Mitochondrial creatine kinase in contact sites: Interaction with porin and adenine nucleotide translocase, role in permeability transition and sensitivity to oxidative damage

NeuroSignals

Volumn 10, Issue 1-2, 2001, Pages 93-111

  Dolder, Max ^a   Wendt, Silke ^a   Wallimann, Theo ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Adenine nucleotide translocase; Creatine kinase; Creatine supplementation; Creatine stimulated respiration; Mitochondria; Oxidative damage; Permeability transition; Porin

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CARDIOLIPIN; CREATINE KINASE; CREATINE PHOSPHATE; MITOCHONDRIAL ENZYME; PORIN;

ARTICLE; CELL MEMBRANE PERMEABILITY; ENERGY BALANCE; ENZYME ACTIVITY; GLYCOLYSIS; HUMAN; ISCHEMIA; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN PROTEIN INTERACTION; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

CELL DEATH; CREATINE KINASE; MITOCHONDRIA; MITOCHONDRIAL ADP, ATP TRANSLOCASES; OXIDATIVE STRESS; PERMEABILITY; PORINS; PROTEIN BINDING;

EID: 0035107677     PISSN: 1424862X     EISSN: 14248638     Source Type: Journal    
DOI: 10.1159/000046878     Document Type: Article

References (169)

1. Klivenyi P, Ferrante RJ, Matthews RT, Bogdanov MB, Klein AM, An-dreassen OA, Mueller G, Wermer M, Kaddurah-Daouk R, Beal MF: Neuroprotective effects of creatine in a transgenic animal model of amyotrophic lateral sclerosis. Nat Med 1999;5:347-350.
2. Malcon C, Kaddurah-Daouk R, Beal MF: Neuroprotective effects of creatine administration against NMDA and malonate toxicity. Brain Res 2000;860:195-198.
3. Brewer GJ, Wallimann TW: Protective effect of the energy precursor creatine against toxicity of glutamate and beta-amyloid in rat hippocampal neurons. J Neurochem 2000;74:1968-1978.
4. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM: Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: The ‘phosphocreatine circuit’ for cellular energy homeostasis. Biochem J 1992;281:21-40.
5. Bernardi P: Mitochondrial transport of cations: Channels, exchangers, and permeability transition. Physiol Rev 1999;79:1127-1155.
6. Fontaine E, Bernardi P: Progress on the mitochondrial permeability transition pore: Regulation by complex I and ubiquinone analogs. J Bioenerg Biomembr 1999;31:335-345.
7. Crompton M, Virji S, Ward JM: Cy-clophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. Eur J Bio-chem 1998;258:729-735.
8. Ruck A, Dolder M, Wallimann T, Brdiczka D: Reconstituted adenine nucleotide translocase forms a channel for small molecules comparable to the mitochondrial permeability transition pore. FEBS Lett 1998; 426:97-101.
9. 2+. Biochemistry 1996;35:8483-8488.
10. Susin SA, Zamzami N, Kroemer G: Mitochondria as regulators of apoptosis: Doubt no more. Biochim Bio-phys Acta 1998;1366:151-165.
11. Kroemer G, Dallaporta B, Resche-Rigon M: The mitochondrial death/ life regulator in apoptosis and necrosis. Annu Rev Physiol 1998;60:619-642.
12. Loeffler M, Kroemer G: The mitochondrion in cell death control: Certainties and incognita. Exp Cell Res 2000;256:19-26.
13. Bernardi P, Scorrano L, Colonna R, Petronilli V, Di Lisa F: Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur J Biochem 1999;264:687-701.
14. Green D, Kroemer G: The central executioners of apoptosis: Caspases or mitochondria? Trends Cell Biol 1998;8:267-271.
15. Bernardi P: Mitochondria in cell death. Biochim Biophys Acta 1998; 1366:1-2.
16. Wallimann T, Dolder M, Schlattner U, Eder M, Hornemann T, O’gorman E, Ruck A, Brdiczka D: Some new aspects of creatine kinase (CK): Compartmentation, structure, function and regulation for cellular and mitochondrial bioenergetics and physiology. Biofactors 1998;8:229-234.
17. Wyss M, Smeitink J, Wevers RA, Wallimann T: Mitochondrial creatine kinase: A key enzyme of aerobic energy metabolism. Biochim Bio-phys Acta 1992;1102:119-166.
18. 2+ regulation by the sarcoplasmic reticulum in mechanically skinned rat skeletal muscle fibres. J Physiol (Lond) 1999;517:447-458.
19. 2+ uptake by cardiac sarcoplasmic reticulum ATPase in situ strongly depends on bound creatine kinase. Pflugers Arch 1996;432: 904-912.
