Conformational trajectory of allosteric gating of the human cone photoreceptor cyclic nucleotide-gated channel.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
18 07 2023
18 07 2023
Historique:
received:
11
01
2023
accepted:
05
07
2023
medline:
21
7
2023
pubmed:
19
7
2023
entrez:
18
7
2023
Statut:
epublish
Résumé
Cyclic nucleotide-gated (CNG) channels transduce chemical signals into electrical signals in sensory receptors and neurons. They are activated by cGMP or cAMP, which bind to the cyclic nucleotide-binding domain (CNBD) to open a gate located 50-60 Å away in the central cavity. Structures of closed and open vertebrate CNG channels have been solved, but the conformational landscape of this allosteric gating remains to be elucidated and enriched. Here, we report structures of the cGMP-activated human cone photoreceptor CNGA3/CNGB3 channel in closed, intermediate, pre-open and open states in detergent or lipid nanodisc, all with fully bound cGMP. The pre-open and open states are obtained only in the lipid nanodisc, suggesting a critical role of lipids in tuning the energetic landscape of CNGA3/CNGB3 activation. The different states exhibit subunit-unique, incremental and distinct conformational rearrangements that originate in the CNBD, propagate through the gating ring to the transmembrane domain, and gradually open the S6 cavity gate. Our work illustrates a spatial conformational-change wave of allosteric gating of a vertebrate CNG channel by its natural ligand and provides an expanded framework for studying CNG properties and channelopathy.
Identifiants
pubmed: 37463923
doi: 10.1038/s41467-023-39971-8
pii: 10.1038/s41467-023-39971-8
pmc: PMC10354024
doi:
Substances chimiques
Cyclic Nucleotide-Gated Cation Channels
0
Lipids
0
Nucleotides, Cyclic
0
Cyclic GMP
H2D2X058MU
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
Pagination
4284Subventions
Organisme : NEI NIH HHS
ID : R01 EY032880
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103310
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM085234
Pays : United States
Organisme : NIGMS NIH HHS
ID : U24 GM129539
Pays : United States
Organisme : NIH HHS
ID : S10 OD019994
Pays : United States
Informations de copyright
© 2023. The Author(s).
Références
Proc Natl Acad Sci U S A. 2019 Jul 9;116(28):13989-13995
pubmed: 31235590
Neuron. 2002 Feb 28;33(5):731-9
pubmed: 11879650
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Proc Natl Acad Sci U S A. 2023 Apr 11;120(15):e2300309120
pubmed: 37011209
Nature. 2017 Feb 2;542(7639):60-65
pubmed: 28099415
Nature. 1985 Jan 24-30;313(6000):310-3
pubmed: 2578616
Nat Methods. 2009 Jul;6(7):532-7
pubmed: 19525958
Acta Crystallogr D Struct Biol. 2019 Oct 1;75(Pt 10):861-877
pubmed: 31588918
Commun Biol. 2022 Mar 1;5(1):190
pubmed: 35233102
J Neurosci. 2000 Apr 15;20(8):2792-9
pubmed: 10751430
Nat Commun. 2022 Nov 14;13(1):6919
pubmed: 36376326
Proc Natl Acad Sci U S A. 2017 Apr 25;114(17):4430-4435
pubmed: 28396445
Biol Chem. 2013 Nov;394(11):1439-51
pubmed: 24021595
Nature. 1987 Jan 29-Feb 4;325(6103):442-4
pubmed: 3027574
Nat Struct Mol Biol. 2022 Jan;29(1):32-39
pubmed: 34969975
Am J Physiol Cell Physiol. 2013 Jul 15;305(2):C147-59
pubmed: 23552282
Structure. 2016 May 3;24(5):797-805
pubmed: 27041595
Nat Commun. 2020 Jul 27;11(1):3752
pubmed: 32719334
J Physiol. 2022 Nov;600(21):4585-4601
pubmed: 35412676
J Biol Chem. 2014 May 9;289(19):13680-90
pubmed: 24675082
Elife. 2021 Oct 08;10:
pubmed: 34623258
J Mol Graph. 1996 Dec;14(6):354-60, 376
pubmed: 9195488
Biomolecules. 2022 Jun 10;12(6):
pubmed: 35740939
J Gen Physiol. 2013 Apr;141(4):413-30
pubmed: 23530136
J Biol Chem. 2010 Nov 19;285(47):37082-91
pubmed: 20829353
Trends Neurosci. 2022 Oct;45(10):763-776
pubmed: 35934530
Neuron. 2021 Apr 21;109(8):1302-1313.e4
pubmed: 33651975
Nat Chem Biol. 2020 Dec;16(12):1314-1320
pubmed: 33199904
J Struct Biol. 2016 Jan;193(1):1-12
pubmed: 26592709
Nat Methods. 2017 Mar;14(3):290-296
pubmed: 28165473
Nat Chem Biol. 2020 Dec;16(12):1331-1342
pubmed: 33199909
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
pubmed: 20057044
Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14577-82
pubmed: 25197093
Physiol Rev. 2002 Jul;82(3):769-824
pubmed: 12087135
Nature. 2022 May;605(7908):172-178
pubmed: 35444281
Elife. 2018 Jul 20;7:
pubmed: 30028291
Cell Rep. 2022 Apr 26;39(4):110737
pubmed: 35476976
Nature. 2003 Sep 11;425(6954):200-5
pubmed: 12968185
Nat Struct Mol Biol. 2020 Jul;27(7):625-634
pubmed: 32483338
Acta Crystallogr D Struct Biol. 2018 Jun 1;74(Pt 6):531-544
pubmed: 29872004
Sci Rep. 2018 Jan 8;8(1):45
pubmed: 29311674
Nat Commun. 2021 May 14;12(1):2802
pubmed: 33990563
Neuron. 2022 Jan 5;110(1):86-95.e5
pubmed: 34699778
J Membr Biol. 2004 Sep 1;201(1):51-7
pubmed: 15635812
Nat Struct Mol Biol. 2022 Jan;29(1):40-46
pubmed: 34969976
Nat Commun. 2022 May 24;13(1):2874
pubmed: 35610228
Protein Sci. 2021 Jan;30(1):70-82
pubmed: 32881101
J Struct Biol. 2021 Jun;213(2):107702
pubmed: 33582281
Annu Rev Neurosci. 1996;19:235-63
pubmed: 8833443
Nature. 1990 Sep 13;347(6289):184-7
pubmed: 1697649
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Int J Mol Sci. 2018 Mar 07;19(3):
pubmed: 29518895
Mol Pharmacol. 2007 Jan;71(1):176-83
pubmed: 17018579
J Struct Biol. 2022 Mar;214(1):107828
pubmed: 34971760
Nature. 1989 Dec 14;342(6251):762-6
pubmed: 2481236
Elife. 2018 Nov 09;7:
pubmed: 30412051
Mol Cell. 2021 Dec 2;81(23):4771-4783.e7
pubmed: 34678168
J Struct Biol. 2005 Jul;151(1):41-60
pubmed: 15890530
Nature. 1993 Jul 1;364(6432):61-4
pubmed: 7686276
J Biol Chem. 2011 Dec 30;286(52):44811-20
pubmed: 22006928
Science. 2022 Oct 14;378(6616):eadd1268
pubmed: 36227998
Nat Methods. 2017 Apr;14(4):331-332
pubmed: 28250466
J Gen Physiol. 2016 Feb;147(2):189-200
pubmed: 26755772
J Gen Physiol. 2000 Dec;116(6):755-68
pubmed: 11099345
Nat Struct Mol Biol. 2022 Nov;29(11):1092-1100
pubmed: 36352139