Potassium leak channels and the KCNK family of two-p-domain subunits

Nature Reviews Neuroscience

Volumn 2, Issue 3, 2001, Pages 175-184

  Goldstein, Steve A N ^a   Bockenhauer, Detlef ^a   O’Kelly, Ita ^a   Zilberberg, Noam ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE PROTEIN; POTASSIUM; POTASSIUM CHANNEL; POTASSIUM CHANNEL SUBFAMILY K MEMBER 3; PROTEIN SUBUNIT; TANDEM PORE DOMAIN POTASSIUM CHANNEL;

ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; ELECTROPHYSIOLOGY; GENETICS; HEART MUSCLE; HUMAN; METABOLISM; NERVE CELL; OOCYTE; PATCH CLAMP; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; REVIEW;

ANIMALS; ELECTROPHYSIOLOGY; HUMANS; MODELS, MOLECULAR; MYOCARDIUM; NERVE TISSUE PROTEINS; NEURONS; OOCYTES; PATCH-CLAMP TECHNIQUES; POTASSIUM; POTASSIUM CHANNELS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

EID: 0035287002     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/35058574     Document Type: Article

References (116)

1. Goldman, D. E. Potential, impedance, and rectification in membranes. J. Gen. Physiol. 27, 37–60 (1943).
2. Hodgkin, A. L. & Katz, B. The effect of sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. 108, 37–77 (1949).
3. Hodgkin, A. L. & Huxely, A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500–544 (1952).
4. Adams, D. J., Smith, S. J. & Thompson, S. H. Ionic currents in molluscan soma. Annu. Rev. Neurosci. 3, 141–167 (1980).
5. Jones, S. W. On the resting potential of isolated frog sympathetic neurons. Neuron 3, 153–161 (1989).
6. Koyano, K., Tanaka, K. & Kuba, K. A patch-clamp study on the muscarine-sensitive potassium channel in bullfrog sympathetic ganglion cells. J. Physiol. 454, 231–246 (1992).
7. Chang, D. C. Is the K+ permeability of the resting membrane controlled by the excitable K+ channel? Biophys. J. 50, 1095–1100 (1986).
8. Schmidt, H. & Stampfli, R. The effect of tetraethylammonium chloride on single Ranvier’s nodes. Pflugers Arch. Gesamte Physiol. Menschen Tiere 287, 311–325 (1966).
9. Hille, B. Potassium channels in myelinated nerve. Selective permeability to small cations. J. Gen. Physiol. 61, 669–686 (1973).
10. Baker, M., Bostock, H., Grafe, P. & Martius, P. Function and distribution of three types of rectifying channel in rat spinal root myelinated axons. J. Physiol. 383, 45–67 (1987).
11. Nicoll, R. A., Malenka, R. C. & Kauer, J. A. Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol. Rev. 70, 513–565 (1990).
12. McCormick, D. A. & Bal, T. Sleep and arousal: thalamocortical mechanisms. Annu. Rev. Neurosci. 20, 185–215 (1997).
13. Koh, D. S., Jonas, P., Brau, M. E. & Vogel, W. A TEAinsensitive flickering potassium channel active around the resting potential in myelinated nerve. J. Membr. Biol. 130, 149–162 (1992).
14. Wu, J. V., Rubinstein, C. T. & Shrager, P. Single channel characterization of multiple types of potassium channels in demyelinated Xenopus axons. J. Neurosci. 13, 5153–5163 (1993).
15. Apkon, M. & Nerbonne, J. M. Are there multiple types of depolarization–activated K+ channels in adult ventricular myocytes? Biophys. J. 53, 458a (1988).
16. Yue, D. T. & Marban, E. A novel cardiac potassium channel that is active and conductive at depolarized potentials. Pfluegers Arch. 413, 127–133 (1988).
17. Boyle, W. A. & Nerbonne, J. M. Two functionally distinct 4- aminopyridine-sensitive outward K+ currents in rat atrial myocytes. J. Gen. Physiol. 100, 1041–1067 (1992).
18. Wang, Z., Fermini, B. & Nattel, S. Sustained depolarizationinduced outward current in human atrial myocytes. Evidence for a novel delayed rectifier K+ current similar to Kv1.5 cloned channel currents. Circ. Res. 73, 1061–1076 (1993).
19. Backx, P. H. & Marban, E. Background potassium current active during the plateau of the action potential in guinea pig ventricular myocytes. Circ. Res. 72, 890–900 (1993).
