Mitochondrial potassium and chloride channels.

• Authors: Anna Kicińska , Grażyna Dębska , Wolfram Kunz , Adam Szewczyk
• Languages of publication: EN

Abstracts

EN

Channels selective for potassium or chloride ions are present in inner mitochondrial membranes. They probably play an important role in mitochondrial events such as the formation of ΔpH and regulation of mitochondrial volume changes. Mitochondrial potassium and chloride channels could also be the targets for pharmacologically active compounds such as potassium channel openers and antidiabetic sulfonylureas. This review describes the properties, pharmacology, and current observations concerning the functional role of mitochondrial potassium and chloride channels.

Keywords

EN

ATP; ion channels; mitochondria; chloride channel; potassium channel; channel openers; sulfonylurea

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2000
• Volume: 47
• Issue: 3
• Pages: 541-551

Dates

published

2000

received

2000-07-06

accepted

2000-07-27

Contributors

author

Anna Kicińska

• Laboratory of Intracellular Ion Channels, Nencki Institute of Experimental Biology, L. Pasteura 3, 02-096 Warszawa, Poland

author

Grażyna Dębska

• Laboratory of Intracellular Ion Channels, Nencki Institute of Experimental Biology, L. Pasteura 3, 02-096 Warszawa, Poland

author

Wolfram Kunz

• Department of Neurochemistry, Bonn University, , Germany

author

Adam Szewczyk

• Laboratory of Intracellular Ion Channels, Nencki Institute of Experimental Biology, L. Pasteura 3, 02-096 Warszawa, Poland

