Effects of aging, TNF-α, and exercise training on angiotensin II-induced vasoconstriction of rat skeletal muscle arterioles

Journal of Applied Physiology

Volumn 113, Issue 7, 2012, Pages 1091-1100

  Park, Yoonjung ^a   Prisby, Rhonda D ^b   Behnke, Brad J ^c   Dominguez II, James M ^c   Lesniewski, Lisa A ^d   Donato, Anthony J ^d   Muller Delp, Judy ^c   Delp, Michael D ^c  

^a TEXAS TECH UNIVERSITY   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; TUMOR NECROSIS FACTOR ALPHA;

AGING; ANIMAL; ANIMAL EXPERIMENT; ARTERIOLE; ARTICLE; DRUG ANTAGONISM; EDUCATION; FISCHER 344 RAT; MALE; METABOLISM; METHODOLOGY; PHYSIOLOGY; RAT; SKELETAL MUSCLE; VASCULAR ENDOTHELIUM; VASCULAR RESISTANCE; VASCULARIZATION; VASOCONSTRICTION;

AGING; ANGIOTENSIN II; ANIMALS; ARTERIOLES; EDUCATION; ENDOTHELIUM, VASCULAR; MALE; MUSCLE, SKELETAL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, INBRED F344; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR RESISTANCE; VASOCONSTRICTION;

EID: 84867029040     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00292.2012     Document Type: Article

References (67)

