Correlation of cardiac performance with cellular energetic components in the oxygen-deprived turtle heart

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 3, 2009, Pages

  Stecyk, Jonathan A W ^a,d,e   Bock, Christian ^b   Overgaard, Johannes ^c   Wang, Tobias ^c   Farrell, Anthony P ^a   Pörtner, Hans O ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^c AARHUS UNIVERSITY   (Denmark)

^d UNIVERSITY OF ALBERTA   (Canada)

^e UNIVERSITY OF OSLO   (Norway)

Author keywords

Anoxic turtle cardiac performance; High energy phosphate metabolism; In vivo magnetic resonance spectroscopy

Indexed keywords

ADENOSINE TRIPHOSPHATE; CREATINE PHOSPHATE; PHOSPHATE;

ANIMAL EXPERIMENT; ANOXIA; ARTICLE; CELL ENERGY; CELL PH; CORRELATION ANALYSIS; FEEDBACK SYSTEM; HEART PERFORMANCE; HIGH ENERGY PHOSPHATE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHATE METABOLISM; PRIORITY JOURNAL; TURTLE;

ADAPTATION, PHYSIOLOGICAL; ADENOSINE TRIPHOSPHATE; ANIMALS; ANOXIA; AORTA; AUTONOMIC NERVOUS SYSTEM; ENERGY METABOLISM; HEART; HEART RATE; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MYOCARDIAL CONTRACTION; MYOCARDIUM; PHOSPHATES; PHOSPHOCREATINE; PULMONARY CIRCULATION; REGIONAL BLOOD FLOW; TEMPERATURE; TIME FACTORS; TURTLES;

EID: 69249151742     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00102.2009     Document Type: Article

References (84)

