Chilian WM, Zhang C. Tumor necrosis factor-alpha induces endothelial dysfunction in Lepr(db) mice. Circulation 115: 245-254, 2007.
15. Hachamovitch R, Wicker P, Capasso JM, Anversa P. Alterations of coronary blood flow and reserve with aging in Fischer 344 rats. Am J Physiol Heart Circ Physiol 256: H66-H73, 1989.
16. Herspring KF, Ferreira LF, Copp SW, Snyder BS, Poole DC, Musch TI. Effects of antioxidants on contracting spinotrapezius muscle microvascular oxygenation and blood flow in aged rats. J Appl Physiol 105: 1889-1896, 2008.
17. Horiuchi M, Tsutsui M, Tasaki H, Morishita T, Suda O, Nakata S, Nihei S, Miyamoto M, Kouzuma R, Okazaki M, Yanagihara N, Adachi T, Nakashima Y. Upregulation of vascular extracellular superoxide dismutase in patients with acute coronary syndromes. Arterioscler Thromb Vasc Biol 24: 106-111, 2004.
18. 2 contribute to reactive dilation of isolated coronary arterioles. Am J Physiol Heart Circ Physiol 287: H2461-H2467, 2004.
19. Kuo L, Chilian WM, Davis MJ. Interaction of pressure- and flow-induced responses in porcine coronary resistance vessels. Am J Physiol Heart Circ Physiol 261: H1706-H1715, 1991.
20. Kuo L, Davis MJ, Chilian WM. Endothelium-dependent, flow-induced dilation of isolated coronary arterioles. Am J Physiol Heart Circ Physiol 259: H1063-H1070, 1990.
21. LeBlanc AJ, Shipley RD, Kang LS, Muller-Delp JM. Age impairs Flk-1 signaling and NO-mediated vasodilation in coronary arterioles. Am J Physiol Heart Circ Physiol 295: H2280-H2288, 2008.
22. Li J, Li W, Liu W, Altura BT, Altura BM. Mechanisms of hydroxyl radical-induced contraction of rat aorta. Eur J Pharmacol 499: 171-178, 2004.
23. Liu Y, Li H, Bubolz AH, Zhang DX, Gutterman DD. Endothelial cytoskeletal elements are critical for flow-mediated dilation in human coronary arterioles. Med Biol Eng Comput 46: 469-478, 2008.
24. Miura H, Bosnjak JJ, Ning G, Saito T, Miura M, Gutterman DD. Role for hydrogen peroxide in flow-induced dilation of human coronary arterioles. Circ Res 92: e31-e40, 2003.
25. Morikawa K, Fujiki T, Matoba T, Kubota H, Hatanaka M, Takahashi S, Shimokawa H. Important role of superoxide dismutase in EDHF-mediated responses of human mesenteric arteries. J Cardiovasc Pharmacol 44: 552-556, 2004.
26. Muller-Delp JM, Spier SA, Ramsey MW, Delp MD. Aging impairs endothelium-dependent vasodilation in rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 283: H1662-H1672, 2002.
27. Newaz MA, Yousefipour Z, Oyekan A. Oxidative stress-associated vascular aging is xanthine oxidase-dependent but not NAD(P)H oxidase-dependent. J Cardiovasc Pharmacol 48: 88-94, 2006.
28. Phillips SA, Hatoum OA, Gutterman DD. The mechanism of flow-induced dilation in human adipose arterioles involves hydrogen peroxide during CAD. Am J Physiol Heart Circ Physiol 292: H93-H100, 2007.
29. Pittner J, Wolgast M, Persson AE. Perfusate composition influences nitric oxide homeostasis in rat juxtamedullary afferent arterioles. Acta Physiol Scand 179: 85-91, 2003.
30. 2 activates redox- and 4-aminopyridine-sensitive Kv channels in coronary vascular smooth muscle. Am J Physiol Heart Circ Physiol 292: H1404-H1411, 2007.
31. + channels. Am J Physiol Heart Circ Physiol 291: H2473-H2482, 2006.
32. Saitoh S, Zhang C, Tune JD, Potter B, Kiyooka T, Rogers PA, Knudson JD, Dick GM, Swafford A, Chilian WM. Hydrogen peroxide: a feed-forward dilator that couples myocardial metabolism to coronary blood flow. Arterioscler Thromb Vasc Biol 26: 2614-2621, 2006.
33. Samora JB, Frisbee JC, Boegehold MA. Hydrogen peroxide emerges as a regulator of tone in skeletal muscle arterioles during juvenile growth. Microcirculation 15: 151-161, 2008.
34. Sato A, Sakuma I, Gutterman DD. Mechanism of dilation to reactive oxygen species in human coronary arterioles. Am J Physiol Heart Circ Physiol 285: H2345-H2354, 2003.
