Mitochondrial permeability transition and cell death: The role of cyclophilin D

Frontiers in Physiology

Volumn 4 APR, Issue , 2013, Pages

  Javadov, Sabzali ^a   Kuznetsov, Andrey ^b  

^a UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Cell death; Cyclophilin D; Mitochondria; Permeability transition pore

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; CALCIUM ION; CYCLOPHILIN D; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN P53; SIRTUIN 3; VOLTAGE DEPENDENT ANION CHANNEL;

APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CALCIUM TRANSPORT; CANCER CELL; CELL DEATH; CELLULAR DISTRIBUTION; CHANNEL GATING; CONFORMATIONAL TRANSITION; DIABETES MELLITUS; HEART MUSCLE ISCHEMIA; HUMAN; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; TUMOR CELL;

EID: 84881555646     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00076     Document Type: Article

References (43)

1. Altschuld, R. A., Hohl, C. M., Castillo, L. C., Garleb, A. A., Starling, R. C., and Brierley, G. P. (1992). Cyclosporin inhibits mitochondrial calcium efflux in isolated adult rat ventricular cardiomyocytes. Am. J. Physiol. 262, H1699-H1704.
2. Baines, C. P., Kaiser, R. A., Purcell, N. H., Blair, N. S., Osinska, H., Hambleton, M. A., et al. (2005). Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658-662.
3. Baines, C. P., Kaiser, R. A., Sheiko, T., Craigen, W. J., and Molkentin, J. D. (2007). Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell Biol. 9, 550-555.
4. Bao, H., Ge, Y., Zhuang, S., Dworkin, L. D., Liu, Z., and Gong, R. (2012). Inhibition of glycogen synthase kinase-3beta prevents NSAID-induced acute kidney injury. Kidney Int. 81, 662-673.
5. Basso, E., Fante, L., Fowlkes, J., Petronilli, V., Forte, M. A., and Bernardi, P. (2005). Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D. J. Biol. Chem. 280, 18558-18561.
6. Basso, E., Petronilli, V., Forte, M. A., and Bernardi, P. (2008). Phosphate is essential for inhibition of the mitochondrial permeability transition pore by cyclosporin A and by cyclophilin D ablation. J. Biol. Chem. 283, 26307-26311.
7. Bernardi, P. (1999). Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev. 79, 1127-1155.
8. Brenner, C., and Moulin, M. (2012). Physiological roles of the permeability transition pore. Circ. Res. 111, 1237-1247.
9. Burwell, L. S., and Brookes, P. S. (2008). Mitochondria as a target for the cardioprotective effects of nitric oxide in ischemia-reperfusion injury. Antioxid. Redox Signal. 10, 579-599.
10. Connern, C. P., and Halestrap, A. P. (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(Pt 2), 381-385.
11. 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.
12. Crompton, M. (1999). The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341(Pt 2), 233-249.
13. 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.
14. Eliseev, R. A., Malecki, J., Lester, T., Zhang, Y., Humphrey, J., and Gunter, T. E. (2009). Cyclophilin D interacts with Bcl2 and exerts an anti-apoptotic effect. J. Biol. Chem. 284, 9692-9699.
15. Ghosh, J. C., Siegelin, M. D., Dohi, T., and Altieri, D. C. (2010). Heat shock protein 60 regulation of the mitochondrial permeability transition pore in tumor cells. Cancer Res. 70, 8988-8993.
16. Giorgio, V., Bisetto, E., Soriano, M. E., Dabbeni-Sala, F., Basso, E., Petronilli, V., et al. (2009). Cyclophilin D modulates mitochondrial F0F 1-ATP synthase by interacting with the lateral stalk of the complex. J. Biol. Chem. 284, 33982-33988.
17. Hafner, A. V., Dai, J., Gomes, A. P., Xiao, C. Y., Palmeira, C. M., Rosenzweig, A., et al. (2010). Regulation of the mPTP by SIRT3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy. Aging (Albany NY) 2, 914-923.
18. Halestrap, A. P., and Brenner, C. (2003). The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem. 10, 1507-1525.
19. 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.
20. 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.
21. Ichas, F., Jouaville, L. S., and Mazat, J. P. (1997). Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89, 1145-1153.
