Cyclosporin A, but not FK 506, protects mitochondria and neurons against hypoglycemic damage and implicates the mitochondrial permeability transition in cell death

Journal of Neuroscience

Volumn 18, Issue 14, 1998, Pages 5151-5159

  Friberg, Hans ^a,b   Ferrand Drake, Michel ^a   Bengtsson, Finn ^b   Halestrap, Andrew P ^c   Wieloch, Tadeusz ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Brain damage; Cell death; Cyclosporin A; Hippocampal mitochondria; Hypoglycemia; Mitochondrial permeability transition

Indexed keywords

CYCLOSPORIN A; TACROLIMUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INJURY; CELL DEATH; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; HIPPOCAMPUS; HYPOGLYCEMIA; HYPOGLYCEMIC COMA; MALE; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION SWELLING; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; ULTRASTRUCTURE;

EID: 0032528154     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-14-05151.1998     Document Type: Article

References (60)

1. Agardh CD, Smith ML, Siesjö BK (1992) The influence of hypothermia on hypoglycemia-induced brain damage in the rat. Acta Neuropathol (Berl) 83:379-385.
2. Aguilar HI, Botla R, Arora AS, Bronk SF, Gores GJ (1996) Induction of the mitochondnal permeability transition by protease activity in rats: a mechanism of hepatocyte necrosis. Gastroenterology 110:558-566.
3. Auer R, Kalimo H, Olsson Y, Wieloch T (1985) The dentate gyrus in hypoglycemia: pathology implicating excitotoxin-mediated neuronal necrosis. Acta Neuropathol (Berl) 67:279-288.
4. Auer RN, Siesjo BK (1993) Hypoglycaemia: brain neurochemistry and neuropathology. Baillieres Clin Endocrinol Metab 7:611-625.
5. Begley DJ, Squires LK, Zlokovic BV, Mitrovic DM, Hughes CC, Revest PA, Greenwood J (1990) Permeability of the blood-brain barrier to the immunosuppressive cyclic peptide cyclosporin A, J Neurochem 55:1222-1230.
6. Bernardi P, Vassanelli S, Veronese P, Colonna R, Szabo I, Zoratti M (1992) Modulation of the mitochondrial permeability transition pore. Effect of protons and divalent cations. J Biol Chem 267:2934-2939.
7. Bernardi P, Broekemeier KM, Pfeiffer DR (1994) Recent progress on regulation of the mitochondrial permeability transition pore: a cyclosporin-sensitive pore in the inner mitochondrial membrane. J Bioenerg Biomembr 26:509-517.
8. Bernareggi A, Rowland M (1991) Physiologic modeling of cyclosporin kinetics in rat and man. J Pharmacokinet Biopharm 19:21-50.
9. Brillantes AB, Ondrias K, Scott A, Kobrinsky E, Ondriasova E, Moschella MC, Jayaraman T, Landers M, Ehrlich BE, Marks AR (1994) Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77:513-523.
10. Buchan A, Pulsinelli WA (1990) Hypothermia but not the N-methyl-D-aspartate antagonist, MK-801, attenuates neuronal damage in gerbils subjected to transient global ischemia. J Neurosci 10:311-316.
11. Butcher SP, Henshall DC, Teramura Y, Iwasaki K, Sharkey J (1997) Neuroprotective actions of FK506 in experimental stroke: in vivo evidence against an antiexcitotoxic mechanism. J Neurosci 17:6939-6946.
12. Cameron AM, Steiner JP, Sabatini DM, Kaplin AI, Walensky LD, Snyder SH (1995) Immunophilin FK506 binding protein associated with inositol 1,4,5-trisphosphate receptor modulates calcium flux. Proc Natl Acad Sci USA 92:1784-1788.
13. Clipstone NA, Crabtree GR (1992) Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357:695-697.
14. Connern CP, Halestrap AP (1992) 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 284:381-385.
15. Connern CP, Halestrap AP (1994) Recruitment of mitochondrial cyrlophilin to the mitochondrial inner membrane under conditions of oxidative stress that enhance the opening of a calcium-sensitive non-specific channel. Biochem J 302:321-324.
16. Crompton M, Costi A, Hayat L (1987) Evidence for the presence of a reversible Ca2+-dependent pore activated by oxidative stress in heart mitochondria. Biochem J 245:915-918.
17. Crompton M, Ellinger H, Costi A (1988) Inhibition by cyclosporin A of a Ca2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 255:357-360.
18. Dawson TM, Steiner JP, Dawson VL, Dinerman JL, Uhl GR, Snyder SH (1993) Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc Natl Acad Sci USA 90:9808-9812.
19. Drake M, Friberg H, Boris-Moller F, Sakata K, Wieloch T (1996) The immunosuppressant FK506 ameliorates ischaemic damage in the rat brain. Acta Physiol Scand 158:155-159.
20. Galat A, Metcalfe SM (1995) Peptidylproline cis/trans isomerases. Prog Biophys Mol Biol 63:67-118.
21. Ginsberg MD (1997) Hypothermic neuroprotection in cerebral ischemia. In: Primer on cerebrovascular disease (Welch KMA, Reis DJ, Siesjo BK, Weir B, eds), pp 272-275. Los Angeles: Academic Press.
22. Griffiths EJ, Halestrap AP (1991) 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 274:611-614.
23. Griffiths EJ, Halestrap AP (1993a) Protection by cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. J Mol Cell Cardiol 25:1461-1469.
24. Griffiths EJ, Halestrap AP (1993b) Pyrophosphate metabolism in the perfused heart and isolated heart mitochondria and its role in regulation of mitochondrial function by calcium. Biochem J 290:489-495.
25. Gunter TE, Pfeiffer DR (1990) Mechanisms by which mitochondria transport calcium. Am J Physiol 258:C755-786.
26. Halestrap AP (1991) 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.
