Effects of aging and exercise training on spinotrapezius muscle microvascular PO2 dynamics and vasomotor control

Journal of Applied Physiology

Volumn 110, Issue 3, 2011, Pages 695-704

  McCullough, Danielle J ^a   Davis III, Robert T ^a   Dominguez II, James M ^a   Stabley, John N ^a   Bruells, Christian S ^a,b   Behnke, Bradley J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

Isolated microvessel aging; Microvascular oxygen pressures; Muscle contraction

Indexed keywords

OXYGEN;

ADRENERGIC SYSTEM; AGING; ANIMAL; ANIMAL EXPERIMENT; ARTICLE; EXERCISE; FEEDBACK SYSTEM; FISCHER 344 RAT; MALE; METABOLISM; METHODOLOGY; OXYGEN CONSUMPTION; PHYSIOLOGY; RAT; SKELETAL MUSCLE; VASCULARIZATION;

AGING; ANIMALS; FEEDBACK, PHYSIOLOGICAL; MALE; MUSCLE, SKELETAL; OXYGEN; OXYGEN CONSUMPTION; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL EXERTION; RATS; RATS, INBRED F344; VASOMOTOR SYSTEM;

EID: 79954622540     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01084.2010     Document Type: Article

References (94)

1. Aaker A, Laughlin MH. Diaphragm arterioles are less responsive to α(1)-adrenergic constriction than gastrocnemius arterioles. J Appl Physiol 92: 1808-1816, 2002. (Pubitemid 34666405)
2. Armstrong RB, Delp MD, Goljan EF, Laughlin MH. Distribution of blood flow in muscles of miniature swine during exercise. J Appl Physiol 62: 1285-1298, 1987. (Pubitemid 17073935)
3. Armstrong RB, Hayes DA, Delp MD. Blood flow distribution in rat muscles during preexercise anticipatory response. J Appl Physiol 67: 1855-1861, 1989. (Pubitemid 20039393)
4. Armstrong RB, Laughlin MH. Exercise blood flow patterns within and among rat muscles after training. Am J Physiol Heart Circ Physiol 246: H59-H68, 1984. (Pubitemid 14147889)
5. Bailey JK, Kindig CA, Behnke BJ, Musch TI, Schmid-Schoenbein GW, Poole DC. Spinotrapezius muscle microcirculatory function: Effects of surgical exteriorization. Am J Physiol Heart Circ Physiol 279: H3131-H3137, 2000. (Pubitemid 32005905)
6. Bearden SE, Linn E, Ashley BS, Looft-Wilson RC. Age-related changes in conducted vasodilation: Effects of exercise training and role in functional hyperemia. Am J Physiol Regul Integr Comp Physiol 293: R1717-R1721, 2007. (Pubitemid 47541993)
7. Beckman JS, Koppenol WH. Nitric oxide, superoxide, peroxynitrite: The good, the bad, and ugly. Am J Physiol Cell Physiol 271: C1424-C1437, 1996.
8. Behnke B, Prisby RD, Lesniewski LA, Donato AJ, Olin H, Delp MD. Influence of aging and physical activity on vascular morphology in rat skeletal muscle. J Physiol 575: 617-626, 2006. (Pubitemid 44270185)
9. Behnke BJ, Barstow TJ, Kindig CA, McDonough P, Musch TI, Poole DC. Dynamics of oxygen uptake following exercise onset in rat skeletal muscle. Respir Physiol Neurobiol 133: 229-239, 2002. (Pubitemid 35300235)
10. Behnke BJ, Delp MD. Aging blunts the dynamics of vasodilation in isolated skeletal muscle resistance vessels. J Appl Physiol 108: 14-20, 2010.
11. 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. (Pubitemid 40349096)
12. Behnke BJ, Delp MD, Poole DC, Musch TI. Aging potentiates the effect of congestive heart failure on muscle microvascular oxygenation. J Appl Physiol 103: 1757-1763, 2007. (Pubitemid 350033863)
13. Behnke BJ, Kindig CA, Musch TI, Koga S, Poole DC. Dynamics of microvascular oxygen pressure across the rest-exercise transition in rat skeletal muscle. Respir Physiol 126: 53-63, 2001. (Pubitemid 32318524)
