Biochemistry (Moscow)

, Volume 75, Issue 3, pp 297–303 | Cite as

Induction of permeability of the inner membrane of yeast mitochondria

  • M. V. Kovaleva
  • E. I. Sukhanova
  • T. A. Trendeleva
  • K. M. Popova
  • M. V. Zylkova
  • L. A. Uralskaya
  • R. A. ZvyagilskayaEmail author


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.

Key words

mitochondria yeasts Yarrowia lipolytica Dipodascus (Endomyces) magnusii Ca2+ inorganic phosphate saturated fatty acids pH membrane potential swelling pore apoptosis 



cyclosporin A


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


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


inorganic phosphate


yeast mitochondrial unspecific channel


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Circu, M. L., and Aw, T. Y. (2008) Free Radic. Res., 1, 1–18.Google Scholar
  2. 2.
    Hanada, M., Aime-Sempe, C., Sato, T., and Reed, J. C. (1995) J. Biol. Chem., 270, 11962–11969.CrossRefPubMedGoogle Scholar
  3. 3.
    Priault, M., Cartron, P. F., Camougrand, N., Antonsson, D., Vallette, F. M., and Manon, S. (2003) Cell. Death Differ., 10, 1068–1077.CrossRefPubMedGoogle Scholar
  4. 4.
    Madeo, F., Frolich, E., and Frohlich, K. U. (1997) J. Cell Biol., 139, 729–734.CrossRefPubMedGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. 7.
    Almeida, B., Silva, A., Mesquita, A., Sampaio-Marques, B., Rodrigues, F., and Ludovico, P. (2008) Biochim. Biophys. Acta, 1783, 1436–1448.CrossRefPubMedGoogle Scholar
  8. 8.
    Eisenberg, T., Buttner, S., and Kroemer, G. (2007) Apoptosis, 12, 1011–1023.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. 10.
    Madeo, F., Herker, E., Wissing, S., Jungwirth, H., Eisenberg, T., and Frohlich, K. U. (2004) Curr. Opin. Microbiol., 7, 655–660.CrossRefPubMedGoogle Scholar
  11. 11.
    Madeo, F., and Frohlich, K. U. (2008) Biochim. Biophys. Acta, 1783, 1271.CrossRefPubMedGoogle Scholar
  12. 12.
    Perrone, G. G., Tan, S. X., and Dawes, I. W. (2008) Biochim. Biophys. Acta, 1783, 1354–1368.CrossRefPubMedGoogle Scholar
  13. 13.
    Reiter, J., Herker, E., Madeo, F., and Schmitt, M. J. (2005) Cell Biol., 168, 353–358.CrossRefGoogle Scholar
  14. 14.
    Schmitt, M. J., and Reiter, J. (2008) Biochim. Biophys. Acta, 1783, 1413–1417.CrossRefPubMedGoogle Scholar
  15. 15.
    Severin, F. F., Meer, M. V., Smirnova, E. A., Knorre, D. A., and Skulachev, V. P. (2008) Biochim. Biophys. Acta, 1783, 1350–1353.CrossRefPubMedGoogle Scholar
  16. 16.
    Laun, P., Rinnerthaler, M., Bogengruber, E., Heeren, G., and Breitenbach, M. (2006) Exp. Gerontol., 241, 1208–1212.CrossRefGoogle Scholar
  17. 17.
    Laun, P., Heeren, G., Rinnerthaler, M., Rid, R., Kossler, S., Koller, L., and Breitenbach, M. (2008) Biochim. Biophys. Acta, 1783, 1328–1334.CrossRefPubMedGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. 19.
    Fahrenkrog, B., Sauder, U., and Aebi, U. (2004) J. Cell. Sci., 117, 115–126.CrossRefPubMedGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. 22.
    Ludovico, P., Rodrigues, F., Almeida, A., Silva, M. T., Barrientos, A., and Corte-Real, M. (2002) Mol. Biol. Cell, 13, 2598–2606.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. 25.
    Cymerman, I. A., Chung, I., Beckmann, B. M., Bujnicki, J. M., and Meiss, G. (2008) Nucleic Acids Res., 36, 1369–1379.CrossRefPubMedGoogle Scholar
