Biochemistry (Moscow)

, Volume 75, Issue 7, pp 825–831 | Cite as

Inorganic polyphosphates in mitochondria

  • T. V. KulakovskayaEmail author
  • L. P. Lichko
  • V. M. Vagabov
  • I. S. Kulaev


Current data concerning the crucial role of inorganic polyphosphates (polyP) in mitochondrial functions and dysfunctions in yeast and animal cells are reviewed. Biopolymers with short chain length (∼15 phosphate residues) were found in the mitochondria of Saccharomyces cerevisiae. They comprised 7–10% of the total polyP content of the cell. The polyP are located in the membranes and intermembrane space of mitochondria. The mitochondrial membranes possess polyP/Ca2+/polyhydroxybutyrate complexes. PolyP accumulation is typical of promitochondria but not of functionally active mitochondria. Yeast mitochondria possess two exopolyphosphatases splitting Pi from the end of the polyP chain. One of them, encoded by the PPX1 gene, is located in the matrix; the other one, encoded by the PPN1 gene, is membrane-bound. Formation of well-developed mitochondria in the cells of S. cerevisiae after glucose depletion is accompanied by decrease in the polyP level and the chain length. In PPN1 mutants, the polyP chain length increased under glucose consumption, and the formation of well-developed mitochondria was blocked. These mutants were defective in respiration functions and consumption of oxidizable carbon sources such as lactate and ethanol. Since polyP is a compound with high-energy bonds, its metabolism vitally depends on the cell bioenergetics. The maximal level of short-chain acid-soluble polyP was observed in S. cerevisiae under consumption of glucose, while the long-chain polyP prevailed under ethanol consumption. In insects, polyP in the mitochondria change drastically during ontogenetic development, indicating involvement of the polymers in the regulation of mitochondrial metabolism during ontogenesis. In human cell lines, specific reduction of mitochondrial polyP under expression of yeast exopolyphosphatase PPX1 significantly modulates mitochondrial bioenergetics and transport.

Key words

inorganic polyphosphate mitochondria polyP/Ca2+/polyhydroxybutyrate exopolyphosphatase membrane potential glucose repression yeast animal insect 





