Advertisement

Calcium Fluxes and Reperfusion Damage: The Role of Mitochondria

  • D. Stone
  • V. Darley-Usmar
  • J. F. Martin
Chapter

Abstract

Myocardial ischaemia in the absence of reperfusion ultimately leads to cell necrosis and the development of infarction (Mergner and Schaper, 1982; Lucchesi and Mullane, 1986; Smith et al., 1988). While restoration of flow is clearly a prerequisite for tissue recovery, the process of reperfusion itself results in the development of metabolic and functional abnormalities that were not apparent during the ischaemic period and can be regarded as the response of the myocardium to reperfusion. This response encompasses a variety of phenomena, including reperfusion arrhythmias (Woodward and Zakaria, 1985; Manning et al., 1985; Sugiyama and Ozawa, 1987), myocardial stunning (Gross et al., 1986; Bolli et al., 1989), cell lysis (Shen and Jennings, 1972a,b) and an inflammatory component characterized by neutrophil infiltration (Mullane et al., 1984; Lucchesi and Mullane, 1986; Smith et al., 1988). One of the key responses that occur as part of this continuum is the acute cell damage that occurs at the point of reperfusion. A component of this damage has been shown to be dependent on the reintroduction of oxygen to the tissue and on this basis it is frequently referred to as the ‘oxygen paradox’. Perturbations of cell calcium homoeostasis have been implicated in most aspects of reperfusion damage (Shen and Jennings, 1972a,b; Mergner and Schaper, 1982; Sugiyama and Ozawa, 1987), but in this present chapter we shall concentrate on the oxygen paradox and examine the role that calcium plays in this phenomenon.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. Al-Nasser, I. and Crompton, M. (1986a). The reversible Ca2+-induced permeabilization of rat liver mitochondria. Biochem. J., 239, 19–29PubMedPubMedCentralCrossRefGoogle Scholar
  2. Al-Nasser, I. and Crompton, M. (1986b). The entrapment of the Ca2+ indicator arsenazo II in the matrix space of rat liver mitochondria by permeabilization and resealing. Biochem. J., 239, 31–40PubMedPubMedCentralCrossRefGoogle Scholar
  3. Altschuld, R., Hostetler, B., Brierley, G. P. (1981). Response of isolated rat heart cells to hypoxia re-oxygenation and acidosis. Circ. Res., 49, 307–316PubMedCrossRefGoogle Scholar
  4. Belli, R., Jeroudi, M. O., Patel, B. S., Aruoma, O. I., Halliwell, B., Lai, E. K. and McCay, P. B. (1989). Marked reduction of free radical generation and contractile dysfunction by antioxidant therapy begun at the time of reperfusion. Circ. Res., 65, 607–622CrossRefGoogle Scholar
  5. Bourdillon, P. D. and Poole-Wilson, A. (1982). The effects of verapamil, quiescence, and cardioplegia on calcium exchange and mechanical function in ischemic rabbit myocardium. Circ. Res., 50, 360–368PubMedCrossRefGoogle Scholar
  6. Crompton, M. (1985a). The regulation of mitochondrial calcium transport in heart. Curr. Topics Membr. Transpt, 25, 231–276CrossRefGoogle Scholar
  7. Crompton, M. (1985b). The calcium carriers of mitochondria. In Martonosi, A. (Ed.), Enzymes of Biological Membranes, Vol. 3, Plenum Press, New York, pp. 249–286CrossRefGoogle Scholar
  8. Crompton, M., Costi, A. and Hayat, L. (1987). Evidence for the presence of a reversible Ca2+-dependent pore activated by oxidative stress in heart mitochondria. Biochem. J., 245, 915–918PubMedPubMedCentralCrossRefGoogle Scholar
  9. Crompton, M., Ellinger, H. and Costi, A. (1988). Inhibition by cyclosporin A of a Ca2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem. J., 255, 357–360PubMedPubMedCentralGoogle Scholar
  10. Darley-Usmar, V. M., Smith, D. R., O’Leary, V. J., Stone, D., Hardy, D. L. and Clark, J. B. (1990). Hypoxia-reoxygenation induced damage in the myocardium: the role of mitochondria. Biochem. Soc. Trans., 18, 526PubMedCrossRefGoogle Scholar