  26. 26.
    Singh, K., Kang, P. J., and Park, H. O. (2008) Proc. Natl. Acad. Sci. USA, 105, 1522–1527.CrossRefPubMedGoogle Scholar
  27. 27.
    Owsianowski, E., Walter, D., and Fahrenkrog, B. (2008) Biochim. Biophys. Acta, 1783, 1303–1310.CrossRefPubMedGoogle Scholar
  28. 28.
    Kerscher, S., Durstewitz, G., Casaregola, S., Gaillardin, C., and Brandt, U. (2001) Comp. Funct. Genom., 2, 80–90.CrossRefGoogle Scholar
  29. 29.
    Webb, J. S., Givskov, M., and Kjelleberg, S. (2003) Curr. Opin. Microbiol., 6, 578–585.CrossRefPubMedGoogle Scholar
  30. 30.
    Palkova, Z. (2004) EMBO Rep., 5, 470–476.CrossRefPubMedGoogle Scholar
  31. 31.
    Vachova, L., Kucerova, H., Devaux, F., Ultholova, M., and Palkova, Z. (2009) Environ. Microbiol., 11, 494–504.CrossRefPubMedGoogle Scholar
  32. 32.
    Smardova, J., Smarda, J., and Koptikova, J. (2005) Differention, 73, 261–277.CrossRefGoogle Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 34.
    Sheridan, C., Delivani, P., Cullen, S. P., and Martin, S. J. (2008) Mol. Cell, 31, 570–585.CrossRefPubMedGoogle Scholar
  35. 35.
    Colin, J., Garibal, J., Mignotte, B., and Guenal, I. (2009) Biochem. Biophys. Res. Commun., 379, 931–943.CrossRefGoogle Scholar
  36. 36.
    Lucken-Ardjomande, S., Montessuit, S., and Martinou, J. C. (2008) Cell Death Differ., 15, 923–937.Google Scholar
  37. 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.CrossRefPubMedGoogle Scholar
  38. 38.
    Halestrap, A. P. (2009) J. Mol. Cardiol., 46, 821–831.CrossRefGoogle Scholar
  39. 39.
    Leung, A. W., and Halestrap, A. P. (2008) Biochim. Biophys. Acta, 1777, 946–952.CrossRefPubMedGoogle Scholar
  40. 40.
    Sultan, A., and Sokolove, P. (2001) Arch. Biochem. Biophys., 386, 52–61.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar
  42. 42.
    Kristian, T., Bernardi, P., and Siesjo, B. K. (2001) J. Neurotrauma, 18, 1059–1074.CrossRefPubMedGoogle Scholar
  43. 43.
    Knorre, D. A., Dedukhova, V. I., Vyssokikh, M. Y., and Mokhova, E. N. (2003) Biosci. Rep., 23, 67–75.CrossRefPubMedGoogle Scholar
  44. 44.
    Gao, W., Pu, Y., Luo, K. Q., and Chang, D. C. (2001) J. Cell Sci., 114, 2855–2862.PubMedGoogle Scholar
  45. 45.
    Gogvadze, V., Robertson, J. D., Enoksson, M., Zhivotovsky, B., and Orrenius, S. (2004) Biochem. J., 378, 213–217.CrossRefPubMedGoogle Scholar
  46. 46.
    Ott, M., Robertson, J. D., Gogvadze, V., Zhivotovsky, B., and Orrenius, S. (2002) Proc. Natl. Acad. Sci. USA, 99, 1259–1263.CrossRefPubMedGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. 48.
    Mironova, G. D., Kachaeva, E. V., and Kopylov, A. T. (2007) Vestnik RAMN, 2, 44–50.Google Scholar
  49. 49.
    Costa, A. D., and Garlid, K. D. (2009) J. Bioenerg. Biomembr., 41, 123–126.CrossRefPubMedGoogle Scholar
  50. 50.
    Jung, D. W., Bradshaw, P. C., and Pfeiffer, D. R. (1997) J. Biol. Chem., 272, 21104–21112.CrossRefPubMedGoogle Scholar
  51. 51.
    Carafoli, E., Balcavage, W. X., Lehninger, A. L., and Mattoon, R. (1970) Biochim. Biophys. Acta, 205, 18–26.CrossRefPubMedGoogle Scholar
  52. 52.
    Lohret, T. A., and Kinnally, K. W. (1995) Biophys. J., 68, 2299–2309.CrossRefPubMedGoogle Scholar
  53. 53.
    Kowaltowski, A. J., Vercesi, A. E., Rhee, S. G., and Netto, L. E. (2000) FEBS Lett., 473, 177–182.CrossRefPubMedGoogle Scholar
  54. 54.
