Powerful cyclosporin inhibition of calcium-induced permeability transition in brain mitochondria

Brain Research

Volumn 960, Issue 1-2, 2003, Pages 99-111

  Hansson, Magnus J ^a,c   Persson, Tanja ^a   Friberg, Hans ^a   Keep, Marcus F ^b,c   Rees, Anthony ^d   Wieloch, Tadeusz ^a   Elmér, Eskil ^a,c  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c Maas BiolAB   (United States)

^d Synt:em   (France)

Author keywords

Cyclosporin A; Disorders of the nervous system; Ischemia; Mitochondrial permeability transition; Neurodegeneration; Neuroprotection

Indexed keywords

CALCIUM ION; CYCLOSPORIN A;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; BRAIN SYNAPTOSOME; CALCIUM CELL LEVEL; CELL SWELLING; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENERGY; KINETICS; LIGHT SCATTERING; LIVER MITOCHONDRION; MALE; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; RAT; SPECTROPHOTOMETRY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN CHEMISTRY; CALCIUM; CYCLOSPORINE; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MICROSCOPY, ELECTRON; MITOCHONDRIA; MITOCHONDRIA, LIVER; MITOCHONDRIAL SWELLING; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; OXYGEN CONSUMPTION; PERMEABILITY; RATS; RATS, WISTAR;

EID: 0037449449     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(02)03798-8     Document Type: Article

References (84)

