Mechanical effects of muscle contraction increase intravascular ATP draining quiescent and active skeletal muscle in humans

Journal of Applied Physiology

Volumn 114, Issue 8, 2013, Pages 1085-1093

  Crecelius, Anne R ^a   Kirby, Brett S ^a   Richards, Jennifer C ^a   Dinenno, Frank A ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Adenosine triphosphate; Blood flow; Exercise; Muscle compression; Vasodilation

Indexed keywords

ADENOSINE TRIPHOSPHATE;

ADULT; ARTICLE; BIOMECHANICS; BLOOD; BLOOD FLOW; BLOOD FLOW VELOCITY; BLOOD GAS ANALYSIS; DOPPLER FLOWMETRY; ECHOGRAPHY; FEMALE; FOREARM; HAND STRENGTH; HEMODYNAMICS; HUMAN; MALE; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; SKELETAL MUSCLE; TIME; UPREGULATION; VASCULARIZATION; VEIN;

ADENOSINE TRIPHOSPHATE; BIOMECHANICS; BLOOD FLOW VELOCITY; BLOOD GAS ANALYSIS; FEMALE; FOREARM; HAND STRENGTH; HEMODYNAMICS; HUMANS; MALE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; REGIONAL BLOOD FLOW; TIME FACTORS; ULTRASONOGRAPHY, DOPPLER; UP-REGULATION; VEINS; YOUNG ADULT;

EID: 84878589657     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01465.2012     Document Type: Article

References (46)

