Sex differences with aging in nutritive skeletal muscle blood flow: Impact of exercise training, nitric oxide, and α-adrenergic-mediated mechanisms

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 307, Issue 4, 2014, Pages

  La Favor, Justin D ^a,d   Kraus, Raymond M ^a   Carrithers, Jonathan A ^a   Roseno, Steven L ^a   Gavin, Timothy P ^a,b   Hickner, Robert C ^a,b,c  

^a EAST CAROLINA UNIVERSITY   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Healthy aging; Inducible nitric oxide synthase; Microdialysis; Phentolamine; Sex differences

Indexed keywords

ACETYLCHOLINE; ALCOHOL; ALPHA ADRENERGIC RECEPTOR; ARGININE; NITRIC OXIDE; NITROPRUSSIDE SODIUM; NORADRENALIN; PHENTOLAMINE; ALPHA ADRENERGIC RECEPTOR BLOCKING AGENT; ALPHA ADRENERGIC RECEPTOR STIMULATING AGENT; ENZYME INHIBITOR; N(G) METHYLARGININE; NITRIC OXIDE DONOR; VASODILATOR AGENT;

ADULT; AEROBIC EXERCISE; AGING; ARTICLE; BLOOD FLOW; CONTROLLED STUDY; EXERCISE; FEMALE; HUMAN; MALE; MICRODIALYSIS; MUSCLE BLOOD FLOW; MUSCLE PERFUSION; NORMAL HUMAN; NUTRITION; PHYSICAL ACTIVITY; PRIORITY JOURNAL; REGULATORY MECHANISM; SEX DIFFERENCE; VASOCONSTRICTION; VASODILATATION; YOUNG ADULT; AGED; DRUG EFFECTS; MIDDLE AGED; PHYSIOLOGY; SKELETAL MUSCLE; VASCULARIZATION;

ACETYLCHOLINE; ADRENERGIC ALPHA-AGONISTS; ADRENERGIC ALPHA-ANTAGONISTS; ADULT; AGED; AGING; ENZYME INHIBITORS; EXERCISE; FEMALE; HUMANS; MALE; MIDDLE AGED; MUSCLE, SKELETAL; NITRIC OXIDE DONORS; NITROPRUSSIDE; NOREPINEPHRINE; OMEGA-N-METHYLARGININE; PHENTOLAMINE; REGIONAL BLOOD FLOW; SEX FACTORS; VASOCONSTRICTION; VASODILATOR AGENTS;

EID: 84906100428     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00247.2014     Document Type: Article

References (70)

