Cholesterol's location in lipid bilayers

Marquardt, Drew; Kučerka, Norbert; Wassall, Stephen R.; Harroun, Thad A.; Katsaras, John

doi:10.1016/j.chemphyslip.2016.04.001

Title: Cholesterol's location in lipid bilayers

Abstract

It is well known that cholesterol modifies the physical properties of lipid bilayers. For example, the much studied liquid-ordered L_o phase contains rapidly diffusing lipids with their acyl chains in the all trans configuration, similar to gel phase bilayers. Moreover, the L_o phase is commonly associated with cholesterol-enriched lipid rafts, which are thought to serve as platforms for signaling proteins in the plasma membrane. Cholesterol's location in lipid bilayers has been studied extensively, and it has been shown – at least in some bilayers – to align differently from its canonical upright orientation, where its hydroxyl group is in the vicinity of the lipid–water interface. In this study we review recent works describing cholesterol's location in different model membrane systems with emphasis on results obtained from scattering, spectroscopic and molecular dynamics studies.

Authors:

Marquardt, Drew ^[1]; Kučerka, Norbert ^[2]; Wassall, Stephen R. ^[3]; Harroun, Thad A. ^[4]; Katsaras, John ^[5]

Univ. of Graz, Graz (Austria); BioTechMed-Graz (Austria)
Joint Institute for Nuclear Research, Dubna (Moscow); Comenius Univ., Bratislava (Slovakia)
Indiana Univ. Purdue Univ. Indianapolis, Indianapolis, IN (United States)
Brock Univ., St. Catharines, ON (Canada)
Brock Univ., St. Catharines, ON (Canada); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Joint Institute for Neutron Sciences, Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)

Publication Date:: Mon Apr 04 00:00:00 EDT 2016

Research Org.:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1324179

Alternate Identifier(s):: OSTI ID: 1396442

Grant/Contract Number:: AC05-00OR22725

Resource Type:: Accepted Manuscript

Journal Name:: Chemistry and Physics of Lipids

Additional Journal Information:: Journal Volume: 199; Journal Issue: C; Journal ID: ISSN 0009-3084

Publisher:: Elsevier

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; biomembranes; cholesterol; neutron scattering; sterol; membrane dynamics; membrane structure; lipid domains

Citation Formats


                    Marquardt, Drew, Kučerka, Norbert, Wassall, Stephen R., Harroun, Thad A., and Katsaras, John. Cholesterol's location in lipid bilayers.  United States: N. p., 2016. 
Web.  doi:10.1016/j.chemphyslip.2016.04.001.

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                    Marquardt, Drew, Kučerka, Norbert, Wassall, Stephen R., Harroun, Thad A., & Katsaras, John. Cholesterol's location in lipid bilayers.  United States.  https://doi.org/10.1016/j.chemphyslip.2016.04.001

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                    Marquardt, Drew, Kučerka, Norbert, Wassall, Stephen R., Harroun, Thad A., and Katsaras, John. Mon .  
"Cholesterol's location in lipid bilayers".  United States.  https://doi.org/10.1016/j.chemphyslip.2016.04.001.  https://www.osti.gov/servlets/purl/1324179.

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@article{osti_1324179,

  title        = {Cholesterol's location in lipid bilayers},

  author       = {Marquardt, Drew and Kučerka, Norbert and Wassall, Stephen R. and Harroun, Thad A. and Katsaras, John},

  abstractNote = {It is well known that cholesterol modifies the physical properties of lipid bilayers. For example, the much studied liquid-ordered Lo phase contains rapidly diffusing lipids with their acyl chains in the all trans configuration, similar to gel phase bilayers. Moreover, the Lo phase is commonly associated with cholesterol-enriched lipid rafts, which are thought to serve as platforms for signaling proteins in the plasma membrane. Cholesterol's location in lipid bilayers has been studied extensively, and it has been shown – at least in some bilayers – to align differently from its canonical upright orientation, where its hydroxyl group is in the vicinity of the lipid–water interface. In this study we review recent works describing cholesterol's location in different model membrane systems with emphasis on results obtained from scattering, spectroscopic and molecular dynamics studies.},

