Abstract
Electrocytes from the electric organ of Electrophorus electricus exhibited sodium action potentials that have been proposed to be repolarized by leak currents and not by outward voltage-gated potassium currents. However, patch-clamp recordings have suggested that electrocytes may contain a very low density of voltage-gated K+ channels. We report here the cloning of a K+ channel from an eel electric organ cDNA library, which, when expressed in mammalian tissue culture cells, displayed delayed-rectifier K+ channel characteristics. The amino-acid sequence of the eel K+ channel had the highest identity to Kv1.1 potassium channels. However, different important functional regions of eel Kv1.1 had higher amino-acid identity to other Kv1 members, for example, the eel Kv1.1 S4-S5 region was identical to Kv1.5 and Kv1.6. Northern blot analysis indicated that eel Kv1.1 mRNA was expressed at appreciable levels in the electric organ but it was not detected in eel brain, muscle, or cardiac tissue. Because electrocytes do not express robust outward voltage-gated potassium currents we speculate that eel Kv1.1 channels are chronically inhibited in the electric organ and may be functionally recruited by an unknown mechanism.
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References
F.M. Ausubel R. Brent R.E. Kingston D.D. More J.G. Seidman J.A. Smith . Struhl (1990) Current Protocols in Molecular Biology: vol 1 and 2. John Wiley & Sons New York, NY
P. Chomczyznski N. Sacchi (1987) ArticleTitleSingle-step method of RNA isolation by guanidinium thiocyanate-phenol-chloroform extraction. Analyt. Biochem. 162 156–159 Occurrence Handle10.1006/abio.1987.9999 Occurrence Handle2440339
K. Bielefeldt M.B. Jackson (1994) ArticleTitlePhosphorylation and dephosphorylation modulate a Ca-activated K channel in rat peptidergic nerve terminals. J. Physiol. 475 241–254 Occurrence Handle1:CAS:528:DyaK2cXivFGjtrY%3D Occurrence Handle8021831
M.J. Christie J.P. Adelman J. Douglass R.A. North (1989) ArticleTitleExpression of a cloned rat brain potassium channel in Xenopus oocytes. Science 244 221–224 Occurrence Handle1:CAS:528:DyaK3cXjtFCjtA%3D%3D Occurrence Handle2539643
G.C. Frech A.M.J. VanDongen G. Schuster A.M. Brown R.H. Joho (1989) ArticleTitleA novel potassium channel with delayed rectifier properties isolated from rat brain by expression cloning. Nature 340 642–645 Occurrence Handle1:CAS:528:DyaK3cXitlSmt7w%3D Occurrence Handle2770868
A. Grupe K.H. Schroter J.P. Ruppersberg M. Stocker T. Drewes S. Beckh O. Pongs (1990) ArticleTitleCloning and expression of a human voltage-gated potassium channel. A novel member of the RCK potassium channel family. EMBO J. 9 1749–1756 Occurrence Handle1:CAS:528:DyaK3cXmtVGku70%3D Occurrence Handle2347305
B. Hille (2001) Ionic channels of excitable membranes, 3rd ed. Sinauer Sunderland, Massachusetts
E.Y. Isacoff Y.N. Jan L.Y. Jan (1991) ArticleTitlePutative receptor for the cytoplasmic inactivation gate in the Shaker K+ channel. Nature 353 86–89 Occurrence Handle10.1038/353086a0 Occurrence Handle1:CAS:528:DyaK3MXlvVSisbY%3D Occurrence Handle1881453
T. Ivanina T. Perez W.B. Thornhill G. Levin N. Dascal I. Lotan (1994) ArticleTitlePhosphorylation of RCK1 K+ channels expressed in Xenopus oocytes by protein kinase A. Biochemistry 33 8786–8792 Occurrence Handle1:CAS:528:DyaK2cXksl2hsr0%3D Occurrence Handle8038169
L.Y. Jan Y.N. Jan (1990) ArticleTitleHow might the diversity of potassium channels be generated? Trends Neurosci. 13 415–419 Occurrence Handle10.1016/0166-2236(90)90123-R Occurrence Handle1:CAS:528:DyaK3MXjvFClsA%3D%3D Occurrence Handle1700515
L.K. Kaczmareck I.B. Levitan (1987) Neuromodulation: The biochemical control of neuronal excitability. Oxford University Press N. Y.
