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Induction of calcium-dependent nonspecific permeability of the inner membrane in liver mitochondria of mammals and birds: A comparative study

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Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

The kinetics of the processes accompanying the induction of Ca2+-dependent permeability (pore opening) of the inner membrane—swelling of organelles and Ca2+ release from the matrix—was studied in isolated liver mitochondria of mammals (mice, rats, and rabbits) and birds (pigeons and guinea fowls). It was found that the mitochondria of rats, pigeons, and guinea fowls of the gray-speckled population (GSP) are similar in terms of respiration and oxidative ATP synthesis, whereas mitochondria of rabbits exhibit a greater degree of coupling of respiration and ATP synthesis, and mitochondria of mice and Zagorskaya White breed (ZWB) guinea fowls, a lower degree of coupling. It was established that mammalian mitochondria energized by succinate oxidation and incubated with 1 mM of inorganic phosphate are able to swell upon the addition of 125 nmol of CaCl2 per 1 mg protein. Under these conditions, mitochondria of GSP and ZWB guinea fowls and pigeons are capable of swelling upon addition of at least 875, 875 and 1000 nmol of CaCl2 per 1 mg protein, respectively. Cyclosporin A (CsA, 1 μM) inhibits mitochondrial swelling. It was shown that mitochondria of mammalians and guinea fowls but not of pigeons are able to effectively absorb and retain Ca2+ in the matrix. Calcium retention capacity of mitochondria from rats, mice, rabbits, GSP, and ZWB guinea fowls were, respectively, 70, 57, 38, 844 and 793 nmol of CaCl2 per 1 mg of protein. In the presence of an oxidizing agent tert-butylhydroperoxide (TBH), the induction of the Ca2+-dependent pore in the mitochondria was observed upon addition of CaCl2 in substantially smaller quantities. TBH was most effective in the case of rabbit mitochondria and had the lowest efficiency in the case of guinea fowl and pigeon mitochondria.

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References

  1. Saris N.E., Carafoli E. 2005. A historical review of cellular calcium handling, with emphasis on mitochondria. Biokhimia. (Rus.). 70, 231–239.

    Google Scholar 

  2. Lemasters J.J., Theruvath T.P., Zhong Z., Nieminen A.L. 2009. Mitochondrial calcium and the permeability transition in cell death. Biochim. Biophys. Acta. 1787, 1395–1401.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Rasola A., and Bernardi P. 2011. Mitochondrial permeability transition in Ca2+-dependent apoptosis and necrosis. Cell. Calcium. 50, 222–233.

    Article  CAS  PubMed  Google Scholar 

  4. Zorov D.B., Juhaszova M., Sollott S.J. 2014. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev. 94, 909–950.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Gellerich F.N., Gizatullina Z., Gainutdinov T., Muth K., Seppet E., Orynbayeva Z., Vielhaber S. 2013. The control of brain mitochondrial energization by cytosolic calcium: The mitochondrial gas pedal. IUBMB Life. 65, 180–190.

    Article  CAS  PubMed  Google Scholar 

  6. Chalmers S., Nicholls D.G. 2003. The relationship between free and total calcium concentrations in the matrix of liver and brain mitochondria. J. Biol. Chem. 278, 19062–19070.

    Article  CAS  PubMed  Google Scholar 

  7. Skulachev V.P., Bogachev A.V., Kasparinsky F.O. 2010. Membrannaja bioenergetika (Membrane bioenergetics). M.: Moscow University Press.

    Google Scholar 

  8. Siemen D., Ziemer M. 2013. What is the nature of the mitochondrial permeability transition pore and what is it not? IUBMB Life. 65, 255–262.

    Article  CAS  PubMed  Google Scholar 

  9. Malhi H., Guicciardi M.E., Gores G.J. 2010. Hepatocyte death: A clear and present danger. Physiol. Rev. 90, 1165–1194.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Zorov D.B., Plotnikov E.Y., Jankauskas S.S., Isaev N.K., Silachev D.N., Zorova L.D., Pevzner I.B., Pulkova N.V., Zorov S.D., Morosanova M.A. 2012. The phenoptosis problem: What is causing the death of an organism? Lessons from acute kidney injury. Biokhimia. (Rus.). 77, 893–906.

