Nitric oxide and muscle blood flow in exercise

Applied Physiology, Nutrition and Metabolism

Volumn 33, Issue 1, 2008, Pages 151-161

  Tschakovsky, Michael E ^a   Joyner, Michael J ^b  

^a QUEEN S UNIVERSITY   (Canada)

^b DEPARTMENT OF UROLOGY   (United States)

Author keywords

Endothelium; eNOS; Hyperemia; nNOS; Vasodilation

Indexed keywords

NITRIC OXIDE;

ANIMAL; ANIMAL EXPERIMENT; BLOOD FLOW; BLOOD VESSEL; CONFERENCE PAPER; EXERCISE; HUMAN; INNERVATION; PHYSIOLOGY; SKELETAL MUSCLE; VASCULARIZATION;

ANIMALS; BLOOD VESSELS; EXERCISE; HUMANS; MUSCLE, SKELETAL; NITRIC OXIDE; PHYSICAL CONDITIONING, ANIMAL; REGIONAL BLOOD FLOW;

EID: 39749120410     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H07-148     Document Type: Conference Paper

References (81)

1. Andersen, P., and Saltin, B. 1985. Maximal perfusion of skeletal muscle in human. J. Physiol. 366: 233-249.
2. Boushel, R., Langberg, H., Gemmer, C., Olesen, J., Crameri, R., Scheede, C., et al. 2002. Combined inhibition of nitric oxide and prostaglandins reduces human skeletal muscle blood flow during exercise. J. Physiol. 543: 691-698. doi:10.1113/jphysiol.2002.021477.
3. Britton, S.L., Metting, P.J., Ronau, T.F., Strader, J.R., and Weldy, D.L. 1985. Autoregulation of hind-limb blood flow in conscious dogs. J. Physiol. 368: 409-422.
4. Brock, R.W., Tschakovsky, M.E., Shoemaker, J.K., Halliwill, J.R., Joyner, M.J., and Hughson, R.L. 1998. Effects of acetylcholine and nitric oxide on forearm blood flow at rest and after a single muscle contraction. J. Appl. Physiol. 85: 2249-2254.
5. Buckwalter, J.B., Mueller, P.J., and Clifford, P.S. 1997. Sympathetic vasoconstriction in active skeletal muscles during dynamic exercise. J. Appl. Physiol. 83: 1575-1580.
6. Buckwalter, J.B., Taylor, J.C., Hamann, J.J., and Clifford, P.S. 2004. Role of nitric oxide in exercise sympatholysis. J. Appl. Physiol. 97: 417-423. doi:10.1152/japplphysiol.01181.2003.
7. Budel, S., Bartlett, I.S., and Segal, S.S. 2003. Homocellular conduction along endothelium and smooth muscle of arterioles in hamster cheek pouch: unmasking an NO wave. Circ. Res. 93: 61-68. doi:10.1161/01.RES. 0000080318.81205.FD.
8. Calbet, J.A. 2000. Oxygen tension and content in the regulation of limb blood flow. Acta Physiol. Scand. 168: 465-472. doi:10.1046/j.1365-201x. 2000.00698.x.
9. Cherry, P.D., Furchgott, R.F., Zawadzki, J.V., and Jothianandan, D. 1982. Role of endothelial cells in relaxation of isolated arteries by bradykinin. Proc. Natl. Acad. Sci. U.S.A. 79: 2106-2110. doi:10.1073/pnas.79.6.2106.
10. Clifford, P.S., and Hellsten, Y. 2004. Vasodilatory mechanisms in contracting skeletal muscle. J. Appl. Physiol. 97: 393-403. doi:10.1152/japplphysiol.00179.2004.
11. Clifford, P.S., Kluess, H.A., Hamann, J.J., Buckwalter, J.B., and Jasperse, J.L. 2006. Mechanical compression elicits vasodilatation in rat skeletal muscle feed arteries. J. Physiol. 572: 561-567. doi:10.1113/jphysiol.2005.099507.
12. Cohen, K.D., and Sarelius, I.H. 2002. Muscle contraction under capillaries in hamster muscle induces arteriolar dilatation via K(ATP) channels and nitric oxide. J. Physiol. 539: 547-555. doi:10.1113/jphysiol.2001. 013388.
13. Dinenno, F.A., and Joyner, M.J. 2003. Blunted sympathetic vasoconstriction in contracting skeletal muscle of healthy humans: is nitric oxide obligatory? J. Physiol. 553: 281-292. doi:10.1113/jphysiol.2003. 049940.
14. Dinenno, F.A., and Joyner, M.J. 2004. Combined NO and PG inhibition augments alpha-adrenergic vasoconstriction in contracting human skeletal muscle. Am. J. Physiol. Heart Circ. Physiol. 287: H2576-H2584. doi:10.1152/ajpheart.00621.2004.