  11. Darley-Usmar, V. M., Stone, D. and Smith, D. R. (1989). Oxygen and reperfusion damage: an overview. Free Rad. Res. Comms, 7, 247–254CrossRefGoogle Scholar
  12. De Jong, J. W., Harmsen, E. and De Tombe, P. P. (1984). Diltiazem administered before or during myocardial ischaemia decreases adenine nucleotide catabolism. J. Mol. Cell. Cardiol., 16, 363–370PubMedCrossRefGoogle Scholar
  13. Denton, R. M. and McCormack, J. G. (1985). Ca2+ transport by mammalian mitochondria and its role in hormone action. Am. J. Physiol., 249, E543–E554PubMedGoogle Scholar
  14. Fischer, G., Whittmann-Liebold, B., Lang, K., Kiefhaber, T. and Schmid, F. X. (1989). Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature, 337,476–478PubMedCrossRefGoogle Scholar
  15. Ganote, C. E. and Kaltenbach, J. P. (1979). Oxygen-induced enzyme release: early events and proposed mechanism. J. Mol. Cell. Cardiol., 11, 389–406PubMedCrossRefGoogle Scholar
  16. Ganote, C. E., Seabra-Goames, R., Nayler, W. G. and Jennings, R. B. (1975). Irreversible myocardial injury in anoxic perfused rat hearts. Am. J. Pathol., 80, 419–450PubMedPubMedCentralGoogle Scholar
  17. Ganote, C. E., Worstell, J. and Kaltenbach, J. P. (1976). Oxygen-induced enzyme release after irreversible myocardial injury. Am. J. Pathol., 84, 327–350PubMedPubMedCentralGoogle Scholar
  18. Gross, G. J., Farber, N. E., Hardman, H. F. and Warltier, D. C. (1986). Beneficial actions of superoxide dismutase and catalase in stunned myocardium of dogs. Am. J. Physiol., 250, H372–H377PubMedGoogle Scholar
  19. Grinwald, P. M. and Brosnahan, C. (1987). Sodium imbalance as a cause of calcium overload in post-hypoxic reoxygenation injury. J. Mol. Cell. Cardiol., 19, 487–495PubMedCrossRefGoogle Scholar
  20. Halestrap, A. P. and Davidsoh, A. M. (1990). Inhibition of calcium ion-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitory binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem. J., 268, 153–160PubMedPubMedCentralCrossRefGoogle Scholar
  21. Hansford, R. G. (1987). Relation between cytosolic free Ca2+ concentration and the control of pyruvate dehydrogenase in isolated cardiac myocytes. Biochem. J., 241, 145–151PubMedPubMedCentralCrossRefGoogle Scholar
  22. Harding, D. A. and Poole-Wilson, P. A. (1980). Calcium exchange in rabbit myocardium during and after hypoxia: effect of temperature and substrate. Cardiovasc. Res., 14, 435–445PubMedCrossRefGoogle Scholar
  23. Hardy, D. L., Clark, J. B., Darley-Usmar, V., Smith, D. R. and Stone, D. (1991). Reoxygenation dependent decrease in mitochondrial NADH CoO reductase [Complex I] activity in the hypoxic-reoxygenated rat heart. Biochem. J., 274, 133–137PubMedPubMedCentralCrossRefGoogle Scholar
  24. Harmsen, E., De Tombe, P. P. and De Jong, J. W. (1983). Synergistic effect of nifedipine and propranolol on adenosine (catabolite) release from ischaemic rat heart. Eur. J. Pharm., 90, 401–409CrossRefGoogle Scholar
  25. Haworth, R. A., Goknur, A. B., Hunter, D. R., Hegge, J. O. and Berkoff, H. A. (1987). Inhibition of calcium influx in isolated adult rat heart cells by ATP depletion. Circ. Res., 60, 586–594PubMedCrossRefGoogle Scholar
  26. Hearse, D. J. and Humphrey, S. M. (1975). Enzyme release during myocardial anoxia: a study of metabolic protection. J. Mot. Cell. Cardiol., 7, 463–482CrossRefGoogle Scholar
  27. Hearse, D. J., Humphrey, S. M. and Bullock, G. R. (1978). The oxygen paradox and the calcium paradox: two facets of the same problem? J. Mot. Cell. Cardiol., 10, 641–668CrossRefGoogle Scholar
  28. Ingebretsen, O. C. and Bakken, A. M. (1982). Determination of adenine nucleotides and inosine in human myocardium by ion-pair reversed-phase high-performance liquid chromatography. J. Chromatog., 242, 119–126CrossRefGoogle Scholar
