Molecular Structure of Sphingomyelin in Fluid Phase Bilayers Determined by the Joint Analysis of Small-Angle Neutron and X-ray Scattering Data

Doktorova, Milka; Kučerka, Norbert; Kinnun, Jacob J.; Pan, Jianjun; Marquardt, Drew; Scott, Haden L.; Venable, Richard M.; Pastor, Richard W.; Wassall, Stephen R.; Katsaras, John; Heberle, Frederick A.

doi:10.1021/acs.jpcb.0c03389

Title: Molecular Structure of Sphingomyelin in Fluid Phase Bilayers Determined by the Joint Analysis of Small-Angle Neutron and X-ray Scattering Data

Journal Article · Fri May 29 00:00:00 EDT 2020 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI:https://doi.org/10.1021/acs.jpcb.0c03389· OSTI ID:1684662

Doktorova, Milka ^[1]; Kučerka, Norbert ^[2]; Kinnun, Jacob J. ^[3];

^[4];

^[5]; Scott, Haden L. ^[6]; Venable, Richard M. ^[7];

^[7]; Wassall, Stephen R. ^[3]; Katsaras, John ^[8];

^[9]

Univ. of Texas Health Science Center, Houston, TX (United States)
Joint Inst. for Nuclear Research (JINR), Dubna (Russian Federation). Frank Lab. of Neutron Physics; Comenius Univ., Bratislava (Slovakia)
Indiana Univ.-Purdue Univ. Indianapolis, Indianapolis, IN (United States)
Univ. of South Florida, Tampa, FL (United States)
Univ. of Windsor, ON (Canada)
Univ. of Tennessee, Knoxville, TN (United States). Center for Environmental Biotechnology
National Inst. of Health (NIH), Bethesda, MD (United States). Lab. of Computational Biology, National Heart, Lung and Blood Inst.
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States)

In this work, we have determined the fluid bilayer structure of palmitoyl sphingomyelin (PSM) and stearoyl sphingomyelin (SSM) by simultaneously analyzing small-angle neutron and X-ray scattering data. Using a newly developed scattering density profile (SDP) model for sphingomyelin lipids, we report structural parameters including the area per lipid, total bilayer thickness, and hydrocarbon thickness, in addition to lipid volumes determined by densitometry. Unconstrained all-atom simulations of PSM bilayers at 55 °C using the C36 CHARMM force field produced a lipid area of 56 Å², a value that is 10% lower than the one determined experimentally by SDP analysis (61.9 Å2). Furthermore, scattering form factors calculated from the unconstrained simulations were in poor agreement with experimental form factors, even though segmental order parameter (S_CD) profiles calculated from the simulations were in relatively good agreement with S_CD profiles obtained from NMR experiments. Conversely, constrained area simulations at 61.9 Å² resulted in good agreement between the simulation and experimental scattering form factors, but not with S_CD profiles from NMR. We discuss possible reasons for the discrepancies between these two types of data that are frequently used as validation metrics for molecular dynamics force fields.

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Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: AC05-00OR22725; MCB-1817929; 1F32GM134704-01

OSTI ID:: 1684662

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Vol. 124, Issue 25; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

