Abstract
Sodium (Na) channel gating currents were measured in squid (Loligo forbesi) axons to study transitions among states occupied by the Na channel when it is inactivated. These measurements were made at high temporal resolution with a low-noise voltage clamp. The inactivation-resistant gating current, I(g,inact), could be separated into a very fast (tau = 5-25 mus) and a slower (tau = 40-200 mus) component over a wide range of test potentials (-140 mV to 80 mV) and for three different starting potentials (-70 mV, 0 mV, and 50 mV). The time constants for these components plotted against test potential lay on two bell-shaped curves; the time constants at any particular test potential did not depend on the starting potential. Both components had charge-voltage curves that saturated between -150 mV and 50 mV. A fast spike, similar to the fast component of I(g, inact), was also apparent in recordings of the fully recovered total "on" gating current. I(g, inact)(fast) and I(g, inact)(slow) could not together be described by the simplest possible model, a linear three-state scheme; however, I(g, inact)(fast) could be modeled by a two-state scheme operating in parallel with other gating processes. I(g, inact)(slow) and the gating current due to recovery from inactivated states into resting states could together be well described by a three-state scheme. This lends support to models in which a pair of inactivated states are connected by a single voltage-dependent step to the resting states of the Na system.
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alicata D. A., Rayner M. D., Starkus J. G. Osmotic and pharmacological effects of formamide on capacity current, gating current, and sodium current in crayfish giant axons. Biophys J. 1989 Feb;55(2):347–353. doi: 10.1016/S0006-3495(89)82811-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M., Bezanilla F. Inactivation of the sodium channel. II. Gating current experiments. J Gen Physiol. 1977 Nov;70(5):567–590. doi: 10.1085/jgp.70.5.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M., Croop R. S. Simulation of Na channel inactivation by thiazine dyes. J Gen Physiol. 1982 Nov;80(5):641–662. doi: 10.1085/jgp.80.5.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M., Gilly W. F. Fast and slow steps in the activation of sodium channels. J Gen Physiol. 1979 Dec;74(6):691–711. doi: 10.1085/jgp.74.6.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong C. M. Sodium channels and gating currents. Physiol Rev. 1981 Jul;61(3):644–683. doi: 10.1152/physrev.1981.61.3.644. [DOI] [PubMed] [Google Scholar]
- Bekkers J. M., Greeff N. G., Keynes R. D., Neumcke B. The effect of local anaesthetics on the components of the asymmetry current in the squid giant axon. J Physiol. 1984 Jul;352:653–668. doi: 10.1113/jphysiol.1984.sp015315. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Bezanilla F. Gating of sodium and potassium channels. J Membr Biol. 1985;88(2):97–111. doi: 10.1007/BF01868424. [DOI] [PubMed] [Google Scholar]
- Boron W. F., Hogan E., Russell J. M. pH-sensitive activation of the intracellular-pH regulation system in squid axons by ATP-gamma-S. Nature. 1988 Mar 17;332(6161):262–265. doi: 10.1038/332262a0. [DOI] [PubMed] [Google Scholar]
- Chandler W. K., Meves H. Evidence for two types of sodium conductance in axons perfused with sodium fluoride solution. J Physiol. 1970 Dec;211(3):653–678. doi: 10.1113/jphysiol.1970.sp009298. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Colquhoun D., Hawkes A. G. Relaxation and fluctuations of membrane currents that flow through drug-operated channels. Proc R Soc Lond B Biol Sci. 1977 Nov 14;199(1135):231–262. doi: 10.1098/rspb.1977.0137. [DOI] [PubMed] [Google Scholar]
- Forster I. C., Greeff N. G. High resolution recording of asymmetry currents from the squid giant axon: technical aspects of voltage clamp design. J Neurosci Methods. 1990 Aug;33(2-3):185–205. doi: 10.1016/0165-0270(90)90023-9. [DOI] [PubMed] [Google Scholar]
- Gilly W. F., Armstrong C. M. Gating current and potassium channels in the giant axon of the squid. Biophys J. 1980 Mar;29(3):485–492. doi: 10.1016/S0006-3495(80)85147-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Greeff N. G., Keynes R. D., Van Helden D. F. Fractionation of the asymmetry current in the squid giant axon into inactivating and non-inactivating components. Proc R Soc Lond B Biol Sci. 1982 Jun 22;215(1200):375–389. doi: 10.1098/rspb.1982.0048. [DOI] [PubMed] [Google Scholar]
- Keynes R. D. A series-parallel model of the voltage-gated sodium channel. Proc R Soc Lond B Biol Sci. 1990 Jun 22;240(1299):425–432. doi: 10.1098/rspb.1990.0046. [DOI] [PubMed] [Google Scholar]
- Matteson D. R., Armstrong C. M. Evidence for a population of sleepy sodium channels in squid axon at low temperature. J Gen Physiol. 1982 May;79(5):739–758. doi: 10.1085/jgp.79.5.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stimers J. R., Bezanilla F., Taylor R. E. Sodium channel activation in the squid giant axon. Steady state properties. J Gen Physiol. 1985 Jan;85(1):65–82. doi: 10.1085/jgp.85.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stimers J. R., Bezanilla F., Taylor R. E. Sodium channel gating currents. Origin of the rising phase. J Gen Physiol. 1987 Apr;89(4):521–540. doi: 10.1085/jgp.89.4.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
- White M. M., Bezanilla F. Activation of squid axon K+ channels. Ionic and gating current studies. J Gen Physiol. 1985 Apr;85(4):539–554. doi: 10.1085/jgp.85.4.539. [DOI] [PMC free article] [PubMed] [Google Scholar]