Peripheral mechanisms of thermoregulatory control of skin blood flow in aged humans

Journal of Applied Physiology

Volumn 109, Issue 5, 2010, Pages 1538-1544

  Holowatz, Lacy A ^a   Kenney, W Larry ^a,b  

^a Department of Kinesiology ^*  (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Cold; Heat; Microvascular; Temperature regulation; Vascular

Indexed keywords

ADRENERGIC SYSTEM; AGING; BLOOD FLOW; HEMODYNAMICS; HUMAN; INNERVATION; MICROCIRCULATION; MICROVASCULATURE; PHYSIOLOGY; REFLEX; REVIEW; SKIN; THERMOREGULATION; VASCULARIZATION; VASOCONSTRICTION; VASODILATATION;

AGING; BODY TEMPERATURE REGULATION; HEMODYNAMICS; HUMANS; MICROCIRCULATION; MICROVESSELS; REFLEX; REGIONAL BLOOD FLOW; SKIN; SYMPATHETIC NERVOUS SYSTEM; VASOCONSTRICTION; VASODILATION;

EID: 78149350061     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00338.2010     Document Type: Review

References (76)

1. Armstrong CG, Kenney WL. Effects of age and acclimation on responses to passive heat exposure. J Appl Physiol 75: 2162-2167, 1993.
2. Bailey SR, Eid AH, Mitra S, Flavahan S, Flavahan NA. Rho kinase mediates cold-induced constriction of cutaneous arteries: role of alpha2Cadrenoceptor translocation. Circ Res 94: 1367-1374, 2004.
3. Bailey SR, Mitra S, Flavahan S, Flavahan NA. Reactive oxygen species from smooth muscle mitochondria initiate cold-induced constriction of cutaneous arteries. Am J Physiol Heart Circ Physiol 289: H243-H250, 2005.
4. 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.
5. Boignard A, Salvat-Melis M, Carpentier PH, Minson CT, Grange L, Duc C, Sarrot-Reynauld F, Cracowski JL. Local hyperemia to heating is impaired in secondary Raynaud's phenomenon. Arthriris Res Ther 7: R1103-R1112, 2005.
6. Busse R, Ogilvie A, Pohl U. Vasomotor activity of diadenosine triphosphate and diadenosine tetraphosphate in isolated arteries. Am J Physiol Heart Circ Physiol 254: H828-H832, 1988.
7. Charkoudian N. Mechanisms and modifiers of reflex induced cutaneous vasodilation and vasoconstriction in humans. Journal of Applied Physiology. In press.
8. Collins KJ, Dore C, Exton-Smith AN, Fox RH, MacDonald IC, Woodward PM. Accidental hypothermia and impaired temperature homoeostasis in the elderly. Br Med J 1: 353-356, 1977.
9. Connat JL, Busseuil D, Gambert S, Ody M, Tebaldini M, Gamboni S, Faivre B, Quiquerez AL, Millet M, Michaut P, Rochette L. Modification of the rat aortic wall during ageing; possible relation with decrease of peptidergic innervation. Anat Embryol (Berl) 204: 455-468, 2001.
10. DeGroot DW, Havenith G, Kenney WL. Responses to mild cold stress are predicted by different individual characteristics in young and older subjects. J Appl Physiol 101: 1607-1615, 2006.
11. Degroot DW, Kenney WL. Impaired defense of core temperature in aged humans during mild cold stress. Am J Physiol Regul Integr Comp Physiol 292: R103-R108, 2007.
12. Delp MD, Behnke BJ, Spier S, Wu G, Muller-Delp J. Ageing diminishes endothelium-dependent vasodilation and tetrahydrobiopterin content in rat skeletal muscle arterioles. The Journal of physiology 586: 1161-1168, 2008.
13. Demougeot C, Prigent-Tessier A, Bagnost T, Andre C, Guillaume Y, Bouhaddi M, Marie C, Berthelot A. Time course of vascular arginase expression and activity in spontaneously hypertensive rats. Life Sci 80: 1128-1134, 2007.
14. Demougeot C, Prigent-Tessier A, Marie C, Berthelot A. Arginase inhibition reduces endothelial dysfunction and blood pressure rising in spontaneously hypertensive rats. J Hypertens 23: 971-978, 2005.
15. Donoso V, Gomez CR, Orriantia MA, Perez V, Torres C, Coddou C, Nelson P, Maisey K, Morales B, Fernandez R, Imarai M, Huidobro- Toro JP, Sierra F, Acuna-Castillo C. The release of sympathetic neurotransmitters is impaired in aged rats after an inflammatory stimulus: a possible link between cytokine production and sympathetic transmission. Mech Ageing Dev 129: 728-734, 2008.
