Voltage-dependent gating of Shaker A-type potassium channels in Drosophila muscle
- PMID: 2299331
- PMCID: PMC2216290
- DOI: 10.1085/jgp.95.1.29
Voltage-dependent gating of Shaker A-type potassium channels in Drosophila muscle
Abstract
The voltage-dependent gating mechanism of A1-type potassium channels coded for by the Shaker locus of Drosophila was studied using macroscopic and single-channel recording techniques on embryonic myotubes in primary culture. From a kinetic analysis of data from single A1 channels, we have concluded that all of the molecular transitions after first opening, including the inactivation transition, are voltage independent and therefore not associated with charge movement through the membrane. In contrast, at least some of the activation transitions leading to first opening are considerably voltage dependent and account for all of the voltage dependence seen in the macroscopic currents. This mechanism is similar in many ways to that of vertebrate neuronal voltage-sensitive sodium channels, and together with the sequence similarities in the S4 region suggests a conserved mechanism for voltage-dependent gating among channels with different selectivities. By testing independent and coupled models for activation and inactivation we have determined that the final opening transition and inactivation are not likely to arise from the independent action of multiple subunits, each with simple gating transitions, but rather come about through their aggregate properties. A partially coupled model accurately reproduces all of the single-channel and macroscopic data. This model will provide a framework on which to organize and understand alterations in gating that occur in Shaker variants and mutants.
Similar articles
-
Gating of single Shaker potassium channels in Drosophila muscle and in Xenopus oocytes injected with Shaker mRNA.Proc Natl Acad Sci U S A. 1989 Sep;86(18):7243-7. doi: 10.1073/pnas.86.18.7243. Proc Natl Acad Sci U S A. 1989. PMID: 2506548 Free PMC article.
-
Mutations in the S4 region isolate the final voltage-dependent cooperative step in potassium channel activation.J Gen Physiol. 1999 Mar;113(3):389-414. doi: 10.1085/jgp.113.3.389. J Gen Physiol. 1999. PMID: 10051516 Free PMC article.
-
Gating of single non-Shaker A-type potassium channels in larval Drosophila neurons.J Gen Physiol. 1990 Jul;96(1):135-65. doi: 10.1085/jgp.96.1.135. J Gen Physiol. 1990. PMID: 2212978 Free PMC article.
-
Voltage-dependent potassium channels: minK and Shaker families.New Biol. 1991 Apr;3(4):315-23. New Biol. 1991. PMID: 2065015 Review.
-
An essential 'set' of K+ channels conserved in flies, mice and humans.Trends Neurosci. 1992 May;15(5):161-6. doi: 10.1016/0166-2236(92)90165-5. Trends Neurosci. 1992. PMID: 1377421 Review.
Cited by
-
Voltage gating by molecular subunits of Na+ and K+ ion channels: higher-dimensional cubic kinetics, rate constants, and temperature.J Neurophysiol. 2015 Jun 1;113(10):3759-77. doi: 10.1152/jn.00551.2014. Epub 2015 Apr 1. J Neurophysiol. 2015. PMID: 25867741 Free PMC article.
-
Tetraethylammonium blockade distinguishes two inactivation mechanisms in voltage-activated K+ channels.Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5092-5. doi: 10.1073/pnas.88.12.5092. Proc Natl Acad Sci U S A. 1991. PMID: 2052588 Free PMC article.
-
Dampening of hyperexcitability in CA1 pyramidal neurons by polyunsaturated fatty acids acting on voltage-gated ion channels.PLoS One. 2012;7(9):e44388. doi: 10.1371/journal.pone.0044388. Epub 2012 Sep 25. PLoS One. 2012. PMID: 23049748 Free PMC article.
-
Modification of potassium channel kinetics by amino group reagents.J Gen Physiol. 1992 Jan;99(1):109-29. doi: 10.1085/jgp.99.1.109. J Gen Physiol. 1992. PMID: 1740669 Free PMC article.
-
Elimination of rapid potassium channel inactivation by phosphorylation of the inactivation gate.Neuron. 1994 Dec;13(6):1403-12. doi: 10.1016/0896-6273(94)90425-1. Neuron. 1994. PMID: 7993631 Free PMC article.
References
Publication types
MeSH terms
Substances
Grants and funding
LinkOut - more resources
Full Text Sources
Molecular Biology Databases