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.

View Accepted Manuscript (DOE)

Cite

Export

Save

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) (SC-22); National Institute of Standards and Technology (NIST)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1609126

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

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

References (66)

Lipid distribution and transport across cellular membranes Pomorski, Thomas; Hrafnsdóttir, Sigrún; Devaux, Philippe F. Seminars in Cell & Developmental Biology, Vol. 12, Issue 2 https://doi.org/10.1006/scdb.2000.0231	journal	April 2001
Recent developments in methodology employed to study the interactions between nanomaterials and model lipid membranes Wu, Lie; Jiang, Xiue Analytical and Bioanalytical Chemistry, Vol. 408, Issue 11 https://doi.org/10.1007/s00216-015-9157-5	journal	November 2015
Estimation of the location of natural α-tocopherol in lipid bilayers by 13C-NMR spectroscopy Perly, B.; Smith, I. C. P.; Hughes, L. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 819, Issue 1 https://doi.org/10.1016/0005-2736(85)90203-2	journal	September 1985
Phase equilibria in the phosphatidylcholine-cholesterol system Hjort Ipsen, J.; Karlström, G.; Mourtisen, O. G. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 905, Issue 1 https://doi.org/10.1016/0005-2736(87)90020-4	journal	November 1987
Membrane bending energy concept of vesicle- and cell-shapes and shape-transitions Sackmann, E. FEBS Letters, Vol. 346, Issue 1 https://doi.org/10.1016/0014-5793(94)00484-6	journal	June 1994
Effect of Chain Length and Unsaturation on Elasticity of Lipid Bilayers Rawicz, W.; Olbrich, K. C.; McIntosh, T. Biophysical Journal, Vol. 79, Issue 1 https://doi.org/10.1016/S0006-3495(00)76295-3	journal	July 2000
Statistical Thermodynamics of Membrane Bending-Mediated Protein–Protein Attractions Chou, Tom; Kim, Ken S.; Oster, George Biophysical Journal, Vol. 80, Issue 3 https://doi.org/10.1016/S0006-3495(01)76086-9	journal	March 2001
Lipid topogenesis Bell, R. M.; Ballas, L. M.; Coleman, R. A. Journal of Lipid Research, Vol. 22, Issue 3 https://doi.org/10.1016/S0022-2275(20)34952-X	journal	March 1981
Structure and mechanism in prokaryotic mechanosensitive channels Perozo, Eduardo; Rees, Douglas C. Current Opinion in Structural Biology, Vol. 13, Issue 4 https://doi.org/10.1016/S0959-440X(03)00106-4	journal	August 2003
Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature Kučerka, Norbert; Nieh, Mu-Ping; Katsaras, John Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1808, Issue 11 https://doi.org/10.1016/j.bbamem.2011.07.022	journal	November 2011
Monolayer Spontaneous Curvature of Raft-Forming Membrane Lipids Kollmitzer, Benjamin; Heftberger, Peter; Rappolt, Michael Biophysical Journal, Vol. 106, Issue 2 https://doi.org/10.1016/j.bpj.2013.11.2802	journal	January 2014
Tuning Membrane Thickness Fluctuations in Model Lipid Bilayers Ashkar, Rana; Nagao, Michihiro; Butler, Paul D. Biophysical Journal, Vol. 109, Issue 1 https://doi.org/10.1016/j.bpj.2015.05.033	journal	July 2015
Intrinsic Curvature-Mediated Transbilayer Coupling in Asymmetric Lipid Vesicles Eicher, Barbara; Marquardt, Drew; Heberle, Frederick A. Biophysical Journal, Vol. 114, Issue 1 https://doi.org/10.1016/j.bpj.2017.11.009	journal	January 2018
Gramicidin Increases Lipid Flip-Flop in Symmetric and Asymmetric Lipid Vesicles Doktorova, Milka; Heberle, Frederick A.; Marquardt, Drew Biophysical Journal, Vol. 116, Issue 5 https://doi.org/10.1016/j.bpj.2019.01.016	journal	March 2019
Methanol Accelerates DMPC Flip-Flop and Transfer: A SANS Study on Lipid Dynamics Nguyen, Michael H. L.; DiPasquale, Mitchell; Rickeard, Brett W. Biophysical Journal, Vol. 116, Issue 5 https://doi.org/10.1016/j.bpj.2019.01.021	journal	March 2019
Elastic curvature constants of lipid monolayers and bilayers Marsh, Derek Chemistry and Physics of Lipids, Vol. 144, Issue 2 https://doi.org/10.1016/j.chemphyslip.2006.08.004	journal	November 2006