20. 2+-ATPase. Eur J Bio-chem 1993;213:973-980.
21. Veksler VI, Lechene P, Matrougui K, Ventura-Clapier R: Rigor tension in single skinned rat cardiac cell: Role of myofibrillar creatine kinase. Cardiovasc Res 1997;36:354-362.
22. Ventura-Clapier R, Veksler V, Hoerter JA: Myofibrillar creatine kinase and cardiac contraction. Mol Cell Biochem 1994; 133-134:125144.
23. 2+ uptake and regulate local ATP/ADP ratios. J Biol Chem 1990;265:5258-5266.
24. Wallimann T, Schlosser T, Eppen-berger HM: Function of M-line-bound creatine kinase as intramyofibrillar ATP regenerator at the receiving end of the phosphorylcrea-tine shuttle in muscle. J Biol Chem 1984;259:5238-5246.
25. Guerrero ML, Beron J, Spindler B, Groscurth P, Wallimann T, Verrey F: Metabolic support of Na+ pump in apically permeabilized A6 kidney cell epithelia: Role of creatine kinase. Am J Physiol 1997;272:C697-C706.
26. Kottke M, Wallimann T, Brdiczka D: Dual electron microscopic localization of mitochondrial creatine kinase in brain mitochondria. Bio-chem Med Metab Biol 1994;51: 105-117.
27. Kay L, Nicolay K, Wieringa B, Saks V, Wallimann T: Direct evidence for the control of mitochondrial respiration by mitochondrial creatine kinase in oxidative muscle cells in situ. J Biol Chem 2000;275:6937-6944.
28. Saks VA, Kuznetsov AV, Khuchua ZA, Vasilyeva EV, Belikova JO, Kesvatera T, Tiivel T: Control of cellular respiration in vivo by mitochondrial outer membrane and by creatine kinase. A new speculative hypothesis: Possible involvement of mitochondrial-cytoskeleton interactions. J Mol Cell Cardiol 1995;27: 625-645.
29. Lipskaya T, Geiger PJ, Bessman SP: Compartmentation and metabolic parameters of mitochondrial hexo-kinase and creatine kinase depend on the rate of oxidative phosphorylation. Biochem Mol Med 1995;55: 81-89.
30. BeltrandelRio H, Wilson JE: Interaction of mitochondrially bound rat brain hexokinase with intramitochondrial compartments of ATP generated by oxidative phosphorylation and creatine kinase. Arch Biochem Biophys 1992;299:116-124.
31. Hemmer W, Riesinger I, Wallimann T, Eppenberger HM, Quest AF: Brain-type creatine kinase in photoreceptor cell outer segments: Role of a phosphocreatine circuit in outer segment energy metabolism and phototransduction. J Cell Sci 1993; 106:671-683.
32. Kaldis P, Stolz M, Wyss M, Zanolla E, Rothen-Rutishauser B, Vorherr T, Wallimann T: Identification of two distinctly localized mitochondrial creatine kinase isoenzymes in spermatozoa. J Cell Sci 1996;109: 2079-2088.
33. Kaldis P, Kamp G, Piendl T, Walli-mann T: Functions of creatine kinase isoenzymes in spermatozoa. Adv Dev Biol 1997;5:275-312.
34. Hochachka PW: The metabolic implications of intracellular circulation. Proc Natl Acad Sci USA 1999; 96:12233-12239.
35. Tombes RM, Brokaw CJ, Shapiro BM: Creatine kinase-dependent energy transport in sea urchin spermatozoa. Flagellar wave attenuation and theoretical analysis of high energy phosphate diffusion. Biophys J 1987;52:75-86.
36. Wallimann T, Hemmer W: Creatine kinase in non-muscle tissues and cells. Mol Cell Biochem 1994; 133/ 134:193-220.
37. Schlegel J, Zurbriggen B, Wegmann G, Wyss M, Eppenberger HM, Wal-limann T: Native mitochondrial creatine kinase forms octameric structures. I. Isolation of two interconvertible mitochondrial creatine kinase forms, dimeric and octameric mitochondrial creatine kinase: Characterization, localization, and structure-function relationships. J Biol Chem 1988;263:16942-16953.
38. Furter R, Kaldis P, Furter-Graves EM, Schnyder T, Eppenberger HM, Wallimann T: Expression of active octameric chicken cardiac mitochondrial creatine kinase in Escherichia coli. Biochem J 1992;288:771-775.
39. Eder M, Schlattner U, Becker A, Wallimann T, Kabsch W, Fritz-Wolf K: Crystal structure of brain-type creatine kinase at 1.41 A resolution. Protein Sci 1999;8:2258-2269.
