Potassium fluxes across the endoplasmic reticulum and their role in endoplasmic reticulum calcium homeostasis

Cell Calcium

Volumn 58, Issue 1, 2015, Pages 79-85

  Kuum, Malle ^a   Veksler, Vladimir ^b,c   Kaasik, Allen ^a  

^a Faculty of Medicine   (Estonia)

^b INSERM   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Calcium homeostasis; Endoplasmic reticulum; Intracellular potassium fluxes

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM ION; CATION CHANNEL; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; POTASSIUM CHANNEL; POTASSIUM ION; POTASSIUM PROTON EXCHANGE PROTEIN; RYANODINE RECEPTOR; TRIMERIC INTRACELLULAR CATION CHANNEL; UNCLASSIFIED DRUG; CALCIUM; POTASSIUM;

CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL MEMBRANE POTENTIAL; COUNTER ION FLUX; CYTOSOL; ENDOPLASMIC RETICULUM MEMBRANE; ION TRANSPORT; MEMBRANE TRANSPORT; NONHUMAN; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SARCOPLASMIC RETICULUM; ANIMAL; CHEMISTRY; ENDOPLASMIC RETICULUM; METABOLISM;

ANIMALS; CALCIUM; ENDOPLASMIC RETICULUM; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; POTASSIUM; POTASSIUM CHANNELS; POTASSIUM-HYDROGEN ANTIPORTERS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84930525987     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.11.004     Document Type: Review

References (106)

