Lipid Rafts: Buffers of Cell Membrane Physical Properties

Nickels, Jonathan D.; Smith, Micholas Dean; Alsop, Richard J.; Himbert, Sebastian; Yahya, Ahmad; Cordner, Destini; Zolnierczuk, Piotr A.; Stanley, Christopher B.; Katsaras, John; Cheng, Xiaolin; Rheinstädter, Maikel C.

doi:10.1021/acs.jpcb.8b12126

Title: Lipid Rafts: Buffers of Cell Membrane Physical Properties

Abstract

Lateral organization of lipids in the cell membrane appears to be an ancient feature of the cell, given the existence of lipid rafts in both eukaryotic and prokaryotic cells. Currently seen as platforms for protein partitioning, we posit that lipid rafts are capable of playing another role: stabilizing membrane physical properties over varying temperatures and other environmental conditions. Membrane composition defines the mechanical and viscous properties of the bilayer. The composition also varies strongly with temperature, with systematic changes in the partitioning of high and low melting temperature membrane components. In this way, rafts function as buffers of membrane physical properties, progressively counteracting environmental changes via compositional changes; i.e., more high melting lipids partition to the fluid phase with increasing temperature, increasing the bending modulus and viscosity, as thermal effects decrease these same properties. To provide an example of this phenomenon, we have performed neutron scattering experiments and atomistic molecular dynamics simulations on a phase separated model membrane. The results demonstrate a buffering effect in both the lateral diffusion coefficient and the bending modulus of the fluid phase upon changing temperature. Furthermore, this demonstration highlights the potentially advantageous stabilizing effect of complex lipid compositions in response to temperature and potentiallymore »« less

Authors:

^[1];

^[2];

^[3]; Himbert, Sebastian ^[3]; Yahya, Ahmad ^[1]; Cordner, Destini ^[1];

^[4];

^[5]; Katsaras, John ^[5];

^[6];

^[3]

Univ. of Cincinnati, Cincinnati, OH (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
McMaster Univ., Hamilton, ON (Canada)
Forschungszentrum Juelich GmbH, Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
The Ohio State Univ., Columbus, OH (United States)

Publication Date:: 2019-01-03

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

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

OSTI Identifier:: 1545220

Grant/Contract Number:: AC05-00OR22725

Resource Type:: Accepted Manuscript

Journal Name:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

Additional Journal Information:: Journal Volume: 123; Journal Issue: 9; Journal ID: ISSN 1520-6106

Publisher:: American Chemical Society

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 71 CLASSICAL AND QUANTUM MECHANICS, GENERAL PHYSICS

Citation Formats


                    Nickels, Jonathan D., Smith, Micholas Dean, Alsop, Richard J., Himbert, Sebastian, Yahya, Ahmad, Cordner, Destini, Zolnierczuk, Piotr A., Stanley, Christopher B., Katsaras, John, Cheng, Xiaolin, and Rheinstädter, Maikel C. Lipid Rafts: Buffers of Cell Membrane Physical Properties.  United States: N. p., 2019. 
Web.  doi:10.1021/acs.jpcb.8b12126.

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                    Nickels, Jonathan D., Smith, Micholas Dean, Alsop, Richard J., Himbert, Sebastian, Yahya, Ahmad, Cordner, Destini, Zolnierczuk, Piotr A., Stanley, Christopher B., Katsaras, John, Cheng, Xiaolin, & Rheinstädter, Maikel C. Lipid Rafts: Buffers of Cell Membrane Physical Properties.  United States.  https://doi.org/10.1021/acs.jpcb.8b12126

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                    Nickels, Jonathan D., Smith, Micholas Dean, Alsop, Richard J., Himbert, Sebastian, Yahya, Ahmad, Cordner, Destini, Zolnierczuk, Piotr A., Stanley, Christopher B., Katsaras, John, Cheng, Xiaolin, and Rheinstädter, Maikel C. Thu .  
"Lipid Rafts: Buffers of Cell Membrane Physical Properties".  United States.  https://doi.org/10.1021/acs.jpcb.8b12126.  https://www.osti.gov/servlets/purl/1545220.

