Ukr.Biochem.J. 2013; Volume 85, Issue 1, Jan-Feb, pp. 33-41

doi: http://dx.doi.org/10.15407/ubj85.01.033

The effect of potential-dependent potassium uptake on membrane potential in rat brain mitochondria

O. V. Akopova, V. I. Nosar, L. I. Kolchinskaya,
I. N. Mankovska, M. K. Malysheva, V. F. Sagach

Bogomoletz Institute of Physiology, National Academy of Sciences of Ukraine, Kyiv;
e-mail: luko@biph.kiev.ua

The effect of potential-dependent potassium uptake on the transmembrane potential difference (ΔΨm) in rat brain mitochondria has been studied­. It was shown that in potassium concentration range of 0-120 mM the potential-dependent K+-uptake into matrix leads to the increase in respiration rate and mitochondrial depolarization. ATP-dependent potassium channel (K+ATP-channel) blockers, gliben­clamide and 5-hydroxydecanoate, block ~35% of potential-dependent potassium uptake in the brain mitochondria. It was shown that K+ATP-channel blockage results in membrane repolarization by ~20% of control, which is consistent with experimental dependence of ΔΨm on the rate of potential-dependent potassium uptake. Obtained experimental data give the evidence that functional activity of K+ATP-channel is physiologically important in the regulation of membrane potential and energy-dependent processes in brain mitochondria.

Keywords: , , , , ,


References:

