Nitrite and S-Nitrosohemoglobin Exchange Across the Human Cerebral and Femoral Circulation: Relationship to Basal and Exercise Blood Flow Responses to Hypoxia

Circulation

Volumn 135, Issue 2, 2017, Pages 166-176

  Bailey, Damian M ^a,b   Rasmussen, Peter ^c   Overgaard, Morten ^c   Evans, Kevin A ^b   Bohm, Aske M ^c   Seifert, Thomas ^c   Brassard, Patrice ^c,d   Zaar, Morten ^c   Nielsen, Henning B ^c   Raven, Peter B ^e   Secher, Niels H ^c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF GLAMORGAN   (United Kingdom)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITÉ LAVAL   (Canada)

^e UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

Brain; Hypoxia, exercise; Muscles; Nitric oxide; Physiology

Indexed keywords

DEOXYHEMOGLOBIN; HEMOGLOBIN DERIVATIVE; NITRIC OXIDE; NITRITE; NITROSOHEMOGLOBIN; OXYGEN; UNCLASSIFIED DRUG; HEMOGLOBIN; S-NITROSOHEMOGLOBIN;

ADULT; ARTICLE; BLOOD OXYGEN TENSION; BLOOD OXYGENATION; BLOOD SAMPLING; BRACHIAL ARTERY; BRAIN BLOOD FLOW; CHEMOLUMINESCENCE; CYCLING; ERYTHROCYTE; EXERCISE; FEMALE; FEMORAL ARTERY FLOW; FEMORAL VEIN; HUMAN; HYPOXEMIA; HYPOXIA; INTERNAL JUGULAR VEIN; MALE; NORMAL HUMAN; PRIORITY JOURNAL; REST; THERMODILUTION; TRANSCRANIAL DOPPLER ULTRASONOGRAPHY; YOUNG ADULT; BLOOD; BRAIN CIRCULATION; CONTROLLED STUDY; METABOLISM; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; SKELETAL MUSCLE; VASCULARIZATION;

ADULT; CEREBROVASCULAR CIRCULATION; ERYTHROCYTES; EXERCISE; FEMALE; HEMOGLOBINS; HUMANS; HYPOXIA; MALE; MUSCLE, SKELETAL; NITRIC OXIDE; NITRITES; OXYGEN;

EID: 85002375730     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.116.024226     Document Type: Article

References (42)