  doi          = {10.1016/j.chemphyslip.2016.04.001},

  journal      = {Chemistry and Physics of Lipids},

  number       = C,

  volume       = 199,

  place        = {United States},

  year         = {Mon Apr 04 00:00:00 EDT 2016},

  month        = {Mon Apr 04 00:00:00 EDT 2016}

}

Copy to clipboard

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Fig. 1: (a) The structure of cholesterol showing its steroid skeleton of four fused rings, and its fatty acid tail. Molecular dimensions were taken from Marquardt et al. (2015d), Kucerka et al. (2008). (b) Schematic showing differences between the molecule’s α- and β-faces. Hydrogen atoms are not shown for bettermore »

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Biophysical Journal, Vol. 83, Issue 4
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Physical properties of lipid bilayers from EPR spin labeling and their influence on chemical reactions in a membrane environment
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Subczynski, Witold K.; Widomska, Justyna; Feix, Jimmy B.
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Tieleman, D. Peter; Marrink, Siewert-Jan
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Structure of Cholesterol in Lipid Rafts
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Toppozini, Laura; Meinhardt, Sebastian; Armstrong, Clare L.
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Vitamin E, antioxidant and nothing more
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Traber, Maret G.; Atkinson, Jeffrey
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Seeing spots: Complex phase behavior in simple membranes
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Veatch, Sarah L.; Keller, Sarah L.
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Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: deuterium nuclear magnetic resonance and differential scanning calorimetry
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Docosahexaenoic acid domains: the ultimate non-raft membrane domain
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Wassall, Stephen R.; Stillwell, William
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Cholesterol Depletion Results in Site-specific Increases in Epidermal Growth Factor Receptor Phosphorylation due to Membrane Level Effects
journal, December 2003

Westover, Emily J.; Covey, Douglas F.; Brockman, Howard L.
Journal of Biological Chemistry, Vol. 278, Issue 51
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Dependence of Cholesterol-Phospholipid Affinity on Degree of Acyl Chain Unsaturation as Determined by EPR
journal, January 2013

Williams, Justin; Wassall, Cynthia D.; Kemple, Marvin D.
Biophysical Journal, Vol. 104, Issue 2
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Cholesterol asymmetry in synaptic plasma membranes: Brain membrane cholesterol asymmetry
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Gibson Wood, W.; Igbavboa, Urule; Müller, Walter E.
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Worcester, D. L.; Franks, N. P.
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Detailed Comparison of Deuterium Quadrupole Profiles between Sphingomyelin and Phosphatidylcholine Bilayers
journal, February 2014

Yasuda, Tomokazu; Kinoshita, Masanao; Murata, Michio
Biophysical Journal, Vol. 106, Issue 3
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How cholesterol is distributed between monolayers in asymmetric lipid membranes
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Yesylevskyy, Semen O.; Demchenko, Alexander P.
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Works referencing / citing this record:

Two sterols, two bilayers: insights on membrane structure from molecular dynamics
text, January 2017

Monje-Galvan, Viviana; Klauda, Jeffery B.
Taylor & Francis
DOI: 10.6084/m9.figshare.5224453.v1

Cholesterol in phospholipid bilayers: positions and orientations inside membranes with different unsaturation degrees
journal, January 2019

Ermilova, Inna; Lyubartsev, Alexander P.
Soft Matter, Vol. 15, Issue 1
DOI: 10.1039/c8sm01937a

The asymmetry of plasma membranes and their cholesterol content influence the uptake of cisplatin
journal, April 2019

Rivel, Timothée; Ramseyer, Christophe; Yesylevskyy, Semen
Scientific Reports, Vol. 9, Issue 1
DOI: 10.1038/s41598-019-41903-w

Anandamide Revisited: How Cholesterol and Ceramides Control Receptor-Dependent and Receptor-Independent Signal Transmission Pathways of a Lipid Neurotransmitter
journal, May 2018