1. Aoki N, Siegfried M, Lefer AM. Anti-EDRF effect of tumor necrosis factor in isolated, perfused cat carotid arteries. Am J Physiol Heart Circ Physiol 256: H1509-H1512, 1989.
2. Beere PA, Russell SD, Morey MC, Kitzman DW, Higginbotham MB. Aerobic exercise training can reverse age-related peripheral circulatory changes in healthy older men. Circulation 100: 1085-1094, 1999.
3. Behnke BJ, Delp MD, Dougherty PJ, Musch TI, Poole DC. Effects of aging on microvascular oxygen pressures in rat skeletal muscle. Respir Physiol Neurobiol 146: 259-268, 2005.
4. Belmin J, Bernard C, Corman B, Merval R, Esposito B, Tedgui A. Increased production of tumor necrosis factor and interleukin-6 by arterial wall of aged rats. Am J Physiol Heart Circ Physiol 268: H2288-H2293, 1995.
5. Berry C, Touyz R, Dominiczak AF, Webb RC, Johns DG. Angiotensin receptors: signaling, vascular pathophysiology, and interactions with ceramide. Am J Physiol Heart Circ Physiol 281: H2337-H2365, 2001.
6. Booth AD, Jayne DR, Kharbanda RK, McEniery CM, Mackenzie IS, Brown J, Wilkinson IB. Infliximab improves endothelial dysfunction in systemic vasculitis: a model of vascular inflammation. Circulation 109: 1718-1723, 2004.
7. Boulanger CM, Caputo L, Levy B. Endothelial AT1-mediated release of nitric oxide decreases angiotensin II contractions in rat carotid artery. Hypertension 26: 752-757, 1995.
8. Bruunsgaard H, Skinhoj P, Pedersen AN, Schroll M, Pedersen BK. Ageing, tumour necrosis factor-alpha (TNF-alpha) and atherosclerosis. Clin Exp Immunol 121: 255-260, 2000.
9. Carey RM, Wang ZQ, Siragy HM. Update: role of the angiotensin type-2 [AT(2)] receptor in blood pressure regulation. Curr Hypertens Rep 2: 198-201, 2000.
10. Csiszar A, Labinskyy N, Smith K, Rivera A, Orosz Z, Ungvari Z. Vasculoprotective effects of anti-tumor necrosis factor-treatment in aging. Am J Pathol 170: 388-398, 2007.
11. Csiszar A, Wang M, Lakatta EG, Ungvari Z. Inflammation and endothelial dysfunction during aging: role of NF-B. J Appl Physiol 105: 1333-1341, 2008.
12. Delp MD, Behnke BJ, Spier SA, Wu G, Muller-Delp JM. Ageing diminishes endothelium-dependent vasodilatation and tetrahydrobiopterin content in rat skeletal muscle arterioles. J Physiol 586: 1161-1168, 2008.
13. Delp MD, Duan C. Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J Appl Physiol 80: 261-270, 1996.
14. Delp MD, Laughlin MH. Time course of enhanced endothelium-mediated dilation in aorta of trained rats. Med Sci Sports Exerc 29: 1454-1461, 1997.
15. Delp MD, McAllister RM, Laughlin MH. Exercise training alters endothelium-dependent vasoreactivity of rat abdominal aorta. J Appl Physiol 75: 1354-1363, 1993.
16. DeSouza CA, Clevenger CM, Greiner JJ, Smith DT, Hoetzer GL, Shapiro LF, Stauffer BL. Evidence for agonist-specific endothelial vasodilator dysfunction with ageing in healthy humans. J Physiol 542: 255-262, 2002.
17. DeSouza CA, Shapiro LF, Clevenger CM, Dinenno FA, Monahan KD, Tanaka H, Seals DR. Regular aerobic exercise prevents and restores age-related declines in endothelium-dependent vasodilation in healthy men. Circulation 102: 1351-1357, 2000.
18. Dinenno FA, Jones PP, Seals DR, Tanaka H. Limb blood flow and vascular conductance are reduced with age in healthy humans: relation to elevations in sympathetic nerve activity and declines in oxygen demand. Circulation 100: 164-170, 1999.
19. Donato AJ, Black AD, Jablonski KL, Gano LB, Seals DR. Aging is associated with greater nuclear NF-B, reduced I-B-, and increased expression of proinflammatory cytokines in vascular endothelial cells of healthy humans. Aging Cell 7: 805-812, 2008.
20. Donato AJ, Lesniewski LA, Delp MD. The effects of aging and exercise training on endothelin-1 vasoconstrictor responses in rat skeletal muscle arterioles. Cardiovasc Res 66: 393-401, 2005.
21. Donato AJ, Lesniewski LA, Delp MD. The effects of aging and exercise training on adrenergic vasoreactivity in skeletal muscle arterioles. J Physiol 579: 115-125, 2007.
22. Dudley GA, Abraham WM, Terjung RL. Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle. J Appl Physiol 53: 844-850, 1982.