16. Durante W, Tulis DA, Liu X, Sankaranarayanan K, Wang H, Peyton KJ. Arginase promotes vascular smooth muscle cell proliferation and neointimal formation (Abstract). Circulation 114: 2-69, 2006.
17. Feletou M, Verbeuren TJ, Vanhoutte PM. Endothelium-dependent contractions in SHR: a tale of prostanoid TP and IP receptors. Br J Pharmacol 156: 563-574, 2009.
18. Forstermann U, Mugge A, Bode SM, Frolich JC. Response of human coronary arteries to aggregating platelets: importance of endotheliumderived relaxing factor and prostanoids. Circ Res 63: 306-312, 1988.
19. Forstermann U, Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113: 1708-1714, 2006.
20. Frank SM, Raja SN, Bulcao C, Goldstein DS. Age-related thermoregulatory differences during core cooling in humans. Am J Physiol Regul Integr Comp Physiol 279: R349-R354, 2000.
21. Frantom PA, Seravalli J, Ragsdale SW, Fitzpatrick PF. Reduction and oxidation of the active site iron in tyrosine hydroxylase: kinetics and specificity. Biochemistry 45: 2372-2379, 2006.
22. Grassi G, Seravalle G, Turri C, Bertinieri G, Dell'Oro R, Mancia G. Impairment of thermoregulatory control of skin sympathetic nerve traffic in the elderly. Circulation 108: 729-735, 2003.
23. Hajat S, Kovats RS, Lachowycz K. Heat-related and cold-related deaths in England and Wales: who is at risk? Occup Environ Med 64: 93-100, 2007.
24. Holowatz LA, Houghton BL, Wong BJ, Wilkins BW, Harding AW, Kenney WL, Minson CT. Nitric oxide and attenuated reflex cutaneous vasodilation in aged skin. Am J Physiol Heart Circ Physiol 284: H1662-H1667, 2003.
25. Holowatz LA, Jennings JD, Lang JA, Kenney WL. Ketorolac alters blood flow during normothermia but not during hyperthermia in middle aged human skin. J Appl Physiol 107: 1121-1127, 2009.
26. Holowatz LA, Jennings JD, Lang JA, Kenney WL. Systemic low-dose aspirin and clopidogrel independently attenuate reflex cutaneous vasodilation in middle aged humans. J Appl Physiol 108: 1575-1581, 2010.
27. Holowatz LA, Kenney WL. Chronic low-dose aspirin therapy attenuates reflex cutaneous vasodilation in middle-aged humans. J Appl Physiol 106: 500-505, 2008.
28. Holowatz LA, Kenney WL. Local ascorbate administration augments NO- and non-NO-dependent reflex cutaneous vasodilation in hypertensive humans. Am J Physiol Heart Circ Physiol 293: H1090-H1096, 2007.
29. Holowatz LA, Kenney WL. Up-regulation of arginase activity contributes to attenuated reflex cutaneous vasodilatation in hypertensive humans. J Physiol 581: 863-872, 2007.
30. Holowatz LA, Thompson-Torgerson C, Kenney WL. Aging and the control of human skin blood flow. Front Biosci 15: 718-739.
31. Holowatz LA, Thompson CS, Kenney WL. L-Arginine supplementation or arginase inhibition augments reflex cutaneous vasodilatation in aged human skin. J Physiol 574: 573-581, 2006.
32. Holowatz LA, Thompson CS, Kenney WL. L-Arginine supplementation or arginase inhibition augments reflex cutaneous vasodilatation in aged human skin. J Physiol 574: 573-581, 2006.
33. Holowatz LA, Thompson CS, Minson CT, Kenney WL. Mechanisms of acetylcholine-mediated vasodilatation in young and aged human skin. J Physiol 563: 965-973, 2005.
34. Katusic ZS, Vanhoutte PM. Superoxide anion is an endothelium-derived contracting factor. Am J Physiol Heart Circ Physiol 257: H33-H37, 1989.
35. Kaul S, Padgett RC, Waack BJ, Brooks RM, Heistad DD. Effect of atherosclerosis on responses of the perfused rabbit carotid artery to human platelets. Arterioscler Thromb 12: 1206-1213, 1992.
36. Kellogg DL Jr, Crandall CG, Liu Y, Charkoudian N, Johnson JM. Nitric oxide and cutaneous active vasodilation during heat stress in humans. J Appl Physiol 85: 824-829, 1998.