    Google Scholar 

  11. Skulachev V.P. 2012. What is “phenoptosis” and how to fight it? Biokhimia. (Rus.). 77, 827–846.

    Google Scholar 

  12. Leung A.W., Varanyuwatana P., Halestrap A.P. 2008. The mitochondrial phosphate carrier interacts with cyclophilin D and may play a key role in the permeability transition. J. Biol. Chem. 283, 26312–26323.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Giorgio V., von Stockum S., Antoniel M., Fabbro A., Fogolari F., Forte M., Glick G.D., Petronilli V., Zoratti M., Szabó I., Lippe G., Bernardi P. 2013. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc. Natl. Acad. Sci USa. 110, 5887–5892.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Bonora M., Bononi A., De Marchi E., Giorgi C., Lebiedzinska M., Marchi S., Patergnani S., Rimessi A., Suski J.M., Wojtala A., Wieckowski M.R., Kroemer G., Galluzzi L., Pinton P. 2013. Role of the c subunit of the FOATP synthase in mitochondrial permeability transition. Cell Cycle. 12, 674–683.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Basso E., Petronilli V., Forte M.A., Bernardi P. 2008. Phosphate is essential for inhibition of the mitochondrial permeability transition pore by cyclosporin A and by cyclophilin D ablation. J. Biol. Chem. 283, 26307–26311.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Varanyuwatana P., Halestrap A.P. 2012. The roles of phosphate and the phosphate carrier in the mitochondrial permeability transition pore. Mitochondrion. 12, 120–125.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Kozhina O.V., Samartsev V.N. 2010. Uncoupling activity of fatty acids in liver mitochondria in the presence of substrates of ADP/ATPand aspartate/glutamate antiporters is increased under oxidative stress. Biol. Membrany (Rus.). 27, 184–188.

    CAS  Google Scholar 

  18. Ronchi J.A., Vercesi A.E., Castilho R.F. 2011. Reactive oxygen species and permeability transition pore in rat liver and kidney mitoplasts. J. Bioenerg. Biomembr. 43, 709–715.

    Article  CAS  PubMed  Google Scholar 

  19. Azzolin L., von Stockum S., Basso E., Petronilli V., Forte M.A., Bernardi P. 2010. The mitochondrial permeability transition from yeast to mammals. FEBS Lett. 584, 2504–2509.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Barja G. 2002. Rate of generation of oxidative stressrelated damage and animal longevity. Free Radic. Biol. Med. 33, 1167–1172.

    Article  CAS  PubMed  Google Scholar 

  21. Speakman J.R. 2005. Body size, energy metabolism and lifespan. J. Exp. Biol. 208, 1717–1730.

    Article  PubMed  Google Scholar 

  22. Hulbert A.J., Pamplona R., Buffenstein R., Buttemer W.A. 2007. Life and death: Metabolic rate, membrane composition, and life span of animals. Physiol. Rev. 87, 1175–1213.

    Article  CAS  PubMed  Google Scholar 

  23. Furness L.J., Speakman J.R. 2008. Energetics and longevity in birds. Age (Dordr). 30, 75–87.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Montgomery M.K., Hulbert A.J., Buttemer W.A. 2011. The long life of birds: The rat-pigeon comparison revisited. PLoS One. 6, e24138. doi: 10.1371/journalpone.0024138.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Vedernikov A.A., Dubinin M.V., Zabiakin V.A., Samartsev V.N. 2015. Ca2+-dependent nonspecific permeability of the inner membrane of liver mitochondria in the guinea fowl (Numida meleagris). J. Bioenerg. Biomembr. doi: 10.1007/s10863-015-9606-z.

    Google Scholar 

  26. Lukyanov A.S. 2008. Bioetika s osnovami bioprava: uchebnoe posobie (Bioethics with Grounds of Biolaws. A handbook). M.: Nauchnyi Mir.

    Google Scholar 

  27. Markova O.V., Bondarenko D.I., Samartsev V.N. 1999. The anion-carrier mediated uncoupling effect of dicarboxylic fatty acids in liver mitochondria depends on the position of the second carboxyl group. Biokhimia. (Rus.). 64, 679–685.