1. Andreyev A., Fiskum G. Calcium induced release of mitochondrial cytochrome c by different mechanisms selective for brain versus liver. Cell Death Differ. 6:1999;825-832.
2. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron. 15:1995;961-973.
3. Ankarcrona M., Dypbukt J.M., Orrenius S., Nicotera P. Calcineurin and mitochondrial function in glutamate-induced neuronal cell death. FEBS Lett. 394:1996;321-324.
4. Anneser J.M., Gmerek A., Gerkrath J., Borasio G.D., Heumann R. Immunosuppressant FK506 does not exert beneficial effects in symptomatic G93A superoxide dismutase-1 transgenic mice. Neuroreport. 12:2001;2663-2665.
5. Berman S.B., Watkins S.C., Hastings T.G. Quantitative biochemical and ultrastructural comparison of mitochondrial permeability transition in isolated brain and liver mitochondria: evidence for reduced sensitivity of brain mitochondria. Exp. Neurol. 164:2000;415-425.
6. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev. 79:1999;1127-1155.
7. Bernardi P., Broekemeier K.M., Pfeiffer D.R. Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporin-sensitive pore in the inner mitochondrial membrane. J. Bioenerg. Biomembr. 26:1994;509-517.
8. Bernardi P., Petronilli V. The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal. J. Bioenerg. Biomembr. 28:1996;131-138.
9. Bernardi P., Vassanelli S., Veronese P., Colonna R., Szabo I., Zoratti M. Modulation of the mitochondrial permeability transition pore. Effect of protons and divalent cations. J. Biol. Chem. 267:1992;2934-2939.
10. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA. 92:1995;7162-7166.
11. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
12. Broekemeier K., Pfeiffer D. 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. 34:1995;16440-16449.
13. Broekemeier K.M., Dempsey M.E., Pfeiffer D.R. Cyclosporin A is a potent inhibitor of the inner membrane permeability transition in liver mitochondria. J. Biol. Chem. 264:1989;7826-7830.
14. Brustovetsky N., Dubinsky J.M. Limitations of cyclosporin A inhibition of the permeability transition in CNS mitochondria. J. Neurosci. 20:2000;8229-8237.
15. Budd S.L., Nicholls D.G. Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem. 67:1996;2282-2291.
16. Buki A., Okonkwo D.O., Povlishock J.T. Postinjury cyclosporin A administration limits axonal damage and disconnection in traumatic brain injury. J. Neurotrauma. 16:1999;511-521.
17. Chappell J.B., Hansford R.G. Preparation of mitochondria from animal tissues and yeasts. Birnie G.D. Subcellular Components; Preparation and Fractionation. 1972;77-91 Butterworths, London.
18. Connern C.P., Halestrap A.P. Purification and N-terminal sequencing of peptidyl-prolyl cis-trans -isomerase from rat liver mitochondrial matrix reveals the existence of a distinct mitochondrial cyclophilin. Biochem. J. 284:1992;381-385.
19. Connern C.P., Halestrap A.P. Recruitment of mitochondrial cyclophilin to the mitochondrial inner membrane under conditions of oxidative stress that enhance the opening of a calcium-sensitive non-specific channel. Biochem. J. 302:1994;321-324.
20. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341:1999;233-249.
21. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem. J. 255:1988;357-360.
22. Du C., Fang M., Li Y., Li L., Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 102:2000;33-42.
23. Dubinsky J.M., Levi Y. Calcium-induced activation of the mitochondrial permeability transition in hippocampal neurons. J. Neurosci. Res. 53:1998;728-741.
24. Fournier N., Ducet G., Crevat A. Action of cyclosporine on mitochondrial calcium fluxes. J. Bioenerg. Biomembr. 19:1987;297-303.
25. Friberg H., Connern C., Halestrap A.P., Wieloch T. Differences in the activation of the mitochondrial permeability transition among brain regions in the rat correlate with selective vulnerability. J. Neurochem. 72:1999;2488-2497.
26. Friberg H., Ferrand-Drake M., Bengtsson F., Halestrap A.P., Wieloch T. Cyclosporin A, but not FK 506, protects mitochondria and neurons against hypoglycemic damage and implicates the mitochondrial permeability transition in cell death. J. Neurosci. 18:1998;5151-5159.
27. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
28. Griffiths E.J., Halestrap A.P. Further evidence that cyclosporin A protects mitochondria from calcium overload by inhibiting a matrix peptidyl-prolyl cis-trans isomerase. Implications for the immunosuppressive and toxic effects of cyclosporin. Biochem. J. 274:1991;611-614.