The membrane protein universe: what's out there and why bother? von Heijne, G. Journal of Internal Medicine, Vol. 261, Issue 6 https://doi.org/10.1111/j.1365-2796.2007.01792.x	journal	June 2007
Plasma membranes are asymmetric in lipid unsaturation, packing and protein shape Lorent, J. H.; Levental, K. R.; Ganesan, L. Nature Chemical Biology, Vol. 16, Issue 6 https://doi.org/10.1038/s41589-020-0529-6	journal	May 2020
Lipid Rafts: Controversies Resolved, Mysteries Remain Levental, Ilya; Levental, Kandice R.; Heberle, Frederick A. Trends in Cell Biology, Vol. 30, Issue 5 https://doi.org/10.1016/j.tcb.2020.01.009	journal	May 2020
Lipid Rafts As a Membrane-Organizing Principle Lingwood, D.; Simons, K. Science, Vol. 327, Issue 5961 https://doi.org/10.1126/science.1174621	journal	December 2009
Conformational studies of sphingolipids by NMR spectroscopy. II. Sphingomyelin Talbott, C. Mark; Vorobyov, Igor; Borchman, Douglas Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1467, Issue 2 https://doi.org/10.1016/S0005-2736(00)00229-7	journal	August 2000
Lipid sorting in epithelial cells Simons, Kai; Van Meer, Gerrit Biochemistry, Vol. 27, Issue 17 https://doi.org/10.1021/bi00417a001	journal	August 1988
Hexagonal Substructure and Hydrogen Bonding in Liquid-Ordered Phases Containing Palmitoyl Sphingomyelin Sodt, Alexander J.; Pastor, Richard W.; Lyman, Edward Biophysical Journal, Vol. 109, Issue 5 https://doi.org/10.1016/j.bpj.2015.07.036	journal	September 2015
Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure Wiener, M. C.; White, S. H. Biophysical Journal, Vol. 61, Issue 2 https://doi.org/10.1016/S0006-3495(92)81849-0	journal	February 1992
Lipid Bilayer Structure Determined by the Simultaneous Analysis of Neutron and X-Ray Scattering Data Kučerka, Norbert; Nagle, John F.; Sachs, Jonathan N. Biophysical Journal, Vol. 95, Issue 5 https://doi.org/10.1529/biophysj.108.132662	journal	September 2008
Mantid—Data analysis and visualization package for neutron scattering and $μ$ SR experiments Arnold, O.; Bilheux, J. C.; Borreguero, J. M. Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 764 https://doi.org/10.1016/j.nima.2014.07.029	journal	November 2014
The molecular structure of a phosphatidylserine bilayer determined by scattering and molecular dynamics simulations Pan, Jianjun; Cheng, Xiaolin; Monticelli, Luca Soft Matter, Vol. 10, Issue 21 https://doi.org/10.1039/c4sm00066h	journal	January 2014
Molecular Structures of Fluid Phosphatidylethanolamine Bilayers Obtained from Simulation-to-Experiment Comparisons and Experimental Scattering Density Profiles Kučerka, Norbert; van Oosten, Brad; Pan, Jianjun The Journal of Physical Chemistry B, Vol. 119, Issue 5 https://doi.org/10.1021/jp511159q	journal	December 2014
Model-based approaches for the determination of lipid bilayer structure from small-angle neutron and X-ray scattering data Heberle, Frederick A.; Pan, Jianjun; Standaert, Robert F. European Biophysics Journal, Vol. 41, Issue 10 https://doi.org/10.1007/s00249-012-0817-5	journal	May 2012
Structural Significance of Lipid Diversity as Studied by Small Angle Neutron and X-ray Scattering Kučerka, Norbert; Heberle, Frederick; Pan, Jianjun Membranes, Vol. 5, Issue 3 https://doi.org/10.3390/membranes5030454	journal	September 2015
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
Revisiting the bilayer structures of fluid phase phosphatidylglycerol lipids: Accounting for exchangeable hydrogens Pan, Jianjun; Marquardt, Drew; Heberle, Frederick A. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1838, Issue 11 https://doi.org/10.1016/j.bbamem.2014.08.009	journal	November 2014
Dynamics and ordering of lipid spin-labels along the coexistence curve of two membrane phases: An ESR study Smith, Andrew K.; Freed, Jack H. Chemistry and Physics of Lipids, Vol. 165, Issue 3 https://doi.org/10.1016/j.chemphyslip.2012.02.009	journal	April 2012
Extracting order parameters from powder EPR lineshapes for spin-labelled lipids in membranes Schorn, Karl; Marsh, Derek Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 53, Issue 12 https://doi.org/10.1016/S1386-1425(97)00136-4	journal	October 1997
Docosahexaenoic and Eicosapentaenoic Acids Segregate Differently between Raft and Nonraft Domains Williams, Justin A.; Batten, Shawn E.; Harris, Mitchel Biophysical Journal, Vol. 103, Issue 2 https://doi.org/10.1016/j.bpj.2012.06.016	journal	July 2012
The description of membrane lipid conformation, order and dynamics by 2H-NMR Davis, James H. Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 737, Issue 1 https://doi.org/10.1016/0304-4157(83)90015-1	journal	March 1983
Deuterium magnetic resonance: theory and application to lipid membranes Seelig, Joachim Quarterly Reviews of Biophysics, Vol. 10, Issue 3 https://doi.org/10.1017/S0033583500002948	journal	August 1977
Molecular structures of fluid phase phosphatidylglycerol bilayers as determined by small angle neutron and X-ray scattering Pan, Jianjun; Heberle, Frederick A.; Tristram-Nagle, Stephanie Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1818, Issue 9 https://doi.org/10.1016/j.bbamem.2012.05.007	journal	September 2012
CHARMM-GUI Membrane Builder toward realistic biological membrane simulations Wu, Emilia L.; Cheng, Xi; Jo, Sunhwan Journal of Computational Chemistry, Vol. 35, Issue 27 https://doi.org/10.1002/jcc.23702	journal	August 2014
CHARMM-GUI Input Generator for NAMD, GROMACS, AMBER, OpenMM, and CHARMM/OpenMM Simulations Using the CHARMM36 Additive Force Field Lee, Jumin; Cheng, Xi; Swails, Jason M. Journal of Chemical Theory and Computation, Vol. 12, Issue 1 https://doi.org/10.1021/acs.jctc.5b00935	journal	December 2015
CHARMM-GUI Membrane Builder for Mixed Bilayers and Its Application to Yeast Membranes Jo, Sunhwan; Lim, Joseph B.; Klauda, Jeffery B. Biophysical Journal, Vol. 97, Issue 1 https://doi.org/10.1016/j.bpj.2009.04.013	journal	July 2009
CHARMM-GUI: A web-based graphical user interface for CHARMM Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G. Journal of Computational Chemistry, Vol. 29, Issue 11 https://doi.org/10.1002/jcc.20945	journal	March 2008
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
CHARMM All-Atom Additive Force Field for Sphingomyelin: Elucidation of Hydrogen Bonding and of Positive Curvature Venable, Richard M.; Sodt, Alexander J.; Rogaski, Brent Biophysical Journal, Vol. 107, Issue 1 https://doi.org/10.1016/j.bpj.2014.05.034	journal	July 2014
Improving the CHARMM Force Field for Polyunsaturated Fatty Acid Chains Klauda, Jeffery B.; Monje, Viviana; Kim, Taehoon The Journal of Physical Chemistry B, Vol. 116, Issue 31 https://doi.org/10.1021/jp304056p	journal	July 2012
Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types Klauda, Jeffery B.; Venable, Richard M.; Freites, J. Alfredo The Journal of Physical Chemistry B, Vol. 114, Issue 23 https://doi.org/10.1021/jp101759q	journal	June 2010
Computing 1-D atomic densities in macromolecular simulations: The density profile tool for VMD Giorgino, Toni Computer Physics Communications, Vol. 185, Issue 1 https://doi.org/10.1016/j.cpc.2013.08.022	journal	January 2014
Simulation-Based Methods for Interpreting X-Ray Data from Lipid Bilayers Klauda, Jeffery B.; Kučerka, Norbert; Brooks, Bernard R. Biophysical Journal, Vol. 90, Issue 8 https://doi.org/10.1529/biophysj.105.075697	journal	April 2006
Structural analysis of weakly ordered membrane stacks Pabst, Georg; Koschuch, Richard; Pozo-Navas, Beatriz Journal of Applied Crystallography, Vol. 36, Issue 6 https://doi.org/10.1107/S0021889803017527	journal	November 2003
On the Mechanism of Bilayer Separation by Extrusion, or Why Your LUVs Are Not Really Unilamellar Scott, Haden L.; Skinkle, Allison; Kelley, Elizabeth G. Biophysical Journal, Vol. 117, Issue 8 https://doi.org/10.1016/j.bpj.2019.09.006	journal	October 2019
