Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1996 Oct 1;108(4):325–332. doi: 10.1085/jgp.108.4.325

Surface Charges of K channels. Effects of strontium on five cloned channels expressed in Xenopus oocytes

PMCID: PMC2229333  PMID: 8894980

Abstract

The effects of strontium (Sr2+; 7-50 mM) on five different cloned rat K channels (Kv1.1, Kv1.5, Kv1.6, Kv2.1, and Kv3.4), expressed in oocytes of Xenopus laevis, were investigated with a two-electrode voltage clamp technique. The main effect was a shift of the Gk(V) curve along the potential axis, different in size for the different channels. Kv1.1 was shifted most and Kv3.4 least, 21 and 8 mV, respectively, at 50 mM. The effect was interpreted in terms of screening of fixed surface charges. The estimated charge densities ranged from -0.37 (Kv1.1) to -0.11 (Kv3.4) e nm-2 and showed good correlation with the total net charge of the extracellularly located amino acid residues of the channel as well as with the charge of a specific region (the loop between the S5 segment and the pore forming segment). The estimated surface potentials were found to be linearly related to the activation midpoint potential, suggesting a functional role for the surface charges.

Full Text

The Full Text of this article is available as a PDF (716.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arhem P. Effects of some heavy metal ions on the ionic currents of myelinated fibres from Xenopus laevis. J Physiol. 1980 Sep;306:219–231. doi: 10.1113/jphysiol.1980.sp013393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chandler W. K., Hodgkin A. L., Meves H. The effect of changing the internal solution on sodium inactivation and related phenomena in giant axons. J Physiol. 1965 Oct;180(4):821–836. doi: 10.1113/jphysiol.1965.sp007733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cukierman S., Krueger B. K. Modulation of sodium channel gating by external divalent cations: differential effects on opening and closing rates. Pflugers Arch. 1990 Jun;416(4):360–367. doi: 10.1007/BF00370741. [DOI] [PubMed] [Google Scholar]
  4. Cukierman S., Zinkand W. C., French R. J., Krueger B. K. Effects of membrane surface charge and calcium on the gating of rat brain sodium channels in planar bilayers. J Gen Physiol. 1988 Oct;92(4):431–447. doi: 10.1085/jgp.92.4.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dascal N. The use of Xenopus oocytes for the study of ion channels. CRC Crit Rev Biochem. 1987;22(4):317–387. doi: 10.3109/10409238709086960. [DOI] [PubMed] [Google Scholar]
  6. Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
  7. Elinder F., Arhem P. Effects of gadolinium on ion channels in the myelinated axon of Xenopus laevis: four sites of action. Biophys J. 1994 Jul;67(1):71–83. doi: 10.1016/S0006-3495(94)80456-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Elinder F., Arhem P. The modulatory site for the action of gadolinium on surface charges and channel gating. Biophys J. 1994 Jul;67(1):84–90. doi: 10.1016/S0006-3495(94)80457-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Frech G. C., VanDongen A. M., Schuster G., Brown A. M., Joho R. H. A novel potassium channel with delayed rectifier properties isolated from rat brain by expression cloning. Nature. 1989 Aug 24;340(6235):642–645. doi: 10.1038/340642a0. [DOI] [PubMed] [Google Scholar]
  11. Grupe A., Schröter K. H., Ruppersberg J. P., Stocker M., Drewes T., Beckh S., Pongs O. Cloning and expression of a human voltage-gated potassium channel. A novel member of the RCK potassium channel family. EMBO J. 1990 Jun;9(6):1749–1756. doi: 10.1002/j.1460-2075.1990.tb08299.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hille B., Woodhull A. M., Shapiro B. I. Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):301–318. doi: 10.1098/rstb.1975.0011. [DOI] [PubMed] [Google Scholar]
  13. Keynes R. D. The kinetics of voltage-gated ion channels. Q Rev Biophys. 1994 Dec;27(4):339–434. doi: 10.1017/s0033583500003097. [DOI] [PubMed] [Google Scholar]
  14. Li M., Unwin N., Stauffer K. A., Jan Y. N., Jan L. Y. Images of purified Shaker potassium channels. Curr Biol. 1994 Feb 1;4(2):110–115. doi: 10.1016/s0960-9822(94)00026-6. [DOI] [PubMed] [Google Scholar]
  15. Madeja M., Musshoff U., Speckmann E. J. A concentration-clamp system allowing two-electrode voltage-clamp investigations in oocytes of Xenopus laevis. J Neurosci Methods. 1991 Jul;38(2-3):267–269. doi: 10.1016/0165-0270(91)90178-3. [DOI] [PubMed] [Google Scholar]
  16. McLaughlin S. The electrostatic properties of membranes. Annu Rev Biophys Biophys Chem. 1989;18:113–136. doi: 10.1146/annurev.bb.18.060189.000553. [DOI] [PubMed] [Google Scholar]
  17. Papazian D. M., Timpe L. C., Jan Y. N., Jan L. Y. Alteration of voltage-dependence of Shaker potassium channel by mutations in the S4 sequence. Nature. 1991 Jan 24;349(6307):305–310. doi: 10.1038/349305a0. [DOI] [PubMed] [Google Scholar]
  18. Peitzsch R. M., Eisenberg M., Sharp K. A., McLaughlin S. Calculations of the electrostatic potential adjacent to model phospholipid bilayers. Biophys J. 1995 Mar;68(3):729–738. doi: 10.1016/S0006-3495(95)80253-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Recio-Pinto E., Thornhill W. B., Duch D. S., Levinson S. R., Urban B. W. Neuraminidase treatment modifies the function of electroplax sodium channels in planar lipid bilayers. Neuron. 1990 Nov;5(5):675–684. doi: 10.1016/0896-6273(90)90221-z. [DOI] [PubMed] [Google Scholar]
  20. Rettig J., Wunder F., Stocker M., Lichtinghagen R., Mastiaux F., Beckh S., Kues W., Pedarzani P., Schröter K. H., Ruppersberg J. P. Characterization of a Shaw-related potassium channel family in rat brain. EMBO J. 1992 Jul;11(7):2473–2486. doi: 10.1002/j.1460-2075.1992.tb05312.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Santacruz-Toloza L., Huang Y., John S. A., Papazian D. M. Glycosylation of shaker potassium channel protein in insect cell culture and in Xenopus oocytes. Biochemistry. 1994 May 10;33(18):5607–5613. doi: 10.1021/bi00184a033. [DOI] [PubMed] [Google Scholar]
  22. Stühmer W., Ruppersberg J. P., Schröter K. H., Sakmann B., Stocker M., Giese K. P., Perschke A., Baumann A., Pongs O. Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO J. 1989 Nov;8(11):3235–3244. doi: 10.1002/j.1460-2075.1989.tb08483.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stühmer W., Stocker M., Sakmann B., Seeburg P., Baumann A., Grupe A., Pongs O. Potassium channels expressed from rat brain cDNA have delayed rectifier properties. FEBS Lett. 1988 Dec 19;242(1):199–206. doi: 10.1016/0014-5793(88)81015-9. [DOI] [PubMed] [Google Scholar]
  24. Swanson R., Marshall J., Smith J. S., Williams J. B., Boyle M. B., Folander K., Luneau C. J., Antanavage J., Oliva C., Buhrow S. A. Cloning and expression of cDNA and genomic clones encoding three delayed rectifier potassium channels in rat brain. Neuron. 1990 Jun;4(6):929–939. doi: 10.1016/0896-6273(90)90146-7. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES