Antagonism of soluble guanylyl cyclase attenuates cutaneous vasodilation during whole body heat stress and local warming in humans

Journal of Applied Physiology

Volumn 110, Issue 5, 2011, Pages 1406-1413

  Kellogg Jr , Dean L ^a,b,c   Zhao, Joan L ^a,b   Wu, Yubo ^a,b   Johnson, John M ^c  

^a SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Guanosine 3=,5= cyclic monophosphate; Microdialysis; Nitric oxide; Skin; Thermoregulation

Indexed keywords

GUANYLATE CYCLASE; NITRIC OXIDE;

ADULT; ARTICLE; BLOOD FLOW VELOCITY; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; HEAT SHOCK RESPONSE; HUMAN; METABOLISM; PHYSIOLOGY; SKIN; SKIN TEMPERATURE; SOLUBILITY; THERMOREGULATION; VASCULARIZATION; VASODILATATION;

ADULT; BLOOD FLOW VELOCITY; BODY TEMPERATURE REGULATION; FEMALE; GUANYLATE CYCLASE; HEAT-SHOCK RESPONSE; HUMANS; NITRIC OXIDE; SKIN; SKIN TEMPERATURE; SOLUBILITY; VASODILATION;

EID: 79956089457     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00702.2010     Document Type: Article

References (64)

