Abstract
An N-terminus peptide or a C-terminus mechanism involving a single residue in transmembrane segment 6 produces inactivation in voltage-dependent K+ channels. Here we show that a single position in the pore of K+ channels can produce inactivation having characteristics distinct from either N- or C-type inactivation. In a chimeric K+ channel (CHM), the point reversion CHM V369K produced fast inactivation and CHM V369S had the additional effect of halving K+ conductance consistent with a position in the pore. The result was not restricted to CHM; mutating position 369 in the naturally occurring channel Kv2.1 also produced fast inactivation. Like N- and C-types of inactivation, pore or P-type inactivation was characterized by short bursts terminated by rapid entry into the inactivated state. Unlike C-type inactivation, in which external tetraethylammonium (TEA) produced a simple blockade that slowed inactivation and reduced currents, in P-type inactivation external TEA increased currents. Unlike N-type inactivation, internal TEA produced a simple reduction in current and K+ occupancy of the pore had no effect. External TEA was not the only cation to increase current; external K+ enhanced channel availability and recovery from inactivation. Additional features of P-type inactivation were residue-specific effects on the extent of inactivation and removal of inactivation by a point reversion at position 374, which also regulates conductance. The demonstration of P-type inactivation indicates that pore residues in K+ channels may be part of the inactivation gating machinery.
MeSH Terms
Chimera/genetics,physiology
DNA, Recombinant
Humans
Ion Channel Gating/physiology
Membrane Potentials/physiology
Mutagenesis, Site-Directed
Oocytes/physiology
Potassium Channels/genetics,physiology
Chemicals
DNA, Recombinant
Potassium Channels
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
De Biasi M
Department of Molecular Physiology and Biophysics, Baylor College of Medicine, Houston, TX 77030.
Hartmann H A
Drewe J A
Taglialatela M
Brown A M
Kirsch G E
References (27)
27 references, click to expand
-
TEA prevents inactivation while blocking open K+ channels in human T lymphocytes.
Biophys J. 1989 Jan;55(1):203-6
PMID: 2784693
-
Restoration of inactivation in mutants of Shaker potassium channels by a peptide derived from ShB.
Science. 1990 Oct 26;250(4980):568-71
PMID: 2122520
-
Putative receptor for the cytoplasmic inactivation gate in the Shaker K+ channel.
Nature. 1991 Sep 5;353(6339):86-90
PMID: 1881453
-
Extracellular K+ specifically modulates a rat brain K+ channel.
Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2466-70
PMID: 1549610
-
The inactivation gate of the Shaker K+ channel behaves like an open-channel blocker.
Neuron. 1991 Nov;7(5):743-53
PMID: 1742023
-
Voltage-dependent gating of Shaker A-type potassium channels in Drosophila muscle.
J Gen Physiol. 1990 Jan;95(1):29-60
PMID: 2299331
-
Patterns of internal and external tetraethylammonium block in four homologous K+ channels.
Mol Pharmacol. 1991 Aug;40(2):299-307
PMID: 1875913
-
Exchange of conduction pathways between two related K+ channels.
Science. 1991 Feb 22;251(4996):942-4
PMID: 2000495
-
Two types of inactivation in Shaker K+ channels: effects of alterations in the carboxy-terminal region.
Neuron. 1991 Oct;7(4):547-56
PMID: 1931050
-
A novel potassium channel with delayed rectifier properties isolated from rat brain by expression cloning.
Nature. 1989 Aug 24;340(6235):642-5
PMID: 2770868
-
Biophysical and molecular mechanisms of Shaker potassium channel inactivation.
Science. 1990 Oct 26;250(4980):533-8
PMID: 2122519
-
A single nonpolar residue in the deep pore of related K+ channels acts as a K+:Rb+ conductance switch.
Biophys J. 1992 Apr;62(1):136-43; discussion 143-4
PMID: 1600093
-
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
PMID: 2506548
-
Four cDNA clones from the Shaker locus of Drosophila induce kinetically distinct A-type potassium currents in Xenopus oocytes.
Neuron. 1988 Oct;1(8):659-67
PMID: 3272184
-
Current inactivation involves a histidine residue in the pore of the rat lymphocyte potassium channel RGK5.
Biochem Biophys Res Commun. 1991 Sep 30;179(3):1384-90
PMID: 1930184
-
Alteration and restoration of K+ channel function by deletions at the N- and C-termini.
Neuron. 1990 Oct;5(4):433-43
PMID: 2206531
-
Expression of functional potassium channels from Shaker cDNA in Xenopus oocytes.
Nature. 1988 Jan 14;331(6152):143-5
PMID: 2448636
-
Single-channel analysis of four distinct classes of potassium channels in Drosophila muscle.
J Neurosci. 1988 Dec;8(12):4765-79
PMID: 3199204
-
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
PMID: 2052588
-
Interaction of tetraethylammonium ion derivatives with the potassium channels of giant axons.
J Gen Physiol. 1971 Oct;58(4):413-37
PMID: 5112659
-
Gating of single non-Shaker A-type potassium channels in larval Drosophila neurons.
J Gen Physiol. 1990 Jul;96(1):135-65
PMID: 2212978
-
Gating of Na channels. Inactivation modifiers discriminate among models.
J Gen Physiol. 1987 Feb;89(2):253-74
PMID: 2435840
-
Differences between the deep pores of K+ channels determined by an interacting pair of nonpolar amino acids.
Neuron. 1992 Mar;8(3):499-505
PMID: 1550675
-
Alternative Shaker transcripts express either rapidly inactivating or noninactivating K+ channels.
Proc Natl Acad Sci U S A. 1990 Nov;87(22):8903-7
PMID: 1701056
-
Inactivation of the sodium channel. I. Sodium current experiments.
J Gen Physiol. 1977 Nov;70(5):549-66
PMID: 591911
-
Gating mechanism of a cloned potassium channel expressed in frog oocytes and mammalian cells.
Neuron. 1990 Jan;4(1):39-51
PMID: 2310574
-
The role of the divergent amino and carboxyl domains on the inactivation properties of potassium channels derived from the Shaker gene of Drosophila.
J Neurosci. 1990 Sep;10(9):2903-16
PMID: 1697898