Deuterium isotope effect on the stability of molecules: phospholipids Guard-Friar, Deborah; Chen, Chang Hwei; Engle, Adam S. The Journal of Physical Chemistry, Vol. 89, Issue 9 https://doi.org/10.1021/j100255a054	journal	April 1985
Absence of chiral domains in mixtures of dipalmitoylphosphatidylcholine molecules of opposite chirality Katsaras, J.; Epand, R. F.; Epand, R. M. Physical Review E, Vol. 55, Issue 3 https://doi.org/10.1103/PhysRevE.55.3751	journal	March 1997
Mechanical aspects of membrane thermodynamics. Estimation of the mechanical properties of lipid membranes close to the chain melting transition from calorimetry Heimburg, Thomas Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1415, Issue 1 https://doi.org/10.1016/S0005-2736(98)00189-8	journal	December 1998
Acyl chain orientational order in large unilamellar vesicles: comparison with multilamellar liposomes: a 2H and 31P nuclear magnetic resonance study Fenske, D. B.; Cullis, P. R. Biophysical Journal, Vol. 64, Issue 5 https://doi.org/10.1016/S0006-3495(93)81515-7	journal	May 1993
Rapid deconvolution of NMR powder spectra by weighted fast Fourier transformation McCabe, M. Alan; Wassail, Stephen R. Solid State Nuclear Magnetic Resonance, Vol. 10, Issue 1-2 https://doi.org/10.1016/S0926-2040(97)00024-6	journal	December 1997
Structure and Lipid Interaction of N-Palmitoylsphingomyelin in Bilayer Membranes as Revealed by 2H-NMR Spectroscopy Mehnert, Thomas; Jacob, Kochurani; Bittman, Robert Biophysical Journal, Vol. 90, Issue 3 https://doi.org/10.1529/biophysj.105.063271	journal	February 2006
Continuous distribution model for the investigation of complex molecular architectures near interfaces with scattering techniques Shekhar, Prabhanshu; Nanda, Hirsh; Lösche, Mathias Journal of Applied Physics, Vol. 110, Issue 10 https://doi.org/10.1063/1.3661986	journal	November 2011
The component group structure of DPPC bilayers obtained by specular neutron reflectometry Belička, Michal; Gerelli, Yuri; Kučerka, Norbert Soft Matter, Vol. 11, Issue 31 https://doi.org/10.1039/C5SM00274E	journal	January 2015
Global small-angle X-ray scattering data analysis for multilamellar vesicles: the evolution of the scattering density profile model Heftberger, Peter; Kollmitzer, Benjamin; Heberle, Frederick A. Journal of Applied Crystallography, Vol. 47, Issue 1 https://doi.org/10.1107/S1600576713029798	journal	December 2013
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
Cholesterol Promotes Protein Binding by Affecting Membrane Electrostatics and Solvation Properties Doktorova, Milka; Heberle, Frederick A.; Kingston, Richard L. Biophysical Journal, Vol. 113, Issue 9 https://doi.org/10.1016/j.bpj.2017.08.055	journal	November 2017
Resolving the structural interactions between antimicrobial peptides and lipid membranes using small-angle scattering methods: the case of indolicidin Nielsen, Josefine Eilsø; Bjørnestad, Victoria Ariel; Lund, Reidar Soft Matter, Vol. 14, Issue 43 https://doi.org/10.1039/C8SM01888J	journal	January 2018
Selective Interaction of Colistin with Lipid Model Membranes Dupuy, Fernando G.; Pagano, Isabella; Andenoro, Kathryn Biophysical Journal, Vol. 114, Issue 4 https://doi.org/10.1016/j.bpj.2017.12.027	journal	February 2018
Hydroperoxide and carboxyl groups preferential location in oxidized biomembranes experimentally determined by small angle X-ray scattering: Implications in membrane structure Rosa, Raffaela De; Spinozzi, Francesco; Itri, Rosangela Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1860, Issue 11 https://doi.org/10.1016/j.bbamem.2018.05.011	journal	November 2018
Scattering Density Profile Model of POPG Bilayers As Determined by Molecular Dynamics Simulations and Small-Angle Neutron and X-ray Scattering Experiments Kučerka, Norbert; Holland, Bryan W.; Gray, Chris G. The Journal of Physical Chemistry B, Vol. 116, Issue 1 https://doi.org/10.1021/jp208920h	journal	December 2011