1. Allen DG, Orchard CH. Myocardial contractile function during ischemia and hypoxia. Circ Res 60: 153-168, 1987.
2. Arai AE, Pantely GA, Thoma WJ, Anselone CG, Bristow JD. Energy metabolism and contractile function after 15 beats of moderate myocardial ischemia. Circ Res 70: 1137-1145, 1992.
3. Askenasy N. Sensitivity of mechanical and metabolic functions to changes in coronary perfusion: A metabolic basis of perfusion-contraction coupling. J Mol Cell Cardiol 32: 791-803, 2000.
4. Bailey JR, Driedzic WR. Decreased total ventricular and mitochondrial protein synthesis during extended anoxia in the heart. Am J Physiol Regul Integr Comp Physiol 271: R1660-R1667, 1996.
5. Beamish FWH. Respiration of fishes with special emphasis on standard oxygen consumption. III. Influence of oxygen. Can J Zool 42: 355-366, 1964.
6. Beard DA. Modeling of oxygen transport and cellular energetics explains observations on in vivo cardiac energy metabolism. PLoS Compt Biol 2: e107, 2006.
7. 31P-NMR surface coil studies in living rat. Circ Res 60: 871-878, 1987.
8. Bock C, Frederich M, Wittig RM, Pörtner HO. Simultaneous observations of haemolymph flow and ventilation in marine spider crabs at different temperatures: a flow weighted MRI study. Magn Reson Imaging 19: 1113-1124, 2001.
9. Bock C, Sartoris FJ, Wittig RM, Pörtner HO. Temperature dependent pH regulation in stenothermal Antarctic and eurythermal temperate eelpout (Zoarcidae): an in vivo NMR study. Polar Biol 24: 869-874, 2001.
10. Bock C, Sartoris FJ, Pörtner HO. In vivo MR spectroscopy and MR imaging on non-anaesthetized marine fish: techniques and first results. Magn Reson Imaging 20: 165-172, 2002.
11. Boutilier RG. Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 204: 3171-3181, 2001.
12. Chen F, Clarke K, Vaughan-Jones R, Noble D. Modeling of internal pH, ion concentration, and bioenergetic changes during myocardial ischemia. Adv Exp Med Biol 430: 281-290, 1997.
13. Cheng H, Smith GL, Orchard CH, Hancox JC. Acidosis inhibits spontaneous activity and membrane currents in myocytes isolated from the rabbit atrioventricular node. J Mol Cell Cardiol 46:75-85, 2009.
14. Clarke K, O'Connor AJ, Willis RJ. Temporal relation between energy metabolism and myocardial function during ischemia and reperfusion. Am J Physiol Heart Circ Physiol 253: H412-H421, 1987.
15. Eisner DA, Elliott AC, Smith GL. The contribution of intracellular acidosis to the decline of developed pressure in ferret hearts exposed to cyanide. J Physiol 391: 99-108, 1987.
16. Elliott AC, Smith GL, Eisner DA, Allen DG. Metabolic changes during ischaemia and their role in contractile failure in isolated ferret hearts. J Physiol 454: 467-490, 1992.
17. Farrell AP, Stecyk JAW. The heart as a working model to explore themes and strategies for anoxic survival in ectothermic vertebrates. Comp Biochem Physiol A 147: 300-312, 2007.
18. Farrell AP, Franklin CE, Arthur PG, Thorarensen H, Cousins KL. Mechanical performance of an in situ perfused heart from the turtle Chrysemys scripta during normoxia and anoxia at 5°C and 15°C. J Exp Biol 191: 207-229, 1994.
19. Galli GLJ, Gesser H, Taylor EW, Shiels HA, Wang T. The role of the sarcoplasmic reticulum in the generation of high heart rates and blood pressures in reptiles. J Exp Biol 209: 1956-1963, 2006.
20. Galli GLJ, Taylor EW, Shiels HA. Calcium flux in turtle ventricular myocytes. Am J Physiol Regul Integr Comp Physiol 291: R1781-R1789, 2006.
21. i, contractility and Ca-balance under hypercapnic adicosis in the myocardium of different vertebrate species. J Exp Biol 96: 405-412, 1982.
22. Godt RE, Nosek TM. Changes of intracellular milieu with fatigue or hypoxia depress contraction of skinned rabbit skeletal and cardiac muscle. J Physiol 412: 155-180, 1989.
23. +-perfusion. J Mol Cell Cardiol 20: 1189-1201, 1988.
24. Hartmund T, Gesser H. Cardiac force and high-energy phosphates under metabolic inhibition in four ectothermic vertebrates. Am J Physiol Regul Integr Comp Physiol 271: R946-R954, 1996.
25. Hasse A. Snapshot FLASH MRI: Applications to T1, T2, and chemical-shift imaging. Magn Reson Med 13: 77-89, 1990.
26. He MX, Wang S, Downey HF. Correlation between myocardial contractile force and cytosolic inorganic phosphate during early ischemia. Am J Physiol Heart Circ Physiol 272: H1333-H1341, 1997.
27. Hearse DJ. Oxygen deprivation and early myocardial contractile failure: a reassessment of the possible role of adenosine triphosphate. Am J Cardiol 44: 1115-1121, 1979.