Scala, Coralie; Fantini, Jacques; Yahi, Nouara
Biomolecules, Vol. 8, Issue 2
DOI: 10.3390/biom8020031

Drug‐induced increase in lysobisphosphatidic acid reduces the cholesterol overload in Niemann–Pick type C cells and mice
journal, April 2019

Moreau, Dimitri; Vacca, Fabrizio; Vossio, Stefania
EMBO reports, Vol. 20, Issue 7
DOI: 10.15252/embr.201847055

Structure of lateral heterogeneities in a coarse-grained model for multicomponent membranes
journal, January 2019

Meinhardt, Sebastian; Schmid, Friederike
Soft Matter, Vol. 15, Issue 9
DOI: 10.1039/c8sm02261e

Transverse distribution of plasma membrane bilayer cholesterol: Picking sides
journal, July 2018

Steck, Theodore L.; Lange, Yvonne
Traffic, Vol. 19, Issue 10
DOI: 10.1111/tra.12586

Modelling of interactions between Aβ(25–35) peptide and phospholipid bilayers: effects of cholesterol and lipid saturation
journal, January 2020

Ermilova, Inna; Lyubartsev, Alexander P.
RSC Advances, Vol. 10, Issue 7
DOI: 10.1039/c9ra06424a

Rapid diffusion of cholesterol along polyunsaturated membranes via deep dives
journal, January 2019

Javanainen, Matti; Martinez-Seara, Hector
Physical Chemistry Chemical Physics, Vol. 21, Issue 22
DOI: 10.1039/c9cp02022e

Drug-induced increase in lysobisphosphatidic acid reduces the cholesterol overload in Niemann-Pick type C cells and mice
journal, March 2019

Moreau, Dimitri; Vacca, Fabrizio; Vossio, Stefania
EMBO reports
DOI: 10.1101/416479

Molecular AFM imaging of Hsp70-1A association with dipalmitoyl phosphatidylserine reveals membrane blebbing in the presence of cholesterol
journal, February 2018

Lamprecht, Constanze; Gehrmann, Mathias; Madl, Josef
Cell Stress and Chaperones, Vol. 23, Issue 4
DOI: 10.1007/s12192-018-0879-0

In Search for the Membrane Regulators of Archaea
journal, September 2019

Salvador-Castell, Marta; Tourte, Maxime; Oger, Philippe M.
International Journal of Molecular Sciences, Vol. 20, Issue 18
DOI: 10.3390/ijms20184434

Two sterols, two bilayers: insights on membrane structure from molecular dynamics
journal, May 2017

Monje-Galvan, Viviana; Klauda, Jeffery B.
Molecular Simulation, Vol. 43, Issue 13-16
DOI: 10.1080/08927022.2017.1353690

Two sterols, two bilayers: insights on membrane structure from molecular dynamics
text, January 2017

Monje-Galvan, Viviana; Klauda, Jeffery B.
Taylor & Francis
DOI: 10.6084/m9.figshare.5224453

Drug-induced increase in lysobisphosphatidic acid reduces the cholesterol overload in Niemann-Pick type C cells and mice
journal, March 2019

Moreau, Dimitri; Vacca, Fabrizio; Vossio, Stefania
EMBO reports
DOI: 10.1101/416479

Free cholesterol and cholesterol esters in bovine oocytes: Implications in survival and membrane raft organization after cryopreservation
journal, July 2017

Buschiazzo, Jorgelina; Ríos, Glenda L.; Canizo, Jesica R.
PLOS ONE, Vol. 12, Issue 7
DOI: 10.1371/journal.pone.0180451

Anandamide Revisited: How Cholesterol and Ceramides Control Receptor-Dependent and Receptor-Independent Signal Transmission Pathways of a Lipid Neurotransmitter
journal, May 2018

Scala, Coralie; Fantini, Jacques; Yahi, Nouara
Biomolecules, Vol. 8, Issue 2
DOI: 10.3390/biom8020031

In Search for the Membrane Regulators of Archaea
journal, September 2019

Salvador-Castell, Marta; Tourte, Maxime; Oger, Philippe M.
International Journal of Molecular Sciences, Vol. 20, Issue 18
DOI: 10.3390/ijms20184434

Figures / Tables found in this record:

Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.

