Line Tension Controls Liquid-Disordered + Liquid-Ordered Domain Size Transition in Lipid Bilayers

Rebecca D. Usery; Thais A. Enoki; Sanjula P. Wickramasinghe; Michael D. Weiner; Wen Chyan Tsai; Mary B. Kim; Shu Wang; Thomas L. Torng; David G. Ackerman; Frederick A. Heberle; John Katsaras; Gerald W. Feigenson

doi:10.1016/j.bpj.2017.02.033

Line Tension Controls Liquid-Disordered + Liquid-Ordered Domain Size Transition in Lipid Bilayers

Rebecca D. Usery, Thais A. Enoki, Sanjula P. Wickramasinghe, Michael D. Weiner, Wen Chyan Tsai, Mary B. Kim, Shu Wang, Thomas L. Torng, David G. Ackerman, Frederick A. Heberle, John Katsaras, Gerald W. Feigenson

Research output: Contribution to journal › Article › peer-review

73 Scopus citations

Abstract

To better understand animal cell plasma membranes, we studied simplified models, namely four-component lipid bilayer mixtures. Here we describe the domain size transition in the region of coexisting liquid-disordered (Ld) + liquid-ordered (Lo) phases. This transition occurs abruptly in composition space with domains increasing in size by two orders of magnitude, from tens of nanometers to microns. We measured the line tension between coexisting Ld and Lo domains close to the domain size transition for a variety of lipid mixtures, finding that in every case the transition occurs at a line tension of ∼0.3 pN. A computational model incorporating line tension and dipole repulsion indicated that even small changes in line tension can result in domains growing in size by several orders of magnitude, consistent with experimental observations. We find that other properties of the coexisting Ld and Lo phases do not change significantly in the vicinity of the abrupt domain size transition.

Original language	English
Pages (from-to)	1431-1443
Number of pages	13
Journal	Biophysical Journal
Volume	112
Issue number	7
DOIs	https://doi.org/10.1016/j.bpj.2017.02.033
State	Published - Apr 11 2017

Funding

This work was supported by U.S. National Science Foundation grant No. MCB-1410926, U.S. National Institutes of Health grant No. GM105684, and OLCF/Titan grant No. DD-2015-BIP125 (to G.W.F.); NIH Training grant No. 1-T32-GM08267 (to D.G.A. and M.D.W.); National Science Foundation Graduate Research Fellowship Program under grant No. DGE-1144153ESR (to R.D.U.); Brazil Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq (to T.A.E.); the University of Tennessee-ORNL Joint Institute for Biological Sciences (to F.A.H.); and the Laboratory Directed Research and Development Program (to J.K. and F.A.H.) of ORNL, managed by UT-Battelle under US Department of Energy (DOE) contract No. DE-AC05-00OR22725. ESR studies were supported by NIH/NIGMS grant No. P41GM103521 to J. Freed. Neutron scattering studies conducted using the EQ-SANS instrument at the ORNL Spallation Neutron Source, and the BioSANS instrument at ORNL's High Flux Isotope Reactor, were sponsored by the Scientific User Facilities Division of the DOE Office of Science, Basic Energy Sciences (BES) and Biological and Environmental Research (BER). The MD simulations in this work used resources of the Oak Ridge Leadership Computing Facility at the ORNL, which is supported by the Office of Science of the U.S. Department of Energy under contract No. DE-AC05-00OR22725.

Funders	Funder number
OLCF
Titan	DD-2015-BIP125
University of Tennessee-ORNL Joint Institute for Biological Sciences
National Science Foundation	MCB-1410926, DGE-1144153ESR
National Science Foundation
National Institutes of Health	GM105684
National Institutes of Health
U.S. Department of Energy	DE-AC05-00OR22725
U.S. Department of Energy
National Institute of General Medical Sciences	T32GM008267, P41GM103521
National Institute of General Medical Sciences
Office of Science
Basic Energy Sciences
Biological and Environmental Research
Oak Ridge National Laboratory
Laboratory Directed Research and Development
UT-Battelle
Conselho Nacional de Desenvolvimento Científico e Tecnológico

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Usery, R. D., Enoki, T. A., Wickramasinghe, S. P., Weiner, M. D., Tsai, W. C., Kim, M. B., Wang, S., Torng, T. L., Ackerman, D. G., Heberle, F. A., Katsaras, J., & Feigenson, G. W. (2017). Line Tension Controls Liquid-Disordered + Liquid-Ordered Domain Size Transition in Lipid Bilayers. Biophysical Journal, 112(7), 1431-1443. https://doi.org/10.1016/j.bpj.2017.02.033

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title = "Line Tension Controls Liquid-Disordered + Liquid-Ordered Domain Size Transition in Lipid Bilayers",

abstract = "To better understand animal cell plasma membranes, we studied simplified models, namely four-component lipid bilayer mixtures. Here we describe the domain size transition in the region of coexisting liquid-disordered (Ld) + liquid-ordered (Lo) phases. This transition occurs abruptly in composition space with domains increasing in size by two orders of magnitude, from tens of nanometers to microns. We measured the line tension between coexisting Ld and Lo domains close to the domain size transition for a variety of lipid mixtures, finding that in every case the transition occurs at a line tension of ∼0.3 pN. A computational model incorporating line tension and dipole repulsion indicated that even small changes in line tension can result in domains growing in size by several orders of magnitude, consistent with experimental observations. We find that other properties of the coexisting Ld and Lo phases do not change significantly in the vicinity of the abrupt domain size transition.",

author = "Usery, {Rebecca D.} and Enoki, {Thais A.} and Wickramasinghe, {Sanjula P.} and Weiner, {Michael D.} and Tsai, {Wen Chyan} and Kim, {Mary B.} and Shu Wang and Torng, {Thomas L.} and Ackerman, {David G.} and Heberle, {Frederick A.} and John Katsaras and Feigenson, {Gerald W.}",

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AU - Usery, Rebecca D.

AU - Enoki, Thais A.

AU - Wickramasinghe, Sanjula P.

AU - Weiner, Michael D.

AU - Tsai, Wen Chyan

AU - Kim, Mary B.

AU - Wang, Shu

AU - Torng, Thomas L.

AU - Ackerman, David G.

AU - Heberle, Frederick A.

AU - Katsaras, John

AU - Feigenson, Gerald W.

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AB - To better understand animal cell plasma membranes, we studied simplified models, namely four-component lipid bilayer mixtures. Here we describe the domain size transition in the region of coexisting liquid-disordered (Ld) + liquid-ordered (Lo) phases. This transition occurs abruptly in composition space with domains increasing in size by two orders of magnitude, from tens of nanometers to microns. We measured the line tension between coexisting Ld and Lo domains close to the domain size transition for a variety of lipid mixtures, finding that in every case the transition occurs at a line tension of ∼0.3 pN. A computational model incorporating line tension and dipole repulsion indicated that even small changes in line tension can result in domains growing in size by several orders of magnitude, consistent with experimental observations. We find that other properties of the coexisting Ld and Lo phases do not change significantly in the vicinity of the abrupt domain size transition.

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Line Tension Controls Liquid-Disordered + Liquid-Ordered Domain Size Transition in Lipid Bilayers

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