Interactions between Ether Phospholipids and Cholesterol As Determined by Scattering and Molecular Dynamics Simulations Pan, Jianjun; Cheng, Xiaolin; Heberle, Frederick A. The Journal of Physical Chemistry B, Vol. 116, Issue 51 https://doi.org/10.1021/jp310345j	journal	December 2012
The structures of polyunsaturated lipid bilayers by joint refinement of neutron and X-ray scattering data Marquardt, Drew; Heberle, Frederick A.; Pan, Jianjun Chemistry and Physics of Lipids, Vol. 229 https://doi.org/10.1016/j.chemphyslip.2020.104892	journal	July 2020
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
The Affinity of Sterols for Different Phospholipid Classes and Its Impact on Lateral Segregation Nyholm, Thomas K. M.; Jaikishan, Shishir; Engberg, Oskar Biophysical Journal, Vol. 116, Issue 2 https://doi.org/10.1016/j.bpj.2018.11.3135	journal	January 2019
Miscibility Phase Diagrams of Giant Vesicles Containing Sphingomyelin Veatch, Sarah L.; Keller, Sarah L. Physical Review Letters, Vol. 94, Issue 14 https://doi.org/10.1103/PhysRevLett.94.148101	journal	April 2005
Phase behavior and domain size in sphingomyelin-containing lipid bilayers Petruzielo, Robin S.; Heberle, Frederick A.; Drazba, Paul Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 4 https://doi.org/10.1016/j.bbamem.2013.01.007	journal	April 2013
The Effect of Membrane Lipid Composition on the Formation of Lipid Ultrananodomains Pathak, Priyadarshini; London, Erwin Biophysical Journal, Vol. 109, Issue 8 https://doi.org/10.1016/j.bpj.2015.08.029	journal	October 2015
Sphingomyelin Stereoisomers Reveal That Homophilic Interactions Cause Nanodomain Formation Yano, Yo; Hanashima, Shinya; Yasuda, Tomokazu Biophysical Journal, Vol. 116, Issue 8 https://doi.org/10.1016/j.bpj.2019.03.031	journal	April 2019
N -Palmitoyl Sphingomyelin Bilayers: Structure and Interactions with Cholesterol and Dipalmitoylphosphatidylcholine Maulik, P. R.; Shipley, G. G. Biochemistry, Vol. 35, Issue 24 https://doi.org/10.1021/bi9528356	journal	January 1996
Structure and thermotropic properties of hydrated N-stearoyl sphingomyelin bilayer membranes Maulik, P. R.; Sripada, P. K.; Shipley, G. G. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1062, Issue 2 https://doi.org/10.1016/0005-2736(91)90395-O	journal	February 1991
X-ray diffraction and calorimetric study of N-lignoceryl sphingomyelin membranes Maulik, P. R.; Shipley, G. G. Biophysical Journal, Vol. 69, Issue 5 https://doi.org/10.1016/S0006-3495(95)80061-5	journal	November 1995
Revisiting Volumes of Lipid Components in Bilayers Nagle, John F.; Venable, Richard M.; Maroclo-Kemmerling, Ezekiel The Journal of Physical Chemistry B, Vol. 123, Issue 12 https://doi.org/10.1021/acs.jpcb.8b12010	journal	March 2019
Determination of bending rigidity and tilt modulus of lipid membranes from real-space fluctuation analysis of molecular dynamics simulations Doktorova, M.; Harries, D.; Khelashvili, G. Physical Chemistry Chemical Physics, Vol. 19, Issue 25 https://doi.org/10.1039/C7CP01921A	journal	January 2017
Phase behavior of palmitoyl and egg sphingomyelin Arsov, Zoran; González-Ramírez, Emilio J.; Goñi, Felix M. Chemistry and Physics of Lipids, Vol. 213 https://doi.org/10.1016/j.chemphyslip.2018.03.003	journal	July 2018
Structure of gel phase saturated lecithin bilayers: temperature and chain length dependence Sun, W. J.; Tristram-Nagle, S.; Suter, R. M. Biophysical Journal, Vol. 71, Issue 2 https://doi.org/10.1016/S0006-3495(96)79290-1	journal	August 1996
Structure and Dynamics of Sphingomyelin Bilayer: Insight Gained through Systematic Comparison to Phosphatidylcholine Niemelä, Perttu; Hyvönen, Marja T.; Vattulainen, Ilpo Biophysical Journal, Vol. 87, Issue 5 https://doi.org/10.1529/biophysj.104.048702	journal	November 2004
Mixing Properties of Sphingomyelin Ceramide Bilayers: A Simulation Study Metcalf, Rainer; Pandit, Sagar A. The Journal of Physical Chemistry B, Vol. 116, Issue 15 https://doi.org/10.1021/jp212325e	journal	April 2012
Another Piece of the Membrane Puzzle: Extending Slipids Further Jämbeck, Joakim P. M.; Lyubartsev, Alexander P. Journal of Chemical Theory and Computation, Vol. 9, Issue 1 https://doi.org/10.1021/ct300777p	journal	October 2012
Structure of Sphingomyelin Bilayers: A Simulation Study Chiu, S. W.; Vasudevan, S.; Jakobsson, Eric Biophysical Journal, Vol. 85, Issue 6 https://doi.org/10.1016/S0006-3495(03)74780-8	journal	December 2003
Impact of amphiphilic molecules on the structure and stability of homogeneous sphingomyelin bilayer: Insights from atomistic simulations Kumari, Pratibha; Kaur, Supreet; Sharma, Shobha The Journal of Chemical Physics, Vol. 148, Issue 16 https://doi.org/10.1063/1.5021310	journal	April 2018
Method for obtaining structure and interactions from oriented lipid bilayers Lyatskaya, Yulia; Liu, Yufeng; Tristram-Nagle, Stephanie Physical Review E, Vol. 63, Issue 1 https://doi.org/10.1103/PhysRevE.63.011907	journal	December 2000
Applications of neutron and X-ray scattering to the study of biologically relevant model membranes Pabst, G.; Kučerka, N.; Nieh, M. -P. Chemistry and Physics of Lipids, Vol. 163, Issue 6 https://doi.org/10.1016/j.chemphyslip.2010.03.010	journal	June 2010
Theory of spin‐lattice relaxation in lipid bilayers and biological membranes. ² H and ¹⁴ N quadrupolar relaxation Brown, Michael F. The Journal of Chemical Physics, Vol. 77, Issue 3 https://doi.org/10.1063/1.443940	journal	August 1982
Computational Modeling of Realistic Cell Membranes Marrink, Siewert J.; Corradi, Valentina; Souza, Paulo C. T. Chemical Reviews, Vol. 119, Issue 9 https://doi.org/10.1021/acs.chemrev.8b00460	journal	January 2019
The intrinsic structural asymmetry of highly curved phospholipid bilayer membranes Chrzeszczyk, Adela; Wishnia, Arnold; Springer, Charles S. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 470, Issue 2 https://doi.org/10.1016/0005-2736(77)90097-9	journal	October 1977
NMR studies on phospholipid bilayers. Some factors affecting lipid distribution Berden, Jan A.; Barker, Richard W.; Radda, George K. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 375, Issue 2 https://doi.org/10.1016/0005-2736(75)90188-1	journal	January 1975
An extensive simulation study of lipid bilayer properties with different head groups, acyl chain lengths, and chain saturations Zhuang, Xiaohong; Dávila-Contreras, Eder M.; Beaven, Andrew H. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 12 https://doi.org/10.1016/j.bbamem.2016.09.016	journal	December 2016
A systematic molecular dynamics simulation study of temperature dependent bilayer structural properties Zhuang, Xiaohong; Makover, Judah R.; Im, Wonpil Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1838, Issue 10 https://doi.org/10.1016/j.bbamem.2014.06.010	journal	October 2014
Comparison of Additive and Polarizable Models with Explicit Treatment of Long-Range Lennard-Jones Interactions Using Alkane Simulations Leonard, Alison N.; Simmonett, Andrew C.; Pickard, Frank C. Journal of Chemical Theory and Computation, Vol. 14, Issue 2 https://doi.org/10.1021/acs.jctc.7b00948	journal	January 2018
Characterization of the Ternary Mixture of Sphingomyelin, POPC, and Cholesterol: Support for an Inhomogeneous Lipid Distribution at High Temperatures Bunge, Andreas; Müller, Peter; Stöckl, Martin Biophysical Journal, Vol. 94, Issue 7 https://doi.org/10.1529/biophysj.107.112904	journal	April 2008

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Title: Molecular Structure of Sphingomyelin in Fluid Phase Bilayers Determined by the Joint Analysis of Small-Angle Neutron and X-ray Scattering Data

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