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Lipid bilayer thickness determines cholesterol's location in model membranes

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Cholesterol is an essential biomolecule of animal cell membranes, and an important precursor for the biosynthesis of certain hormones and vitamins. It is also thought to play a key role in cell signaling processes associated with functional plasma membrane microdomains (domains enriched in cholesterol), commonly referred to as rafts. In all of these diverse biological phenomena, the transverse location of cholesterol in the membrane is almost certainly an important structural feature. Using a combination of neutron scattering and solid-state ²H NMR, we have determined the location and orientation of cholesterol in phosphatidylcholine (PC) model membranes having fatty acids of differentmore »« less
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The influence of cholesterol on the dynamic organization of 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC) bilayers was studied by deuteron nuclear magnetic resonance ({sup 2}H NMR) using unoriented and macroscopically aligned samples. Analysis of the various temperature- and orientation-dependent experiments was performed using a comprehensive NMR model based on the stochastic Liouville equation. Computer simulations of the relaxation data obtained from phospholipids deuterated at the 6-, 13- and 14-position of the sn-2 chain and cholesterol labeled at the 3{alpha}-position of the rigid steroid ring system allowed the unambiguous assignment of the various motional modes and types of molecular order present in the system. Abovemore »« less
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Lipid raft/domain formation may arise as a result of the effects of specific sterols on the physical properties of membranes. Here, using molecular dynamics simulation, we examine the effects of three closely-related sterols, ergosterol, cholesterol, and lanosterol, at a biologically relevant concentration (40 mol %) on the structural properties of a model dipalmitoyl phosphatidylcholine (DPPC) membrane at 309 and 323 K. All three sterols are found to order the DPPC acyl tails and condense the membrane relative to the DPPC liquid-phase membrane, but each one does this to a significantly different degree. The smooth {alpha}-face of ergosterol, together with themore »« less
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Similar Records

Title: Cholesterol's location in lipid bilayers

Abstract

Citation Formats

Figures / Tables:

Tilt: Major Factor in Sterols' Ordering Capability in Membranes journal, December 2006

Bilayer Thickness and Membrane Protein Function: An Energetic Perspective journal, June 2007

Co-existence of gel and fluid lipid domains in single-component phospholipid membranes journal, January 2012

The Observation of Highly Ordered Domains in Membranes with Cholesterol journal, June 2013

Molecular mechanism of α-tocopherol action journal, July 2007

Transmembrane movement of cholesterol in small unilamellar vesicles detected by cholesterol oxidase. journal, January 1981

Raftlike Mixtures of Sphingomyelin and Cholesterol Investigated by Solid-State 2 H NMR Spectroscopy journal, October 2008

Molecular View of Cholesterol Flip-Flop and Chemical Potential in Different Membrane Environments journal, September 2009

Flip-Flop-Induced Relaxation of Bending Energy: Implications for Membrane Remodeling journal, December 2009

Molecular organization of cholesterol in polyunsaturated phospholipid membranes: a solid state 2 H NMR investigation journal, May 1999

Molecular Organization of Cholesterol in Polyunsaturated Membranes: Microdomain Formation journal, January 2002

Controlling Membrane Cholesterol Content. A Role for Polyunsaturated (Docosahexaenoate) Phospholipids † journal, October 2002

Characterization of the Ternary Mixture of Sphingomyelin, POPC, and Cholesterol: Support for an Inhomogeneous Lipid Distribution at High Temperatures journal, April 2008

Cholesterol-Induced Modifications in Lipid Bilayers: A Simulation Study journal, October 2002

The description of membrane lipid conformation, order and dynamics by 2H-NMR journal, March 1983

Structural and dynamical details of cholesterol-lipid interaction as revealed by deuterium NMR journal, December 1984