    Google Scholar 

  28. Hinkle P.C., Yu M.L. 1979. The phosphorus/oxygen ratio of mitochondrial oxidative phosphorilation. J. Biol. Chem. 254, 2450–2455.

    CAS  PubMed  Google Scholar 

  29. Dubinin M.V., Adakeeva S.I., Samartsev V.N. 2013. Long-chain a,?-dioic acids as inducers of cyclosporin A-insensitive nonspecific permeability of the inner membrane of liver mitochondria loaded with calcium or strontium ions. Biokhimia. (Rus.). 78, 533–540.

    Google Scholar 

  30. Novgorodov S.A., Gudz T.I., Obeid L.M. 2008. Longchain ceramide is a potent inhibitor of the mitochondrial permeability transition pore. J. Biol. Chem. 283, 24707–24717.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Rolfe D.E. Brand M.D. 1997. The physiological significance of mitochondrial proton leak in animal cells and tissues. Biosci. Rep. 17, 9–16.

    Article  CAS  PubMed  Google Scholar 

  32. Brand M.D., Turner N., Ocloo A., Else P.L., Hulbert A.J. 2003. Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds. Biochem. J. 376, 741–748.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Samartsev V.N., Polishchuk L.S., Paydyganov A.P., Zeldi I.P. 2004. Features of the uncoupling effect of fatty acids in liver mitochondria of mammals with different body weight. Biokhimia (Rus.). 69, 832–842.

    Google Scholar 

  34. Zabiyakin V.A. 2005. Polyvariability of pigmentation of fowl feathering. Ptitsevodstvo (Rus.). 10, 14–17.

    Google Scholar 

  35. Samartsev V.N., Vedernikov A.A., Dubinin M.V., Zabiyakin V.A. 2014. Comparative study of free oxidation in liver mitochondria of “wild”gray-speckled population and productive domestic breeds of guinea fowl (Numida meleagris). Zh. Evol. Biokhim. Fiziol. (Rus.). 50, 160–162.

    CAS  Google Scholar 

  36. Petronilli V., Cola C., Massari S., Colonna R., Bernardi P. 1993. Physiological effectors modify valtage sensing by the cyclosporine A-sensitive permeability transition pore of mitochondria. J. Biol. Chem. 268, 21939–21945.

    CAS  PubMed  Google Scholar 

  37. Gostimskaya I.S., Grivennikova V.G., Zharova T.V., Bakeeva L.E., Vinogradov A.D. 2003. In situ assay of the intramitochondrial enzymes: use of alamethicin for permeabilization of mitochondria. Anal. Biochem. 313, 46–52.

    Article  CAS  PubMed  Google Scholar 

  38. Brustovetsky N., Brustovetsky T., Jemmerson R., Dubinsky J.M. 2002. Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. J. Neurochem. 80, 207–218.

    Article  CAS  PubMed  Google Scholar 

  39. Murphy A.N., Bredesen D.E., Gortopassi G., Wang E., Fiskum G. 1996. Bcl-2 potentiates the maximal calcium uptake capacity of neural cell mitochondria. Proc. Natl. Acad. Sci. USA. 93, 9893–9898.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Mari State University, pl. Lenina 1, Yoshkar-Ola, 424001, Russia

    M. V. Dubinin, A. A. Vedernikov, E. I. Khoroshavina, S. I. Adakeeva & V. N. Samartsev

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  1. M. V. Dubinin
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  2. A. A. Vedernikov
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  3. E. I. Khoroshavina
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  4. S. I. Adakeeva
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  5. V. N. Samartsev
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Correspondence to M. V. Dubinin.

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Original Russian Text © M.V. Dubinin, A.A. Vedernikov, E.I. Khoroshavina, S.I. Adakeeva, V.N. Samartsev, 2015, published in Biologicheskie Membrany, 2015, Vol. 32, No. 5–6, pp. 328–337.

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Dubinin, M.V., Vedernikov, A.A., Khoroshavina, E.I. et al. Induction of calcium-dependent nonspecific permeability of the inner membrane in liver mitochondria of mammals and birds: A comparative study. Biochem. Moscow Suppl. Ser. A 10, 19–27 (2016). https://doi.org/10.1134/S1990747815050037

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  • DOI: https://doi.org/10.1134/S1990747815050037

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