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Induction of permeability of the inner membrane of yeast mitochondria

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Abstract

The current view on apoptosis is given, with a special emphasis placed on apoptosis in yeasts. Induction of a non-specific permeability transition pore (mPTP) in mammalian and yeast mitochondria is described, particularly in mitochon-dria from Yarrowia lipolytica and Dipodascus (Endomyces) magnusii yeasts, which are aerobes possessing the fully competent respiratory chain with all three points of energy conservation and well-structured mitochondria. They were examined for their ability to induce an elevated permeability transition of the inner mitochondrial membrane, being subjected to virtually all conditions known to induce the mPTP in animal mitochondria. Yeast mitochondria do not form Ca2+-dependent pores, neither the classical Ca2+/Pi-dependent, cyclosporin A-sensitive pore even under deenergization of mitochondria or depletion of the intramitochondrial nucleotide pools, nor a pore induced in mammalian mitochondria upon concerted action of moderate Ca2+ concentrations (in the presence of the Ca2+ ionophore ETH129) and saturated fatty acids. No pore formation was found in yeast mitochondria in the presence of elevated phosphate concentrations at acidic pH values. It is concluded that the permeability transition in yeast mitochondria is not coupled with Ca2+ uptake and is differently regulated compared to the mPTP of animal mitochondria.

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Abbreviations

CsA:

cyclosporin A

ETH129:

specific Ca2+-ionophore N,N,N′N′-tetra(cyclohexyl)diamide of diglycolic acid

mPTP:

(mitochondrial permeability transition pore), non-specific permeability of the inner mitochondrial membrane

Pi :

inorganic phosphate

YMUC:

yeast mitochondrial unspecific channel

References

  1. Circu, M. L., and Aw, T. Y. (2008) Free Radic. Res., 1, 1–18.

    Google Scholar 

  2. Hanada, M., Aime-Sempe, C., Sato, T., and Reed, J. C. (1995) J. Biol. Chem., 270, 11962–11969.

    Article  CAS  PubMed  Google Scholar 

  3. Priault, M., Cartron, P. F., Camougrand, N., Antonsson, D., Vallette, F. M., and Manon, S. (2003) Cell. Death Differ., 10, 1068–1077.

    Article  CAS  PubMed  Google Scholar 

  4. Madeo, F., Frolich, E., and Frohlich, K. U. (1997) J. Cell Biol., 139, 729–734.

    Article  CAS  PubMed  Google Scholar 

  5. Madeo, F., Herker, E., Maldener, C., Wissing, S., Lachelt, S., Herlan, M., Fehr, M., Lauber, K., Sigrist, S. J., Wesselborg, S., and Frohlich, K. U. (2002) Mol. Cell, 9, 911–917.

    Article  CAS  PubMed  Google Scholar 

  6. Almeida, B., Buttner, S., Ohlmeier, S., Silva, A., Mesquita, A., Sampaio-Marques, B., Osorio, N. S., Kollau, A., Mayer, B., Leao, C., Laranjinha, J., Rodrigues, F., Madeo, F., and Ludovico, P. (2007) J. Cell Sci., 120, 3279–3288.

    Article  CAS  PubMed  Google Scholar 

  7. Almeida, B., Silva, A., Mesquita, A., Sampaio-Marques, B., Rodrigues, F., and Ludovico, P. (2008) Biochim. Biophys. Acta, 1783, 1436–1448.

    Article  CAS  PubMed  Google Scholar 

  8. Eisenberg, T., Buttner, S., and Kroemer, G. (2007) Apoptosis, 12, 1011–1023.

    Article  CAS  PubMed  Google Scholar 

  9. Low, C. P., Shui, G., Liew, L. P., Buttner, S., Madeo, F., Dawes, I. W., Wenk, M. R., and Yang, H. (2008) J. Cell Sci., 121, 2671–2684.

    Article  CAS  PubMed  Google Scholar 

  10. Madeo, F., Herker, E., Wissing, S., Jungwirth, H., Eisenberg, T., and Frohlich, K. U. (2004) Curr. Opin. Microbiol., 7, 655–660.

