Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence

Biophysical Journal

Volumn 76, Issue 2, 1999, Pages 725-734

  Petronilli, Valeria ^a   Miotto, Giovanni ^a   Canton, Marcella ^a   Brini, Marisa ^a   Colonna, Raffaele ^a   Bernardi, Paolo ^a   Di Lisa, Fabio ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCEIN; CALCIUM ION;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CHANNEL GATING; CONFOCAL MICROSCOPY; FLUORESCENCE; MITOCHONDRION; NONHUMAN; PERMEABILITY; RAT; SPECTROFLUOROMETRY; STAINING; TRANSPORT KINETICS;

ANIMALIA;

EID: 0033021780     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77239-5     Document Type: Article

References (43)

1. Altschuld, R. A., C. M. Hohl, L. C. Castillo, A. A. Garleb, R. C. Starling, and G. P. Brierley. 1992. Cyclosporin inhibits mitochondrial calcium efflux in isolated adult rat ventricular cardiomyocytes. Am. J. Physiol. 262:H1699-H1704.
2. 2+ by liver mitochondria. J. Biol. Chem. 259:1279-1287.
3. Benachir, T., and M. Lafleur. 1995. Study of vesicle leakage induced by melittin. Biochim. Biophys. Acta. 1235:452-460.
4. Bennett, W. M., and D. J. Norman. 1986. Action and toxicity of cyclosporine. Annu Rev. Med. 37:215-224.
5. Bernardi, P. 1992. Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J. Biol. Chem. 267:8834-8839.
6. Bernardi, P., K. M. Broekemeier, and D. R. Pfeiffer. 1994. Recent progress on regulation of the mitochondrial permeability transition pore: a cyclosporin-sensitive pore in the inner mitochondrial membrane. J. Bioenerg. Biomembr. 26:509-517.
7. Bernardi, P., and V. Petronilli. 1996. The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal. J. Bioenerg. Biomembr. 28:131-138.
8. Braut Boucher, F., J. Pichon, P. Rat, M. Adolphe, M. Aubery, and J. Font. 1995. A non-isotopic, highly sensitive, fluorimetric, cell-cell adhesion microplate assay using calcein AM-labeled lymphocytes. J. Immunol. Methods. 178:41-51.
9. Costantini, P., V. Petronilli, R. Colonna, and P. Bernardi. 1995. On the effects of paraquat on isolated mitochondria. Evidence that paraquat causes opening of the cyclosporin A-sensitive permeability transition pore synergistically with nitric oxide. Toxicology. 99:77-88.
10. Darzynkiewicz, Z., F. Traganos, C. L. Staiano, J. Kapuscinski, and M. R. Melamed. 1982. Interaction of rhodamine 123 with living cells studied by flow cytometry. Cancer Res. 42:799-806.
11. Dietel, M., I. Herzig, A. Reymann, I. Brandt, B. Schaefer, A. Bunge, H. J. Heidebrecht, and A. Seidel. 1994. Secondary combined resistance to the multidrug-resistance-reversing activity of cyclosporin A in the cell line F4-6RADR-CsA. J. Cancer Res. Clin. Oncol. 120:263-271.
12. Ehrenberg, B., V. Montana, M. D. Wei. J. P. Wuskell, and L. M. Loew. 1988. Membrane potential can be determined in individual cells from the nemstian distribution of cationic dyes. Biophys. J. 53:785-794.
13. Gores, G. J., A. L. Nieminen, K. E. Fleishman, T. L. Dawson, B. Herman, and J. J. Lemasters. 1988. Extracellular acidosis delays onset of cell death in ATP-depleted hepatocytes. Am. J. Physiol. 255:C315-C322.
14. Gunter, T. E., K. K. Gunter, S. S. Sheu, and C. E. Gavin. 1994. Mitochondrial calcium transport: physiological and pathological relevance. Am. J. Physiol. 267:C313-C339.
15. Hollo, Z., L. Homolya, C. W. Davis, and B. Sarkadi. 1994. Calcein accumulation as a fluorometric functional assay of the multidrug transporter. Biochim. Biophys. Acta. 1191:384-388.
16. 2+ release. Arch. Biochem. Biophys. 195:468-477.
17. Huser, J., C. E. Rechenmacher, and L. A. Blatter. 1998. Imaging the permeability pore transition in single mitochondria. Biophys. J. 74: 2129-2137.
18. Ichas, F., L. S. Jouaville, and J. P. Mazat. 1997. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell. 89:1145-1153.
19. Ichas, F., L. S. Jouaville, S. S. Sidash, J. P. Mazat, and E. L. Holmuhamedov. 1994. Mitochondrial calcium spiking: a transduction mechanism based on calcium-induced permeability transition involved in cell calcium signalling. FEBS Lett. 348:211-215.
