The in vivo structure of biological membranes and evidence for lipid domains

Nickels, Jonathan D.; Chatterjee, Sneha; Stanley, Christopher B.; Qian, Shuo; Cheng, Xiaolin; Myles, Dean A.  A.; Standaert, Robert F.; Elkins, James G.; Katsaras, John; Lopez, Daniel

doi:10.1371/journal.pbio.2002214

Title: The in vivo structure of biological membranes and evidence for lipid domains

Journal Article · Tue May 23 00:00:00 EDT 2017 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.2002214· OSTI ID:1362249

Nickels, Jonathan D. ^[1]; Chatterjee, Sneha ^[2]; Stanley, Christopher B. ^[3]; Qian, Shuo ^[3]; Cheng, Xiaolin ^[4]; Myles, Dean A. A. ^[3]; Standaert, Robert F. ^[5]; Elkins, James G. ^[6];

^[7]; Lopez, Daniel ^[8]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Shull Wollan Center - A Joint Inst. for Neutron Sciences and Biology and Soft Matter Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Physics and Astronomy
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biology and Soft Matter Division and Biosciences Division
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biology and Soft Matter Division
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Molecular Biophysics; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemistry & Cellular and Molecular Biology
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Shull Wollan Center - A Joint Inst. for Neutron Sciences and Biology, Soft Matter Division, and Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemistry & Cellular and Molecular Biology
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Shull Wollan Center - A Joint Inst. for Neutron Sciences and Biology, Soft Matter Division, and Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Physics and Astronomy
Centro Nacional de Biotecnologia, Madrid (Spain)

Examining the fundamental structure and processes of living cells at the nanoscale poses a unique analytical challenge, as cells are dynamic, chemically diverse, and fragile. A case in point is the cell membrane, which is too small to be seen directly with optical microscopy and provides little observational contrast for other methods. As a consequence, nanoscale characterization of the membrane has been performed ex vivo or in the presence of exogenous labels used to enhance contrast and impart specificity. Here, we introduce an isotopic labeling strategy in the gram-positive bacterium Bacillus subtilis to investigate the nanoscale structure and organization of its plasma membrane in vivo. Through genetic and chemical manipulation of the organism, we labeled the cell and its membrane independently with specific amounts of hydrogen (H) and deuterium (D). These isotopes have different neutron scattering properties without altering the chemical composition of the cells. From neutron scattering spectra, we confirmed that the B. subtilis cell membrane is lamellar and determined that its average hydrophobic thickness is 24.3 ± 0.9 Ångstroms (Å). Furthermore, by creating neutron contrast within the plane of the membrane using a mixture of H- and D-fatty acids, we detected lateral features smaller than 40 nm that are consistent with the notion of lipid rafts. These experiments—performed under biologically relevant conditions—answer long-standing questions in membrane biology and illustrate a fundamentally new approach for systematic in vivo investigations of cell membrane structure.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1362249

Journal Information:: PLoS Biology (Online), Vol. 15, Issue 5; ISSN 1545-7885

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 102 works

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References (77)

