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Interaction of tetraphenylphosphonium and dodecyltriphenylphosphonium with lipid membranes and mitochondria

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Abstract

The permeability of a planar lipid membrane (composed of diphytanoylphosphatidylcholine) for tetraphenylphosphonium (TPP) was investigated. The observed level of the diffusion potential generated as a function of the TPP concentration gradient differed from the theoretically expected value, possibly due to proton leakage of the membrane mediated by the traces of fatty acids in the phospholipid forming the membrane. Using the molecular dynamics approach to study movement of TPP and dodecyltriphenylphosphonium (C12TPP) with different affinity to the lipid bilayer through a bilayer lipid membrane, it was found that C12TPP has a greater affinity to the membrane surface than TPP. However, the two cations have the same activation energy for transmembrane transfer. Interaction of TPP and C12TPP with tightly-coupled mitochondria from the yeast Yarrowia lipolytica was also investigated. At low, micromolar concentrations, both cations are “relatively weak, mild uncouplers”, do not shunt electron transfer along the respiratory chain, do not disturb (damage) the inner mitochondrial membrane, and profoundly promote the uncoupling effect of fatty acids. At higher concentrations they inhibit respiration in state 3, and at much higher concentrations they induce swelling of mitochondria, possibly due to their detergent action.

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Abbreviations

Ala:

alamethicin

CCCP:

carbonyl cyanide m-chlorophenylhydrazone

C12TPP:

dodecyltriphenylphosphonium

MES:

2-(N-morpholino)ethanesulfonic acid

ROS:

reactive oxygen species

TPP:

tetraphenylphosphonium

ΔΨ :

trans-membrane electric potential difference

References

  1. Liberman, E. A., Topaly, V. P., Tsofina, L. M., Jasaitis, A. A., and Skulachev, V. P. (1969) Nature, 222, 1076–1078.

    Article  PubMed  CAS  Google Scholar 

  2. Skulachev, V. P., Sharaf, A. A., and Liberman, E. A. (1967) Nature, 16, 718–719.

    Article  Google Scholar 

  3. Skulachev, V. P. (1970) FEBS Lett., 11, 301–308.

    Article  PubMed  CAS  Google Scholar 

  4. Green, D. E. (1974) Biochim. Biophys. Acta, 346, 27–78.

    Article  PubMed  CAS  Google Scholar 

  5. Skulachev, V. P., Anisimov, V. N., Antonenko, Yu. N., Bakeeva, L. E., Chernyak, B. V., Erichev, V. P., Filenki, O. F., Kalinina, N. I., Kapelko, V. I., Kolosova, N. G., Kopnin, B. P., Korshunova, G. A., Lichinitser, M. R., Obukhova, L. A., Pasyukova, E. G., Pisarenko, O. I., Roginsky, V. A., Ruuge, E. K., Senin, I. I., Severina, I. I., Skulachev, M. V., Spivak, I. M., Tashlitsky, B. N., Tkachuk, V. A., Vyssokikh, M. Yu., Jaguzhinsky, L. S., and Zorov, D. B. (2009) Biochim. Biophys. Acta, 1782, 437–461.

    Google Scholar 

  6. Smith, R. A., Porteous, C. M., Coulter, C. V., and Murphy, M. P. (1999) Eur. J. Biochem., 263, 709–716.

    Article  PubMed  CAS  Google Scholar 

  7. Murphy, M. P., Echtay, K. S., Blaikie, F. H., Asin-Cayuela, J., Cocheme, H. M., Green, K., Buckingham, J. A., Taylor, E. R., Hurrell, F., Hughes, G., Miwa, S., Cooper, C. E., Svistunenko, D. A., Smith, R. A., and Brand, M. D. (2003) J. Biol. Chem., 278, 48534–48545.

    Article  PubMed  CAS  Google Scholar 

  8. Brown, S. E., Ross, M. F., Sanjuan-Pla, A., Manas, A. R., Smith, R. A., and Murphy, M. P. (2007) Free Radic. Biol. Med., 42, 1766–1780.

    Article  PubMed  CAS  Google Scholar 

  9. Antonenko, Y. N., Avetisyan, A. V., Bakeeva, L. E., Chernyak, B. V., Chertkov, V. A., Domnina, L. V., Ivanova, O. Y., Izyumov, D. S., Khailova, L. S., Klishin, S. S., Korshunova, G. A., Lyamzaev, K. G., Muntyan, M. S., Nepryakhina, O. K., Pashkovskaya, A. A., Pletjushkina, O. Y., Pustovidko, A. V., Roginsky, V. A., Rokitskaya, T. I., Ruuge, E. K., Saprunova, V. B., Severina, I. I., Simonyan, R. A., Skulachev, I. V., Skulachev, M. V., Sumbatyan, N. V., Sviryaeva, I. V., Tashlitsky, V. N., Vassiliev, J. M., Vyssokikh, M. Y., Yaguzhinsky, L. S., Zamyatnin, A. A., Jr., and Skulachev, V. P. (2008) Biochemistry (Moscow), 73, 1273–1287.

    Article  CAS  Google Scholar 

  10. Skulachev, M. V., Antonenko, Y. N., Anisimov, V. N., Chernyak, B. V., Cherepanov, D. A., Chistyakov, V. A., Egorov, M. V., Kolosova, N. G., Korshunova, G. A., Lyamzaev, K. G., Plotnikov, E. Y., Roginsky, V. A., Savchenko, A. Y., Severina, I. I., Severin, F. F., Shkurat, T. P., Tashlitsky, V. N., Shidlovsky, K. M., Vyssokikh, M. Y., Zamyatnin, A. A., Jr., Zorov, D. B., and Skulachev, V. P. (2011) Curr. Drug Targets, 12, 800–826.