28. Herbert CV, Jackson DC. Temperature effects on the responses to prolonged submergence in the turtle Chrysemys picta bellii. II. Metabolic rate, blood acid-base and ionic changes and cardiovascular function in aerated and anoxic water. Physiol Zool 58: 670-681, 1985.
29. Hicks JMT, Farrell AP. The cardiovascular responses of the red-eared slider (Trachemys scripta) acclimated to either 22 or 5°C. I. Effects of anoxia exposure on in vivo cardiac performance. J Exp Biol 203: 3765-3774, 2000.
30. Hicks JMT, Farrell AP. The cardiovascular responses of the red-eared slider (Trachemys scripta) acclimated to either 22 or 5°C. II Effects of anoxia on adrenergic and cholinergic control. J Exp Biol 203: 3775-3784, 2000.
31. Hicks JW, Wang T. Cardiovascular regulation during anoxia in the turtle: An in vivo study. Physiol Zool 71: 1-14, 1998.
32. Hochachka PW, Buck LT, Doll CJ, Land SC. Unifying theory of hypoxia tolerance: Molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93: 9493-9498, 1996.
33. Ingwall JS, Weiss RG. Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ Res 95: 135-145, 2004.
34. Jackson DC. Metabolic depression and oxygen depletion in the diving turtle. J Appl Physiol 24: 503-509, 1968.
35. Jackson DC. Cardiovascular function in turtles during anoxia and acidosis: In vivo and in vitro studies. Am Zool 27: 49-56, 1987.
36. Jackson DC. Living without oxygen: lessons from the freshwater turtle. Comp Biochem Physiol A 125: 299-315, 2000.
37. 31P-NMR study. Am J Physiol Regul Integr Comp Physiol 268: R683-R689, 1995.
38. 31P-NMR study. J Comp Physiol [B] 165: 77-84, 1995.
39. Jensen MA, Gesser H. Influence of inorganic phosphate and energy state on force in skinned cardiac muscle from freshwater turtle and rainbow trout. J Comp Physiol [B] 169: 439-444, 1999.
40. Kammermeier H. High-energy phosphate of the myocardium: Concentration versus free energy change. Basic Res Cardiol 82 Suppl 2: 31-36, 1987.
41. Kammermeier H, Schmidt P, Jüngling E. Free energy change of ATP-hydrolysis: A casual factor of early hypoxic failure of the myocardium? J Mol Cell Cardiol 14: 267-277, 1982.
42. Kentish JC, Allen DG. Is force production in the myocardium directly dependent upon the free energy change of ATP hydrolysis? J Mol Cell Cardiol 18: 879-882, 1986.
43. Keiver KM, Weinberg J, Hochachka PW. Roles of catecholamines and corticosterone during anoxia and recovery at 5°C in turtles. Am J Physiol Regul Integr Comp Physiol 263: R770-R774, 1992.
44. Koretsune Y, Corretti MC, Kusuoka H, Marban E. Mechanism of early ischemic contractile failure. Inexcitability, metabolite accumulation, or vascular collapse. Circ Res 68: 255-262, 1991.
45. Krogh A. The progress of physiology. Am J Physiol 90: 243, 1929.
46. Kübler W, Katz AM. Mechanism of early "pump" failure of the ischemic heart: Possible role of adenosine triphosphate depletion and inorganic phosphate accumulation. Am J Cardiol 40: 467-471, 1977.
47. Lannig G, Bock C, Sartoris FJ, Pörtner HO. Oxygen limitation of thermal tolerance in cod, Gadus morhua L., studied by magnetic resonance imaging and on-line venous oxygen monitoring. Am J Physiol Regul Integr Comp Physiol 287: R902-R910, 2004.
48. eq of the creatine kinase reaction and other phosphate hydrolyses and phosphate transfer reactions. J Biol Chem 254: 6528-6537, 1979.
49. Matthews PW, Taylor DG, Radda GK. Biochemical mechanisms of acute contractile failure in the hypoxic rat heart. Cardiovasc Res 20: 13-19, 1986.
50. Miller DD, Salinas F, Walsh RA. Simultaneous cardiac mechanics and phosphorus-31 NMR spectroscopy during global myocardial ischemia and reperfusion in the intact dog. Magn Reson Med 17: 41-52, 1991.
51. Nilsson GE, Lutz PL. Anoxia tolerant brains. J Cereb Blood Flow Metab 24: 475-486, 2004.
52. Orchard CH, Kentish JC. Effects of changes of pH on the contractile function of cardiac muscle. Am J Physiol Cell Physiol 258: C967-C981, 1990.
53. Overgaard J, Gesser H. Force development, energy state and ATP production of cardiac muscle from turtles and trout during normoxia and severe hypoxia. J Exp Biol 207: 1915-1924, 2004.
54. Overgaard J, Wang T, Nielsen OB, Gesser H. Extracellular determinants of cardiac contractility in the cold anoxic turtle. Physiol Biochem Zool 78: 976-995, 2005.
55. Overgaard J, Gesser H, Wang T. Tribute to P. L. Lutz: cardiac performance and cardiovascular regulation during anoxia/hypoxia in freshwater turtles. J Exp Biol 210: 1687-1699, 2007.
56. Palmer S, Kentish JC. The role of troponin C in modulating the Ca sensitivity of mammalian skinned cardiac and skeletal muscle fibres. J Physiol 480: 45-60, 1994.
57. 2. Physiol Zool 64: 836-849, 1991.