Lateral organization, bilayer asymmetry, and inter-leaflet coupling of biological membranes Nickels, Jonathan D.; Smith, Jeremy C.; Cheng, Xiaolin Chemistry and Physics of Lipids, Vol. 192 https://doi.org/10.1016/j.chemphyslip.2015.07.012	journal	November 2015
Mechanical Properties of Nanoscopic Lipid Domains Nickels, Jonathan D.; Cheng, Xiaolin; Mostofian, Barmak Journal of the American Chemical Society, Vol. 137, Issue 50 https://doi.org/10.1021/jacs.5b08894	journal	October 2015
Cardiolipin Domains in Bacillus subtilis Marburg Membranes Kawai, F.; Shoda, M.; Harashima, R. Journal of Bacteriology, Vol. 186, Issue 5 https://doi.org/10.1128/JB.186.5.1475-1483.2004	journal	February 2004
Bilayer thickness and lipid interface area in unilamellar extruded 1,2-diacylphosphatidylcholine liposomes: a small-angle neutron scattering study Balgavý, Pavol; Dubničková, Martina; Kučerka, Norbert Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1512, Issue 1 https://doi.org/10.1016/S0005-2736(01)00298-X	journal	May 2001
Evaluation of extraction methods for recovery of fatty acids from lipid-producing microheterotrophs Lewis, Tom; Nichols, Peter D.; McMeekin, Tom A. Journal of Microbiological Methods, Vol. 43, Issue 2 https://doi.org/10.1016/S0167-7012(00)00217-7	journal	December 2000
The study of biological structures by neutron scattering from solution Jacrot, B. Reports on Progress in Physics, Vol. 39, Issue 10 https://doi.org/10.1088/0034-4885/39/10/001	journal	October 1976
Visualization of Phospholipid Domains in Escherichia coli by Using the Cardiolipin-Specific Fluorescent Dye 10-N-Nonyl Acridine Orange Mileykovskaya, E.; Dowhan, W. Journal of Bacteriology, Vol. 182, Issue 4 https://doi.org/10.1128/JB.182.4.1172-1175.2000	journal	February 2000
Lipid rafts: at a crossroad between cell biology and physics Jacobson, Ken; Mouritsen, Ole G.; Anderson, Richard G. W. Nature Cell Biology, Vol. 9, Issue 1 https://doi.org/10.1038/ncb0107-7	journal	January 2007
Models to analyze small-angle neutron scattering from unilamellar lipid vesicles Kučerka, Norbert; Nagle, John F.; Feller, Scott E. Physical Review E, Vol. 69, Issue 5 https://doi.org/10.1103/PhysRevE.69.051903	journal	May 2004
Structure of lipid bilayers Nagle, John F.; Tristram-Nagle, Stephanie Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 1469, Issue 3 https://doi.org/10.1016/S0304-4157(00)00016-2	journal	November 2000
Numerical Analysis of Fatty Acid Profiles in the Identification of Staphylococci O'Donnell, A. G.; Nahaie, M. R.; Goodfellow, M. Microbiology, Vol. 131, Issue 8 https://doi.org/10.1099/00221287-131-8-2023	journal	August 1985
Area per Lipid and Acyl Length Distributions in Fluid Phosphatidylcholines Determined by 2H NMR Spectroscopy Petrache, Horia I.; Dodd, Steven W.; Brown, Michael F. Biophysical Journal, Vol. 79, Issue 6 https://doi.org/10.1016/S0006-3495(00)76551-9	journal	December 2000
Preparation of fatty acid methyl esters for gas-liquid chromatography Ichihara, Ken'ichi; Fukubayashi, Yumeto Journal of Lipid Research, Vol. 51, Issue 3 https://doi.org/10.1194/jlr.D001065	journal	September 2009
Bilayer Thickness Mismatch Controls Domain Size in Model Membranes Heberle, Frederick A.; Petruzielo, Robin S.; Pan, Jianjun Journal of the American Chemical Society, Vol. 135, Issue 18 https://doi.org/10.1021/ja3113615	journal	February 2013
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
Spin labels as enzyme substrates Heterogeneous lipid distribution in liver microsomal membranes Stier, A.; Sackmann, E. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 311, Issue 3 https://doi.org/10.1016/0005-2736(73)90320-9	journal	July 1973
Predictable Deuteration of Recombinant Proteins Expressed inEscherichia coli Leiting, Barbara; Marsilio, Frank; O'Connell, John F. Analytical Biochemistry, Vol. 265, Issue 2 https://doi.org/10.1006/abio.1998.2904	journal	December 1998
Neutron scattering lengths and cross sections Sears, Varley F. Neutron News, Vol. 3, Issue 3 https://doi.org/10.1080/10448639208218770	journal	January 1992
