ATP-induced vasodilation and purinergic receptors in the human leg: Roles of nitric oxide, prostaglandins, and adenosine

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 296, Issue 4, 2009, Pages

  Mortensen, Stefan P ^a   González Alonso, José ^b   Bune, Laurids T ^a   Saltin, Bengt ^a   Pilegaard, Henriette ^a,c   Hellsten, Ylva ^a,c  

^a International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

^b BRUNEL UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Adenosine 5 triphosphate; Nitric oxide; Prostaglandins; Purinergic receptors; Skeletal muscle

Indexed keywords

ADENOSINE; ADENOSINE RECEPTOR BLOCKING AGENT; ADENOSINE TRIPHOSPHATE; INDOMETACIN; N(G) METHYLARGININE; NITRIC OXIDE; OXYGEN; PROSTAGLANDIN; PURINERGIC P2 RECEPTOR; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC RECEPTOR; THEOPHYLLINE;

ARTICLE; CONDUCTANCE; CONTROLLED STUDY; ENDOTHELIUM; HEART OUTPUT; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; HYPEREMIA; IMMUNOHISTOCHEMISTRY; LEG BLOOD FLOW; MALE; MICROVASCULATURE; MUSCLE BLOOD FLOW; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SARCOLEMMA; SKELETAL MUSCLE; SMOOTH MUSCLE FIBER; VASODILATATION; VASTUS LATERALIS MUSCLE;

ADENOSINE; ADENOSINE TRIPHOSPHATE; ADULT; BLOOD FLOW VELOCITY; CYCLOOXYGENASE INHIBITORS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; HUMANS; INDOMETHACIN; INFUSIONS, INTRA-ARTERIAL; LOWER EXTREMITY; MALE; MUSCLE, SKELETAL; MUSCLE, SMOOTH, VASCULAR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OMEGA-N-METHYLARGININE; PROSTAGLANDINS; RECEPTORS, PURINERGIC P1; RECEPTORS, PURINERGIC P2; REGIONAL BLOOD FLOW; RNA, MESSENGER; SIGNAL TRANSDUCTION; THEOPHYLLINE; VASODILATION; YOUNG ADULT;

EID: 65949095846     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90822.2008     Document Type: Article

References (52)

1. Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58: 281-341, 2006. (Pubitemid 44394905)
2. Andersen P, Saltin B. Maximal perfusion of skeletal muscle in man. J Physiol 366: 233-249, 1985. (Pubitemid 16245480)
3. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35: 609-616, 1975.
4. Boushel R, Langberg H, Gemmer C, Olesen J, Crameri R, Scheede C, Sander M, Kjaer M. Combined inhibition of nitric oxide and prostaglandins reduces human skeletal muscle blood flow during exercise. J Physiol 543: 691-698, 2002.
5. Burnstock G. Release of vasoactive substances from endothelial cells by shear stress and purinergic mechanosensory transduction. J Anat 194: 335-342, 1999. (Pubitemid 29241485)
6. Burnstock G. Purine and pyrimidine receptors. Cell Mol Life Sci 64: 1471-1483, 2007. (Pubitemid 46954150)
7. Busse R, Edwards G, Feletou M, Fleming I, Vanhoutte PM, Weston AH. EDHF: bringing the concepts together. Trends Pharmacol Sci 23: 374-380, 2002.
8. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987. (Pubitemid 17064313)
9. Clifford PS, Hellsten Y. Vasodilatory mechanisms in contracting skeletal muscle. J Appl Physiol 97: 393-403, 2004. (Pubitemid 38802543)
10. Collins DM, McCullough WT, Ellsworth ML. Conducted vascular responses: communication across the capillary bed. Microvasc Res 56: 43-53, 1998.
11. Dietrich HH, Ellsworth ML, Sprague RS, Dacey RG Jr. Red blood cell regulation of microvascular tone through adenosine triphosphate. Am J Physiol Heart Circ Physiol 278: H1294-H1298, 2000.
12. Duza T, Sarelius IH. Conducted dilations initiated by purines in arterioles are endothelium dependent and require endothelial Ca2+. Am J Physiol Heart Circ Physiol 285: H26-H37, 2003. (Pubitemid 36736411)
13. 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)
14. Frandsen U, Bangsbo J, Sander M, Hoffner L, Betak A, Saltin B, Hellsten Y. Exercise-induced hyperaemia and leg oxygen uptake are not altered during effective inhibition of nitric oxide synthase with N(G)-nitro- L-arginine methyl ester in humans. J Physiol 531: 257-264, 2001. (Pubitemid 32178042)
15. González-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. González-Alonso J, Mortensen SP, Jeppesen TD, Ali L, Barker H, Damsgaard R, Secher NH, Dawson EA, Dufour SP. Haemodynamic responses to exercise, ATP infusion and thigh compression in humans: insight into the role of muscle mechanisms on cardiovascular function. J Physiol 586: 2405-2417, 2008.
17. González-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)
18. González-Alonso J, Quistorff B, Krustrup P, Bangsbo J, Saltin B. Heat production in human skeletal muscle at the onset of intense dynamic exercise. J Physiol 524: 603-615, 2000. (Pubitemid 30229522)
19. Gordon JL. Extracellular ATP: effects, sources and fate. Biochem J 233: 309-319, 1986.
20. Hammer LW, Ligon AL, Hester RL. ATP-mediated release of arachidonic acid metabolites from venular endothelium causes arteriolar dilation. Am J Physiol Heart Circ Physiol 280: H2616-H2622, 2001.
21. Harrington LS, Evans RJ, Wray J, Norling L, Swales KE, Vial C, Ali F, Carrier MJ, Mitchell JA. Purinergic 2X1 receptors mediate endothelial dependent vasodilation to ATP. Mol Pharmacol 72: 1132-1136, 2007. (Pubitemid 350012587)
22. Kardos A, Taylor DJ, Thompson C, Styles P, Hands L, Collin J, Casadei B. Sympathetic denervation of the upper limb improves forearm exercise performance and skeletal muscle bioenergetics. Circulation 101: 2716-2720, 2000. (Pubitemid 30390575)
23. 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.
24. Lundby C, Nordsborg N, Kusuhara K, Kristensen KM, Neufer PD, Pilegaard H. Gene expression in human skeletal muscle: alternative normalization method and effect of repeated biopsies. Eur J Appl Physiol 95: 351-360, 2005. (Pubitemid 43055098)
25. Lynge J, Hellsten Y. Distribution of adenosine A1, A2A and A2B receptors in human skeletal muscle. Acta Physiol Scand 169: 283-290, 2000.
26. Mathieson JJ, Burnstock G. Purine-mediated relaxation and constriction of isolated rabbit mesenteric artery are not endothelium-dependent. Eur J Pharmacol 118: 221-229, 1985. (Pubitemid 16179846)