inorganic polyphosphates


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  1. 1.
    Kulaev, I. S. (1979) The Biochemistry of Inorganic Polyphosphates, Wiley, Chichester.Google Scholar
  2. 2.
    Kulaev, I. S., and Vagabov, V. M. (1983) Adv. Microbiol. Physiol., 24, 83–171.CrossRefGoogle Scholar
  3. 3.
    Kornberg, A., Rao, N., and Ault-Riche, D. (1999) Ann. Rev. Biochem., 68, 89–125.CrossRefPubMedGoogle Scholar
  4. 4.
    Kulaev I., Vagabov, V., and Kulakovskaya, T. (1999) J. Biosci. Bioeng., 88, 111–129.CrossRefPubMedGoogle Scholar
  5. 5.
    Kulaev, I. S., and Kulakovskaya, T. V. (2000) Ann. Rev. Microbiol., 54, 709–735.CrossRefGoogle Scholar
  6. 6.
    Kulaev, I. S., Vagabov, V. M., and Kulakovskaya, T. V. (2004) The Biochemistry of Inorganic Polyphosphates, Wiley, Chichester.CrossRefGoogle Scholar
  7. 7.
    Omelon, S. J., and Grynpas, M. D. (2008) Chem. Rev., 208, 4694–4715.CrossRefGoogle Scholar
  8. 8.
    Rao, N. N., Gomez-Garcia, M. R., and Kornberg, A. (2009) Ann. Rev. Biochem., 78, 605–647.CrossRefPubMedGoogle Scholar
  9. 9.
    Woese, C. R., Kandler, O., and Wheekis, M. L. (1990) Proc. Natl. Acad. Sci. USA, 87, 4576–4579.CrossRefPubMedGoogle Scholar
  10. 10.
    Margulis, L. (1993) Symbiosis in Cell Evolution, Freeman, San Francisco.Google Scholar
  11. 11.
    Nelson, N. (1992) Biochim. Biophys. Acta, 1100, 109–124.CrossRefPubMedGoogle Scholar
  12. 12.
    Baltscheffsky, H. (1997) J. Theor. Biol., 187, 495–501.CrossRefPubMedGoogle Scholar
  13. 13.
    Cavalier-Smith, T. (2006) Philos. Trans. Roy. Soc. B, 361, 969–1006.CrossRefGoogle Scholar
  14. 14.
    Clements, A., Bursac, D., Gatsos, X., Perry, A. J., Civciristov, S., Celik, N., Likic, V. A., Poggio, S., Jacobs-Wagner, C., Strugnell, R. A., and Lithgow, T. (2009) Proc. Natl. Acad. Sci. USA, 106, 15791–15795.CrossRefPubMedGoogle Scholar
  15. 15.
    Kulaev, I. S., Mansurova, S. E., and Vagabov, V. M. (1982) in Biological Reviews (Skulachev, V. P., ed.) Vol. 3, Cambridge University Press, London, pp. 26–57.Google Scholar
  16. 16.
    Mansurova, S. E. (1989) Biochim. Biophys. Acta, 977, 237–247.CrossRefPubMedGoogle Scholar
  17. 17.
    Tuena de Gomez-Puyou, M., de Jesus Garcia, J., and Gomez-Puyou, A. (1993) Biochemistry, 32, 2213–2218.CrossRefPubMedGoogle Scholar
  18. 18.
    Smirnova, I. N., Kasho, V. N., Volk, S. E., Ivanov, A. H., and Baykov, A. A. (1995) Arch. Biochem. Biophys., 318, 340–348.CrossRefPubMedGoogle Scholar
  19. 19.
    Baykov, A. A., Cooperman, B. S., Goldman, A., and Lahti, R. (1999) in Inorganic Polyphosphates. Biochemistry, Biology, Biotechnology, Prog. Mol. Cell. Biol. (Schroder, H. C., and Muller, W. E. G., eds.) Vol. 23, Springer, Berlin, pp. 127–150.Google Scholar
  20. 20.
    Serrano, A., Perez-Castineira, J. R., Baltscheffsky, M., and Baltscheffsky, H. (2007) IUBMB Life, 59, 76–83.CrossRefPubMedGoogle Scholar
  21. 21.
    Lichko, L. P., Andreeva, N. A., Kulakovskaya, T. V., and Kulaev, I. S. (2003) FEMS Yeast Res., 3, 233–238.CrossRefPubMedGoogle Scholar
  22. 22.
    Hothorn, M., Neumann, H., Lenherr, E. D., Wehner, M., Rybin, V., Hassa, P. O., Uttenweiler, A., Reinhardt, M., Schmidt, A., Seiler, J., Ladurner, A. G., Herrmann, C., Scheffzek, K., and Mayer, A. (2009) Science, 324, 513–516.CrossRefPubMedGoogle Scholar
  23. 23.
    Kumble, K. D., and Kornberg, A. (1996) J. Biol. Chem., 271, 27146–27151.CrossRefPubMedGoogle Scholar
  24. 24.