14. Bell C, Paterson DH, Kowalchuk JM, Cunningham DA. Oxygen uptake kinetics of older humans are slowed with age but are unaffected by hyperoxia. Exp Physiol 84: 747-759, 1999. (Pubitemid 29401731)
15. Berkowitz DE, White R, Li D, Minhas KM, Cernetich A, Kim S, Burke S, Shoukas AA, Nyhan D, Champion HC, Hare JM. Arginase reciprocally regulates nitric oxide synthase activity and contributes to endothelial dysfunction in aging blood vessels. Circulation 108: 2000- 2006, 2003. (Pubitemid 37296546)
16. Bexfield NA, Parcell AC, Nelson WB, Foote KM, Mack GW. Adaptations to high-intensity intermittent exercise in rodents. J Appl Physiol 107: 749-754, 2009.
17. Copp SW, Ferreira LF, Herspring KF, Musch TI, Poole DC. The effects of aging on capillary hemodynamics in contracting rat spinotrapezius muscle. Microvasc Res 77: 113-119, 2009.
18. 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. (Pubitemid 34786900)
19. DeLorey DS, Kowalchuk JM, Paterson DH. Effect of age on O(2) uptake kinetics and the adaptation of muscle deoxygenation at the onset of moderate-intensity cycling exercise. J Appl Physiol 97: 165-172, 2004. (Pubitemid 38802516)
20. 2 utilization and muscle oxygenation during the transition to moderateintensity exercise. Appl Physiol Nutr Metab 32: 1251-1262, 2007.
21. Delp MD. Effects of exercise training on endothelium-dependent peripheral vascular responsiveness. Med Sci Sports Exerc 27: 1152-1157, 1995.
22. 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. (Pubitemid 351267353)
23. Delp MD, Brown M, Laughlin MH, Hasser EM. Rat aortic vasoreactivity is altered by old age and hindlimb unloading. J Appl Physiol 78: 2079-2086, 1995.
24. 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.
25. Diederich ER, Behnke BJ, McDonough P, Kindig CA, Barstow TJ, Poole DC, Musch TI. Dynamics of microvascular oxygen partial pressure in contracting skeletal muscle of rats with chronic heart failure. Cardiovasc Res 56: 479-486, 2002. (Pubitemid 35351570)
26. Donato AJ, Lesniewski LA, Delp MD. Ageing and exercise training alter adrenergic vasomotor responses of rat skeletal muscle arterioles. J Physiol 579: 115-125, 2007.
27. 2 uptake kinetics. Eur J Appl Physiol 110: 739-751, 2010.
28. Eskurza I, Myerburgh LA, Kahn ZD, Seals DR. Tetrahydrobiopterin augments endothelium-dependent dilatation in sedentary but not in habitually exercising older adults. J Physiol 568: 1057-1065, 2005. (Pubitemid 41646042)
29. 2 exchange. Respir Physiol Neurobiol 147: 91-103, 2005. (Pubitemid 40545904)
30. Flaim SF, Nellis SH, Toggart EJ, Drexler H, Kanda K, Newman ED. Multiple simultaneous determinations of hemodynamics and flow distribution in conscious rat. J Pharmacol Methods 11: 1-39, 1984. (Pubitemid 14192360)
31. Frisbee JC, Hollander JM, Brock RW, Yu HG, Boegehold MA. Integration of skeletal muscle resistance arteriolar reactivity for perfusion responses in the metabolic syndrome. Am J Physiol Regul Integr Comp Physiol 296: R1771-R1782, 2009.
32. Gomes VA, Casella-Filho A, Chagas AC, Tanus-Santos JE. Enhanced concentrations of relevant markers of nitric oxide formation after exercise training in patients with metabolic syndrome. Nitric Oxide 19: 345-350, 2008.
33. Green DJ, Maiorana AJ, Cable NT. Point: Exercise training does induce vascular adaptations beyond the active muscle beds. J Appl Physiol 105: 1002-1004; discussion 1007, 2008.
34. Gryglewski RJ, Palmer RM, Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320: 454-456, 1986. (Pubitemid 16097810)