    Article  PubMed  CAS  Google Scholar 

  11. Severin, F. F., Severina, I. I., Antonenko, Y. N., Rokitskaya, T. I., Cherepanov, D. A., Mokhova, E. N., Vyssokikh, M. Y., Pustovidko, A. V., Markova, O. V., Yaguzhinsky, L. S., Korshunova, G. A., Sumbatyan, N. V., Skulachev, M. V., and Skulachev, V. P. (2010) Proc. Nat. Acad. Sci. USA, 107, 663–668.

    Article  PubMed  CAS  Google Scholar 

  12. 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. Bienerg. Biomembr., 41, 239–249.

    Article  CAS  Google Scholar 

  13. Kovaleva, M. V., Sukhanova, E. I., Trendeleva, T. A., Popova, K. M., Zylkova, M. V., Uralskaya, L. A., and Zvyagilskaya, R. A. (2010) Biochemistry (Moscow), 75, 297–303.

    Article  CAS  Google Scholar 

  14. Trendeleva, T., Sukhanova, E., Ural’skaya, L., Saris, N.-E., and Zvyagilskaya, R. (2011) J. Bienerg. Biomembr., 43, 623–631.

    Article  CAS  Google Scholar 

  15. Trendeleva, T., Sukhanova, E., Ural’skaya, L., Saris, N.-E., and Zvyagilskaya, R. (2011) J. Bienerg. Biomembr., 43, 633–644.

    Article  CAS  Google Scholar 

  16. Severina, I. I. (1982) Biochim. Biophys. Acta, 681, 311–317.

    Article  CAS  Google Scholar 

  17. Van der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. (2005) J. Comput. Chem., 26, 1701–1718.

    Article  Google Scholar 

  18. Brooks, B. R., Brooks, C. L., III, Mackerell, A. D., Jr., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) J. Comp. Chem., 30, 1545–1615.

    Article  CAS  Google Scholar 

  19. Price, D. J., and Brooks, C. L. (2004) J. Chem. Phys., 121, 10096–10103.

    Article  PubMed  CAS  Google Scholar 

  20. Torrie, G. M., and Valleau, J. P. (1977) Comput. Phys., 23, 187–193.

    Article  Google Scholar 

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

    Article  Google Scholar 

  22. Zvyagilskaya, R. A., Parchomenko, O. A., and Persson, B. L. (2000) IUBMB Life, 50, 151–155.

    PubMed  CAS  Google Scholar 

  23. Zvyagilskaya, R. A., Parchomenko, O., Abramova, N., Allard, P., Panaretakis, T., Pattison-Granberg, J., and Persson, B. L. (2001) J. Membr. Biol., 183, 39–50.

    Article  PubMed  CAS  Google Scholar 

  24. Zvyagilskaya, R., and Persson, B. L. (2003) IUBMB Life, 55, 151–154.

    Article  PubMed  CAS  Google Scholar 

  25. Zvyagilskaya, R. A., and Persson, B. L. (2004) Biochemistry (Moscow), 69, 1310–1317.

    Article  CAS  Google Scholar 

  26. Zvyagilskaya, R. A., and Persson, B. L. (2005) Cell Biol. Int., 29, 87–94.

    Article  PubMed  CAS  Google Scholar 

  27. Zvyagilskaya, R. A., Parkhomenko, O. A., Gordeeva, A. V., Deryabina, Y. I., and Persson, B. L. (2004) Biosci. Reps., 24, 117–125.

    Article  CAS  Google Scholar 

  28. Andreishcheva, E. N., Isakova, E. P., Sidorov, N. N., Abramova, N. B., Ushakova, N. A., Shaposhnikov, G. L., Soares, M. I., and Zvyagilskaya, R. A. (1999) Biochemistry (Moscow), 64, 1061–1067.

    CAS  Google Scholar 

  29. Chance, B., and Williams, G. R. (1955) Nature, 175, 1120–1121.

    Article  PubMed  CAS  Google Scholar 

  30. Akerman, K. E. O., and Wikstrom, M. K. F. (1976) FEBS Lett., 68, 191–197.

    Article  PubMed  CAS  Google Scholar 

  31. Bradford, M. M. (1976) Anal. Biochem., 72, 248–254.

    Article  PubMed  CAS  Google Scholar 

  32. Murphy, M. P., Krueger, M. J., Sablin, S. O., Ramsay, R. R., and Singer, T. P. (1995) Biochem. J., 306, 359–365.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

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

    T. A. Trendeleva, A. G. Rogov, E. I. Sukhanova & R. A. Zvyagilskaya

  2. Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of Sciences, Leninsky pr. 31, 119991, Moscow, Russia

    D. A. Cherepanov

  3. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    T. M. Il’yasova & I. I. Severina

Authors
  1. T. A. Trendeleva
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  2. A. G. Rogov
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  3. D. A. Cherepanov
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  4. E. I. Sukhanova
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  5. T. M. Il’yasova
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  6. I. I. Severina
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  7. R. A. Zvyagilskaya
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Correspondence to R. A. Zvyagilskaya.

Additional information

Published in Russian in Biokhimiya, 2012, Vol. 77, No. 9, pp. 1230–1239.

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Trendeleva, T.A., Rogov, A.G., Cherepanov, D.A. et al. Interaction of tetraphenylphosphonium and dodecyltriphenylphosphonium with lipid membranes and mitochondria. Biochemistry Moscow 77, 1021–1028 (2012). https://doi.org/10.1134/S000629791209009X

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  • DOI: https://doi.org/10.1134/S000629791209009X

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