Temperature-dependent release of ATP from human erythrocytes: Mechanism for the control of local tissue perfusion

Experimental Physiology

Volumn 97, Issue 3, 2012, Pages 419-432

  Kalsi, Kameljit K ^a   González Alonso, José ^a  

^a BRUNEL UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANION; GLIBENCLAMIDE; MEMBRANE PROTEIN; NIFLUMIC ACID; NUCLEOSIDE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ADULT; ANION EXCHANGE; ARTERIAL BLOOD; ARTICLE; BATH; BLOOD; BLOOD SAMPLING; BODY TEMPERATURE; CONTROLLED STUDY; ENZYME RELEASE; ERYTHROCYTE; EXERCISE; FEMORAL VEIN; HEATING; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; HYPOTHESIS; IN VITRO STUDY; IN VIVO STUDY; LEG MUSCLE; MALE; NORMAL HUMAN; NUCLEOSIDE TRANSPORT; PLASMA; REST; ROOM TEMPERATURE; SERUM; TEMPERATURE DEPENDENCE; TISSUE PERFUSION; VASODILATATION;

EID: 84857643722     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2011.064238     Document Type: Article

References (57)

1. Abraham EH, Prat AG, Gerweck L, Seneveratne T, Arceci RJ, Kramer R, Guidotti G & Cantiello HF (1993). The multidrug resistance (mdr1) gene product functions as an ATP channel. Proc Natl Acad Sci U S A 90, 312-316.
2. Akyurekli D, Gerig LH & Raaphorst GP (1997). Changes in muscle blood flow distribution during hyperthermia. Int J Hyperthermia 13, 481-496.
3. Baar S (1967). Osmotic resistance of heat-damaged erythrocytes. J Clin Pathol 20, 239-243.
4. Barcroft J & King WO (1909). The effect of temperature on the dissociation curve of blood. J Physiol 39, 374-384.
5. Bazett HC & McGlone B (1927). Temperature gradients in the tissues in man. Am J Physiol 82, 415-451.
6. Bergfeld GR & Forrester T (1992). Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia. Cardiovasc Res 26, 40-47.
7. Black MA, Green DJ & Cable NT (2008). Exercise prevents age-related decline in nitric-oxide-mediated vasodilator function in cutaneous microvessels. J Physiol 586, 3511-3524.
8. Cheng J, Cebotaru V, Cebotaru L & Guggino WB (2010). Syntaxin 6 and CAL mediate the degradation of the cystic fibrosis transmembrane conductance regulator. Mol Biol Cell 21, 1178-1187.
9. Coade SB & Pearson JD (1989). Metabolism of adenine nucleotides in human blood. Circ Res 65, 531-537.
10. Cripps CM (1968). Rapid method for the estimation of plasma haemoglobin levels. J Clin Pathol 21, 110-112.
11. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE & Welsh MJ (1992). Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358, 761-764.
12. Deussen A, Moser G & Schrader J (1986). Contribution of coronary endothelial cells to cardiac adenosine production. Pflugers Arch 406, 608-614.
13. Dill DB & Costill DL (1974). Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol 37, 247-248.
14. Duc G & Engel K (1969). A method for determination of oxyhemoglobin dissociation curves at constant temperature, pH, and PCO2. Respir Physiol 8, 118-126.
15. Dufour SP, Patel RP, Brandon A, Teng X, Pearson J, Barker H, Ali L, Yuen AH, Smolenski RT & González-Alonso J (2010). 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.
16. Ellsworth ML, Forrester T, Ellis CG & Dietrich HH (1995). The erythrocyte as a regulator of vascular tone. Am J Physiol Heart Circ Physiol 269, H2155-H2161.
17. Feliciano L & Henning RJ (1999). Coronary artery blood flow: physiologic and pathophysiologic regulation. Clin Cardiol 22, 775-786.