20. Van Wagoner, D. R., Pond, A. L., McCarthy, P. M., Trimmer, J. S. & Nerbonne, J. M. Outward K+ current densities and Kv1.5 expression are reduced in chronic human atrial fibrillation. Circ. Res. 80, 772–781 (1997).
21. Siegelbaum, S. A., Camardo, J. S. & Kandel, E. R. Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurons. Nature 299, 413–417 (1982).
22. Shen, K. Z., North, R. A. & Surprenant, A. Potassium channels opened by noradrenaline and other transmitters in excised membrane patches of guinea-pig submucosal neurons. J. Physiol. (Lond.) 445, 581–599 (1992).
23. Buckler, K. J. A novel oxygen-sensitive potassium current in rat carotid body type I cells. J. Physiol. 498, 649–662 (1997).
24. Wagner, P. G. & Dekin, M. S. cAMP modulates an S-type K+ channel coupled to GABAB receptors in mammalian respiratory neurons. Neuroreport 8, 1667–1670 (1997).
25. Ketchum, K. A., Joiner, W. J., Sellers, A. J., Kaczmarek, L. K. & Goldstein, S. A. N. A new family of outwardly-rectifying potassium channel proteins with two pore domains in tandem. Nature 376, 690–695 (1995).
26. Zhou, X. L., Vaillant, B., Loukin, S. H., Kung, C. & Saimi, Y. YKC1 encodes the depolarization-activated K+ channel in the plasma membrane of yeast. FEBS Lett. 373, 170–176 (1995).
27. Reid, J. D. et al. The S. cerevisiae outwardly-rectifying potassium channel (DUK1) identifies a new family of channels with duplicated pore domains. Receptors Channels 4, 51–62 (1996).
28. Vergani, P., Miosga, T., Jarvis, S. M. & Blatt, M. R. Extracellular K+ and Ba2+ mediate voltage-dependent inactivation of the outward-rectifying K+ channel encoded by the yeast gene TOK1. FEBS Lett. 405, 337–344 (1997).
29. Yost, C. S., Gray, A. T., Winegar, B. D. & Leonoudakis, D. Baseline K+ channels as targets of general anesthetics: studies of the action of volatile anesthetics on TOK1. Toxicol Lett. 100, 293–300 (1998).
30. Gray, A. T., Winegar, B. D., Leonoudakis, D. J., Forsayeth, J. R. & Yost, C. S. TOK1 is a volatile anesthetic stimulated K+ channel. Anesthesiology 88, 1076–1084 (1998).
31. Vergani, P., Hamilton, D., Jarvis, S. & Blatt, M. R. Mutations in the pore regions of the yeast K+ channel YKC1 affect gating by extracellular K+. EMBO J. 17, 7190–7198 (1998).
32. Fairman, C., Zhou, X. L., & Kung, C. Potassium uptake through the TOK1 K+ channel in the budding yeast. J. Membr. Biol. 168, 149–157 (1999).
33. Ahmed, A. et al. A molecular target for viral killer toxin: TOK1 potassium channels. Cell 99, 283–291 (1999).
34. Loukin, S. H. & Saimi, Y. K+-dependent composite gating of the yeast K+ channel, Tok1. Biophys. J. 77, 3060–3070 (1999).
35. Sesti, F., Shih, T., Nikoleva, N. & Goldstein, S. A. N. The basis for immunity to killer toxin: channel block. Biophys. J. 80, 446a (2001).
36. Goldstein, S. A. N., Price, L. A., Rosenthal, D. N. & Pausch, M. H. ORK1, a potassium-selective leak channel with two pore domains cloned from Drosophila melanogaster by expression in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 93, 13256–13261 (1996).
37. Zilberberg, N., Ilan, N., Gonzalez-Colaso, R. & Goldstein, S. A. N. Opening and closing of KCNK0 potassium leak channels is tightly-regulated. J. Gen. Physiol. 116, 721–734 (2000).
38. Ilan, N. & Goldstein, S. A. N. KCNK0: single, cloned potassium leak channels are multi-ion pores. Biophys. J. 80, 241–254 (2001).
39. Yellen, G., Jurman, M. E., Abramson, T. & MacKinnon, R. Mutations affecting internal TEA blockade identify the probable pore-forming region of a K+ channel. Science 251, 939–942 (1991).
40. Heginbotham, L., Lu, Z., Abramson, T. & MacKinnon, R. Mutations in the K+ channel signature sequence. Biophys. J. 66, 1061–1067 (1994).
