Reversal of permeability transition during recovery of hearts from ischemia and its enhancement by pyruvate

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 276, Issue 2 45-2, 1999, Pages

  Kerr, Paul M ^a   Suleiman, M Saadeh ^a   Halestrap, Andrew P ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Apoptosis; Deoxyglucose; PH(i); Rat; Reperfusion injury

Indexed keywords

DEOXYGLUCOSE; FREE RADICAL; LACTIC ACID; PYRUVIC ACID;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; HEART LEFT VENTRICLE PRESSURE; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; HEART PERFUSION; HEART PROTECTION; MALE; NONHUMAN; PERMEABILITY; PH; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; TISSUE INJURY;

EID: 0032988868     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.1999.276.2.h496     Document Type: Article

References (41)

1. 2+ overload. Am. J. Physiol. 270 (Heart Circ. Physiol. 39): H2149-H2156, 1996.
2. Bernardi, P. Modulation of the mitochondrial cyclosporin-A-sensitive permeability transition pore by the proton electrochemical gradient - evidence that the pore can be opened by membrane depolarization. J. Biol. Chem. 267: 8834-8839, 1992.
3. Bernardi, P., S. Vassanelli, P. Veronese, R. Colonna, I. Szabo, and M. Zoratti. Modulation of the mitochondrial permeability transition pore - effect of protons and divalent cations. J. Biol. Chem. 267: 2934-2939, 1992.
4. 2+ homeostasis in the pH paradox of reperfusion injury to neonatal rat cardiac myocytes. Am. J. Physiol. 265 (Cell Physiol. 34): C129-C137, 1993.
5. Borle, A. B., and R. T. Stanko. Pyruvate reduces anoxic injury and free radical formation in perfused rat hepatocytes. Am. J. Physiol. 270 (Gastrointest. Liver Physiol. 33): G535-G540, 1996.
6. Bunger, R., R. T. Mallet, and D. A. Hartman. Pyruvate-enhanced phosphorylation potential and inotropism in normoxic and post-ischemic isolated working heart. Eur. J. Biochem. 180: 221-233, 1989.
7. Cavallini, L., M. Valente, and M. P. Rigobello. The protective action of pyruvate on recovery of ischemic rat heart - comparison with other oxidizable substrates. J. Mol. Cell. Cardiol. 22: 143-154, 1990.
8. Constantopoulos, G., and J. A. Barranger. Nonenzymatic decarboxylation of pyruvate. Anal. Biochem. 139: 353-358, 1984.
9. 2+ in the function and dysfunction of heart mitochondria. In: Calcium and the Heart, edited by G. A. Langer. New York: Raven, 1990, p. 167-198.
10. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem. J. 255: 357-360, 1988.
11. Cross, H. R., K. Clarke, L. H. Opie, and G. K. Radda. Is lactate-induced myocardial ischaemic injury mediated by decreased pH or increased intracellular lactate? J. Mol. Cell. Cardiol. 27: 1369-1381, 1995.
12. Deboer, L. W. V., P. A. Bekx, L. H. Han, and L. Steinke. Pyruvate enhances recovery of rat hearts after ischemia and reperfusion by preventing free radical generation. Am. J. Physiol. 265 (Heart Circ. Physiol. 34): H1571-H1576, 1993.
13. Fliss, H., and D. Gattinger. Apoptosis in ischemic and reperfused rat myocardium. Circ. Res. 79: 949-956, 1996.
14. Gottlieb, R. A., K. O. Burleson, R. A. Kloner, B. M. Babior, and R. L. Engler. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J. Clin. Invest. 94: 1621-1628, 1994.
15. Griffiths, E. J., and A. P. Halestrap. Protection by cyclosporin A of ischemia reperfusion-induced damage in isolated rat hearts. J. Mol. Cell. Cardiol. 25: 1461-1469, 1993.
16. Griffiths, E. J., and A. P. Halestrap. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem. J. 307: 93-98, 1995.
17. Halestrap, A. P. Calcium-dependent opening of a non-specific pore in the mitochondrial inner membrane is inhibited at pH values below 7 - implications for the protective effect of low pH against chemical and hypoxic cell damage. Biochem. J. 278: 715-719, 1991.
18. Halestrap, A. P. The nature of the stimulation of the respiratory chain of rat liver mitochondria by glucagon pretreatment of animals. Biochem. J. 204: 37-47, 1982.
19. Halestrap, A. P. Interactions between oxidative stress and calcium overload on mitochondrial function. In: Mitochondria: DNA, Proteins and Disease, edited by V. Darley-Usmar and A. H. V. Schapira. London: Portland, 1994, p. 113-142.