References

• Aguilar-Bryan, L., Nichols, C.G., Wechsler, S.W., Clement, J.P. 4th, Boyd, A.E. 3rd, Gonzalez, G., Herrera-Sosa, H., Nguy, K., Bryan, J. & Nelson, D.A. (1995) Cloning of the beta cell high-affinity sulfonylurea receptor: A regulator of insulin secretion. Science 268, 423-426.
• Ahmet, I., Sawa, Y., Nishimura, M., Kitakaze, M. & Matsuda, H. (2000) Cardioprotective effect of diadenosine tetraphosphate (AP4A) preservation in hypothermic storage and its relation with mitochondrial ATP-sensitive potassium channels. Transplantation 69, 16-20.
• Asemu, G., Papousek, F., Ostadal, B. & Kolar, F. (1999) Adaptation to high altitude hypoxia protects the rat heart against ischemia-induced arrhythmias. Involvement of mitochondrial K(ATP) channel. J. Mol. Cell Cardiol. 31, 1821-1831.
• Baines, C.P., Cohen, M.V. & Downey, J.M. (1999a) Signal transduction in ischemic preconditioning: The role of kinases and mitochondrial K(ATP) channels. J. Cardiovasc. Electrophysiol. 10, 741-754.
• Baines, C.P., Liu, G.S., Birincioglu, M., Critz, S.D., Cohen, M.V. & Downey, J.M. (1999b) Ischemic preconditioning depends on interaction between mitochondrial KATP channels and actin cytoskeleton. Am. J. Physiol. 276, H1361-H1368.
• Bernardi, P. (1999) Mitochondrial transport of cations: Channels, exchangers, and permeability transition. Physiol. Rev. 79, 1127-1155.
• Chuang, J., Milner, T.A., Zhu, M. & Sung, C. (1999) A 29 kDa intracellular chloride channel p64H1 is associated with large dense-core vesicles in rat hippocampal neurons. J. Neurosci. 19, 2919-2928.
• Czyż, A., Szewczyk, A., Nałęcz, M.J. & Wojtczak, L. (1995) The role of mitochondrial potassium fluxes in controlling the protonmotive force in energized mitochondria. Biochem. Biophys. Res. Commun. 210, 98-104.
• Duncan, R.R., Westwood, P.K., Boyd, A. & Ashley, R.H. (1997) Rat brain p64H1, expression of a new member of the p64 chloride channel protein family in endoplasmic reticulum. J. Biol. Chem. 272, 23880-23886.
• Edwards, J.C., Tulk, B. & Schlesinger, P.H. (1998) Functional expression of p64, an intracellular chloride channel protein. J. Membr. Biol. 163, 119-127.
• Edwards, G. & Weston, A.H. (1993) Structure-activity relationships of K+ channel openers. Trends Pharmacol. Sci. 11, 417-422.
• Fernández-Salas, E., Sagar, M., Cheng, C., Yuspa, S.H. & Weinberg, W.C. (1999) p53 and tumor necrosis factor regulate the expression of a mitochondrial chloride channel protein. J. Biol. Chem. 274, 36488-36497.
• Fryer, R.M., Hsu, A.K., Eells, J.T., Nagase, H. & Gross, G.J. (1999) Opioid-induced second window of cardioprotection: Potential role of mitochondrial KATP channels. Circ. Res. 84, 846-851.
• Fryer, R.M., Eells, J.T., Hsu, A.K., Henry, M.M. & Gross, G.J. (2000) Ischemic preconditioning in rats: Role of mitochondrial K(ATP) channel in preservation of mitochondrial function. Am. J. Physiol. Heart Circ. Physiol. 278, H305-H312.
• Garlid, K.D., Paucek, P., Yarov-Yarovoy, V., Sun, X. & Schindler, P.A. (1996) The mitochondrial KATP channel as a receptor for potassium channel openers. J. Biol. Chem. 271, 8796- 8799.
• Garlid, K.D., Paucek, P., Yarov-Yarovoy, V., Murray, H.N., Darbenzio, R.B., D'Alonzo, A.J., Lodge, N.J., Smith, M.A. & Grover, G.J. (1997) Cardioprotective effect of diazoxide and its interaction with mitochondrial ATP-sensitive K+ channels. Possible mechanism of cardioprotection. Circ. Res. 81, 1072-1082.
• Ghosh, S., Standen, N.B. & Galinanes, M. (2000) Evidence for mitochondrial KATP channels as effectors of human myocardial preconditioning. Cardiovasc. Res. 45, 934-940.
• Giovannucci, D.R., Hlubek, M.D. & Stuenkel, E.L. (1999) Mitochondria regulate the Ca2+-exocytosis relationship of bovine adrenal chromaffin cells. J. Neurosci. 19, 9261-9270.
• Gross, G.J. & Fryer, R.M. (1999) Sarcolemmal versus mitochondrial ATP-sensitive K+ channels and myocardial preconditioning. Circ. Res. 84, 973-979.
• Halestrap, A.P. (1994) Regulation of mitochondrial metabolism through changes in matrix volume. Biochem. Soc. Trans. 22, 522-529.
• Holmuhamedov, E.L., Jovanovic, S., Dzeja, P.P., Jovanovic, A. & Terzic, A. (1998) Mitochondrial ATP-sensitive K+ channels modulate cardiac mitochondrial function. Am. J. Physiol. 275, H1567-H1576.
• Inagaki, N., Gonoi, T., Clement, J.P. 4th, Namba, N., Inazawa, J., Gonzalez, G., Aguilar-Bryan, L., Seino, S. & Bryan, J. (1995) Reconstitution of IKATP: An inward rectifier subunit plus the sulfonylurea receptor. Science 270, 1166- 1170.
• Inoue, I., Nagase, H., Kishi, K. & Higuti, T. (1991) ATP-sensitive K+ channel in the mitochondrial inner membrane. Nature 352, 244-247.
• Iwai, T., Tanonaka, K., Koshimizu, M. & Takeo, S. (2000) Preservation of mitochondrial function by diazoxide during sustained ischaemia in the rat heart. Br. J. Pharmacol. 129, 1219- 1227.
