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Water orientation and dynamics in the closed and open influenza B virus M2 proton channels

The influenza B M2 protein forms a water-filled tetrameric channel to conduct protons across the lipid membrane. To understand how channel water mediates proton transport, we have investigated the water orientation and dynamics using solid-state NMR spectroscopy and molecular dynamics (MD) simulatio...

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Autores principales: Gelenter, Martin D., Mandala, Venkata S., Niesen, Michiel J. M., Sharon, Dina A., Dregni, Aurelio J., Willard, Adam P., Hong, Mei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7955094/
https://www.ncbi.nlm.nih.gov/pubmed/33712696
http://dx.doi.org/10.1038/s42003-021-01847-2
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author Gelenter, Martin D.
Mandala, Venkata S.
Niesen, Michiel J. M.
Sharon, Dina A.
Dregni, Aurelio J.
Willard, Adam P.
Hong, Mei
author_facet Gelenter, Martin D.
Mandala, Venkata S.
Niesen, Michiel J. M.
Sharon, Dina A.
Dregni, Aurelio J.
Willard, Adam P.
Hong, Mei
author_sort Gelenter, Martin D.
collection PubMed
description The influenza B M2 protein forms a water-filled tetrameric channel to conduct protons across the lipid membrane. To understand how channel water mediates proton transport, we have investigated the water orientation and dynamics using solid-state NMR spectroscopy and molecular dynamics (MD) simulations. (13)C-detected water (1)H NMR relaxation times indicate that water has faster rotational motion in the low-pH open channel than in the high-pH closed channel. Despite this faster dynamics, the open-channel water shows higher orientational order, as manifested by larger motionally-averaged (1)H chemical shift anisotropies. MD simulations indicate that this order is induced by the cationic proton-selective histidine at low pH. Furthermore, the water network has fewer hydrogen-bonding bottlenecks in the open state than in the closed state. Thus, faster dynamics and higher orientational order of water molecules in the open channel establish the water network structure that is necessary for proton hopping.
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spelling pubmed-79550942021-03-28 Water orientation and dynamics in the closed and open influenza B virus M2 proton channels Gelenter, Martin D. Mandala, Venkata S. Niesen, Michiel J. M. Sharon, Dina A. Dregni, Aurelio J. Willard, Adam P. Hong, Mei Commun Biol Article The influenza B M2 protein forms a water-filled tetrameric channel to conduct protons across the lipid membrane. To understand how channel water mediates proton transport, we have investigated the water orientation and dynamics using solid-state NMR spectroscopy and molecular dynamics (MD) simulations. (13)C-detected water (1)H NMR relaxation times indicate that water has faster rotational motion in the low-pH open channel than in the high-pH closed channel. Despite this faster dynamics, the open-channel water shows higher orientational order, as manifested by larger motionally-averaged (1)H chemical shift anisotropies. MD simulations indicate that this order is induced by the cationic proton-selective histidine at low pH. Furthermore, the water network has fewer hydrogen-bonding bottlenecks in the open state than in the closed state. Thus, faster dynamics and higher orientational order of water molecules in the open channel establish the water network structure that is necessary for proton hopping. Nature Publishing Group UK 2021-03-12 /pmc/articles/PMC7955094/ /pubmed/33712696 http://dx.doi.org/10.1038/s42003-021-01847-2 Text en © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Gelenter, Martin D.
Mandala, Venkata S.
Niesen, Michiel J. M.
Sharon, Dina A.
Dregni, Aurelio J.
Willard, Adam P.
Hong, Mei
Water orientation and dynamics in the closed and open influenza B virus M2 proton channels
title Water orientation and dynamics in the closed and open influenza B virus M2 proton channels
title_full Water orientation and dynamics in the closed and open influenza B virus M2 proton channels
title_fullStr Water orientation and dynamics in the closed and open influenza B virus M2 proton channels
title_full_unstemmed Water orientation and dynamics in the closed and open influenza B virus M2 proton channels
title_short Water orientation and dynamics in the closed and open influenza B virus M2 proton channels
title_sort water orientation and dynamics in the closed and open influenza b virus m2 proton channels
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7955094/
https://www.ncbi.nlm.nih.gov/pubmed/33712696
http://dx.doi.org/10.1038/s42003-021-01847-2
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