Nonequilibrium gating and voltage dependence of the ClC-0 Cl- channel (original) (raw)

Abstract

The gating of ClC-0, the voltage-dependent Cl- channel from Torpedo electric organ, is strongly influenced by Cl- ions in the external solution. Raising external Cl- over the range 1-600 mM favors the fast- gating open state and disfavors the slow-gating inactivated state. Analysis of purified single ClC-0 channels reconstituted into planar lipid bilayers was used to identify the role of Cl- ions in the channel's fast voltage-dependent gating process. External, but not internal, Cl- had a major effect on the channel's opening rate constant. The closing rate was more sensitive to internal Cl- than to external Cl-. Both opening and closing rates varied with voltage. A model was derived that postulates (a) that in the channel's closed state, Cl- is accessible to a site located at the outer end of the conduction pore, where it binds in a voltage-independent fashion, (b) that this closed conformation can open, whether liganded by Cl- or not, in a weakly voltage-dependent fashion, (c) that the Cl(-)-liganded closed channel undergoes a conformational change to a different closed state, such that concomitant with this change, Cl- ion moves inward, conferring voltage-dependence to this step, and (d) that this new Cl(-)- liganded closed state opens with a very high rate. According to this picture, Cl- movement within the pre-open channel is the major source of voltage dependence, and charge movement intrinsic to the channel protein contributes very little to voltage-dependent gating of ClC-0. Moreover, since the Cl- activation site is probably located in the ion conduction pathway, the fast gating of ClC-0 is necessarily coupled to ion conduction, a nonequilibrium process.