23. Edwards CK 3rd, Martin SW, Seely J, Kinstler O, Buckel S, Bendele AM, Ellen Cosenza M, Feige U, Kohno T. Design of PEGylated soluble tumor necrosis factor receptor type I (PEG sTNF-RI) for chronic inflammatory diseases. Adv Drug Deliv Rev 55: 1315-1336, 2003.
24. Fichtlscherer S, Rossig L, Breuer S, Vasa M, Dimmeler S, Zeiher AM. Tumor necrosis factor antagonism with etanercept improves systemic endothelial vasoreactivity in patients with advanced heart failure. Circulation 104: 3023-3025, 2001.
25. 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.
26. Gerhard M, Roddy MA, Creager SJ, Creager MA. Aging progressively impairs endothelium-dependent vasodilation in forearm resistance vessels of humans. Hypertension 27: 849-853, 1996.
27. Goodwin BL, Pendleton LC, Levy MM, Solomonson LP, Eichler DC. Tumor necrosis factor-alpha reduces argininosuccinate synthase expression and nitric oxide production in aortic endothelial cells. Am J Physiol Heart Circ Physiol 293: H1115-H1121, 2007.
28. Greiwe JS, Chang B, Rubin DC, Yarasheski KE, Semenkovich CF. Resistance exercise decreases skeletal muscle tumor necrosis factor alpha in frail elderly humans. FASEB J 15: 475-482, 2001.
29. Gruetter CA, Ryan ET, Lemke SM, Fox MK, Schoepp DD. Endothelium-dependent modulation of angiotensin II-induced contraction in blood vessels. Eur J Pharmacol 146: 85-95, 1988.
30. Haberl RL, Anneser F, Villringer A, Einhaupl KM. Angiotensin II induces endothelium-dependent vasodilation of rat cerebral arterioles. Am J Physiol Heart Circ Physiol 258: H1840-H1846, 1990.
31. Hannan RE, Widdop RE. Vascular angiotensin II actions mediated by angiotensin II type 2 receptors. Curr Hypertens Rep 6: 117-123, 2004.
32. Hennington BS, Zhang H, Miller MT, Granger JP, Reckelhoff JF. Angiotensin II stimulates synthesis of endothelial nitric oxide synthase. Hypertension 31: 283-288, 1998.
33. Holloszy JO, Kohrt WM. Exercise. In: Handbook of Physiology. Aging. Bethesda, MD: Am. Physiol. Soc., 1995, sect. 11, chapt. 24, p. 633-666.
34. Joyner W, Davis M. Pressure profile along the microvascular network and its control. Fed Proc 46: 266-269, 1987.
35. Lawrenson L, Poole JG, Kim J, Brown C, Patel P, Richardson RS. Vascular and metabolic response to isolated small muscle mass exercise: effect of age. Am J Physiol Heart Circ Physiol 285: H1023-H1031, 2003.
36. Martin WHI, Kohrt WM, Malley MT, Korte E, Stoltz S. Exercise training enhances leg vasodilatory capacity of 65-yr-old men and women. J Appl Physiol 69: 1804-1809, 1990.
37. Matrougui K, Loufrani L, Heymes C, Levy BI, Henrion D. Activation of AT2 receptors by endogenous angiotensin II is involved in flowinduced dilation in rat resistance arteries. Hypertension 34: 659-665, 1999.
38. McCurdy MR, Colleran PN, Muller-Delp J, Delp MD. Physiology of a microgravity environment: selected contribution: effects of fiber composition and hindlimb unloading on the vasodilator properties of skeletal muscle arterioles. J Appl Physiol 89: 398-405, 2000.
39. Meininger G, Harris P, Joshua I. Distributions of microvascular pressure in skeletal muscle of one-kidney, one clip, two-kidney, one clip, and deoxycorticosterone-salt hypertensive rats. Hypertension 6: 27-34, 1984.
40. Muller-Delp J, Spier SA, Ramsey MW, Lesniewski LA, Papadopoulos A, Humphrey JD, Delp MD. Effects of aging on vasoconstrictor and mechanical properties of rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 282: H1843-H1854, 2002.
41. 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.
42. Olson SC, Dowds TA, Pino PA, Barry MT, Burke-Wolin T. ANG II stimulates endothelial nitric oxide synthase expression in bovine pulmonary artery endothelium. Am J Physiol Lung Cell Mol Physiol 273: L315-L321, 1997.
43. Payne GW. Effect of inflammation on the aging microcirculation: Impact on skeletal muscle blood flow control. Microcirculation 13: 343-352, 2006.
44. Picchi A, Gao X, Belmadani S, Potter BJ, Focardi M, Chilian WM, Zhang C. Tumor necrosis factor-alpha induces endothelial dysfunction in the prediabetic metabolic syndrome. Circ Res 99: 69-77, 2006.
