Mitochondrial permeability transition in the central nervous system: Induction by calcium cycling-dependent and -independent pathways

Journal of Neurochemistry

Volumn 69, Issue 2, 1997, Pages 524-538

  Kristal, Bruce S ^a,c   Dubinsky, Janet M ^b  

^a Mays Cancer Center at UT Health San Antonio   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c BURKE MEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

Astrocytes; CNS; Ischemia; Mitochondria; Permeability transition; Reperfusion

Indexed keywords

ADENOSINE DIPHOSPHATE; BROMOCALCIMYCIN; BUTACAINE; CALCIUM CHLORIDE; CALCIUM ION; CYCLOSPORIN A; DIGITONIN; DITHIOTHREITOL; FURA 2; MAGNESIUM ION; N ETHYLMALEIMIDE; RUTHENIUM RED;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; BRAIN MITOCHONDRION; CALCIUM TRANSPORT; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE TRANSPORT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; MALE; MITOCHONDRIAL MEMBRANE; NERVE CELL CULTURE; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY;

ANIMALIA;

EID: 0030800033     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69020524.x     Document Type: Article

References (67)

1. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A., and Nicotera P. (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
2. Bernardi P. (1992) Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electro-chemical gradient: evidence that the pore can be opened by membrane depolarization. J. Biol. Chem. 267, 8834-8839.
3. Bernardi P., Vassanelli S., Veronese P., Colonna R., Szabo I., and Zoratti M. (1992) Modulation of the mitochondrial permeability transition pore: effect of protons and divalent cations. J. Biol. Chem. 267, 2934-2939.
4. Brierly J. B. (1976) Cerebral hypoxia, in Greenfield's Neuropathology (McDowell F. H. and Brennan R. W., eds), pp. 43-85.
5. Broekemeier K. M. and Pfeiffer D. R. (1995) Inhibition of the mitochondrial permeability transition by cyclosporin A during long time frame experiments - relationship between pore opening and the activity of mitochondrial phospholipases. Biochemistry 34, 16440-16449.
6. Broekemeier K. M., Dempsey M. E., and Pfeiffer D. R. (1989) Cyclosporin A is a potent inhibitor of the inner membrane permeability transition in liver mitochondria. J. Biol. Chem. 264, 7826-7830.
7. Chacon E., Ohata H., Harper I. S., Trollinger D. R., Herman B., and Lemasters J. J. (1996) Mitochondrial free calcium transients during excitation-contraction coupling in rabbit cardiac myocytes. FEBS Lett. 382, 31-36.
8. Choi D. W. (1987) Ionic dependence of glutamate neurotoxicity. J. Neurosci. 7, 369-379.
9. Costantini P., Chernyak B. V., Petronilli V., and Bernardi P. (1996) Modulation of the mitochondrial permeability transition by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol. Chem. 271, 6746-6751.
10. 2+-dependent pore activated by oxidative stress in heart mitochondria. Biochem. J. 245, 195-198.
11. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem. J. 255, 357-360.
12. Dorbani L., Jancsik V., Linden M., Leterrier J. F., Nelson B. D., and Rendon A. (1987) Subfractionation of the outer membrane of rat brain mitochondria: evidence for the existence of a domain containing the porin-hexokinase complex. Arch. Biochem. Biophys. 252, 188-196.
13. Dubinsky J. M. (1993) Intracellular calcium levels during the period of delayed excitotoxicity. J. Neurosci. 13, 623-631.
14. Dubinsky J. M., Kristal B. S., and Elizondo-Fournier M. (1995) An obligate role for oxygen in the early stages of glutamate-induced delayed neuronal death. J. Neurosci. 15, 7071-7078.
15. 2+-dependent changes in the mitochondrial energetics in single dissociated mouse sensory neurons. Biochem. J. 283, 41-50.
16. +: implications for neurodegeneration. J. Neurochem. 63, 584-591.