29. Griffiths E.J., Halestrap A.P. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem. J. 307:1995;93-98.
30. 2+ transients. Biochim. Biophys. Acta. 1366:1998;5-15.
31. Gunter T.E., Pfeiffer D.R. Mechanisms by which mitochondria transport calcium. Am. J. Physiol. 258:1990;C755-C786.
32. 2+. Biochem. J. 244:1987;159-164.
33. Halestrap A.P. Interaction between oxidative stress and calcium overload on mitochondrial function. Darley-Usmar V., Schapira A.H.V. Mitochondria: DNA, Proteins and Disease. 1994;113-142 Portland Press, London.
34. 2+-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin 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. 268:1990;153-160.
35. Halestrap A.P., Quinlan P.T., Whipps D.E., Armston A.E. Regulation of the mitochondrial matrix volume in vivo and in vitro. The role of calcium. Biochem. J. 236:1986;779-787.
36. 2+ trigger site. Arch. Biochem. Biophys. 195:1979;460-467.
37. 2+-activated hydrophilic channel of the mitochondrial inner membrane by nucleotides. J. Membr. Biol. 54:1980;231-236.
38. 2+-induced membrane transition in mitochondria. I. The protective mechanisms. Arch. Biochem. Biophys. 195:1979;453-459.
39. 2+ release. Arch. Biochem. Biophys. 195:1979;468-477.
40. Hunter D.R., Haworth R.A., Southard J.H. Relationship between configuration, function, and permeability in calcium-treated mitochondria. J. Biol. Chem. 251:1976;5069-5077.
41. Ichas F., Mazat J.P. From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim. Biophys. Acta. 1366:1998;33-50.
42. Keep M., Elmér E., Fong K., Csiszar K. Intrathecal cyclosporin prolongs survival of late-stage ALS mice. Brain Res. 894:2001;327-331.
43. Kristal B.S., Dubinsky J.M. Mitochondrial permeability transition in the central nervous system: induction by calcium cycling-dependent and -independent pathways. J. Neurochem. 69:1997;524-538.
44. Kristal B.S., Staats P.N., Shestopalov A.I. Biochemical characterization of the mitochondrial permeability transition in isolated forebrain mitochondria. Dev. Neurosci. 22:2000;376-383.
45. Kristian T., Bernardi P., Siesjö B.K. Acidosis promotes the permeability transition in energized mitochondria: implications for reperfusion injury. J. Neurotrauma. 18:2001;1059-1074.
46. Kristian T., Gertsch J., Bates T.E., Siesjö B.K. Characteristics of the calcium-triggered mitochondrial permeability transition in nonsynaptic brain mitochondria: effect of cyclosporin A and ubiquinone O. J. Neurochem. 74:2000;1999-2009.
47. Kristian T., Siesjö B.K. Calcium in ischemic cell death. Stroke. 29:1998;705-718.
48. Kroemer G., Dallaporta B., Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60:1998;619-642.
49. Kuroda S., Janelidze S., Siesjö B.K. The immunosuppressants cyclosporin A and FK506 equally ameliorate brain damage due to 30-min middle cerebral artery occlusion in hyperglycemic rats. Brain Res. 835:1999;148-153.
50. Lemasters J.J., Nieminen A.L., Qian T., Trost L.C., Elmore S.P., Nishimura Y., Crowe R.A., Cascio W.E., Bradham C.A., Brenner D.A., Herman B. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta. 1366:1998;177-196.
51. Li P., He Q.P., Siesjö B.K. Effects of intracarotid arterial injection of cyclosporin A and spontaneous hypothermia on brain damage incurred after a long period of global ischemia. Brain. Res. 890:2001;306-313.
52. Li P.A., Kristian T., He Q.P., Siesjö B.K. Cyclosporin A enhances survival, ameliorates brain damage, and prevents secondary mitochondrial dysfunction after a 30-min period of transient cerebral ischemia. Exp. Neurol. 165:2000;153-163.
53. Li P.A., Uchino H., Elmér E., Siesjö B.K. Amelioration by cyclosporin A of brain damage following 5 or 10 min of ischemia in rats subjected to preischemic hyperglycemia. Brain Res. 753:1997;133-140.
54. Liu J., Farmer J.D. Jr., Lane W.S., Friedman J., Weissman I., Schreiber S.L. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell. 66:1991;807-815.
55. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 86:1996;147-157.
56. Matsumoto S., Friberg H., Ferrand-Drake M., Wieloch T. Blockade of the mitochondrial permeability transition pore diminishes infarct size in the rat after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 19:1999;736-741.
57. Murchison D., Griffith W.H. Mitochondria buffer non-toxic calcium loads and release calcium through the mitochondrial permeability transition pore and sodium/calcium exchanger in rat basal forebrain neurons. Brain Res. 854:2000;139-151.
58. Murphy A.N., Fiskum G., Beal M.F. Mitochondria in neurodegeneration: bioenergetic function in cell life and death. J. Cereb. Blood Flow Metab. 19:1999;231-245.
