An investigation of the occurrence and properties of the mitochondrial intermediate-conductance Ca2+-activated K+ channel mtKCa3.1

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 6-7, 2010, Pages 1260-1267

  Sassi, Nicola ^a   De Marchi, Umberto ^a   Fioretti, Bernard ^b   Biasutto, Lucia ^a   Gulbins, Erich ^c   Franciolini, Fabio ^b   Szabò, Ildikò ^a   Zoratti, Mario ^a,d  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF PERUGIA   (Italy)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d CNR   (Italy)

Author keywords

Calcium; HeLa cells; IK(Ca); Inner mitochondrial membrane; Patch clamp; TRAM 34

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; POTASSIUM CHANNEL KV1.3; PROTEIN BAX;

APOPTOSIS; ARTICLE; CELL GROWTH; CELL MEMBRANE; CELL MEMBRANE CONDUCTANCE; CELL PROLIFERATION; CONTROLLED STUDY; DNA FRAGMENTATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; LYMPHOCYTE; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; CELL PROLIFERATION; HCT116 CELLS; HUMANS; INTERMEDIATE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; PATCH-CLAMP TECHNIQUES;

EID: 77953777012     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.12.015     Document Type: Article

References (90)

1. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev. 1999, 79:1127-1155.
2. + cycle. Biochim. Biophys. Acta 2003, 1606:23-41.
3. O'Rourke B. Mitochondrial ion channels. Annu. Rev. Physiol. 2007, 69:19-49.
4. Nowikowsky K., Schweyen R.J., Bernardi P. Pathophysiology of mitochondrial volume homeostasis: potassium transport and permeability transition. Biochim. Biophys. Acta Bioenerg. 2009, 1787:345-350.
5. Zoratti M., De Marchi U., Gulbins E., Szabò I. Novel channels of the inner mitochondrial membrane. Biochim. Biophys. Acta Bioenerg. 2009, 1787:351-363.
6. Szewczyk A., Jarmuszkiewicz W., Kunz W.S. Mitochondrial potassium channels. IUBMB Life 2009, 61:134-143.
7. +-channel in the mitochondrial inner membrane. Nature 1991, 352:244-247.
8. ATP channel is modulated by calcium and nitric oxide: a patch-clamp approach. Biochim. Biophys. Acta 2004, 1656:46-56.
9. Choma K., Bednarczyk P., Koszela-Piotrowska I., Kulawiak B., Kudin A., Kunz W.S., Dołowy K., Szewczyk A. Single channel studies of the ATP-regulated potassium channel in brain mitochondria. J. Bioenerg. Biomembr. 2009, 41:323-334.
10. Szabò I., Bock J., Jekle A., Soddemann M., Adams C., Lang F., Zoratti M., Gulbins E. A novel potassium channel in lymphocyte mitochondria. J. Biol. Chem. 2005, 280:12790-12798.
11. V1.3 mediates Bax-induced apoptosis in lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14861-14866.
12. Gulbins E., Sassi N., Grassmè H., Zoratti M., Szabò I. Role of Kv1.3 mitochondrial potassium channel in apoptotic signalling in lymphocytes. Biochim. Biophys. Acta 2010, 1797:1251-1259.
13. Rusznák Z., Bakondi G., Kosztka L., Pocsai K., Dienes B., Fodor J., Telek A., Gönczi M., Szucs G., Csernoch L. Mitochondrial expression of the two-pore domain TASK-3 channels in malignantly transformed and non-malignant human cells. Virchows Arch. 2008, 452:415-426.
14. 2+-activated K channel of the BK-type in the inner mitochondrial membrane of a human glioma cell line. Biochem. Biophys. Res. Commun. 1999, 257:549-554.
15. + channels in the cardiac inner mitochondrial membrane. Science 2002, 298:1029-1033.
16. Skalska J., Piwonska M., Wyroba E., Surmacz L., Wieczorek R., Koszela-Piotrowska I., Zielinska J., Bednarczyk P., Dolowy K., Wilczynski G.M., Szewczyk A., Kunz W.S. A novel potassium channel in skeletal muscle mitochondria. Biochim. Biophys. Acta 2008, 1777:651-659.