    Beauvoit, B., Rigonlet, M., Guerin, B., and Canioni, P. (1989) FEBS Lett., 252, 17–22.CrossRefGoogle Scholar
  25. 25.
    Pestov, N. A., Kulakovskaya, T. V., and Kulaev, I. S. (2004) FEMS Yeast Res., 4, 643–648.CrossRefPubMedGoogle Scholar
  26. 26.
    Pestov, N. A. (2004) Polyphosphates and Exopolyphosphatases of Mitochondria of Yeast Saccharomyces cerevisiae: PhD Thesis [in Russian], Pushchino.Google Scholar
  27. 27.
    Andreeva, N. A., Kulakovskaya, T. V., Kulakovskaya, E. V., and Kulaev, I. S. (2008) Biochemistry (Moscow), 73, 65–69.Google Scholar
  28. 28.
    Vagabov, V. M., Trilisenko, L. V., and Kulaev, I. S. (2000) Biochemistry (Moscow), 65, 349–354.Google Scholar
  29. 29.
    Campos, E., Facanha, A., Moraes, J., da Silva Vaz, I., Jr., Masuda, A., and Logullo, C. (2007) Insect Biochem. Mol. Biol., 37, 1103–1107.CrossRefPubMedGoogle Scholar
  30. 30.
    Reusch, R. N. (1989) Roc. Soc. Exp. Biol. Med., 191, 377–381.Google Scholar
  31. 31.
    Reusch, R. N. (1992) FEMS Rev., 103, 119–130.Google Scholar
  32. 32.
    Reusch, R. N. (1999) in Inorganic Polyphosphates. Biochemistry, Biology, Biotechnology, Prog. Mol. Cell. Biol. (Schroder, H. C., and Muller, W. E. G., eds.) Vol. 23, Springer, Berlin, pp. 151–183.Google Scholar
  33. 33.
    Reusch, R. N. (2000) Biochemistry (Moscow), 65, 280–295.Google Scholar
  34. 34.
    Pavlov, E., Zakharian., E., Bladen, C., Diao, C. T. M., Grimbly, C., Reusch, R. N., and French, R. J. (2005) Biophys. J., 88, 2614–2625.CrossRefPubMedGoogle Scholar
  35. 35.
    Lichko, L. P., Kulakovskaya, T. V., and Kulaev, I. S. (1998) Biochim. Biophys. Acta, 1372, 153–162.CrossRefPubMedGoogle Scholar
  36. 36.
    Lichko, L., Pestov, N., Kulakovskaya, T., and Kulaev, I. (2006) Biosci. Rep., 26, 45–54.CrossRefPubMedGoogle Scholar
  37. 37.
    Wurst, H., Shiba, T., and Kornberg, A. (1995) J. Bacteriol., 177, 898–906.PubMedGoogle Scholar
  38. 38.
    Sethuraman, A., Rao, N. N., and Kornberg, A. (2001) Proc. Natl. Acad. Sci. USA, 98, 8542–8547.CrossRefPubMedGoogle Scholar
  39. 39.
    Pestov, N. A., Kulakovskaya, T. V., and Kulaev, I. S. (2005) FEMS Yeast Res., 5, 823–828.CrossRefPubMedGoogle Scholar
  40. 40.
    Zinzer, E., and Daum, G. (1995) Yeast, 11, 493–536.CrossRefGoogle Scholar
  41. 41.
    Daum, G., Bohni, P. C., and Schatz, G. (1982) J. Biol. Chem., 257, 13028–13033.PubMedGoogle Scholar
  42. 42.
    Vagabov, V. M., Trilisenko, L. V., Kulakovskaya, T. V., and Kulaev, I. S. (2008) FEMS Yeast Res., 8, 877–882.CrossRefPubMedGoogle Scholar
  43. 43.
    Meijer, M. M. C., Boonstra, J., Verkleij, A. J., and Verrips, C. T. (1998) J. Biol. Chem., 278, 24102–24107.CrossRefGoogle Scholar
  44. 44.
    Kulakovskaya, T. V., Andreeva, N. A., Karpov, A. V., Sidorov, I. A., and Kulaev, I. S. (1997) Biochemistry (Moscow), 64, 990–993.Google Scholar
  45. 45.
    Abramov, A. Y., Fraley, C., Diao, C. T., Winkfein, R., Colicos, M. A., Duchen, M. R., French, R. J., and Pavlov, E. (2007) Proc. Natl. Acad. Sci. USA, 13, 18091–18096.CrossRefGoogle Scholar
  46. 46.
    Streichan, M. J., Golecki, R., and Schon, G. (1990) FEMS Microbiol. Ecol., 73, 113–124.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  • T. V. Kulakovskaya
    • 1
    Email author
  • L. P. Lichko
    • 1
  • V. M. Vagabov
    • 1
  • I. S. Kulaev
    • 1
  1. 1.Skryabin Institute of Biochemistry and Physiology of MicroorganismsRussian Academy of SciencesPushchino, Moscow RegionRussia

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