15. Duffy, S.J., New, G., Tran, B.T., Harper, R.W., and Meredith, I.T. 1999. Relative contribution of vasodilator prostanoids and NO to metabolic vasodilation in the human forearm. Am. J. Physiol. 276: H663-H670.
16. Dyke, C.K., Proctor, D.N., Dietz, N.M., and Joyner, M.J. 1995. Role of nitric oxide in exercise hyperaemia during prolonged rhythmic handgripping in humans. J. Physiol. 488: 259-265.
17. Dyke, C.K., Dietz, N.M., Lennon, R.L., Warner, D.O., and Joyner, M.J. 1998. Forearm blood flow responses to handgripping after local neuromuscular blockade. J. Appl. Physiol. 84: 754-758.
18. Ellsworth, M.L. 2004. Red blood cell-derived ATP as a regulator of skeletal muscle perfusion. Med. Sci. Sports Exerc. 36: 35-41. doi:10.1249/01.MSS.0000106284.80300.B2.
19. Endo, T., Imaizumi, T., Tagawa, T., Shiramoto, M., Ando, S., and Takeshita, A. 1994. Role of nitric oxide in exercise-induced vasodilation of the forearm. Circulation, 90: 2886-2890.
20. Fadel, P.J., Ogoh, S., Watenpaugh, D.E., Wasmund, W., Olivencia-Yurvati, A., Smith, M.L., et al. 2001. Carotid baroreflex regulation of sympathetic nerve activity during dynamic exercise in humans. Am. J. Physiol. Heart Circ. Physiol. 280: H1383-H1390.
21. Frandsenn, U., Bangsbo, J., Sander, M., Hoffner, L., Betak, A., Saltin, B., et al. 2001. Exercise-induced hyperaemia and leg oxygen uptake are not altered during effective inhibition of nitric oxide synthase with N(G)-nitro-L-arginine methyl ester in humans. J. Physiol. 531: 257-264. doi:10.1111/j.1469-7793.2001.0257j.x.
22. Frisbee, J.C. 2002. Regulation of in situ skeletal muscle arteriolar tone: interactions between two parameters. Microcirculation, 9: 443-462. doi:10.1038/sj.mn.7800160.
23. Furchgott, R.F. 1988. Studies on relaxation of rabbit aorta by sodium nitrite: the basis for the proposal that the acid-activatable inhibitory factor from retractor penis is inorganic nitrite and the endothelium-derived relaxing factor is nitric oxide. In Vasodilatation: Vascular Smooth Muscle, Peptides, and Endothelium, ed. Vanhoutte, P. M., pp. 401-414. Raven Press, New York.
24. Furchgott, R.F., and Zawadzki, J.V. 1980. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature, 288: 373-376. doi:10.1038/288373a0.
25. Gilligan, D.M., Panza, J.A., Kilcoyne, C.M., Waclawiw, M.A., Casino, P.R., and Quyyumi, A.A. 1994. Contribution of endothelium-derived nitric oxide to exercise-induced vasodilation. Circulation, 90: 2853-2858.
26. Gordon, M.B., Jain, R., Beckman, J.A., and Creager, M.A. 2002. The contribution of nitric oxide to exercise hyperemia in the human forearm. Vasc. Med. 7: 163-168. doi:10.1191/1358863x02vm439oa.
27. Grange, R.W., Isotani, E., Lau, K.S., Kamm, K.E., Huang, P.L., and Stull, J.T. 2001. Nitric oxide contributes to vascular smooth muscle relaxation in contracting fast-twitch muscles. Physiol. Genomics, 5: 35-44.
28. Green, D.J., O'Driscoll, G., Blanksby, B.A., and Taylor, R.R. 1996. Control of skeletal muscle blood flow during dynamic exercise: contribution of endothelium-derived nitric oxide. Sports Med. 21: 119-146.
29. Haddy, F.J. 1983. Potassium effects on contraction in arterial smooth muscle mediated by Na+, K+-ATPase. Fed. Proc. 42: 239-245.
30. Hamann, J.J., Kluess, H.A., Buckwalter, J.B., and Clifford, P.S. 2005. Blood flow response to muscle contractions is more closely related to metabolic rate than contractile work. J. Appl. Physiol. 98: 2096-2100. doi:10.1152/japplphysiol.00400.2004.
