Impaired skeletal muscle blood flow control with advancing age in humans: Attenuated ATP release and local vasodilation during erythrocyte deoxygenation

Circulation Research

Volumn 111, Issue 2, 2012, Pages 220-230

  Kirby, Brett S ^a   Crecelius, Anne R ^a   Voyles, Wyatt F ^b,c   Dinenno, Frank A ^a  

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

^b Poudre Valley Health System   (United States)

^c UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

aging; ATP; blood flow; erythrocytes; hypoxia

Indexed keywords

ADENOSINE TRIPHOSPHATE; OXYHEMOGLOBIN;

ADULT; AGE DISTRIBUTION; AGING; ARTICLE; CARDIOVASCULAR DISEASE; CELL ISOLATION; CLINICAL ARTICLE; CONTROLLED STUDY; DEOXYGENATION; DISEASE ASSOCIATION; ERYTHROCYTE FUNCTION AND CHARACTERISTICS; EXERCISE; FOREARM BLOOD FLOW; HAND GRIP; HEART RATE; HUMAN; HYDROLYSIS; HYPOXIA; MEAN ARTERIAL PRESSURE; MUSCLE BLOOD FLOW; PRIORITY JOURNAL; PROTEIN SECRETION; VASODILATATION;

ADENOSINE TRIPHOSPHATE; AGED; AGING; BLOOD FLOW VELOCITY; ERYTHROCYTES; FEMALE; FOREARM; HUMANS; MALE; MIDDLE AGED; MUSCLE, SKELETAL; OXIMETRY; OXYGEN CONSUMPTION; VASODILATION; YOUNG ADULT;

EID: 84863723701     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.112.269571     Document Type: Article

References (39)