20. Halestrap, A. P., C. P. Connern, E. J. Griffiths, and P. M. Kerr. Cyclosporin A binding to mitochondrial cyclophilin inhibits the permeability transition pore and protects hearts from ischaemia/reperfusion injury. Mol. Cell. Biochem. 174: 167-172, 1997.
21. 2+-induced large amplitude swelling of liver and heart mitochondria by cyclosporin A is probably caused by the inhibitor binding to mitochondrial matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem. J. 268: 153-160, 1990.
22. Halestrap, A. P., X. Wang, R. C. Poole, V. N. Jackson, and N. T. Price. Lactate transport in heart in relation to ischemia. Am. J. Cardiol. 80: 17A-25A, 1997.
23. Halestrap, A. P., K. Y. Woodfield, and C. P. Connern. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J. Biol. Chem. 272: 3346-3354, 1997.
24. Harada, K. A., R. G. Franklin, W. Johnson, W. Grossman, and J. P. Morgan. Acidemia and hypernatremia enhance post-ischemic recovery of exitation-contraction coupling. Circ. Res. 74: 1197-1209, 1994.
25. 2+ trigger site. Arch. Biochem. Biophys. 195: 460-467, 1979.
26. Hirsch, T., I. Marzo, and G. Kroemer. Role of the mitochondrial permeability transition pore in apoptosis. Biosci. Rep. 17: 67-76, 1997.
27. Kantrow, S. P., and C. A. Piantadosi. Release of cytochrome c from liver mitochondria during permeability transition. Biochem. Biophys. Res. Commun. 232: 669-671, 1997.
28. Kitakaze, M., S. Takashima, H. Funaya, T. Minamino, K. Node, Y. Shinozaki, H. Mori, and M. Hori. Temporary acidosis during reperfusion limits myocardial infarct size in dogs. Am. J. Physiol. 272 (Heart Circ. Physiol. 41): H2071-H2078, 1997.
29. Kluck, R. M., E. Bossy-Wetzel, D. R. Green, and D. D. Newmeyer. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136, 1997.
30. Kluck, R. M., S. J. Martin, B. M. Hoffman, J. S. Zhou, D. R. Green, and D. D. Newmeyer. Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO J. 16: 4639-4649, 1997.
31. Nazareth, W., N. Yafei, and M. Crompton. Inhibition of anoxia-induced injury in heart myocytes by cyclosporin-A. J. Mol. Cell. Cardiol. 23: 1351-1354, 1991.
32. Neely, J. R., R. M. Denton, P. J. England, and P. J. Randle. The effects of increased heart work on the tricarboxylate cycle and its interaction with glycolysis in the perfused rat heart. Biochem. J. 128: 147-159, 1972.
33. Olivetti, G., F. Quaini, R. Sala, C. Lagrasta, D. Corradi, E. Bonacina, S. R. Gambert, E. Cigola, and P. Anversa. Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. J. Mol. Cell. Cardiol. 28: 2005-2016, 1996.
34. Poole, R. C., and A. P. Halestrap. Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am. J. Physiol. 264 (Cell Physiol. 33): C761-C782, 1993.
35. Reimer, K. A., and R. B. Jennings. Myocardial ischemia, hypoxia and infarction. In: The Heart and Cardiovascular System (2nd ed.), edited by H. A. Fozzard, R. B. Jennings, E. Huber, A. M. Katz, and H. E. Morgan. New York: Raven, 1992, p. 1875-1973.
36. Susin, S. A., N. Zamzami, M. Castedo, E. Daugas, H. G. Wang, S. Geley, F. Fassy, J. C. Reed, and G. Kroemer. The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Pas/APO-1/CD95- and ceramide-induced apoptosis. J. Exp. Med. 186: 25-37, 1997.
37. Umansky, S. R., and L. D. Tomei. Apoptosis in the heart. Adv. Pharmacol. 41: 383-407, 1997.
38. Van Bilsen M., G. J. van der Vusse, L. H. E. H. Snoeckx, T. Arts, W. A. Coumans, P. H. M. Willemsen, and R. S. Reneham. Effects of pyruvate on post-ischemic myocardial recovery at various workloads. Pflügers Arch. 413: 167-173, 1988.
39. Vandenberg, J. I., J. C. Metcalfe, and A. A. Grace. Mechanisms of intracellular pH recovery following global ischaemia in the perfused heart. Circ. Res. 72: 993-1003, 1993.
40. Yang, J., X. S. Liu, K. Bhalla, C. N. Kim, A. M. Ibrado, J. Y. Cai, T. I. Peng, D. P. Jones, and X. D. Wang. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129-1132, 1997.
41. Zoratti, M., and I. Szabo. The mitochondrial permeability transition. Biochim. Biophys. Acta 1241: 139-176, 1995.