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 Lab. (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 = {2019},
month = {11}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 16 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Steric Interaction of Fluid Membranes in Multilayer Systems
journal, January 1978
- Helfrich, W.
- Zeitschrift für Naturforschung A, Vol. 33, Issue 3
Phase equilibria in the phosphatidylcholine-cholesterol system
journal, November 1987
- Hjort Ipsen, J.; Karlström, G.; Mourtisen, O. G.
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 905, Issue 1
Docosahexaenoic Acid Enhances Segregation of Lipids between Raft and Nonraft Domains: 2H-NMR Study
journal, July 2008
- Soni, Smita P.; LoCascio, Daniel S.; Liu, Yidong
- Biophysical Journal, Vol. 95, Issue 1
Membrane tension controls the assembly of curvature-generating proteins
journal, May 2015
- Simunovic, Mijo; Voth, Gregory A.
- Nature Communications, Vol. 6, Issue 1
Recent developments in methodology employed to study the interactions between nanomaterials and model lipid membranes
journal, November 2015
- Wu, Lie; Jiang, Xiue
- Analytical and Bioanalytical Chemistry, Vol. 408, Issue 11
Probing Elastic and Viscous Properties of Phospholipid Bilayers Using Neutron Spin Echo Spectroscopy
journal, September 2017
- Nagao, Michihiro; Kelley, Elizabeth G.; Ashkar, Rana
- The Journal of Physical Chemistry Letters, Vol. 8, Issue 19
Structure of the MscL Homolog from Mycobacterium tuberculosis: A Gated Mechanosensitive Ion Channel
journal, December 1998
- Chang, G.; Spencer, R. H.; Lee, A. T.
- Science, Vol. 282, Issue 5397
Lipid distribution and transport across cellular membranes
journal, April 2001
- Pomorski, Thomas; Hrafnsdóttir, Sigrún; Devaux, Philippe F.
- Seminars in Cell & Developmental Biology, Vol. 12, Issue 2
Oleic and Docosahexaenoic Acid Differentially Phase Separate from Lipid Raft Molecules: A Comparative NMR, DSC, AFM, and Detergent Extraction Study
journal, September 2004
- Shaikh, Saame Raza; Dumaual, Alfred C.; Castillo, Alicia
- Biophysical Journal, Vol. 87, Issue 3
Effect of Chain Length and Unsaturation on Elasticity of Lipid Bilayers
journal, July 2000
- Rawicz, W.; Olbrich, K. C.; McIntosh, T.
- Biophysical Journal, Vol. 79, Issue 1
Domain-induced budding of vesicles
journal, May 1993
- Jülicher, Frank; Lipowsky, Reinhard
- Physical Review Letters, Vol. 70, Issue 19
Membrane lipids: where they are and how they behave
journal, February 2008
- van Meer, Gerrit; Voelker, Dennis R.; Feigenson, Gerald W.
- Nature Reviews Molecular Cell Biology, Vol. 9, Issue 2
Measurements of the effect of membrane asymmetry on the mechanical properties of lipid bilayers
journal, January 2015
- Elani, Yuval; Purushothaman, Sowmya; Booth, Paula J.
- Chemical Communications, Vol. 51, Issue 32
Fluctuation dynamics of bilayer vesicles with intermonolayer sliding: Experiment and theory
journal, January 2015
- Mell, Michael; Moleiro, Lara H.; Hertle, Yvonne
- Chemistry and Physics of Lipids, Vol. 185
The 30 m Small-Angle Neutron Scattering Instruments at the National Institute of Standards and Technology
journal, June 1998
- Glinka, C. J.; Barker, J. G.; Hammouda, B.
- Journal of Applied Crystallography, Vol. 31, Issue 3, p. 430-445
Joint small-angle X-ray and neutron scattering data analysis of asymmetric lipid vesicles
journal, February 2017
- Eicher, Barbara; Heberle, Frederick A.; Marquardt, Drew
- Journal of Applied Crystallography, Vol. 50, Issue 2
Tuning Membrane Thickness Fluctuations in Model Lipid Bilayers
journal, July 2015
- Ashkar, Rana; Nagao, Michihiro; Butler, Paul D.
- Biophysical Journal, Vol. 109, Issue 1
Line Tension and Interaction Energies of Membrane Rafts Calculated from Lipid Splay and Tilt
journal, February 2005
- Kuzmin, Peter I.; Akimov, Sergey A.; Chizmadzhev, Yuri A.
- Biophysical Journal, Vol. 88, Issue 2
Transmembrane Asymmetry and Lateral Domains in Biological Membranes: Rafts and Transmembrane Asymmetry
journal, March 2004
- Devaux, Philippe F.; Morris, Roger
- Traffic, Vol. 5, Issue 4
Phase Separation in Lipid Membranes
journal, March 2011
- Heberle, F. A.; Feigenson, G. W.
