Transverse lipid organization dictates bending fluctuations in model plasma membranes

Rickeard, Brett W.; Nguyen, Michael H.  L.; DiPasquale, Mitchell; Yip, Caesar G.; Baker, Hamilton; Heberle, Frederick A.; Zuo, Xiaobing; Kelley, Elizabeth G.; Nagao, Michihiro; Marquardt, Drew

doi:10.1039/c9nr07977g

Title: Transverse lipid organization dictates bending fluctuations in model plasma membranes

Journal Article · 12 November 2019 · Nanoscale

DOI: https://doi.org/10.1039/c9nr07977g · OSTI ID:1609126

Rickeard, Brett W. ^[1]; Nguyen, Michael H. L. ^[1]; DiPasquale, Mitchell ^[1]; Yip, Caesar G. ^[1]; Baker, Hamilton ^[1];

^[2]; Zuo, Xiaobing ^[3];

^[4];

^[5];

^[1]

Univ. of Windsor, ON (Canada)
Univ. of Texas Health Science Center, Houston, TX (United States); Univ. of Tennessee, Knoxville, TN (United States)
Argonne National Lab. (ANL), Argonne, IL (United States)
National Inst. of Standards and Technology (NIST), Gaithersburg, MD (United States)
National Inst. of Standards and Technology (NIST), Gaithersburg, MD (United States); Indiana Univ., Bloomington, IN (United States)

Membrane undulations play a vital role in many biological processes, including the regulation of membrane protein activity. The asymmetric lipid composition of most biological membranes complicates theoretical description of these bending fluctuations, yet experimental data that would inform any such a theory is scarce. In this work, we used neutron spin-echo (NSE) spectroscopy to measure the bending fluctuations of large unilamellar vesicles (LUV) having an asymmetric transbilayer distribution of high- and lowmelting lipids. The asymmetric vesicles were prepared using cyclodextrin-mediated lipid exchange, and were composed of an outer leaflet enriched in egg sphingomyelin (ESM) and an inner leaflet enriched in 1-palmitoyl-2-oleoyl-phosphoethanolamine (POPE), which have main transition temperatures of 37 °C and 25 °C, respectively. The overall membrane bending rigidity was measured at three temperatures: 15 °C, where both lipids are in a gel state; 45 °C, where both lipids are in a fluid state; and 30 °C, where there is gel-fluid co-existence. Remarkably, the dynamics for the fluid asymmetric LUVs (aLUVs) at 30 °C and 45 °C do not follow trends predicted by their symmetric counterparts. At 30 °C, compositional asymmetry suppressed the bending fluctuations, with the asymmetric bilayer exhibiting a larger bending modulus than that of symmetric bilayers corresponding to either the outer or inner leaflet. We conclude that the compositional asymmetry and leaflet coupling influence the internal dissipation within the bilayer and result in membrane properties that cannot be directly predicted from corresponding symmetric bilayers.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Natural Sciences and Engineering Research Council of Canada (NSERC); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institute of Standards and Technology (NIST)

Grant/Contract Number:: AC02-06CH11357; MCB-1817929

OSTI ID:: 1609126

Alternate ID(s):: OSTI ID: 1577879

Journal Information:: Nanoscale, Vol. 12, Issue 3; ISSN 2040-3364

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 22 works

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