17. 2+ after toxic NMDA-receptor activity. J. Neurochem. 65, 739-743.
18. Esterbauer H., Schaur R. J., and Zollner H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malondialdehyde, and related aldehydes. Free Radic. Biol. Med. 11, 81-128.
19. Fagian M. M., Pereira-da-Silva L., Martins I. S., and Vercesi A. E. (1990) Membrane protein thiol cross-linking associated with the permeabilization of the inner mitochondrial membrane. J. Biol. Chem. 265, 19955-19960.
20. Fiskum G. (1983) Involvement of mitochondria in ischemic cell injury and in regulation of intracellular calcium. Am. J. Emerg. Med. 1, 147-153.
21. 2+ in digitonin-permeabilized cells. Cell Calcium 6, 25-37.
22. i. J. Neurosci. 14, 4007-4024.
23. Giulivi C., Boveris A., and Cadenas E. (1995) Hydroxyl radical generation during mitochondrial electron transfer and the formation of 8-hydroxydesoxyguanosine in mitochondrial DNA. Arch. Biochem. Biophys. 316, 909-916.
24. Griffiths E. J. and Halestrap A. P. (1995) Mitochondrial non-specific pores remain closed during cardiac ischemia, but open upon reperfusion. Biochem. J. 307, 93-98.
25. Groskreutz J. L., Bronk S. F., and Gores G. J. (1992) Ruthenium red delays the onset of cell death during oxidative stress of rat hepatocytes. Gastroenterology 102, 1030-1038.
26. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
27. Gunter T. E. and Pfeiffer D. R. (1990) Mechanisms by which mitochondria transport calcium. Am. J. Physiol. 258, C755-C786.
28. Gunter T. E., Gunter K. K., Sheu S. S., and Gavin C. E. (1994) Mitochondrial calcium transport: physiological and pathological relevance. Am. J. Physiol. 267, C313-C339.
29. Imberti R., Nieminen A. L., Herman B., and Lemasters J. J. (1993) Mitochondrial and glycolytic dysfunction in lethal injury to hepatocytes by t-butylhydroperoxide: protection by fructose, cyclosporin A and trifluoperazine. J. Pharmacol. Exp. Ther. 265, 392-400.
30. 2+ ions - a proposed model for phosphate-stimulated lipid peroxidation. J. Biol. Chem. 271, 2929-2934.
31. Kristal B. S., Park B. K., and Yu B. P. (1996) 4-Hydroxyhexenal is a potent inducer of the mitochondrial permeability transition. J. Biol. Chem. 271, 6033-6038.
32. Lafon-Cazal M., Pietri S., Culcasi M., and Bockaert J. (1993) NMDA-dependent superoxide production and neurotoxicity. Nature 364, 535-537.
33. 2+ release from mitochondria by the oxidation-reduction state of pyridine nucleotides. Prof. Natl. Acad. Sci. USA 75, 1690-1694.
34. Lipton S. A., Choi Y. B., Pan Z. H., Lei S. Z., Chen H. V., Sucher N. J., Loscalzo J., Singel D. J., and Stamler J. S. (1993) A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364, 626-632.
35. Loew L. M., Tuft R. A., Carrington W., and Fay F. S. (1993) Imaging in five dimensions: time-dependent membrane potentials in individual mitochondria. Biophys. J. 65, 2396-2407.
36. Loschen G., Azzi A., Richter C., and Flohe L. (1974) Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett. 42, 68-72.
37. Mattson M. P., Zhang Y., and Bose S. (1993) Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp. Neurol 121, 1-13.
38. Newman E. A. and Zahs K. R. (1997) Calcium waves in retinal glial cells. Science 275, 844-847.
39. Nicholls D. G. (1985) A role for the mitochondrion in the protection of cells against calcium overload? Prog. Brain Res. 63, 97-106.
40. Nicholls D. G. and Ackerman K. E. O. (1982) Mitochondrial calcium transport. Biochim. Biophys. Acta 683, 57-88.
41. Nohl H., Jordan W., and Hegner D. (1981) Identification of free hydroxyl radicals in respiring rat heart mitochondria by spin trapping with the nitrone DMPO. FEBS Lett. 123, 241-244.
42. 2 release as a byproduct of respiration. Free Radic. Res. Commun. 18, 127-137.
43. Novgorodov S. A., Gudz T. I., Milgrom Y. M., and Brierly G. P. (1992) The permeability transition in heart mitochondria is regulated synergistically by ADP and cyclosporin A. J. Biol. Chem. 267, 16274-16282.