  29. Kehrer, J. P., Park, Y. and Sies, H. (1988). Energy dependence of enzyme release from hypoxic isolated perfused rat heart tissue. Pfiiigers Arch., 61, 291–332Google Scholar
  30. Lazdunski, M., Frelin, C. and Vigne, P. (1985). The sodium/hydrogen exchange system in cardiac cells: its biochemical and pharmacological properties and its role in regulating internal concentrations of sodium and internal pH. J. Mot. Cell. Cardiol., 17, 1029–1042CrossRefGoogle Scholar
  31. Lucchesi, B. R. and Mullane, K. M. (1986). Leukocytes and ischemia-induced myocardial injury. Ann. Rev. Pharmacol. Toxicol., 26, 201–224CrossRefGoogle Scholar
  32. McCormack, J. G. and Denton, R. M. (1986). Ca2+ as a second messenger within mitochondria. Trends Biochem. Sci., 11, 258–262CrossRefGoogle Scholar
  33. Manning, A. S., Kinoshita, K., Buschmans, E., Coltart, D. J. and Hearse, D. J. (1985). The genesis of arrhythmias during myocardial ischemia. Circ. Res., 57, 668–675PubMedCrossRefGoogle Scholar
  34. Marban, E., Kitakaze, M., Koretsune, Y., Yue, D. T., Chacko, V. P. and Pike, M. M. (1990). Quantification of [Ca2+]; in perfused hearts. Circ. Res., 66, 1255–1267PubMedCrossRefGoogle Scholar
  35. Marban, E., Kitakaze, M., Kusuoka, H., Porterfield, J. K., Yue, D. T. and Chacko, V. P. (1987). Intracellular free calcium concentration measured with 19FNMR spectroscopy in intact ferret hearts. Proc. NatlAcad. Sci. USA, 84, 6005–6009CrossRefGoogle Scholar
  36. Mergner, W. J. and Schaper, J. (1982). Cellular and subcellular changes in myocardial infarction. In Cowley, R. A. and Trump, B. F. (Eds), Pathophysiology of Shock, Anoxia and Ischaemia. Williams and Wilkins, London, pp. 658–680Google Scholar
  37. Mullane, K. M., Read, N., Salmon, J. A. and Moncada, S. (1984). Role of leukocytes in acute myocardial infarction in anaesthetized dogs: relationship to myocardial salvage by anti-inflammatory drugs. J. Pharmacol. Exp. Ther., 228, 510–522PubMedGoogle Scholar
  38. Nagelkerke, J. F., Dogterom, P., De Bont, H. J. G. M. and Mulder, G. J. (1989). Prolonged high intracellular free calcium concentrations induced by ATP are not immediately cytotoxic in isolated rat hepatocytes. Biochem. J., 263, 347–353PubMedPubMedCentralCrossRefGoogle Scholar
  39. Nakanishi, T., Nishioka, K. and Jarmakani, J. M. (1982). Mechanism of tissue Ca2+ gain during reoxygenation after hypoxia in rabbit myocardium. Am. J. Physiol., 242, H437–H449PubMedGoogle Scholar
  40. Nayler, W. G. (1980). Cardioprotective effects of calcium ion antagonists in myocardial ischaemia. Clin. Invest. Med., 3, 91–99PubMedGoogle Scholar
  41. Nayler, W. G., Ferrari, R. and Williams, A. (1980). Protective effect of pretreatment with verapamil nifedipine and propranolol on itochondrial function in the ischaemic and reperfused myocardium. Am. J. Cardiol., 46, 242–249PubMedCrossRefGoogle Scholar
  42. Nayler, W. G., Sturrock, W. J. and Panagiotopoulos, S. (1985). Calcium and myocardial ischaemia. In Parratt, J. R. (Ed.), Control and Manipulation of Calcium Movement. Raven Press, New York, pp. 303–324Google Scholar
  43. Nicholls, D. G. and Crompton, M. (1980). Mitochondrial calcium transport. FEBS Lett., 111, 261–268PubMedCrossRefGoogle Scholar
  44. Parr, D. R., Wimhurst, J. M. and Harris, E. J. (1975). Calcium-induced damage of rat heart mitochondria. Cardiovasc. Res., 9, 366–372PubMedCrossRefGoogle Scholar
  45. Philipson, K. D., Bersohn, M. M. and Nishimoto, A. Y. (1982). Effects of pH on Na+-Ca2+ exchange in canine cardiac sarcolemmal vesicles. Circ. Res., 50, 287PubMedCrossRefGoogle Scholar
  46. Poole-Wilson, P. A. (1985). The nature of myocardial damage following reoxygenation. In Parratt, J. R. (Ed.), Control and Manipulation of Calcium Movement. Raven Press, New York, pp. 325–340Google Scholar
