Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore

Biochemical Journal

Volumn 367, Issue 2, 2002, Pages 541-548

  McStay, Gavin P ^a   Clarke, Samantha J ^a   Halestrap, Andrew P ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Apoptosis; Cell death; Cyclophilin D; Diamide; Oxidative stress; Phenylarsine oxide

Indexed keywords

CONFORMATIONS; CROSSLINKING; ENZYME INHIBITION; STRESSES;

TRANSITION PORES;

BIOCHEMISTRY;

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ADENINE NUCLEOTIDE TRANSLOCASE; ARSENOSOBENZENE; CALCIUM ION; CYCLOPHILIN; CYCLOPHILIN D; CYSTEINE; DIAMIDE; EOSIN 5 MALEIMIDE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MALEIMIDE DERIVATIVE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; THIOL DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING KINETICS; CALCIUM TRANSPORT; CHANNEL GATING; CONTROLLED STUDY; ENZYME MECHANISM; INHIBITION KINETICS; MALE; MEMBRANE CHANNEL; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MOLECULAR INTERACTION; MOLECULAR STABILITY; NONHUMAN; OXIDATIVE STRESS; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN MODIFICATION; RAT; SOLUBILITY; SURFACE PROPERTY;

ADENOSINE DIPHOSPHATE; ANIMALS; ARSENICALS; CHROMATOGRAPHY, AFFINITY; CROSS-LINKING REAGENTS; CYCLOPHILINS; CYSTEINE; DIAMIDE; DIMERIZATION; EOSINE YELLOWISH-(YS); GLUTATHIONE TRANSFERASE; INTRACELLULAR MEMBRANES; MALE; MITOCHONDRIA; MITOCHONDRIAL ADP, ATP TRANSLOCASES; OXIDATIVE STRESS; PERMEABILITY; PHENANTHROLINES; RATS; RATS, WISTAR; SULFHYDRYL COMPOUNDS; SULFHYDRYL REAGENTS;

ANIMALIA; FORMICIDAE;

EID: 0037109064     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20011672     Document Type: Article

References (35)