44. Packer M. A. and Murphy M. P. (1995) Peroxynitrite formed by simultaneous nitric oxide and superoxide generation causes cyclosporin A-sensitive mitochondrial calcium efflux and depolarisation. Eur. J. Biochem. 234, 231-239.
45. Pastorino J. G., Snyder J. W., Serroni A., Hoek J. B., and Farber J. L. (1993) Cyclosporin and carnitine prevent the anoxic death of cultured hepatocytes by inhibiting the mitochondrial permeability transition. J. Biol. Chem. 268, 13791-13796.
46. 2+ depletion prevents anoxic death of hepatocytes by inhibiting mitochondrial permeability transition. Am. J. Physiol. Cell Physiol. 268, C676-C685.
47. Petronilli V., Nicolli A., Costantini P., Colonna R., and Bernardi P. (1994) Regulation of the permeability transition pore, a voltage-dependent mitochondrial channel inhibited by cyclosporin A. Biochim. Biophys. Acta 1187, 255-259.
48. Reed K. C. and Bygrave F. L. (1974) Inhibition of mitochondrial calcium transport by lanthanides and ruthenium red. Biochem. J. 140, 143-155.
49. Reed P. W. and Lardy H. A. (1972) A23187: a divalent cation ionophore. J. Biol. Chem. 247, 6970-6977.
50. 2+ release from liver mitochondria. Ann. NY Acad. Sci. 663, 262-268.
51. Richter C., Gogvadze V., Schlapbach R., Schweizer M., and Schlegel J. (1994) Nitric oxide kills hepatocytes by mobilizing cellular calcium. Biochem. Biophys. Res. Commun. 205, 1143-1150.
52. 2+-mediated permeability changes in mitochondria. J. Biol. Chem. 260, 12416-12425.
53. Rothman S. M., Thurston J. H., and Hauhart R. E. (1987) Delayed neurotoxicity of excitatory amino acids in vitro. Neuroscience 22, 471-480.
54. Schinder A. F., Olson E. C., Spitzer N. C., and Montai M. (1996) Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J. Neurosci. 16, 6125-6133.
55. Schwaiger M., Herzog V., and Neupert W. (1987) Characterization of translocation contact sites involved in the import of mitochondrial proteins. J. Cell Biol. 105, 235-246.
56. Schweizer M. and Richter C. (1994) Nitric oxide potently and reversibly deenergizes mitochondria at low oxygen tension. Biochem. Biophys. Res. Commun. 204, 169-174.
57. Sims N. R. (1991) Selective impairment of respiration in mitochondria isolated from brain subregions following transient forebrain ischemia in the rat. J. Neurochem. 56, 1836-1844.
58. Smiley S. T., Reers M., Mottola-Hartshorn C., Lin M., Chen A., Smith T. W., Steele G. D. Jr., and Chen L. B. (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA 88, 3671-3675.
59. Snedecor G. W. and Cochran W. G. (1980) Statistical Methods, 7th edit., p. 98. Iowa State University Press, Iowa City, Iowa.
60. Sun D. and Gilboe D. D. (1994) Ischemia-induced changes in cerebral mitochondrial free fatty acids, phospholipids, and respiration in the rat. J. Neurochem. 62, 1921-1928.
61. Turrens J. F., Alexandre A., and Lehninger A. L. (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch. Biochem. Biophys. 237, 408-414.
62. +-induced alterations of rat liver and hepatoma mitochondrial membrane permeability. Biochem. Biophys. Res. Commun. 154, 934-941.
63. Werth J. L. and Thayer S. A. (1994) Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons. J. Neurosci. 14, 348-356.
64. White R. J. and Reynolds I. J. (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J. Neurosci. 16, 5688-5697.
65. 2+ following intense glutamate stimulation of cultured rat forebrain neurones. J. Physiol. (Lond.) 498, 31-47.
66. Yu B. P., Masoro E. J., and McMahan C. A. (1985) Nutritional influences on aging of Fischer 344 rats. I. Physical, metabolic and longevity characteristics. J. Gerontol. 40, 657-670.
67. Zoratti M. and Szabo I. (1995) The mitochondrial permeability transition. Biochim. Biophys. Acta 1241, 139-176.