  1. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature. 1961 Jul 8;191(4784):144-8. PubMed, CrossRef
  2. Skulachev VP. Transformation of energy in biomembranes. Moscow: Nauka, 1972. 203 p.
  3. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol. 2004 Oct;287(4):C817-33. Review. PubMed, CrossRef
  4. Garlid KD, Paucek P. Mitochondrial potassium transport: the K(+) cycle. Biochim Biophys Acta. 2003 Sep 30;1606(1-3):23-41. Review. PubMed, CrossRef
  5. Beavis AD. Upper and lower limits of the charge translocation stoichiometry of mitochondrial electron transport. J Biol Chem. 1987 May 5;262(13):6165-73. PubMed
  6. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J. 2009 Jan 1;417(1):1-13. PubMed, PubMedCentral, CrossRef
  7. Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL, Parker N. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med. 2004 Sep 15;37(6):755-67. Review. PubMed, CrossRef
  8. Stucki JW. Efficiency of oxidative phosphorylation and energy dissipation by H+ ion recycling in rat-liver mitochondrial metabolizing pyruvate. Eur J Biochem. 1976 Sep 15;68(2):551-62. PubMed, CrossRef
  9. Liu SS. Cooperation of a “reactive oxygen cycle” with the Q cycle and the proton cycle in the respiratory chain–superoxide generating and cycling mechanisms in mitochondria. J Bioenerg Biomembr. 1999 Aug;31(4):367-76. Review. PubMed
  10.  Akerman KE, Wikström MK. Safranine as a probe of the mitochondrial membrane potential. FEBS Lett. 1976 Oct 1;68(2):191-7. PubMed, CrossRef
  11. Moore CL. Profiles of mitochondrial monovalent ion transport. Curr Top Bioenerg. 1971;4:191-236. CrossRef
  12. Szewczyk A, Kajma A, Malinska D, Wrzosek A, Bednarczyk P, Zabłocka B, Dołowy K. Pharmacology of mitochondrial potassium channels: dark side of the field. FEBS Lett. 2010 May 17;584(10):2063-9.  Review. PubMed, CrossRef
  13. O’Rourke B. Evidence for mitochondrial K+ channels and their role in cardioprotection. Circ Res. 2004 Mar 5;94(4):420-32.  PubMed, PubMedCentral, CrossRef
  14. Facundo HT, Fornazari M, Kowaltowski AJ. Tissue protection mediated by mitochondrial K+ channels. Biochim Biophys Acta. 2006 Feb;1762(2):202-12. Review. PubMed, CrossRef
  15. Cancherini DV, Trabuco LG, Rebouças NA, Kowaltowski AJ. ATP-sensitive K+ channels in renal mitochondria. Am J Physiol Renal Physiol. 2003 Dec;285(6):F1291-6. PubMed, CrossRef
  16. Debska G, Kicinska A, Skalska J, Szewczyk A, May R, Elger CE, Kunz WS. Opening of potassium channels modulates mitochondrial function in rat skeletal muscle. Biochim Biophys Acta. 2002 Dec 2;1556(2-3):97-105. PubMed, CrossRef
  17. Kowaltowski AJ, Seetharaman S, Paucek P, Garlid KD. Bioenergetic consequences of opening the ATP-sensitive K(+) channel of heart mitochondria. Am J Physiol Heart Circ Physiol. 2001 Feb;280(2):H649-57. PubMed
  18. Facundo HT, de Paula JG, Kowaltowski AJ. Mitochondrial ATP-sensitive K+ channels prevent oxidative stress, permeability transition and cell death. J Bioenerg Biomembr. 2005 Apr;37(2):75-82. PubMed, CrossRef
  19. Costa AD, Quinlan CL, Andrukhiv A, West IC, Jabůrek M, Garlid KD. The direct physiological effects of mitoK(ATP) opening on heart mitochondria. Am J Physiol Heart Circ Physiol. 2006 Jan;290(1):H406-15. PubMed, CrossRef
  20. Starkov AA, Polster BM, Fiskum G. Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J Neurochem. 2002 Oct;83(1):220-8. PubMed, CrossRef
  21. Cai J, Jones DP. Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J Biol Chem. 1998 May 8;273(19):11401-4. PubMed, CrossRef
  22. Gogvadze V, Robertson JD, Enoksson M, Zhivotovsky B, Orrenius S. Mitochondrial cytochrome c release may occur by volume-dependent mechanisms not involving permeability transition. Biochem J. 2004 Feb 15;378(Pt 1):213-7. PubMed, PubMedCentral, CrossRef
  23. Aon MA, Cortassa S, Wei AC, Grunnet M, O’Rourke B. Energetic performance is improved by specific activation of K+ fluxes through K(Ca) channels in heart mitochondria. Biochim Biophys Acta. 2010 Jan;1797(1):71-80. PubMed, PubMedCentral, CrossRef
  24. Andrukhiv A, Costa AD, West IC, Garlid KD. Opening mitoKATP increases superoxide generation from complex I of the electron transport chain. Am J Physiol Heart Circ Physiol. 2006 Nov;291(5):H2067-74. PubMed, CrossRef
  25. Bajgar R, Seetharaman S, Kowaltowski AJ, Garlid KD, Paucek P. Identification and properties of a novel intracellular (mitochondrial) ATP-sensitive potassium channel in brain. J Biol Chem. 2001 Sep 7;276(36):33369-74. Epub 2001 Jul 5. PubMed, CrossRef
  26. Akopova OV,  Nosar VI,  Bouryi VA,  MankovskayaIN, Sagach VF. Influence of ATP dependent K+ channel opener on K+ cycle and oxygen consumption in rat liver mitochondria. Biochemistry (Mosc). 2010 Sep;75(9):1139-47. PubMed, CrossRef
  27. Akopova O. V. The influence of ATP-dependent K+-channel diazoxide opener on the opening of mitochondrial permeability transition pore in rat liver mitochondria. Ukr Biokhim Zhurn. 2011 May-Jun;83(3):37-47. Russian. PubMed
  28. Debska G, May R, Kicińska A, Szewczyk A, Elger CE, Kunz WS. Potassium channel openers depolarize hippocampal mitochondria. Brain Res. 2001 Feb 16;892(1):42-50. PubMed, CrossRef
  29. Dixon M., Webb  E. Enzymes. M.: Mir, 1982. Vol. 1. 392 p.
  30. Beavis AD, Lu Y, Garlid KD. On the regulation of K+ uniport in intact mitochondria by adenine nucleotides and nucleotide analogs. J Biol Chem. 1993 Jan 15;268(2):997-1004 PubMed
  31. Szewczyk A, Wójcik G, Nałecz MJ. Potassium channel opener, RP 66471, induces membrane depolarization of rat liver mitochondria. Biochem Biophys Res Commun. 1995 Feb 6;207(1):126-32. PubMed, CrossRef
  32. The membranes: ion channels. Ed. Yu. A. Chizmadzhaeva. M.: Mir, 1981. 320 p.
  33. Kapus A, Szászi K, Káldi K, Ligeti E, Fonyó A. Ruthenium red inhibits mitochondrial Na+ and K+ uniports induced by magnesium removal. J Biol Chem. 1990 Oct 25;265(30):18063-6. PubMed
  34. Tomaskova Z, Ondrias K. Mitochondrial chloride channels–What are they for? FEBS Lett. 2010 May 17;584(10):2085-92. Review. PubMed, CrossRef

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License.