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. 1994 Feb 1;103(2):217–230. doi: 10.1085/jgp.103.2.217

Hyperpolarization-activated chloride currents in Xenopus oocytes

PMCID: PMC2216841  PMID: 7514644

Abstract

During hyperpolarizing pulses, defolliculated Xenopus oocytes have time- and voltage-dependent inward chloride currents. The currents vary greatly in amplitude from batch to batch; activate slowly and, in general, do not decay; have a selectivity sequence of I- > NO3- > Br- > Cl- > propionate > acetate; are insensitive to Ca2+ and pH; are blocked by Ba2+ and some chloride channel blockers; and have a gating valence of approximately 1.3 charges. In contrast to hyperpolarization- activated chloride currents induced after expression of phospholemman (Palmer, C. J., B. T. Scott, and L. R. Jones. 1991. Journal of Biological Chemistry. 266:11126; Moorman, J. R., C. J. Palmer, J. E. John, J. E. Durieux, and L. R. Jones. 1992. 267:14551), these endogenous currents are smaller; have a different pharmacologic profile; have a lower threshold for activation and lower voltage- sensitivity of activation; have different activation kinetics; and are insensitive to pH. Nonetheless, the endogenous and expressed current share striking similarities. Recordings of macroscopic oocyte currents may be inadequate to determine whether phospholemman is itself an ion channel and not a channel-modulating molecule.

