Inhibition of complex i regulates the mitochondrial permeability transition through a phosphate-sensitive inhibitory site masked by cyclophilin D

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 9, 2012, Pages 1628-1634

  Li, Bo ^a   Chauvin, Christiane ^b   De Paulis, Damien ^a   De Oliveira, Frédéric ^b   Gharib, Abdallah ^a   Vial, Guillaume ^b   Lablanche, Sandrine ^b,c   Leverve, Xavier ^b   Bernardi, Paolo ^d   Ovize, Michel ^a,e   Fontaine, Eric ^b,c  

^a UNIVERSITÉ LYON 1   (France)

^b INSERM   (France)

^c GRENOBLE UNIVERSITY HOSPITAL   (France)

^d UNIVERSITY OF PADOVA   (Italy)

^e LOUIS PRADEL HOSPITAL   (France)

Author keywords

Cyclophilin D; Cyclosporin A; Metformin; Mitochondria; Permeability transition; Rotenone

Indexed keywords

CALCIUM ION; CYCLOPHILIN D; CYCLOSPORIN; METFORMIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENZYME INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; CYCLOPHILINS; CYCLOSPORINE; ELECTRON TRANSPORT COMPLEX I; HUMANS; METFORMIN; MICE; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; ROTENONE;

EID: 84862247742     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.05.011     Document Type: Article

References (44)