59. O'Gorman E., Beutner G., Dolder M., Koretsky A.P., Brdiczka D., Wallimann T. The role of creatine kinase in inhibition of mitochondrial permeability transition. FEBS Lett. 414:1997;253-257.
60. Okonkwo D.O., Buki A., Siman R., Povlishock J.T. Cyclosporin A limits calcium-induced axonal damage following traumatic brain injury. NeuroReport. 10:1999;353-358.
61. Okonkwo D.O., Povlishock J.T. An intrathecal bolus of cyclosporin A before injury preserves mitochondrial integrity and attenuates axonal disruption in traumatic brain injury. J. Cereb. Blood Flow Metab. 19:1999;443-451.
62. Petronilli V., Cola C., Massari S., Colonna R. Physiological effectors modify voltage sensing by the cyclosporin A-sensitive permeability transition pore of mitochondria. J. Biol. Chem. 268:1993;21939-21945.
63. 2+ plus N-ethylmaleimide on mitochondrial function. J. Biol. Chem. 254:1979;11485-11494.
64. Portera-Cailliau C., Price D.L., Martin L.J. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J. Comp. Neurol. 378:1997;70-87.
65. Scheff S.W., Sullivan P.G. Cyclosporin A significantly ameliorates cortical damage following experimental traumatic brain injury in rodents. J. Neurotrauma. 16:1999;783-792.
66. 2+ thresholds determine cytochrome c release or permeability transition pore opening in brain mitochondria. FASEB J. 15:2001;565-567.
67. Shephard D., Garland P.B. Citrate synthase from rat liver. Lowenstein J.M. Methods in Enzymology. Vol. XIII:1969;11-16 Academic Press, New York.
68. Siesjö B.K. Cell damage in the brain: a speculative synthesis. J. Cereb. Blood Flow Metab. 1:1981;155-185.
69. Sims N. Rapid isolation of metabolically active mitochondria from rat brain and subregions using percoll density gradient centrifugation. J. Neurochem. 55:1990;698-707.
70. Sims N.R., Anderson M.F., Hobbs L.M., Powell J.A., Zaidan E. Brain mitochondrial responses to postischemic reperfusion: a role for calcium and hydrogen peroxide? Dev. Neurosci. 22:2000;366-375.
71. Stout A.K., Raphael H.M., Kanterewicz B.I., Klann E., Reynolds I.J. Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat. Neurosci. 1:1998;366-373.
72. Sullivan P.G., Rabchevsky A.G., Hicks R.R., Gibson T.R., Fletcher-Turner A., Scheff S.W. Dose-response curve and optimal dosing regimen of cyclosporin A after traumatic brain injury in rats. Neuroscience. 101:2000;289-295.
73. Sullivan P.G., Thompson M., Scheff S.W. Continuous infusion of cyclosporin A postinjury significantly ameliorates cortical damage following traumatic brain injury. Exp. Neurol. 161:2000;631-637.
74. Sullivan P.G., Thompson M.B., Scheff S.W. Cyclosporin A attenuates acute mitochondrial dysfunction following traumatic brain injury. Exp. Neurol. 160:1999;226-234.
75. Susin S.A., Zamzami N., Castedo M., Hirsch T., Marchetti P., Macho A., Daugas E., Geuskens M., Kroemer G. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184:1996;1331-1341.
76. Szabo I., Zoratti M. The mitochondrial megachannel is the permeability transition pore. J. Bioenerg. Biomembr. 24:1992;111-117.
77. Uchino H., Elmér E., Uchino K., Li P.A., He Q.P., Smith M.L., Siesjö B.K. Amelioration by cyclosporin A of brain damage in transient forebrain ischemia in the rat. Brain Res. 812:1998;216-226.
78. Uchino H., Elmér E., Uchino K., Lindvall O., Siesjö B.K. Cyclosporin A dramatically ameliorates CA1 hippocampal damage following transient forebrain ischaemia in the rat. Acta Physiol. Scand. 155:1995;469-471.
79. Verhagen A.M., Ekert P.G., Pakusch M., Silke J., Connolly L.M., Reid G.E., Moritz R.L., Simpson R.J., Vaux D.L. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 102:2000;43-53.
80. Weeber E.J., Levy M., Sampson M.J., Anflous K., Armstrong D.L., Brown S.E., Sweatt J.D., Craigen W.J. The role of mitochondrial porins and the permeability transition pore in learning and synaptic plasticity. J. Biol. Chem. 277:2002;18891-18897.
81. White R.J., Reynolds I.J. Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J. Neurosci. 16:1996;5688-5697.
82. Yoshimoto T., Siesjö B.K. Posttreatment with the immunosuppressant cyclosporin A in transient focal ischemia. Brain Res. 839:1999;283-291.
83. Zamzami N., Hirsch T., Dallaporta B., Petit P.X., Kroemer G. Mitochondrial implication in accidental and programmed cell death: apoptosis and necrosis. J. Bioenerg. Biomembr. 29:1997;185-193.
84. Zoratti M., Szabo I. The mitochondrial permeability transition. Biochim. Biophys. Acta. 1241:1995;139-176.