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Selected References

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  1. Anderson M. P., Gregory R. J., Thompson S., Souza D. W., Paul S., Mulligan R. C., Smith A. E., Welsh M. J. Demonstration that CFTR is a chloride channel by alteration of its anion selectivity. Science. 1991 Jul 12;253(5016):202–205. doi: 10.1126/science.1712984. [DOI] [PubMed] [Google Scholar]
  2. Bahinski A., Nairn A. C., Greengard P., Gadsby D. C. Chloride conductance regulated by cyclic AMP-dependent protein kinase in cardiac myocytes. Nature. 1989 Aug 31;340(6236):718–721. doi: 10.1038/340718a0. [DOI] [PubMed] [Google Scholar]
  3. Barish M. E. A transient calcium-dependent chloride current in the immature Xenopus oocyte. J Physiol. 1983 Sep;342:309–325. doi: 10.1113/jphysiol.1983.sp014852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bear C. E., Duguay F., Naismith A. L., Kartner N., Hanrahan J. W., Riordan J. R. Cl- channel activity in Xenopus oocytes expressing the cystic fibrosis gene. J Biol Chem. 1991 Oct 15;266(29):19142–19145. [PubMed] [Google Scholar]
  5. Blatz A. L., Magleby K. L. Single voltage-dependent chloride-selective channels of large conductance in cultured rat muscle. Biophys J. 1983 Aug;43(2):237–241. doi: 10.1016/S0006-3495(83)84344-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chenoy-Marchais D. A Cl- conductance activated by hyperpolarization in Aplysia neurones. Nature. 1982 Sep 23;299(5881):359–361. doi: 10.1038/299359a0. [DOI] [PubMed] [Google Scholar]
  7. Chesnoy-Marchais D. Characterization of a chloride conductance activated by hyperpolarization in Aplysia neurones. J Physiol. 1983 Sep;342:277–308. doi: 10.1113/jphysiol.1983.sp014851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Coulombe A., Coraboeuf E. Large-conductance chloride channels of new-born rat cardiac myocytes are activated by hypotonic media. Pflugers Arch. 1992 Nov;422(2):143–150. doi: 10.1007/BF00370413. [DOI] [PubMed] [Google Scholar]
  9. Coulombe A., Duclohier H., Coraboeuf E., Touzet N. Single chloride-permeable channels of large conductance in cultured cardiac cells of new-born rats. Eur Biophys J. 1987;14(3):155–162. doi: 10.1007/BF00253840. [DOI] [PubMed] [Google Scholar]
  10. Durieux M. E., Salafranca M. N., Lynch K. R., Moorman J. R. Lysophosphatidic acid induces a pertussis toxin-sensitive Ca(2+)-activated Cl- current in Xenopus laevis oocytes. Am J Physiol. 1992 Oct;263(4 Pt 1):C896–C900. doi: 10.1152/ajpcell.1992.263.4.C896. [DOI] [PubMed] [Google Scholar]
  11. Ehara T., Ishihara K. Anion channels activated by adrenaline in cardiac myocytes. Nature. 1990 Sep 20;347(6290):284–286. doi: 10.1038/347284a0. [DOI] [PubMed] [Google Scholar]
  12. Franciolini F., Nonner W. Anion and cation permeability of a chloride channel in rat hippocampal neurons. J Gen Physiol. 1987 Oct;90(4):453–478. doi: 10.1085/jgp.90.4.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gabriel S. E., Clarke L. L., Boucher R. C., Stutts M. J. CFTR and outward rectifying chloride channels are distinct proteins with a regulatory relationship. Nature. 1993 May 20;363(6426):263–268. doi: 10.1038/363263a0. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Harvey R. D., Hume J. R. Autonomic regulation of a chloride current in heart. Science. 1989 May 26;244(4907):983–985. doi: 10.1126/science.2543073. [DOI] [PubMed] [Google Scholar]
  16. Isom L. L., De Jongh K. S., Patton D. E., Reber B. F., Offord J., Charbonneau H., Walsh K., Goldin A. L., Catterall W. A. Primary structure and functional expression of the beta 1 subunit of the rat brain sodium channel. Science. 1992 May 8;256(5058):839–842. doi: 10.1126/science.1375395. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Kokubun S., Saigusa A., Tamura T. Blockade of Cl channels by organic and inorganic blockers in vascular smooth muscle cells. Pflugers Arch. 1991 Apr;418(3):204–213. doi: 10.1007/BF00370515. [DOI] [PubMed] [Google Scholar]
  19. Lacerda A. E., Kim H. S., Ruth P., Perez-Reyes E., Flockerzi V., Hofmann F., Birnbaumer L., Brown A. M. Normalization of current kinetics by interaction between the alpha 1 and beta subunits of the skeletal muscle dihydropyridine-sensitive Ca2+ channel. Nature. 1991 Aug 8;352(6335):527–530. doi: 10.1038/352527a0. [DOI] [PubMed] [Google Scholar]
  20. Levesque P. C., Hart P. J., Hume J. R., Kenyon J. L., Horowitz B. Expression of cystic fibrosis transmembrane regulator Cl- channels in heart. Circ Res. 1992 Oct;71(4):1002–1007. doi: 10.1161/01.res.71.4.1002. [DOI] [PubMed] [Google Scholar]
  21. Loo D. D., McLarnon J. G., Vaughan P. C. Some observations on the behaviour of chloride current--voltage relations in Xenopus muscle membrane in acid solutions. Can J Physiol Pharmacol. 1981 Jan;59(1):7–13. doi: 10.1139/y81-002. [DOI] [PubMed] [Google Scholar]
  22. Matsuoka S., Ehara T., Noma A. Chloride-sensitive nature of the adrenaline-induced current in guinea-pig cardiac myocytes. J Physiol. 1990 Jun;425:579–598. doi: 10.1113/jphysiol.1990.sp018119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Miledi R. A calcium-dependent transient outward current in Xenopus laevis oocytes. Proc R Soc Lond B Biol Sci. 1982 Jul 22;215(1201):491–497. doi: 10.1098/rspb.1982.0056. [DOI] [PubMed] [Google Scholar]
  24. Moorman J. R., Palmer C. J., John J. E., 3rd, Durieux M. E., Jones L. R. Phospholemman expression induces a hyperpolarization-activated chloride current in Xenopus oocytes. J Biol Chem. 1992 Jul 25;267(21):14551–14554. [PubMed] [Google Scholar]
  25. Palmer C. J., Scott B. T., Jones L. R. Purification and complete sequence determination of the major plasma membrane substrate for cAMP-dependent protein kinase and protein kinase C in myocardium. J Biol Chem. 1991 Jun 15;266(17):11126–11130. [PubMed] [Google Scholar]
  26. Parker I., Gundersen C. B., Miledi R. A transient inward current elicited by hyperpolarization during serotonin activation in Xenopus oocytes. Proc R Soc Lond B Biol Sci. 1985 Jan 22;223(1232):279–292. doi: 10.1098/rspb.1985.0002. [DOI] [PubMed] [Google Scholar]
  27. Parker I., Miledi R. A calcium-independent chloride current activated by hyperpolarization in Xenopus oocytes. Proc R Soc Lond B Biol Sci. 1988 Mar 22;233(1271):191–199. doi: 10.1098/rspb.1988.0018. [DOI] [PubMed] [Google Scholar]
  28. Peres A., Bernardini G. A hyperpolarization-activated chloride current in Xenopus laevis oocytes under voltage-clamp. Pflugers Arch. 1983 Oct;399(2):157–159. doi: 10.1007/BF00663914. [DOI] [PubMed] [Google Scholar]
  29. Rich D. P., Gregory R. J., Anderson M. P., Manavalan P., Smith A. E., Welsh M. J. Effect of deleting the R domain on CFTR-generated chloride channels. Science. 1991 Jul 12;253(5016):205–207. doi: 10.1126/science.1712985. [DOI] [PubMed] [Google Scholar]
  30. Saigusa A., Kokubun S. Protein kinase C may regulate resting anion conductance in vascular smooth muscle cells. Biochem Biophys Res Commun. 1988 Sep 15;155(2):882–889. doi: 10.1016/s0006-291x(88)80578-3. [DOI] [PubMed] [Google Scholar]
  31. Schwarze W., Kolb H. A. Voltage-dependent kinetics of an anionic channel of large unit conductance in macrophages and myotube membranes. Pflugers Arch. 1984 Nov;402(3):281–291. doi: 10.1007/BF00585511. [DOI] [PubMed] [Google Scholar]
  32. Soejima M., Kokubun S. Single anion-selective channel and its ion selectivity in the vascular smooth muscle cell. Pflugers Arch. 1988 Mar;411(3):304–311. doi: 10.1007/BF00585119. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Taglietti V., Tanzi F., Romero R., Simoncini L. Maturation involves suppression of voltage-gated currents in the frog oocyte. J Cell Physiol. 1984 Dec;121(3):576–588. doi: 10.1002/jcp.1041210317. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Vaughan P. Substitute anions and the chloride conductance of frog muscle: effects of chlorate and bromate on steady-state values and kinetics. Pflugers Arch. 1991 Sep;419(2):152–159. doi: 10.1007/BF00373001. [DOI] [PubMed] [Google Scholar]
  37. Warner A. E. Kinetic properties of the chloride conductance of frog muscle. J Physiol. 1972 Dec;227(1):291–312. doi: 10.1113/jphysiol.1972.sp010033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Woll K. H., Leibowitz M. D., Neumcke B., Hille B. A high-conductance anion channel in adult amphibian skeletal muscle. Pflugers Arch. 1987 Dec;410(6):632–640. doi: 10.1007/BF00581324. [DOI] [PubMed] [Google Scholar]

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