Reversible membrane reorganizations during photosynthesis in vivo: revealed by small-angle neutron scattering Nagy, Gergely; Posselt, Dorthe; Kovács, László Biochemical Journal, Vol. 436, Issue 2 https://doi.org/10.1042/BJ20110180	journal	May 2011
Cholesterol Lipids of Borrelia burgdorferi Form Lipid Rafts and Are Required for the Bactericidal Activity of a Complement-Independent Antibody LaRocca, Timothy J.; Crowley, Jameson T.; Cusack, Brian J. Cell Host & Microbe, Vol. 8, Issue 4 https://doi.org/10.1016/j.chom.2010.09.001	journal	October 2010
Cholesterol, lipid rafts, and disease Simons, Kai; Ehehalt, Robert Journal of Clinical Investigation, Vol. 110, Issue 5 https://doi.org/10.1172/JCI0216390	journal	September 2002
Flotillins functionally organize the bacterial membrane: Flotillin-mediated membrane organization Bach, Juri Niño; Bramkamp, Marc Molecular Microbiology, Vol. 88, Issue 6 https://doi.org/10.1111/mmi.12252	journal	May 2013
Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol Mitra, K.; Ubarretxena-Belandia, I.; Taguchi, T. Proceedings of the National Academy of Sciences, Vol. 101, Issue 12 https://doi.org/10.1073/pnas.0307332101	journal	March 2004
The extended Q -range small-angle neutron scattering diffractometer at the SNS Zhao, J. K.; Gao, C. Y.; Liu, D. Journal of Applied Crystallography, Vol. 43, Issue 5 https://doi.org/10.1107/S002188981002217X	journal	July 2010
Neutron Diffraction Studies on the Location of Water in Lecithin Bilayer Model Membranes Zaccai, G.; Blasie, J. K.; Schoenborn, B. P. Proceedings of the National Academy of Sciences, Vol. 72, Issue 1 https://doi.org/10.1073/pnas.72.1.376	journal	January 1975
Potentials of Small-angle Neutron Scattering for Studies of the Structure of “Live” Mitochondria Murugova, T. N.; Solodovnikova, I. M.; Yurkov, V. I. Neutron News, Vol. 22, Issue 3 https://doi.org/10.1080/10448632.2011.598800	journal	July 2011
Lipid bilayer structure in the membrane of Mycoplasma laidlawii Engelman, Donald M. Journal of Molecular Biology, Vol. 58, Issue 1 https://doi.org/10.1016/0022-2836(71)90238-5	journal	May 1971
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Synthesis of per-deuterated alkyl amines for the preparation of deuterated organic pyromellitamide gelators Yepuri, Nageshwar R.; Jamieson, Scott A.; Darwish, Tamim A. Tetrahedron Letters, Vol. 54, Issue 20 https://doi.org/10.1016/j.tetlet.2013.03.031	journal	May 2013
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
Lipid Asymmetry in Membranes Op den Kamp, J. A. F. Annual Review of Biochemistry, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.bi.48.070179.000403	journal	June 1979
Lipid domains in bacterial membranes Matsumoto, Kouji; Kusaka, Jin; Nishibori, Ayako Molecular Microbiology, Vol. 61, Issue 5 https://doi.org/10.1111/j.1365-2958.2006.05317.x	journal	September 2006
Lipid rafts: now you see them, now you don't Shaw, Andrey S. Nature Immunology, Vol. 7, Issue 11 https://doi.org/10.1038/ni1405	journal	November 2006
Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space: Gram-positive cell walls and periplasm shown by cryo-TEM Matias, Valério R. F.; Beveridge, Terry J. Molecular Microbiology, Vol. 56, Issue 1 https://doi.org/10.1111/j.1365-2958.2005.04535.x	journal	February 2005
The State of Lipid Rafts: From Model Membranes to Cells Edidin, Michael Annual Review of Biophysics and Biomolecular Structure, Vol. 32, Issue 1 https://doi.org/10.1146/annurev.biophys.32.110601.142439	journal	June 2003
X-ray diffraction studies of phase transitions in the membrane of Mycoplasma laidlawii Engelman, Donald M. Journal of Molecular Biology, Vol. 47, Issue 1 https://doi.org/10.1016/0022-2836(70)90407-9	journal	January 1970
Lipid conformation in model membranes and biological membranes Seelig, Joachim; Seelig, Anna Quarterly Reviews of Biophysics, Vol. 13, Issue 1 https://doi.org/10.1017/S0033583500000305	journal	February 1980
The energized membrane and cellular autolysis in Bacillus subtilis Jolliffe, Linda K.; Doyle, Ronald J.; Streips, Uldis N. Cell, Vol. 25, Issue 3 https://doi.org/10.1016/0092-8674(81)90183-5	journal	September 1981