1. Segal SS, Duling BR. Flow control among microvessels coordinated by intercellular conduction. Science. 1986;234:868-870.
2. Jia L, Bonaventura C, Bonaventura J, Stamler JS. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature. 1996;380:221-226. doi: 10.1038/380221a0.
3. Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO 3rd, Gladwin MT. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med. 2003;9:1498-1505. doi: 10.1038/nm954.
4. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, Gernert K, Piantadosi CA. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science. 1997;276:2034-2037.
5. Green DJ, Maiorana A, O'Driscoll G, Taylor R. Effect of exercise training on endothelium-derived nitric oxide function in humans. J Physiol. 2004;561(pt 1):1-25. doi: 10.1113/jphysiol.2004.068197.
6. Gladwin MT, Schechter AN. NO contest: nitrite versus S-nitrosohemoglobin. Circ Res. 2004;94:851-855. doi: 10.1161/01. RES.0000126697.64381.37.
7. Pawloski JR, Hess DT, Stamler JS. Export by red blood cells of nitric oxide bioactivity. Nature. 2001;409:622-626. doi: 10.1038/35054560.
8. Gladwin MT, Shelhamer JH, Schechter AN, Pease-Fye ME, Waclawiw MA, Panza JA, Ognibene FP, Cannon RO 3rd. Role of circulating nitrite and S-nitrosohemoglobin in the regulation of regional blood flow in humans. Proc Natl Acad Sci U S A. 2000;97:11482-11487. doi: 10.1073/pnas.97.21.11482.
9. McMahon TJ, Moon RE, Luschinger BP, Carraway MS, Stone AE, Stolp BW, Gow AJ, Pawloski JR, Watke P, Singel DJ, Piantadosi CA, Stamler JS. Nitric oxide in the human respiratory cycle. Nat Med. 2002;8:711-717. doi: 10.1038/nm718.
10. Peebles KC, Richards AM, Celi L, McGrattan K, Murrell CJ, Ainslie PN. Human cerebral arteriovenous vasoactive exchange during alterations in arterial blood gases. J Appl Physiol (1985). 2008;105:1060-1068. doi: 10.1152/japplphysiol. 90613.2008.
11. Cannon RO 3rd, Schechter AN, Panza JA, Ognibene FP, Pease-Fye ME, Waclawiw MA, Shelhamer JH, Gladwin MT. Effects of inhaled nitric oxide on regional blood flow are consistent with intravascular nitric oxide delivery. J Clin Invest. 2001;108:279-287. doi: 10.1172/JCI12761.
12. Dejam A, Hunter CJ, Pelletier MM, Hsu LL, Machado RF, Shiva S, Power GG, Kelm M, Gladwin MT, Schechter AN. Erythrocytes are the major intravascular storage sites of nitrite in human blood. Blood. 2005;106:734-739. doi: 10.1182/blood-2005-02-0567.
13. Dufour SP, Patel RP, Brandon A, Teng X, Pearson J, Barker H, Ali L, Yuen AH, Smolenski RT, González-Alonso J. Erythrocyte-dependent regulation of human skeletal muscle blood flow: role of varied oxyhemoglobin and exercise on nitrite, S-nitrosohemoglobin, and ATP. Am J Physiol Heart Circ Physiol. 2010;299:H1936-H1946. doi: 10.1152/ajpheart.00389.2010.
14. Bailey DM, Taudorf S, Berg RM, Lundby C, McEneny J, Young IS, Evans KA, James PE, Shore A, Hullin DA, McCord JM, Pedersen BK, Möller K. Increased cerebral output of free radicals during hypoxia: implications for acute mountain sickness? Am J Physiol Regul Integr Comp Physiol. 2009;297:R1283-R1292. doi: 10.1152/ajpregu.00366.2009.
15. Bailey DM, Dehnert C, Luks AM, Menold E, Castell C, Schendler G, Faoro V, Gutowski M, Evans KA, Taudorf S, James PE, McEneny J, Young IS, Swenson ER, Mairbäurl H, Bärtsch P, Berger MM. High-altitude pulmonary hypertension is associated with a free radical-mediated reduction in pulmonary nitric oxide bioavailability. J Physiol. 2010;588(pt 23):4837-4847. doi: 10.1113/jphysiol.2010.194704.
16. Gow AJ, Stamler JS. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature. 1998;391:169-173. doi: 10.1038/34402.
17. Gow AJ, Luchsinger BP, Pawloski JR, Singel DJ, Stamler JS. The oxyhemoglobin reaction of nitric oxide. Proc Natl Acad Sci U S A. 1999;96:9027-9032.
18. Blitzer ML, Lee SD, Creager MA. Endothelium-derived nitric oxide mediates hypoxic vasodilation of resistance vessels in humans. Am J Physiol. 1996;271(pt 2):H1182-H1185.
19. Gilligan DM, Panza JA, Kilcoyne CM, Waclawiw MA, Casino PR, Quyyumi AA. Contribution of endothelium-derived nitric oxide to exercise-induced vasodilation. Circulation. 1994;90:2853-2858.
20. Endo T, Imaizumi T, Tagawa T, Shiramoto M, Ando S, Takeshita A. Role of nitric oxide in exercise-induced vasodilation of the forearm. Circulation. 1994;90:2886-2890.
21. Katz SD, Krum H, Khan T, Knecht M. Exercise-induced vasodilation in forearm circulation of normal subjects and patients with congestive heart failure: role of endothelium-derived nitric oxide. J Am Coll Cardiol. 1996;28:585-590.
22. Ainslie PN, Ashmead JC, Ide K, Morgan BJ, Poulin MJ. Differential responses to CO2 and sympathetic stimulation in the cerebral and femoral circulations in humans. J Physiol. 2005;566(pt 2):613-624. doi: 10.1113/jphysiol.2005.087320.