40. Schnyder T, Engel A, Lustig A, Wal-limann T: Native mitochondrial creatine kinase forms octameric structures. II. Characterization of dimers and octamers by ultracentrifugation, direct mass measurements by scanning transmission electron microscopy, and image analysis of single mitochondrial creatine kinase octamers. J Biol Chem 1988;263: 16954-16962.
41. Schnyder T, Gross H, Winkler H, Eppenberger HM, Wallimann T: Structure of the mitochondrial creatine kinase octamer: High-resolution shadowing and image averaging of single molecules and formation of linear filaments under specific staining conditions. J Cell Biol 1991;112: 95-101.
42. Schnyder T, Cyrklaff M, Fuchs K, Wallimann T: Crystallization of mitochondrial creatine kinase on negatively charged lipid layers. J Struct Biol 1994;112:136-147.
43. Fritz-Wolf K, Schnyder T, Walli-mann T, Kabsch W: Structure of mitochondrial creatine kinase. Nature 1996;381:341-345.
44. Eder M, Fritz-Wolf K, Kabsch W, Wallimann T, Schlattner U: Crystal structure of human ubiquitous mitochondrial creatine kinase. Proteins 2000;39:216-225.
45. Schlattner U, Wallimann T: Octa-mers of mitochondrial creatine kinase isoenzymes differ in stability and membrane binding. J Biol Chem 2000;275:17314-17320.
46. Stachowiak O, Schlattner U, Dolder M, Wallimann T: Oligomeric state and membrane binding behaviour of creatine kinase isoenzymes: Implications for cellular function and mitochondrial structure. Mol Cell Biochem 1998;184:141-151.
47. Schlattner U, Forstner M, Eder M, Stachowiak O, Fritz-Wolf K, Walli-mann T: Functional aspects of the X-ray structure of mitochondrial creatine kinase: A molecular physiology approach. Mol Cell Biochem 1998;184:125-140.
48. Vacheron MJ, Clottes E, Chautard C, Vial C: Mitochondrial creatine kinase interaction with phospholipid vesicles. Arch Biochem Biophys 1997;344:316-324.
49. Stachowiak O, Dolder M, Walli-mann T: Membrane-binding and lipid vesicle cross-linking kinetics of the mitochondrial creatine kinase octamer. Biochemistry 1996;35: 15522-15528.
50. Rojo M, Hovius R, Demel R, Wallimann T, Eppenberger HM, Nicolay K: Interaction of mitochondrial creatine kinase with model membranes. A monolayer study. FEBS Lett 1991;281:123-129.
51. Rojo M, Hovius R, Demel RA, Ni-colay K, Wallimann T: Mitochondrial creatine kinase mediates contact formation between mitochondrial membranes. J Biol Chem 1991;266:20290-20295.
52. Schlegel J, Wyss M, Eppenberger HM, Wallimann T: Functional studies with the octameric and dimeric form of mitochondrial creatine kinase. Differential pH-dependent association of the two oligomeric forms with the inner mitochondrial membrane. J Biol Chem 1990;265: 9221-9227.
53. Sperka-Gottlieb CD, Hermetter A, Paltauf F, Daum G: Lipid topology and physical properties of the outer mitochondrial membrane of the yeast, Saccharomyces cerevisiae. Biochim Biophys Acta 1988;946: 227-234.
54. Ardail D, Privat JP, Egret-Charlier M, Levrat C, Lerme F, Louisot P: Mitochondrial contact sites. Lipid composition and dynamics. J Biol Chem 1990;265:18797-18802.
55. de Kroon AI, Dolis D, Mayer A, Lill R, de Kruijff B: Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa. Is car-diolipin present in the mitochondrial outer membrane? Biochim Biophys Acta 1997;1325:108-116.
56. Dekker PJ, Martin F, Maarse AC, Bomer U, Muller H, Guiard B, Meijer M, Rassow J, Pfanner N: The Tim core complex defines the number of mitochondrial translocation contact sites and can hold arrested preproteins in the absence of matrix Hsp70-Tim44. EMBO J 1997; 16: 5408-5419.
57. Bauer MF, Hofmann S, Neupert W, Brunner M: Protein translocation into mitochondria: The role of TIM complexes. Trends Cell Biol 2000; 10:25-31.
58. Neupert W: Protein import into mitochondria. Annu Rev Biochem 1997;66:863-917.
59. Simbeni R, Pon L, Zinser E, Paltauf F, Daum G: Mitochondrial membrane contact sites of yeast. Characterization of lipid components and possible involvement in intramitochondrial translocation of phospholipids. J Biol Chem 1991;266: 10047-10049.