18. Fischer DJ, Torrence NJ, Sprung RJ & Spence DM (2003). Determination of erythrocyte deformability and its correlation to cellular ATP release using microbore tubing with diameters that approximate resistance vessels in vivo. Analyst 128, 1163-1168.
19. González-Alonso J, Calbet JA & Nielsen B (1999a). Metabolic and thermodynamic responses to dehydration-induced reductions in muscle blood flow in exercising humans. J Physiol 520, 577-589.
20. González-Alonso J, Olsen DB & Saltin B (2002). Erythrocyte and the regulation of human skeletal muscle blood flow and oxygen delivery: role of circulating ATP. Circ Res 91, 1046-1055.
21. González-Alonso J, Teller C, Andersen SL, Jensen FB, Hyldig T & Nielsen B (1999b). Influence of body temperature on the development of fatigue during prolonged exercise in the heat. J Appl Physiol 86, 1032-1039.
22. Gordon JL (1986). Extracellular ATP: effects, sources and fate. Biochem J 233, 309-319.
23. Gorman MW, Feigl EO & Buffington CW (2007). Human plasma ATP concentration. Clin Chem 53, 318-325.
24. Gorman MW, Marble DR, Ogimoto K & Feigl EO (2003). Measurement of adenine nucleotides in plasma. Luminescence 18, 173-181.
25. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K & Kasparov S (2010). Astrocytes control breathing through pH-dependent release of ATP. Science 329, 571-575.
26. Green DJ, Carter HH, Fitzsimons MG, Cable NT, Thijssen DH & Naylor LH (2010). Obligatory role of hyperaemia and shear stress in microvascular adaptation to repeated heating in humans. J Physiol 588, 1571-1577.
27. He Q, Zhu L, Lemons DE & Weinbaum S (2002). Experimental measurements of the temperature variation along artery-vein pairs from 200 to 1000 microns diameter in rat hind limb. J Biomech Eng 124, 656-661.
28. Keller DM, Sander M, Stallknecht B & Crandall CG (2010). α-Adrenergic vasoconstrictor responsiveness is preserved in the heated human leg. J Physiol 588, 3799-3808.
29. Kirby BS, Crecelius AR, Voyles WF & Dinenno FA (2010). Vasodilatory responsiveness to adenosine triphosphate in ageing humans. J Physiol 588, 4017-4027.
30. Kirby BS, Voyles WF, Carlson RE & Dinenno FA (2008). Graded sympatholytic effect of exogenous ATP on postjunctional α-adrenergic vasoconstriction in the human forearm: implications for vascular control in contracting muscle. J Physiol 586, 4305-4316.
31. Llaudet E, Hatz S, Droniou M & Dale N (2005). Microelectrode biosensor for real-time measurement of ATP in biological tissue. Anal Chem 77, 3267-3273.
32. Locovei S, Bao L & Dahl G (2006). Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci U S A 103, 7655-7659.
33. Malinauskas RA (1997). Plasma hemoglobin measurement techniques for the in vitro evaluation of blood damage caused by medical devices. Artif Organs 21, 1255-1267.
34. Mortensen SP, González-Alonso J, Bune LT, Saltin B, Pilegaard H & Hellsten Y (2009a). ATP-induced vasodilation and purinergic receptors in the human leg: roles of nitric oxide, prostaglandins, and adenosine. Am J Physiol Regul Integr Comp Physiol 296, R1140-R1148.
35. Mortensen SP, González-Alonso J, Nielsen JJ, Saltin B & Hellsten Y (2009b). Muscle interstitial ATP and norepinephrine concentrations in the human leg during exercise and ATP infusion. J Appl Physiol 107, 1757-1762.
36. Mortensen SP, Thaning P, Nyberg M, Saltin B & Hellsten Y (2011). 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.
37. Niimi Y, Matsukawa T, Sugiyama Y, Shamsuzzaman AS, Ito H, Sobue G & Mano T (1997). Effect of heat stress on muscle sympathetic nerve activity in humans. J Auton Nerv Syst 63, 61-67.