  47. Poole-Wilson, P. A. and Tones, M. A. (1988). Sodium exchange during hypoxia and on reoxygenation in the isolated rabbit heart. J. Mot. Cell. Cardiol., 20, 15–22CrossRefGoogle Scholar
  48. Reeves, J. P. (1984). Na-Ca exchange, [Cali and myocardial contraction. In Stone, L. and Weglicki, W. B. (Eds), Pathobiology of Cardiovascular Injury. Martinus Nijhoff, Boston, pp. 232–244Google Scholar
  49. Reeves, J. P. and Hale, C. C. (1984). The stoichiometry of the cardiac sodium-calcium exchange system. J. Biol. Chem., 259, 7733–7739PubMedGoogle Scholar
  50. Richter, C. (1990). The prooxidant-induced and spontaneous mitochondrial calcium release: inhibition by meta-iodo-benzylguanidine (MIBG), a substrate for mono(ADP-ribosylation). Free Rad. Res. Comms, 8, 329–334CrossRefGoogle Scholar
  51. Richter, C. and Frei, B. (1988). Cat’ release from mitochondria induced by prooxidants. Free Rad. Biol. Med., 4, 365–375PubMedCrossRefGoogle Scholar
  52. Schwartz, P., Piper, H. M., Spahr, R. and Spieckermann, P. G. (1984). Ultrastructure of cultured adult myocardial cells during anoxia and reoxygenation. Am. J. Pathol., 115, 349–361PubMedPubMedCentralGoogle Scholar
  53. Shen, A. C. and Jennings, R. B. (1972a). Myocardial calcium and magnesium in acute ischemic injury. Am. J. Pathol., 67, 417–440PubMedPubMedCentralGoogle Scholar
  54. Shen, A. C. and Jennings, R. B. (1972b). Kinetics of calcium accumulation in acute myocardial ischemic injury. Am. J. Pathol., 67, 441–452PubMedPubMedCentralGoogle Scholar
  55. Shine, K. I. and Douglas, A. M. (1983). Low calcium reperfusion of ischemic myocardium. J. Mol. Cell. Cardiol., 15, 251–260PubMedCrossRefGoogle Scholar
  56. Smith, D. R., Darley-Usmar, V. M. and Stone, D. (1990). Effects of caffeine, oligomycin and ruthenium red on the reoxygenation-induced increase in total Ca2+ in rat cardiomyocytes. J. Mol. Cell. Cardiol., 22 (Suppl. III), 58CrossRefGoogle Scholar
  57. Smith, E. F., Egan, J. W., Bugelski, P. J., Hillegas, L. M., Hill, D. E. and Griswold, D. E. (1988). Temporal relation between neutrophil accumulation and myocardial reperfusion injury. Am. J. Physiol., 255, H1060–H1068PubMedGoogle Scholar
  58. Smith, G. L. and Allen, D. G. (1988). Effects of metabolic blockade on intracellular calcium concentration in isolated ferret ventricular muscle. Circ. Res., 62, 1223–1236PubMedCrossRefGoogle Scholar
  59. Steenbergen, C., Murphy, E., Levy, L. and London, R. E. (1987). Elevation in cytosolic free calcium concentration early in myocardial ischemia in perfused rat heart. Circ. Res., 60, 700–707PubMedCrossRefGoogle Scholar
  60. Stone, D., Darley-Usmar, V., Smith, D. R. and O’Leary, V. (1989). Hypoxia-reoxygenation induced increase in cellular Ca2+ in myocytes and perfused hearts: the role of mitochondria. J. Mol. Cell. Cardiol., 21, 963–973PubMedCrossRefGoogle Scholar
  61. Sugiyama, S. and Ozawa, T. (1987). Biochemical basis for reperfusion arrhythmias. J. Mol. Cell. Cardiol., 19, 67–75PubMedCrossRefGoogle Scholar
  62. Tani, M. and Neely, J. R. (1990). Na+ accumulation increases Ca2+ overload and impairs function in anoxic rat heart. J. Mol. Cell. Cardiol., 22, 57–72PubMedCrossRefGoogle Scholar
  63. Veitch, K., Caucheteux, D., Hombroeckx, A. and Hue, L. (1990). Mitochondrial damage during cardiac ischaemia and reperfusion: the role of oxygen. Biochem. Soc. Trans., 18, 526–528CrossRefGoogle Scholar
  64. Woodward, B. and Zakaria, M. N. M. (1985). Effect of some free radical scavengers on reperfusion induced arrhythmias in the isolated rat heart. J. Mol. Cell. Cardiol., 17, 485–493PubMedCrossRefGoogle Scholar

Copyright information

© Macmillan Publishers Limited 1992

Authors and Affiliations

  • D. Stone
  • V. Darley-Usmar
  • J. F. Martin

There are no affiliations available

Personalised recommendations