1. Halestrap, A. P., Kerr, P. M., Javadov, S. and Woodfield, K. Y. (1998) Elucidating the molecular mechanism of the permeability transition pore and its role in reperfusion injury of the heart. Biochim. Biophys. Acta 1366, 79-94
2. Crompton, M. (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341, 233-249
3. Bernardi, P. (1999) Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev. 79, 1127-1155
4. Halestrap, A. P., Doran, E., Gillespie, J. P. and O'Toole, A. (2000) Mitochondria and cell death. Biochem. Soc. Trans 28, 170-177
5. Kroemer, G. and Reed, J. C. (2000) Mitochondrial control of cell death. Nat. Med. 6, 513-519
6. Martinou, J. C. and Green, D. R. (2001) Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell Biol. 2, 63-67
7. Bernardi, P., Petronilli, V., DiLisa, F. and Forte, M. (2001) A mitochondrial perspective on cell death. Trends Biochem. Sci. 26, 112-117
8. Woodfield, K., Rück, A., Brdiczka, D. and Halestrap, A. P. (1998) Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochem. J. 336, 287-290
9. 2+-induced large amplitude swelling of liver and heart mitochondria by cyclosporin A is probably caused by the inhibitor binding to mitochondrial matrix peptidylprolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem. J. 268, 153-160
10. Connern, C. P. and Halestrap, A. P. (1992) Purification and N-terminal sequencing of peptidylprolyl cis-trans isomerase from rat liver mitochondrial matrix reveals the existence of a distinct mitochondrial cyclophilin. Biochem. J. 284, 381-385
11. Halestrap, A. P., Woodfield, K. Y. and Connern, C. P. (1997) Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J. Biol. Chem. 272, 3346-3354
12. Connern, C. P. and Halestrap, A. P. (1994) 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, 321-324
13. 2+-dependent pore activated by oxidative stress in heart mitochondria Biochem. J. 245, 915-918
14. Costantini, P., Chernyak, B. V., Petronilli, V. and Bernardi, P. (1995) Selective inhibition of the mitochondrial permeability transition pore at the oxidation-reduction sensitive dithiol by monobromobimane. FEBS Lett. 362, 239-242
15. Costantini, P., Chernyak, B. V., Petronilli, V. and Bernardi, P. (1996) Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol, Chem. 271, 6746-6751
16. Chernyak, B. V. and Bernardi, P. (1996) The mitochondrial permeability transition pore is modulated by oxidative agents through both pyridine nucleotides and glutathione at two separate sites. Eur. J. Biochem. 238, 623-630
17. Owen, M. R., Doran, E. and Halestrap, A. P. (2000) Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem. J. 348, 607-614
18. Poole, R. C. and Halestrap, A. P. (1997) Interaction of the erythrocyte lactate transporter (monocarboxylate transporter 1) with an integral 70-kDa membrane glycoprotein of the immunoglobulin superfamily. J. Biol. Chem. 272, 14624-14628
19. 2+], Biochemistry 35, 8172-8180
20. Majima, E., Shinohara, Y., Yamaguchi, N., Hong, Y. M. and Terada, H. (1994) Importance of loops of mitochondrial ADP/ATP carrier for its transport activity deduced from reactivities of its cysteine residues with the sulfhydryl reagent eosin-5-maleimide. Biochemistry 33, 9530-9536
21. Majima, E, Koike, H., Hong, Y. M., Shinohara, Y. and Terada, H. (1993) Characterization of cysteine residues of mitochondrial ADP/ATP carrier with the SH-reagents eosin 5-maleimide and N-ethylmaleimide. J. Biol. Chem. 268, 22181-22187
22. Majima, E., Yamaguchi, N., Chuman, H., Shinohara, Y., Ishida, M., Goto, S. and Terada, H. (1998) Binding of the fluorescein derivative eosin Y to the mitochondrial ADP/ATP carrier: Characterization of the adenine nucleotide binding site. Biochemistry 37, 424-432
23. Costantini, P., Belzacq, A. S., LaVieira, H., Larochette, N., dePablo, M. A., Zamzami, N., Susin, S. A., Brenner, C. and Kroemer, G. (2000) Oxidation of a critical thiol residue of the adenine nucleotide translocator enforces Bcl-2-independent permeability transition pore opening and apoptosis. Oncogene 19. 307-314
24. Thomas, A. P. and Halestrap, A. P. (1981) Identification of the protein responsible for pyruvate transport into rat liver and heart mitochondria by specific labelling with N-phenylmaleimide. Biochem. J. 196, 471-479
25. Aquila, H. and Klingenberg, M. (1982) The reactivity of -SH groups in the ADP/ATP carrier isolated from beef heart mitochondria. Eur. J. Biochem. 122, 141-145
26. 3H]ethylmaleimide. Eur. J. Biochem. 122, 133-139
27. Crompton, M., Virji, S. and Ward, J. M. (1998) Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. Eur. J. Biochem. 258, 729-735
28. Klingenberg, M., Winkler, E. and Huang, S. G. (1995) ADP/ATP carrier and uncoupling protein. Methods Enzymol. 260, 369-389
29. Torok, K. and Joshi, S. (1985) Formation of an intramolecular disulfide bond in the mitochondrial adenine nucleotide translocase. FEBS Lett. 182, 340-344
30. Majima, E., Takeda, M., Miki, S., Shinohara, Y. and Terada, H. (2002) Close location of the first loop to the third loop of the mitochondrial ADP/ATP carrier deduced from cross-linking catalyzed by copper-o-phenanthroline of the solubilized carrier with Triton X-100. J, Biochem. (Tokyo) 131, 461-468
31. Majima, E., Ikawa, K., Takeda, M., Hashimoto, M., Shinohara, Y. and Terada, H. (1995) Translocation of loops regulates transport activity of mitochondrial ADP-ATP carrier deduced from formation of a specific intermolecular disulfide bridge catalyzed by copper-o-phenanthroline. J. Biol. Chem. 270, 29548-29554
32. Rigobello, M. P., Turcato, F. and Bindoli, A. (1995) Inhibition of rat liver mitochondrial permeability transition by respiratory substrates. Arch. Biochem. Biophys. 319, 225-230
33. Bindoli, A., Callegaro, M. T., Barzon, E., Benetti, M. and Rigobello, M. P. (1997) Influence of the redox state of pyridine nucleotides on mitochondrial sulfhydryl groups and permeability transition. Arch. Biochem. Biophys. 342, 22-28
34. Wudarczyk, J., Debska, G. and Lenartowicz, E. (1996) Relation between the activities reducing disulfides and the protection against membrane permeability transition in rat liver mitochondria. Arch. Biochem. Biophys. 327, 215-221
35. 2+-induced permeabilization of rat liver mitochondria. Biochem. J. 239, 19-29