An analysis of lamellar x-ray diffraction from disordered membrane multilayers with application to data from retinal rod outer segments Schwartz, S.; Cain, J. E.; Dratz, E. A. Biophysical Journal, Vol. 15, Issue 12 https://doi.org/10.1016/S0006-3495(75)85895-4	journal	December 1975
Copper catalyzed reaction of Grignard reagents with chloromagnesium salts of -bromoacids Baer, Ted A.; Carney, Robert L. Tetrahedron Letters, Vol. 17, Issue 51 https://doi.org/10.1016/S0040-4039(00)92999-X	journal	December 1976
GC-MS Analysis of Amino Acids Rapidly Provides Rich Information for Isotopomer Balancing Dauner, M.; Sauer, U. Biotechnology Progress, Vol. 16, Issue 4 https://doi.org/10.1021/bp000058h	journal	August 2000
The Chemical Composition of the Cytoplasmic Membrane of Bacillus subtilis Bishop, D. G.; Rutberg, L.; Samuelsson, B. European Journal of Biochemistry, Vol. 2, Issue 4 https://doi.org/10.1111/j.1432-1033.1967.tb00158.x	journal	November 1967
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
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
Three-dimensional model of purple membrane obtained by electron microscopy Henderson, R.; Unwin, P. N. T. Nature, Vol. 257, Issue 5521 https://doi.org/10.1038/257028a0	journal	September 1975
Autolysis of Bacillus subtilis induced by monovalent cations Svarachorn, Ancharida; Shinmyo, Atsuhiko; Tsuchido, Tetsuaki Applied Microbiology and Biotechnology, Vol. 30, Issue 3 https://doi.org/10.1007/BF00256222	journal	March 1989
Organization and Flexibility of Cyanobacterial Thylakoid Membranes Examined by Neutron Scattering Liberton, Michelle; Page, Lawrence E.; O'Dell, William B. Journal of Biological Chemistry, Vol. 288, Issue 5 https://doi.org/10.1074/jbc.M112.416933	journal	December 2012
Membrane Domains Mukherjee, Sushmita; Maxfield, Frederick R. Annual Review of Cell and Developmental Biology, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.cellbio.20.010403.095451	journal	November 2004
Functional microdomains in bacterial membranes Lopez, D.; Kolter, R. Genes & Development, Vol. 24, Issue 17 https://doi.org/10.1101/gad.1945010	journal	August 2010
Direct observation of the nanoscale dynamics of membrane lipids in a living cell Eggeling, Christian; Ringemann, Christian; Medda, Rebecca Nature, Vol. 457, Issue 7233 https://doi.org/10.1038/nature07596	journal	December 2008
Lipid rafts and signal transduction Simons, Kai; Toomre, Derek Nature Reviews Molecular Cell Biology, Vol. 1, Issue 1 https://doi.org/10.1038/35036052	journal	October 2000
Detection of submicron-sized raft-like domains in membranes by small-angle neutron scattering Pencer, J.; Mills, T.; Anghel, V. The European Physical Journal E, Vol. 18, Issue 4 https://doi.org/10.1140/epje/e2005-00046-5	journal	November 2005
Organization and Function of the YsiA Regulon of Bacillus subtilis Involved in Fatty Acid Degradation Matsuoka, Hiroshi; Hirooka, Kazutake; Fujita, Yasutaro Journal of Biological Chemistry, Vol. 282, Issue 8 https://doi.org/10.1074/jbc.M606831200	journal	December 2006
Exploring the Existence of Lipid Rafts in Bacteria Bramkamp, Marc; Lopez, Daniel Microbiology and Molecular Biology Reviews, Vol. 79, Issue 1 https://doi.org/10.1128/MMBR.00036-14	journal	February 2015
Functional rafts in cell membranes Simons, Kai; Ikonen, Elina Nature, Vol. 387, Issue 6633 https://doi.org/10.1038/42408	journal	June 1997
Characterization and subcellular localization of a bacterial flotillin homologue Donovan, C.; Bramkamp, M. Microbiology, Vol. 155, Issue 6 https://doi.org/10.1099/mic.0.025312-0	journal	April 2009
Hopanoids as functional analogues of cholesterol in bacterial membranes Sáenz, James P.; Grosser, Daniel; Bradley, Alexander S. Proceedings of the National Academy of Sciences, Vol. 112, Issue 38 https://doi.org/10.1073/pnas.1515607112	journal	September 2015
Lipid raft microdomains and neurotransmitter signalling Allen, John A.; Halverson-Tamboli, Robyn A.; Rasenick, Mark M. Nature Reviews Neuroscience, Vol. 8, Issue 2 https://doi.org/10.1038/nrn2059	journal	December 2006
