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PMID: 6304231 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A quantitative study of potassium channel kinetics in rat skeletal muscle from 1 to 37 degrees C.

The Journal of general physiology ·Vol. 81 ·No. 4 ·1983-04-00 ·Pages 485-512

Beam KG, Donaldson PL

Abstract

Potassium currents were measured using the three-microelectrode voltage-clamp technique in rat omohyoid muscle at temperatures from 1 to 37 degrees C. The currents were fitted according to the Hodgkin-Huxley equations as modified for K currents in frog skeletal muscle (Adrian et al., 1970a). The equations provided an approximate description of the time course of activation, the voltage dependence of the time constant of activation (tau n), and the voltage dependence of gK infinity. At higher temperatures the relationship between gK infinity and voltage was shifted in the hyperpolarizing direction. The effect of temperature on tau n was much greater in the cold than in the warm: tau n had a Q10 of nearly 6 at temperatures below 10 degrees C, but a Q10 of only approximately 2 over the range of 30-38 degrees C. The decreasing dependence of tau n on temperature was gradual and the Arrhenius plot of tau n revealed no obvious break-points. In addition to its quantitative effect on activation kinetics, temperature also had a qualitative effect. Near physiological temperatures (above approximately 25 degrees C), the current was well described by n4 kinetics. At intermediate temperatures (approximately 15-25 degrees C), the current was well described by n4 kinetics, but only if the n4 curve was translated rightward along the time axis (i.e., the current had a greater delay than could be accounted for by simple n4 kinetics). At low temperatures (below approximately 15 degrees C), n4 kinetics provided only an approximate fit whether or not the theoretical curve was translated along the time axis. In particular, currents in the cold displayed an initial rapid phase of activation followed by a much slower one. Thus, low temperatures appear to reveal steps in the gating process which are kinetically "hidden" at higher temperatures. Taken together, the effects of temperature on potassium currents in rat skeletal muscle demonstrate that the behavior of potassium channels at physiological temperatures cannot be extrapolated, either quantitatively or qualitatively, from experiments carried out in the cold.