27. McCullough WT, Collins DM, Ellsworth ML. Arteriolar responses to extracellular ATP in striated muscle. Am J Physiol Heart Circ Physiol 272: H1886-H1891, 1997.
28. McMillan MR, Burnstock G, Haworth SG. Vasodilatation of intrapulmonary arteries to P2-receptor nucleotides in normal and pulmonary hypertensive newborn piglets. Br J Pharmacol 128: 543-548, 1999. (Pubitemid 29504741)
29. 2 during high-intensity whole-body exercise in humans. J Physiol 586: 2621-2635, 2008.
30. Mortensen SP, González-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)
31. Nelson MT, Quayle JM. Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol Cell Physiol 268: C799-C822, 1995.
32. Newcomer SC, Leuenberger UA, Hogeman CS, Handly BD, Proctor DN. Different vasodilator responses of human arms and legs. J Physiol 556: 1001-1011, 2004.
33. Pilegaard H, Ordway GA, Saltin B, Neufer PD. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279: E806-E814, 2000.
34. Pilegaard H, Saltin B, Neufer PD. Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol 546: 851-858, 2003. (Pubitemid 36204518)
35. Radegran G. Ultrasound Doppler estimates of femoral artery blood flow during dynamic knee extensor exercise in humans. J Appl Physiol 83: 1383-1388, 1997. (Pubitemid 27433108)
36. Radegran G, Saltin B. Muscle blood flow at onset of dynamic exercise in humans. Am J Physiol Heart Circ Physiol 274: H314-H322, 1998. (Pubitemid 28092597)
37. Radegran G, Saltin B. Nitric oxide in the regulation of vasomotor tone in human skeletal muscle. Am J Physiol Heart Circ Physiol 276: H1951-H1960, 1999. (Pubitemid 29323479)
38. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev 50: 413-492, 1998. (Pubitemid 28477681)
39. Rongen GA, Smits P, Thien T. Characterization of ATP-induced vasodilation in the human forearm vascular bed. Circulation 90: 1891-1898, 1994. (Pubitemid 24320940)
40. Rosenmeier JB, Hansen J, González-Alonso J. Circulating ATP-induced vasodilatation overrides sympathetic vasoconstrictor activity in human skeletal muscle. J Physiol 558: 351-365, 2004. (Pubitemid 39077414)
41. Rosenmeier JB, Yegutkin GG, Gonzalez-Alonso J. Activation of ATP/ UTP selective receptors increase blood flow and blunt sympathetic vasoconstriction in human skeletal muscle. J Physiol 586: 4993-5002, 2008.
42. Rowell LB, Saltin B, Kiens B, Christensen NJ. Is peak quadriceps blood flow in humans even higher during exercise with hypoxemia? Am J Physiol Heart Circ Physiol 251: H1038-H1044, 1986. (Pubitemid 17187578)
43. Schrage WG, Joyner MJ, Dinenno FA. Local inhibition of nitric oxide and prostaglandins independently reduces forearm exercise hyperaemia in humans. J Physiol 557: 599-611, 2004.
44. Shiramoto M, Imaizumi T, Hirooka Y, Endo T, Namba T, Oyama J, Hironaga K, Takeshita A. Role of nitric oxide towards vasodilator effects of substance P and ATP in human forearm vessels. Clin Sci (Lond) 92: 123-131, 1997. (Pubitemid 27075713)
45. Shoemaker JK, Halliwill JR, Hughson RL, Joyner MJ. Contributions of acetylcholine and nitric oxide to forearm blood flow at exercise onset and recovery. Am J Physiol Heart Circ Physiol 273: H2388-H2395, 1997.
46. Smits P, Williams SB, Lipson DE, Banitt P, Rongen GA, Creager MA. Endothelial release of nitric oxide contributes to the vasodilator effect of adenosine in humans. Circulation 92: 2135-2141, 1995.
47. 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.
48. Strobaek D, Olesen SP, Christophersen P, Dissing S. P2- purinoceptormediated formation of inositol phosphates and intracellular Ca2+ transients in human coronary artery smooth muscle cells. Br J Pharmacol 118: 1645-1652, 1996. (Pubitemid 26252657)
49. Taddei S, Pedrinelli R, Salvetti A. Theophylline is an antagonist of adenosine in human forearm arterioles. Am J Hypertens 4: 256-259, 1991.
50. van Ginneken EE, Meijer P, Verkaik N, Smits P, Rongen GA. ATP-induced vasodilation in human skeletal muscle. Br J Pharmacol 141: 842-850, 2004. (Pubitemid 38446185)
51. Wang L, Karlsson L, Moses S, Hultgardh-Nilsson A, Andersson M, Borna C, Gudbjartsson T, Jern S, Erlinge D. P2 receptor expression profiles in human vascular smooth muscle and endothelial cells. J Cardiovasc Pharmacol 40: 841-853, 2002. (Pubitemid 35365082)
52. 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)