20. Imberti, R., A. L. Nieminen, B. Herman, and J. J. Lemasters. 1993. Mitochondrial and glycolytic dysfunction in lethal injury to hepatocytes by t-butylhydroperoxide: protection by fructose, cyclosporin A and trifluoperazine. J. Pharmacol. Exp. Ther. 265:392-400.
21. Kendall, D. A., and R. C. MacDonald. 1982. A fluorescence assay to monitor vesicle fusion and lysis. J. Biol. Chem. 257:13892-13895.
22. Kroemer, G., P. Petit, N. Zamzami, J. L. Vayssiere, and B. Mignotte. 1995. The biochemistry of programmed cell death. FASEB J. 9:1277-1287.
23. Kroemer, G., N. Zamzami, and S. A. Susin. 1997. Mitochondrial control of apoptosis. Immunol. Today. 18:44-51.
24. Latorre, R., and O. Alvarez. 1981. Voltage-dependent channels in planar lipid bilayer membranes. Physiol. Rev. 61:77-150.
25. Loew, L. M., R. A. Tuft, W. Carrington, and F. S. Fay. 1993. Imaging in five dimensions: time-dependent membrane potentials in individual mitochondria. Biophys. J. 65:2396-2407.
26. 2+ concentration in living single rat cardiac myocytes. Am. J Physiol. 261: H1123-H1134.
27. Nicolli, A., E. Basso, V. Petronilli, R. M. Wenger, and P. Bernardi. 1996. Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, and cyclosporin A-sensitive channel. J. Biol. Chem. 271:2185-2192.
28. Nieminen, A. L., A. K. Saylor, S. A. Tesfai, B. Herman, and J. J. Lemasters. 1995. Contribution of the mitochondrial permeability ransition to lethal injury after exposure of hepatocytes to t-butylhydroperoxide. Biochem. J. 307:99-106.
29. O'Rourke, B., B. M. Ramza, and E. Marban 1994. Oscillations of membrane current and excitability driven by metabolic oscillations in heart cells. Science. 265:962-966.
30. Pastorino, J. G., J. W. Snyder, A. Serroni, J. B. Hoek, and J. L. Farber. 1993. Cyclosporin and carnitine prevent the anoxic death of cultured hepatocytes by inhibiting the mitochondrial permeability transition. J. Biol. Chem. 268:13791-13798.
31. Perin, M. S., and R. C. MacDonald. 1989. Fusion of synaptic vesicle membranes with planar bilayer membranes. Biophys. J. 55:973-986.
32. Petronilli, V., P. Bernardi, M. Canton, R. Colonna, G. Miotto, and F. Di Lisa. 1998. Direct evidence of the mitochondrial permeability transition pore (MTP) in single living cells. Biophys. J. 74:A383 (Abstr.).
33. Petronilli, V., C. Cola, S. Massari, R. Colonna, and P. Bernardi. 1993. Physiological effectors modify voltage sensing by the cyclosporin A-sensitive permeability transition pore of mitochondria. J. Biol. Chem. 268:21939-21945.
34. Petronilli, V., G. Miotto, R. Colonna, P. Bernardi, and F. Di Lisa. 1997. Tetramethylrodamine (TMRM) quenching of calcein fluorescence limits the evaluation of intracellular distribution of calcein. Biophys. J. 70: A210 (Abstr.).
35. 2+ with recombinant targeted aequorin: significance for the regulation of pyruvate dehydrogenase activity. Proc. Natl. Acad. Sci. USA. 93:5489-5494.
36. Seglen, P. O. 1976. Preparation of isolated rat liver cells. Methods Cell Biol. 13:29-83.
37. Szabo, I., P. Bernardi, and M. Zoratti. 1992. Modulation of the mitochondrial megachannel by divalent cations and protons. J. Biol. Chem. 267:2940-2946.
38. Szabo, I., and M. Zoratti. 1991. The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A. J. Biol. Chem. 266: 3376-3379.
39. Szabo, I., and M. Zoratti. 1992. The mitochondrial megachannel is the permeability transition pore. J. Bioenerg. Biomembr. 24:111-117.
40. Venerando, R., G. Miotto, M. Kadowaki, N. Siliprandi, and G. E. Mortimore. 1994. Multiphasic control of proteolysis by leucine and alanine in the isolated rat hepatocyte. Am. J. Physiol. 266:C455-C461.
41. Wallach, D. F. H., and T. L. Steck. 1963. Fluorescence techniques in the microdetermination of metals in biological materials. Anal. Chem. 35: 1035-1044.
42. Woodbury, D. J., and J. E. Hall. 1988. Role of channels in the fusion of vesicles with a planar bilayer. Biophys. J. 54:1053-1063.
43. Zoratti, M., and I. Szabo. 1995. The mitochondrial permeability transition. Biochim. Biophys. Acta. 1241:139-176.