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@article{osti_1545220,

  title        = {Lipid Rafts: Buffers of Cell Membrane Physical Properties},

  author       = {Nickels, Jonathan D. and Smith, Micholas Dean and Alsop, Richard J. and Himbert, Sebastian and Yahya, Ahmad and Cordner, Destini and Zolnierczuk, Piotr A. and Stanley, Christopher B. and Katsaras, John and Cheng, Xiaolin and Rheinstädter, Maikel C.},

  abstractNote = {Lateral organization of lipids in the cell membrane appears to be an ancient feature of the cell, given the existence of lipid rafts in both eukaryotic and prokaryotic cells. Currently seen as platforms for protein partitioning, we posit that lipid rafts are capable of playing another role: stabilizing membrane physical properties over varying temperatures and other environmental conditions. Membrane composition defines the mechanical and viscous properties of the bilayer. The composition also varies strongly with temperature, with systematic changes in the partitioning of high and low melting temperature membrane components. In this way, rafts function as buffers of membrane physical properties, progressively counteracting environmental changes via compositional changes; i.e., more high melting lipids partition to the fluid phase with increasing temperature, increasing the bending modulus and viscosity, as thermal effects decrease these same properties. To provide an example of this phenomenon, we have performed neutron scattering experiments and atomistic molecular dynamics simulations on a phase separated model membrane. The results demonstrate a buffering effect in both the lateral diffusion coefficient and the bending modulus of the fluid phase upon changing temperature. Furthermore, this demonstration highlights the potentially advantageous stabilizing effect of complex lipid compositions in response to temperature and potentially other membrane destabilizing environmental conditions.},

  doi          = {10.1021/acs.jpcb.8b12126},

  journal      = {Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry},

  number       = 9,

  volume       = 123,

  place        = {United States},

  year         = {2019},

  month        = {1}

}

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Title: Lipid Rafts: Buffers of Cell Membrane Physical Properties

Abstract

Citation Formats

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Sassena — X-ray and neutron scattering calculated from molecular dynamics trajectories using massively parallel computers journal, July 2012

Molecular dynamics with coupling to an external bath journal, October 1984

LINCS: A linear constraint solver for molecular simulations journal, September 1997

Canonical dynamics: Equilibrium phase-space distributions journal, March 1985

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Constant pressure molecular dynamics for molecular systems journal, December 1983

Polymorphic transitions in single crystals: A new molecular dynamics method journal, December 1981

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Probing Elastic and Viscous Properties of Phospholipid Bilayers Using Neutron Spin Echo Spectroscopy journal, September 2017

Molecular rheometry: direct determination of viscosity in Lo and Ld lipid phases via fluorescence lifetime imaging journal, January 2013

Lateral Diffusion Coefficients of Separate Lipid Species in a Ternary Raft-Forming Bilayer: A Pfg-NMR Multinuclear Study journal, July 2005

Implications of lipid microdomains for membrane curvature, budding and fission journal, August 2001

Membrane heterogeneity: Manifestation of a curvature-induced microemulsion journal, March 2012

Mechanical Properties of Nanoscopic Lipid Domains journal, October 2015

Effect of Chain Length and Unsaturation on Elasticity of Lipid Bilayers journal, July 2000

Determination of fluid and gel domain sizes in two-component, two-phase lipid bilayers. An electron spin resonance spin label study journal, August 1992

Lateral diffusion in phospholipid multibilayers measured by fluorescence recovery after photobleaching journal, August 1977

Translational diffusion of lipids in liquid crystalline phase phosphatidylcholine multibilayers. A comparison of experiment with theory journal, January 1985

Lateral Diffusion Rates of Lipid, Water, and a Hydrophobic Drug in a Multilamellar Liposome journal, September 2003

Relaxation in liquids, polymers and plastic crystals — strong/fragile patterns and problems journal, June 1991

Domain Shapes and Patterns: The Phenomenology of Modulated Phases journal, January 1995

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

Bacillus subtilis Lipid Extract, A Branched-Chain Fatty Acid Model Membrane journal, August 2017

High-resolution neutron spectroscopy using backscattering and neutron spin-echo spectrometers in soft and hard condensed matter journal, January 2020

Self‐assembly of lipid rafts revealed by fluorescence correlation spectroscopy in living breast cancer cells journal, November 2019

Lipidomics: coming to grips with lipid diversity
journal, July 2010

The Fluid Mosaic Model of the Structure of Cell Membranes
journal, February 1972

Functional rafts in cell membranes
journal, June 1997

Structure of Cholesterol in Lipid Rafts
journal, November 2014

The in vivo structure of biological membranes and evidence for lipid domains
journal, May 2017

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

Membrane Domains
journal, November 2004

Lipid raft microdomains and neurotransmitter signalling
journal, December 2006

Lipid rafts: now you see them, now you don't
journal, November 2006

Cholesterol, lipid rafts, and disease
journal, September 2002

Lipid rafts and signal transduction
journal, October 2000

Cardiolipin Domains in Bacillus subtilis Marburg Membranes
journal, February 2004

Functional microdomains in bacterial membranes
journal, August 2010

Membrane Microdomain Disassembly Inhibits MRSA Antibiotic Resistance
journal, November 2017