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Selected References

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  1. Bauer C. K., Steinmeyer K., Schwarz J. R., Jentsch T. J. Completely functional double-barreled chloride channel expressed from a single Torpedo cDNA. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11052–11056. doi: 10.1073/pnas.88.24.11052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bryant S. H., Morales-Aguilera A. Chloride conductance in normal and myotonic muscle fibres and the action of monocarboxylic aromatic acids. J Physiol. 1971 Dec;219(2):367–383. doi: 10.1113/jphysiol.1971.sp009667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. George A. L., Jr, Crackower M. A., Abdalla J. A., Hudson A. J., Ebers G. C. Molecular basis of Thomsen's disease (autosomal dominant myotonia congenita). Nat Genet. 1993 Apr;3(4):305–310. doi: 10.1038/ng0493-305. [DOI] [PubMed] [Google Scholar]
  5. Goldberg A. F., Miller C. Solubilization and functional reconstitution of a chloride channel from Torpedo californica electroplax. J Membr Biol. 1991 Dec;124(3):199–206. doi: 10.1007/BF01994354. [DOI] [PubMed] [Google Scholar]
  6. Gründer S., Thiemann A., Pusch M., Jentsch T. J. Regions involved in the opening of CIC-2 chloride channel by voltage and cell volume. Nature. 1992 Dec 24;360(6406):759–762. doi: 10.1038/360759a0. [DOI] [PubMed] [Google Scholar]
  7. Hanke W., Miller C. Single chloride channels from Torpedo electroplax. Activation by protons. J Gen Physiol. 1983 Jul;82(1):25–45. doi: 10.1085/jgp.82.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jentsch T. J., Günther W., Pusch M., Schwappach B. Properties of voltage-gated chloride channels of the ClC gene family. J Physiol. 1995 Jan;482:19S–25S. doi: 10.1113/jphysiol.1995.sp020560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jentsch T. J., Steinmeyer K., Schwarz G. Primary structure of Torpedo marmorata chloride channel isolated by expression cloning in Xenopus oocytes. Nature. 1990 Dec 6;348(6301):510–514. doi: 10.1038/348510a0. [DOI] [PubMed] [Google Scholar]
  10. Kawasaki M., Uchida S., Monkawa T., Miyawaki A., Mikoshiba K., Marumo F., Sasaki S. Cloning and expression of a protein kinase C-regulated chloride channel abundantly expressed in rat brain neuronal cells. Neuron. 1994 Mar;12(3):597–604. doi: 10.1016/0896-6273(94)90215-1. [DOI] [PubMed] [Google Scholar]
  11. Larsson H. P., Baker O. S., Dhillon D. S., Isacoff E. Y. Transmembrane movement of the shaker K+ channel S4. Neuron. 1996 Feb;16(2):387–397. doi: 10.1016/s0896-6273(00)80056-2. [DOI] [PubMed] [Google Scholar]
  12. Lloyd S. E., Pearce S. H., Fisher S. E., Steinmeyer K., Schwappach B., Scheinman S. J., Harding B., Bolino A., Devoto M., Goodyer P. A common molecular basis for three inherited kidney stone diseases. Nature. 1996 Feb 1;379(6564):445–449. doi: 10.1038/379445a0. [DOI] [PubMed] [Google Scholar]
  13. Middleton R. E., Pheasant D. J., Miller C. Purification, reconstitution, and subunit composition of a voltage-gated chloride channel from Torpedo electroplax. Biochemistry. 1994 Nov 15;33(45):13189–13198. doi: 10.1021/bi00249a005. [DOI] [PubMed] [Google Scholar]
  14. Miller C. Open-state substructure of single chloride channels from Torpedo electroplax. Philos Trans R Soc Lond B Biol Sci. 1982 Dec 1;299(1097):401–411. doi: 10.1098/rstb.1982.0140. [DOI] [PubMed] [Google Scholar]
  15. Miller C., White M. M. A voltage-dependent chloride conductance channel from Torpedo electroplax membrane. Ann N Y Acad Sci. 1980;341:534–551. doi: 10.1111/j.1749-6632.1980.tb47197.x. [DOI] [PubMed] [Google Scholar]
  16. Moczydlowski E., Latorre R. Gating kinetics of Ca2+-activated K+ channels from rat muscle incorporated into planar lipid bilayers. Evidence for two voltage-dependent Ca2+ binding reactions. J Gen Physiol. 1983 Oct;82(4):511–542. doi: 10.1085/jgp.82.4.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Neyton J., Miller C. Potassium blocks barium permeation through a calcium-activated potassium channel. J Gen Physiol. 1988 Nov;92(5):549–567. doi: 10.1085/jgp.92.5.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. O'Neill G. P., Grygorczyk R., Adam M., Ford-Hutchinson A. W. The nucleotide sequence of a voltage-gated chloride channel from the electric organ of Torpedo californica. Biochim Biophys Acta. 1991 Dec 2;1129(1):131–134. doi: 10.1016/0167-4781(91)90228-e. [DOI] [PubMed] [Google Scholar]
  19. Palade P. T., Barchi R. L. On the inhibition of muscle membrane chloride conductance by aromatic carboxylic acids. J Gen Physiol. 1977 Jun;69(6):879–896. doi: 10.1085/jgp.69.6.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pusch M., Jentsch T. J. Molecular physiology of voltage-gated chloride channels. Physiol Rev. 1994 Oct;74(4):813–827. doi: 10.1152/physrev.1994.74.4.813. [DOI] [PubMed] [Google Scholar]
  21. Pusch M., Ludewig U., Rehfeldt A., Jentsch T. J. Gating of the voltage-dependent chloride channel CIC-0 by the permeant anion. Nature. 1995 Feb 9;373(6514):527–531. doi: 10.1038/373527a0. [DOI] [PubMed] [Google Scholar]
  22. Richard E. A., Miller C. Steady-state coupling of ion-channel conformations to a transmembrane ion gradient. Science. 1990 Mar 9;247(4947):1208–1210. doi: 10.1126/science.2156338. [DOI] [PubMed] [Google Scholar]
  23. Steinmeyer K., Klocke R., Ortland C., Gronemeier M., Jockusch H., Gründer S., Jentsch T. J. Inactivation of muscle chloride channel by transposon insertion in myotonic mice. Nature. 1991 Nov 28;354(6351):304–308. doi: 10.1038/354304a0. [DOI] [PubMed] [Google Scholar]
  24. Steinmeyer K., Lorenz C., Pusch M., Koch M. C., Jentsch T. J. Multimeric structure of ClC-1 chloride channel revealed by mutations in dominant myotonia congenita (Thomsen). EMBO J. 1994 Feb 15;13(4):737–743. doi: 10.1002/j.1460-2075.1994.tb06315.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Steinmeyer K., Ortland C., Jentsch T. J. Primary structure and functional expression of a developmentally regulated skeletal muscle chloride channel. Nature. 1991 Nov 28;354(6351):301–304. doi: 10.1038/354301a0. [DOI] [PubMed] [Google Scholar]
  26. Stevens C. F. Interactions between intrinsic membrane protein and electric field. An approach to studying nerve excitability. Biophys J. 1978 May;22(2):295–306. doi: 10.1016/S0006-3495(78)85490-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Swenson R. P., Jr, Armstrong C. M. K+ channels close more slowly in the presence of external K+ and Rb+. Nature. 1981 Jun 4;291(5814):427–429. doi: 10.1038/291427a0. [DOI] [PubMed] [Google Scholar]
  28. Thiemann A., Gründer S., Pusch M., Jentsch T. J. A chloride channel widely expressed in epithelial and non-epithelial cells. Nature. 1992 Mar 5;356(6364):57–60. doi: 10.1038/356057a0. [DOI] [PubMed] [Google Scholar]
  29. Uchida S., Sasaki S., Furukawa T., Hiraoka M., Imai T., Hirata Y., Marumo F. Molecular cloning of a chloride channel that is regulated by dehydration and expressed predominantly in kidney medulla. J Biol Chem. 1993 Feb 25;268(6):3821–3824. [PubMed] [Google Scholar]
  30. White M. M., Miller C. A voltage-gated anion channel from the electric organ of Torpedo californica. J Biol Chem. 1979 Oct 25;254(20):10161–10166. [PubMed] [Google Scholar]
  31. Woodbury D. J., Miller C. Nystatin-induced liposome fusion. A versatile approach to ion channel reconstitution into planar bilayers. Biophys J. 1990 Oct;58(4):833–839. doi: 10.1016/S0006-3495(90)82429-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Yang N., George A. L., Jr, Horn R. Molecular basis of charge movement in voltage-gated sodium channels. Neuron. 1996 Jan;16(1):113–122. doi: 10.1016/s0896-6273(00)80028-8. [DOI] [PubMed] [Google Scholar]