1. Akita Y, Otani H, Matsuhisa S, Kyoi S, Enoki C, Hattori R, Imamura H, Kamihata H, Kimura Y, Iwasaka T. Exercise-induced activation of cardiac sympathetic nerve triggers cardioprotection via redox-sensitive activation of eNOS and upregulation of iNOS. Am J Physiol Heart Circ Physiol 292: H2051-H2059, 2007.
2. Cho MM, Ziats NP, Pal D, Utian WH, Gorodeski GI. Estrogen modulates paracellular permeability of human endothelial cells by eNOSand iNOS-related mechanisms. Am J Physiol Cell Physiol 276: C337-C349, 1999.
3. Clark MG, Rattigan S, Clerk LH, Vincent MA, Clark AD, Youd JM, Newman JM. Nutritive and non-nutritive blood flow: rest and exercise. Acta Physiol Scand 168: 519-530, 2000.
4. Credeur DP, Holwerda SW, Boyle LJ, Vianna LC, Jensen AK, Fadel PJ. Effect of aging on carotid baroreflex control of blood pressure and leg vascular conductance in women. Am J Physiol Heart Circ Physiol 306: H1417-H1425, 2014.
5. Darkow DJ, Lu L, White RE. Estrogen relaxation of coronary artery smooth muscle is mediated by nitric oxide and cGMP. Am J Physiol Heart Circ Physiol 272: H2765-H2773, 1997.
6. 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.
7. 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.
8. Dinenno FA, Joyner MJ. Alpha-adrenergic control of skeletal muscle circulation at rest and during exercise in aging humans. Microcirculation 13: 329-341, 2006.
9. Dinenno FA, Tanaka H, Stauffer BL, Seals DR. Reductions in basal limb blood flow and vascular conductance with human ageing: role for augmented alpha-adrenergic vasoconstriction. J Physiol 536: 977-983, 2001.
10. Donato AJ, Uberoi A, Wray DW, Nishiyama S, Lawrenson L, Richardson RS. Differential effects of aging on limb blood flow in humans. Am J Physiol Heart Circ Physiol 290: H272-H278, 2006.
11. Evans WJ, Phinney SD, Young VR. Suction applied to a muscle biopsy maximizes sample size. Med Sci Sports Exerc 14: 101-102, 1982.
12. Ferrer M, Meyer M, Osol G. Estrogen replacement increases betaadrenoceptor-mediated relaxation of rat mesenteric arteries. J Vasc Res 33: 124-131, 1996.
13. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18: 499-502, 1972.
14. Garten RS, Groot HJ, Rossman MJ, Gifford JR, Richardson RS. The role of muscle mass in exercise-induced hyperemia. J Appl Physiol 116: 1204-1209, 2014.
15. Gavin TP, Ruster RS, Carrithers JA, Zwetsloot KA, Kraus RM, Evans CA, Knapp DJ, Drew JL, McCartney JS, Garry JP, Hickner RC. No difference in the skeletal muscle angiogenic response to aerobic exercise training between young and aged men. J Physiol 585: 231-239, 2007.
16. Gomez-Cabrera MC, Borrás C, Pallardó FV, Sastre J, Ji LL, Viña J. Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J Physiol 567: 113-120, 2005.
17. Groot HJ, Trinity JD, Layec G, Rossman MJ, Ives SJ, Richardson RS. Perfusion pressure and movement-induced hyperemia: evidence of limited vascular function and vasodilatory reserve with age. Am J Physiol Heart Circ Physiol 304: H610-H619, 2013.
18. Gudbjörnsdóttir S, Sjöstrand M, Strindberg L, Wahren J, Lönnroth P. Direct measurement of the permeability surface area for insulin and glucose in human skeletal muscle. J Clin Endocrinol Metab 88: 4559-4564, 2003.
19. Hart EC, Charkoudian N, Wallin BG, Curry TB, Eisenach J, Joyner MJ. Sex and ageing differences in resting arterial pressure regulation: the role of the beta-adrenergic receptors. J Physiol 589: 5285-5297, 2011.
20. Hart EC, Charkoudian N, Wallin BG, Curry TB, Eisenach JH, Joyner MJ. Sex differences in sympathetic neural-hemodynamic balance: implications for human blood pressure regulation. Hypertension 53: 571-576, 2009.
21. Hart EC, Wallin BG, Barnes JN, Joyner MJ, Charkoudian N. Sympathetic nerve activity and peripheral vasodilator capacity in young and older men. Am J Physiol Heart Circ Physiol 306: H904-H909, 2014.
22. 133Xe clearance. Clin Sci 86: 15-25, 1994.
23. Hickner RC, Ekelund U, Mellander S, Ungerstedt U, Henriksson J. Muscle blood flow in cats: comparison of microdialysis ethanol technique with direct measurement. J Appl Physiol 79: 638-647, 1995.
24. Hickner RC, Kemeny G, McIver K, Harrison K, Hostetler ME. Lower skeletal muscle nutritive blood flow in older women is related to eNOS protein content. J Gerontol A Biol Sci Med Sci 58: 20-25, 2003.