27. Halestrap AP (1994) Interaction between oxidative stress and calcium overload on mitochondrial function. In: Mitochondria: DNA, proteins and disease (Darley-Usmar V, Schapira AHV, eds), pp 113-142, London: Portland.
28. Halestrap AP, Davidson AM (1990) Inhibition of Ca2(+)-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 268:153-160.
29. Harris RJ, Wieloch T, Symon L, Siesjo BK (1984) Cerebral extracellular calcium activity in severe hypoglycemia; relation to extracellular potassium and energy state. J Cereb Blood Flow Metab 4:187-193.
30. Haworth RA, Hunter DR (1979) The Ca2+-induced membrane transition in mitochondria. II. Nature of the Ca2+ trigger site. Arch Biochem Biophys 195:460-467.
31. Ide T, Morikawa E, Kirino T (1996) An immunosuppressant, FK506, protects hippocampal neurons from forebrain ischemia in the mongolian gerbil. Neurosci Lett 204:157-160.
32. Jurkowitz MS, Brierley GP (1982) H+-dependent efflux of Ca2+ from heart mitochondria. J Bioenerg Biomembr 14:435-449.
33. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132-1136.
34. Kristal BS, Dubinsky JM (1997) Mitochondrial permeability transition in the central nervous system: induction by calcium cyclin-dependent and -independent pathways, J Neurochem 69:524-538.
35. Kroemer G (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 3:614-620.
36. Liu J, Farmer Jr JD, Lane WS, Friedman J, Weissman I, Schreiber SL (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66:807-815.
37. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, Haeffner A, Hirsch F, Geuskens M, Kroemer G (1996a) Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 184:1155-1160.
38. Marchetti P, Hirsch T, Zamzami N, Castedo M, Decaudin D, Susin SA, Masse B, Kroemer G (1996b) Mitochondrial permeability transition triggers lymphocyte apoptosis. J Immunol 157:4830-4836.
39. Nicholson DW, Thornberry NA (1997) Caspases: killer proteases. Trends Biochem Sci 22:299-306.
40. Nieminen AL, Petrie TG, Lemasters JJ, Selman WR (1996) Cyclosporin A delays mitochondrial depolarization induced by N-methyl-D-aspartate in cortical neurons: evidence of the mitochondrial permeability transition, Neuroscience 75:993-997.
41. O'Keefe SJ, Tamura J, Kincaid RL, Tocci MJ, O'Neill EA (1992) FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357:692-694.
42. Sakata A, Tamai I, Kawazu K, Deguchi Y, Ohnishi T, Saheki A, Tsuji A (1994) In vivo evidence for ATP-dependent and P-glycoproteinmediated transport of cyclosporin A at the blood-brain barrier. Biochem Pharmacol 48:1989-1992.
43. Sandberg M, Butcher SP, Hagberg H (1986) Extracellular overflow of neuroactive amino acids during severe insulin-induced hypoglycemia: in vivo dialysis of the rat hippocampus. J Neurochem 47:178-184.
44. Schinder AF, Oison EC, Spitzer NC, Montai M (1996) Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J Neurosci 16:6125-6133.
45. Sharkey J, Butcher SP (1994) Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia. Nature 371:336-339.
46. Shibasaki F, Kondo E, Akagi T, McKeon F (1997) Suppression of signalling through transcription factor NF-AT by interactions between calcineurin and Bcl-2. Nature 386:728-731.
47. Shiga Y, Onodera H, Matsuo Y, Kogure K (1992) Cyclosporin A protects against ischemia-reperfusion injury in the brain. Brain Res 595:145-148.
48. Siesjo BK, Bengtsson F (1989) Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: a unifying hypothesis. J Cereb Blood Flow Metab 9:127-140.
49. Sims NR (1990) Rapid isolation of metabolically active mitochondria from rat brain and subregions using Percoll density gradient centrifugation. J Neurochem 55:698-707.
50. Steiner JP, Connolly MA, Valentine HL, Hamilton GS, Dawson TM, Hester L, Snyder SH (1997) Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin and cyclosporin A. Nat Med 3:421-428.
51. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M, Kroemer G (1996) Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 184:1331-1341.
52. Susin SA, Zamzami N, Castedo M, Daugas E, Wang HG, Geley S, Fassy F, Reed JC, Kroemer G (1997) The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-l/CD95- and ceramide-induced apoptosis. J Exp Med 186:25-37.
53. Uchino H, Elmer E, Uchino K, Lindvall O, Siesjo BK (1995) Cyclosporin A dramatically ameliorates CA1 hippocampal damage following transient forebrain ischaemia in the rat. Acta Physiol Scand 155:469-471.
54. White RJ, Reynolds IJ (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J Neurosci 16:5688-5697.
55. Wieloch T, Harris RJ, Symon L, Siesjo BK (1984) Influence of severe hypoglycemia on brain extracellular calcium and potassium activities, energy, and phospholipid metabolism. J Neurochem 43:160-168.
56. Woodfield KY, Price NT, Halestrap AP (1997) cDNA cloning of rat mitochondrial cyclophilin. Biochem Biophys Acta 1351:27-30.
57. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129-1132.
58. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, Kroemer G (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182:367-377.
59. Zoratti M, Szabo I (1995) The mitochondrial permeability transition. Biochim Biophys Acta 1241:139-176.
60. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X (1997) Apaf-1, a human protein homologous to C. elegans CED-4: participates in cytochrome c-dependent activation of caspase-3. Cell 90:405-413.