Switch from inhibition to activation of the mitochondrial permeability transition during hematoporphyrin-mediated photooxidative stress. Unmasking pore-regulating external thiols

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 7, 2009, Pages 897-904

  Petronilli, Valeria ^a   Šileikyte, Justina ^a   Zulian, Alessandra ^a   Dabbeni Sala, Federica ^a   Jori, Giulio ^a   Gobbo, Silvano ^a   Tognon, Giuseppe ^a   Nikolov, Peter ^b   Bernardi, Paolo ^a   Ricchelli, Fernanda ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b INSTITUTE OF ORGANIC CHEMISTRY   (Bulgaria)

Author keywords

External thiols; Mitochondria; Permeability transition pore; Photooxidation; Porphyrin

Indexed keywords

CYSTEINE; HEMATOPORPHYRIN; HISTIDINE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REACTIVE OXYGEN METABOLITE; THIOL DERIVATIVE;

ANIMAL TISSUE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME LOCALIZATION; LIVER MITOCHONDRION; MITOCHONDRIAL PERMEABILITY; NONHUMAN; OXIDATIVE STRESS; PHOTODEGRADATION; PHOTOOXIDATION; PHOTOSENSITIVITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; RAT;

ANIMALS; CALCIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; HEMATOPORPHYRINS; HYDROGEN PEROXIDE; LIGHT; MITOCHONDRIA, LIVER; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; OXIDANTS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PERMEABILITY; PHOTOCHEMISTRY; RATS; RATS, WISTAR; SINGLET OXYGEN; SULFHYDRYL COMPOUNDS; TIME FACTORS; ULTRAVIOLET RAYS;

EID: 67649295443     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.03.014     Document Type: Article

References (37)