Anisotropic Motion and Molecular Dynamics of Cholesterol, Lanosterol, and Ergosterol in Lecithin Bilayers Studied by Quasi-elastic Neutron Scattering † journal, October 2002

Ternary Phase Diagram of Dipalmitoyl-PC/Dilauroyl-PC/Cholesterol: Nanoscopic Domain Formation Driven by Cholesterol journal, June 2001

The structure of lipid bilayers and the effects of general anaesthetics journal, October 1979

“Entropic Traps” in the Kinetics of Phase Separation in Multicomponent Membranes Stabilize Nanodomains journal, July 2006

Partial volumes of cholesterol and monounsaturated diacylphosphatidylcholines in mixed bilayers journal, September 2015

Noninvasive Neutron Scattering Measurements Reveal Slower Cholesterol Transport in Model Lipid Membranes journal, July 2011

Structure and dynamics of polyunsaturated hydrocarbon chains in lipid bilayers—significance for GPCR function journal, May 2008

How Cholesterol Could Be Drawn to the Cytoplasmic Leaf of the Plasma Membrane by Phosphatidylethanolamine journal, November 2014

Cholesterol in aqueous solution. Hydrophobicity and self-association journal, January 1975

Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms journal, October 2001

Partial molecular volumes of lipids and cholesterol journal, September 2006

Self-association of Cholesterol in Aqueous Solution journal, August 1973

Fast flip-flop of cholesterol and fatty acids in membranes: implications for membrane transport proteins journal, January 2003

Lipid rafts: contentious only from simplistic standpoints journal, April 2006

Cholesterol Hydroxyl Group Is Found To Reside in the Center of a Polyunsaturated Lipid Membrane journal, January 2006

Cholesterol Is Found To Reside in the Center of a Polyunsaturated Lipid Membrane journal, July 2008

Phase Separation in Lipid Membranes journal, March 2011

Bilayer Thickness Mismatch Controls Domain Size in Model Membranes journal, February 2013

Molecular Dynamics Simulations of Phospholipid Bilayers with Cholesterol journal, April 2003

Phase equilibria in the phosphatidylcholine-cholesterol system journal, November 1987

Effect of Cholesterol on the Chain-Ordering Transition of 1-Palmitoyl-2-arachidonoyl Phosphatidylcholine journal, October 1999

Cholesterol Flip-Flop: Insights from Free Energy Simulation Studies journal, October 2010

Interactions of Cholesterol with Lipid Bilayers: The Preferred Configuration and Fluctuations journal, August 2001

How Cholesterol Tilt Modulates the Mechanical Properties of Saturated and Unsaturated Lipid Membranes journal, January 2013

Phase diagram of a 4-component lipid mixture: DSPC/DOPC/POPC/chol journal, September 2013

Cholesterol through the Looking Glass journal, September 2012

Cholesterol in Bilayers with PUFA Chains: Doping with DMPC or POPC Results in Sterol Reorientation and Membrane-Domain Formation journal, September 2010

Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature journal, November 2011

What determines the thickness of a biological membrane journal, January 2009

Influence of cholesterol on the bilayer properties of monounsaturated phosphatidylcholine unilamellar vesicles journal, July 2007

The Effect of Cholesterol on Short- and Long-Chain Monounsaturated Lipid Bilayers as Determined by Molecular Dynamics Simulations and X-Ray Scattering journal, September 2008

Line Tension and Interaction Energies of Membrane Rafts Calculated from Lipid Splay and Tilt journal, February 2005

Modulation of the orientational order profile of the lipid acyl chain in the L? phase journal, November 1990

Analysis of the distribution of cholesterol in the intact cell. journal, December 1983

α-Tocopherol Is Well Designed to Protect Polyunsaturated Phospholipids: MD Simulations journal, October 2015

Location of Cholesterol in DMPC Membranes. A Comparative Study by Neutron Diffraction and Molecular Mechanics Simulation † journal, March 2001

Lipid Rafts As a Membrane-Organizing Principle journal, December 2009

Asymmetric Lipid Membranes: Towards More Realistic Model Systems journal, May 2015

