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Changes in ion selectivity following the asymmetrical addition of charge to the selectivity filter of bacterial sodium channels

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Fedorenko, Olena A., Khovanov, Igor A., Roberts, Stephen K. and Guardiani, Carlo (2020) Changes in ion selectivity following the asymmetrical addition of charge to the selectivity filter of bacterial sodium channels. Entropy, 22 (12). 1390. doi:10.3390/e22121390 ISSN 1099-4300.

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Official URL: https://doi.org/10.3390/e22121390

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Abstract

Voltage-gated sodium channels (NaVs) play fundamental roles in eukaryotes, but their exceptional size hinders their structural resolution. Bacterial NaVs are simplified homologues of their eukaryotic counterparts, but their use as models of eukaryotic Na+ channels is limited by their homotetrameric structure at odds with the asymmetric Selectivity Filter (SF) of eukaryotic NaVs. This work aims at mimicking the SF of eukaryotic NaVs by engineering radial asymmetry into the SF of bacterial channels. This goal was pursued with two approaches: the co-expression of different monomers of the NaChBac bacterial channel to induce the random assembly of heterotetramers, and the concatenation of four bacterial monomers to form a concatemer that can be targeted by site-specific mutagenesis. Patch-clamp measurements and Molecular Dynamics simulations showed that an additional gating charge in the SF leads to a significant increase in Na+ and a modest increase in the Ca2+ conductance in the NavMs concatemer in agreement with the behavior of the population of random heterotetramers with the highest proportion of channels with charge −5e. We thus showed that charge, despite being important, is not the only determinant of conduction and selectivity, and we created new tools extending the use of bacterial channels as models of eukaryotic counterparts.

Item Type: Journal Article
Subjects: Q Science > QH Natural history
Q Science > QP Physiology
Divisions: Faculty of Science, Engineering and Medicine > Engineering > Engineering
Library of Congress Subject Headings (LCSH): Ion channels , Sodium channels , Eukaryotic cells
Journal or Publication Title: Entropy
Publisher: M D P I AG
ISSN: 1099-4300
Official Date: 9 December 2020
Dates:
DateEvent
9 December 2020Published
7 December 2020Accepted
Volume: 22
Number: 12
Article Number: 1390
DOI: 10.3390/e22121390
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access (Creative Commons)
Date of first compliant deposit: 28 April 2021
Date of first compliant Open Access: 29 April 2021
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
EP/M015831/1 [EPSRC] Engineering and Physical Sciences Research Councilhttp://dx.doi.org/10.13039/501100000266
EP/M016889/1[EPSRC] Engineering and Physical Sciences Research Councilhttp://dx.doi.org/10.13039/501100000266
803213Horizon 2020 Framework Programmehttp://dx.doi.org/10.13039/100010661
Is Part Of: 1
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