MeSH Terms
Animals Ion Channels/metabolism Kinetics Male Mathematics Muscles/metabolism Potassium/metabolism Rats Rats, Inbred Strains Temperature
Chemicals
Ion Channels Potassium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Beam K G
Donaldson P L
References (38)
38 references, click to expand
  1. The effect o f calcium on contraction and conductance thresholds in frog skeletal muscle.
    J Physiol. 1968 Mar;195(1):119-32 PMID: 5639795
  2. The effect of the tetraethylammonium ion on the delayed currents of frog skeletal muscle.
    J Physiol. 1970 Jul;209(1):209-29 PMID: 5499043
  3. Voltage clamp experiments in striated muscle fibres.
    J Physiol. 1970 Jul;208(3):607-44 PMID: 5499787
  4. Slow changes in potassium permeability in skeletal muscle.
    J Physiol. 1970 Jul;208(3):645-68 PMID: 5499788
  5. The effect of diameter on the electrical constants of frog skeletal muscle fibres.
    J Physiol. 1972 Feb;221(1):105-20 PMID: 4536963
  6. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling.
    Nature. 1973 Mar 23;242(5395):244-6 PMID: 4540479
  7. Ionic blockage of sodium channels in nerve.
    J Gen Physiol. 1973 Jun;61(6):687-708 PMID: 4541078
  8. How many conductance states do potassium channels have?
    Biophys J. 1975 Aug;15(8):843-6 PMID: 1148365
  9. Effect of conditioning potential on potassium current kinetics in the frog node.
    Biophys J. 1976 Mar;16(3):261-73 PMID: 1082776
  10. Effects of membrane potential on the capacitance of skeletal muscle fibers.
    J Gen Physiol. 1976 Feb;67(2):125-63 PMID: 1082924
  11. Effects of denervation and colchicine treatment on the chloride conductance of rat skeletal muscle fibers.
    J Neurobiol. 1976 May;7(3):221-8 PMID: 1271053
  12. Action potentials reconstructed in normal and myotonic muscle fibres.
    J Physiol. 1976 Jun;258(1):125-43 PMID: 940049
  13. A discontinuous relationship between the acetylcholine-activated channel conductance and temperature.
    Nature. 1976 Sep 9;263(5573):150-1 PMID: 967250
  14. Potassium current kinetics in Myxicola axons. Effects of conditioning prepulses.
    J Gen Physiol. 1976 Oct;68(4):397-403 PMID: 993766
  15. The M. omohyoideus of the mouse as a convenient mammalian muscle preparation. A study of junctional and extrajunctional acetylcholine receptors by noise analysis and cooperativity.
    Pflugers Arch. 1976 Dec 28;367(2):115-22 PMID: 1034907
  16. Characteristics of the chloride conductance in muscle fibers of the rat diaphragm.
    J Gen Physiol. 1977 Mar;69(3):325-42 PMID: 15046
  17. Sodium currents in mammalian muscle.
    J Physiol. 1977 Jun;268(1):223-50 PMID: 874895
  18. Ionic currents in mammalian fast skeletal muscle.
    J Physiol. 1978 May;278:403-23 PMID: 671323
  19. Anomalous temperature dependence of the sodium conductance in rabbit nerve compared with frog nerve.
    Nature. 1979 May 24;279(5711):327-8 PMID: 313012
  20. Inactivation of delayed outward current in molluscan neurone somata.
    J Physiol. 1979 Jun;291:507-30 PMID: 480244
  21. Potential clamp analysis of membrane currents in rat myelinated nerve fibres.
    J Physiol. 1980 Jan;298:171-84 PMID: 7359387
  22. The ansa cervicalis and the infrahyoid muscles of the rat. I. Anatomy; distribution, number and diameter of fiber types; motor units.
    Anat Embryol (Berl). 1980;159(1):49-57 PMID: 6445169
  23. Electrical models of excitation-contraction coupling and charge movement in skeletal muscle.
    J Gen Physiol. 1980 Jul;76(1):1-31 PMID: 7411109
  24. Some kinetic and steady-state properties of sodium channels after removal of inactivation.
    J Gen Physiol. 1981 Jan;77(1):1-22 PMID: 6162910
  25. Ionic currents in slow twitch skeletal muscle in the rat.
    J Physiol. 1980 Oct;307:23-41 PMID: 7205665
  26. Comparison between the delayed outward current in slow and fast twitch skeletal muscle in the rat.
    J Physiol. 1980 Oct;307:43-57 PMID: 7205672
  27. Modification of sodium and potassium channel gating kinetics by ether and halothane.
    J Gen Physiol. 1981 Mar;77(3):233-53 PMID: 6265590
  28. Conditioning hyperpolarization-induced delays in the potassium channels of myelinated nerve.
    Biophys J. 1979 Aug;27(2):257-65 PMID: 233581
  29. Some effects of n-pentane on the sodium and potassium currents of the squid giant axon.
    J Physiol. 1981 Mar;312:57-70 PMID: 6267268
  30. Evidence for the existence of three types of potassium channels in the frog Ranvier node membrane.
    J Physiol. 1981 Sep;318:297-316 PMID: 6275068
  31. Inactivation of voltage-gated delayed potassium current in molluscan neurons. A kinetic model.
    Biophys J. 1981 Dec;36(3):519-32 PMID: 6275919
  32. Dynamics of potassium ion currents in squid axon membrane. A re-examination.
    Biophys J. 1981 Dec;36(3):715-22 PMID: 6275921
  33. Potassium ion currents in the crayfish giant axon. Dynamic characteristics.
    Biophys J. 1981 Dec;36(3):723-33 PMID: 6275922
  34. Delayed kinetics of squid axon potassium channels do not always superpose after time translation.
    Biophys J. 1982 Mar;37(3):677-80 PMID: 6280785
  35. Properties of sodium and potassium channels of the squid giant axon far below 0 degrees C.
    J Membr Biol. 1982;68(2):151-60 PMID: 6286975
  36. Slow components of potassium tail currents in rat skeletal muscle.
    J Gen Physiol. 1983 Apr;81(4):513-30 PMID: 6304232
  37. A quantitative description of membrane current and its application to conduction and excitation in nerve.
    J Physiol. 1952 Aug;117(4):500-44 PMID: 12991237
  38. Potassium ion current in the squid giant axon: dynamic characteristic.
    Biophys J. 1960 Sep;1:1-14 PMID: 13694549
Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
Published
1983-04-00
Pages
485-512
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2215581
Subset
IM
Grants
NINDS NIH HHS · NS 14901 · United States
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