45. Pinaud F, Bocquet A, Dumont O, Retailleau K, Baufreton C, Andriantsitohaina R, Loufrani L, Henrion D. Paradoxical role of angiotensin II type 2 receptors in resistance arteries of old rats. Hypertension 50: 96-102, 2007.
46. Proctor DN, Koch DW, Newcomer SC, Le KU, Leuenberger UA. Impaired leg vasodilation during dynamic exercise in healthy older women. J Appl Physiol 95: 1963-1970, 2003.
47. Proctor DN, Shen PH, Dietz NM, Eickhoff TJ, Lawler LA, Ebersold EJ, Loeffler DL, Joyner MJ. Reduced leg blood flow during dynamic exercise in older endurance-trained men. J Appl Physiol 85: 68-75, 1998.
48. Pueyo ME, Arnal JF, Rami J, Michel JB. Angiotensin II stimulates the production of NO and peroxynitrite in endothelial cells. Am J Physiol Cell Physiol 274: C214-C220, 1998.
49. Schulz S, Schagdarsurengin U, Suss T, Muller-Werdan U, Werdan K, Glaser C. Relation between the tumor necrosis factor-alpha (TNF-alpha) gene and protein expression, and clinical, biochemical, and genetic markers: age, body mass index and uric acid are independent predictors for an elevated TNF-alpha plasma level in a complex risk model. Eur Cytokine Netw 15: 105-111, 2004.
50. Sindler AL, Delp MD, Reyes R, Wu G, Muller-Delp JM. Effects of aging and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J Physiol 587: 3885-3897, 2009.
51. 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.
52. Spier SA, Laughlin MH, Delp MD. Effects of acute and chronic exercise on vasoconstrictor responsiveness of rat abdominal aorta. J Appl Physiol 87: 1752-1757, 1999.
53. Srere PA. Citrate synthase. Methods Enzymol 13: 3-5, 1969.
54. Stebbins CL, Symons JD. Role of angiotensin II in hemodynamic responses to dynamic exercise in miniswine. J Appl Physiol 78: 185-190, 1995.
55. Sun D, Huang A, Koller A, Kalley G. Short-term daily exercise activity enhances endothelial NO synthesis in skeletal muscle arterioles of rats. J Appl Physiol 76: 2241-2247, 1994.
56. Symons JD, Musch TI, Hageman KS, Stebbins CL. Regional blood flow responses to acute ANGII infusion: effects of nitric oxide synthase inhibition. J Cardiovasc Pharmacol 34: 116-123, 1999.
57. Symons JD, Stebbins CL, Musch TI. Interactions between angiotensin II and nitric oxide during exercise in normal and heart failure rats. J Appl Physiol 87: 574-581, 1999.
58. 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.
59. Tidgren B, Hjemdahl P, Theodorsson E, Nussberger J. Renal neurohormonal and vascular responses to dynamic exercise in humans. J Appl Physiol 70: 2279-2286, 1991.
60. Touyz RM, Schiffrin EL. Signal transduction mechanisms mediating the physiological and pathophysiological actions of angiotensin II in vascular smooth muscle cells. Pharmacol Rev 52: 639-672, 2000.
61. Warren JH, Lewis W, Wraa CE, Stebbins CL. Central and peripheral effects of angiotensin II on the cardiovascular response to exercise. J Cardiovasc Pharmacol 38: 693-705, 2001.
62. Wiemer G, Schölkens BA, Busse R, Wagner A, Heitsch H, Linz W. The functional role of angiotensin II subtype AT2-receptors in endothelial cells and isolated ischemic rat hearts. Pharm Pharmacol Lett 3: 24-27, 1993.
63. 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.
64. Wray DW, Nishiyama SK, Harris RA, Richardson RS. Angiotensin II in the elderly: impact of angiotensin II type 1 receptor sensitivity on peripheral hemodynamics. Hypertension 51: 1611-1616, 2008.
65. Xia Z, Liu M, Wu Y, Sharma V, Luo T, Ouyang J, McNeill JH. N-acetylcysteine attenuates TNF-alpha-induced human vascular endothelial cell apoptosis and restores eNOS expression. Eur J Pharmacol 550: 134-142, 2006.
66. Zhang C, Hein TW, Wang W, Kuo L. Divergent roles of angiotensin II AT1 and AT2 receptors in modulating coronary microvascular function. Circ Res 92: 322-329, 2003.
67. Zhang JJ, Van Meel CA, Pfaffendorf M, Zhang J, Van Zwiten PA. Endothelium-dependent, nitric oxide-mediated inhibition of angiotensin II-induced contraction in rabbit aorta. Eur J Pharmacol 262: 247-253, 1994.