Biochemistry (Moscow)

, Volume 74, Issue 4, pp 371–376 | Cite as

Features of mitochondrial energetics in living unicellular eukaryote Tetrahymena pyriformis. A model for study of mammalian intracellular adaptation

  • E. A. Prikhodko
  • I. V. Brailovskaya
  • S. M. Korotkov
  • E. N. MokhovaEmail author
Accelerated Publication


Tetrahymena pyriformis is used in diverse studies as a non-mammalian alternative due to their resemblance in many main metabolic cycles. However, such basic features of mitochondrial energetics as ΔΨ (electrical potential difference across the inner mitochondrial membrane) or maximal stimulation of respiration by uncouplers with different mechanisms of uncoupling, such as DNP (2,4-dinitrophenol) and FCCP (p-trifluoromethoxycarbonylcyanide phenylhydrazone), have not been studied in living ciliates. Tetrahymena pyriformis GL cells during stationary growth phase after incubation under selected conditions were used in this study. Maximal stimulation of cellular respiration by FCCP was about six-fold, thus the proton motive force was high. The DNP uncoupling effect was significantly lower. This suggests low activity of the ATP/ADP-antiporter, which performs not only exchange of intramitochondrial ATP to extramitochondrial ADP, but also helps in the uncoupling process. It participates by a similar mechanism in electrophoretic transport from matrix to cytosol of ATP4− and DNP anion, but not FCCP anion. Thus, in contrast with mammalian mitochondria, T. pyriformis mitochondria cannot rapidly supply the cytosol with ATP; possibly the cells need high intramitochondrial ATP. The difference between DNP and FCCP is hypothetically explained by low ΔΨ value and/or an increase in concentration of long-chain acyl-CoAs, inhibitors of the ATP/ADP-antiporter. The first suggestion is confirmed by absence of mitochondria with bright fluorescence in T. pyriformis stained with the ΔΨ-sensitive probe MitoTracker Red. These data suggest that T. pyriformis cells are useful as a model for study of mitochondrial role in adaptation at the intracellular level.

Key words

ATP/ADP-antiporter membrane potential mitochondria Tetrahymena pyriformis uncouplers DNP intracellular adaptation 



bovine serum albumin




p-trifluoromethoxycarbonylcyanide phenylhydrazone


transmembrane difference of electrical potential across the inner mitochondrial membrane


difference in hydrogen ion concentrations between the two sides of the inner mitochondrial membrane