1. Lemasters J.J., Qian T., Bradham C.A., Brenner D.A., Cascio W.E., Trost L.C., Nishimura Y., Nieminen A.L., and Herman B. Mitochondrial dysfunction in the pathogenesis of necrotic and apoptotic cell death. J. Bioenerg. Biomembr. 31 (1999) 305-319
2. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341 (1999) 233-249
3. Leung A.W., and Halestrap A.P. Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore. Biochim. Biophys. Acta 1777 7-8 (2008) 946-952
4. Bernardi P., Krauskopf A., Basso E., Petronilli V., Blachly-Dyson E., Di Lisa F., and Forte M.A. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS J. 273 (2006) 2077-2099
5. Baines C.P., Kaiser R.A., Purcell N.H., Scott Blair N., Osinska H., Hambleton M.A., Brunskill E.W., Sayen M.R., Gottlieb R.A., Dorn II G.W., Robbins J., and Molkentin J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434 (2005) 658-662
6. Basso E., Fante L., Fowlkes J., Petronilli V., Forte M.A., and Bernardi P. Properties of the permeability transition pore in mitochondria devoid of cyclophilin D. J. Biol. Chem. 280 (2005) 18558-18561
7. Basso E., Petronilli V., Forte M.A., and Bernardi P. 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
8. Kokoszka J.E., Waymire K.G., Levy S.E., Sligh J.E., Cai J., Jones D.P., MacGregor G.R., and Wallace D.C. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427 (2004) 461-465
9. Baines C.P., Kaiser R.A., Sheiko T., Craigen W.J., and Molkentin J.D. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat. Cell. Biol. 9 (2007) 550-555
10. Bernardi P., and Forte M. The mitochondrial permeability transition pore. Novartis Found Symp. 287 (2007) 157-164
11. Rasola A., and Bernardi P. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 12 (2007) 815-833
12. Bernardi P. The permeability transition pore. Control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death. Biochim. Biophys. Acta 1275 (1996) 5-9
13. Nicolli A., Petronilli V., and Bernardi P. Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by matrix pH. Evidence that the pore open-closed probability is regulated by reversible histidine protonation. Biochemistry 32 (1993) 4461-4465
14. Petronilli V., Cola C., Massari S., Colonna R., and Bernardi P. Physiological effectors modify voltage sensing by the cyclosporin A-sensitive permeability transition pore of mitochondria. J. Biol. Chem. 268 (1993) 21939-21945
15. Petronilli V., Costantini P., Scorrano L., Colonna R., Passamonti S., and Bernardi P. The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. J. Biol. Chem. 269 (1994) 16638-16642
16. Costantini P., Chernyak B.V., Petronilli V., and Bernardi P. Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol. Chem. 271 (1996) 6746-6751
17. Costantini P., Colonna R., and Bernardi P. Induction of the mitochondrial permeability transition by N-ethylmaleimide depends on secondary oxidation of critical thiol groups. Potentiation by copper-ortho-phenanthroline without dimerization of the adenine nucleotide translocase. Biochim. Biophys. Acta 1365 (1998) 385-392
18. Salet C., Moreno G., Ricchelli F., and Bernardi P. Singlet oxygen produced by photodynamic action causes inactivation of the mitochondrial permeability transition pore. J. Biol. Chem. 272 (1997) 21938-21943
19. Morgan J., and Oseroff A.R. Mitochondria-based photodynamic anti-cancer therapy. Adv. Drug Deliv. Rev. 49 (2001) 71-86
20. Moan J., and Berg K. The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen. Photochem. Photobiol. 53 (1991) 353-549
21. Moreno G., Poussin K., Ricchelli F., and Salet C. The effects of singlet oxygen produced by photodynamic action on the mitochondrial permeability transition differ in accordance with the localization of the sensitizer. Arch. Biochem. Biophys. 386 (2001) 243-250
22. Ricchelli F., Gobbo S., Moreno G., and Salet C. Changes of the fluidity of mitochondrial membranes induced by the permeability transition. Biochemistry 38 (1999) 9295-9300
23. Ricchelli F., Jori G., Gobbo S., Nikolov P., and Petronilli V. Discrimination between two steps in the mitochondrial permeability transition process. Int. J. Biochem. Cell Biol. 37 (2005) 1858-1868
24. Fontaine E., Ichas F., and Bernardi P. A ubiquinone-binding site regulates the mitochondrial permeability transition pore. J. Biol. Chem. 273 (1998) 25734-25740
25. Costantini P., Chernyak B.V., Petronilli V., and Bernardi P. Selective inhibition of the mitochondrial permeability transition pore at the oxidation-reduction sensitive dithiol by monobromobimane. FEBS Lett. 362 (1995) 239-242
26. Kosower N.S., Kosower N.M., Newton G.L., and Ranney H.M. Bimane fluorescent labels: labeling of normal human red cells under physiological conditions. Proc. Natl. Acad. Sci. U.S.A. 76 (1979) 3382-3386
27. Zulian A., Petronilli V., Bova S., Dabbeni-Sala F., Cargnelli G., Cavalli M., Rennison D., Stäb J., Laita O., Brimble M.A., Hopkins B., Bernardi P., and Ricchelli F. Assessing the molecular basis for rat-selective induction of the mitochondrial permeability transition by norbormide. Biochim. Biophys. Acta Bioenerg. 1767 (2007) 980-988
28. Hackenbrock C.R. Ultrastructural bases for metabolically linked mechanical activity in mitocondria. II. Electron transport-linked ultrastructural transformations in mitochondria. J. Cell Biol. 37 (1968) 345-369
29. Hackenbrock C.R. Energy-linked ultrastructural transformations in isolated liver mitochondria and mitoplasts. Preservation of configurations by freeze-cleaving compared to chemical fixation. J. Cell Biol. 53 (1972) 450-465
30. Teixera B.M., Kowaltowski A.J., Castilho R.F., and Vercesi A.E. Inhibition of mitochondrial permeability transition by low pH is associated with less extensive membrane protein thiol oxidation. Biosci. Rep. 19 (1999) 525-533
31. Salet C., and Moreno G. Photosensitization of mitochondria. Molecular and cellular aspects. J. Photochem. Photobiol., B. Biol. 5 2 (1990) 133-150
32. Costantini P., Belzacq A.-S., Vieira H.L.A., Larochette N., de Pablo M.A., Zamzami N., Susin S.A., Brenner C., and Kroemer G. Oxidation of a critical thiol residue of the adenine nucleotide translocator enforces Bcl-2-independent permeability transition pore opening and apoptosis. Oncogene 19 2 (2000) 307-314
33. 2+-induced permeability transition of mitochondria. Free Rad. Res. 38 1 (2004) 27-35
34. 2+: correlation with mitochondrial permeability transition. Biochim. Biophys. Acta. 1318 3 (1997) 395-402
35. McStay G.P., Clarke S.J., and Halestrap A.P. 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. 36 (2002) 541-548
36. Halestrap A.P., Woodfield K.Y., and Connern C.P. 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 6 (1997) 3346-3354
37. Leung A.W., Varanyuwatana P., and Halestrap A.P. The mitochondrial phosphate carrier interacts with cyclophilin D and may play a key role in the permeability transition. J. Biol. Chem. 283 39 (2008) 26312-26323