Abstract
We have provided evidence that mitochondrial membrane permeability transition induced by inorganic phosphate, uncouplers or prooxidants such as t-butyl hydroperoxide and diamide is caused by a Ca2+-stimulated production of reactive oxygen species (ROS) by the respiratory chain, at the level of the coenzyme Q. The ROS attack to membrane protein thiols produces cross-linkage reactions, that may open membrane pores upon Ca2+ binding. Studies with submitochondrial particles have demonstrated that the binding of Ca2+ to these particles (possibly to cardiolipin) induces lipid lateral phase separation detected by electron paramagnetic resonance experiments exploying stearic acids spin labels. This condition leads to a disorganization of respiratory chain components, favoring ROS production and consequent protein and lipid oxidation.
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REFERENCES
Nicholls, D. G. and Åkerman, K. E. O. (1982). Biochim. Biophys. Acta. 683:57–88.
Gunter, T. E. and Pfeiffer, D. R. (1990) Am. J. Physiol. 258:C755–C786.
Hunter, D. R., Haworth, R. A. and Southard, J. H. (1976). J. Biol. Chem. 251:5069–5077.
Gunter, T. E., Gunter, K. K., Sheu, S.-S. and Gavin, C. E. (1994) Am. J. Physiol. 267:C313–C339.
Zoratti, M. and Szabò, I. (1995) Biochim. Biophys. Acta 1241:139–176.
Lehninger, A. L., Vercesi, A. E. and Bababunmi, E. A. (1978) Proc. Natl. Acad. Sci. USA 75:1690–1694.
Vercesi, A. E., Reynafarje, B. and Lehninger, A. L. (1978) J. Biol. Chem. 253:6379–6385.
Bellomo, G., Jewell, S. A., Thor, H. and Orrenius, S. (1982) Proc. Natl. Acad. Sci. USA 79:6842–6846.
Sies, H., Graf, P. and Estrela, J. M. (1981) Proc. Natl. Acad. Sci. USA 78:3358–3362.
Richter, C. and Frei, B. (1988) Free Radical Biol. Med. 4:365–375.
Crompton, M., Ellinger, H. and Costi, A. (1988) Biochem. J. 255:357–360.
Broekemeier, K. M., Dempsey, M. E. and Pfeiffer, D. R. (1989) J. Biol. Chem. 264:7826–7830.
Bernardi, P. (1992) J. Biol. Chem. 267:8334–8339.
Bernardi, P., Vassanelli, S., Veronese, P., Colonna, R., Szabó, I. and Zoratti, M. (1992) J. Biol. Chem. 267:2934–2939.
Nazareth, W., Yafei, N. and Crompton, M. (1991) J. Mol. Cell. Cardiol. 23:1351–1354.
Pastorino, J. G., Snyder, J. W., Serroni, A., Hoek, J. B. and Farber, J. L. (1993) J. Biol. Chem. 268:13791–13798.
Brustovetsky, N. N., Egorova, M. V. and Gnuton, D. Yu. (1993) Comp. Biochem. Physiol. 106B:423–426.
Bernardi, P., Broekemeier, K. M. an Pfeiffer, D. R. (1994) J. Bioenerg. Biomembr. 26:509–517.
Boveris, A., Oshino, N. and Chance, B. (1972) Biochem. J. 128:617–630.
Cadenas, E., Boveris, A., Ragan, C. I. and Stoppani, A. O. M. (1977) Arch. Biochem. Biophys. 180:248–257.
Dunford, H. B. (1987) Free Radical Biol. Med. 3:405–421.
Sutton, H. C. and Winterbourn, C. C. (1989) Free Radical. Biol. Med. 6:53–60.
Halliwell, B. and Gutteridge, J. M. C. (1989) in: Free Radicals in Biology and Medicine (B. Halliwell and J. M. C. Gutteridge, eds.) Oxford Univ. Press (Clarendon), Oxford.