41. Sigworth, F. J. Voltage gating of ion channels. Q. Rev. Biophys. 27, 1–40 (1994).
42. Yellen, G. The moving parts of voltage-gated ion channels. Q. Rev. Biophys. 31, 239–295 (1998).
43. Vandenberg, C. A. Inward rectification of a potassium channel in cardiac ventricular cells depends on internal magnesium ions. Proc. Natl Acad. Sci. USA 84, 2560–2564 (1987).
44. Jan, L. Y. & Jan, Y. N. Potassium channels and their evolving gates. Nature 371, 119–122 (1994).
45. Lopatin, A. N., Makhina, E. N. & Nichols, C. G. Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372, 366–369 (1994).
46. MacKinnon, R. Determination of the subunit stoichiometry of a voltage-activated potassium channel. Nature 350, 232–235 (1991).
47. Doyle, D. A. et al. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280, 69–77 (1998).
48. Lesage, F. et al. TWIK-1, a ubiquitous human weakly inward rectifying K+ channel with a novel structure. EMBO J. 15, 1004–1011 (1996).
49. Goldstein, S. A. N., Wang, K. W., Ilan, N. & Pausch, M. Sequence and function of the two P domain potassium channels: implications of an emerging superfamily. J. Mol. Med. 76, 13–20 (1998).
50. Pountney, D. J. et al. Identification and cloning of TWIKoriginated similarity sequence (TOSS): a novel human 2-pore K+ channel principal subunit. FEBS Lett. 450, 191–196 (1999).
51. Bockenhauer, D., Nimmakayalu, M. A., Ward, D. C., Goldstei, S. A. N. & Gallagher, P. G. Genomic organization and chromosomal localization of the murine 2 P domain potassium channel gene Kcnk8: conservation of gene structure in 2 P domain potassium channels. Gene (in the press.)
52. Salinas, M. et al. Cloning of a new mouse two-P domain channel subunit and a human homologue with a unique pore structure. J. Biol. Chem. 274, 11751–11760 (1999).
53. Chavez, R. A. et al. TWIK-2, a new weak inward rectifying member of the tandem pore domain potassium channel family. J. Biol. Chem. 274, 7887–7892 (1999).
54. Wang, Z. W., Kunkel, M. T., Wei, A., Butler, A. & Salkoff, L. Genomic organization of nematode 4TM K+ channels. Ann. NY Acad. Sci. 868, 286–303 (1999).
55. Kunkel, M. T., Johnstone, D. B., Thomas, J. H. & Salkoff, L. Mutants of a temperature-sensitive two-P domain potassium channel. J. Neurosci. 20, 7517–7524 (2000).
56. Czempinski, K., Zimmermann, S., Ehrhardt, T. & Muller-Rober, B. New structure and function in plant K+ channels: KCO1, an outward rectifier with a steep Ca2+ dependency. EMBO J. 16, 2565–2575 (1997).
57. Bockenhauer, D., Zilberberg, N. & Goldstein, S. A. N. A hippocampal potassium leak pore into a voltage-dependent channel by phosphorylation. (submitted).
58. Bockenhauer, D. & Goldstein, S. A. N. Excitement: creating a voltage-dependent potassium channel from a leak. Biophys. J. 80, 193a (2001).
59. Loukin, S. H. et al. Random mutagenesis reveals a region important for gating of the yeast K+ channel Ykc1. EMBO J. 16, 4817–4825 (1997).
60. Kim, Y., Bang, H. & Kim, D. TASK-3, a new member of the tandem pore K+ channel family. J. Biol. Chem. 275, 9340–9347 (2000).
61. Lopes, C. M. B., Gallagher, P. G., Buck, M. E., Butler, M. H. & Goldstein, S. A. N. Proton block and voltage-gating are potassium-dependent in the cardiac leak channel Kcnk3. J. Biol. Chem. 275, 16969–16978 (2000).
62. Hille, B. & Schwarz, W. Potassium channels as multi-ion single-file pores J. Gen. Physiol. 72, 409–442 (1978).
63. Yellen, G. Ionic permeation and blockade in Ca2+-activated K+ channels of bovine chromaffin cells. J. Gen. Physiol. 84, 157–186 (1984).
64. 2+-activated K+ channel. J. Gen. Physiol. 92, 569-586 (1988).
65. Heginbotham, L. & MacKinnon, R. Conduction properties of the cloned Shaker K+ channel. Biophys. J. 65, 2089-2096 (1993).