60. Ardail D, Lerme F, Louisot P: Involvement of contact sites in phos-phatidylserine import into liver mitochondria. J Biol Chem 991;266: 7978-7981.
61. Ardail D, Lerme F, Louisot P: Phospholipid import into mitochondria: Possible regulation mediated through lipid polymorphism. Bio-chem Biophys Res Commun 1992; 186:1384-1390.
62. Xu FY, Hatch GM: Cytidine-5'-diphosphate-1,2-diacyl-sn-glycerol import into mitochondria through mitochondrial membrane contact sites in permeabilized rat liver hepa-tocytes. Biochem Biophys Res Com-mun 1997;232:261-265.
63. Culty M, Li H, Boujrad N, Amri H, Vidic B, Bernassau JM, Reversat JL, Papadopoulos V: In vitro studies on the role of the peripheral-type benzodiazepine receptor in steroidogenesis. J Steroid Biochem Mol Biol 1999;69:123-130.
64. Marzulli D, La Piana G, Fransvea E, Lofrumento NE: Modulation of cytochrome c-mediated extramitochondrial NADH oxidation by contact site density. Biochem Biophys Res Commun 1999;259:325-330.
65. Gellerich FN, Schlame M, Bohnen-sack R, Kunz W: Dynamic compart-mentation of adenine nucleotides in the mitochondrial intermembrane space of rat-heart mitochondria. Biochim Biophys Acta 1987;890: 117-126.
66. Gellerich FN, Khuchua ZA, Kuznetsov AV: Influence of the mitochondrial outer membrane and the binding of creatine kinase to the mitochondrial inner membrane on the compartmentation of adenine nucleotides in the intermembrane space of rat heart mitochondria. Biochim Biophys Acta 1993;1140: 327-334.
67. Brdiczka D: Function of the outer mitochondrial compartment in regulation of energy metabolism. Bio-chim Biophys Acta 1994; 1187:264-269.
68. Saks VA, Ventura-Clapier R, Aliev MK: Metabolic control and metabolic capacity: Two aspects of creatine kinase functioning in the cells. Biochim Biophys Acta 1996;1274: 81-88.
69. Brdiczka D, Wallimann T: The importance of the outer mitochondrial compartment in regulation of energy metabolism. Mol Cell Biochem 1994; 133/134:69-83.
70. Khuchua ZA, Qin W, Boero J, Cheng J, Payne RM, Saks VA, Strauss AW: Octamer formation and coupling of cardiac sarcomeric mitochondrial creatine kinase are mediated by charged N-terminal residues. J Biol Chem 1998;273: 22990-22996.
71. Soboll S, Brdiczka D, Jahnke D, Schmidt A, Schlattner U, Wendt S, Wyss M, Wallimann T: Octamer-dimer transitions of mitochondrial creatine kinase in heart disease. J Mol Cell Cardiol 1999;31:857-866.
72. Beutner G, Ruck A, Riede B, Welte W, Brdiczka D: Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett 1996;396:189-195.
73. Bucheler K, Adams V, Brdiczka D: Localization of the ATP/ADP translocator in the inner membrane and regulation of contact sites between mitochondrial envelope membranes by ADP. A study on freeze-fractured isolated liver mitochondria. Bio-chim Biophys Acta 1991; 1056:233-242.
74. Hackenberg H, Klingenberg M: Molecular weight and hydrodynamic parameters of the adenosine 5'-diphosphate-adenosine 5'-triphos-phate carrier in Triton X-100. Biochemistry 1980;19:548-555.
75. 31P nuclear magnetic resonance. Biochemistry 1985;24:3821-3826.
76. Hoffmann B, Stockl A, Schlame M, Beyer K, Klingenberg M: The reconstituted ADP/ATP carrier activity has an absolute requirement for car-diolipin as shown in cysteine mutants. J Biol Chem 1994;269:1940-1944.
77. Adams V, Bosch W, Schlegel J, Wal-limann T, Brdiczka D: Further characterization of contact sites from mitochondria of different tissues: Topology of peripheral kinases. Bio-chim Biophys Acta 1989;981:213-225.
78. Kottke M, Adam V, Riesinger I, Bremm G, Bosch W, Brdiczka D, Sandri G, Panfili E: Mitochondrial boundary membrane contact sites in brain: Points of hexokinase and creatine kinase location, and control of Ca2+ transport. Biochim Biophys Acta 1988;935:87-102.
79. Kottke M, Adams V, Wallimann T, Nalam VK, Brdiczka D: Location and regulation of octameric mitochondrial creatine kinase in the contact sites. Biochim Biophys Acta 1991;1061:215-225.