α- Tocopherol’s Location in Membranes Is Not Affected by Their Composition journal, October 2014

Hydrocarbon Thickness Dictates Cholesterol's Location, Orientation and Motion in a Phospholipid Bilayer journal, January 2015

Dimyristoyl Phosphatidylcholine: A Remarkable Exception to α-Tocopherol’s Membrane Presence journal, December 2013

Tocopherol Activity Correlates with Its Location in a Membrane: A New Perspective on the Antioxidant Vitamin E journal, May 2013

Cholesterol Orientation and Dynamics in Dimyristoylphosphatidylcholine Bilayers: A Solid State Deuterium NMR Analysis journal, January 1999

Monolayer curvature stabilizes nanoscale raft domains in mixed lipid bilayers journal, March 2013

Structure and Dynamics of Cholesterol-Containing Polyunsaturated Lipid Membranes Studied by Neutron Diffraction and NMR journal, December 2010

A detailed analysis of partial molecular volumes in DPPC/cholesterol binary bilayers journal, December 2014

Sterol orientations in phosphatidylcholine liposomes as determined by deuterium NMR journal, March 1986

Lateral organization, bilayer asymmetry, and inter-leaflet coupling of biological membranes journal, November 2015

Determination of Membrane Cholesterol Partition Coefficient Using a Lipid Vesicle–Cyclodextrin Binary System: Effect of Phospholipid Acyl Chain Unsaturation and Headgroup Composition journal, December 2002

Spectroscopic studies of specifically deuterium labeled membrane systems. Nuclear magnetic resonance investigation of the effects of cholesterol in model systems journal, July 1978

Interactions between Ether Phospholipids and Cholesterol As Determined by Scattering and Molecular Dynamics Simulations journal, December 2012

Cholesterol Perturbs Lipid Bilayers Nonuniversally journal, May 2008

Radiation induced oxidative damage modification by cholesterol in liposomal membrane journal, May 1999

Cholesterol-dependent Lipid Assemblies Regulate the Activity of the Ecto-nucleotidase CD39 journal, July 2005

Cholesterol protects the phospholipid bilayer from oxidative damage journal, October 1995

Transient Translocation of the B Cell Receptor and Src Homology 2 Domain-Containing Inositol Phosphatase to Lipid Rafts: Evidence Toward a Role in Calcium Regulation journal, August 2000

Structure of the L c ′ Phase in a Hydrated Lipid Multilamellar System journal, May 1995

Effects of Epicholesterol on the Phosphatidylcholine Bilayer: A Molecular Simulation Study journal, March 2003

Lateral diffusion in binary mixtures of cholesterol and phosphatidylcholines. journal, January 1979

Deuterium magnetic resonance: theory and application to lipid membranes journal, August 1977

Tilt: Major Factor in Sterols' Ordering Capability in Membranes
journal, December 2006

Bilayer Thickness and Membrane Protein Function: An Energetic Perspective
journal, June 2007

Co-existence of gel and fluid lipid domains in single-component phospholipid membranes
journal, January 2012

The Observation of Highly Ordered Domains in Membranes with Cholesterol
journal, June 2013

Molecular mechanism of α-tocopherol action
journal, July 2007

Transmembrane movement of cholesterol in small unilamellar vesicles detected by cholesterol oxidase.
journal, January 1981

Raftlike Mixtures of Sphingomyelin and Cholesterol Investigated by Solid-State ² H NMR Spectroscopy
journal, October 2008

Molecular View of Cholesterol Flip-Flop and Chemical Potential in Different Membrane Environments
journal, September 2009

Flip-Flop-Induced Relaxation of Bending Energy: Implications for Membrane Remodeling
journal, December 2009

Molecular organization of cholesterol in polyunsaturated phospholipid membranes: a solid state ² H NMR investigation
journal, May 1999

Molecular Organization of Cholesterol in Polyunsaturated Membranes: Microdomain Formation
journal, January 2002

Controlling Membrane Cholesterol Content. A Role for Polyunsaturated (Docosahexaenoate) Phospholipids ^†
journal, October 2002