35. 2 uptake kinetics, pyruvate dehydrogenase activity, and muscle deoxygenation in young and older adults during the transition to moderate-intensity exercise. Am J Physiol Regul Integr Comp Physiol 294: R577-R584, 2008. (Pubitemid 351213764)
36. 2 kinetics during moderate-intensity exercise in young adults. J Appl Physiol 98: 1371-1378, 2005. (Pubitemid 40396513)
37. Hahn SA, Ferreira LF, Williams JB, Jansson KP, Behnke BJ, Musch TI, Poole DC. Downhill treadmill running trains the rat spinotrapezius muscle. J Appl Physiol 102: 412-416, 2007. (Pubitemid 46091595)
38. 2 delivery. J Appl Physiol 94: 744-751, 2003. (Pubitemid 36158254)
39. Hirai DM, Copp SW, Herspring KF, Ferreira LF, Poole DC, Musch TI. Aging impacts microvascular oxygen pressures during recovery from contractions in rat skeletal muscle. Respir Physiol Neurobiol 169: 315-322, 2009.
40. Irion GL, Vasthare US, Tuma RF. Age-related change in skeletal muscle blood flow in the rat. J Gerontol 42: 660-665, 1987. (Pubitemid 17164621)
41. Ishise S, Pegram BL, Yamamoto J, Kitamura Y, Frohlich ED. Reference sample microsphere method: Cardiac output and blood flows in conscious rat. Am J Physiol Heart Circ Physiol 239: H443-H449, 1980. (Pubitemid 10008871)
42. Jackson DN, Moore AW, Segal SS. Blunting of rapid onset vasodilatation and blood flow restriction in arterioles of exercising skeletal muscle with ageing in male mice. J Physiol 588: 2269-2282, 2010.
43. 2. Am J Physiol Heart Circ Physiol 297: H1087-H1095, 2009.
44. Kano Y, Padilla D, Hageman KS, Poole DC, Musch TI. Downhill running: A model of exercise hyperemia in the rat spinotrapezius muscle. J Appl Physiol 97: 1138-1142, 2004. (Pubitemid 39121444)
45. Kindig CA, Poole DC. A comparison of the microcirculation in the rat spinotrapezius and diaphragm muscles. Microvasc Res 55: 249-259, 1998. (Pubitemid 28368694)
46. Koller A, Huang A, Sun D, Kaley G. Exercise training augments flow-dependent dilation in rat skeletal muscle arterioles. Role of endothelial nitric oxide and prostaglandins. Circ Res 76: 544-550, 1995.
47. Larkin LM, Halter JB, Supiano MA. Effect of aging on rat skeletal muscle beta-AR function in male Fischer 344 brown Norway rats. Am J Physiol Regul Integr Comp Physiol 270: R462-R468, 1996.
48. Lash JM. Exercise training enhances adrenergic constriction and dilation in the rat spinotrapezius muscle. J Appl Physiol 85: 168-174, 1998. (Pubitemid 28334921)
49. Lash JM, Bohlen HG. Functional adaptations of rat skeletal muscle arterioles to aerobic exercise training. J Appl Physiol 72: 2052-2062, 1992.
50. Lash JM, Bohlen HG. Time- and order-dependent changes in functional and NO-mediated dilation during exercise training. J Appl Physiol 82: 460-468, 1997. (Pubitemid 27090171)
51. Laughlin MH, Armstrong RB, White J, Rouk K. A method for using microspheres to measure muscle blood flow in exercising rats. J Appl Physiol 52: 1629-1635, 1982. (Pubitemid 12044358)
52. Laughlin MH, Korthuis RJ, Duncker DJ, Bache RJ. Control of blood flow to cardiac and skeletal muscle during exercise. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, chapt. 16, p. 705-769.
53. Lenaz G, Bovina C, Castelluccio C, Fato R, Formiggini G, Genova ML, Marchetti M, Pich MM, Pallotti F, Parenti Castelli G, Biagini G. Mitochondrial complex I defects in aging. Mol Cell Biochem 174: 329-333, 1997. (Pubitemid 27404210)