22. Kang, B. H., Plescia, J., Dohi, T., Rosa, J., Doxsey, S. J., and Altieri, D. C. (2007). Regulation of tumor cell mitochondrial homeostasis by an organelle-specific Hsp90 chaperone network. Cell 131, 257-270.
23. Karch, J., and Molkentin, J. D. (2012). Is p53 the long-sought molecular trigger for cyclophilin D-regulated mitochondrial permeability transition pore formation and necrosis? Circ. Res. 111, 1258-1260.
24. Kohr, M. J., Aponte, A. M., Sun, J., Wang, G., Murphy, E., Gucek, M., et al. (2011). Characterization of potential S-nitrosylation sites in the myocardium. Am. J. Physiol. Heart Circ. Physiol. 300, H1327-1335.
25. Kokoszka, J. E., Waymire, K. G., Levy, S. E., Sligh, J. E., Cai, J., Jones, D. P., et al. (2004). The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427, 461-465.
26. Lee, J., and Kim, S. S. (2010). An overview of cyclophilins in human cancers. J. Int. Med. Res. 38, 1561-1574.
27. Li, B., Chauvin, C., De Paulis, D., De Oliveira, F., Gharib, A., Vial, G., et al. (2012). Inhibition of complex I regulates the mitochondrial permeability transition through a phosphate-sensitive inhibitory site masked by cyclophilin D. Biochim. Biophys. Acta 1817, 1628-1634.
28. Linard, D., Kandlbinder, A., Degand, H., Morsomme, P., Dietz, K. J., and Knoops, B. (2009). Redox characterization of human cyclophilin D: identification of a new mammalian mitochondrial redox sensor? Arch. Biochem. Biophys. 491, 39-45.
29. 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.
30. Martin, L. J., Adams, N. A., Pan, Y., Price, A., and Wong, M. (2011). The mitochondrial permeability transition pore regulates nitric oxide-mediated apoptosis of neurons induced by target deprivation. J. Neurosci. 31, 359-370.
31. Matouschek, A., Rospert, S., Schmid, K., Glick, B. S., and Schatz, G. (1995). Cyclophilin catalyzes protein folding in yeast mitochondria. Proc. Natl. Acad. Sci. U.S.A. 92, 6319-6323.
32. McStay, G. P., Clarke, S. J., and Halestrap, A. P. (2002). Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore. Biochem. J. 367, 541-548.
33. Nakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., et al. (2005). Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434, 652-658.
34. Nguyen, T. T., Stevens, M. V., Kohr, M., Steenbergen, C., Sack, M. N., and Murphy, E. (2011). Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore. J. Biol. Chem. 286, 40184-40192.
35. Parodi-Rullan, R., Barreto-Torres, G., Ruiz, L., Casasnovas, J., and Javadov, S. (2012). Direct renin inhibition exerts an anti-hypertrophic effect associated with improved mitochondrial function in post-infarction heart failure in diabetic rats. Cell. Physiol. Biochem. 29, 841-850.
36. Rasola, A., Sciacovelli, M., Chiara, F., Pantic, B., Brusilow, W. S., and Bernardi, P. (2010). Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition. Proc. Natl. Acad. Sci. U.S.A. 107, 726-731.
37. Rieusset, J., Fauconnier, J., Paillard, M., Belaidi, E., Tubbs, E., Chauvin, M. A., et al. (2012). Disruption of cyclophilin D-mediated calcium transfer from the ER to mitochondria contributes to hepatic ER stress and insulin resistance. Hepatology. doi:10.1002/hep.26189. [Epub ahead of print].
38. Shulga, N., and Pastorino, J. G. (2010). Ethanol sensitizes mitochondria to the permeability transition by inhibiting deacetylation of cyclophilin-D mediated by sirtuin-3. J. Cell. Sci. 123, 4117-4127.
39. Varanyuwatana, P., and Halestrap, A. P. (2012). The roles of phosphate and the phosphate carrier in the mitochondrial permeability transition pore. Mitochondrion 12, 120-125.
40. Vaseva, A. V., Marchenko, N. D., Ji, K., Tsirka, S. E., Holzmann, S., and Moll, U. M. (2012). p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 149, 1536-1548.
41. Vieira, H. L., Belzacq, A. S., Haouzi, D., Bernassola, F., Cohen, I., Jacotot, E., et al. (2001). The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene 20, 4305-4316.
42. Weiss, J. N., Korge, P., Honda, H. M., and Ping, P. (2003). Role of the mitochondrial permeability transition in myocardial disease. Circ. Res. 93, 292-301.
43. Woodfield, K., Ruck, 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(Pt 2), 287-290.