80. Kaldis P, Furter R, Wallimann T: The N-terminal heptapeptide of mitochondrial creatine kinase is important for octamerization. Biochemistry 1994;33:952-959.
81. Brdiczka D, Kaldis P, Wallimann T: In vitro complex formation between the octamer of mitochondrial creatine kinase and porin. J Biol Chem 1994;269:27640-27644.
82. Colombini M, Yeung CL, Tung J, Konig T: The mitochondrial outer membrane channel, VDAC, is regulated by a synthetic polyanion. Bio-chim Biophys Acta 1987;905:279-286.
83. Colombini M: Regulation of the mitochondrial outer membrane channel, VDAC. J Bioenerg Biomembr 1987;19:309-320.
84. Song J, Midson C, Blachly-Dyson E, Forte M, Colombini M: The topology of VDAC as probed by biotin modification. J Biol Chem 1998; 273:24406-24413.
85. Stanley S, Dias JA, D’arcangelis D, Mannella CA: Peptide-specific antibodies as probes of the topography of the voltage-gated channel in the mitochondrial outer membrane of Neurospora crassa. J Biol Chem 1995;270:16694-16700.
86. Song J, Midson C, Blachly-Dyson E, Forte M, Colombini M: The sensor regions of VDAC are translocated from within the membrane to the surface during the gating processes. Biophys J 1998;74:2926-2944.
87. Colombini M, Blachly-Dyson E, Forte M: VDAC, a channel in the outer mitochondrial membrane;in Narahashi T (ed): Ion Channels. New York, Plenum Press, 1996, vol 4, pp 169-202.
88. Liu MY, Torgrimson A, Colombini M: Characterization and partial purification of the VDAC-channel-mo-dulating protein from calf liver mitochondria. Biochim Biophys Acta 1994;1185:203-212.
89. Holden MJ, Colombini M: The outer mitochondrial membrane channel, VDAC, is modulated by a protein localized in the intermembrane space. Biochim Biophys Acta 1993; 1144:396-402.
90. Liu MY, Colombini M: Regulation of mitochondrial respiration by controlling the permeability of the outer membrane through the mitochondrial channel, VDAC. Biochim Biophys Acta 1992;1098:255-260.
91. Dolder M, Zeth K, Tittmann P, Gross H, Welte W, Wallimann T: Crystallization of the human, mitochondrial voltage-dependent anion-selective channel in the presence of phospholipids. J Struct Biol 1999; 127:64-71.
92. 2+-induced membrane transition in mitochondria. I. The protective mechanisms. Arch Biochem Bio-phys 1979;195:453-459.
93. 2+ trigger site. Arch Biochem Biophys 1979;195:460-467.
94. Zoratti M, Szabo I: The mitochondrial permeability transition. Bio-chim Biophys Acta 1995; 1241:139-176.
95. Bernardi P, Basso E, Colonna R, Costantini P, Di Lisa F, Eriksson O, Fontaine E, Forte M, Ichas F, Mas-sari S, Nicolli A, Petronilli V, Scor-rano L: Perspectives on the mitochondrial permeability transition. Biochim Biophys Acta 1998; 1365: 200-206.
96. Le Quoc K, Le Quoc D: Involvement of the ADP/ATP carrier in calcium-induced perturbations of the mitochondrial inner membrane permeability: Importance of the orientation of the nucleotide binding site. Arch Biochem Biophys 1988;265: 249-257.
97. 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. Bio-chem J 1990;268:153-160.
98. Halestrap AP, Woodfield KY, Con-nern CP: Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J Biol Chem 1997;272:3346-3354.
99. Hashimoto M, Majima E, Goto S, Shinohara Y, Terada H: Fluctuation of the first loop facing the matrix of the mitochondrial ADP/ ATP carrier deduced from intermolecular cross-linking of Cys56 residues by bifunctional dimaleim-ides. Biochemistry 1999;38:1050-1056.
100. Majima E, Ikawa K, Takeda M, Hashimoto M, Shinohara Y, Ter-ada H: Translocation of loops regulates transport activity of mitochondrial ADP/ATP carrier deduced from formation of a specific intermolecular disulfide bridge catalyzed by copper-o-phenan-throline. J Biol Chem 1995;270: 29548-29554.
101. Brustovetsky N, Becker A, Klin-genberg M, Bamberg E: Electrical currents associated with nucleotide transport by the reconstituted mitochondrial ADP/ATP carrier. Proc Natl Acad Sci USA 1996;93: 664-668.
102. Klingenberg M: The ADP/ATP Carrier in Mitochondrial Membranes; in Martonosi AN (ed): The Enzymes of Biological Membranes. New York, Plenum, 1985, vol 4, pp 511-553.