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Levy, M. R. (1973) in Biology of Tetrahymena (Elliott, A. M., ed.) Dowden, Hutchinson and Ross, Inc, Stroudsburg, Pennsylvania, pp. 227–257.Google Scholar
  2. 2.
    Hutner, S. H., Baker, H., Frank, O., and Cox, D. (1973) in Biology of Tetrahymena (Elliott, A. M., ed.) Dowden, Hutchinson and Ross, Inc, Stroudsburg, Pennsylvania, pp. 411–433.Google Scholar
  3. 3.
    Kohidai, L., Vakkuri, O., Keresztesi, M., Leppaluoto, J., and Csaba, G. (2002) Cell Biochem. Funct., 20, 269–272.PubMedCrossRefGoogle Scholar
  4. 4.
    Csaba, G., and Pallinger, E. (2008) Cell Biochem. Funct., 26, 303–308.PubMedCrossRefGoogle Scholar
  5. 5.
    Sauvant, M. P., Pepin, D., and Piccini, E. (1999) Chemosphere, 38, 1631–1669.PubMedCrossRefGoogle Scholar
  6. 6.
    Kilpatrick, L., and Erecinska, M. (1977) Biochim. Biophys. Acta, 460, 346–363.PubMedCrossRefGoogle Scholar
  7. 7.
    Mitchell, P. (1961) Nature, 191, 144–148.PubMedCrossRefGoogle Scholar
  8. 8.
    Skulachev, V. P. (1988) Membrane Bioenergetics, Springer-Verlag, Berlin.Google Scholar
  9. 9.
    Kramer, R., and Klingenberg, M. (1980) Biochemistry, 19, 556–560.PubMedCrossRefGoogle Scholar
  10. 10.
    Vignais, P. V., Block, M. R., Boulay, F., Brandolin, V., and Lauquin, G. J. M. (1985) in Structure and Properties of Cell. Membrane (Bengha, V., ed.) Vol. 2, CRC Press, Paris, pp. 139–179.Google Scholar
  11. 11.
    Andreyev, A. Yu., Bondareva, T. O., Dedukhova, V. I., Mokhova, E. N., Skulachev, V. P., Tsofina, L. M., Volkov, N. I., and Vygodina, T. V. (1989) Eur. J. Biochem., 182, 585–592.PubMedCrossRefGoogle Scholar
  12. 12.
    Skulachev, V. P. (1998) Biochim. Biophys. Acta, 1363, 100–124.PubMedCrossRefGoogle Scholar
  13. 13.
    Mokhova, E. N., and Khailova, L. S. (2005) Biochemistry. (Moscow), 70, 159–163.CrossRefGoogle Scholar
  14. 14.
    Skulachev, V. P. (1991) FEBS Lett., 294, 158–162.PubMedCrossRefGoogle Scholar
  15. 15.
    Starkov, A. A., Dedukhova, V. I., and Skulachev, V. P. (1994) FEBS Lett., 355, 305–308.PubMedCrossRefGoogle Scholar
  16. 16.
    Starkov, A. A., Bloch, D. A., Chernyak, B. V., Dedukhova, V. I., Mansurova, S. E., Severina, I. I., Simonyan, R. A., Vygodina, T. V., and Skulachev, V. P. (1997) Biochim. Biophys. Acta, 1318, 159–172.PubMedCrossRefGoogle Scholar
  17. 17.
    Starkov, A. A. (2006) Chem. Biol. Interact., 161, 57–68.PubMedCrossRefGoogle Scholar
  18. 18.
    Brailovskaya, I. V., Kudryavtseva, T. A., Larionov, V. N., Prikhodko, E. A., and Mokhova, E. N. (2007) Doklady. Biokhim. Biofiz., 413, 72–75.Google Scholar
  19. 19.
    Akerman, K. E., and Wikstrom, M. K. (1976) FEBS Lett., 68, 191–197.PubMedCrossRefGoogle Scholar
  20. 20.
    Sobierajska, K., Fabczak, H., and Fabczak, S. (2006) J. Photochem. Photobiol. B, Biol., 83, 163–171.PubMedCrossRefGoogle Scholar
  21. 21.
    Markova, O. V., Mokhova, E. N., and Tarakanova, A. N. (1990) J. Bioenerg. Biomembr., 22, 51–59.PubMedCrossRefGoogle Scholar
  22. 22.
    Holcomb, M., Cloud, J. G., Woolsey, J., and Ingermann, R. L. (2004) Comp. Biochem. Physiol., Part A. Mol. Integr. Physiol., 138, 349–354.PubMedCrossRefGoogle Scholar
  23. 23.
    Elliott, A. M., and Bak, I. J. (1964) J. Cell Biol., 20, 113–129.PubMedCrossRefGoogle Scholar
  24. 24.
    Chernyak, B. V., Izyumov, D. S., Lyamzaev, K. G., Pashkovskaya, A. A., Pletjushkina, O. Y., Antonenko, Y. N., Sakharov, D. V., Wirtz, K. W., and Skulachev, V. P. (2006) Biochim. Biophys. Acta, 1757, 525–534.PubMedCrossRefGoogle Scholar
  25. 25.
    Liberman, E. A., Mokhova, E. N., Skulachev, V. P., and Topaly, V. P. (1968) Biofizika, 13, 188–193.PubMedGoogle Scholar
  26. 26.
    Mitchell, P., and Moyle, J. (1967) Biochem. J., 104, 588–600.PubMedGoogle Scholar
  27. 27.
    Brustovetsky, N. N., Dedukhova, V. I., Egorova, M. V., Mokhova, E. N., and Skulachev, V. P. (1991) FEBS Lett., 295, 51–54.CrossRefGoogle Scholar
  28. 28.
    Samartsev, V. N., Smirnov, A. V., Zeldi, I. P., Markova, O. V., Mokhova, E. N., and Skulachev, V. P. (1997) Biochim. Biophys. Acta, 1319, 251–257.PubMedCrossRefGoogle Scholar
  29. 29.
    Skulachev, V. P. (2003) in Selected Topics in the History of. Biochemistry: Personal Recollections VII (Comprehensive. Biochemistry) (Semenza, G., and Turner, A. J., eds.) Vol. 42, Elsevier Science B. V., pp. 319–410.Google Scholar
  30. 30.
    Kobayashi, T., and Endoh, H. (2005) FEBS J., 272, 5378–5387.PubMedCrossRefGoogle Scholar
  31. 31.
    Lerner, E., Shug, A. L., Elson, C., and Shrago, E. (1972) J. Biol. Chem., 247, 1513–1519.PubMedGoogle Scholar
  32. 32.
    Panov, A. V., Konstantinov, Y. M., and Lyakhovich, V. V. (1975) J. Bioenerg., 7, 75–85.PubMedCrossRefGoogle Scholar
  33. 33.
    Dias, N., Mortara, R. A., and Lima, N. (2003) Toxicol. in. vitro, 17, 357–366.PubMedGoogle Scholar
  34. 34.
    Prlina, I. S., Gabova, A. V., Raikov, I. B., and Tairbekov, M. G. (1989) Tsitologiya, 31, 829–838.Google Scholar
  35. 35.
    Brdiczka, D., Zorov, D. B., and Sheu, S. S. (2006) Biochim. Biophys. Acta, 1762, 148–163.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2009

Authors and Affiliations

  • E. A. Prikhodko
    • 1
    • 2
  • I. V. Brailovskaya
    • 3
  • S. M. Korotkov
    • 3
  • E. N. Mokhova
    • 1
    Email author
  1. 1.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia
  2. 2.Faculty of Bioengineering and BioinformaticsLomonosov Moscow State UniversityMoscowRussia
  3. 3.Sechenov Institute of Evolutionary Physiology and BiochemistryRussian Academy of SciencesSt. PetersburgRussia

Personalised recommendations