1. M. Zoratti, and I. Szabo The mitochondrial permeability transition Biochim. Biophys. Acta 1241 1995 139 176
2. C.P. Baines, R.A. Kaiser, N.H. Purcell, N.S. Blair, H. Osinska, M.A. Hambleton, E.W. Brunskill, M.R. Sayen, R.A. Gottlieb, G.W. Dorn, J. Robbins, and J.D. Molkentin Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death Nature 434 2005 658 662 (Pubitemid 40488559)
3. E. Basso, L. Fante, J. Fowlkes, V. Petronilli, M.A. Forte, and P. Bernardi Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D J. Biol. Chem. 280 2005 18558 18561 (Pubitemid 41379552)
4. T. Nakagawa, S. Shimizu, T. Watanabe, O. Yamaguchi, K. Otsu, H. Yamagata, H. Inohara, T. Kubo, and Y. Tsujimoto Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death Nature 434 2005 652 658 (Pubitemid 40488558)
5. A.C. Schinzel, O. Takeuchi, Z. Huang, J.K. Fisher, Z. Zhou, J. Rubens, C. Hetz, N.N. Danial, M.A. Moskowitz, and S.J. Korsmeyer Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia Proc. Natl. Acad. Sci. U. S. A. 102 2005 12005 12010 (Pubitemid 41291119)
6. C.P. Connern, and A.P. Halestrap Chaotropic agents and increased matrix volume enhance binding of mitochondrial cyclophilin to the inner mitochondrial membrane and sensitize the mitochondrial permeability transition to [Ca2+] Biochemistry 35 1996 8172 8180 (Pubitemid 26234917)
7. A. Nicolli, E. Basso, V. Petronilli, R.M. Wenger, and P. Bernardi Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, and cyclosporin A-sensitive channel J. Biol. Chem. 271 1996 2185 2192 (Pubitemid 26047809)
8. E. Basso, V. Petronilli, M.A. Forte, and P. Bernardi Phosphate is essential for inhibition of the mitochondrial permeability transition pore by cyclosporin A and by cyclophilin D ablation J. Biol. Chem. 283 2008 26307 26311
9. S. Desagher, and J.C. Martinou Mitochondria as the central control point of apoptosis Trends Cell Biol. 10 2000 369 377 (Pubitemid 30612469)
10. C. Piot, P. Croisille, P. Staat, H. Thibault, G. Rioufol, N. Mewton, R. Elbelghiti, T.T. Cung, E. Bonnefoy, D. Angoulvant, C. Macia, F. Raczka, C. Sportouch, G. Gahide, G. Finet, X. Andre-Fouet, D. Revel, G. Kirkorian, J.P. Monassier, G. Derumeaux, and M. Ovize Effect of cyclosporine on reperfusion injury in acute myocardial infarction N. Engl. J. Med. 359 2008 473 481
11. D. Detaille, B. Guigas, C. Chauvin, C. Batandier, E. Fontaine, N. Wiernsperger, and X. Leverve Metformin prevents high-glucose-induced endothelial cell death through a mitochondrial permeability transition-dependent process Diabetes 54 2005 2179 2187 (Pubitemid 40911282)
12. M.Y. El-Mir, V. Nogueira, E. Fontaine, N. Averet, M. Rigoulet, and X. Leverve Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I J. Biol. Chem. 275 2000 223 228 (Pubitemid 30038975)
13. B. Guigas, D. Detaille, C. Chauvin, C. Batandier, F. De Oliveira, E. Fontaine, and X. Leverve Metformin inhibits mitochondrial permeability transition and cell death: a pharmacological in vitro study Biochem. J. 382 2004 877 884 (Pubitemid 39312902)
14. C. Chauvin, F. De Oliveira, X. Ronot, M. Mousseau, X. Leverve, and E. Fontaine Rotenone inhibits the mitochondrial permeability transition-induced cell death in U937 and KB cells J. Biol. Chem. 276 2001 41394 41398
15. S. Lablanche, C. Cottet-Rousselle, F. Lamarche, P.Y. Benhamou, S. Halimi, X. Leverve, and E. Fontaine Protection of pancreatic INS-1 beta-cells from glucose- and fructose-induced cell death by inhibiting mitochondrial permeability transition with cyclosporin A or metformin Cell Death Dis. 2 2011 e134
16. A.K. Groen, H.J. Sips, R.C. Vervoorn, and J.M. Tager Intracellular compartmentation and control of alanine metabolism in rat liver parenchymal cells Eur. J. Biochem. 122 1982 87 93 (Pubitemid 12142822)
17. O. Gateau-Roesch, E. Pavlov, A.V. Lazareva, E.A. Limarenko, C. Levrat, N.E. Saris, P. Louisot, and G.D. Mironova Calcium-binding properties of the mitochondrial channel-forming hydrophobic component J. Bioenerg. Biomembr. 32 2000 105 110 (Pubitemid 30241263)
18. J. Benard, J. Da Silva, M.C. De Blois, P. Boyer, P. Duvillard, E. Chiric, and G. Riou Characterization of a human ovarian adenocarcinoma line, IGROV1, in tissue culture and in nude mice Cancer Res. 45 1985 4970 4979 (Pubitemid 16236181)
19. E. Galiana, I. Borde, P. Marin, M. Rassoulzadegan, F. Cuzin, F. Gros, P. Rouget, and C. Evrard Establishment of permanent astroglial cell lines, able to differentiate in vitro, from transgenic mice carrying the polyoma virus large T gene: an alternative approach to brain cell immortalization J. Neurosci. Res. 26 1990 269 277 (Pubitemid 20264019)
20. E. Fontaine, O. Eriksson, F. Ichas, and P. Bernardi Regulation of the permeability transition pore in skeletal muscle mitochondria. Modulation by electron flow through the respiratory chain complex i J. Biol. Chem. 273 1998 12662 12668 (Pubitemid 28240645)
21. E. Fontaine, F. Ichas, and P. Bernardi A ubiquinone-binding site regulates the mitochondrial permeability transition pore J. Biol. Chem. 273 1998 25734 25740 (Pubitemid 28475797)