38. i is involved in a signal transduction pathway for ATP release from erythrocytes. Am J Physiol Heart Circ Physiol 286, H940-H945.
39. Pearson J, Low DA, Stohr E, Kalsi K, Ali L, Barker H & González-Alonso J (2011). Hemodynamic responses to heat stress in the resting and exercising human leg: insight into the effect of temperature on skeletal muscle blood flow. Am J Physiol Regul Integr Comp Physiol 300, R663-R673.
40. Ray CA & Gracey KH (1997). Augmentation of exercise-induced muscle sympathetic nerve activity during muscle heating. J Appl Physiol 82, 1719-1725.
41. Rosenmeier JB, Hansen J & González-Alonso J (2004). Circulating ATP-induced vasodilatation overrides sympathetic vasoconstrictor activity in human skeletal muscle. J Physiol 558, 351-365.
42. Rowell LB (1974). Human cardiovascular adjustments to exercise and thermal stress. Physiol Rev 54, 75-159.
43. Ruiter MS, van Golde JM, Schaper NC, Stehouwer CD & Huijberts MS (2010). Diabetes impairs arteriogenesis in the peripheral circulation: review of molecular mechanisms. Clin Sci (Lond) 119, 225-238.
44. Saltin B, Gagge AP, Bergh U & Stolwijk JA (1972). Body temperatures and sweating during exhaustive exercise. J Appl Physiol 32, 635-643.
45. Schrage WG, Eisenach JH & Joyner MJ (2007). Ageing reduces nitric-oxide- and prostaglandin-mediated vasodilatation in exercising humans. J Physiol 579, 227-236.
46. - channel by niflumic acid. Mol Membr Biol 21, 27-38.
47. - channels expressed in a murine cell line. J Physiol 503, 333-346.
48. Sprague RS, Ellsworth ML, Stephenson AH, Kleinhenz ME & Lonigro AJ (1998). Deformation-induced ATP release from red blood cells requires CFTR activity. Am J Physiol Heart Circ Physiol 275, H1726-H1732.
49. Sprague RS, Ellsworth ML, Stephenson AH & Lonigro AJ (1996). ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am J Physiol Heart Circ Physiol 271, H2717-H2722.
50. Sridharan M, Adderley SP, Bowles EA, Egan TM, Stephenson AH, Ellsworth ML & Sprague RS (2010). Pannexin 1 is the conduit for low oxygen tension-induced ATP release from human erythrocytes. Am J Physiol Heart Circ Physiol 299, H1146-H1152.
51. Sterling KM Jr, Shah S, Kim RJ, Johnston NI, Salikhova AY & Abraham EH (2004). Cystic fibrosis transmembrane conductance regulator in human and mouse red blood cell membranes and its interaction with ecto-apyrase. J Cell Biochem 91, 1174-1182.
52. Tu J, Le G & Ballard HJ (2010). Involvement of the cystic fibrosis transmembrane conductance regulator in the acidosis-induced efflux of ATP from rat skeletal muscle. J Physiol 588, 4563-4578.
53. Williamson JR, Shanahan MO & Hochmuth RM (1975). The influence of temperature on red cell deformability. Blood 46, 611-624.
54. Yegutkin GG, Samburski SS & Jalkanen S (2003). Soluble purine-converting enzymes circulate in human blood and regulate extracellular ATP level via counteracting pyrophosphatase and phosphotransfer reactions. FASEB J 17, 1328-1330.
55. Yegutkin GG, Samburski SS, Mortensen SP, Jalkanen S & González-Alonso J (2007). Intravascular ADP and soluble nucleotidases contribute to acute prothrombotic state during vigorous exercise in humans. J Physiol 579, 553-564.
56. Zimmermann H (2006a). Ectonucleotidases in the nervous system. Novartis Found Symp 276, 113-128; discussion 128-130, 233-237, 275-281.
57. Zimmermann H (2006b). Nucleotide signaling in nervous system development. Pflugers Arch 452, 573-588.