How proteins move lipids and lipids move proteins
journal, July 2001

Homeoviscous Adaptation--A Homeostatic Process that Regulates the Viscosity of Membrane Lipids in Escherichia coli
journal, February 1974

Critical demixing in fluid bilayers of phospholipid mixtures. A neutron diffraction study
journal, October 1983

Direct Detection of Domains in Phospholipid Bilayers by Grazing Incidence Diffraction of Neutrons and Atomic Force Microscopy
journal, May 1998

Geometrical Properties of Gel and Fluid Clusters in DMPC/DSPC Bilayers: Monte Carlo Simulation Approach Using a Two-State Model
journal, November 2001

Tuning Membrane Thickness Fluctuations in Model Lipid Bilayers
journal, July 2015

Near-Critical Fluctuations and Cytoskeleton-Assisted Phase Separation Lead to Subdiffusion in Cell Membranes
journal, January 2011

Investigation of phase transitions of lipids and lipid mixtures by sensitivity differential scanning calorimetry.
journal, November 1976

Lateral phase separation in phospholipid membranes
journal, June 1973

The Molecular Structure of the Liquid-Ordered Phase of Lipid Bilayers
journal, January 2014

CHARMM-GUI: A web-based graphical user interface for CHARMM
journal, March 2008

CHARMM-GUI Membrane Builder toward realistic biological membrane simulations
journal, August 2014

CHARMM-GUI Input Generator for NAMD, GROMACS, AMBER, OpenMM, and CHARMM/OpenMM Simulations Using the CHARMM36 Additive Force Field
journal, December 2015

CHARMM-GUI 10 years for biomolecular modeling and simulation: Biomolecular Modeling and Simulation
journal, November 2016

GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers
journal, September 2015

VMD: Visual molecular dynamics
journal, February 1996

Sassena — X-ray and neutron scattering calculated from molecular dynamics trajectories using massively parallel computers
journal, July 2012

Molecular dynamics with coupling to an external bath
journal, October 1984

LINCS: A linear constraint solver for molecular simulations
journal, September 1997

Canonical dynamics: Equilibrium phase-space distributions
journal, March 1985

A molecular dynamics method for simulations in the canonical ensemble
journal, June 1984

Constant pressure molecular dynamics for molecular systems
journal, December 1983

Polymorphic transitions in single crystals: A new molecular dynamics method
journal, December 1981

Calculating the Bending Modulus for Multicomponent Lipid Membranes in Different Thermodynamic Phases
journal, August 2013

Structure of lipid bilayers
journal, November 2000

How lipids affect the activities of integral membrane proteins
journal, November 2004

Is the protein/lipid hydrophobic matching principle relevant to membrane organization and functions?
journal, September 1999

Lipids do influence protein function—the hydrophobic matching hypothesis revisited
journal, November 2004

Brownian motion in biological membranes.
journal, August 1975

Probing Elastic and Viscous Properties of Phospholipid Bilayers Using Neutron Spin Echo Spectroscopy
journal, September 2017

Molecular rheometry: direct determination of viscosity in Lo and Ld lipid phases via fluorescence lifetime imaging
journal, January 2013

Lateral Diffusion Coefficients of Separate Lipid Species in a Ternary Raft-Forming Bilayer: A Pfg-NMR Multinuclear Study
journal, July 2005

Implications of lipid microdomains for membrane curvature, budding and fission
journal, August 2001

Membrane heterogeneity: Manifestation of a curvature-induced microemulsion
journal, March 2012

Mechanical Properties of Nanoscopic Lipid Domains
journal, October 2015

Effect of Chain Length and Unsaturation on Elasticity of Lipid Bilayers
journal, July 2000

Determination of fluid and gel domain sizes in two-component, two-phase lipid bilayers. An electron spin resonance spin label study
journal, August 1992

Lateral diffusion in phospholipid multibilayers measured by fluorescence recovery after photobleaching
journal, August 1977

Translational diffusion of lipids in liquid crystalline phase phosphatidylcholine multibilayers. A comparison of experiment with theory
journal, January 1985

Lateral Diffusion Rates of Lipid, Water, and a Hydrophobic Drug in a Multilamellar Liposome
journal, September 2003

Relaxation in liquids, polymers and plastic crystals — strong/fragile patterns and problems
journal, June 1991

Domain Shapes and Patterns: The Phenomenology of Modulated Phases
journal, January 1995

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

Bacillus subtilis Lipid Extract, A Branched-Chain Fatty Acid Model Membrane
journal, August 2017

High-resolution neutron spectroscopy using backscattering and neutron spin-echo spectrometers in soft and hard condensed matter
journal, January 2020

Self‐assembly of lipid rafts revealed by fluorescence correlation spectroscopy in living breast cancer cells
journal, November 2019