1. 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. 2001;530:331-341. (Pubitemid 32998881)
2. 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. 2002;91:1046-1055. (Pubitemid 35416642)
3. 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. 2001;280:H2833-H2839.
4. Crawford JH, Isbell TS, Huang Z, Shiva S, Chacko BK, Schechter AN, Darley-Usmar VM, Kerby JD, Lang JD Jr, Kraus D, Ho C, Gladwin MT, Patel RP. Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood. 2006;107:566-574. (Pubitemid 43076380)
5. Diesen DL, Hess DT, Stamler JS. Hypoxic vasodilation by red blood cells: evidence for an S-nitrosothiol-based signal. Circ Res. 2008;103: 545-553.
6. Wang L, Olivecrona G, Gotberg M, Olsson ML, Winzell MS, Erlinge D. ADP acting on P2Y13 receptors is a negative feedback pathway for ATP release from human red blood cells. Circ Res. 2005;96:189-196. (Pubitemid 40209366)
7. Ellsworth ML, Ellis CG, Goldman D, Stephenson AH, Dietrich HH, Sprague RS. Erythrocytes: oxygen sensors and modulators of vascular tone. Physiology (Bethesda). 2009;24:107-116.
8. Rosenmeier JB, Hansen J, Gonzalez-Alonso J. Circulating ATP-induced vasodilatation overrides sympathetic vasoconstrictor activity in human skeletal muscle. J Physiol. 2004;558:351-365. (Pubitemid 39077414)
9. 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. 2008;586:4305-4316.
10. Taylor JA, Hand GA, Johnson DG, Seals DR. Augmented forearm vasoconstriction during dynamic exercise in healthy older men. Circulation. 1992;86:1789-1799.
11. Davy KP, Jones PP, Seals DR. Influence of age on the sympathetic neural adjustments to alterations in systemic oxygen levels in humans. Am J Physiol Regul Integr Comp Physiol. 1997;273:R690-R695.
12. Luscher TF, Tanner FC, Tschudi MR, Noll G. Endothelial dysfunction in coronary artery disease. Annu Rev Med. 1993;44:395-418. (Pubitemid 23117878)
13. Fleg JL, Morrell CH, Bos AG, Brant LJ, Talbot LA, Wright JG, Lakatta EG. Accelerated longitudinal decline of aerobic capacity in healthy older adults. Circulation. 2005;112:674-682. (Pubitemid 41099046)
14. 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. 2011;589:3671-3683.
15. 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. 2007; 579:553-564. (Pubitemid 46351769)
16. Duarte MM, Loro VL, Rocha JB, Leal DB, Bem AF, Dorneles A, Morsch VM, Schetinger MR. Enzymes that hydrolyze adenine nucleotides of patients with hypercholesterolemia and inflammatory processes. FEBS J. 2007;274:2707-2714. (Pubitemid 46800541)
17. Coade SB, Pearson JD. Metabolism of adenine nucleotides in human blood. Circ Res. 1989;65:531-537. (Pubitemid 19226429)
18. Sprague RS, Bowles EA, Achilleus D, Stephenson AH, Ellis CG, Ellsworth ML. A selective phosphodiesterase 3 inhibitor rescues low PO2-induced ATP release from erythrocytes of humans with type 2 diabetes: implication for vascular control [published correction appears in Am J Physiol Heart Circ Physiol. 2012;302:H378]. Am J Physiol Heart Circ Physiol. 2011;301:H2466-H2472.
19. Sridharan M, Adderley SP, Bowles EA, Egan TM, Stephenson AH, Ellsworth ML, Sprague RS. Pannexin 1 is the conduit for low oxygen tension-induced ATP release from human erythrocytes. Am J Physiol Heart Circ Physiol. 2010;299:H1146-H1152.
20. 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. 2009;119:1625-1633.
21. Kohler D, Eckle T, Faigle M, Grenz A, Mittelbronn M, Laucher S, Hart ML, Robson SC, Muller CE, Eltzschig HK. CD39/ectonucleoside triphosphate diphosphohydrolase 1 provides myocardial protection during cardiac ischemia/reperfusion injury. Circulation. 2007;116:1784-1794. (Pubitemid 350287103)
22. Kirby BS, Voyles WF, Simpson CB, Carlson RE, Schrage WG, Dinenno FA. Endothelium-dependent vasodilatation and exercise hyperaemia in ageing humans: impact of acute ascorbic acid administration. J Physiol. 2009;587:1989-2003.
23. Kirby BS, Crecelius AR, Voyles WF, Dinenno FA. Modulation of postjunctional-adrenergic vasoconstriction during exercise and exogenous ATP infusions in ageing humans. J Physiol. 2011;589: 2641-2653.
24. Kirby BS, Crecelius AR, Voyles WF, Dinenno FA. Vasodilatory responsiveness to adenosine triphosphate in ageing humans. J Physiol. 2010; 588:4017-4027.
25. Poole JG, Lawrenson L, Kim J, Brown C, Richardson RS. Vascular and metabolic response to cycle exercise in sedentary humans: effect of age. Am J Physiol Heart Circ Physiol. 2003;284:H1251-H1259. (Pubitemid 36348588)
26. 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). 2010;235:1142-1148.
27. Gelmini G, Coiro V, Ferretti P, Baroni MC, Delsignore R. Evaluation of whole blood filterability with increasing age in healthy men and women. Haematologica. 1989;74:15-18. (Pubitemid 19088877)
28. 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. 2011;589:1847-1857.
29. Edwards J, Sprung R, Sprague R, Spence D. Chemiluminescence detection of ATP release from red blood cells upon passage through microbore tubing. Analyst. 2001;126:1257-1260. (Pubitemid 32747740)
30. Pries AR, Secomb TW, Gaehtgens P, Gross JF. Blood flow in microvascular networks: experiments and simulation. Circ Res. 1990;67: 826-834. (Pubitemid 20315014)
31. 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. 2002;543:691-698. (Pubitemid 35012220)
32. Wan J, Ristenpart WD, Stone HA. Dynamics of shear-induced ATP release from red blood cells. Proc Natl Acad Sci USA. 2008;105: 16432-16437.
33. 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. 2009;107:1757-1762.
34. Skinner MR, Marshall JM. Studies on the roles of ATP, adenosine and nitric oxide in mediating muscle vasodilatation induced in the rat by acute systemic hypoxia. J Physiol. 1996;495(part 2):553-560. (Pubitemid 26331835)
35. Sprague RS, Goldman D, Bowles EA, Achilleus D, Stephenson AH, Ellis CG, Ellsworth ML. Divergent effects of low-O2 tension and iloprost on ATP release from erythrocytes of humans with type 2 diabetes: implications for O2 supply to skeletal muscle. Am J Physiol Heart Circ Physiol. 2010;299:H566-H573.
36. Zhu H, Zennadi R, Xu BX, Eu JP, Torok JA, Telen MJ, McMahon TJ. Impaired adenosine-5-triphosphate release from red blood cells promotes their adhesion to endothelial cells: a mechanism of hypoxemia after transfusion. Crit Care Med. 2011;39:2478-2486.
37. Erlinge D, Burnstock G. P2 receptors in cardiovascular regulation and disease. Purinergic Signal. 2008;4:1-20.
38. 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. 2010;299:H1936-H1946.
39. Clifford PS, Hellsten Y. Vasodilatory mechanisms in contracting skeletal muscle. J Appl Physiol. 2004;97:393-403. (Pubitemid 38802543)