Characterization of the Ternary Mixture of Sphingomyelin, POPC, and Cholesterol: Support for an Inhomogeneous Lipid Distribution at High Temperatures
journal, April 2008

Cholesterol-Induced Modifications in Lipid Bilayers: A Simulation Study
journal, October 2002

The description of membrane lipid conformation, order and dynamics by 2H-NMR
journal, March 1983

Structural and dynamical details of cholesterol-lipid interaction as revealed by deuterium NMR
journal, December 1984

Anisotropic Motion and Molecular Dynamics of Cholesterol, Lanosterol, and Ergosterol in Lecithin Bilayers Studied by Quasi-elastic Neutron Scattering ^†
journal, October 2002

Ternary Phase Diagram of Dipalmitoyl-PC/Dilauroyl-PC/Cholesterol: Nanoscopic Domain Formation Driven by Cholesterol
journal, June 2001

The structure of lipid bilayers and the effects of general anaesthetics
journal, October 1979

“Entropic Traps” in the Kinetics of Phase Separation in Multicomponent Membranes Stabilize Nanodomains
journal, July 2006

Partial volumes of cholesterol and monounsaturated diacylphosphatidylcholines in mixed bilayers
journal, September 2015

Noninvasive Neutron Scattering Measurements Reveal Slower Cholesterol Transport in Model Lipid Membranes
journal, July 2011

Structure and dynamics of polyunsaturated hydrocarbon chains in lipid bilayers—significance for GPCR function
journal, May 2008

How Cholesterol Could Be Drawn to the Cytoplasmic Leaf of the Plasma Membrane by Phosphatidylethanolamine
journal, November 2014

Cholesterol in aqueous solution. Hydrophobicity and self-association
journal, January 1975

Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms
journal, October 2001

Partial molecular volumes of lipids and cholesterol
journal, September 2006

Self-association of Cholesterol in Aqueous Solution
journal, August 1973

Fast flip-flop of cholesterol and fatty acids in membranes: implications for membrane transport proteins
journal, January 2003

Lipid rafts: contentious only from simplistic standpoints
journal, April 2006

Cholesterol Hydroxyl Group Is Found To Reside in the Center of a Polyunsaturated Lipid Membrane
journal, January 2006

Cholesterol Is Found To Reside in the Center of a Polyunsaturated Lipid Membrane
journal, July 2008

Phase Separation in Lipid Membranes
journal, March 2011

Bilayer Thickness Mismatch Controls Domain Size in Model Membranes
journal, February 2013

Molecular Dynamics Simulations of Phospholipid Bilayers with Cholesterol
journal, April 2003

Phase equilibria in the phosphatidylcholine-cholesterol system
journal, November 1987

Effect of Cholesterol on the Chain-Ordering Transition of 1-Palmitoyl-2-arachidonoyl Phosphatidylcholine
journal, October 1999

Cholesterol Flip-Flop: Insights from Free Energy Simulation Studies
journal, October 2010

Interactions of Cholesterol with Lipid Bilayers: The Preferred Configuration and Fluctuations
journal, August 2001

How Cholesterol Tilt Modulates the Mechanical Properties of Saturated and Unsaturated Lipid Membranes
journal, January 2013

Phase diagram of a 4-component lipid mixture: DSPC/DOPC/POPC/chol
journal, September 2013

Cholesterol through the Looking Glass
journal, September 2012

Cholesterol in Bilayers with PUFA Chains: Doping with DMPC or POPC Results in Sterol Reorientation and Membrane-Domain Formation
journal, September 2010

Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature
journal, November 2011

What determines the thickness of a biological membrane
journal, January 2009

Influence of cholesterol on the bilayer properties of monounsaturated phosphatidylcholine unilamellar vesicles
journal, July 2007

The Effect of Cholesterol on Short- and Long-Chain Monounsaturated Lipid Bilayers as Determined by Molecular Dynamics Simulations and X-Ray Scattering
journal, September 2008

Line Tension and Interaction Energies of Membrane Rafts Calculated from Lipid Splay and Tilt
journal, February 2005

