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Ca2+-dependent nonspecific permeability of the inner membrane of liver mitochondria in the guinea fowl (Numida meleagris)

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Abstract

This comparative study presents the results of the induction of Ca2+-dependent nonspecific permeability of the inner membrane (pore opening) of rat and guinea fowl liver mitochondria by mechanisms that are both sensitive and insensitive to cyclosporin A (CsA). It was established that energized rat and guinea fowl liver mitochondria incubated with 1 mM of inorganic phosphate (Pi) are capable of swelling upon addition of at least 125 and 875 nmol of CaCl2 per 1 mg protein, respectively. Under these conditions, the Ca2+ release from the mitochondria of these animals and a drop in Δψ are observed. All of these processes are inhibited by 1 μM of CsA. FCCP, causing organelle de-energization, induces pore opening in rat and guinea fowl liver mitochondria upon addition of 45 и 625 nmol of CaCl2 per 1 mg protein, respectively. These results suggest the existence of a CsA-sensitive mechanism for the induction of Ca2+-dependent pores in guinea fowl liver mitochondria, which has been reported in rat liver mitochondria. However, guinea fowl liver mitochondria have a significantly greater resistance to Ca2+ as a pore inducer compared to rat liver mitochondria. It was found that the addition of α,ω-hexadecanedioic acid (HDA) to rat and guinea fowl liver mitochondria incubated with CsA and loaded with Ca2+ causes organelle swelling and Ca2+ release from the matrix. It is assumed that in contrast to the CsA-sensitive pore, the CsA-insensitive pore induced by HDA in the inner membrane of guinea fowl liver mitochondria, as well as in rat liver mitochondria, is lipid in nature.

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Abbreviations

HDA:

α,ω-hexadecanedioic acid

CRC:

calcium retention capacity

TPP+ :

tetraphenylphosphonium

CsA:

cyclosporin A

Pi :

inorganic phosphate

Δψ:

transmembrane electric potential

References

  • Agafonov AV, Gritsenko EN, Shlyapnikova EN, Kharakoz DP, Belosludtseva NV, Lezhnev EI, Saris NE, Mironova GD (2007) Ca2+-induced phase separation in the membrane of palmitate-containing liposomes and its possible relation to membrane permeabilization. J Membr Biol 215:57–68

    Article  CAS  Google Scholar 

  • Azzolin L, von Stockum S, Basso E, Petronilli V, Forte MA, Bernardi P (2010) The mitochondrial permeability transition from yeast to mammals. FEBS Lett 584:2504–2509

    Article  CAS  Google Scholar 

  • Basso E, Petronilli V, Forte MA, 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  CAS  Google Scholar 

  • Belosludtsev KN, Saris NE, Belosludtseva NV, Trudovishnikov AS, Lukyanova LD, Mironova GD (2009) Physiological aspects of the mitochondrial cyclosporin A-insensitive palmitate/Ca2 + −induced pore: tissue specificity, age profile and dependence on the animal’s adaptation to hypoxia. J Bioenerg Biomembr 41:395–401

    Article  CAS  Google Scholar 

  • Bodrova ME, Dedukhova VI, Samartsev VN, Mokhova EN (2000) Role of the ADP/ATP-antiporter in fatty acid-induced uncoupling of Ca2+-loaded rat liver mitochondria. IUBMB Life 50:189–194

    Article  CAS  Google Scholar 

  • Bonora M, Bononi A, De Marchi E, Giorgi C, Lebiedzinska M, Marchi S, Patergnani S, Rimessi A, Suski JM, Wojtala A, Wieckowski MR, Kroemer G, Galluzzi L, Pinton P (2013) Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition. Cell Cycle 12:674–683

    Article  CAS  Google Scholar 

  • Chalmers S, Nicholls DG (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  Google Scholar 

  • Chance B, Williams GR (1955) Respiratory enzymes in oxidative phosphorylation: III. The steady state. J Biol Chem 217:409–427

    CAS  Google Scholar 

  • Di Paola M, Lorusso M (2006) Interaction of free fatty acids with mitochondria: Coupling, uncoupling and permeability transition. Biochim Biophys Acta 1757:1330–1337

    Article  Google Scholar 

  • Dubinin MV, Adakeeva SI, Samartsev VN (2013) Long-chain α, ω-dioic acids as inducers of cyclosporin A-insensitive nonspecific permeability of the inner membrane of liver mitochondria loaded with calcium or strontium ions. Biochem Mosc 78:412–417

    Article  CAS  Google Scholar 

  • Dubinin MV, Samartsev VN, Astashev ME, Kazakov AS, Belosludtsev KN (2014) A permeability transition in liver mitochondria and liposomes induced by α, ω-dioic acids and Ca(2+). Eur Biophys J 43:565–572

    Article  CAS  Google Scholar 

  • Furness LJ, Speakman JR (2008) Energetics and longevity in birds. Age (Dordr) 30:75–87

    Article  CAS  Google Scholar 

  • Gellerich FN, 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  Google Scholar 

  • Giorgio V, von Stockum S, Antoniel M, Fabbro A, Fogolari F, Forte M, Glick GD, 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 U S A 110:5887–5892