1. Fink R.H., Veigel C. Calcium uptake and release modulated by counter-ion conductances in the sarcoplasmic reticulum of skeletal muscle. Acta Physiol. Scand. 1996, 156:387-396.
2. Meissner G. Monovalent ion and calcium ion fluxes in sarcoplasmic reticulum. Mol. Cell. Biochem. 1983, 55:65-82.
3. 2+-pump. J. Biochem. 1986, 99:1071-1080.
4. Baylor S.M., Chandler W.K., Marshall M.W. Calcium release and sarcoplasmic reticulum membrane potential in frog skeletal muscle fibers. J. Physiol. 1984, 348:209-238.
5. Oetliker H. An appraisal of the evidence for a sarcoplasmic reticulum membrane potential and its relation to calcium release in skeletal muscle. J. Muscle Res. Cell. Motil. 1982, 3:247-272.
6. Somlyo A.V., Gonzalez-Serratos H.G., Shuman H., McClellan G., Somlyo A.P. Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: an electron-probe study. J. Cell Biol. 1981, 90:577-594.
7. 2+ movements across the sarcoplasmic reticulum in situ. J. Biol. Chem. 1985, 260:6801-6807.
8. Kitazawa T., Somlyo A.P., Somlyo A.V. The effects of valinomycin on ion movements across the sarcoplasmic reticulum in frog muscle. J. Physiol. 1984, 350:253-268.
9. 2+-ATPase during calcium transport in reconstituted proteoliposomes with low ionic permeability. J. Biol. Chem. 1990, 265:19524-19534.
10. 2+ uptake. J. Biochem. 1981, 89:1247-1252.
11. 2+ pump in reconstituted proteoliposomes. Biophys. J. 1993, 64:1232-1242.
12. Kim J.H., Johannes L., Goud B., Antony C., Lingwood C.A., Daneman R., Grinstein S. Noninvasive measurement of the pH of the endoplasmic reticulum at rest and during calcium release. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:2997-3002.
13. Kneen M., Farinas J., Li Y., Verkman A.S. Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys. J. 1998, 74:1591-1599.
14. 2+) interaction with the ion-binding sites of the SR Ca-ATPase. Biophys. J. 2002, 82:170-181.
15. Kuum M., Veksler V., Liiv J., Ventura-Clapier R., Kaasik A. Endoplasmic reticulum potassium-hydrogen exchanger and small conductance calcium-activated potassium channel activities are essential for ER calcium uptake in neurons and cardiomyocytes. J. Cell. Sci. 2012, 125:625-633.
16. 2+ handling in intracellular stores. Nature 2007, 448:78-82.
17. Ng K.-E., Schwarzer S., Duchen M.R., Tinker A. The intracellular localization and function of the ATP-Sensitive K+ channel subunit Kir6.1. J. Membr. Biol. 2010, 234:137-147.
18. Gillespie D., Fill M. Intracellular calcium release channels mediate their own countercurrent: the ryanodine receptor case study. Biophys. J. 2008, 95:3706-3714.
19. 2+ overload and sarcoplasmic reticulum instability in tric-a null skeletal muscle. J. Biol. Chem. 2010, 285:37370-37376.
20. Yamazaki D., Tabara Y., Kita S., et al. TRIC-A channels in vascular smooth muscle contribute to blood pressure maintenance. Cell Metab. 2011, 14:231-241.
21. 2+ handling of alveolar epithelial cells and in perinatal lung maturation. Development 2009, 136:2355-2361.
22. Venturi E., Sitsapesan R., Yamazaki D., Takeshima H. TRIC channels supporting efficient Ca(2+) release from intracellular stores. Pflugers Arch. 2013, 465:187-195.
23. Guo T., Nani A., Shonts S., et al. Sarcoplasmic reticulum K(+) (TRIC) channel does not carry essential countercurrent during Ca(2+) release. Biophys. J. 2013, 105:1151-1160.
24. Clement IV J.P., Kunjilwar K., Gonzalez G., Schwanstecher M., Panten U., Aguilar-Bryan L., et al. Association and stoichometry of KATP channel subunits. Neuron 1997, 18:827-838.
25. Shyng S., Nichols C.G. Octameric stoichiometry of the KATP channel complex. J. Gen. Physiol. 1997, 110:655-664.
26. Erginel-Unaltuna N., Yang W.P., Blanar M.A. Genomic organization and expression of KCNJ8/Kir6.1: a gene encoding a subunit of an ATP-sensitive potassium channel. Gene 1998, 211:71-78.