66. Lu, Z. & MacKinnon, R. A conductance maximum observed in an inward-rectifier potassium channel. J. Gen. Physiol. 104, 477-486 (1994).
67. Chapman, M. L., Krovetz, H. S. & VanDongen, A. M. J. GYGD pore motifs in neighbouring potassium channel subunits interact to determine ion selectivity. J. Physiol. 530, 21-33 (2001).
68. Levitan, I. B. Modulation of ion channels by protein phosphorylation and dephosphorylation. Annu. Rev. Physiol. 56, 193-212 (1994).
69. +channel. EMBO J. 15, 6854-6862 (1996).
70. +channel. EMBO J. 19, 2483-2491 (2000).
71. Maingret, F., Patel, A. J., Lesage, F., Lazdunski, M. & Honore, E. Lysophospholipids open the two-pore domain mechano-gated K+ channels TREK-1 and TRAAK. J. Biol. Chem. 275, 10128-10133 (2000).
72. Meadows, H. J. et al. Cloning, localisation and functional expression of the human orthologue of the TREK-1 potassium channel. PflugersArch. Eur. J. Physiol. 439, 714-722 (2000).
73. Rajan, S. et al. THIK-1 and THIK-2, a novel subfamily of tandem pore domain K+ channels. J. Biol. Chem. (in the press).
74. Greenwald, I. S. & Horvitz, H. R. unc-93(e1500): A behavioral mutant of Caenorhabditis elegansthat defines a gene with a wild-type null phenotype. Genetics 96, 147-164 (1980).
75. + channel to sense external pH variations near physiological pH. EMBO J. 16, 5464-5471 (1997).
76. Leonoudakis, D. et al. An open rectifier potassium channel with two pore domains in tandem cloned from rat cerebellum. J. Neurosci. 18, 868-877 (1998).
77. Kim, D., Fujita, A., Horio, Y. & Kurachi, Y. Cloning and functional expression of a novel cardiac two-pore background K+channel (cTBAK-1). Circ. Res. 82, 513-518 (1998).
78. Lopes, C. M. B., Gallagher, P. G., Wong, C., Buck, M. & Goldstein, S. A. N. OATs: open, acid-sensitive, two P domain K+ channels from mouse heart. J. Biophys. 74, A44 (1998).
79. Kindler, C. H., Yost, C. S. & Gray, A. T. Local anesthetic inhibition of baseline potassium channels with two pore domains in tandem. Anesthesiology 90, 1092-1102 (1999).
80. Manjunath, N. A., Bray-Ward, P., Goldstein, S. A. N. & Gallagher, P. G. Assignment of the 2 P domain, acid- sensitive potassium channel gene OAT1 (KCNK3) to human chromosome 2p23. 3-p24. 1 and murine chromosome band 5B by in situ hybridization. Cytogen. Cell Gen. 86, 242-243 (1999).
81. + channel subunits: kinetic properties and expression in rat heart. Am. J. Physiol. 277, H1669-H1678 (1999).
82. Millar, J. A. et al. A functional role for the two-pore domain potassium channel TASK-1 in cerebellar granule neurons. Proc. Natl Acad. Sci. USA 97, 3614-3618 (2000).
83. + channel, is modulated by multiple neurotransmitters in motoneurons. Neuron 25, 399-410 (2000).
84. Buckler, K. J., Williams, B. A. & Honore, E. An oxygen-, acid- and anaesthetic-sensitive TASK-like background potassium channel in rat arterial chemoreceptor cells. J. Physiol. (Lond.) 525, 135-142 (2000).
85. + channel) is expressed in glomerulosa cells of rat adrenal cortex and inhibited by angiotensin II. Mol. Endocrinol. 14, 863-874 (2000).
86. + channel is a molecular substrate for neuronal effects of inhalation anesthetics. J. Neurosci. 20, 6347-6354 (2000).
87. Gray, A. T. et al. Volatile anesthetics activate the human tandem pore domain baseline K+ channel KCNK5. Anesthesiology 92, 1722-1730 (2000).
88. + channel diversity in the mammalian myocardium. J. Physiol. 525, 285-298 (2000).
89. + current in a vertebrate neuron. Nature 283, 673-676 (1980).
90. Wang, H. S. et al. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282, 1890-1893 (1998).
91. Jentsch, T. J. Neuronal KCNQ potassium channels: physiology and role in disease. Nature Rev. Neurosci. 1, 21-30 (2000).