1. + currents in frog cardiac myocytes. Br J Pharmacol 121: 1369-1377, 1997. (Pubitemid 27317549)
2. Ahern GP, Klyachko VA, Jackson MB. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 25: 510-517, 2002. (Pubitemid 35246321)
3. Anderson C, Andersson T, Wardell K. Changes in skin circulation after insertion of a microdialysis probe visualized by laser-Doppler perfusion imaging. J Invest Dermatol 102: 808-811, 1994.
4. Aoki K, Stephens DP, Johnson JM. Diurnal variation in cutaneous vasodilator and vasoconstrictor systems during heat stress. Am J Physiol Regul Integr Comp Physiol 281: R591-R595, 2001.
5. Bellamy TC, Wood J, Garthwaite J. On the activation of soluble guanylyl cyclase by nitric oxide. Proc Natl Acad Sci U S A 99: 507-510, 2002. (Pubitemid 34060391)
6. Bennett LA, Johnson JM, Stephens DP, Saad AR, Kellogg DL Jr. Evidence for a role for vasoactive intestinal peptide in active vasodilation in the cutaneous vasculature in humans. J Physiol 552: 223-232, 2003. (Pubitemid 37265480)
7. Carvajal JA, Germain AM, Huidobro-Toro JP, Weiner CP. Molecular mechanism of cGMP-mediated smooth muscle relaxation. J Cell Physiol 184: 409-420, 2000. (Pubitemid 30625505)
8. Cracowski JL, Minson CT, Salvat-Melis M, Halliwill JR. Methodological issues in the assessment of skin microvascular endothelial function in humans. Trends Pharmacol Sci 27: 503-508, 2006. (Pubitemid 44233694)
9. Deak F, Xu Y, Chang W, Khvotchev M, Liu X, Sudhof TC, Rizo J. Munc18-1 binding to the neuronal SNARE complex controls synaptic vesicle priming. J Cell Biol 184: 751-764, 2009.
10. Dietz NM, Rivera JM, Warner DO, Joyner MJ. Is nitric oxide involved in cutaneous vasodilation during body heating in humans? J Appl Physiol 76: 2047-2053, 1994. (Pubitemid 24158635)
11. Friebe A, Koesling D. Regulation of nitric oxide-sensitive guanylyl cyclase. Circ Res 93: 96-105, 2003. (Pubitemid 36919696)
12. Garthwaite J, Southan GJ, Boulton CL, Nielsen EB, Schmidt K, Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. J Pharmacol Exp Ther 48: 184-188, 1995.
13. Gonzalez DR, Fernandez IC, Ordenes PP, Treuer AV, Eller G, Boric MP. Differential role of S-nitrosylation and the NO-cGMP-PKG pathway in cardiac contractility. Nitric Oxide 18: 157-167, 2008. (Pubitemid 351447291)
14. Hill BG, Dranka BP, Bailey SM, Lancaster JR Jr, Darley-Usmar VM. What part of NO don't you understand? Some answers to the cardinal questions in nitric oxide biology. J Biol Chem 285: 19699-19704, 2010.
15. Hodges GJ, Chu C, Kosiba WA, Zhao K, Johnson JM. The effect of microdialysis needle trauma on cutaneous vascular responses in humans. J Appl Physiol 106: 1112-1118, 2009.
16. Hwang T, Wu C, Teng C. Comparison of two soluble guanylyl cyclase inhibitors, methylene blue and ODQ, of sodium nitroprussideinduced relaxation in guinea-pig trachea. Br J Pharmacol 125: 1158-1163, 1998. (Pubitemid 28542522)
17. Jackson EB Jr, Mukhopadhyay S, Tulis DA. Pharmacologic modulators of soluble guanylate cyclase/cyclic guanosine monophosphate in the vascular system-from bench top to bedside. Curr Vasc Pharmacol 5: 1-14, 2007.
18. Johnson JM, Park MK. Effect of upright exercise on threshold for cutaneous vasodilation and sweating. J Appl Physiol 50: 814-818, 1981. (Pubitemid 11102307)
19. Johnson JM, Proppe DW. Cardiovascular adjustments to heat stress. In: Handbook of physiology. Environmental Physiology. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 4, vol. I, chapt. 11, p. 215-243.
20. Johnson JM, Taylor WF, Shepherd AP, Park MK. Laser-Doppler measurement of skin blood flow: comparison with plethysmography. J Appl Physiol 56: 798-803, 1984. (Pubitemid 14149493)
21. Kellogg DL Jr. In vivo mechanisms of cutaneous vasodilation and vasoconstriction in humans. J Appl Physiol 100: 1709-1718, 2006.
22. 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. (Pubitemid 28413257)
23. Kellogg DL Jr, Johnson JM, Kenney WL, Pergola PE, Kosiba WA. Mechanisms of control of skin blood flow during prolonged exercise in humans. Am J Physiol Heart Circ Physiol 265: H562-H568, 1993. (Pubitemid 23273592)
24. Kellogg DL Jr, Liu Y, Kosiba IF, O'Donnell D. Role of nitric oxide in the vascular effects of local warming of the skin in humans. J Appl Physiol 86: 1185-1190, 1999. (Pubitemid 29172150)
25. Kellogg DL Jr, Pérgola PE, Kosiba WA, Grossmann M, Johnson JM. Cutaneous active vasodilation in humans is mediated by cholinergic nerve co-transmission. Circ Res 77: 1222-1228, 1995.
26. Kellogg DL Jr, Zhao JL, Coey U, Green JV. Acetylcholine induced vasodilation is mediated by nitric oxide and prostaglandins in human skin. J Appl Physiol 98: 629-632, 2005. (Pubitemid 40129975)
27. Kellogg DL Jr, Zhao JL, Friel C, Roman LJ. Nitric oxide concentration increases in the cutaneous interstitial space during heat stress in humans. J Appl Physiol 94: 1971-1977, 2003. (Pubitemid 36457450)
28. Kellogg DL Jr, Zhao JL, Wu Y. Endothelial nitric oxide synthase control mechanisms in the cutaneous vasculature of humans in vivo. Am J Physiol Heart Circ Physiol 295: H123-H129, 2008.
29. Kellogg DL Jr, Zhao JL, Wu Y. Neuronal nitric oxide synthase mechanisms in the cutaneous vasculature of humans in vivo. J Physiol 586: 847-857, 2008. (Pubitemid 351194122)
30. Kellogg DL Jr, Zhao JL, Wu Y. Roles of nitric oxide synthase isoforms in cutaneous vasodilation induced by local warming of the skin and whole body heat stress in humans. J Appl Physiol 107: 1438-1444, 2009.
31. Koesling D, Russwurm M, Mergia E, Mullershausen F, Friebe A. Nitric oxide-sensitive guanylyl cyclase: structure and regulation. Neurochem Int 45: 813-819, 2004. (Pubitemid 39108053)