Fluctuation dynamics of bilayer vesicles with intermonolayer sliding: Experiment and theory Mell, Michael; Moleiro, Lara H.; Hertle, Yvonne Chemistry and Physics of Lipids, Vol. 185 https://doi.org/10.1016/j.chemphyslip.2014.11.005	journal	January 2015
Recent developments in the field of bending rigidity measurements on membranes Dimova, Rumiana Advances in Colloid and Interface Science, Vol. 208 https://doi.org/10.1016/j.cis.2014.03.003	journal	June 2014
Probing Elastic and Viscous Properties of Phospholipid Bilayers Using Neutron Spin Echo Spectroscopy Nagao, Michihiro; Kelley, Elizabeth G.; Ashkar, Rana The Journal of Physical Chemistry Letters, Vol. 8, Issue 19 https://doi.org/10.1021/acs.jpclett.7b01830	journal	September 2017
Subnanometer Structure of an Asymmetric Model Membrane: Interleaflet Coupling Influences Domain Properties Heberle, Frederick A.; Marquardt, Drew; Doktorova, Milka Langmuir, Vol. 32, Issue 20 https://doi.org/10.1021/acs.langmuir.5b04562	journal	May 2016
Reconciling Differences between Lipid Transfer in Free-Standing and Solid Supported Membranes: A Time-Resolved Small-Angle Neutron Scattering Study Wah, Benny; Breidigan, Jeffrey M.; Adams, Joseph Langmuir, Vol. 33, Issue 14 https://doi.org/10.1021/acs.langmuir.6b04013	journal	March 2017
¹ H NMR Shows Slow Phospholipid Flip-Flop in Gel and Fluid Bilayers Marquardt, Drew; Heberle, Frederick A.; Miti, Tatiana Langmuir, Vol. 33, Issue 15 https://doi.org/10.1021/acs.langmuir.6b04485	journal	February 2017
Stability of Ligands on Nanoparticles Regulating the Integrity of Biological Membranes at the Nano–Lipid Interface Wang, Liming; Quan, Peiyu; Chen, Serena H. ACS Nano, Vol. 13, Issue 8 https://doi.org/10.1021/acsnano.9b00114	journal	July 2019
Transbilayer Movement of Phospholipids in Biogenic Membranes Kol, Matthijs A.; de Kroon, Anton I. P. M.; Killian, J. Antoinette Biochemistry, Vol. 43, Issue 10 https://doi.org/10.1021/bi036200f	journal	March 2004
Neutron Spin Echo Spectroscopy at the NIST Center for Neutron Research Rosov, N.; Rathgeber, S.; Monkenbusch, M. ACS Symposium Series https://doi.org/10.1021/bk-2000-0739.ch007	book	July 1999
Membrane-induced interactions between inclusions Dan, N.; Pincus, P.; Safran, S. A. Langmuir, Vol. 9, Issue 11 https://doi.org/10.1021/la00035a005	journal	November 1993
Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension Baumgart, Tobias; Hess, Samuel T.; Webb, Watt W. Nature, Vol. 425, Issue 6960 https://doi.org/10.1038/nature02013	journal	October 2003
Membrane tension controls the assembly of curvature-generating proteins Simunovic, Mijo; Voth, Gregory A. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8219	journal	May 2015
Membrane fluctuations mediate lateral interaction between cadherin bonds Fenz, Susanne F.; Bihr, Timo; Schmidt, Daniel Nature Physics, Vol. 13, Issue 9 https://doi.org/10.1038/nphys4138	journal	June 2017
Membrane lipids: where they are and how they behave van Meer, Gerrit; Voelker, Dennis R.; Feigenson, Gerald W. Nature Reviews Molecular Cell Biology, Vol. 9, Issue 2 https://doi.org/10.1038/nrm2330	journal	February 2008
Preparation of asymmetric phospholipid vesicles for use as cell membrane models Doktorova, Milka; Heberle, Frederick A.; Eicher, Barbara Nature Protocols, Vol. 13, Issue 9 https://doi.org/10.1038/s41596-018-0033-6	journal	September 2018
Measurements of the effect of membrane asymmetry on the mechanical properties of lipid bilayers Elani, Yuval; Purushothaman, Sowmya; Booth, Paula J. Chemical Communications, Vol. 51, Issue 32 https://doi.org/10.1039/C5CC00712G	journal	January 2015
Studying the effects of asymmetry on the bending rigidity of lipid membranes formed by microfluidics Karamdad, K.; Law, R. V.; Seddon, J. M. Chemical Communications, Vol. 52, Issue 30 https://doi.org/10.1039/C5CC10307J	journal	January 2016
Membrane stiffness is modified by integral membrane proteins Fowler, Philip W.; Hélie, Jean; Duncan, Anna Soft Matter, Vol. 12, Issue 37 https://doi.org/10.1039/C6SM01186A	journal	January 2016