25. Hickner RC, Rosdahl H, Borg I, Ungerstedt U, Jorfeldt L, Henriksson J. Ethanol may be used with the microdialysis technique to monitor blood flow changes in skeletal muscle: dialysate glucose concentration is bloodflow-dependent. Acta Physiol Scand 143: 355-356, 1991.
26. Hickner RC, Rosdahl H, Borg I, Ungerstedt U, Jorfeldt L, Henriksson J. The ethanol technique of monitoring local blood flow changes in rat skeletal muscle: implications for microdialysis. Acta Physiol Scand 146: 87-97, 1992.
27. Hickner RC, Ungerstedt U, Henriksson J. Regulation of skeletal muscle blood flow during acute insulin-induced hypoglycemia in the rat. Diabetes 43: 1340-1344, 1994.
28. Hirai DM, Copp SW, Hageman KS, Poole DC, Musch TL. Aging alters the contribution of nitric oxide to regional muscle hemodynamic control at rest and during exercise in rats. J Appl Physiol 111: 989-998, 2011.
29. Hogarth AJ, Mackintosh AF, Mary DA. Gender-related differences in the sympathetic vasoconstrictor drive of normal subjects. Clin Sci (Lond) 112: 353-361, 2007.
30. Jennings G, Nelson L, Nestel P, Esler M, Korner P, Burton D, Bazelmans J. The effects of changes in physical activity on major cardiovascular risk factors, hemodynamics, sympathetic function, and glucose utilization in man: a controlled study of four levels of activity. Circulation 73: 30-40, 1986.
31. Kaneki M, Shimizu N, Yamada D, Chang K. Nitrosative stress and pathogenesis of insulin resistance. Antioxid Redox Signal 9: 319-329, 2007.
32. Kety SS. Measurement of regional circulation by the local clearance of radioactive sodium. Am Heart J 38: 321-328, 1949.
33. Kneale BJ, Chowienczyk PJ, Brett SE, Coltart DJ, Ritter JM. Gender differences in sensitivity to adrenergic agonists of forearm resistance vasculature. J Am Coll Cardiol 36: 1233-1238, 2000.
34. La Favor JD, Anderson EJ, Dawkins JT, Hickner RC, Wingard CJ. Exercise prevents Western diet-associated erectile dysfunction and coronary artery endothelial dysfunction: response to acute apocynin and sepiapterin treatment. Am J Physiol Regul Integr Comp Physiol 305: R423-R434, 2013.
35. La Favor JD, Anderson EJ, Hickner RC. Novel method for detection of reactive oxygen species in vivo in human skeletal muscle. Physiol Res 63: 387-392, 2014.
36. Lahtinen T, Alhava EM, Karjalainen P, Romppanen T. The effect of age on blood flow in the proximal femur in man. J Nucl Med 22: 966-972, 1981.
37. Lakatta EG, Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises. I. Aging arteries: a "set up" for vascular disease. Circulation 107: 139-146, 2003.
38. Lakatta EG, Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises. II. The aging heart in health: links to heart disease. Circulation 107: 346-354, 2003.
39. Li T, Xiao X, Zhang J, Zhu Y, Hu Y, Zang J, Lu K, Yang T, Ge H, Peng X, Lan D, Liu L. Age-and sex-differences in vascular responsiveness in healthy and trauma patients: contribution of estrogen receptormediated Rho kinase and PKC pathways. Am J Physiol Heart Circ Physiol 306: H1101-H1115, 2014.
40. Lind L, Lithell H. Decreased peripheral blood flow in the pathogenesis of the metabolic syndrome comprising hypertension, hyperlipidemia, and hyperinsulinemia. Am Heart J 125: 1494-1497, 1993.
41. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and betacell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412-419, 1985.
42. McDaniel J, Hayman MA, Ives S, Fjeldstad A, Trinity JD, Wray DW, Richardson RS. Attenuated exercise induced hyperaemia with age: mechanistic insight from passive limb movement. J Physiol 588: 4507-4517, 2010.
43. Meredith IT, Friberg P, Jennings GL, Dewar EM, Fazio VA, Lambert GW, Esler MD. Exercise training lowers resting renal but not cardiac sympathetic activity in humans. Hypertension 18: 575-582, 1991.
44. Moreau KL, Donato AJ, Tanaka H, Jones PP, Gates PE, Seals DR. Basal leg blood flow in healthy women is related to age and hormone replacement therapy status. J Physiol 547: 309-316, 2003.
45. Mortensen SP, Askew CD, Walker M, Nyberg M, Hellsten Y. The hyperaemic response to passive leg movement is dependent on nitric oxide: a new tool to evaluate endothelial nitric oxide function. J Physiol 590: 4391-4400, 2012.
46. 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.
47. Newcomer SC, Leuenberger UA, Hogeman CS, Proctor DN. Heterogeneous vasodilator responses of human limbs: influence of age and habitual endurance training. Am J Physiol Heart Circ Physiol 289: H308-H315, 2005.
48. 2O in perfused rat hindlimb. Am J Physiol Heart Circ Physiol 281: H2731-H2737, 2001.
49. Ng AV, Callister R, Johnson DG, Seals DR. Endurance exercise training is associated with elevated basal sympathetic nerve activity in healthy older humans. J Appl Physiol 77: 1366-1374, 1994.
50. Nishiyama SK, Wray DW, Richardson RS. Aging affects vascular structure and function in a limb-specific manner. J Appl Physiol 105: 1661-1670, 2008.
51. Orshal JM, Khalil RA. Gender, sex hormones, and vascular tone. Am J Physiol Regul Integr Comp Physiol 286: R233-R249, 2004.
52. Parker BA, Ridout SJ, Proctor DN. Age and flow-mediated dilation: a comparison of dilatory responsiveness in the brachial and popliteal arteries. Am J Physiol Heart Circ Physiol 291: H3043-H3049, 2006.
53. Parker BA, Smithmyer SL, Jarvis SS, Ridout SJ, Pawelczyk JA, Proctor DN. Evidence for reduced sympatholysis in leg resistance vasculature of healthy older women. Am J Physiol Heart Circ Physiol 292: H1148-H1156, 2007.
54. Ropelle ER, Pauli JR, Cintra DE, da Silva AS, De Souza CT, Guadagnini D, Carvalho BM, Caricilli AM, Katashima CK, Carvalho-Filho MA, Hirabara S, Curi R, Valloso LA, Saad MJ, Carvalheira JB. Targeted disruption of inducible nitric oxide synthase protects against aging, S-nitrosation, and insulin resistance in muscle of male mice. Diabetes 62: 466-470, 2013.
55. Rudroff T, Weissman JA, Bucci M, Seppänen M, Kaskinoro K, Heinonen I, Kalliokoski KK. Positron emission tomography detects greater blood flow and less blood flow heterogeneity in the exercising skeletal muscles of old compared with young men during fatiguing contractions. J Physiol 592: 337-349, 2014.
56. Saeed M, Sommer O, Holtz J, Bassenge E. Alpha-adrenoceptor blockade by phentolamine causes beta-adrenergic vasodilation by increased catecholamine release due to presynaptic alpha-blockade. J Cardiovasc Pharmacol 4: 44-52, 1982.
57. Seals DR, DeSouza CA, Donato AJ, Tanaka H. Habitual exercise and arterial aging. J Appl Physiol 105: 1323-1332, 2008.
58. Seals DR, Dinenno FA. Collateral damage: cardiovascular consequences of chronic sympathetic activation with human aging. Am J Physiol Heart Circ Physiol 287: H1895-H1905, 2004.
59. Siri WE. Body composition from fluid space and density. In: Techniques for Measuring Body Composition, edited by Brozek J, Hanschel A. Washington, DC: National Academy of Science, 1961.
60. 2O. J Appl Physiol 86: 1054-1061, 1999.
61. Su SH, Jen CJ, Chen HI. NO signaling in exercise training-induced anti-apaptotic effects in human neutrophils. Biochem Biophys Res Commun 405: 58-63, 2011.
62. Sugawara J, Komine H, Hayashi K, Yoshizawa M, Otsuki T, Shimojo N, Miyauchi T, Yokoi T, Maeda S, Tanaka H. Systemic alpha-adrenergic and nitric oxide inhibition on basal limb blood flow: effects of endurance training in middle-aged and older adults. Am J Physiol Heart Circ Physiol 293: H1466-H1472, 2007.
63. Trinity JD, Groot HJ, Layec G, Rossman MJ, Ives SJ, Richardson RS. Impact of age and body position on the contribution of nitric oxide to femoral artery shear rate: implications for atherosclerosis. Hypertension 63: 1019-1025, 2014.
64. Wallgren F, Amberg G, Hickner RC, Ekelund U, Jorfeldt L, Henriksson J. A mathematical model for measuring blood flow in skeletal muscle with the microdialysis ethanol technique. J Appl Physiol 79: 648-659, 1995.
65. Wilmore JH, Vodak PA, Parr RB, Girandola RN, Billing JE. Further simplification of a method for determination of residual lung volume. Med Sci Sports Exerc 12: 216-218, 1980.
66. 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.
67. Wray DW, Nishiyama SK, Richardson RS. Role of α1-adrenergic vasoconstriction in the regulation of skeletal muscle blood flow with advancing age. Am J Physiol Heart Circ Physiol 296: H497-H504, 2009.
68. Wray DW, Uberoi A, Lawrenson L, Richardson RS. Evidence of preserved endothelial function and vascular plasticity with age. Am J Physiol Heart Circ Physiol 290: H1271-H1277, 2006.
69. Yang AL, Tsai SJ, Jiang MJ, Jen CJ, Chen HI. Chronic exercise increases both inducible and endothelial nitric oxide synthase gene expression in endothelial cells of rat aorta. J Biomed Sci 9: 149-155, 2002.
70. Yang H, Drummer TD, Carter JR. Sex differences in sympathetic neural and limb vascular reactivity to mental stress in humans. Am J Physiol Heart Circ Physiol 304: H436-H443, 2013.