Vercesi, A. E. and Hoffman, M. E. (1993) in: Methods in Toxicology. Mitochondrial Dysfunction, Vol. 2, Chapter 21. (D. P. Jones, L. H. Lash, eds) Academic Press, New York.
Radi, R., Turrens, J. F., Chang, L. Y., Brush, K. M., Crapo, J. D. and Freeman, B. A. (1991) J. Biol. Chem. 266:22028–22034.
Phung, C. D., Ezieme, J. A. and Turrens, J. F. (1994) Arch. Biochem. Biophys. 315:479–482.
Cadenas, E. and Boveris, A. (1980) Biochem. J. 188:31–37.
Grijalba, M. T., Vercesi, A. E. and Schreier, S. (1996) XXV Annual Meeting of the Brazilian Society for Biochemistry and Molecular Biology, Caxambu, Mg, Brazil, May 4–7. Abstract P.4, page 151.
Castilho, R. F., Kowaltowski, A. J., Meinicke, A. R., Bechara, E. J. H. and Vercesi, A. E. (1995) Free Radical Biol. Med. 18:479–486.
Lotscher, H. R., Winterhalter, K. H., Carafoli, E. and Richter, C. (1979) Proc. Natl. Acad. Sci. USA 76:4340–4344.
Beatrice, M. C., Stiers, D. L. and Pfeiffer, D. R. (1984) J. Biol. Chem. 259:1279–1287.
Bernardes, C. F., Pereira-da-Silva, L. and Vercesi, A. E. (1986) Biochim. Biophys. Acta. 850:41–48.
Vercesi, A. E. (1993) Braz. J. Med. Biol. Res. 26:441–457.
Valle, V. G. R., Fagian, M. M., Parentoni, L. S., Meinicke, A. R. and Vercesi, A. E. (1993) Arch. Biochem. Biophys. 307:1–7.
Petronilli, V., Costantini, P., Scorrano, L., Colonna, R., Passamonti, S. and Bernardi, P. (1994) J. Biol. Chem. 269:16638–16642.
Carbonera, D., Angrilli, A. and Azzone, G. F. (1988) Biochim. Biophys. Acta. 936:139–147.
Hermes-Lima, M., Valle, V. G. R., Vercesi, A. E. and Bechara, E. J. H. (1991) Biochim. Biophys. Acta. 1056:57–63.
Vercesi, A. E., Castilho, R. F., Meinicke, A. R., Valle, V. G. R., Hermes-Lima, M. and Bechara, E. J. H. (1994) Biochim. Biophys. Acta. 1188:201–206.
Inoue, T., Yoshida, Y., Nishimura, M., Kurosawwa, K. and Tagawa, K. (1993) Biochim. Biophys. Acta. 1140:313–320.
Takeyama, N., Matsuo, N. and Tanaka, T. (1993) Biochem. J. 294:719–725.
Tangeras, A., Flatmark, T., Bäckström, D. and Ehrenberg, A. (1980) Biochim. Biophys. Acta 589:162–175.
Merryfield, M. L. and Lardy, H. A. (1982) J. Biol Chem. 257:3628–3635.
Biemond, P., van Eijk, H. G., Swaak, A. J. G. and Koster, J. F. (1984) J. Clin. Invest. 73:1576–1579.
Kowaltowski, A. J., Castilho, R. F. and Vercesi, A. E. (1995) Am. J. Physiol. 269:C141–C147.
Castilho, R. F., Lowaltowski, A. J., Meinicke, A. R. and Vercesi, A. E. (1995) Free Radical Biol. Med. 18:55–59.
Kowaltowski, A. J., Castilho, R. F. and Vercesi, A. E. (1996) FEBS Lett. 378:150–152.
Kowaltowski, A. J., Castilho, R. F., Grijalba, M. T., Bechara, E. J. H. and Vercesi, A. E. (1996) J. Biol. Chem. 271:2929–2934.