• Jaburek, M., Yarov-Yarovoy, V., Paucek, P. & Garlid, K.D. (1998) State-dependent inhibition of mitochondrial KATP channel by glyburide and 5-hydroxydecanoate. J. Biol. Chem. 273, 13578-13582.
• Jakob, R., Bindokas, V. P. & Miller, R.J. (2000) Action of KATP channel openers on mitochondria in hippocampal neurons. Eur. J. Med. Res. 5, 41.
• Jentsch, T.J. & Gunther, W. (1997) Chloride channels: An emerging molecular picture. Bioessays 19, 117-126.
• Jonas, E.A., Buchanan, J. & Kaczmarek, L.K. (1999) Prolonged activation of mitochondrial conductances during synaptic transmission. Science 286, 1347-1350.
• Kevelaitis, E., Oubenaissa, A., Peynet, J., Mouas, C. & Menasche, P. (1999) Preconditioning by mitochondrial ATP-sensitive potassium channel openers: An effective approach for improving the preservation of heart transplants. Circulation 100, II345-II350.
• Latorre, R., Oberhauser, A., Labarca, P. & Alvarez, O. (1989) Varieties of calcium-activated potassium channels. Annu. Rev. Physiol. 51, 385-339.
• Laver, D. & Walker, N.A. (1991) Activation by Ca2+ and block by divalent ions of the K+ channel in the membrane of cytoplasmic drops from Chara australis. J. Membr. Biol. 120, 131-139.
• Lazdunski, M. (1994) ATP-sensitive potassium channels: An overview. J. Cardiovasc. Pharmacol. 24, S1-5.
• Liang, B.T. & Gross, G.J. (1999) Direct preconditioning of cardiac myocytes via opioid receptors and KATP channels. Circ. Res. 84, 1396-1400.
• Liu, Y., Sato, T., O'Rourke, B. & Marban, E. (1998) Mitochondrial ATP-dependent potassium channels: Novel effectors of cardioprotection? Circulation 97, 2463-2469.
• Miura, T. & Tsuchida, A. (1999) Adenosine and preconditioning revisited. Clin. Exp. Pharmacol. Physiol. 26, 92-99.
• Ockaili, R., Emani, V.R., Okubo, S., Brown, M., Krottapalli, K. & Kukreja, R.C. (1999) Opening of mitochondrial KATP channel induces early and delayed cardioprotective effect: Role of nitric oxide. Am. J. Physiol. 277, H2425-H2434.
• Paucek, P., Mironova, G., Mahdi, F., Beavis, A.D., Woldegiorgis, G. & Garlid, K.D. (1992) Reconstitution and partial purification of the glibenclamide-sensitive, ATP-dependent K+ channel from rat liver and beef heart mitochondria. J. Biol. Chem. 267, 26062-26069.
• Petersen, O.H. (1992) Stimulus-secretion coupling: Cytoplasmic calcium signals and the control of channels in exocrine acinar cells. J. Physiol. 448, 1-51.
• Sasaki, N., Sato, T., Ohler, A., O'Rourke, B. & Marban, E. (2000) Activation of mitochondrial ATP-dependent potassium channels by nitric oxide. Circulation 101, 439-445.
• Sato, T., O'Rourke, B. & Marban, E. (1998) Modulation of mitochondrial ATP-dependent K+ channels by protein kinase C. Circ. Res. 83, 110-114.
• Sato, T., Sasaki, N., O'Rourke, B. & Marban, E. (2000) Nicorandil, a potent cardioprotective agent, acts by opening mitochondrial ATP-dependent potassium channels. J. Am. Coll. Cardiol. 35, 514-518.
• Schwarz, A., Bhardwaj, R., Aragane, Y., Mahnke, K., Riemann, H., Metze, D., Luger, T.A. & Schwarz, T. (1995) Ultraviolet-B-induced apoptosis of keratinocytes: Evidence for partial involvement of tumor necrosis factor-alpha in the formation of sunburn cells. J. Invest. Dermatol. 104, 922-927.
• Siemen, D., Loupatatzis, C., Borecky, J., Gulbins, E. & Lang, F. (1999) Ca2+-activated K channel of BK-type in inner mitochondrial membrane of a human glioma cell line. Biochem. Biophys. Res. Commun. 257, 549-554.
• Singer, J.J. & Walsh, J.V., Jr. (1987) Characterization of calcium-activated potassium channels in single smooth muscle cells using the patch-clamp technique. Pfluegers Arch. 408, 98-111.
• Szewczyk, A. (1998) The intracellular potassium and chloride channels: Properties, pharmacology and function. Mol. Membr. Biol. 15, 49-58.
• Szewczyk, A. & Marban, E. (1999) Mitochondria: A new target for potassium channel openers? Trends Pharmacol. Sci. 20, 157-161.
• Suzuki, M., Kotake, K., Fujikura, K., Inagaki, N., Suzuki, T., Gonoi, T., Seino, S. & Takata, K. (1997) Kir6.1: A possible subunit of ATP-sensitive K+ channels in mitochondria. Biochem. Biophys. Res. Commun. 241, 693-697.
• Wang, Y. & Ashraf, M. (1999) Role of protein kinase C in mitochondrial KATP channel-mediated protection against Ca2+ overload injury in rat myocardium. Circ. Res. 84, 1156-1165.
• Wang, Y., Hirai, K. & Ashraf, M. (1999) Activation of mitochondrial ATP-sensitive K(+) channel for cardiac protection against ischemic injury is dependent on protein kinase C activity. Circ. Res. 85, 731-741.
• Ziegler, A., Jonason, A.S., Leffell, D.J., Simon, J.A., Sharma, H.W., Kimmelman, J., Remington, L., Jacks, T. & Brash, D.E. (1994) Sunburn and p53 in the onset of skin cancer. Nature 372, 773-776.
• Zhou, M., Tanaka, O., Sekiguchi, M., Sakabe, K., Anzai, M., Izumida, I., Inoue, T., Kawahara, K. & Abe, H. (1999) Localization of the ATP-sensitive potassium channel subunit (Kir6.1/ uK(ATP)-1) in rat brain. Brain Res. Mol. Brain Res. 74, 15-25.