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Am J Physiol Regul Integr Comp Physiol 297: R756-R768, 2009. First published July 8, 2009; doi:10.1152/ajpregu.00102.2009
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ARTICLES

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

Jonathan A. W. Stecyk,1 Christian Bock,2 Johannes Overgaard,3 Tobias Wang,3 Anthony P. Farrell,4 and Hans-O. Pörtner2

1Department of Zoology, University of British Columbia, Vancouver, BC, Canada; 2Integrative Ecophysiology, Alfred-Wegener-Institute for Marine and Polar Research, Bremerhaven, Germany; 3Zoophysiology, Department of Biological Sciences, University of Aarhus, Aarhus, Denmark; and 4Department of Zoology and Faculty of Food and Land Systems, University of British Columbia, Vancouver, BC, Canada

Submitted 13 February 2009 ; accepted in final form 6 July 2009

The relationship between cardiac energy metabolism and the depression of myocardial performance during oxygen deprivation has remained enigmatic. Here, we combine in vivo 31P-NMR spectroscopy and MRI to provide the first temporal profile of in vivo cardiac energetics and cardiac performance of an anoxia-tolerant vertebrate, the freshwater turtle (Trachemys scripta) during long-term anoxia exposure (~3 h at 21°C and 11 days at 5°C). During anoxia, phosphocreatine (PCr), unbound levels of inorganic phosphate (effective Pi2–), intracellular pH (pHi), and free energy of ATP hydrolysis (dG/d{xi}) exhibited asymptotic patterns of change, indicating that turtle myocardial high-energy phosphate metabolism and energetic state are reset to new, reduced steady states during long-term anoxia exposure. At 21°C, anoxia caused a reduction in pHi from 7.40 to 7.01, a 69% decrease in PCr and a doubling of effective Pi2–. ATP content remained unchanged, but the free energy of ATP hydrolysis (dG/d{xi}) decreased from –59.6 to –52.5 kJ/mol. Even so, none of these cellular changes correlated with the anoxic depression of cardiac performance, suggesting that autonomic cardiac regulation may override putative cellular feedback mechanisms. In contrast, during anoxia at 5°C, when autonomic cardiac control is severely blunted, the decrease of pHi from 7.66 to 7.12, 1.9-fold increase of effective Pi2–, and 6.4 kJ/mol decrease of dG/d{xi} from –53.8 to –47.4 kJ/mol were significantly correlated to the anoxic depression of cardiac performance. Our results provide the first evidence for a close, long-term coordination of functional cardiac changes with cellular energy status in a vertebrate, with a potential for autonomic control to override these immediate relationships.

high-energy phosphate metabolism; anoxic turtle cardiac performance; in vivo magnetic resonance spectroscopy



Address for reprint requests and other correspondence: J. A. W. Stecyk, Dept. of Physiology, Rm. 473-HMRC, University of Alberta, Edmonton, Alberta, Canada (e-mail: jstecyk{at}ualberta.ca)







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