58. Pörtner HO, Finke E, Lee PG. Metabolic and energy correlates of intracellular pH in progressive fatigue of squid (L. brevis) mantle muscle. Am J Physiol Regul Integr Comp Physiol 271: R1403-R1414, 1996.
59. Reeves RB. Energy cost of work in aerobic and anaerobic turtle heart muscle. Am J Physiol 205: 17-22, 1963.
60. Satoh H, Hashimoto K. Effect of pH on the sino-atrial node cells and atrial muscle of dog. Arch Int Pharmacodyn Ther 261: 67-78, 1983.
61. Satoh H, Seyama I. On the mechanism by which changes in extracellular pH affect the electrical activity of the rabbit sino-atrial node. J Physiol 381: 181-191, 1986.
62. Saupe KW, Eberli FR, Ingwall JS, Apstein CS. Hypoperfusion-induced contractile failure does not require changes in cardiac energetics. Am J Physiol Heart Circ Physiol 276: H1715-H1723, 1999.
63. Schwartz GG, Schaefer S, Meyerhoff DJ, Gober J, Fochler P, Massie B, Weiner MW. Dynamic relation between myocardial contractility and energy metabolism during and following brief coronary occlusion in the pig. Circ Res 67: 490-500, 1990.
64. Shi H, Jackson DC. Effects of anoxia, acidosis and temperature on the contractile properties of turtle cardiac muscle strips. J Exp Biol 200: 1965-1973, 1997.
65. Shi H, Hamm PH, Lawler RG, Jackson DC. Different effects of simple anoxic lactic acidosis and simulated in vivo anoxic acidosis on turtle heart. Comp Biochem Physiol A 122: 173-180, 1999.
66. Stecyk JAW, Farrell AP. Effects of extracellular changes on spontaneous heart rate of normoxia- and anoxia-acclimated turtles (Trachemys scripta). J Exp Biol 210: 421-431, 2007.
67. Stecyk JAW, Overgaard J, Farrell AP, Wang T. α-Adrenergic regulation of systemic peripheral resistance and blood flow distribution in the turtle (Trachemys scripta) during anoxic submergence at 5°C and 21°C. J Exp Biol 207: 269-283, 2004.
68. Stecyk JAW, Stensløkken KO, Farrell AP, Nilsson GE. Maintained cardiac pumping in anoxic crucian carp. Science 306: 77, 2004.
69. Stecyk JAW, Stensløkken KO, Nilsson GE, Farrell AP. Adenosinergic cardiovascular control in anoxia-tolerant vertebrates during prolonged oxygen deprivation. Comp Biochem Physiol A 147: 961-973, 2007.
70. Stecyk JAW, Paajanen V, Farrell AP, Vornanen M. Effect of temperature and prolonged anoxia exposure on electrophysiological properties of the turtle (Trachemys scripta) heart. Am J Physiol Regul Integr Comp Physiol 293: R421-R437, 2007.
71. Stecyk JAW, Galli GL, Shiels HA, Farrell AP. Cardiac survival in anoxia-tolerant vertebrates: An electrophysiological perspective. Comp Biochem Physiol C 148: 339-354, 2008.
72. Storey KB. Metabolic adaptations supporting anoxia tolerance in reptiles: Recent advances. Comp Biochem Physiol B 113: 23-35, 1996.
73. Ultsch GR. The ecology of overwintering among turtles: where turtles overwinter and its consequences. Biol Rev Camb Philos Soc 81: 339-367, 2006.
74. Vornanen M, Shiels HA, Farrell AP. Plasticity of excitation-contraction coupling in fish cardiac myocytes. Comp Biochem Physiol A 132: 827-846, 2002.
75. Wasser JS, Freund EV, Gonzalez LA, Jackson DC. Force and acid-base state of turtle cardiac tissue exposed to combined anoxia and acidosis. Am J Physiol Regul Integr Comp Physiol 259: R15-R20, 1990.
76. i and high-energy phosphates in isolated turtle hearts during anoxia and acidosis. Am J Physiol Regul Integr Comp Physiol 259: R521-R530, 1990.
77. Wasser JS, Meinertz EA, Chang SY, Lawler RG, Jackson DC. Metabolic and cardiodynamic responses of isolated turtle hearts to ischemia and reperfusion. Am J Physiol Regul Integr Comp Physiol 262: R437-R443, 1992.
78. 31P-NMR determinations of cytostolic phosphodiesters in turtle hearts. Comp Biochem Physiol A 118: 1193-1200, 1997.
79. Wasser JS, Guthrie SS, Chari M. In vitro tolerance to anoxia and ischemia in isolated hearts from hypoxia sensitive and hypoxia tolerant turtles. Comp Biochem Physiol A 118: 1359-1370, 1997.
80. 31P-NMR. Biochim Biophys Acta 720: 281-287, 1982.
81. Wu F, Zhang EY, Zhang J, Bache DA, Beard RJ. Phosphate metabolite concentrations and ATP hydrolysis potential in normal and ischemic hearts. J Physiol 586: 4193-4208, 2008.
82. Vaughn-Jones RD, Spitzer KW, Swietach P. Intracellular pH regulation in heart. J Mol Cell Cardiol 46: 318-331, 2009.
83. Yee HP, Jackson DC. The effects of different types of acidosis and extracellular calcium on the mechanical activity of turtle atria. J Comp Physiol [B] 154: 385-391, 1984.
84. Zhou L, Yu X, Cabrera ME, Stanley WC. Role of cellular compartmentation in the metabolic response to stress: mechanistic insights from computational models. Ann N Y Acad Sci 1080: 120-139, 2006.