Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1987 Feb 1;89(2):239–251. doi: 10.1085/jgp.89.2.239

Temperature dependence of Na currents in rabbit and frog muscle membranes

PMCID: PMC2215894  PMID: 2435839

Abstract

The effect of temperature (0-22 degrees C) on the kinetics of Na channel conductance was determined in voltage-clamped rabbit and frog skeletal muscle fibers using the triple-Vaseline-gap technique. The Hodgkin-Huxley model was used to extract kinetic parameters; the time course of the conductance change during step depolarization followed m3h kinetics. Arrhenius plots of activation time constants (tau m), determined at both moderate (-10 to -20 mV) and high (+100 mV) depolarizations, were linear in both types of muscle. In rabbit muscle, Arrhenius plots of the inactivation time constant (tau h) were markedly nonlinear at +100 mV, but much less so at -20 mV. The reverse situation was found in frog muscle. The contrast between the highly nonlinear Arrhenius plot of tau h at +100 mV in rabbit muscle, compared with that of frog muscle, was interpreted as revealing an intrinsic nonlinearity in the temperature dependence of mammalian muscle Na inactivation. These results are consistent with the notion that mammalian cell membranes undergo thermotropic membrane phase transitions that alter lipid-channel interactions in the 0-22 degrees C range. Furthermore, the observation that Na channel activation appears to be resistant to this effect suggests that the gating mechanisms that govern activation and inactivation reside in physically distinct regions of the channel.

Full Text

The Full Text of this article is available as a PDF (723.7 KB).

Selected References

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

  1. Aldrich R. W., Corey D. P., Stevens C. F. A reinterpretation of mammalian sodium channel gating based on single channel recording. Nature. 1983 Dec 1;306(5942):436–441. doi: 10.1038/306436a0. [DOI] [PubMed] [Google Scholar]
  2. Aldrich R. W., Stevens C. F. Inactivation of open and closed sodium channels determined separately. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 1):147–153. doi: 10.1101/sqb.1983.048.01.017. [DOI] [PubMed] [Google Scholar]
  3. Anderson C. R., Cull-Candy S. G., Miledi R. Potential-dependent transition temperature of ionic channels induced by glutamate in locust muscle. Nature. 1977 Aug 18;268(5621):663–665. doi: 10.1038/268663a0. [DOI] [PubMed] [Google Scholar]
  4. Beam K. G., Donaldson P. L. A quantitative study of potassium channel kinetics in rat skeletal muscle from 1 to 37 degrees C. J Gen Physiol. 1983 Apr;81(4):485–512. doi: 10.1085/jgp.81.4.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bezanilla F., Armstrong C. M. Inactivation of the sodium channel. I. Sodium current experiments. J Gen Physiol. 1977 Nov;70(5):549–566. doi: 10.1085/jgp.70.5.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Campbell D. T. Sodium channel gating currents in frog skeletal muscle. J Gen Physiol. 1983 Nov;82(5):679–701. doi: 10.1085/jgp.82.5.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chiu S. Y., Mrose H. E., Ritchie J. M. Anomalous temperature dependence of the sodium conductance in rabbit nerve compared with frog nerve. Nature. 1979 May 24;279(5711):327–328. doi: 10.1038/279327a0. [DOI] [PubMed] [Google Scholar]
  8. Duggleby R. G. Regression analysis of nonlinear Arrhenius plots: an empirical model and a computer program. Comput Biol Med. 1984;14(4):447–455. doi: 10.1016/0010-4825(84)90045-3. [DOI] [PubMed] [Google Scholar]
  9. FRANKENHAEUSER B., MOORE L. E. THE EFFECT OF TEMPERATURE ON THE SODIUM AND POTASSIUM PERMEABILITY CHANGES IN MYELINATED NERVE FIBRES OF XENOPUS LAEVIS. J Physiol. 1963 Nov;169:431–437. doi: 10.1113/jphysiol.1963.sp007269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. French R. J., Horn R. Sodium channel gating: models, mimics, and modifiers. Annu Rev Biophys Bioeng. 1983;12:319–356. doi: 10.1146/annurev.bb.12.060183.001535. [DOI] [PubMed] [Google Scholar]
  11. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hille B., Campbell D. T. An improved vaseline gap voltage clamp for skeletal muscle fibers. J Gen Physiol. 1976 Mar;67(3):265–293. doi: 10.1085/jgp.67.3.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kirsch G. E., Anderson M. F. Sodium channel kinetics in normal and denervated rabbit muscle membrane. Muscle Nerve. 1986 Oct;9(8):738–747. doi: 10.1002/mus.880090810. [DOI] [PubMed] [Google Scholar]
  14. Kniffki K. D., Siemen D., Vogel W. Development of sodium permeability inactivation in nodal membranes. J Physiol. 1981;313:37–48. doi: 10.1113/jphysiol.1981.sp013649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kumamoto J., Raison J. K., Lyons J. M. Temperature "breaks" in Arrhenius plots: a thermodynamic consequence of a phase change. J Theor Biol. 1971 Apr;31(1):47–51. doi: 10.1016/0022-5193(71)90120-2. [DOI] [PubMed] [Google Scholar]
  16. Pappone P. A. Voltage-clamp experiments in normal and denervated mammalian skeletal muscle fibres. J Physiol. 1980 Sep;306:377–410. doi: 10.1113/jphysiol.1980.sp013403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Romey G., Chicheportiche R., Lazdunski M. Transition temperatures of the electrical activity of ion channels in the nerve membrane. Biochim Biophys Acta. 1980 Nov 18;602(3):610–620. doi: 10.1016/0005-2736(80)90339-9. [DOI] [PubMed] [Google Scholar]
  18. Sandermann H., Jr Regulation of membrane enzymes by lipids. Biochim Biophys Acta. 1978 Sep 29;515(3):209–237. doi: 10.1016/0304-4157(78)90015-1. [DOI] [PubMed] [Google Scholar]
  19. Schwarz J. R. The effect of temperature on Na currents in rat myelinated nerve fibres. Pflugers Arch. 1986 Apr;406(4):397–404. doi: 10.1007/BF00590943. [DOI] [PubMed] [Google Scholar]
  20. Schwarz W. Temperature experiments on nerve and muscle membranes of frogs. Indications for a phase transition. Pflugers Arch. 1979 Oct;382(1):27–34. doi: 10.1007/BF00585900. [DOI] [PubMed] [Google Scholar]
  21. Vijverberg H. P., van der Zalm J. M., van Kleef R. G., van den Bercken J. Temperature- and structure-dependent interaction of pyrethroids with the sodium channels in frog node of Ranvier. Biochim Biophys Acta. 1983 Feb 9;728(1):73–82. doi: 10.1016/0005-2736(83)90438-8. [DOI] [PubMed] [Google Scholar]

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

RESOURCES