37. Kenney WL. Control of heat-induced cutaneous vasodilatation in relation to age. Eur J Appl Physiol Occup Physiol 57: 120-125, 1988.
38. Kenney WL, Armstrong CG. Reflex peripheral vasoconstriction is diminished in older men. J Appl Physiol 80: 512-515, 1996.
39. Kenney WL, Morgan AL, Farquhar WB, Brooks EM, Pierzga JM, Derr JA. Decreased active vasodilator sensitivity in aged skin. Am J Physiol Heart Circ Physiol 272: H1609-H1614, 1997.
40. Kenney WL, Munce TA. Invited review: Aging and human temperature regulation. J Appl Physiol 95: 2598-2603, 2003.
41. Kenney WL, Tankersley CG, Newswanger DL, Hyde DE, Puhl SM, Turner NL. Age and hypohydration independently influence the peripheral vascular response to heat stress. J Appl Physiol 68: 1902-1908, 1990.
42. Kikuchi M, Shirasaki H, Himi T. Platelet-activating factor (PAF) increases NO production in human endothelial cells-real-time monitoring by DAR-4M AM. Prostaglandins Leukot Essent Fatty Acids 78: 305-309, 2008.
43. Konishi C, Naito Y, Ohara N. Age-related changes in adenosine 5=- triphosphate-induced constriction of isolated, perfused mesenteric arteries of rats. Life Sci 64: 1265-1273, 1999.
44. Kuzkaya N, Weissmann N, Harrison DG, Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J Biol Chem 278: 22546-22554, 2003.
45. Lambert ML, Callow ID, Feng QP, Arnold JM. The effects of age on human venous responsiveness to neuropeptide Y. Br J Clin Pharmacol 47: 83-89, 1999.
46. Lang JA, Holowatz LA, Kenney WL. Local tetrahydrobiopterin administration augments cutaneous vasoconstriction in aged humans. J Physiol 587: 3967-3974, 2009.
47. Lang JA, Holowatz LA, Kenney WL. Localized tyrosine or tetrahydrobiopterin supplementation corrects the age-related decline in cutaneous vasoconstriction. J Physiol 588: 1361-1368, 2010.
48. Lang JA, Jennings JD, Holowatz LA, Kenney WL. Reflex vasoconstriction in aged human skin increasingly relies on rho-kinase dependent mechanisms during whole-body cooling. Am J Physiol Heart Circ Physiol 297: H1792-H1797, 2009.
49. Li H, Witte K, August M, Brausch I, Godtel-Armbrust U, Habermeier A, Closs EI, Oelze M, Munzel T, Forstermann U. Reversal of endothelial nitric oxide synthase uncoupling and up-regulation of endothelial nitric oxide synthase expression lowers blood pressure in hypertensive rats. J Am Coll Cardiol 47: 2536-2544, 2006.
50. Martin HL, Loomis JL, Kenney WL. Maximal skin vascular conductance in subjects aged 5-85 yr. J Appl Physiol 79: 297-301, 1995.
51. McCord GR, Cracowski JL, Minson CT. Prostanoids contribute to cutaneous active vasodilation in humans. Am J Physiol Regul Integr Comp Physiol 291: R596-R602, 2006.
52. Minson CT, Holowatz LA, Wong BJ, Kenney WL, Wilkins BW. Decreased nitric oxide- and axon reflex-mediated cutaneous vasodilation with age during local heating. J Appl Physiol 93: 1644-1649, 2002.
53. Mombouli JV, Vanhoutte PM. Endothelium-derived hyperpolarizing factor(s): updating the unknown. Trends Pharmacol Sci 18: 252-256, 1997.
54. Nicholson WT, Vaa B, Hesse C, Eisenach JH, Joyner MJ. Aging is associated with reduced prostacyclin-mediated dilation in the human forearm. Hypertension 53: 973-978, 2009.
55. Noguchi K, Matsuzaki T, Shiroma N, Ojiri Y, Sakanashi M. Involvement of nitric oxide and eicosanoids in platelet-activating factor-induced haemodynamic and haematological effects in dogs. Br J Pharmacol 118: 941-950, 1996.
56. Oskarsson HJ, Hofmeyer TG. Platelets from patients with diabetes mellitus have impaired ability to mediate vasodilation. J Am Coll Cardiol 27: 1464-1470, 1996.
57. Pedersen AK, FitzGerald GA. Dose-related kinetics of aspirin. Presystemic acetylation of platelet cyclooxygenase. N Engl J Med 311: 1206-1211, 1984.
58. Peyton KJ, Ensenat D, Azam MA, Keswani AN, Kannan S, Liu XM, Wang H, Tulis DA, Durante W. Arginase promotes neointima formation in rat injured carotid arteries. Arterioscler Thromb 29: 488-494, 2009.