23. Overgaard M, Rasmussen P, Bohm AM, Seifert T, Brassard P, Zaar M, Homann P, Evans KA, Nielsen HB, Secher NH. Hypoxia and exercise provoke both lactate release and lactate oxidation by the human brain. FASEB J. 2012;26:3012-3020. doi: 10.1096/fj.11-191999.
24. Woodside JD, Gutowski M, Fall L, James PE, McEneny J, Young IS, Ogoh S, Bailey DM. Systemic oxidative-nitrosative-inflammatory stress during acute exercise in hypoxia; implications for microvascular oxygenation and aerobic capacity. Exp Physiol. 2014;99:1648-1662. doi: 10.1113/expphysiol.2014.081265.
25. Madsen PL, Holm S, Herning M, Lassen NA. Average blood flow and oxygen uptake in the human brain during resting wakefulness: a critical appraisal of the Kety-Schmidt technique. J Cereb Blood Flow Metab. 1993;13:646-655. doi: 10.1038/jcbfm.1993.83.
26. Andersen P, Saltin B. Maximal perfusion of skeletal muscle in man. J Physiol. 1985;366:233-249.
27. Bailey DM, McEneny J, Mathieu-Costello O, Henry RR, James PE, McCord JM, Pietri S, Young IS, Richardson RS. Sedentary aging increases resting and exercise-induced intramuscular free radical formation. J Appl Physiol (1985). 2010;109:449-456. doi: 10.1152/japplphysiol.00354.2010.
28. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1980;288:373-376.
29. Liu H, Zhang Y, Wu H, D'Alessandro A, Yegutkin GG, Song A, Sun K, Li J, Cheng NY, Huang A, Edward Wen Y, Weng TT, Luo F, Nemkov T, Sun H, Kellems RE, Karmouty-Quintana H, Hansen KC, Zhao B, Subudhi AW, Jameson-Van Houten S, Julian CG, Lovering AT, Eltzschig HK, Blackburn MR, Roach RC, Xia Y. Beneficial role of erythrocyte adenosine A2B receptor-mediated AMP-activated protein kinase activation in high-altitude hypoxia. Circulation. 2016;134:405-421. doi: 10.1161/CIRCULATIONAHA. 116.021311.
30. Joyner MJ, Casey DP. Muscle blood flow, hypoxia, and hypoperfusion. J Appl Physiol (1985). 2014;116:852-857. doi: 10.1152/japplphysiol.00620.2013.
31. Ogoh S, Ainslie PN. Cerebral blood flow during exercise: mechanisms of regulation. J Appl Physiol (1985). 2009;107:1370-1380. doi: 10.1152/japplphysiol.00573.2009.
32. Bailey DM, Taudorf S, Berg RM, Jensen LT, Lundby C, Evans KA, James PE, Pedersen BK, Moller K. Transcerebral exchange kinetics of nitrite and calcitonin gene-related peptide in acute mountain sickness: evidence against trigeminovascular activation? Stroke. 2009;40:2205-2208. doi: 10.1161/STROKEAHA.108.543959.
33. Howarth C, Gleeson P, Attwell D. Updated energy budgets for neural computation in the neocortex and cerebellum. J Cereb Blood Flow Metab. 2012;32:1222-1232. doi: 10.1038/jcbfm. 2012.35.
34. Bailey DM, Evans KA, James PE, McEneny J, Young IS, Fall L, Gutowski M, Kewley E, McCord JM, Møller K, Ainslie PN. Altered free radical metabolism in acute mountain sickness: implications for dynamic cerebral autoregulation and blood-brain barrier function. J Physiol. 2009;587:73-85. doi: 10.1113/jphysiol. 2008.159855.
35. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Aktdependent phosphorylation. Nature. 1999;399:601-605. doi: 10.1038/21224.
36. Morgan MA, Frasier LM, Stewart JC, Mack CM, Gough MS, Graves BT, Apostolakos MJ, Doolin KP, Darling DC, Frampton MW, Pietropaoli AP. Artery-to-vein differences in nitric oxide metabolites are diminished in sepsis. Crit Care Med. 2010;38:1069-1077. doi: 10.1097/CCM.0b013e3181d16a3e.
37. Felig P, Wahren J. Fuel homeostasis in exercise. N Engl J Med. 1975;293:1078-1084. doi: 10.1056/NEJM197511202932107.
38. Kingwell BA, Sherrard B, Jennings GL, Dart AM. Four weeks of cycle training increases basal production of nitric oxide from the forearm. Am J Physiol. 1997;272(pt 2):H1070-H1077.
39. Beall CM, Laskowski D, Erzurum SC. Nitric oxide in adaptation to altitude. Free Radic Biol Med. 2012;52:1123-1134. doi: 10.1016/j.freeradbiomed.2011.12.028.
40. Wilson MH, Edsell ME, Davagnanam I, Hirani SP, Martin DS, Levett DZ, Thornton JS, Golay X, Strycharczuk L, Newman SP, Montgomery HE, Grocott MP, Imray CH; Caudwell Xtreme Everest Research Group. Cerebral artery dilatation maintains cerebral oxygenation at extreme altitude and in acute hypoxia-an ultrasound and MRI study. J Cereb Blood Flow Metab. 2011;31:2019-2029. doi: 10.1038/jcbfm.2011.81.
41. Rogers SC, Khalatbari A, Datta BN, Ellery S, Paul V, Frenneaux MP, James PE. NO metabolite flux across the human coronary circulation. Cardiovasc Res. 2007;75:434-441. doi: 10.1016/j. cardiores.2007.04.019.
42. Marley R, Feelisch M, Holt S, Moore K. A chemiluminescensebased assay for S-nitrosoalbumin and other plasma S-nitrosothiols. Free Radic Res. 2000;32:1-9.