17. Cheng Y., Gu X.Q., Bednarczyk P., Wiedemann F.R., Haddad G.G., Siemen D. Hypoxia increases activity of the BK-channel in the inner mitochondrial membrane and reduces activity of the permeability transition pore. Cell. Physiol. Biochem. 2008, 22:127-136.
18. Skalska J., Bednarczyk P., Piwonska M., Kulawiak B., Wilczynski G., Dolowy K., Kudin A.P., Kunz W.S., Szewczyk A. Calcium ions regulate K uptake into brain mitochondria: the evidence for a novel potassium channel. Int. J. Mol. Sci. 2009, 10:1104-1120.
19. Koszela-Piotrowska I., Matkovic K., Szewczyk A., Jarmuszkiewicz W. A large-conductance calcium-activated potassium channel in potato tuber mitochondria. Biochem. J. 2009, 424:307-316.
20. Ca3.1) in the inner mitochondrial membrane of human colon cancer cells. Cell Calcium 2009, 45:509-516.
21. + channels: physiological roles and pharmacology. Curr. Med. Chem. 2003, 10:649-661.
22. Wei A.D., Gutman G.A., Aldrich R., Chandy K.G., Grissmer S., Wulff H. International Union of Pharmacology. LII. Nomenclature and molecular relationships of calcium-activated potassium channels. Pharmacol. Rev. 2005, 57:463-472.
23. + channel of intermediate conductance: a possible target for immune suppression. Expert Opin. Ther. Targets 2002, 6:623-636.
24. Ca3.1: target and marker for cancer, autoimmune disorder and vascular inflammation?. Expert Rev. Mol. Diagn. 2008, 8:179-187.
25. + channels: molecular identity determinants and function of the SK family. Nat. Rev. Neurosci. 2004, 5:758-770.
26. + channels in murine endothelial cells: block by intracellular calcium and magnesium. J. Gen. Physiol. 2008, 131:125-135.
27. + channels and regulates channel gating. Neuron 2004, 43:847-858.
28. Ca-channel activity in human cardiac fibroblasts to electrical coupling of cardiomyocytes-fibroblasts. J. Membr. Biol. 2006, 213:175-185.
29. + channel modulators on human prostate cancer cell proliferation. Eur. J. Pharmacol. 2003, 471:157-164.
30. + channel expression in human breast cancer cells: involvement in cell cycle regulation and carcinogenesis. J. Membr. Biol. 2008, 221:1-6.
31. + channel in glioblastoma CL-15 cells. Cell. Physiol. Biochem. 2006, 18:47-56.
32. Ca channels enhance agonist-evoked endothelial nitric oxide synthesis and arteriolar vasodilation. FASEB J. 2009, 23:1138-1145.
33. Ca3.1 contributes to atherogenesis in mice and humans. J. Clin. Invest. 2008, 118:3025-3037.
34. Félétou M. Calcium-activated potassium channels and endothelial dysfunction: therapeutic options?. Br. J. Pharmacol. 2009, 156:545-562.
35. Ca channels in rat proximal colon. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285:G185-G196.
36. + channel Kcnn4. J. Physiol. 2007, 583(Pt 2):705-717.
37. Costa A.D., Quinlan C.L., Andrukhiv A., West I.C., Jaburek M., Garlid K.D. The direct physiological effects of mitoK(ATP) opening on heart mitochondria. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H406-H415.
38. Kaasik A., Safiulina D., Zharkovsky A., Veksler V. Regulation of mitochondrial volume. Am. J. Physiol. Cell. Physiol. 2007, 292:C157-C163.
39. ATP activity in healthy and ischemic hearts. J. Bioenerg. Biomembr. 2009, 41:123-126.
40. Halestrap A.P. The regulation of the matrix volume of mammalian mitochondria in vivo and in vitro and its role in the control of mitochondrial metabolism. Biochim. Biophys. Acta 1989, 973:355-382.
