Transverse lipid organization dictates bending fluctuations in model plasma membranes
Abstract
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 correspondingmore »
- Authors:
-
[2];
[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)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- 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)
- OSTI Identifier:
- 1609126
- Alternate Identifier(s):
- OSTI ID: 1577879
- Grant/Contract Number:
- AC02-06CH11357; MCB-1817929
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nanoscale
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 3; Journal ID: ISSN 2040-3364
- Publisher:
- Royal Society of Chemistry
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Rickeard, Brett W., Nguyen, Michael H. L., DiPasquale, Mitchell, Yip, Caesar G., Baker, Hamilton, Heberle, Frederick A., Zuo, Xiaobing, Kelley, Elizabeth G., Nagao, Michihiro, and Marquardt, Drew. Transverse lipid organization dictates bending fluctuations in model plasma membranes. United States: N. p., 2019.
Web. doi:10.1039/c9nr07977g.
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. Transverse lipid organization dictates bending fluctuations in model plasma membranes. United States. https://doi.org/10.1039/c9nr07977g
Rickeard, Brett W., Nguyen, Michael H. L., DiPasquale, Mitchell, Yip, Caesar G., Baker, Hamilton, Heberle, Frederick A., Zuo, Xiaobing, Kelley, Elizabeth G., Nagao, Michihiro, and Marquardt, Drew. Tue .
"Transverse lipid organization dictates bending fluctuations in model plasma membranes". United States. https://doi.org/10.1039/c9nr07977g. https://www.osti.gov/servlets/purl/1609126.
@article{osti_1609126,
title = {Transverse lipid organization dictates bending fluctuations in model plasma membranes},
author = {Rickeard, Brett W. and Nguyen, Michael H. L. and DiPasquale, Mitchell and Yip, Caesar G. and Baker, Hamilton and Heberle, Frederick A. and Zuo, Xiaobing and Kelley, Elizabeth G. and Nagao, Michihiro and Marquardt, Drew},
abstractNote = {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.},
doi = {10.1039/c9nr07977g},
journal = {Nanoscale},
number = 3,
volume = 12,
place = {United States},
year = {Tue Nov 12 00:00:00 EST 2019},
month = {Tue Nov 12 00:00:00 EST 2019}
}
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