Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations

The passive transport of molecules through a cell membrane relies on thermal motions of the lipids. However, the nature of transmembrane transport and the precise mechanism remain elusive and call for a comprehensive study of phonon excitations. Here we report a high resolution inelastic X-ray scatt...

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Main Authors: Zhernenkov, Mikhail, Bolmatov, Dima, Soloviov, Dmitry, Zhernenkov, Kirill, Toperverg, Boris P., Cunsolo, Alessandro, Bosak, Alexey, Cai, Yong Q.
Format: Online
Language:English
Published: Nature Publishing Group 2016
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4865866/
id pubmed-4865866
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spelling pubmed-48658662016-05-24 Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations Zhernenkov, Mikhail Bolmatov, Dima Soloviov, Dmitry Zhernenkov, Kirill Toperverg, Boris P. Cunsolo, Alessandro Bosak, Alexey Cai, Yong Q. Article The passive transport of molecules through a cell membrane relies on thermal motions of the lipids. However, the nature of transmembrane transport and the precise mechanism remain elusive and call for a comprehensive study of phonon excitations. Here we report a high resolution inelastic X-ray scattering study of the in-plane phonon excitations in 1,2-dipalmitoyl-sn-glycero-3-phosphocholine above and below the main transition temperature. In the gel phase, for the first time, we observe low-frequency transverse modes, which exhibit a phonon gap when the lipid transitions into the fluid phase. We argue that the phonon gap signifies the formation of short-lived nanometre-scale lipid clusters and transient pores, which facilitate the passive molecular transport across the bilayer plane. Our findings suggest that the phononic motion of the hydrocarbon tails provides an effective mechanism of passive transport, and illustrate the importance of the collective dynamics of biomembranes. Nature Publishing Group 2016-05-12 /pmc/articles/PMC4865866/ /pubmed/27175859 http://dx.doi.org/10.1038/ncomms11575 Text en Copyright © 2016, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved. http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Zhernenkov, Mikhail
Bolmatov, Dima
Soloviov, Dmitry
Zhernenkov, Kirill
Toperverg, Boris P.
Cunsolo, Alessandro
Bosak, Alexey
Cai, Yong Q.
spellingShingle Zhernenkov, Mikhail
Bolmatov, Dima
Soloviov, Dmitry
Zhernenkov, Kirill
Toperverg, Boris P.
Cunsolo, Alessandro
Bosak, Alexey
Cai, Yong Q.
Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations
author_facet Zhernenkov, Mikhail
Bolmatov, Dima
Soloviov, Dmitry
Zhernenkov, Kirill
Toperverg, Boris P.
Cunsolo, Alessandro
Bosak, Alexey
Cai, Yong Q.
author_sort Zhernenkov, Mikhail
title Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations
title_short Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations
title_full Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations
title_fullStr Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations
title_full_unstemmed Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations
title_sort revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations
description The passive transport of molecules through a cell membrane relies on thermal motions of the lipids. However, the nature of transmembrane transport and the precise mechanism remain elusive and call for a comprehensive study of phonon excitations. Here we report a high resolution inelastic X-ray scattering study of the in-plane phonon excitations in 1,2-dipalmitoyl-sn-glycero-3-phosphocholine above and below the main transition temperature. In the gel phase, for the first time, we observe low-frequency transverse modes, which exhibit a phonon gap when the lipid transitions into the fluid phase. We argue that the phonon gap signifies the formation of short-lived nanometre-scale lipid clusters and transient pores, which facilitate the passive molecular transport across the bilayer plane. Our findings suggest that the phononic motion of the hydrocarbon tails provides an effective mechanism of passive transport, and illustrate the importance of the collective dynamics of biomembranes.
publisher Nature Publishing Group
publishDate 2016
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4865866/
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