31. Hilsted, J., Galbo, H., Christensen, N.J., Parving, H.H., and Benn, J. 1982. Haemodynamic changes during graded exercise in patients with diabetic autonomic neuropathy. Diabetologia, 22: 318-323. doi:10.1007/BF00253574.
32. Hnik, P., Vyskocil, N., Kriz, N., and Holas, M. 1972. Work-induced increase of extracellular potassium concentration in muscle measured by ion-specific electrodes. Brain Res. 40: 559-562. doi:10.1016/0006- 8993(72)90162-X.
33. Huang, M., Leblanc, M.L., and Hester, R.L. 1994. Systemic and regional hemodynamics after nitric oxide synthase inhibition: role of a neurogenic mechanism. Am. J. Physiol. 267: R84-R88.
34. Keller, D.M., Wasmund, W.L., Wray, D.W., Ogoh, S., Fadel, P.J., Smith, M.L., et al. 2003. Carotid baroreflex control of leg vascular conductance at rest and during exercise. J. Appl. Physiol. 94: 542-548.
35. Keller, D.M., Fadel, P.J., Ogoh, S., Brothers, R.M., Hawkins, M., Olivencia-Yurvati, A., and Raven, P.B. 2004a. Carotid baroreflex control of leg vasculature in exercising and non-exercising skeletal muscle in humans. J. Physiol. 561: 283-293. doi:10.1113/jphysiol.2004.071944.
36. Keller, D.M., Ogoh, S., Greene, S., Olivencia-Yurvati, A., and Raven, P.B. 2004b. Inhibition of KATP channel activity augments baroreflex-mediated vasoconstriction in exercising human skeletal muscle. J. Physiol. 561: 273-282. doi:10.1113/jphysiol.2004.071993.
37. Koller, A., and Kaley, G. 1991. Endothelial regulation of wall shear stress and blood flow in skeletal muscle microcirculation. Am. J. Physiol. 260: H862-H868.
38. Koller, A., Sun, D., and Kaley, G. 1993. Role of shear stress and endothelial prostaglandins in flow- and viscosity-induced dilation of arterioles in vitro. Circ. Res. 72: 1276-1284.
39. Koller-Strametz, J., Matulla, B., Wolzt, M., Muller, M., Entlicher, J., Eichler, H.G., et al. 1998. Role of nitric oxide in exercise-induced vasodilation in man. Life Sci. 62: 1035-1042. doi:10.1016/S0024-3205(98) 00024-1.
40. Lau, K.S., Grange, R.W., Isotani, E., Sarelius, I.H., Kamm, K.E., Huang, P.L., et al. 2000. nNOS and eNOS modulate cGMP formation and vascular response in contracting fast-twitch skeletal muscle. Physiol Genomics. 2: 21-27.
41. MacDonald, M.J., Shoemaker, J.K., Tschakovsky, M.E., and Hughson, R.L. 1998. Alveolar oxygen uptake and femoral artery blood flow dynamics in upright and supine leg exercise in humans. J. Appl. Physiol. 85: 1622-1628.
42. Maiorana, A., O'Driscoll, G., Taylor, R., and Green, D. 2003. Exercise and the nitric oxide vasodilator system. Sports Med. 33: 1013-1035. doi:10.2165/00007256-200333140-00001.
43. Naik, J.S., Valic, Z., Buckwalter, J.B., and Clifford, P.S. 1999. Rapid vasodilation in response to a brief tetanic muscle contraction. J. Appl. Physiol. 87: 1741-1746.
44. O'Leary, D.S., Dunlap, R.C., and Glover, K.W. 1994. Role of endothelium-derived relaxing factor in hindlimb reactive and active hyperemia in conscious dogs. Am. J. Physiol. 266: R1213-R1219.
45. Ogoh, S., Fadel, P.J., Nissen, P., Jans, O., Selmer, C., Secher, N.H., and Raven, P.B. 2003. Baroreflex-mediated changes in cardiac output and vascular conductance in response to alterations in carotid sinus pressure during exercise in humans. J. Physiol. 550: 317-324. doi:10.1113/jphysiol.2003. 041517.
46. Palmer, R.M., Ashton, D.S., and Moncada, S. 1988. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature, 333: 664-666. doi:10.1038/333664a0.
47. Pohl, U., Holtz, J., Busse, R., and Bassenge, E. 1986. Crucial role of endothelium in the vasodilator response to increased flow in vivo. Hypertension, 8: 37-44.