M.P. Kavanaugh M.D. Varnum P.B. Osborne P.B. Christie M.J. Busch J.P. Adelman R.A. North (1991) ArticleTitleInteraction between tetraethylammonium and amino acid residues in the pore of cloned voltage-dependent potassium channels. J. Biol. Chem. 263 7584–7587
R.D. Keynes H. Martins-Ferreira (1953) ArticleTitleMembrane potentials in the electroplates of the electric eel. J. Physiol. 119 315 Occurrence Handle13035755
G.E. Kirsch M. Taglialatela A.M. Brown (1991) ArticleTitleInternal and external TEA block in a single cloned K+ channel. Am. J. Physiol. 261 C583–C590 Occurrence Handle1:CAS:528:DyaK3MXmsFaltb8%3D Occurrence Handle1928322
R. Latorre A. Aberhauser P. Labarca O. Alvarez (1989) ArticleTitleVarieties of calcium-activated potassium channels. Annu. Rev. Physiol. 51 385–399 Occurrence Handle10.1146/annurev.ph.51.030189.002125 Occurrence Handle1:CAS:528:DyaL1MXhvV2rsL4%3D Occurrence Handle2653189
S.R. Levinson D. Duch W.B. Thornhill (1986) ArticleTitleUnusual molecular properties of the sodium channel isolated from the electric organ of Electrophorus electricus. Neurol. Neurobiol. 20 375–393 Occurrence Handle1:CAS:528:DyaL28XkvFaqtrw%3D
I.B. Levitan (1988) ArticleTitleModulation of ion channels in neurons and other cells. Annu. Rev. Neurosci. 11 119–136 Occurrence Handle10.1146/annurev.ne.11.030188.001003 Occurrence Handle1:CAS:528:DyaL1cXhvVahtLw%3D Occurrence Handle2452594
R. MacKinnon C. Yellen (1990) ArticleTitleMutations affecting TEA blockade and ion permeation in voltage-activated K channels. Science 250 271–279 Occurrence Handle2218529
K. McCormack M.A. Tanouye L.E. Iverson J.W. Line M. Ramaswami T. McCormack J.T. Campanelli M.K. Mathew B. Rudy (1991) ArticleTitleA role for hydrophobic residues in the voltage-dependent gating of Shaker K channels. Proc. Natl Acad. Sci. 88 2931–2935 Occurrence Handle1:CAS:528:DyaK3MXhvVaksLk%3D Occurrence Handle2011602
H. Moreno C. Kentros E. Bueno M. Weiser A. Herdandez E. Vega-Saenz de Miera W.B. Thornhill B. Rudy (1995) ArticleTitleThalamocortical projections have a K channel that is phosphorylated and modulated by cAMP-dependent protein kinase. J. Neurosci. 15 5486–5501 Occurrence Handle1:CAS:528:DyaK2MXnsVOrsb0%3D Occurrence Handle7643197
Y. Nakamura S. Nakajima H. Grundfest (1964) ArticleTitleEel electroplaques: spike electrogenesis without potassium activation. Science 146 266 Occurrence Handle1:STN:280:CCuC2czjsVI%3D Occurrence Handle14185324
Y. Nakamura S. Nakajima H. Grundfest (1965) ArticleTitleAnalysis of spike electrogenesis and depolarizing K inactivation in electroplaques of Electrophorus electricus. J. Gen. Physiol. 49 321–348
T.M. Perney L.K. Kaczmarek (1991) ArticleTitleThe molecular biology of K channels. Curr. Opin. Cell Bio. 3 663–670 Occurrence Handle1:CAS:528:DyaK3MXmt1Khs70%3D
O. Pongs (1992) ArticleTitleMolecular biology of voltage-dependent potassium channels. Physiol. Rev. (Supplement on Forty Years of Membrane Current in Nerve) 72 S79–S88
A.B. Ribera (1991) ArticleTitleA K channel gene is expressed at neural induction. Neuron 5 691–701
A.B. Ribera D.A. Nguyen (1993) ArticleTitlePrimary sensory neurons express a Shaker-like K channel gene. J. Neurosci. 13 4988–4996 Occurrence Handle1:CAS:528:DyaK2cXhtValtrk%3D Occurrence Handle8229210