    Bradshaw, P. C., Jung, D. W., and Pfeiffer, D. G. (2001) J. Biol. Chem., 276, 40502–40509.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefPubMedGoogle Scholar
  56. 56.
    Andreishcheva, E. N., Soares, I. M. I., and Zvyagilskaya, R. A. (1997) Fiziol. Rast., 44, 657–664.Google Scholar
  57. 57.
    Zvyagilskaya, R., Andreishcheva, E., Soares, I. M. I., Khozin, I., Berhe, A., and Persson, B. L. (2001) J. Basic Microbiol., 41, 283–303.CrossRefGoogle Scholar
  58. 58.
    Biryuzova, V. I., Zvyagilskaya, R. A., Malatyan, M. N., and Volkova, T. M. (1964) Mikrobiologiya, 33, 442–446.Google Scholar
  59. 59.
    Zvyagilskaya, R. A., Korosteleva, N. L., Mosolova, I. M., and Kotel’nikova, A. V. (1974) Biokhimiya, 39, 991–997.Google Scholar
  60. 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. 61.
    Deryabina, Y. I., Isakova, E. P., Shurubor, E. I., and Zvyagilskaya, R. A. (2004) Biochemistry (Moscow), 69, 1025–1033.CrossRefGoogle Scholar
  62. 62.
    Bazhenova, E. N., Deryabina, Yu. I., Eriksson, O., Zvyagilskaya, R. A., and Saris, N.-E. L. (1998) J. Biol. Chem., 273, 4372–4377.CrossRefPubMedGoogle Scholar
  63. 63.
    Bazhenova, E. N., Saris, N.-E. L., Pentilla, T., and Zvyagilskaya, R. A. (1998) Biochim. Biophys. Acta, 1371, 96–100.CrossRefPubMedGoogle Scholar
  64. 64.
    Deryabina, Y. I., and Zvyagilskaya, R. A. (2000) Biochemistry (Moscow), 65, 1352–1356.CrossRefGoogle Scholar
  65. 65.
    Deryabina, Y. I., Bazhenova, E. N., Saris, N. E., and Zvyagilskaya, R. A. (2001) J. Biol. Chem., 276, 47801–47806.PubMedGoogle Scholar
  66. 66.
    Prieto, S., Bouillaud, F., Ricquier, D., and Rial, E. (1992) Eur. J. Biochem., 208, 487–491.CrossRefPubMedGoogle Scholar
  67. 67.
    Prieto, S., Bouillaud, F., and Rial, E. (1995) Biochem. J., 307, 657–661.PubMedGoogle Scholar
  68. 68.
    Prieto, S., Bouillaud, F., and Rial, E. (1996) Arch. Biochem. Biophys., 334, 43–49.CrossRefPubMedGoogle Scholar
  69. 69.
    Guerin, B., Bunoust, O., Rouqueys, V., and Rigoulet, M. (1994) J. Biol. Chem., 269, 25406–25410.PubMedGoogle Scholar
  70. 70.
    Manon, S., and Guerin, M. (1997) Biochim. Biophys. Acta, 1318, 317–321.CrossRefPubMedGoogle Scholar
  71. 71.
    Manon, S., and Guerin, M. (1998) Biochem. Mol. Biol. Int., 44, 565–575.PubMedGoogle Scholar
  72. 72.
    Manon, S., Roucou, X., Guerin, M., Rigoulet, M., and Guerin, M. (1998) J. Bioenerg. Biomembr., 30, 419–429.CrossRefPubMedGoogle Scholar
  73. 73.
    Roucou, X., Manon, S., and Guerin, M. (1997) Biochem. Mol. Biol. Int., 43, 53–61.PubMedGoogle Scholar
  74. 74.
    Castrejon, V., Pena, A., and Uribe, S. (2002) J. Bioenerg. Biomembr., 34, 299–306.CrossRefPubMedGoogle Scholar
  75. 75.
    Perez-Vazquez, V., Saavedra-Molina, A., and Uribe, S. (2003) J. Bioenerg. Biomembr., 35, 231–241.CrossRefPubMedGoogle Scholar
  76. 76.
    Gutierrez-Aguilar, M., Perez-Vazquez, V., Bunoust, O., Manon, S., Rigoulet, M., and Uribe, S. (2007) Biochim. Biophys. Acta, 1767, 1245–1251.CrossRefPubMedGoogle Scholar
  77. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  • M. V. Kovaleva
    • 1
  • E. I. Sukhanova
    • 1
  • T. A. Trendeleva
    • 1
  • K. M. Popova
    • 1
  • M. V. Zylkova
    • 1
  • L. A. Uralskaya
    • 1
  • R. A. Zvyagilskaya
    • 1
    Email author
  1. 1.Bach Institute of BiochemistryRussian Academy of SciencesMoscowRussia

Personalised recommendations