Indig, G., Campa, A., Bechara, E. J. H. and Cilento, G. (1988) Photochem. Photobiol. 48:719–723.
Nantes, I. L., Cilento, G., Bechara, E. J. H. and Vercesi, A. E. (1995) Photochem. Photobiol. 62:522–527.
Cadenas, E. (1989) Annu. Rev. Biochem. 58:79–110.
Di Mascio, P., Catalani, L. H. and Bechara, E. J. H. (1992) Free Radical Biol. Med. 12:471–478.
Bechara, E. J. H., Faria-Oliveira, O. M. M., Durán, N., Batista, R. C. and Cilento, G. (1979) Photochem. Photobiol. 30:101–110.
Vercesi, A. E. (1987) Arch. Biochem. Biophys. 252:171–178.
Fagian, M. M., Pereira-da-Silva, L., Martins, I. S. and Vercesi, A. E. (1990) J. Biol. Chem. 265:19955–19960.
Castilho, R. F., Kowaltowski, A. J. and Vercesi, A. E. (1996) J. Bioenerg. Biomembr. 29:(in press).
Kowaltowski, A. J., Vercesi, A. E. and Castilho, R. F. (1996) Biochim. Biophys. Acta. (in press).
Kligenberg, M. (1989) Arch. Biochem. Biophys. 270:1–14.
Majima, E., Shinohara, Y., Yamaguchi, N., Hong, Y. and Terada, H. (1994) Biochemistry 33:9530–9536.
Scherer, B. and Kligenberg, M. (1974) Biochemistry 13:161–169.
Vignais, P. V. and Vignais, P. M. (1972) FEBS Lett 26:27–31.
Novgorodov, S. A., Gudz, T. I., Brierley, G. P. and Pfeiffer, D. R. (1994) Arch. Biochem. Biophys. 311:219–228.
Bernardes, C. F., Meyer-Fernandes, J. R., Basseres, D. S., Castilho, R. F. and Vercesi, A. E. (1994) Biochim. Biophys. Acta. 1188:93–100.
Richter, C., Gogvadze, V., Laffranchi, R., Schlapbach, R., Schweizer, M., Suter, M., Walter, P. and Yaffee, M. (1995) Biochim. Biophys. Acta 1271:67–74.
Vercesi, A. E. (1984) Arch. Biochem. Biophys. 231:86–91.
Al-Nasser, I. and Crompton, M. (1986) Biochem. J. 239:19–29.
Crompton, M., Costi, A. and Hayat, L. (1987) Biochem. J. 245:915–918.
Castilho, R. F., Meinicke, A. R., Almeida, A. M., Hermes-Lima, M. and Vercesi, A. E. (1994) Arch. Biochem. Biophys. 308:158–163.
Hermes-Lima, M., Castilho, R. F., Meinicke, A. R. and Vercesi, A. E. (1995) Mol. Cell. Biochem. 145:53–60.
Reed, K. C. and Bygrave, F. L. (1974) Biochem. J. 140:143–155.
Vercesi, A. E., Ferraz, V. L., Macedo, D. V. and Fiskum, G. (1988) Biochem. Biophys. Res. Commun. 154:934–941.
Bernardi, P., Veronese, P. and Petronilli, V. (1993) J. Biol. Chem. 268:1005–1010.
Bernardi, P. and Petronilli, V. (1996) J. Bioenerg. Biomembr. 28:131–138.
Igbavboa, U., Zwizinski, C. W. and Pfeiffer, D. R. (1989) Biochem. Biophys. Res. Commun. 161:619–625.
Griffiths, E. and Halestrap, A. P. (1995) Biochem. J. 307:93–98.
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Vercesi, A.E., Kowaltowski, A.J., Grijalba, M.T. et al. The Role of Reactive Oxygen Species in Mitochondrial Permeability Transition. Biosci Rep 17, 43–52 (1997). https://doi.org/10.1023/A:1027335217774
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DOI: https://doi.org/10.1023/A:1027335217774