    Article  CAS  PubMed  Google Scholar 

  11. Madeo, F., and Frohlich, K. U. (2008) Biochim. Biophys. Acta, 1783, 1271.

    Article  CAS  PubMed  Google Scholar 

  12. Perrone, G. G., Tan, S. X., and Dawes, I. W. (2008) Biochim. Biophys. Acta, 1783, 1354–1368.

    Article  CAS  PubMed  Google Scholar 

  13. Reiter, J., Herker, E., Madeo, F., and Schmitt, M. J. (2005) Cell Biol., 168, 353–358.

    Article  CAS  Google Scholar 

  14. Schmitt, M. J., and Reiter, J. (2008) Biochim. Biophys. Acta, 1783, 1413–1417.

    Article  CAS  PubMed  Google Scholar 

  15. Severin, F. F., Meer, M. V., Smirnova, E. A., Knorre, D. A., and Skulachev, V. P. (2008) Biochim. Biophys. Acta, 1783, 1350–1353.

    Article  CAS  PubMed  Google Scholar 

  16. Laun, P., Rinnerthaler, M., Bogengruber, E., Heeren, G., and Breitenbach, M. (2006) Exp. Gerontol., 241, 1208–1212.

    Article  Google Scholar 

  17. Laun, P., Heeren, G., Rinnerthaler, M., Rid, R., Kossler, S., Koller, L., and Breitenbach, M. (2008) Biochim. Biophys. Acta, 1783, 1328–1334.

    Article  CAS  PubMed  Google Scholar 

  18. Herker, E., Jungwirth, H., Lehmann, K. A., Maldener, C., Frohlich, K. U., Wissing, S., Buttner, S., Fehr, M., Sigrist, S., and Madeo, F. (2004) J. Cell Biol., 164, 501–507.

    Article  CAS  PubMed  Google Scholar 

  19. Fahrenkrog, B., Sauder, U., and Aebi, U. (2004) J. Cell. Sci., 117, 115–126.

    Article  CAS  PubMed  Google Scholar 

  20. Wissing, S., Ludovico, P., Herker, E., Buttner, S., Engelhardt, S. M., Decker, T., Link, A., Proksch, A., Rodrigues, F., Corte-Real, M., Frohlich, K. U., Manns, J., Cande, C., Sigrist, S. J., Kroemer, G., and Madeo, F. (2004) J. Cell. Biol., 166, 969–974.

    Article  CAS  PubMed  Google Scholar 

  21. Fannjiang, Y., Cheng, W. C., Lee, S. J., Qi, B., Pevsner, J., McCaffery, J. M., Hill, R. B., Basanez, G., and Hardwick, J. M. (2004) Genes Dev., 18, 2785–2797.

    Article  CAS  PubMed  Google Scholar 

  22. Ludovico, P., Rodrigues, F., Almeida, A., Silva, M. T., Barrientos, A., and Corte-Real, M. (2002) Mol. Biol. Cell, 13, 2598–2606.

    Article  CAS  PubMed  Google Scholar 

  23. Silva, R. D., Sotoca, R., Johansson, B., Ludovico, P., Sansonetty, F., Silva, M. T., Peinado, J. M., and Corte-Real, M. (2005) Mol. Microbiol., 58, 824–834.

    Article  CAS  PubMed  Google Scholar 

  24. Buttner, S., Eisenberg, T., Carmona-Gutierrez, D., Ruli, D., Knauer, H., Ruckenstuhl, C., Sigrist, C., Wissing, S., Kollroser, M., Frohlich, K. U., Sigrist, S., and Madeo, F. (2007) Mol. Cell., 25, 233–246.

    Article  PubMed  Google Scholar 

  25. Cymerman, I. A., Chung, I., Beckmann, B. M., Bujnicki, J. M., and Meiss, G. (2008) Nucleic Acids Res., 36, 1369–1379.