Modulation of the orientational order profile of the lipid acyl chain in the L? phase
journal, November 1990

Analysis of the distribution of cholesterol in the intact cell.
journal, December 1983

α-Tocopherol Is Well Designed to Protect Polyunsaturated Phospholipids: MD Simulations
journal, October 2015

Location of Cholesterol in DMPC Membranes. A Comparative Study by Neutron Diffraction and Molecular Mechanics Simulation ^†
journal, March 2001

Lipid Rafts As a Membrane-Organizing Principle
journal, December 2009

Asymmetric Lipid Membranes: Towards More Realistic Model Systems
journal, May 2015

α- Tocopherol’s Location in Membranes Is Not Affected by Their Composition
journal, October 2014

Hydrocarbon Thickness Dictates Cholesterol's Location, Orientation and Motion in a Phospholipid Bilayer
journal, January 2015

Dimyristoyl Phosphatidylcholine: A Remarkable Exception to α-Tocopherol’s Membrane Presence
journal, December 2013

Tocopherol Activity Correlates with Its Location in a Membrane: A New Perspective on the Antioxidant Vitamin E
journal, May 2013

Cholesterol Orientation and Dynamics in Dimyristoylphosphatidylcholine Bilayers: A Solid State Deuterium NMR Analysis
journal, January 1999

Monolayer curvature stabilizes nanoscale raft domains in mixed lipid bilayers
journal, March 2013

Structure and Dynamics of Cholesterol-Containing Polyunsaturated Lipid Membranes Studied by Neutron Diffraction and NMR
journal, December 2010

A detailed analysis of partial molecular volumes in DPPC/cholesterol binary bilayers
journal, December 2014

Sterol orientations in phosphatidylcholine liposomes as determined by deuterium NMR
journal, March 1986

Lateral organization, bilayer asymmetry, and inter-leaflet coupling of biological membranes
journal, November 2015

Determination of Membrane Cholesterol Partition Coefficient Using a Lipid Vesicle–Cyclodextrin Binary System: Effect of Phospholipid Acyl Chain Unsaturation and Headgroup Composition
journal, December 2002

Spectroscopic studies of specifically deuterium labeled membrane systems. Nuclear magnetic resonance investigation of the effects of cholesterol in model systems
journal, July 1978

Interactions between Ether Phospholipids and Cholesterol As Determined by Scattering and Molecular Dynamics Simulations
journal, December 2012

Cholesterol Perturbs Lipid Bilayers Nonuniversally
journal, May 2008

Radiation induced oxidative damage modification by cholesterol in liposomal membrane
journal, May 1999

Cholesterol-dependent Lipid Assemblies Regulate the Activity of the Ecto-nucleotidase CD39
journal, July 2005

Cholesterol protects the phospholipid bilayer from oxidative damage
journal, October 1995

Transient Translocation of the B Cell Receptor and Src Homology 2 Domain-Containing Inositol Phosphatase to Lipid Rafts: Evidence Toward a Role in Calcium Regulation
journal, August 2000

Structure of the $L_{c^{'}}$ Phase in a Hydrated Lipid Multilamellar System
journal, May 1995

Effects of Epicholesterol on the Phosphatidylcholine Bilayer: A Molecular Simulation Study
journal, March 2003

Lateral diffusion in binary mixtures of cholesterol and phosphatidylcholines.
journal, January 1979

Deuterium magnetic resonance: theory and application to lipid membranes
journal, August 1977

Molecular order in cis and trans unsaturated phospholipid bilayers
journal, August 1978

Molecular Organization of Cholesterol in Unsaturated Phosphatidylethanolamines: X-ray Diffraction and Solid State ² H NMR Reveal Differences with Phosphatidylcholines
journal, April 2006

How polyunsaturated fatty acids modify molecular organization in membranes: Insight from NMR studies of model systems
journal, January 2015

Macroscopic Phase Separation, Modulated Phases, and Microemulsions: A Unified Picture of Rafts
journal, May 2014