Scaling of lipid membrane rigidity with domain area fraction Kelley, Elizabeth G.; Butler, Paul D.; Nagao, Michihiro Soft Matter, Vol. 15, Issue 13 https://doi.org/10.1039/C8SM02362J	journal	January 2019
Monolayer spontaneous curvature of raft-forming membrane lipids Kollmitzer, Benjamin; Heftberger, Peter; Rappolt, Michael Soft Matter, Vol. 9, Issue 45 https://doi.org/10.1039/c3sm51829a	journal	January 2013
Endocytic vesicle scission by lipid phase boundary forces Liu, J.; Kaksonen, M.; Drubin, D. G. Proceedings of the National Academy of Sciences, Vol. 103, Issue 27 https://doi.org/10.1073/pnas.0601045103	journal	June 2006
Lateral diffusion in binary mixtures of cholesterol and phosphatidylcholines. Rubenstein, J. L.; Smith, B. A.; McConnell, H. M. Proceedings of the National Academy of Sciences, Vol. 76, Issue 1 https://doi.org/10.1073/pnas.76.1.15	journal	January 1979
Phase Separation in Lipid Membranes Heberle, F. A.; Feigenson, G. W. Cold Spring Harbor Perspectives in Biology, Vol. 3, Issue 4 https://doi.org/10.1101/cshperspect.a004630	journal	March 2011
Inhomogeneous fluid membranes: Segregation, ordering, and effective rigidity Netz, Roland R.; Pincus, P. Physical Review E, Vol. 52, Issue 4 https://doi.org/10.1103/PhysRevE.52.4114	journal	October 1995
Thermal Fluctuation and Elasticity of Lipid Vesicles Interacting with Pore-Forming Peptides Lee, Ji-Hwan; Choi, Sung-Min; Doe, Changwoo Physical Review Letters, Vol. 105, Issue 3 https://doi.org/10.1103/PhysRevLett.105.038101	journal	July 2010
Lipid Bilayers and Membrane Dynamics: Insight into Thickness Fluctuations Woodka, Andrea C.; Butler, Paul D.; Porcar, Lionel Physical Review Letters, Vol. 109, Issue 5 https://doi.org/10.1103/PhysRevLett.109.058102	journal	July 2012
Domain-induced budding of vesicles Jülicher, Frank; Lipowsky, Reinhard Physical Review Letters, Vol. 70, Issue 19 https://doi.org/10.1103/PhysRevLett.70.2964	journal	May 1993
Undulations and Dynamic Structure Factor of Membranes Zilman, A. G.; Granek, R. Physical Review Letters, Vol. 77, Issue 23 https://doi.org/10.1103/PhysRevLett.77.4788	journal	December 1996
Reduction and analysis of SANS and USANS data using IGOR Pro Kline, Steven R. Journal of Applied Crystallography, Vol. 39, Issue 6, p. 895-900 https://doi.org/10.1107/S0021889806035059	journal	November 2006
The 30 m Small-Angle Neutron Scattering Instruments at the National Institute of Standards and Technology Glinka, C. J.; Barker, J. G.; Hammouda, B. Journal of Applied Crystallography, Vol. 31, Issue 3, p. 430-445 https://doi.org/10.1107/S0021889897017020	journal	June 1998
Joint small-angle X-ray and neutron scattering data analysis of asymmetric lipid vesicles Eicher, Barbara; Heberle, Frederick A.; Marquardt, Drew Journal of Applied Crystallography, Vol. 50, Issue 2 https://doi.org/10.1107/S1600576717000656	journal	February 2017
Transmembrane Asymmetry and Lateral Domains in Biological Membranes: Rafts and Transmembrane Asymmetry Devaux, Philippe F.; Morris, Roger Traffic, Vol. 5, Issue 4 https://doi.org/10.1111/j.1600-0854.2004.0170.x	journal	March 2004
Capsaicin Regulates Voltage-Dependent Sodium Channels by Altering Lipid Bilayer Elasticity Lundbæk, J. A.; Birn, P.; Tape, S. E. Molecular Pharmacology, Vol. 68, Issue 3 https://doi.org/10.1124/mol.105.013573	journal	June 2005
Structure of the MscL Homolog from Mycobacterium tuberculosis: A Gated Mechanosensitive Ion Channel Chang, G.; Spencer, R. H.; Lee, A. T. Science, Vol. 282, Issue 5397 https://doi.org/10.1126/science.282.5397.2220	journal	December 1998
Dissipative curvature fluctuations in bilayer vesicles: Coexistence of pure-bending and hybrid curvature-compression modes Arriaga, L. R.; Rodríguez-García, R.; López-Montero, I. The European Physical Journal E, Vol. 31, Issue 1 https://doi.org/10.1140/epje/i2010-10551-1	journal	January 2010