    Article  CAS  PubMed  Google Scholar 

  26. Singh, K., Kang, P. J., and Park, H. O. (2008) Proc. Natl. Acad. Sci. USA, 105, 1522–1527.

    Article  CAS  PubMed  Google Scholar 

  27. Owsianowski, E., Walter, D., and Fahrenkrog, B. (2008) Biochim. Biophys. Acta, 1783, 1303–1310.

    Article  CAS  PubMed  Google Scholar 

  28. Kerscher, S., Durstewitz, G., Casaregola, S., Gaillardin, C., and Brandt, U. (2001) Comp. Funct. Genom., 2, 80–90.

    Article  CAS  Google Scholar 

  29. Webb, J. S., Givskov, M., and Kjelleberg, S. (2003) Curr. Opin. Microbiol., 6, 578–585.

    Article  CAS  PubMed  Google Scholar 

  30. Palkova, Z. (2004) EMBO Rep., 5, 470–476.

    Article  CAS  PubMed  Google Scholar 

  31. Vachova, L., Kucerova, H., Devaux, F., Ultholova, M., and Palkova, Z. (2009) Environ. Microbiol., 11, 494–504.

    Article  CAS  PubMed  Google Scholar 

  32. Smardova, J., Smarda, J., and Koptikova, J. (2005) Differention, 73, 261–277.

    Article  CAS  Google Scholar 

  33. Yamaguchi, R., Lartigue, L., Perkins, G., Scott, R. T., Dixit, A., Kushnareva, Y., Kuwana, T., Ellisman, V. Y., and Newmeyer, D. D. (2008) Mol. Cell, 31, 557–569.

    Article  CAS  PubMed  Google Scholar 

  34. Sheridan, C., Delivani, P., Cullen, S. P., and Martin, S. J. (2008) Mol. Cell, 31, 570–585.

    Article  CAS  PubMed  Google Scholar 

  35. Colin, J., Garibal, J., Mignotte, B., and Guenal, I. (2009) Biochem. Biophys. Res. Commun., 379, 931–943.

    Article  Google Scholar 

  36. Lucken-Ardjomande, S., Montessuit, S., and Martinou, J. C. (2008) Cell Death Differ., 15, 923–937.

    Google Scholar 

  37. Bernardi, P., Krauskopf, A., Basso, E., Petronilli, V., Blachly-Dyson, E., Di Lisa, F., and Forte, M. A. (2006) FEBS J., 273, 2077–2099.

    Article  CAS  PubMed  Google Scholar 

  38. Halestrap, A. P. (2009) J. Mol. Cardiol., 46, 821–831.

    Article  CAS  Google Scholar 

  39. Leung, A. W., and Halestrap, A. P. (2008) Biochim. Biophys. Acta, 1777, 946–952.

    Article  CAS  PubMed  Google Scholar 

  40. Sultan, A., and Sokolove, P. (2001) Arch. Biochem. Biophys., 386, 52–61.

    Article  CAS  PubMed  Google Scholar 

  41. Mironova, G. D., Gateau-Roesch, O., Levrat, C., Gritsenko, E., Pavlov, E., Lazareva, A. V., Limarenko, E., Rey, C., Louisot, P., and Saris, N.-E. L. (2001) J. Bioenerg. Biomembr., 33, 319–331.

    Article  CAS  PubMed  Google Scholar 

  42. Kristian, T., Bernardi, P., and Siesjo, B. K. (2001) J. Neurotrauma, 18, 1059–1074.

    Article  CAS  PubMed  Google Scholar 

  43. Knorre, D. A., Dedukhova, V. I., Vyssokikh, M. Y., and Mokhova, E. N. (2003) Biosci. Rep., 23, 67–75.

    Article  CAS  PubMed  Google Scholar 

  44. Gao, W., Pu, Y., Luo, K. Q., and Chang, D. C. (2001) J. Cell Sci., 114, 2855–2862.

    CAS  PubMed  Google Scholar 

  45. Gogvadze, V., Robertson, J. D., Enoksson, M., Zhivotovsky, B., and Orrenius, S. (2004) Biochem. J., 378, 213–217.

    Article  CAS  PubMed  Google Scholar 

  46. Ott, M., Robertson, J. D., Gogvadze, V., Zhivotovsky, B., and Orrenius, S. (2002) Proc. Natl. Acad. Sci. USA, 99, 1259–1263.