B. Rudy (1988) ArticleTitleDiversity and ubiquity of K channels. Neuroscience 25 729–750 Occurrence Handle1:CAS:528:DyaL1cXlt1CntLY%3D Occurrence Handle2457185
B. Rudy C. Kentros E. Vega-Saenz de Miera (1991) ArticleTitleFamilies of K channel genes in mammals: Toward an understanding of the molecular basis of K channel diversity. Mol. Cell. Neurosci. 2 89–102 Occurrence Handle1:CAS:528:DyaK3MXltlans7w%3D
F. Ruiz-Manresa A.C. Ruarte T.L. Schwartz H. Grundfest (1970) ArticleTitlePotassium inactivation and impedance changes during spike electrogenesis in eel electroplaques. J. Gen. Physiol. 55 33–47 Occurrence Handle1:CAS:528:DyaE3cXoslGgsg%3D%3D Occurrence Handle5410488
L. Salkoff K. Baker A. Butler M. Covarrubias M.D.A. Pak A. Wei (1992) ArticleTitleAn essential “set” of K+ channels conserved in flies, mice and humans. Trends Neurosci. 15 161–166 Occurrence Handle10.1016/0166-2236(92)90165-5 Occurrence Handle1:STN:280:By2A3M7pvFY%3D Occurrence Handle1377421
S. Skenkel F.J. Sigworth (1991) ArticleTitlePatch recordings from the electrocytes of Electrophorus electricus. J. Gen Physiol. 97 1013–1041 Occurrence Handle1650809
W. Stuhmer J.P. Ruppersberg K.H. Schruer B. Sakmann M. Stocker K.P. Giese A. Perschke A. Baumann O. Pongs (1989) ArticleTitleMolecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO J. 8 3235–3244 Occurrence Handle1:STN:280:By%2BD2MbptFA%3D Occurrence Handle2555158
R. Swanson J. Marshall J.S. Smith J.B. Williams M.B. Boyle K. Folander C.J. Luneau J. Antanavage C. Oliva S.A. Buhrow C. Vennett R.B. Stein L.K. Kaczmarek (1990) ArticleTitleCloning and expression of cDNA and genomic clones encoding three delayed rectifier potassium channels in rat brain. Neuron 4 929–939 Occurrence Handle1:CAS:528:DyaK38Xlt1Gruw%3D%3D Occurrence Handle2361015
M. Taglialatela A.M.J. VanDongen J.A. Drewe R.H. Joho A.M. Brown G.R. Kirsch (1991) ArticleTitlePatterns of internal and external tetraethylammonium block in four holologous K channels. Mol. Pharmacol. 40 299–307 Occurrence Handle1:CAS:528:DyaK3MXlvVSgu7g%3D Occurrence Handle1875913
W.B. Thormhill M.B. Wu X. Jiang X. Wu P. Morgan J.F. Margiotta (1996) ArticleTitleExpression of Kv1.1 delayed-rectifier potassium channels in Lec Mutant CHO cell lines reveals a role for sialidation in channel function. J. Biol. Chem. 271 19093–19098 Occurrence Handle10.1074/jbc.271.32.19093 Occurrence Handle8702582
E. Vega-Saenz de Miera M.E. Weiser C. Kentros D. Lau H. Moreno P. Serodio B. Rudy (1994) Shaw-related K channels in mammals. Handbook of Membrane Channels Academic Press . 41–78
A. Wei M. Covarrubias A. Bulter K. Baker M. Pak L. Salkoff (1990) ArticleTitleK current diversity is produced by an extended gene family conserved in Drosophila and mouse. Science 248 599–603 Occurrence Handle1:CAS:528:DyaK3cXlvVGltL0%3D Occurrence Handle2333511
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This research was supported by National Institutes of Health Grant NS29633 (W.B.T).
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Thornhill, W., Watanabe, I., Sutachan, J. et al. Molecular Cloning and Expression of a Kv1.1-like Potassium Channel from the Electric Organ of Electrophorus electricus . J. Membrane Biol. 196, 1–8 (2003). https://doi.org/10.1007/s00232-003-0619-x
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DOI: https://doi.org/10.1007/s00232-003-0619-x