35. Shipley RD, Muller-Delp JM. Aging decreases vasoconstrictor responses of coronary resistance arterioles through endothelium-dependent mechanisms. Cardiovasc Res 66: 374-383, 2005.
36. Smith SH, Kramer MF, Reis I, Bishop SP, Ingwall JS. Regional changes in creatine kinase and myocyte size in hypertensive and nonhypertensive cardiac hypertrophy. Circ Res 67: 1334-1344, 1990.
37. Sorop O, Spaan JA, Sweeney TE, VanBavel E. Effect of steady versus oscillating flow on porcine coronary arterioles: involvement of NO and superoxide anion. Circ Res 92: 1344-1351, 2003.
38. Spiekermann S, Landmesser U, Dikalov S, Bredt M, Gamez G, Tatge H, Reepschlager N, Hornig B, Drexler H, Harrison DG. Electron spin resonance characterization of vascular xanthine and NAD(P)H oxidase activity in patients with coronary artery disease: relation to endothelium-dependent vasodilation. Circulation 107: 1383-1389, 2003.
39. Spier SA, Delp MD, Meininger CJ, Donato AJ, Ramsey MW, Muller-Delp JM. Effects of ageing and exercise training on endothelium-dependent vasodilatation and structure of rat skeletal muscle arterioles. J Physiol 556: 947-958, 2004.
40. Subramaniam R, Fan XJ, Scivittaro V, Yang J, Ha CE, Petersen CE, Surewicz WK, Bhagavan NV, Weiss MF, Monnier VM. Cellular oxidant stress and advanced glycation endproducts of albumin: caveats of the dichlorofluorescein assay. Arch Biochem Biophys 400: 15-25, 2002.
41. Sun D, Huang A, Yan EH, Wu Z, Yan C, Kaminski PM, Oury TD, Wolin MS, Kaley G. Reduced release of nitric oxide to shear stress in mesenteric arteries of aged rats. Am J Physiol Heart Circ Physiol 286: H2249-H2256, 2004.
42. Sylven C, Lin L, Kallner A, Jansson F. Regional distribution of citrate synthase and lactate dehydrogenase isoenzymes in the bovine heart. Acta Physiol Scand 136: 331-337, 1989.
43. Taddei S, Galetta F, Virdis A, Ghiadoni L, Salvetti G, Franzoni F, Giusti C, Salvetti A. Physical activity prevents age-related impairment in nitric oxide availability in elderly athletes. Circulation 101: 2896-2901, 2000.
44. Tanguy S, Boucher F, Toufektsian MC, Besse S, de Leiris J. Aging exacerbates hydrogen peroxide-induced alteration of vascular reactivity in rats. Antioxid Redox Signal 2: 363-368, 2000.
45. 2 impairs endothelium-dependent nitric oxide-mediated dilation of coronary arterioles. Arterioscler Thromb Vasc Biol 26: 2035-2042, 2006.
46. Thengchaisri N, Kuo L. Hydrogen peroxide induces endothelium-dependent and -independent coronary arteriolar dilation: role of cyclooxygenase and potassium channels. Am J Physiol Heart Circ Physiol 285: H2255-H2263, 2003.
47. 2 and endothelium-dependent cerebral arteriolar dilation. Implications for the identity of endothelium-derived relaxing factor generated by acetylcholine. Hypertension 16: 162-169, 1990.
48. Wenzel P, Schuhmacher S, Kienhofer J, Muller J, Hortmann M, Oelze M, Schulz E, Treiber N, Kawamoto T, Scharffetter-Kochanek K, Munzel T, Burkle A, Bachschmid MM, Daiber A. Manganese superoxide dismutase and aldehyde dehydrogenase deficiency increase mitochondrial oxidative stress and aggravate age-dependent vascular dysfunction. Cardiovasc Res 80: 280-289, 2008.
49. Woodman CR, Price EM, Laughlin MH. Aging induces muscle-specific impairment of endothelium-dependent dilation in skeletal muscle feed arteries. J Appl Physiol 93: 1685-1690, 2002.
50. Yada T, Shimokawa H, Morikawa K, Takaki A, Shinozaki Y, Mori H, Goto M, Ogasawara Y, Kajiya F. Role of Cu,Zn-SOD in the synthesis of endogenous vasodilator hydrogen peroxide during reactive hyperemia in mouse mesenteric microcirculation in vivo. Am J Physiol Heart Circ Physiol 294: H441-H448, 2008.
51. Zollner S, Haseloff RF, Kirilyuk IA, Blasig IE, Rubanyi GM. Nitroxides increase the detectable amount of nitric oxide released from endothelial cells. J Biol Chem 272: 23076-23080, 1997.