27. Flanagan S.E., Edghill E.L., Gloyn A.L., Ellard S., Hattersley A.T. Mutations in KCNJ11, which encodes Kir6.2, are a common cause of diabetes diagnosed in the first 6 months of life, with the phenotype determined by genotype. Diabetologia 2006, 49:1190-1197.
28. Inagaki N., Tsuura Y., Namba N., et al. Cloning and functional characterization of a novel ATP-sensitive potassium channel ubiquitously expressed in rat tissues, including pancreatic islets, pituitary, skeletal muscle, and heart. J. Biol. Chem. 1995, 270:5691-5694.
29. Aguilar-Bryan L., Nichols C., Wechsler S., et al. Cloning of the beta-cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 1995, 268:423-426.
30. Babenko A.P., Aguilar-Bryan L., Bryan J. A view of sur/KIR6.X, KATP channels. Annu. Rev. Physiol. 1998, 60:667-687.
31. Hibino H., Inanobe A., Furutani K., Murakami S., Findlay I., Kurachi Y. Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol. Rev. 2010, 90:291-366.
32. Zerangue N., Schwappach B., Jan Y.N., Jan L.Y. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 1999, 22:537-548.
33. Inagaki N., Gonoi T., Clement J.P.T., et al. Reconstitution of IKATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 1995, 270:1166-1170.
34. + channel in the mitochondrial inner membrane. Nature 1991, 352:244-247.
35. 2+ transients that modulate nuclear function. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:9544-9549.
36. +-channel subunits on the mitochondria and endoplasmic reticulum of rat cardiomyocytes. J. Histochem. Cytochem. 2005, 53:1491-1500.
37. 3H]glimepiride. Biochim. Biophys. Acta 1994, 1191:278-290.
38. Pu J.-L., Ye B., Kroboth S.L., McNally E.M., Makielski J.C., Shi N.-Q. Cardiac sulfonylurea receptor short form-based channels confer a glibenclamide-insensitive KATP activity. J. Mol. Cell Cardiol. 2008, 44:188-200.
39. Akrouh A., Halcomb S.E., Nichols C.G., Sala-Rabanal M. Molecular biology of KATP channels and implications for health and disease. IUBMB Life 2009, 61:971-978.
40. Tinker A., Aziz Q., Thomas A. The role of ATP-sensitive potassium channels in cellular function and protection in the cardiovascular system. Br. J. Pharmacol. 2014, 171:12-23.
41. Queliconi B.B., Wojtovich A.P., Nadtochiy S.M., Kowaltowski A.J., Brookes P.S. Redox regulation of the mitochondrial K(ATP) channel in cardioprotection. Biochim. Biophys. Acta 2011, 1813:1309-1315.
42. + channels. J. Gen. Physiol. 2004, 124:357-370.
43. + channels are redox-sensitive pathways that control reactive oxygen species production. Free Radic. Biol. Med. 2007, 42:1039-1048.
44. Zhang D.X., Chen Y.F., Campbel W.B., Zou A.P., Gross G.J., Li P.L. Characteristics and superoxide-induced activation of reconstituted myocardial mitochondrial ATP-sensitive potassium channels. Circ. Res. 2001, 89:1177-1183.
45. + channel in brain mitochondria. J. Neurosci. Res. 2008, 86:1548-1556.
46. Costa A.D., Garlid K.D. Intramitochondrial signaling: interactions among mitoKATP, PKCepsilon, ROS, and MPT. Am. J. Physiol. 2008, 295:H874-H882.
47. 2+ channels: the complex thought. Biochim. Biophys. Acta 2014, 14. pii:S0167-4889(14)00083-4 (Epub ahead of print). 10.1016/j.bbamcr.2014.02.019.
48. 2+ sparks to BKCa channels in urinary bladder smooth muscle. Am. J. Physiol. Cell. Physiol. 2001, 280:C481-C490.
49. Sun X.-P., Schlichter L.C., Stanley E.F. Single-channel properties of BK-type calcium-activated potassium channels at a cholinergic presynaptic nerve terminal. J. Physiol. 1999, 518:639-651.
50. Köhler M., Hirschberg B., Bond C.T., Kinzie J.M., Marrion N.V., Maylie J., Adelman J.P. Small-conductance, calcium-activated potassium channels from mammalian brain. Science 1996, 273:1709-1714.
51. Ledoux J., Werner M.E., Brayden J.E., Nelson M.T. Calcium-activated potassium channels and the regulation of vascular tone. Physiology (Bethesda) 2006, 21:69-78.
52. Xia X.M., Fakler B., Rivard A., et al. Mechanism of calcium gating in small-conductance calcium activated potassium channels. Nature 1998, 395:503-507.