1. Bergfeld GR, Forrester T. Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia. Cardiovasc Res 26:40-47, 1992.
2. Bodin P, Bailey D, Burnstock G. Increased flow-induced ATP release from isolated vascular endothelial cells but not smooth muscle cells. Br J Pharmacol 103:1203-1205, 1991.
3. Bodin P, Burnstock G. Synergistic effect of acute hypoxia on flowinduced release of ATP from cultured endothelial cells. Experientia 51:256-259, 1995.
4. Crecelius AR, Kirby BS, Richards JC, Garcia LJ, Voyles WF, Larson DG, Luckasen GJ, Dinenno FA. Mechanisms of ATP-mediated vasodilation in humans: modest role for nitric oxide and vasodilating prostaglandins. Am J Physiol Heart Circ Physiol 301:H1302-H1310, 2011.
5. Crecelius AR, Kirby BS, Voyles WF, Dinenno FA. Augmented skeletal muscle hyperaemia during hypoxic exercise in humans is blunted by combined inhibition of nitric oxide and vasodilating prostaglandins. J Physiol 589:3671-3683, 2011.
6. Crecelius AR, Kirby BS, Voyles WF, Dinenno FA. Nitric oxide, but not vasodilating prostaglandins, contributes to the improvement of exercise hyperemia via ascorbic acid in healthy older adults. Am J Physiol Heart Circ Physiol 299:H1633-H1641, 2010.
7. Dufour SP, Patel RP, Brandon A, Teng X, Pearson J, Barker H, Ali L, Yuen AH, Smolenski RT, Gonzalez-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 299:H1936-H1946, 2010.
8. Edwards J, Sprung R, Sprague R, Spence D. Chemiluminescence detection of ATP release from red blood cells upon passage through microbore tubing. Analyst 126:1257-1260, 2001. (Pubitemid 32747740)
9. Ellsworth ML, Forrester T, Ellis CG, Dietrich HH. The erythrocyte as a regulator of vascular tone. Am J Physiol Heart Circ Physiol 269:H2155-H2161, 1995. (Pubitemid 26023234)
10. Faris A, Spence DM. Measuring the simultaneous effects of hypoxia and deformation on ATP release from erythrocytes. Analyst 133:678-682, 2008. (Pubitemid 351575915)
11. Forrester T. A quantitative estimation of adenosine triphosphate released from human forearm muscle during sustained exercise. J Physiol 221:25P-26P, 1972.
12. Forrester T, Lind AR. Adenosine triphosphate in the venous effluent and its relationship to exercise. Fed Proc 28:1280-1283, 1969.
13. Forrester T, Lind AR. Identification of adenosine triphosphate in human plasma and the concentration in the venous effluent of forearm muscles before, during and after sustained contractions. J Physiol 204:347-364, 1969.
14. Giannarelli C, Virdis A, De Negri F, Magagna A, Duranti E, Salvetti A, Taddei S. Effect of sulfaphenazole on tissue plasminogen activator release in normotensive subjects and hypertensive patients. Circulation 119:1625-1633, 2009.
15. Gonzalez-Alonso J, Mortensen SP, Dawson EA, Secher NH, Damsgaard R. Erythrocytes and the regulation of human skeletal muscle blood flow and oxygen delivery: role of erythrocyte count and oxygenation state of haemoglobin. J Physiol 572:295-305, 2006.
16. Gonzalez-Alonso J, Olsen DB, Saltin B. Erythrocyte and the regulation of human skeletal muscle blood flow and oxygen delivery: role of circulating ATP. Circ Res 91:1046-1055, 2002. (Pubitemid 35416642)
17. Gonzalez-Alonso J, Richardson RS, Saltin B. Exercising skeletal muscle blood flow in humans responds to reduction in arterial oxyhaemoglobin, but not to altered free oxygen. J Physiol 530:331-341, 2001. (Pubitemid 32998881)
18. Gorman MW, Feigl EO, Buffington CW. Human plasma ATP concentration. Clin Chem 53:318-325, 2007. (Pubitemid 46338277)
19. Gorman MW, Marble DR, Ogimoto K, Feigl EO. Measurement of adenine nucleotides in plasma. Luminescence 18:173-181, 2003. (Pubitemid 40326831)
20. Gray SD, Carlsson E, Staub NC. Site of increased vascular resistance during isometric muscle contraction. Am J Physiol 213:683-689, 1967.
21. Heinonen I, Kemppainen J, Kaskinoro K, Peltonen JE, Borra R, Lindroos MM, Oikonen V, Nuutila P, Knuuti J, Hellsten Y, Boushel R, Kalliokoski KK. Comparison of exogenous adenosine and voluntary exercise on human skeletal muscle perfusion and perfusion heterogeneity. J Appl Physiol 108:378-386, 2010.
22. Holmgren A, Linderholm H. Oxygen and carbon dioxide tensions of arterial blood during heavy and exhaustive exercise. Acta Physiol Scand 44:203-215, 1958.
23. Jagger JE, Bateman RM, Ellsworth ML, Ellis CG. Role of erythrocyte in regulating local O2 delivery mediated by hemoglobin oxygenation. Am J Physiol Heart Circ Physiol 280:H2833-H2839, 2001.
24. Joyner MJ, Wilkins BW. Exercise hyperaemia: is anything obligatory but the hyperaemia? J Physiol 583:855-860, 2007. (Pubitemid 47423704)