    Article  CAS  PubMed  Google Scholar 

  47. Scorrano, L., Ashiya, M., Buttle, K., Weiler, S., Oakes, S. A., Mannella, C. A., and Korsmeyer, S. J. (2002) Dev. Cell, 2, 55–67.

    Article  CAS  PubMed  Google Scholar 

  48. Mironova, G. D., Kachaeva, E. V., and Kopylov, A. T. (2007) Vestnik RAMN, 2, 44–50.

    Google Scholar 

  49. Costa, A. D., and Garlid, K. D. (2009) J. Bioenerg. Biomembr., 41, 123–126.

    Article  CAS  PubMed  Google Scholar 

  50. Jung, D. W., Bradshaw, P. C., and Pfeiffer, D. R. (1997) J. Biol. Chem., 272, 21104–21112.

    Article  CAS  PubMed  Google Scholar 

  51. Carafoli, E., Balcavage, W. X., Lehninger, A. L., and Mattoon, R. (1970) Biochim. Biophys. Acta, 205, 18–26.

    Article  CAS  PubMed  Google Scholar 

  52. Lohret, T. A., and Kinnally, K. W. (1995) Biophys. J., 68, 2299–2309.

    Article  CAS  PubMed  Google Scholar 

  53. Kowaltowski, A. J., Vercesi, A. E., Rhee, S. G., and Netto, L. E. (2000) FEBS Lett., 473, 177–182.

    Article  CAS  PubMed  Google Scholar 

  54. Bradshaw, P. C., Jung, D. W., and Pfeiffer, D. G. (2001) J. Biol. Chem., 276, 40502–40509.

    Article  CAS  PubMed  Google Scholar 

  55. Kovaleva, M. V., Sukhanova, E. I., Trendeleva, T. A., Zyl’kova, M. V., Ural’skaya, L. A., Popova, K. M., Saris, N.-E., and Zvyagilskaya, R. A. (2009) J. Bioenerg. Biomembr., 41, 239–249.

    Article  CAS  PubMed  Google Scholar 

  56. Andreishcheva, E. N., Soares, I. M. I., and Zvyagilskaya, R. A. (1997) Fiziol. Rast., 44, 657–664.

    Google Scholar 

  57. Zvyagilskaya, R., Andreishcheva, E., Soares, I. M. I., Khozin, I., Berhe, A., and Persson, B. L. (2001) J. Basic Microbiol., 41, 283–303.

    Article  Google Scholar 

  58. Biryuzova, V. I., Zvyagilskaya, R. A., Malatyan, M. N., and Volkova, T. M. (1964) Mikrobiologiya, 33, 442–446.

    CAS  Google Scholar 

  59. Zvyagilskaya, R. A., Korosteleva, N. L., Mosolova, I. M., and Kotel’nikova, A. V. (1974) Biokhimiya, 39, 991–997.

    CAS  Google Scholar 

  60. Zvyagilskaya, R. A., and Kotel’nikova, A. V. (1991) Structure and Functional Activity of Yeast Mitochondria, in Series in Biological Chemistry, Vol. 36 [in Russian], VINITI, Moscow.

    Google Scholar 

  61. Deryabina, Y. I., Isakova, E. P., Shurubor, E. I., and Zvyagilskaya, R. A. (2004) Biochemistry (Moscow), 69, 1025–1033.

    Article  CAS  Google Scholar 

  62. Bazhenova, E. N., Deryabina, Yu. I., Eriksson, O., Zvyagilskaya, R. A., and Saris, N.-E. L. (1998) J. Biol. Chem., 273, 4372–4377.