53. + channels provide different facets of endothelium-dependent hyperpolarization in rat mesenteric artery. J. Physiol. 2003, 553:183-189.
54. Lancaster B., Nicoll R.A. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J. Physiol. 1987, 389:187-204.
55. Sah P., McLachlan E.M. Potassium currents contributing to action potential repolarization and the afterhyperpolarization in rat vagal motoneurons. J. Neurophysiol. 1992, 68:1834-1841.
56. Viana F., Bayliss D.A., Berger A.J. Multiple potassium conductances and their role in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. J. Neurophysiol. 1993, 69:2150-2163.
57. Villalobos C., Shakkottai V.G., Chandy K.G., Michelhaugh S.K., Andrade R. SKCa channels mediate the medium but not the slow calcium-activated afterhyperpolarization in cortical neurons. J. Neurosci. 2004, 24:3537-3542.
58. Brenner R., Jegla T.J., Wickenden A., Liu Y., Aldrich R.W. Cloning and functional characterization of novel large conductance calcium-activated potassium channel beta-subunits, hKCNMB3 and hKCNMB4. J. Biol. Chem. 2000, 275:6453-6461.
59. + channel from smooth muscle. J. Biol. Chem. 1994, 269:17274-17278.
60. + channel. J. Biol. Chem. 2000, 275:23211-23218.
61. Fanger C.M., Ghanshani S., Logsdon N.J., et al. Calmodulin mediates calcium-dependent activation of the intermediate conductance KCa channel, IKCa1. J. Biol. Chem. 1999, 274:5746-5754.
62. Joiner W.J., Tang M.D., Wang L.Y., et al. Formation of intermediate-conductance calcium-activated potassium channels by interaction of Slack and Slo subunits. Nat. Neurosci. 1998, 1:462-469.
63. + channels: from protein complexes to function. Physiol. Rev. 2010, 90:1437-1459.
64. Orio P., Rojas P., Ferreira G., Lattorre R. New disguises for an old channel: MaxiK channel beta-subunits. News Physiol. Sci. 2002, 17:156-161.
65. Vergara C., Latorre R., Marrion N.V., Adelman J.P. Calcium-activated potassium channels. Curr. Opin. Neurobiol. 1998, 8:321-329.
66. Zarei M.M., Zhu N., Alioua A., Eghbali M., Stefani E., Toro L. A novel MaxiK splice variant exhibits dominant-negative properties for surface expression. J. Biol. Chem. 2001, 276:16232-16239.
67. + channel splice variant. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10072-10077.
68. 2+-gated (Slo1) potassium channels. FEBS Lett. 2007, 581:1000-1008.
69. Toro L., Li M., Zhang Z., Singh H., Wu Y., Stefani E. MaxiK channel and cell signalling. Pflugers Arch. - Eur. J. Physiol. 2014, 466:875-886.
70. Shruti S., Urban-Ciecko J., Fitzpatrick J.A., Brenner R., Bruchez M.P., Barth A.L. The brain-specific Beta4 subunit downregulates BK channel cell surface expression. PLoS ONE 2012, 7:e33429.
71. Marty A. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature 1981, 291:497-500.
72. Quandt F.N., MacVicar B.A. Calcium activated potassium channels in cultured astrocytes. Neuroscience 1986, 19:29-41.
73. Barrett J.N., Magleby K.L., Pallotta B.S. Properties of single calcium-activated potassium channels in cultured rat muscle. J. Physiol. 1982, 331:211-230.
74. Bartschat D.K., Blaustein M.P. Calcium-activated potassium channels in isolated presynaptic nerve terminals from rat brain. J. Physiol. 1985, 361:441-457.
75. Miller C. An overview of the potassium channel family. Genome Biol. 2000, 1. REVIEWS0004.
76. Nelson M.T., Quayle J.M. Physiological roles and properties of potassium channels in arterial smooth muscle. Am. J. Physiol. 1995, 268:C799-C822.
77. Dimmer K.S., Navoni F., Casarin A., et al. LETM1, deleted in Wolf Hirschhorn syndrome is required for normal mitochondrial morphology and cellular viability. Hum. Mol. Genet. 2008, 17:201-214.
78. Hashimi H., McDonald L., Stribrna E., Lukes J. Trypanosome Letm1 protein is essential for mitochondrial potassium homeostasis. J. Biol. Chem. 2013, 288:26914-26925.