48. Radegran, G., and Saltin, B. 1999. Nitric oxide in the regulation of vasomotor tone in human skeletal muscle. Am. J. Physiol. 276: H1951-H1960.
49. Remensnyder, J.P., Mitchell, J.H., and Sarnoff, S.J. 1962. Functional sympatholysis during muscular activity. Circ. Res. 11: 370-380.
50. Rogers, A.M., Saunders, N.R., Pyke, K.E., and Tschakovsky, M.E. 2006. Rapid vasoregulatory mechanisms in exercising human skeletal muscle: dynamic response to repeated changes in contraction intensity. Am. J. Physiol. Heart Circ. Physiol. 291: H1065-H1073. doi:10.1152/ajpheart.00368.2006.
51. Rosenmeier, J.B., Dinenno, F.A., Fritzlar, S.J., and Joyner, M.J. 2003a. Alpha1- and alpha2-adrenergic vasoconstriction is blunted in contracting human muscle. J. Physiol. 547: 971-976.
52. Rosenmeier, J.B., Fritzlar, S.J., Dinenno, F.A., and Joyner, M.J. 2003b. Exogenous NO administration and alpha-adrenergic vasoconstriction in human limbs. J. Appl. Physiol. 95: 2370-2374.
53. Rowell, L.B. 1997. Neural control of muscle blood flow: importance during dynamic exercise. Clin. Exp. Pharmacol. Physiol. 24: 117-125. doi:10.1111/j.1440-1681.1997.tb01793.x.
54. Rowell, L.B. 2004. Ideas about control of skeletal and cardiac muscle blood flow (1876-2003): cycles of revision and new vision. J. Appl. Physiol. 97(1): 384-392.
55. Saunders, N.R., and Tschakovsky, M.E. 2004. Evidence for a rapid vasodilatory contribution to immediate hyperemia in rest-to-mild and mild-to-moderate forearm exercise transitions in humans. J. Appl. Physiol. 97: 1143-1151. doi:10.1152/japplphysiol.01284.2003.
56. Saunders, N.R., Dinenno, F.A., Pyke, K.E., Rogers, A.M., and Tschakovsky, M.E. 2005a. Impact of combined NO and PG blockade on rapid vasodilation in a forearm mild-to-moderate exercise transition in humans. Am. J. Physiol. Heart Circ. Physiol. 288: H214-H220. doi:10.1152/ajpheart.00762.2004.
57. Saunders, N.R., Pyke, K.E., and Tschakovsky, M.E. 2005b. Dynamic response characteristics of local muscle blood flow regulatory mechanisms in human forearm exercise. J. Appl. Physiol. 98: 1286-1296. doi:10.1152/japplphysiol.01118.2004.
58. Schrage, W.G., Eisenach, J.H., Dinenno, F.A., Roberts, S.K., Johnson, C.P., Sandroni, P., et al. 2004a. Effects of midodrine on exercise-induced hypotension and blood pressure recovery in autonomic failure. J. Appl. Physiol. 97: 1978-1984. doi:10.1152/japplphysiol.00547.2004.
59. Schrage, W.G., Joyner, M.J., and Dinenno, F.A. 2004b. Local inhibition of nitric oxide and prostaglandins independently reduces forearm exercise hyperaemia in humans. J. Physiol. 557: 599-611. doi:10.1113/jphysiol.2004.061283.
60. Segal, S.S., Damon, D.N., and Duling, B.R. 1989. Propagation of vasomotor responses coordinates arteriolar resistances. Am. J. Physiol. 256: H832-H837.
61. Segal, S.S., Welsh, D.G., and Kurjiaka, D.T. 1999. Spread of vasodilatation and vasoconstriction along feed arteries and arterioles of hamster skeletal muscle. J. Physiol. 516: 283-291. doi:10.1111/j.1469- 7793.1999.283aa.x.
62. Sheriff, D.D., and Hakeman, A.L. 2001. Role of speed vs. grade in relation to muscle pump function at locomotion onset. J. Appl. Physiol. 91: 269-276.
63. Sheriff, D.D., and Van Bibber, R. 1998. Flow-generating capability of the isolated skeletal muscle pump. Am. J. Physiol. 274: H1502-H1508.
64. Sheriff, D.D., and Zidon, T.M. 2003. Delay of muscle vasodilation to changes in work rate (treadmill grade) during locomotion. J. Appl. Physiol. 94: 1903-1909.
65. Sheriff, D.D., Nelson, C.D., and Sundermann, R.K. 2000. Does autonomic blockade reveal a potent contribution of nitric oxide to locomotion-induced vasodilation? Am. J. Physiol. Heart Circ. Physiol. 279: H726-H732.