- Cold Spring Harbor Perspectives in Biology, Vol. 3, Issue 4
Dissipative curvature fluctuations in bilayer vesicles: Coexistence of pure-bending and hybrid curvature-compression modes
journal, January 2010
- Arriaga, L. R.; Rodríguez-García, R.; López-Montero, I.
- The European Physical Journal E, Vol. 31, Issue 1
Reconciling Differences between Lipid Transfer in Free-Standing and Solid Supported Membranes: A Time-Resolved Small-Angle Neutron Scattering Study
journal, March 2017
- Wah, Benny; Breidigan, Jeffrey M.; Adams, Joseph
- Langmuir, Vol. 33, Issue 14
Transbilayer Movement of Phospholipids in Biogenic Membranes
journal, March 2004
- Kol, Matthijs A.; de Kroon, Anton I. P. M.; Killian, J. Antoinette
- Biochemistry, Vol. 43, Issue 10
Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension
journal, October 2003
- Baumgart, Tobias; Hess, Samuel T.; Webb, Watt W.
- Nature, Vol. 425, Issue 6960
Lipid Bilayers and Membrane Dynamics: Insight into Thickness Fluctuations
journal, July 2012
- Woodka, Andrea C.; Butler, Paul D.; Porcar, Lionel
- Physical Review Letters, Vol. 109, Issue 5
Membrane stiffness is modified by integral membrane proteins
journal, January 2016
- Fowler, Philip W.; Hélie, Jean; Duncan, Anna
- Soft Matter, Vol. 12, Issue 37
Domains in Binary SOPC/POPE Lipid Mixtures Studied by Pulsed Field Gradient 1H MAS NMR
journal, September 2004
- Polozov, Ivan V.; Gawrisch, Klaus
- Biophysical Journal, Vol. 87, Issue 3
DAVE: A Comprehensive Software Suite for the Reduction, Visualization, and Analysis of Low Energy Neutron Spectroscopic Data
journal, November 2009
- Azuah, Richard Tumanjong; Kneller, Larry R.; Qiu, Yiming
- Journal of Research of the National Institute of Standards and Technology, Vol. 114, Issue 6
Intrinsic Curvature-Mediated Transbilayer Coupling in Asymmetric Lipid Vesicles
text, January 2018
- Eicher, Barbara; Marquardt, Drew; Heberle, Frederick A.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Membrane-induced interactions between inclusions
journal, November 1993
- Dan, N.; Pincus, P.; Safran, S. A.
- Langmuir, Vol. 9, Issue 11
Preparation of asymmetric phospholipid vesicles for use as cell membrane models
journal, September 2018
- Doktorova, Milka; Heberle, Frederick A.; Eicher, Barbara
- Nature Protocols, Vol. 13, Issue 9
Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature
journal, November 2011
- Kučerka, Norbert; Nieh, Mu-Ping; Katsaras, John
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1808, Issue 11
Gramicidin Increases Lipid Flip-Flop in Symmetric and Asymmetric Lipid Vesicles
journal, March 2019
- Doktorova, Milka; Heberle, Frederick A.; Marquardt, Drew
- Biophysical Journal, Vol. 116, Issue 5
Membrane bending energy concept of vesicle- and cell-shapes and shape-transitions
journal, June 1994
- Sackmann, E.
- FEBS Letters, Vol. 346, Issue 1
Endocytic vesicle scission by lipid phase boundary forces
journal, June 2006
- Liu, J.; Kaksonen, M.; Drubin, D. G.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 27
Capsaicin Regulates Voltage-Dependent Sodium Channels by Altering Lipid Bilayer Elasticity
journal, June 2005
- Lundbæk, J. A.; Birn, P.; Tape, S. E.
- Molecular Pharmacology, Vol. 68, Issue 3
Stability of Ligands on Nanoparticles Regulating the Integrity of Biological Membranes at the Nano–Lipid Interface
journal, July 2019
- Wang, Liming; Quan, Peiyu; Chen, Serena H.
- ACS Nano, Vol. 13, Issue 8
Asymmetric Lipid Membranes: Towards More Realistic Model Systems
journal, May 2015
- Marquardt, Drew; Geier, Barbara; Pabst, Georg
- Membranes, Vol. 5, Issue 2
1 H NMR Shows Slow Phospholipid Flip-Flop in Gel and Fluid Bilayers
journal, February 2017
- Marquardt, Drew; Heberle, Frederick A.; Miti, Tatiana
- Langmuir, Vol. 33, Issue 15
Membrane Mechanics of Endocytosis in Cells with Turgor
journal, October 2015
- Dmitrieff, Serge; Nédélec, François
- PLOS Computational Biology, Vol. 11, Issue 10
Thermal Fluctuation and Elasticity of Lipid Vesicles Interacting with Pore-Forming Peptides
journal, July 2010
- Lee, Ji-Hwan; Choi, Sung-Min; Doe, Changwoo
- Physical Review Letters, Vol. 105, Issue 3
Reduction and analysis of SANS and USANS data using IGOR Pro
journal, November 2006
- Kline, Steven R.