79. Hasegawa A., van der Bliek A.M. Inverse correlation between expression of the Wolfs Hirschhorn candidate gene Letm1 and mitochondrial volume in C. elegans and in mammalian cells. Hum. Mol. Genet. 2007, 16:2061-2071.
80. McQuibban A.G., Joza N., Megighian A., et al. A Drosophila mutant of LETM1, a candidate gene for seizures in Wolf-Hirschhorn syndrome. Hum. Mol. Genet. 2010, 19:987-1000.
81. + homeostasis with a potential role in the Wolf-Hirschhorn syndrome. J. Biol. Chem. 2004, 279:30307-30315.
82. Mitchell P. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol. Rev. Camb. Philos. Soc. 1966, 41:445-502.
83. Mitchell P. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. 1966. Biochim. Biophys. Acta 2011, 1807:1507-1538.
84. Kaasik A., Safiulina D., Zharkovsky A., Veksler V. Regulation of mitochondrial matrix volume. Am. J. Physiol. Cell. Physiol. 2007, 292:C157-C163.
85. Safiulina D., Veksler V., Zharkovsky A., Kaasik A. Loss of mitochondrial membrane potential is associated with increase in mitochondrial volume: physiological role in neurones. Cell. Physiol. 2006, 206:347-353.
86. Zotova L., Aleschko M., Sponder G., et al. Novel components of an active mitochondrial K(+)/H(+) exchange. J. Biol. Chem. 2010, 285:14399-14414.
87. + exchangers in rat liver mitochondria. J. Biol. Chem. 1982, 257:9252-9254.
88. Lanner J.T., Georgiou D.K., Joshi A.D., Hamilton S.L. Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb. Perspect. Biol. 2010, 2:a003996.
89. 2+ release. Cell Calcium 2012, 51:427-433.
90. Tinker A., Lindsay A.R., Williams A.J. A model for ionic conduction in the ryanodine receptor channel of sheep cardiac muscle sarcoplasmic reticulum. J. Gen. Physiol. 1992, 100:495-517.
91. Zhou X., Lin P., Yamazaki D., et al. Trimeric intracellular cation channels and sarcoplasmic/endoplasmic reticulum calcium homeostasis. Circ. Res. 2014, 114:706-716.
92. Kaasik A., Safiulina D., Choubey V., Kuum M., Zharkovsky A., Veksler V. Mitochondrial swelling impairs the transport of organelles in cerebellar granule neurons. J. Biol. Chem. 2007, 282:32821-32826.
93. Atochina-Vasserman E.N., Biktasova A., Abramova E., et al. Aquaporin11 insufficiency modulates kidney susceptibility to oxidative stress. Am. J. Physiol. Renal. Physiol. 2013, 304:1295-1307.
94. Morishita Y., Matsuzaki T., Hara-chikuma M., et al. Disruption of aquaporin-11 produces polycystic kidneys following vacuolization of the proximal tubule. Mol. Cell Biol. 2005, 25:7770-7779.
95. Nozaki K., Ishii D., Ishibashi K. Intracellular aquaporins: clues for intracellular water transport. Pflugers Arch. 2008, 456:701-707.
96. Klee M., Pimentel-Muiños F.X. Bcl-X(L) specifically activates Bak to induce swelling and restructuring of the endoplasmic reticulum. J. Cell Biol. 2005, 168:723-734.
97. Varadarajan S., Tanaka K., Smalley J.L., et al. Endoplasmic reticulum membrane reorganization is regulated by ionic homeostasis. PLOS ONE 2013, 8:e56603.
98. 2+ translocation through endoplasmic reticulum membrane. Dokl. Biochem. Biophys. 2006, 409:206-210.
99. Edwards J.C., Kahl C.R. Chloride channels of intracellular membranes. FEBS Lett. 2010, 584:2102-2111.
100. 2+ handling in airway smooth muscle. Am. J. Physiol. Lung Cell Mol. Physiol. 2006, 290:L1146-L1153.
101. 2+ uptake by the smooth muscle sarcoplasmic reticulum. Biophys. J. 1998, 75:1759-1766.
102. Jentsch T.J. Chloride and the endosomal-lysosomal pathway: emerging roles of CLC chloride transporters. J. Physiol. 2007, 578:633-640.
103. Picollo A., Pusch M. Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 2005, 436:420-423.
104. Plans V., Rickheit G., Jentsch T.J. Physiological roles of CLC Cl(-)/H(+) exchangers in renal proximal tubules. Pflugers Arch. 2009, 458:23-37.
105. Scheel O., Zdebik A.A., Lourdel S., Jentsch T.J. Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 2005, 436:424-427.
106. + antiporter ClC-7 is the primary chloride permeation pathway in lysosomes. Nature 2008, 453:788-792.