54. Li L, Rezvan A, Salerno JC, Husain A, Kwon K, Jo H, Harrison DG, Chen W. GTP cyclohydrolase I phosphorylation and interaction with GTP cyclohydrolase feedback regulatory protein provide novel regulation of endothelial tetrahydrobiopterin and nitric oxide. Circ Res 106: 328-336, 2010.
55. Lo LW, Vinogradov SA, Koch CJ, Wilson DF. A new, water soluble, phosphor for oxygen measurements in vivo. Adv Exp Med Biol 428: 651-656, 1997. (Pubitemid 28128071)
56. Ma T, Zhu X. Interleukin-6 increases the levels of cyclic GMP and nitrite in rat hippocampal slices. Eur J Pharmacol 321: 343-347, 1997. (Pubitemid 27105937)
57. Maeda S, Tanabe T, Otsuki T, Sugawara J, Iemitsu M, Miyauchi T, Kuno S, Ajisaka R, Matsuda M. Moderate regular exercise increases basal production of nitric oxide in elderly women. Hypertens Res 27: 947-953, 2004. (Pubitemid 40425397)
58. 2 on-kinetics in healthy humans. Am J Physiol Regul Integr Comp Physiol 299: R968-R976, 2010.
59. Minghini A, Britt LD, Hill MA. Interleukin-1 and interleukin-6 mediated skeletal muscle arteriolar vasodilation: In vitro vs. in vivo studies. Shock 9: 210-215, 1998. (Pubitemid 128463287)
60. Miyata N, Tsuchida K, Okuyama S, Otomo S, Kamata K, Kasuya Y. Age-related changes in endothelium-dependent relaxation in aorta from genetically diabetic WBN/Kob rats. Am J Physiol Heart Circ Physiol 262: H1104-H1109, 1992.
61. Moritoki H, Tanioka A, Maeshiba Y, Iwamoto T, Ishida Y, Araki H. Age-associated decrease in histamine-induced vasodilation may be due to reduction of cyclic GMP formation. Br J Pharmacol 95: 1015-1022, 1988. (Pubitemid 19001140)
62. 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.
63. 2 utilization. J Appl Physiol 108: 913-922, 2010.
64. Musch TI, Eklund KE, Hageman KS, Poole DC. Altered regional blood flow responses to submaximal exercise in older rats. J Appl Physiol 96: 81-88, 2004. (Pubitemid 38031985)
65. Musch TI, Poole DC. Blood flow response to treadmill running in the rat spinotrapezius muscle. Am J Physiol Heart Circ Physiol 271: H2730-H2734, 1996.
66. Nishimatsu H, Suzuki E, Takeda R, Takahashi M, Oba S, Kimura K, Nagano T, Hirata Y. Blockade of endogenous proinflammatory cytokines ameliorates endothelial dysfunction in obese Zucker rats. Hypertens Res 31: 737-743, 2008. (Pubitemid 351772865)
67. Ohkawa F, Ikeda U, Kawasaki K, Kusano E, Igarashi M, Shimada K. Inhibitory effect of interleukin-6 on vascular smooth muscle contraction. Am J Physiol Heart Circ Physiol 266: H898-H902, 1994.
68. Ostrowski K, Rohde T, Asp S, Schjerling P, Pedersen BK. Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol 515: 287-291, 1999. (Pubitemid 29092641)
69. Paterson DH, Cunningham DA, Koval JJ, St. Croix CM. Aerobic fitness in a population of independently living men and women aged 55-86 years. Med Sci Sports Exerc 31: 1813-1820, 1999. (Pubitemid 30012899)
70. Pawlowski M, Wilson DF. Monitoring of the oxygen pressure in the blood of live animals using the oxygen dependent quenching of phosphorescence. Adv Exp Med Biol 316: 179-185, 1992. (Pubitemid 23042480)
71. Pedersen BK, Febbraio MA. Muscle as an endocrine organ: Focus on muscle-derived interleukin-6. Physiol Rev 88: 1379-1406, 2008.
72. Poole DC, Barstow TJ, McDonough P, Jones AM. Control of oxygen uptake during exercise. Med Sci Sports Exerc 40: 462-474, 2008. (Pubitemid 351294661)
73. Poole DC, Behnke BJ, McDonough P, McAllister RM, Wilson DF. Measurement of muscle microvascular oxygen pressures: Compartmentalization of phosphorescent probe. Microcirculation 11: 317-326, 2004. (Pubitemid 39619082)