103. Petronilli V, Cola C, Massari S, Colonna R, Bernardi P: Physiological effectors modify voltage sensing by the cyclosporin A-sensitive permeability transition pore of mitochondria. J Biol Chem 1993;268: 21939-21945.
104. Scorrano L, Petronilli V, Bernardi P: On the voltage dependence of the mitochondrial permeability transition pore. A critical appraisal. J Biol Chem 1997;272:12295-12299.
105. Szabo I, Bernardi P, Zoratti M: Modulation of the mitochondrial megachannel by divalent cations and protons. J Biol Chem 1992; 267:2940-2946.
106. Lohret TA, Murphy RC, Drgon T, Kinnally KW: Activity of the mitochondrial multiple conductance channel is independent of the adenine nucleotide translocator. J Biol Chem 1996;271:4846-4849.
107. Fontaine E, Eriksson O, Ichas F, Bernardi P: Regulation of the permeability transition pore in skeletal muscle mitochondria. Modulation by electron flow through the respiratory chain complex I. J Biol Chem 1998;273:12662-12668.
108. Fontaine E, Ichas F, Bernardi P: A ubiquinone-binding site regulates the mitochondrial permeability transition pore. J Biol Chem 1998; 273:25734-25740.
109. Tikhonova IM, Andreyev A, Antonenko Yu N, Kaulen AD, Komra-kov A, Skulachev VP: Ion permeability induced in artificial membranes by the ATP/ADP antiporter. FEBS Lett 1994;337:231-234.
110. Dierks T, Salentin A, Kramer R: Pore-like and carrier-like properties of the mitochondrial aspartate/ glutamate carrier after modification by SH-reagents: Evidence for a performed channel as a structural requirement of carrier-mediated transport. Biochim Biophys Acta 1990;1028:281-288.
111. Dierks T, Salentin A, Heberger C, Kramer R: The mitochondrial aspartate/glutamate and ADP/ ATP carrier switch from obligate counterexchange to unidirectional transport after modification by SH-reagents. Biochim Biophys Acta 1990;1028:268-280.
112. Petronilli V, Nicolli A, Costantini P, Colonna R, Bernardi P: Regulation of the permeability transition pore, a voltage-dependent mitochondrial channel inhibited by cyclosporin A. Biochim Biophys Acta 1994;1187:255-259.
113. 2+ binding sites with opposing effects on the pore open probability. J Biol Chem 1993;268:1005-1010.
114. Griffiths EJ, Halestrap AP: Further evidence that cyclosporin A protects mitochondria from calcium overload by inhibiting a matrix peptidyl-prolyl cis-trans iso-merase. Implications for the immunosuppressive and toxic effects of cyclosporin. Biochem J 1991; 274:611-614.
115. Connern CP, Halestrap AP: Recruitment of mitochondrial cyclo-philin to the mitochondrial inner membrane under conditions of oxidative stress that enhance the opening of a calcium-sensitive non-specific channel. Biochem J 1994;302:321-324.
116. Woodfield K, Ruck A, Brdiczka D, Halestrap AP: Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Bio-chem J 1998;336:287-290.
117. Brenner C, Cadiou H, Vieira HL, Zamzami N, Marzo I, Xie Z, Leber B, Andrews D, Duclohier H, Reed JC, Kroemer G: Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator. Oncogene 2000;19: 329-336.
118. Narita M, Shimizu S, Ito T, Chittenden T, Lutz RJ, Matsuda H, Tsujimoto Y: Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Natl Acad Sci USA 1998;95:14681-14686.
119. Shimizu S, Eguchi Y, Kamiike W, Funahashi Y, Mignon A, Lacroni-que V, Matsuda H, Tsujimoto Y: Bcl-2 prevents apoptotic mitochondrial dysfunction by regulating proton flux. Proc Natl Acad Sci USA 1998;95:1455-1459.
120. Snyder JW, Pastorino JG, Attie AM, Farber JL: Protection by cyclosporin A of cultured hepato-cytes from the toxic consequences of the loss of mitochondrial energization produced by 1-methyl-4-phenylpyridinium. Biochem Pharmacol 1992;44:833-835.
121. Pastorino JG, Snyder JW, Serroni A, Hoek JB, Farber JL: Cyclosporin and carnitine prevent the anoxic death of cultured hepato-cytes by inhibiting the mitochondrial permeability transition. J Biol Chem 1993;268:13791-13798.
122. Obatomi DK, Bach PH: Selective cytotoxicity associated with in vitro exposure of fresh rat renal fragments and continuous cell lines to atractyloside. Arch Toxicol 1996; 71:93-98.
