The activation gate controls steady-state inactivation and recovery from inactivation in Shaker.
Journal
The Journal of general physiology
ISSN: 1540-7748
Titre abrégé: J Gen Physiol
Pays: United States
ID NLM: 2985110R
Informations de publication
Date de publication:
03 08 2020
03 08 2020
Historique:
received:
14
02
2020
accepted:
18
04
2020
entrez:
23
5
2020
pubmed:
23
5
2020
medline:
3
9
2021
Statut:
ppublish
Résumé
Despite major advances in the structure determination of ion channels, the sequence of molecular rearrangements at negative membrane potentials in voltage-gated potassium channels of the Shaker family remains unknown. Four major composite gating states are documented during the gating process: closed (C), open (O), open-inactivated (OI), and closed-inactivated (CI). Although many steps in the gating cycle have been clarified experimentally, the development of steady-state inactivation at negative membrane potentials and mandatory gating transitions for recovery from inactivation have not been elucidated. In this study, we exploit the biophysical properties of Shaker-IR mutants T449A/V474C and T449A/V476C to evaluate the status of the activation and inactivation gates during steady-state inactivation and upon locking the channel open with intracellular Cd2+. We conclude that at negative membrane potentials, the gating scheme of Shaker channels can be refined in two aspects. First, the most likely pathway for the development of steady-state inactivation is C→O→OI⇌CI. Second, the OI→CI transition is a prerequisite for recovery from inactivation. These findings are in accordance with the widely accepted view that tight coupling is present between the activation and C-type inactivation gates in Shaker and underscore the role of steady-state inactivation and recovery from inactivation as determinants of excitability.
Identifiants
pubmed: 32442242
pii: 151805
doi: 10.1085/jgp.202012591
pmc: PMC7398138
pii:
doi:
Substances chimiques
Shaker Superfamily of Potassium Channels
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM052302
Pays : United States
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2020 Szanto et al.
Références
Proc Natl Acad Sci U S A. 2018 May 22;115(21):5426-5431
pubmed: 29735651
Biophys J. 1996 Dec;71(6):3157-66
pubmed: 8968586
Sci Rep. 2016 Nov 16;6:37029
pubmed: 27848984
Elife. 2017 Nov 22;6:
pubmed: 29165243
Physiol Rev. 2000 Apr;80(2):555-92
pubmed: 10747201
Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2466-70
pubmed: 1549610
J Membr Biol. 1997 Jun 1;157(3):215-30
pubmed: 9178609
Receptors Channels. 1993;1(1):61-71
pubmed: 8081712
Am J Physiol. 1997 May;272(5 Pt 2):H2164-72
pubmed: 9176282
Biophys J. 1996 Feb;70(2):798-805
pubmed: 8789096
Neuron. 1997 Jul;19(1):175-84
pubmed: 9247273
Elife. 2013 Dec 10;2:e01289
pubmed: 24327560
Elife. 2018 Aug 15;7:
pubmed: 30109985
Channels (Austin). 2008 Mar-Apr;2(2):139-42
pubmed: 18849651
J Gen Physiol. 2013 Feb;141(2):151-60
pubmed: 23319730
J Gen Physiol. 2007 May;129(5):403-18
pubmed: 17438120
J Gen Physiol. 1998 Mar;111(3):421-39
pubmed: 9482709
J Gen Physiol. 2002 Jul;120(1):87-97
pubmed: 12084778
J Gen Physiol. 1995 Dec;106(6):1069-87
pubmed: 8786351
Prog Biophys Mol Biol. 2006 Oct;92(2):185-208
pubmed: 16316679
Neuron. 1994 Apr;12(4):819-29
pubmed: 8161454
Science. 2005 Aug 5;309(5736):903-8
pubmed: 16002579
J Gen Physiol. 2004 Jul;124(1):83-102
pubmed: 15226366
Neuron. 1998 Sep;21(3):617-21
pubmed: 9768847
J Gen Physiol. 2010 Feb;135(2):135-47
pubmed: 20100893
Nature. 2010 Jul 8;466(7303):203-8
pubmed: 20613835
J Membr Biol. 2014 Apr;247(4):319-30
pubmed: 24487574
J Gen Physiol. 1999 Feb;113(2):347-58
pubmed: 9925829
J Physiol. 2011 Feb 1;589(Pt 3):461-79
pubmed: 21098008
Nature. 1996 Feb 29;379(6568):833-6
pubmed: 8587608
J Physiol. 2012 Jun 1;590(11):2591-9
pubmed: 22431339
Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):19813-8
pubmed: 18077413
Q Rev Biophys. 1998 Aug;31(3):239-95
pubmed: 10384687
Immunol Lett. 2004 Mar 29;92(1-2):55-66
pubmed: 15081528
Nature. 2013 Sep 5;501(7465):121-4
pubmed: 23892782
Am J Physiol Cell Physiol. 2018 Jan 1;314(1):C27-C42
pubmed: 28931540
J Gen Physiol. 2010 Aug;136(2):203-24
pubmed: 20660661
Nat Rev Neurosci. 2007 Jun;8(6):451-65
pubmed: 17514198
Nature. 2010 Jul 8;466(7303):272-5
pubmed: 20613845
Science. 1990 Oct 26;250(4980):533-8
pubmed: 2122519
Nature. 1984 Feb 2-8;307(5950):468-71
pubmed: 6320008
Biophys J. 2001 Aug;81(2):814-26
pubmed: 11463627
Neuron. 2001 Nov 20;32(4):649-56
pubmed: 11719205
J Gen Physiol. 2007 May;129(5):437-55
pubmed: 17470663
Nat Struct Mol Biol. 2017 Oct;24(10):857-865
pubmed: 28846092
Circ Res. 1998 Apr 20;82(7):739-50
pubmed: 9562433
J Gen Physiol. 2006 Nov;128(5):547-59
pubmed: 17043151
J Gen Physiol. 2016 Feb;147(2):105-25
pubmed: 26755771
Biophys J. 2011 May 18;100(10):2387-93
pubmed: 21575572
J Gen Physiol. 1996 Sep;108(3):195-206
pubmed: 8882863
J Gen Physiol. 2006 Aug;128(2):203-17
pubmed: 16847099
Diabetologia. 2003 Aug;46(8):1046-62
pubmed: 12830383
Front Pharmacol. 2012 May 23;3:100
pubmed: 22654758
Biophys J. 1980 Jun;30(3):473-88
pubmed: 6266531
Nature. 2004 Apr 22;428(6985):864-8
pubmed: 15103379
Neuron. 1991 Oct;7(4):547-56
pubmed: 1931050
Biophys J. 1998 Apr;74(4):1808-20
pubmed: 9545043
Neuron. 2003 Apr 10;38(1):61-7
pubmed: 12691664