25. Kirby BS, Carlson RE, Markwald RR, Voyles WF, Dinenno FA. Mechanical influences on skeletal muscle vascular tone in humans: insight into contraction-induced rapid vasodilatation. J Physiol 583:861-874, 2007. (Pubitemid 47423705)
26. Kirby BS, Crecelius AR, Richards JC, Dinenno FA. Sources of intravascular ATP during exercise in humans: critical role for skeletal muscle perfusion Exp Physiol. In press. (DOI: 10.1113/expphysiol.2012.071555).
27. Kirby BS, Crecelius AR, Voyles WF, Dinenno FA. Impaired skeletal muscle blood flow control with advancing age in humans: attenuated ATP release and local vasodilation during erythrocyte deoxygenation. Circ Res 111:220-230, 2012.
28. Kirby BS, Markwald RR, Smith EG, Dinenno FA. Mechanical effects of muscle contraction do not blunt sympathetic vasoconstriction in humans. Am J Physiol Heart Circ Physiol 289:H1610-H1617, 2005. (Pubitemid 41369004)
29. Kirby BS, Voyles WF, Carlson RE, Dinenno FA. Graded sympatholytic effect of exogenous ATP on postjunctional alpha-adrenergic vasoconstriction in the human forearm: implications for vascular control in contracting muscle. J Physiol 586:4305-4316, 2008.
30. Mo FM, Ballard HJ. The effect of systemic hypoxia on interstitial and blood adenosine, AMP, ADP and ATP in dog skeletal muscle. J Physiol 536:593-603, 2001. (Pubitemid 32976138)
31. Mortensen SP, Gonzalez-Alonso J, Damsgaard R, Saltin B, Hellsten Y. Inhibition of nitric oxide and prostaglandins, but not endothelialderived hyperpolarizing factors, reduces blood flow and aerobic energy turnover in the exercising human leg. J Physiol 581:853-861, 2007. (Pubitemid 46831777)
32. Mortensen SP, Gonzalez-Alonso J, Nielsen JJ, Saltin B, Hellsten Y. Muscle interstitial ATP and norepinephrine concentrations in the human leg during exercise and ATP infusion. J Appl Physiol 107:1757-1762, 2009.
33. Mortensen SP, Thaning P, Nyberg M, Saltin B, Hellsten Y. Local release of ATP into the arterial inflow and venous drainage of human skeletal muscle: insight from ATP determination with the intravascular microdialysis technique. J Physiol 589:1847-1857, 2011.
34. Pretorius M, Rosenbaum D, Vaughan DE, Brown NJ. Angiotensinconverting enzyme inhibition increases human vascular tissue-type plasminogen activator release through endogenous bradykinin. Circulation 107:579-585, 2003. (Pubitemid 36176808)
35. Richards JC, Crecelius AR, Kirby BS, Larson DG, Dinenno FA. Muscle contraction duration and fibre recruitment influence blood flow and VO2 independent of contractile work during steady-state exercise in humans. Exp Physiol 97:750-761, 2012.
36. Rosenmeier JB, Hansen J, Gonzalez-Alonso J. Circulating ATP-induced vasodilatation overrides sympathetic vasoconstrictor activity in human skeletal muscle. J Physiol 558:351-365, 2004. (Pubitemid 39077414)
37. Rosenmeier JB, Yegutkin GG, Gonzalez-Alonso J. Activation of ATP/UTP-selective receptors increases blood flow and blunts sympathetic vasoconstriction in human skeletal muscle. J Physiol 586:4993-5002, 2008.
38. Sadamoto T, Bonde-Petersen F, Suzuki Y. Skeletal muscle tension, flow, pressure, and EMG during sustained isometric contractions in humans. Eur J Appl Physiol Occup Physiol 51:395-408, 1983. (Pubitemid 13005076)
39. Sprague RS, Ellsworth ML, Stephenson AH, Kleinhenz ME, Lonigro AJ. Deformation-induced ATP release from red blood cells requires CFTR activity. Am J Physiol Heart Circ Physiol 275:H1726-H1732, 1998.
40. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ. ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am J Physiol Heart Circ Physiol 271:H2717-H2722, 1996.
41. Sprung R, Sprague R, Spence D. Determination of ATP release from erythrocytes using microbore tubing as a model of resistance vessels in vivo. Anal Chem 74:2274-2278, 2002. (Pubitemid 34526032)
42. Sridharan M, Sprague RS, Adderley SP, Bowles EA, Ellsworth ML, Stephenson AH. Diamide decreases deformability of rabbit erythrocytes and attenuates low oxygen tension-induced ATP release. Exp Biol Med (Maywood) 235:1142-1148, 2010.
43. Tschakovsky ME, Shoemaker JK, Hughson RL. Vasodilation and muscle pump contribution to immediate exercise hyperemia. Am J Physiol Heart Circ Physiol 271:H1697-H1701, 1996.
44. Wan J, Ristenpart WD, Stone HA. Dynamics of shear-induced ATP release from red blood cells. Proc Natl Acad Sci USA 105:16432-16437, 2008.
45. Wood RE, Wishart C, Walker PJ, Askew CD, Stewart IB. Plasma ATP concentration and venous oxygen content in the forearm during dynamic handgrip exercise. BMC Physiol 9:24, 2009.
46. Yegutkin GG, Samburski SS, Mortensen SP, Jalkanen S, Gonzalez-Alonso J. Intravascular ADP and soluble nucleotidases contribute to acute prothrombotic state during vigorous exercise in humans. J Physiol 579:553-564, 2007. (Pubitemid 46351769)