    Article  CAS  PubMed  Google Scholar 

  63. Bazhenova, E. N., Saris, N.-E. L., Pentilla, T., and Zvyagilskaya, R. A. (1998) Biochim. Biophys. Acta, 1371, 96–100.

    Article  CAS  PubMed  Google Scholar 

  64. Deryabina, Y. I., and Zvyagilskaya, R. A. (2000) Biochemistry (Moscow), 65, 1352–1356.

    Article  CAS  Google Scholar 

  65. Deryabina, Y. I., Bazhenova, E. N., Saris, N. E., and Zvyagilskaya, R. A. (2001) J. Biol. Chem., 276, 47801–47806.

    CAS  PubMed  Google Scholar 

  66. Prieto, S., Bouillaud, F., Ricquier, D., and Rial, E. (1992) Eur. J. Biochem., 208, 487–491.

    Article  CAS  PubMed  Google Scholar 

  67. Prieto, S., Bouillaud, F., and Rial, E. (1995) Biochem. J., 307, 657–661.

    CAS  PubMed  Google Scholar 

  68. Prieto, S., Bouillaud, F., and Rial, E. (1996) Arch. Biochem. Biophys., 334, 43–49.

    Article  CAS  PubMed  Google Scholar 

  69. Guerin, B., Bunoust, O., Rouqueys, V., and Rigoulet, M. (1994) J. Biol. Chem., 269, 25406–25410.

    CAS  PubMed  Google Scholar 

  70. Manon, S., and Guerin, M. (1997) Biochim. Biophys. Acta, 1318, 317–321.

    Article  CAS  PubMed  Google Scholar 

  71. Manon, S., and Guerin, M. (1998) Biochem. Mol. Biol. Int., 44, 565–575.

    CAS  PubMed  Google Scholar 

  72. Manon, S., Roucou, X., Guerin, M., Rigoulet, M., and Guerin, M. (1998) J. Bioenerg. Biomembr., 30, 419–429.

    Article  CAS  PubMed  Google Scholar 

  73. Roucou, X., Manon, S., and Guerin, M. (1997) Biochem. Mol. Biol. Int., 43, 53–61.

    CAS  PubMed  Google Scholar 

  74. Castrejon, V., Pena, A., and Uribe, S. (2002) J. Bioenerg. Biomembr., 34, 299–306.

    Article  CAS  PubMed  Google Scholar 

  75. Perez-Vazquez, V., Saavedra-Molina, A., and Uribe, S. (2003) J. Bioenerg. Biomembr., 35, 231–241.

    Article  CAS  PubMed  Google Scholar 

  76. Gutierrez-Aguilar, M., Perez-Vazquez, V., Bunoust, O., Manon, S., Rigoulet, M., and Uribe, S. (2007) Biochim. Biophys. Acta, 1767, 1245–1251.

    Article  CAS  PubMed  Google Scholar 

  77. Mironova, G., Negoda, A., Marinov, B., Paucek, P., Costa, A., Grigoriev, S., Skarga, Yu., and Garlid, K. (2004) J. Biol. Chem., 279, 32562–32568.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Bach Institute of Biochemistry, Russian Academy of Sciences, Leninsky pr. 33, 119071, Moscow, Russia

    M. V. Kovaleva, E. I. Sukhanova, T. A. Trendeleva, K. M. Popova, M. V. Zylkova, L. A. Uralskaya & R. A. Zvyagilskaya

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  1. M. V. Kovaleva
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  2. E. I. Sukhanova
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  3. T. A. Trendeleva
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  4. K. M. Popova
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  5. M. V. Zylkova
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  6. L. A. Uralskaya
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  7. R. A. Zvyagilskaya
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Correspondence to R. A. Zvyagilskaya.

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Published in Russian in Biokhimiya, 2010, Vol. 75, No. 3, pp. 365–372.

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Kovaleva, M.V., Sukhanova, E.I., Trendeleva, T.A. et al. Induction of permeability of the inner membrane of yeast mitochondria. Biochemistry Moscow 75, 297–303 (2010). https://doi.org/10.1134/S0006297910030053

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