59. Ramsey AJ, Hillas PJ, Fitzpatrick PF. Characterization of the active site iron in tyrosine hydroxylase. Redox states of the iron. J Biol Chem 271: 24395-24400, 1996.
60. Rousseau P, Tartas M, Fromy B, Godon A, Custaud MA, Saumet JL, Abraham P. Platelet inhibition by low-dose aspirin but not by clopidogrel reduces the axon-reflex current-induced vasodilation in humans. Am J Physiol Regul Integr Comp Physiol 294: R1420-R1426, 2008.
61. Ryoo S, Lemmon CA, Soucy KG, Gupta S, White AR, Nyhan D, Shoukas AA, Romer LH, Berkowitz DE. Oxidized low-density lipoprotein- dependent endothelial arginase II activation contributes to impaired nitric oxide signaling. Circ Res 99: 951-960, 2006.
62. Santhanam L, Lim HK, Lim HK, Miriel V, Brown T, Patel M, Balanson S, Ryoo S, Anderson M, Irani K, Khanday F, Di Costanzo L, Nyhan D, Hare JM, Christianson DW, Rivers R, Shoukas A, Berkowitz DE. Inducible NO synthase dependent S-nitrosylation and activation of arginase1 contribute to age-related endothelial dysfunction. Circ Res 101: 692-702, 2007.
63. Shibasaki M, Wilson TE, Cui J, Crandall CG. Acetylcholine released from cholinergic nerves contributes to cutaneous vasodilation during heat stress. J Appl Physiol 93: 1947-1951, 2002.
64. Sokolnicki LA, Strom NA, Roberts SK, Kingsley-Berg SA, Basu A, Charkoudian N. Skin blood flow and nitric oxide during body heating in type 2 diabetes mellitus. J Appl Physiol 106: 566-570, 2009.
65. Stephens DP, Aoki K, Kosiba WA, Johnson JM. Nonnoradrenergic mechanism of reflex cutaneous vasoconstriction in men. Am J Physiol Heart Circ Physiol 280: H1496-H1504, 2001.
66. Stephens DP, Saad AR, Bennett LA, Kosiba WA, Johnson JM. Neuropeptide Y antagonism reduces reflex cutaneous vasoconstriction in humans. Am J Physiol Heart Circ Physiol 287: H1404-H1409, 2004.
67. Strom NA, Sawyer JR, Roberts SK, Kingsley-Berg SM, Charkoudian N. Local sensory nerve control of skin blood flow during local warming in type 2 diabetes mellitus. J Appl Physiol 108: 293-297, 2010.
68. Tang EH, Vanhoutte PM. Gene expression changes of prostanoid synthases in endothelial cells and prostanoid receptors in vascular smooth muscle cells caused by aging and hypertension. Physiol Genomics 32: 409-418, 2008.
69. Thompson CS, Holowatz LA, Kenney WL. Attenuated noradrenergic sensitivity during local cooling in aged human skin. J Physiol 564: 313-319, 2005.
70. Thompson CS, Holowatz LA, Kenney WL. Cutaneous vasoconstrictor responses to norepinephrine are attenuated in older humans. Am J Physiol Regul Integr Comp Physiol 288: R1108-R1113, 2005.
71. Thompson CS, Kenney WL. Altered neurotransmitter control of reflex vasoconstriction in aged human skin. J Physiol 558: 697-704, 2004.
72. Topal JL, Brunet A, Walch L, Boucher JL, David-Dufilho M. Mitochondrial arginase II modulates nitric-oxide synthesis through nonfreely exchangeable L-arginine pools in human endothelial cells. J Pharmacol Exp Ther 318: 1368-1374, 2006.
73. White AR, Ryoo S, Li D, Champion HC, Steppan J, Wang D, Nyhan D, Shoukas AA, Hare JM, Berkowitz DE. Knockdown of arginase I restores NO signaling in the vasculature of old rats. Hypertension 47: 245-251, 2006.
74. Wong BJ, Minson CT. Neurokinin-1 receptor desensitisation attenuates cutaneous active vasodilatation in humans. J Physiol 577: 1043-1051, 2006.
75. Wong BJ, Wilkins BW, Minson CT. H1 but not H2 histamine receptor activation contributes to the rise in skin blood flow during whole body heating in humans. J Physiol 560: 941-948, 2004.
76. Yi SL, Kantores C, Belcastro R, Cabacungan J, Tanswell AK, Jankov RP. 8-Isoprostane-induced endothelin-1 production by infant rat pulmonary artery smooth muscle cells is mediated by Rho-kinase. Free Radic Biol Med 41: 942-949, 2006.