66. Shoemaker, J.K., Halliwill, J.R., Hughson, R.L., and Joyner, M.J. 1997. Contributions of acetylcholine and nitric oxide to forearm blood flow at exercise onset and recovery. Am. J. Physiol. 273: H2388-H2395.
67. Shoemaker, J.K., Tschakovsky, M.E., and Hughson, R.L. 1998. Vasodilation contributes to the rapid hyperemia with rhythmic contractions in humans. Can. J. Physiol. Pharmacol. 76: 418-427. doi:10.1139/cjpp-76-4-418.
68. Smiesko, V., Kozik, J., and Dolezel, S. 1985. Role of endothelium in the control of arterial diameter by blood flow. Blood Vessels, 22: 247-251.
69. Snow, H.M., McAuliffe, S.J., Moors, J.A., and Brownlie, R. 1994. The relationship between blood flow and diameter in the iliac artery of the anaesthetized dog: the role of endothelium-derived relaxing factor and shear stress. Exp. Physiol. 79: 635-645.
70. Thomas, G.D., and Victor, R.G. 1998. Nitric oxide mediates contraction-induced attenuation of sympathetic vasoconstriction in rat skeletal muscle. J. Physiol. 506: 817-826. doi:10.1111/j.1469-7793.1998.817bv.x.
71. Thomas, G.D., Hansen, J., and Victor, R.G. 1994. Inhibition of alpha2-adrenergic vasoconstriction during contraction of glycolytic, not oxidative, rat hindlimb muscle. Am. J. Physiol. 266: H920-H929.
72. Thomas, G.D., Zhang, W., and Victor, R.G. 2001. Impaired modulation of sympathetic vasoconstriction in contracting skeletal muscle of rats with chronic myocardial infarctions: role of oxidative stress. Circ. Res. 88: 816-823. doi:10.1161/hh0801.089341.
73. Thomas, G.D., Shaul, P.W., Yuhanna, I.S., Froehner, S.C., and Adams, M.E. 2003. Vasomodulation by skeletal muscle-derived nitric oxide requires alpha-syntrophin-mediated sarcolemmal localization of neuronal Nitric oxide synthase. Circ. Res. 92: 554-560. doi:10.1161/01.RES.0000061570.83105.52.
74. Tschakovsky, M.E., Shoemaker, J.K., and Hughson, R.L. 1996. Vasodilation and muscle pump contribution to immediate exercise hyperemia. Am. J. Physiol. 271: H1697-H1701.
75. Tschakovsky, M.E., Sujirattanawimol, K., Ruble, S.B., Valic, Z., and Joyner, M.J. 2002. Is sympathetic neural vasoconstriction blunted in the vascular bed of exercising human muscle? J. Physiol. 541: 623-635. doi:10.1113/jphysiol.2001.014431.
76. Tschakovsky, M.E., Rogers, A.M., Pyke, K.E., Saunders, N.R., Glenn, N., Lee, S.J., et al. 2004. Immediate exercise hyperemia in humans is contraction intensity dependent: evidence for rapid vasodilation. J. Appl. Physiol. 96: 639-644. doi:10.1152/japplphysiol.00769.2003.
77. Van Teeffelen, J.W., and Segal, S.S. 2006. Rapid dilation of arterioles with single contraction of hamster skeletal muscle. Am. J. Physiol. Heart Circ. Physiol. 290: H119-H127. doi:10.1152/ajpheart.00197.2005.
78. Welsh, D.G., and Segal, S.S. 1997. Coactivation of resistance vessels and muscle fibers with acetylcholine release from motor nerves. Am. J. Physiol. 273: H156-H163.
79. Wilson, J.R., and Kapoor, S. 1993. Contribution of endothelium-derived relaxing factor to exercise-induced vasodilation in humans. J. Appl. Physiol. 75: 2740-2744.
80. Wray, D.W., Fadel, P.J., Keller, D.M., Ogoh, S., Sander, M., Raven, P.B., et al. 2004. Dynamic carotid baroreflex control of the peripheral circulation during exercise in humans. J. Physiol. 559: 675-684. doi:10.1113/ jphysiol.2004.066183.
81. Wunsch, S.A., Muller-Delp, J., and Delp, M.D. 2000. Time course of vasodilatory responses in skeletal muscle arterioles: role in hyperemia at onset of exercise. Am. J. Physiol. Heart Circ. Physiol. 279: H1715-H1723.