Calcium binding and permeation in TRPV channels: Insights from molecular dynamics simulations.


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:
04 12 2023
Historique:
received: 09 09 2022
revised: 21 05 2023
revised: 06 08 2023
accepted: 06 09 2023
medline: 21 9 2023
pubmed: 20 9 2023
entrez: 20 9 2023
Statut: ppublish

Résumé

Some calcium channels selectively permeate Ca2+, despite the high concentration of monovalent ions in the surrounding environment, which is essential for many physiological processes. Without atomistic and dynamical ion permeation details, the underlying mechanism of Ca2+ selectivity has long been an intensively studied, yet controversial, topic. This study takes advantage of the homologous Ca2+-selective TRPV6 and non-selective TRPV1 and utilizes the recently solved open-state structures and a newly developed multisite calcium model to investigate the ion binding and permeation features in TRPV channels by molecular dynamics simulations. Our results revealed that the open-state TRPV6 and TRPV1 show distinct ion binding patterns in the selectivity filter, which lead to different ion permeation features. Two Ca2+ ions simultaneously bind to the selectivity filter of TRPV6 compared with only one Ca2+ in the case of TRPV1. Multiple Ca2+ binding at the selectivity filter of TRPV6 permeated in a concerted manner, which could efficiently block the permeation of Na+. Cations of various valences differentiate between the binding sites at the entrance of the selectivity filter in TRPV6. Ca2+ preferentially binds to the central site with a higher probability of permeation, repelling Na+ to a peripheral site. Therefore, we believe that ion binding competition at the selectivity filter of calcium channels, including the binding strength and number of binding sites, determines Ca2+ selectivity under physiological conditions.

Identifiants

pubmed: 37728593
pii: 276280
doi: 10.1085/jgp.202213261
pmc: PMC10510737
pii:
doi:

Substances chimiques

Calcium SY7Q814VUP
Calcium Channels 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023 Liu et al.

Références

J Mol Graph. 1996 Dec;14(6):354-60, 376
pubmed: 9195488
Annu Rev Physiol. 2006;68:685-717
pubmed: 16460288
Nature. 2001 Nov 1;414(6859):73-7
pubmed: 11689945
Cell Metab. 2011 May 4;13(5):601-11
pubmed: 21531342
Biophys J. 2008 Sep 15;95(6):2658-72
pubmed: 18515379
J Mol Biol. 2021 Aug 20;433(17):167002
pubmed: 33891905
Proc Natl Acad Sci U S A. 2022 Oct 25;119(43):e2208081119
pubmed: 36251999
J Chem Inf Model. 2023 Feb 27;63(4):1293-1300
pubmed: 36758214
Annu Rev Biophys Biophys Chem. 1987;16:265-90
pubmed: 2439098
Sci Adv. 2020 Nov 27;6(48):
pubmed: 33246965
J Physiol. 1952 Apr;116(4):449-72
pubmed: 14946713
Science. 2014 Oct 17;346(6207):352-5
pubmed: 25324389
J Biol Chem. 2000 Feb 11;275(6):3963-9
pubmed: 10660551
Nature. 2001 Apr 5;410(6829):705-9
pubmed: 11287959
J Chem Theory Comput. 2008 Mar;4(3):435-47
pubmed: 26620784
J Gen Physiol. 2023 May 1;155(5):
pubmed: 36943243
Nature. 2013 Dec 5;504(7478):113-8
pubmed: 24305161
Pflugers Arch. 2011 Nov;462(5):681-91
pubmed: 21892726
Nat Commun. 2020 Feb 17;11(1):922
pubmed: 32066742
J Mol Biol. 1993 Dec 5;234(3):779-815
pubmed: 8254673
Annu Rev Physiol. 2003;65:133-59
pubmed: 12471162
Nat Chem. 2018 Aug;10(8):813-820
pubmed: 30030538
Nature. 2016 May 18;534(7607):347-51
pubmed: 27281200
Nature. 2014 Jan 2;505(7481):56-61
pubmed: 24270805
J Am Chem Soc. 2012 Jan 25;134(3):1840-6
pubmed: 22191670
Prog Biophys Mol Biol. 1968;18:123-83
pubmed: 4894870
Sci Rep. 2018 Apr 9;8(1):5715
pubmed: 29632318
Nature. 1984 May 31-Jun 6;309(5967):453-6
pubmed: 6328315
J Comput Chem. 2008 Aug;29(11):1859-65
pubmed: 18351591
Front Physiol. 2018 Nov 21;9:1661
pubmed: 30519193
Proc Natl Acad Sci U S A. 2010 Mar 30;107(13):5833-8
pubmed: 20231479
Science. 1995 Apr 14;268(5208):239-47
pubmed: 7716515
Nature. 2016 Jun 13;534(7608):506-11
pubmed: 27296226
PLoS Comput Biol. 2018 Sep 12;14(9):e1006398
pubmed: 30208027
Biophys J. 2013 Jun 4;104(11):2401-9
pubmed: 23746512
Biophys J. 2001 Jan;80(1):195-214
pubmed: 11159395
J Gen Physiol. 2013 May;141(5):619-32
pubmed: 23589581
J Phys Chem Lett. 2021 May 6;12(17):4286-4291
pubmed: 33909426
Annu Rev Biochem. 2007;76:387-417
pubmed: 17579562
Nat Methods. 2017 Jan;14(1):71-73
pubmed: 27819658
Nature. 2018 Jan 11;553(7687):233-237
pubmed: 29258289
J Comput Chem. 2014 Oct 15;35(27):1997-2004
pubmed: 25130509

Auteurs

Chunhong Liu (C)

Center for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University , Beijing, China.

Lingfeng Xue (L)

Center for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University , Beijing, China.

Chen Song (C)

Center for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University , Beijing, China.
Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University , Beijing, China.

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