123. Koya RC, Fujita H, Shimizu S, Ohtsu M, Takimoto M, Tsujimoto Y, Kuzumaki N: Gelsolin inhibits apoptosis by blocking mitochondrial membrane potential loss and cytochrome c release. J Biol Chem 2000;275:15343-15349.
124. Hirsch T, Dallaporta B, Zamzami N, Susin SA, Ravagnan L, Marzo I, Brenner C, Kroemer G: Protea-some activation occurs at an early, premitochondrial step of thymocyte apoptosis. J Immunol 1998; 161:35-40.
125. Marchetti P, Hirsch T, Zamzami N, Castedo M, Decaudin D, Susin SA, Masse B, Kroemer G: Mitochondrial permeability transition triggers lymphocyte apoptosis. J Immunol 1996;157:4830-4836.
126. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, Haeffner A, Hirsch F, Geuskens M, Kroemer G: Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 1996;184:1155-1160.
127. Gross M, Wallimann T: Kinetics of assembly and dissociation of the mitochondrial creatine kinase oc-tamer. A fluorescence study. Biochemistry 1993;32:13933-13940.
128. O’gorman E, Beutner G, Dolder M, Koretsky AP, Brdiczka D, Wal-limann T: The role of creatine kinase in inhibition of mitochondrial permeability transition. FEBS Lett 1997;414:253-257.
129. Brdiczka D, Beutner G, Ruck A, Dolder M, Wallimann T: The molecular structure of mitochondrial contact sites. Their role in regulation of energy metabolism and permeability transition. Biofactors 1998;8:235-242.
130. Boehm EA, Radda GK, Tomlin H, Clark JF: The utilisation of creatine and its analogues by cytosolic and mitochondrial creatine kinase. Biochim Biophys Acta 1996;1274: 119-128.
131. Forstner M, Kriechbaum M, Lagg-ner P, Wallimann T: Structural changes of creatine kinase upon substrate binding. Biophys J 1998; 75:1016-1023.
132. Marzo I, Brenner C, Zamzami N, Susin SA, Beutner G, Brdiczka D, Remy R, Xie ZH, Reed JC, Kroe-mer G: The permeability transition pore complex: A target for apoptosis regulation by caspases and bcl-2-related proteins. J Exp Med 1998;187:1261-1271.
133. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC, Kroemer G: Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 1998; 281:2027-2031.
134. Beutner G, Ruck A, Riede B, Brdiczka D: Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases. Biochim Biophys Acta 1998;1368: 7-18.
135. Novgorodov SA, Gudz TI, Brierley GP, Pfeiffer DR: Magnesium ion modulates the sensitivity of the mitochondrial permeability transition pore to cyclosporin A and ADP. Arch Biochem Biophys 1994;311:219-228.
136. Kaul N, Siveski-Iliskovic N, Hill M, Slezak J, Singal PK: Free radicals and the heart. J Pharmacol Toxicol Methods 1993;30:55-67.
137. Kehrer JP: Free radicals as mediators of tissue injury and disease. Crit Rev Toxicol 1993;23:21-48.
138. Liu P, Hock CE, Nagele R, Wong P: Formation of nitric oxide, superoxide, and peroxynitrite in myocardial ischemia-reperfusion injury in rats. Am J Physiol 1997; 272:H2327-H2336.
139. Yuan G, Kaneko M, Masuda H, Hon RB, Kobayashi A, Yamazaki N: Decrease in heart mitochondrial creatine kinase activity due to oxygen free radicals. Biochim Biophys Acta 1992;1140:78-84.
140. Thomas C, Carr AC, Winterbourn CC: Free radical inactivation of rabbit muscle creatine kinase: Catalysis by physiological and hydrolyzed ICRF-187 (ICRF-198) iron chelates. Free Radic Res 1994;21: 387-397.
141. Arstall MA, Bailey C, Gross WL, Bak M, Balligand JL, Kelly RA: Reversible S-nitrosation of creatine kinase by nitric oxide in adult rat ventricular myocytes. J Mol Cell Cardiol 1998;30:979-988.
142. Gross WL, Bak MI, Ingwall JS, Ar-stall MA, Smith TW, Balligand JL, Kelly RA: Nitric oxide inhibits creatine kinase and regulates rat heart contractile reserve. Proc Natl Acad Sci USA 1996;93:5604-5609.
143. Kaasik A, Minajeva A, De Sousa E, Ventura-Clapier R, Veksler V: Nitric oxide inhibits cardiac energy production via inhibition of mitochondrial creatine kinase. FEBS Lett 1999;444:75-77.
