Protein crowding and lipid complexity influence the nanoscale dynamic organization of ion channels in cell membranes

Duncan, Anna L.; Reddy, Tyler John Edward; Koldsø, Heidi; Hélie, Jean; Fowler, Philip W.; Chavent, Matthieu; Sansom, Mark S. P.

doi:10.1038/s41598-017-16865-6

Title: Protein crowding and lipid complexity influence the nanoscale dynamic organization of ion channels in cell membranes

Journal Article · Thu Nov 30 00:00:00 EST 2017 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-017-16865-6· OSTI ID:1422920

Duncan, Anna L. ^[1];

^[2]; Koldsø, Heidi ^[3]; Hélie, Jean ^[4];

^[1]; Chavent, Matthieu ^[5];

^[1]

Univ. of Oxford, Oxford (United Kingdom)
Univ. of Oxford, Oxford (United Kingdom); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Univ. of Oxford, Oxford (United Kingdom); D. E. Shaw Research, New York, NY (United States)
Univ. of Oxford, Oxford (United Kingdom); Semmle, Oxford (United Kingdom)
Univ. of Oxford, Oxford (United Kingdom); IPBS-CNRS, Midi-Pyrenees (France)

Cell membranes are crowded and complex environments. To investigate the effect of protein-lipid interactions on dynamic organization in mammalian cell membranes, we have performed coarse-grained molecular dynamics simulations containing >100 copies of an inwardly rectifying potassium (Kir) channel which forms specific interactions with the regulatory lipid phosphatidylinositol 4,5-bisphosphate (PIP₂). The tendency of protein molecules to cluster has the effect of organizing the membrane into dynamic compartments. At the same time, the diversity of lipids present has a marked effect on the clustering behavior of ion channels. Sub-diffusion of proteins and lipids is observed. Protein crowding alters the sub-diffusive behavior of proteins and lipids such as PIP₂ which interact tightly with Kir channels. Protein crowding also affects bilayer properties, such as membrane undulations and bending rigidity, in a PIP₂-dependent manner. As a result, this interplay between the diffusion and the dynamic organization of Kir channels may have important implications for channel function.

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Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: Foreign Funding; USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1422920

Report Number(s):: LA-UR-17-25048

Journal Information:: Scientific Reports, Vol. 7, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 55 works

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Nanoclustering as a dominant feature of plasma membrane organization Ken, Jacobson,; Nancy, Thompson,; A., Torreno-Pina, Juan The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/44t7-xz62	text	January 2014
Entropic Tension in Crowded Membranes Lindén, Martin; Sens, Pierre; Phillips, Rob arXiv https://doi.org/10.48550/arxiv.1103.5796	text	January 2011
Anomalous diffusion of phospholipids and cholesterols in a lipid bilayer and its origins Jeon, Jae-Hyung; Monne, Hector Martinez-Seara; Javanainen, Matti arXiv https://doi.org/10.48550/arxiv.1210.5485	text	January 2012

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Biased continuous-time random walks for ordinary and equilibrium cases: facilitation of diffusion, ergodicity breaking and ageing Hou, Ru; Cherstvy, Andrey G.; Metzler, Ralf Physical Chemistry Chemical Physics, Vol. 20, Issue 32 https://doi.org/10.1039/c8cp01863d	journal	January 2018
Transient anomalous diffusion with Prabhakar-type memory Stanislavsky, Aleksander; Weron, Aleksander The Journal of Chemical Physics, Vol. 149, Issue 4 https://doi.org/10.1063/1.5042075	journal	July 2018
Computational Nanoscopy of Tight Junctions at the Blood–Brain Barrier Interface Rajagopal, Nandhini; Irudayanathan, Flaviyan Jerome; Nangia, Shikha International Journal of Molecular Sciences, Vol. 20, Issue 22 https://doi.org/10.3390/ijms20225583	journal	November 2019
Long acyl chain ceramides govern cholesterol and cytoskeleton dependence of membrane outer leaflet dynamics Gupta, Anjali; Muralidharan, Sneha; Torta, Federico Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1862, Issue 3 https://doi.org/10.1016/j.bbamem.2019.183153	journal	March 2020
To infect or not to infect: molecular determinants of bacterial outer membrane vesicle internalization by host membranes Jefferies, Damien; Khalid, Syma Journal of Molecular Biology, Vol. 432, Issue 4 https://doi.org/10.1016/j.jmb.2020.01.008	journal	February 2020

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