41. ATP in response to inotropic stress. Am. J. Physiol. Heart Circ. Physiol. 2006, 291:H152-H160.
42. Ca channels in heart mitochondria. Biochim. Biophys. Acta 2010, 1797:71-80.
43. + channels prevent oxidative stress, permeability transition and cell death. J. Bioenerg. Biomembr. 2005, 37:75-82.
44. Halestrap A.P., Clarke S.J., Khaliulin I. The role of mitochondria in protection of the heart by preconditioning. Biochim. Biophys. Acta 2007, 1767:1007-1031.
45. Clarke S.J., Khaliulin I., Das M., Parker J.E., Heesom K.J., Halestrap A.P. Inhibition of mitochondrial permeability transition pore opening by ischemic preconditioning is probably mediated by reduction of oxidative stress rather than mitochondrial protein phosphorylation. Circ. Res. 2008, 102:1082-1090.
46. Kulawiak B., Kudin A.P., Szewczyk A., Kunz W.S. BK channel openers inhibit ROS production of isolated rat brain mitochondria. Exp. Neurol. 2008, 212:543-547.
47. Kowaltowski A.J., de Souza-Pinto N.C., Castilho R.F., Vercesi A.E. Mitochondria and reactive oxygen species. Free Rad. Biol. Med. 2009, 47:333-343.
48. Tahara E.B., Navarete F.D., Kowaltowsi A.J. Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Rad. Biol. Med. 2009, 46:1283-1297.
49. Hausenloy D.J., Tsang A., Yellon D.M. The reperfusion injury salvage kinase pathway: a common target for both ischemic preconditioning and postconditioning. Trends Cardiovasc. Med. 2005, 15:69-75.
50. Di Lisa F., Canton M., Menabò R., Kaludercic N., Bernardi P. Mitochondria and cardioprotection. Heart Fail. Rev. 2007, 12:249-260.
51. ATP, PKCε, ROS and MPT. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H874-H882.
52. Hausenloy D.J., Yellon D.M. Preconditioning and postconditioning: underlying mechanisms and clinical application. Atherosclerosis 2009, 204:334-341.
53. Krenz M., Oldenburg O., Wimpee H., Cohen M.V., Garlid K.D., Critz S.D., Downey J.M., Benoit J.N. Opening of ATP-sensitive potassium channels causes generation of free radicals in vascular smooth cells. Basic Res. Cardiol. 2002, 97:365-373.
54. 2 inhibit the mitochondrial permeability transition. J. Biol. Chem. 2006, 281:20801-20808.
55. + permeability and reactive oxygen species production by the p13 protein of human T-cell leukemia virus type 1. Biochim. Biophys Acta Bioenerg. 2009, 1787:947-954.
56. 2+ and ROS. Front. Biosci. 2009, 14:1197-1218.
57. 2+-induced permeability transition of isolated mitochondria. J. Biol. Chem. 2004, 279:37415-37422.
58. + channels. Br. J. Pharmacol. 2007, 151:655-665.
59. Ca3.1 potassium channels. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14518-14523.
60. Liou J.Y., Aleksic N., Chen S.F., Han T.J., Shyue S.K., Wu K.K. Mitochondrial localization of cyclooxygenase-2 and calcium-independent phospholipase A2 in human cancer cells: implication in apoptosis resistance. Exp. Cell Res. 2005, 306:75-84.
61. Pelkmans L., Fava E., Grabner H., Hannus M., Habermann B., Krausz E., Zerial M. Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 2005, 436:78-86.
62. Pelkmans L., Zerial M. Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 2005, 436:128-133.
63. Smart E.J., Ying Y.S., Conrad P.A., Anderson R.G. Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 1994, 127:1185-1197.
64. Conrad P.A., Smart E.J., Ying Y.S., Anderson R.G., Bloom G.S. Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J. Cell Biol. 1995, 131:1421-1433.
65. Pelkmans L., Bürli T., Zerial M., Helenius A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 2004, 118:767-780.