92. Patel, A. J. et al. A mammalian two pore domain mechano- gated S-like K+channel. EMBO J. 17, 4283-4290 (1998).
93. Maingret, F., Fosset, M., Lesage, F., Lazdunski, M. & Honore, E. TRAAK is a mammalian neuronal mechano- gated K+channel. J. Biol. Chem. 274, 1381-1387 (1999).
94. Klein, M. & Kandel, E. R. Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization in Aplysia. Proc. Natl Acad. Sci. USA 77, 6912-6916 (1980).
95. O'Kelly, I., Stephens, R. H., Peers, C. & Kemp, P J. Potential identification of the O2-sensitive K+ current in a human neuroepithelial body-derived cell line. Am. J. Physiol. 276, L96-L104 (1999).
96. Lesage, F. et al. Dimerization of TWIK-1 K+channel subunits via a disulfide bridge. EMBO J. 15, 6400-6407 (1996).
97. Dodge, F. A. & Frankenhaeuser, B. Membrane currents in isolated frog nerve fibre under voltage clamp conditions. J. Physiol. 143, 76-90 (1958).
98. Campbell, D. T. & Hille, B. Kinetic and pharmacological properties of the sodium channel of frog skelet al muscle. J. Gen. Physiol. 67, 309-323 (1976).
99. Anderson, J. A., Huprikar, S. S., Kochian, L. V., Lucas, W. J. & Gaber, R. F. Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 89, 3736-3740 (1992).
100. +- channel proteins. Nature 374, 135-141 (1995).
101. Abbott, G. W. MiRP2 forms potassium channels in skelet al muscle with Kv3.4 and is associated with periodic paralysis. Cell 104, 217-231 (2001).
102. Splawski, I. et al. Spectrum of mutations in long-QT syndrome genes. KVLQT1, HERG, SCN5A, KCNE1, and KCNE2. Circulation 102, 1178-1185 (2000).
103. Schroeder, B. C. A constitutively open potassium channel formed by KCNQ1 and KCNE3. Nature 403, 196-199 (2000).
104. Melman, Y. F., Domenech, A., de la Luna, S. & McDonald, T. V. Structural determinants of KvLQT1 control by the KCNE family of proteins. J. Biol. Chem. (in the press).
105. Orias, M., Velazquez, H., Tung, F., Lee, G. & Desir, G. V. Cloning and localization of a double-pore K channel, KCNK1: exclusive expression in distal nephron segments. Am. J. Physiol. 273, F663-F666 (1997).
106. Lesage, F. et al. The structure, function and distribution of the mouse TWIK-1 K+ channel. FEBS Lett. 402, 28-32 (1997).
107. Fink, M. et al. A neuronal two P domain K+ channel stimulated by arachidonic acid and polyunsaturated fatty acids. EMBO J. 17, 3297-3308 (1998).
108. Reyes, R. et al. Immunolocalization of the arachidonic acid and mechanosensitive baseline traak potassium channel in the nervous system. Neuroscience 95, 893-901 (2000).
109. + channel. FEBS Lett. 471, 137-140 (2000).
110. + channel from human kidney. J. Biol. Chem. 273, 30863-30869 (1998).
111. Gray, A. T., Kindler, C. H., Sampson, E. R. & Yost, C. S. Assignment of KCNK6 encoding the human weak inward rectifier potassium channel TWIK-2 to chromosome band 19q13.1 by radiation hybrid mapping. Cytogenet. Cell Genet. 84, 190-191 (1999).
112. Patel, A. J. et al. TWIK-2, an inactivating 2P domain K+ channel. J. Biol. Chem. 275, 28722-28730 (2000).
113. Chapman, C. G. et al. Cloning, localisation and functional expression of a novel human, cerebellum specific, two pore domain potassium channel. Mol. Brain Res. 82, 74-83 (2000).
114. Rajan, S. et al. TASK-3, a novel tandem pore domain acid- sensitive K+ channel — an extracellular histidine as pH sensor. J. Biol. Chem. 275, 16650-16657 (2000).
115. Bang, H., Kim, Y. & Kim, D. TREK-2, a new member of the mechanosensitive tandem-pore K+ channel family. J. Biol. Chem. 275, 17412-17419 (2000).
116. + channel with multiple regulations by polyunsaturated fatty acids, lysophospholipids, and Gs, Gi, and Gq protein-coupled receptors. J. Biol. Chem. 275, 28398-28405 (2000).