144. Konorev EA, Hogg N, Kalyanara-man B: Rapid and irreversible inhibition of creatine kinase by pe-roxynitrite. FEBS Lett 1998;427: 171-174.
145. Stachowiak O, Dolder M, Walli-mann T, Richter C: Mitochondrial creatine kinase is a prime target of peroxynitrite-induced modification and inactivation. J Biol Chem 1998;273:16694-16699.
146. Ghafourifar P, Richter C: Nitric oxide synthase activity in mitochondria. FEBS Lett 1997;418: 291-296.
147. Radi R, Rodriguez M, Castro L, Telleri R: Inhibition of mitochondrial electron transport by peroxy-nitrite. Arch Biochem Biophys 1994;308:89-95.
148. Castro L, Rodriguez M, Radi R: Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J Biol Chem 1994;269:29409-29415.
149. Rubbo H, Denicola A, Radi R: Peroxynitrite inactivates thiol-containing enzymes of Trypanosoma cruzi energetic metabolism and inhibits cell respiration. Arch Biochem Biophys 1994;308:96-102.
150. 2+ release from intact rat liver mitochondria. Biochemistry 1996;35:4524-4528.
151. Padmaja S, Ramezanian MS, Bounds PL, Koppenol WH: Reactions of peroxynitrite with L-tryp-tophan. Redox Report 1996;2: 173-177.
152. Lymar SV, Jiang Q, Hurst JK: Mechanism of carbon dioxide-catalyzed oxidation of tyrosine by peroxynitrite. Biochemistry 1996; 35:7855-7861.
153. Denicola A, Rubbo H, Rodriguez D, Radi R: Peroxynitrite-mediated cytotoxicity to Trypanosoma cruzi. Arch Biochem Biophys 1993;304: 279-286.
154. Koufen P, Stark G: Free radical induced inactivation of creatine kinase: Sites of interaction, protection, and recovery. Biochim Bio-phys Acta 2000; 1501:44-50.
155. Koufen P, Ruck A, Brdiczka D, Wendt S, Wallimann T, Stark G: Free radical-induced inactivation of creatine kinase: Influence on the octameric and dimeric states of the mitochondrial enzyme (Mib-CK). Biochem J 1999;344:413-417.
156. Steenbergen C, Murphy E, Watts JA, London RE: Correlation between cytosolic free calcium, contracture, ATP, and irreversible ischemic injury in perfused rat heart. Circ Res 1990;66:135-146.
157. Kammermeier H, Schmidt P, Jun-gling E: Free energy change of ATP-hydrolysis: A causal factor of early hypoxic failure of the myocardium? J Mol Cell Cardiol 1982; 14:267-277.
158. Murphy E, Perlman M, London RE, Steenbergen C: Amiloride delays the ischemia-induced rise in cytosolic free calcium. Circ Res 1991;68:1250-1258.
159. Piper HM, Siegmund B, Ladilov Yu V, Schluter KD: Calcium and sodium control in hypoxic-reoxy-genated cardiomyocytes. Basic Res Cardiol 1993;88:471-482.
160. 2+-induced inhibition of substrate oxidation. Biochim Biophys Acta 1999;1453:41-48.
161. Crompton M: The mitochondrial permeability transition pore and its role in cell death. Biochem J 1999;341:233-249.
162. Halestrap AP, Kerr PM, Javadov S, Woodfield KY: Elucidating the molecular mechanism of the permeability transition pore and its role in reperfusion injury of the heart. Biochim Biophys Acta 1998; 1366:79-94.
163. Griffiths EJ, Halestrap AP: Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J 1995;307:93-98.
164. McCord JM, Turrens JF: Mitochondrial injury by ischemia and reperfusion. Curr Top Bioenerg 1994;17:173-195.
165. Eppenberger HM: A brief summary of the history of the detection of creatine kinase isoenzymes. Mol Cell Biochem 1994; 133-134:911.
166. Greenhaff PL: The nutritional biochemistry of creatine. J Nutr Biochem 1997;8:610-618.
167. Wallimann T, Schlattner U, Guerrero L, Dolder M: The phospho-creatine circuit and creatine supplementation, both come of age; in Mori A, Ishida M, Clark JF (eds): Guanidino Compounds in Biology and Medicine. Tokyo, Blackwell Science Japan KK, 1999, vol 5, pp 117-129.
168. 2+ handling and survival in mdx skeletal muscle cells. FEBS Lett 1998;439:357-362.
169. Matthews RT, Yang L, Jenkins BG, Ferrante RJ, Rosen BR, Kad-durah-Daouk R, Beal MF: Neuroprotective effects of creatine and cyclocreatine in animal models of Huntington’s disease. J Neurosci 1998;18:156-163.