66. Pelkmans L. Secrets of caveolae- and lipid raft-mediated endocytosis revealed by mammalian viruses. Biochim. Biophys. Acta 2005, 1746:295-304.
67. McMahon K.A., Zhu M., Kwon S.W., Liu P., Zhao Y., Anderson R.G. Detergent-free caveolae proteome suggests an interaction with ER and mitochondria. Proteomics 2006, 6:143-152.
68. Bàthori G., Parolini I., Tombola F., Szabò I., Messina A., Oliva M., De Pinto V., Lisanti M., Sargiacomo M., Zoratti M. Porin is present in the plasma membrane where it is concentrated in caveolae and caveolae-related domains. J. Biol. Chem. 1999, 274:29607-29612.
69. Li W.P., Liu P., Pilcher B.K., Anderson R.G. Cell-specific targeting of caveolin-1 to caveolae, secretory vesicles, cytoplasm or mitochondria. J. Cell Sci. 2001, 114:1397-1408.
70. ATP channels. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H953-H961.
71. Garlid K.D., Costa A.D., Quinlan C.L., Pierre S.V., Dos Santos P. Cardioprotective signaling to mitochondria. J. Mol. Cell. Cardiol. 2009, 46:858-866.
72. García-Ruiz C., Colell A., Morales A., Calvo M., Enrich C., Fernandez-Checa J.C. Trafficking of ganglioside GD3 to mitochondria by tumor necrosis factor-alpha. J. Biol. Chem. 2002, 277:36443-36448.
73. Vance J.E. Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 1990, 265:7248-7256.
74. 2+ responses. Science 1998, 280:1763-1766.
75. Simmen T., Aslan J.E., Blagoveshchenskaya A.D., Thomas L., Wan L., Xiang Y., Feliciangeli S.F., Hung C.H., Crump C.M., Thomas G. PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO J. 2005, 24:717-729.
76. Youker R.T., Shinde U., Day R., Thomas G. At the crossroads of homoeostasis and disease: roles of the PACS proteins in membrane traffic and apoptosis. Biochem. J. 2009, 421:1-15.
77. de Brito O.M., Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456:605-610.
78. Gaigg B., Simbeni R., Hrastnik C., Paltauf F., Daum G. Characterization of a microsomal subfraction associated with mitochondria of the yeast, Saccharomyces cerevisiae. Involvement in synthesis and import of phospholipids into mitochondria. Biochim. Biophys. Acta 1995, 1234:214-220.
79. + channel copurify and coreconstitute to form a functioning signaling module in proteoliposomes. Circ. Res. 2006, 99:878-883.
80. + channels. Hypertension 2008, 52:499-506.
81. Costa A.D., Pierre S.V., Cohen M.V., Downey J.M., Garlid K.D. cGMP signalling in pre- and post-conditioning: the role of mitochondria. Cardiovasc. Res. 2008, 77:344-352.
82. + channels in cardiac myocytes: a mechanism of the cardioprotective effect and modulation by protein kinase A. Circulation 2005, 111:198-203.
83. Ca channels. Cardiovasc. Res. 2008, 77:398-405.
84. Nishida H., Sato T., Ogura T., Nakaya H. New aspects for the treatment of cardiac diseases based on the diversity of functional controls in cardiac muscles: mitochondrial ion channels and cardioprotection. J. Pharmacol. Sci. 2009, 109:341-347.
85. 2+-activated potassium channel Kcnn4. J. Biol. Chem. 2004, 279:47681-47687.
86. + channel. Circ. Res. 2006, 99:537-544.
87. 2+-activated K channel. J. Gen. Physiol. 2006, 127:159-169.
88. 2+-activated K channel. Channels 2009, 3:194-204.
89. + channels. J. Biol. Chem. 2000, 275:1201-1208.
90. Yu K., Fu W., Liu H., Luo X., Chen K.X., Ding J., Shen J., Jiang H. Computational simulations of interactions of scorpion toxins with the voltage-gated potassium ion channel. Biophys. J. 2004, 86:3542-3555.