74. Poole DC, Behnke BJ, Padilla DJ. Dynamics of muscle microcirculatory oxygen exchange. Med Sci Sports Exerc 37: 1559-1566, 2005. (Pubitemid 41368501)
75. 2 kinetics limitation upstream. J Appl Physiol 108: 5-6, 2010.
76. 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. (Pubitemid 28334907)
77. Ramsey MW, Behnke BJ, Prisby RD, Delp MD. Effects of aging on adipose resistance artery vasoconstriction: Possible implications for orthostatic blood pressure regulation. J Appl Physiol 103: 1636-1643, 2007. (Pubitemid 350033848)
78. Renkin EM, Tucker VL. Measurement of microvascular transport parameters of macromolecules in tissues and organs of intact animals. Microcirculation 5: 139-152, 1998. (Pubitemid 128647890)
79. Rumsey WL, Vanderkooi JM, Wilson DF. Imaging of phosphorescence: A novel method for measuring oxygen distribution in perfused tissue. Science 241: 1649-1651, 1988.
80. Russell JA, Kindig CA, Behnke BJ, Poole DC, Musch TI. Effects of aging on capillary geometry and hemodynamics in rat spinotrapezius muscle. Am J Physiol Heart Circ Physiol 285: H251-H258, 2003. (Pubitemid 36736436)
81. Scheuermann BW, Bell C, Paterson DH, Barstow TJ, Kowalchuk JM. Oxygen uptake kinetics for moderate exercise are speeded in older humans by prior heavy exercise. J Appl Physiol 92: 609-616, 2002. (Pubitemid 34671027)
82. Seals DR, Desouza CA, Donato AJ, Tanaka H. Habitual exercise and arterial aging. J Appl Physiol 105: 1323-1332, 2008.
83. Sexton WL, Poole DC. Costal diaphragm blood flow heterogeneity at rest and during exercise. Respir Physiol 101: 171-182, 1995.
84. Sindler AL, Delp MD, Reyes R, Wu G, Muller-Delp JM. Effects of ageing and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J Physiol 587: 3885-3897, 2009.
85. 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. (Pubitemid 38660325)
86. Srere P. Citrate synthase. In: Methods in Enzymology. New York: Academic, 1969, p. 1-11.
87. Steensberg A, van Hall G, Osada T, Sacchetti M, Saltin B, Klarlund Pedersen B. Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin- 6. J Physiol 529: 237-242, 2000.
88. Thijssen DH, Hopman MT. Counterpoint: Exercise training does not induce vascular adaptations beyond the active muscle beds. J Appl Physiol 105: 1004-1006; discussion 1006-1007, 2008.
89. Trott DW, Gunduz F, Laughlin MH, Woodman CR. Exercise training reverses age-related decrements in endothelium-dependent dilation in skeletal muscle feed arteries. J Appl Physiol 106: 1925-1934, 2009.
90. Ueda H, Moritoki H. Possible association of decrease of ATP-induced vascular relaxation with reduction of cyclic GMP during aging. Arch Int Pharmacodyn Ther 310: 35-45, 1991.
91. Vinogradov S, Fernandez-Searra MA, Dugan BW, Wilson DF. Frequency domain instrument for measuring phosphorescence lifetime distributions in heterogeneous samples. Rev Sci Instrum 72: 3396-3406, 2001. (Pubitemid 33606977)
92. Vinogradov SA, Wilson DF. Phosphorescence lifetime analysis with a quadratic programming algorithm for determining quencher distributions in heterogeneous systems. Biophys J 67: 2048-2059, 1994. (Pubitemid 24342077)
93. 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. (Pubitemid 36082980)
94. Woodman CR, Trott DW, Laughlin MH. Short-term increases in intraluminal pressure reverse age-related decrements in endotheliumdependent dilation in soleus muscle feed arteries. J Appl Physiol 103: 1172-1179, 2007. (Pubitemid 47605951)