22. P. Bernardi Mitochondrial transport of cations: channels, exchangers, and permeability transition Physiol. Rev. 79 1999 1127 1155 (Pubitemid 29473313)
23. D.R. Green, and G. Kroemer The pathophysiology of mitochondrial cell death Science 305 2004 626 629 (Pubitemid 39006738)
24. V. Giorgio, M.E. Soriano, E. Basso, E. Bisetto, G. Lippe, M.A. Forte, and P. Bernardi Cyclophilin D in mitochondrial pathophysiology Biochim. Biophys. Acta 1797 2010 1113 1118
25. V. Giorgio, E. Bisetto, M.E. Soriano, F. Dabbeni-Sala, E. Basso, V. Petronilli, M.A. Forte, P. Bernardi, and G. Lippe Cyclophilin D modulates mitochondrial F0F1-ATP synthase by interacting with the lateral stalk of the complex J. Biol. Chem. 284 2009 33982 33988
26. K. Woodfield, A. Ruck, D. Brdiczka, and A.P. Halestrap 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 Pt 2 1998 287 290 (Pubitemid 28564382)
27. J.E. Kokoszka, K.G. Waymire, S.E. Levy, J.E. Sligh, J. Cai, D.P. Jones, G.R. MacGregor, and D.C. Wallace The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore Nature 427 2004 461 465 (Pubitemid 38168501)
28. B.H. Kang, J. Plescia, T. Dohi, J. Rosa, S.J. Doxsey, and D.C. Altieri Regulation of tumor cell mitochondrial homeostasis by an organelle-specific Hsp90 chaperone network Cell 131 2007 257 270 (Pubitemid 47576138)
29. R.A. Eliseev, J. Malecki, T. Lester, Y. Zhang, J. Humphrey, and T.E. Gunter Cyclophilin D interacts with Bcl2 and exerts an anti-apoptotic effect J. Biol. Chem. 284 2009 9692 9699
30. V.G. Grivennikova, A.N. Kapustin, and A.D. Vinogradov Catalytic activity of NADH-ubiquinone oxidoreductase (complex I) in intact mitochondria. evidence for the slow active/inactive transition J. Biol. Chem. 276 2001 9038 9044
31. V.G. Grivennikova, A.B. Kotlyar, J.S. Karliner, G. Cecchini, and A.D. Vinogradov Redox-dependent change of nucleotide affinity to the active site of the mammalian complex I Biochemistry 46 2007 10971 10978 (Pubitemid 47463048)
32. A.D. Vinogradov, and V.G. Grivennikova The mitochondrial complex I: progress in understanding of catalytic properties IUBMB Life 52 2001 129 134 (Pubitemid 33731565)
33. G.C. Brown, and V. Borutaite Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols Biochim. Biophys. Acta 1658 2004 44 49 (Pubitemid 39013232)
34. S. Papa, S. Scacco, D. De Rasmo, A. Signorile, F. Papa, D. Panelli, A. Nicastro, R. Scaringi, A. Santeramo, E. Roca, R. Trentadue, and M. Larizza cAMP-dependent protein kinase regulates post-translational processing and expression of complex I subunits in mammalian cells Biochim. Biophys. Acta 1797 2010 649 658
35. D.M. Nathan, J.B. Buse, M.B. Davidson, E. Ferrannini, R.R. Holman, R. Sherwin, and B. Zinman Medical management of hyperglycemia in type 2 diabetes: a consensus algorithm for the initiation and adjustment of therapy: a consensus statement of the American Diabetes Association and the European Association for the Study of Diabetes Diabetes Care 32 2009 193 203
36. C. Lamanna, M. Monami, N. Marchionni, and E. Mannucci Effect of metformin on cardiovascular events and mortality: a meta-analysis of randomized clinical trials Diabetes Obes. Metab. 13 2011 221 228
37. E. Selvin, S. Bolen, H.C. Yeh, C. Wiley, L.M. Wilson, S.S. Marinopoulos, L. Feldman, J. Vassy, R. Wilson, E.B. Bass, and F.L. Brancati Cardiovascular outcomes in trials of oral diabetes medications: a systematic review Arch. Intern. Med. 168 2008 2070 2080
38. B. Viollet, B. Guigas, N. Sanz Garcia, J. Leclerc, M. Foretz, and F. Andreelli Cellular and molecular mechanisms of metformin: an overview Clin. Sci. (Lond.) 122 2012 253 270
39. M. Foretz, S. Hebrard, J. Leclerc, E. Zarrinpashneh, M. Soty, G. Mithieux, K. Sakamoto, F. Andreelli, and B. Viollet Metformin inhibits hepatic gluconeogenesis in mice independently of the LKB1/AMPK pathway via a decrease in hepatic energy state J. Clin. Invest. 120 2010 2355 2369
40. S.A. Hinke, G.A. Martens, Y. Cai, J. Finsi, H. Heimberg, D. Pipeleers, and M. Van de Casteele Methyl succinate antagonises biguanide-induced AMPK-activation and death of pancreatic beta-cells through restoration of mitochondrial electron transfer Br. J. Pharmacol. 150 2007 1031 1043 (Pubitemid 46625097)
41. K. Fujimoto, Y. Chen, K.S. Polonsky, and G.W. Dorn II Targeting cyclophilin D and the mitochondrial permeability transition enhances beta-cell survival and prevents diabetes in Pdx1 deficiency Proc. Natl. Acad. Sci. U. S. A. 107 2010 10214 10219
42. U. Ahlgren, J. Jonsson, L. Jonsson, K. Simu, and H. Edlund Beta-cell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the beta-cell phenotype and maturity onset diabetes Genes Dev. 12 1998 1763 1768 (Pubitemid 28304328)
43. J.D. Johnson, N.T. Ahmed, D.S. Luciani, Z. Han, H. Tran, J. Fujita, S. Misler, H. Edlund, and K.S. Polonsky Increased islet apoptosis in Pdx1+/- mice J. Clin. Invest. 111 2003 1147 1160 (Pubitemid 36519932)
44. R.N. Kulkarni, U.S. Jhala, J.N. Winnay, S. Krajewski, M. Montminy, and C.R. Kahn PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance J. Clin. Invest. 114 2004 828 836 (Pubitemid 39578742)