    Article  CAS  Google Scholar 

  • Hinkle PC, Yu ML (1979) The phosphorus/oxygen ratio of mitochondrial oxidative phosphorylation. J Biol Chem 254:2450–2455

    CAS  Google Scholar 

  • Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213

    Article  CAS  Google Scholar 

  • Kamo N, Muratsugu M, Hondoh R, Kobatake Y (1979) Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J Membr Biol 49:105–121

    Article  CAS  Google Scholar 

  • Lemasters JJ, Theruvath TP, Zhong Z, Nieminen AL (2009) Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta 1787:1395–1401

    Article  CAS  Google Scholar 

  • Leung AW, Varanyuwatana P, Halestrap AP (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  CAS  Google Scholar 

  • Malhi H, Guicciardi ME, Gores GJ (2010) Hepatocyte death: a clear and present danger. Physiol Rev 90:1165–1194

    Article  CAS  Google Scholar 

  • Markova OV, Bondarenko DI, Samartsev VN (1999) The anion-carrier mediated uncoupling effect of dicarboxylic fatty acids in liver mitochondria depends on the position of the second carboxyl group. Biochem Mosc 64:565–570

    CAS  Google Scholar 

  • Mironova GD, Gritsenko E, Gateau-Roesch O, Levrat C, Agafonov A, Belosludtsev K, Prigent A, Muntean D, Dubois M, Ovize M (2004) Formation of palmitic acid/Ca2+ complexes in the mitochondrial membrane: a possible role in the cyclosporin-insensitive permeability transition. J Bioenerg Biomembr 36:171–178

    Article  CAS  Google Scholar 

  • Novgorodov SA, Gudz TI, Obeid LM (2008) Long-chain ceramide is a potent inhibitor of the mitochondrial permeability transition pore. J Biol Chem 283:24707–24717

    Article  CAS  Google Scholar 

  • Petronilli V, Cola C, Massari S, Colonna R, Bernardi P (1993) Physiological effectors modify voltage sensing by the cyclosporin A-sensitive permeability transition pore of mitochondria. J Biol Chem 268:21939–21945

    CAS  Google Scholar 

  • Rasola A, Bernardi P (2011) Mitochondrial permeability transition in Ca(2+)-dependent apoptosis and necrosis. Cell Calcium 50:222–233

    Article  CAS  Google Scholar 

  • Samartsev VN, Vedernikov AA, Dubinin MV, Zabiyakin VA (2014) Comparative study of free oxidation in liver mitochondria of “wild” gray-speckled population and productive domestic breeds of guinea fowl (Numida meleagris). J Evol Biochem Physiol 50:181–183

    Article  Google Scholar 

  • Schönfeld P, Bohnensack R (1997) Fatty acid-promoted mitochondrial permeability transition by membrane depolarization and binding to the ADP/ATP carrier. FEBS Lett 420:167–170

    Article  Google Scholar 

  • Scorrano L, Petronilli V, Bernardi P (1997) On the voltage dependence of the mitochondrial permeability transition pore. A critical appraisal. J Biol Chem 272:12295–12299

    Article  CAS  Google Scholar 

  • 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  Google Scholar 

  • Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730

    Article  Google Scholar 

  • Sultan A, Sokolove P (2001a) Palmitic acid opens a novel cyclosporin A-insensitive pore in the inner mitochondrial membrane. Arch Biochem Biophys 386:37–51

    Article  CAS  Google Scholar 

  • Sultan A, Sokolove P (2001b) Free fatty acid effects on mitochondrial permeability: an overview. Arch Biochem Biophys 386:52–61

    Article  CAS  Google Scholar 

  • Toninello A, Salvi M, Colombo L (2000) The membrane permeability transition in liver mitochondria of the great green goby Zosterisessor ophiocephalus (Pallas). J Exp Biol 203:3425–3434

    CAS  Google Scholar 

  • Varanyuwatana P, Halestrap AP (2012) The roles of phosphate and the phosphate carrier in the mitochondrial permeability transition pore. Mitochondrion 12:120–125

    Article  CAS  Google Scholar 

  • Zorov DB, Juhaszova M, Yaniv Y, Nuss HB, Wang S, Sollott SJ (2009) Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovasc Res 83:213–225

    Article  CAS  Google Scholar 

  • Zorov DB, Juhaszova M, Sollott SJ (2014) Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 94:909–950

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by a grant from the Russian Foundation for Basic Research (project No. 14-04-00688-a) and partially supported by the Ministry of Education and Science of the Russian Federation (project No. 1365).

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Authors and Affiliations

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

    Aleksander A. Vedernikov, Mikhail V. Dubinin, Vladimir A. Zabiakin & Victor N. Samartsev

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  1. Aleksander A. Vedernikov
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  2. Mikhail V. Dubinin
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  3. Vladimir A. Zabiakin
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  4. Victor N. Samartsev
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Correspondence to Mikhail V. Dubinin.

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Vedernikov, A.A., Dubinin, M.V., Zabiakin, V.A. et al. Ca2+-dependent nonspecific permeability of the inner membrane of liver mitochondria in the guinea fowl (Numida meleagris). J Bioenerg Biomembr 47, 235–242 (2015). https://doi.org/10.1007/s10863-015-9606-z

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  • DOI: https://doi.org/10.1007/s10863-015-9606-z

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