Bio-SANS—A dedicated facility for neutron structural biology at Oak Ridge National Laboratory Lynn, G. W.; Heller, William; Urban, Volker Physica B: Condensed Matter, Vol. 385-386 https://doi.org/10.1016/j.physb.2006.05.133	journal	November 2006
The Fluid Mosaic Model of the Structure of Cell Membranes Singer, S. J.; Nicolson, G. L. Science, Vol. 175, Issue 4023 https://doi.org/10.1126/science.175.4023.720	journal	February 1972
The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy Verkleij, A. J.; Zwaal, R. F. A.; Roelofsen, B. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 323, Issue 2 https://doi.org/10.1016/0005-2736(73)90143-0	journal	October 1973
Inhibition of β-Ketoacyl-Acyl Carrier Protein Synthases by Thiolactomycin and Cerulenin: STRUCTURE AND MECHANISM Price, Allen C.; Choi, Keum-Hwa; Heath, Richard J. Journal of Biological Chemistry, Vol. 276, Issue 9 https://doi.org/10.1074/jbc.M007101200	journal	October 2000
On scattered waves and lipid domains: detecting membrane rafts with X-rays and neutrons Marquardt, Drew; Heberle, Frederick A.; Nickels, Jonathan D. Soft Matter, Vol. 11, Issue 47 https://doi.org/10.1039/C5SM01807B	journal	January 2015
Neutron scattering: a tool to detect in vivo thermal stress effects at the molecular dynamics level in micro-organisms Marty, Vincent; Jasnin, Marion; Fabiani, Elisa Journal of The Royal Society Interface, Vol. 10, Issue 82 https://doi.org/10.1098/rsif.2013.0003	journal	May 2013
A Rapid Method of Total Lipid Extraction and Purification Bligh, E. G.; Dyer, W. J. Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 8 https://doi.org/10.1139/o59-099	journal	August 1959
The separate profile structures of the functional calcium pump protein and the phospholipid bilayer within isolated sarcoplasmic reticulum membranes determined by X-ray and neutron diffraction Herbette, L.; DeFoor, P.; Fleischer, S. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 817, Issue 1 https://doi.org/10.1016/0005-2736(85)90073-2	journal	July 1985
Functions of Lipid Rafts in Biological Membranes Brown, D. A.; London, E. Annual Review of Cell and Developmental Biology, Vol. 14, Issue 1 https://doi.org/10.1146/annurev.cellbio.14.1.111	journal	November 1998
Phospholipid Composition of Bacillus subtilis den Kamp, J. A. F. Op; Redai, I.; van Deenen, L. L. M. Journal of Bacteriology, Vol. 99, Issue 1 https://doi.org/10.1128/JB.99.1.298-303.1969	journal	January 1969
Lipid Rafts McIntosh, Thomas J. Methods in Molecular Biology https://doi.org/10.1007/978-1-59745-513-8	book	January 2007
Cholesterol, lipid rafts, and disease Simons, Kai; Ehehalt, Robert Journal of Clinical Investigation, Vol. 110, Issue 5 https://doi.org/10.1172/jci200216390	journal	September 2002
Bilayer Thickness Mismatch Controls Domain Size in Model Membranes Heberle, Frederick A.; Petruzielo, Robin S.; Pan, Jianjun Biophysical Journal, Vol. 106, Issue 2 https://doi.org/10.1016/j.bpj.2013.11.1686	journal	January 2014
Molecular dynamics of the histamine H3 membrane receptor reveals different mechanisms of GPCR signal transduction Herrera-Zúñiga, Leonardo David; Moreno-Vargas, Liliana Marisol; Ballaud, Luck Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-73483-5	journal	October 2020
Cholesterol, lipid rafts, and disease Simons, Kai; Ehehalt, Robert Journal of Clinical Investigation, Vol. 110, Issue 5 https://doi.org/10.1172/JCI16390	journal	September 2002
Structure of lipid bilayers Nagle, John F.; Tristram-Nagle, Stephanie Carnegie Mellon University https://doi.org/10.1184/r1/6509243.v1	text	January 2000
Lipid conformation in model membranes and biological membranes Seelig, J.; Seelig, A. Cambridge University Press https://doi.org/10.5451/unibas-ep2181	text	January 1980
A Rapid Method of Total Lipid Extraction and Purification Bligh, E. G.; Dyer, W. J. Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 1 https://doi.org/10.1139/y59-099	journal	January 1959
Bilayer Structure in Membranes Wilkins, M. H. F.; Blaurock, A. E.; Engelman, D. M. Nature New Biology, Vol. 230, Issue 11 https://doi.org/10.1038/newbio230072a0	journal	March 1971

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