- Journal of Applied Crystallography, Vol. 39, Issue 6, p. 895-900
Undulations and Dynamic Structure Factor of Membranes
journal, December 1996
- Zilman, A. G.; Granek, R.
- Physical Review Letters, Vol. 77, Issue 23
Recent developments in the field of bending rigidity measurements on membranes
journal, June 2014
- Dimova, Rumiana
- Advances in Colloid and Interface Science, Vol. 208
Bending stiffness of biological membranes: What can be measured by neutron spin echo?
journal, July 2013
- Mell, Michael; Moleiro, Lara H.; Hertle, Yvonne
- The European Physical Journal E, Vol. 36, Issue 7
Viscous Modes of Fluid Bilayer Membranes
journal, July 1993
- Seifert, U.; Langer, S. A.
- Europhysics Letters (EPL), Vol. 23, Issue 1
Elastic curvature constants of lipid monolayers and bilayers
journal, November 2006
- Marsh, Derek
- Chemistry and Physics of Lipids, Vol. 144, Issue 2
Dynamics of an asymmetric bilayer lipid membrane in a viscous solvent
journal, July 2015
- Bingham, R. J.; Smye, S. W.; Olmsted, P. D.
- EPL (Europhysics Letters), Vol. 111, Issue 1
Intrinsic Curvature-Mediated Transbilayer Coupling in Asymmetric Lipid Vesicles
journal, January 2018
- Eicher, Barbara; Marquardt, Drew; Heberle, Frederick A.
- Biophysical Journal, Vol. 114, Issue 1
Methanol Accelerates DMPC Flip-Flop and Transfer: A SANS Study on Lipid Dynamics
journal, March 2019
- Nguyen, Michael H. L.; DiPasquale, Mitchell; Rickeard, Brett W.
- Biophysical Journal, Vol. 116, Issue 5
Studying the effects of asymmetry on the bending rigidity of lipid membranes formed by microfluidics
journal, January 2016
- Karamdad, K.; Law, R. V.; Seddon, J. M.
- Chemical Communications, Vol. 52, Issue 30
Statistical Thermodynamics of Membrane Bending-Mediated Protein–Protein Attractions
journal, March 2001
- Chou, Tom; Kim, Ken S.; Oster, George
- Biophysical Journal, Vol. 80, Issue 3
Subnanometer Structure of an Asymmetric Model Membrane: Interleaflet Coupling Influences Domain Properties
journal, May 2016
- Heberle, Frederick A.; Marquardt, Drew; Doktorova, Milka
- Langmuir, Vol. 32, Issue 20
Lateral diffusion in binary mixtures of cholesterol and phosphatidylcholines.
journal, January 1979
- Rubenstein, J. L.; Smith, B. A.; McConnell, H. M.
- Proceedings of the National Academy of Sciences, Vol. 76, Issue 1
Membrane fluctuations mediate lateral interaction between cadherin bonds
journal, June 2017
- Fenz, Susanne F.; Bihr, Timo; Schmidt, Daniel
- Nature Physics, Vol. 13, Issue 9
Estimation of the location of natural α-tocopherol in lipid bilayers by 13C-NMR spectroscopy
journal, September 1985
- Perly, B.; Smith, I. C. P.; Hughes, L.
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 819, Issue 1
Scaling of lipid membrane rigidity with domain area fraction
journal, January 2019
- Kelley, Elizabeth G.; Butler, Paul D.; Nagao, Michihiro
- Soft Matter, Vol. 15, Issue 13
Inhomogeneous fluid membranes: Segregation, ordering, and effective rigidity
journal, October 1995
- Netz, Roland R.; Pincus, P.
- Physical Review E, Vol. 52, Issue 4
Monolayer spontaneous curvature of raft-forming membrane lipids
journal, January 2013
- Kollmitzer, Benjamin; Heftberger, Peter; Rappolt, Michael
- Soft Matter, Vol. 9, Issue 45
Structure and mechanism in prokaryotic mechanosensitive channels
journal, August 2003
- Perozo, Eduardo; Rees, Douglas C.
- Current Opinion in Structural Biology, Vol. 13, Issue 4
Lipid topogenesis
journal, March 1981
- Bell, R. M.; Ballas, L. M.; Coleman, R. A.
- Journal of Lipid Research, Vol. 22, Issue 3
Monolayer Spontaneous Curvature of Raft-Forming Membrane Lipids
journal, January 2014
- Kollmitzer, Benjamin; Heftberger, Peter; Rappolt, Michael
- Biophysical Journal, Vol. 106, Issue 2
Viscous modes of fluid bilayer membranes
collection, January 1993
- Seifert, Udo; Langer, Stephen A.
- Universität Stuttgart
Dynamics of an asymmetric bilayer lipid membrane in a viscous solvent
text, January 2015
- Bingham, R. J.; Smye, S. W.; Olmsted, P. D.
- arXiv