32. Kreidstein ML, Pang CY, Carlsen LN, Xu N. Evidence for endothelium-dependent and endothelium-independent vasodilation in human skin flaps. Can J Physiol Pharmacol 70: 1208-1216, 1992. (Pubitemid 23036653)
33. Lamas S, Lowenstein CJ, Michel T. Nitric oxide signaling comes of age: 20 years and thriving. Cardiovasc Res 75: 207-209, 2007. (Pubitemid 46961937)
34. 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. (Pubitemid 44352341)
35. Medow MS, Taneja I, Stewart JM. Cyclooxygenase and nitric oxide synthase dependence of cutaneous reactive hyperemia in humans. Am J Physiol Heart Circ Physiol 293: H425-H432, 2007. (Pubitemid 47105099)
36. Meffert MK, Calakos NC, Scheller RH, Schulman H. Nitric oxide modulates synaptic vesicle docking/fusion reactions. Neuron 16: 1229-1236, 1996. (Pubitemid 26230092)
37. Minson CT, Berry LT, Joyner MJ. Nitric oxide and neurally mediated regulation of skin blood flow during local heating. J Appl Physiol 91: 1619-1626, 2001. (Pubitemid 32900352)
38. Palmer ZJ, Duncan RR, Johnson JR, Lian L, Mello LV, Booth D, Barclay JW, Graham ME, Burgoyne RD, Prior IA, Morgan A. S-nitrosylation of syntaxin 1 at Cys145 is a regulatory switch controlling Munc18-1 binding. Biochem J 413: 479-491, 2008.
39. Parati G, Casadei R, Groppelli A, Di Rienzo M, Mancia G. Comparison of finger and intra arterial blood pressure monitoring at rest and during laboratory testing. Hypertension 13: 647-655, 1989. (Pubitemid 19157951)
40. Poulos TL. Soluble guanylate cyclase. Curr Opin Struct Biol 16: 736-743, 2006. (Pubitemid 44834471)
41. Rowell LB. Human cardiovascular adjustments to exercise and thermal stress. Physiol Rev 54: 75-159, 1974.
42. Rowell LB. Human Circulation: Regulation During Physical Stress. New York: Oxford Univ. Press, 1986.
43. Rowell LB, Murray JA, Brengelmann GL, Kraning KK II. Human cardiovascular adjustments to rapid changes in skin temperature during exercise. Cir Res 24: 711-724, 1969.
44. Saumet JL, Kellogg DL Jr, Taylor WF, Johnson JM. Cutaneous laser-Doppler flowmetry: influence of underlying muscle blood flow. J Appl Physiol 65: 478-481, 1988.
45. Schrammel A, Behrends S, Schmidt K, Koesling D, Mayer B. Characterization of 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one as a hemesite inhibitor of nitric oxide-sensitive guanylyl cyclase. J Pharmacol Exp Ther 50: 1-5, 1996. (Pubitemid 26250067)
46. Shastry S, Joyner MJ. Geldanamycin attenuates NO-mediated dilation in human skin. Am J Physiol Heart Circ Physiol 282: H232-H236, 2002. (Pubitemid 34654154)
47. Shastry S, Minson CT, Wilson SA, Dietz NK, Joyner MJ. Effects of atropine and L-NAME on cutaneous blood flow during body heating in humans. J Appl Physiol 88: 467-472, 2000. (Pubitemid 30097088)
48. Shastry S, Reed AS, Halliwill JR, Dietz NM, Joyner MJ. Effects of nitric oxide synthase inhibition on cutaneous vasodilation during body heating in humans. J Appl Physiol 85: 830-834, 1998. (Pubitemid 28413258)
49. 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. (Pubitemid 35379318)
50. Stewart JM, Medow MS, Minson CT, Taneja I. Cutaneous neuronal nitric oxide is specifically decreased in postural tachycardia syndrome. Am J Physiol Heart Circ Physiol 293: H2161-H2167, 2007. (Pubitemid 47605858)
51. Stewart JM, Taneja I, Raghunath N, Clarke D, Medow MS. Intradermal angiotensin II administration attenuates the local cutaneous vasodilator heating response. Am J Physiol Heart Circ Physiol 295: H237-H334, 2008.
52. Taylor WF, Johnson JM, Kosiba WA, Kwan CM. Cutaneous vascular responses to isometric handgrip exercise. J Appl Physiol 66: 1586-1592, 1989. (Pubitemid 19112961)
53. Taylor WF, Johnson JM, O'Leary D, Park MK. Effect of high local temperature on reflex cutaneous vasodilation. J Appl Physiol 57: 191-196, 1984. (Pubitemid 14098698)
54. Taylor WF, Johnson JM, O'Leary D, Park MK. Modification of the cutaneous vascular response to exercise by local skin temperature. J Appl Physiol 57: 1878-1884, 1984. (Pubitemid 15191391)
55. Tseng CL, Tabrizi-Fard M, Fung H. Differential sensitivity among nitric oxide donors toward odq-mediated inhibition of vascular relaxation. J Pharmacol Exp Ther 292: 737-742, 2000. (Pubitemid 30067439)
56. Wanstall JC, Homer KL, Doggrell. Evidence for, and importance of, cGMP-independent mechanisms with NO and NO donors on blood vessels and platelets. Curr Vasc Pharmacol 3: 41-53, 2005. (Pubitemid 40089526)
57. Wilkins BW, Holowatz LA, Wong BJ, Minson CT. Nitric oxide is not permissive for cutaneous active vasodilation in humans. J Physiol 548: 963-969, 2003. (Pubitemid 36592788)
58. Wong BJ, Minson CT. Neurokinin-1 receptor desensitization attenuates cutaneous active vasodilation in humans. J Physiol 577: 1043-1051, 2006. (Pubitemid 44882611)
59. Wong BJ, Wilkins BW, Holowatz LA, Minson CT. Nitric oxide synthase inhibition does not alter the reactive hyperemic response in the cutaneous circulation. J Appl Physiol 95: 504-510, 2003. (Pubitemid 36944270)
60. 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. (Pubitemid 39530130)
61. Zhao JL, Pergola PE, Roman LJ, Kellogg J DL. Bioactive nitric oxide concentration does not increase during reactive hyperemia in humans. J Appl Physiol 96: 628-632, 2004. (Pubitemid 38140165)
62. Zhao Y, Brandish PE, DiValentin M, Schelvis JPM, Babcock GT, MAM. Inhibition of soluble guanylate cyclase by ODQ. Biochemistry 39: 10848-10854, 2000.
63. Zimmet JM, Hare JM. Nitroso-redox interactions in the cardiovascular system. Circulation 114: 1531-1544, 2006. (Pubitemid 44527009)
64. Ziolo MT. The fork in the nitric oxide road: cyclic GMP or nitrosylation. Nitric Oxide 18: 153-156, 2008.