Bending stiffness of biological membranes: What can be measured by neutron spin echo? Mell, Michael; Moleiro, Lara H.; Hertle, Yvonne The European Physical Journal E, Vol. 36, Issue 7 https://doi.org/10.1140/epje/i2013-13075-2	journal	July 2013
Dynamics of an asymmetric bilayer lipid membrane in a viscous solvent Bingham, R. J.; Smye, S. W.; Olmsted, P. D. EPL (Europhysics Letters), Vol. 111, Issue 1 https://doi.org/10.1209/0295-5075/111/18004	journal	July 2015
Viscous Modes of Fluid Bilayer Membranes Seifert, U.; Langer, S. A. Europhysics Letters (EPL), Vol. 23, Issue 1 https://doi.org/10.1209/0295-5075/23/1/012	journal	July 1993
Membrane Mechanics of Endocytosis in Cells with Turgor Dmitrieff, Serge; Nédélec, François PLOS Computational Biology, Vol. 11, Issue 10 https://doi.org/10.1371/journal.pcbi.1004538	journal	October 2015
Steric Interaction of Fluid Membranes in Multilayer Systems Helfrich, W. Zeitschrift für Naturforschung A, Vol. 33, Issue 3 https://doi.org/10.1515/zna-1978-0308	journal	January 1978
Domains in Binary SOPC/POPE Lipid Mixtures Studied by Pulsed Field Gradient 1H MAS NMR Polozov, Ivan V.; Gawrisch, Klaus Biophysical Journal, Vol. 87, Issue 3 https://doi.org/10.1529/biophysj.104.040725	journal	September 2004
Oleic and Docosahexaenoic Acid Differentially Phase Separate from Lipid Raft Molecules: A Comparative NMR, DSC, AFM, and Detergent Extraction Study Shaikh, Saame Raza; Dumaual, Alfred C.; Castillo, Alicia Biophysical Journal, Vol. 87, Issue 3 https://doi.org/10.1529/biophysj.104.044552	journal	September 2004
Line Tension and Interaction Energies of Membrane Rafts Calculated from Lipid Splay and Tilt Kuzmin, Peter I.; Akimov, Sergey A.; Chizmadzhev, Yuri A. Biophysical Journal, Vol. 88, Issue 2 https://doi.org/10.1529/biophysj.104.048223	journal	February 2005
Docosahexaenoic Acid Enhances Segregation of Lipids between Raft and Nonraft Domains: 2H-NMR Study Soni, Smita P.; LoCascio, Daniel S.; Liu, Yidong Biophysical Journal, Vol. 95, Issue 1 https://doi.org/10.1529/biophysj.107.123612	journal	July 2008
Membrane Mechanics of Endocytosis in Cells with Turgor. Dmitrieff, Serge; Nédélec, François Public Library of Science (PLoS) https://doi.org/10.17863/cam.55639	journalarticle	January 2015
Viscous modes of fluid bilayer membranes Seifert, Udo; Langer, Stephen A. Universität Stuttgart https://doi.org/10.18419/opus-7806	collection	January 1993
Intrinsic Curvature-Mediated Transbilayer Coupling in Asymmetric Lipid Vesicles Eicher, Barbara; Marquardt, Drew; Heberle, Frederick A. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2018-05680	text	January 2018
Asymmetric Lipid Membranes: Towards More Realistic Model Systems Marquardt, Drew; Geier, Barbara; Pabst, Georg Membranes, Vol. 5, Issue 2 https://doi.org/10.3390/membranes5020180	journal	May 2015
Dynamics of an asymmetric bilayer lipid membrane in a viscous solvent Bingham, R. J.; Smye, S. W.; Olmsted, P. D. arXiv https://doi.org/10.48550/arxiv.1507.00023	text	January 2015
DAVE: A Comprehensive Software Suite for the Reduction, Visualization, and Analysis of Low Energy Neutron Spectroscopic Data Azuah, Richard Tumanjong; Kneller, Larry R.; Qiu, Yiming Journal of Research of the National Institute of Standards and Technology, Vol. 114, Issue 6 https://doi.org/10.6028/jres.114.025	journal	November 2009

Similar Records

Joint small-angle X-ray and neutron scattering data analysis of asymmetric lipid vesicles

Journal Article · 2017 · Journal of Applied Crystallography (Online) · OSTI ID:1351774

Eicher, Barbara; Heberle, Frederick A.; Marquardt, Drew T.; +3 more

Peptide-Induced Lipid Flip-Flop in Asymmetric Liposomes Measured by Small Angle Neutron Scattering

Journal Article · 2019 · Langmuir · OSTI ID:1561589

Nguyen, Michael H. L.; DiPasquale, Mitchell; Rickeard, Brett W.; +9 more

Phosphatidylserine Asymmetry Promotes the Membrane Insertion of a Transmembrane Helix

Journal Article · 2019 · Biophysical Journal · OSTI ID:1561605

Scott, Haden L.; Heberle, Frederick A.; Katsaras, John; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (66)

Similar Records

Related Subjects