Lipid Rafts: Buffers of Cell Membrane Physical Properties

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.

Copy to clipboard


                    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.  doi:10.1021/acs.jpcb.8b12126.

Copy to clipboard


                    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.  doi:10.1021/acs.jpcb.8b12126.  https://www.osti.gov/servlets/purl/1545220.

Copy to clipboard


                    
@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}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (DOE)

Publisher's Version of Record

DOI: 10.1021/acs.jpcb.8b12126

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 3 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Works referencing / citing this record:

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

Dong, Shiqing; Tang, Xiaoqiong; Wang, Jiao
Journal of Biophotonics, Vol. 13, Issue 2
DOI: 10.1002/jbio.201900214

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

Gardner, Jason S.; Ehlers, Georg; Faraone, Antonio
Nature Reviews Physics, Vol. 2, Issue 2
DOI: 10.1038/s42254-019-0128-1

Similar Records in DOE PAGES and OSTI.GOV collections:

Mechanical Properties of Nanoscopic Lipid Domains

Journal Article Nickels, Jonathan D. ; Cheng, Xiaolin ; Mostofian, Barmak ; ... - Journal of the American Chemical Society

We found that the lipid raft hypothesis presents insight into how the cell membrane organizes proteins and lipids to accomplish its many vital functions. Yet basic questions remain about the physical mechanisms that lead to the formation, stability, and size of lipid rafts. Thus, much interest has been generated in the study of systems that contain similar lateral heterogeneities, or domains. In the current work we present an experimental approach that is capable of isolating the bending moduli of lipid domains. This is accomplished using neutron scattering and its unique sensitivity to the isotopes of hydrogen. Combining contrast matching approachesmore »« less
Cited by 22
DOI: 10.1021/jacs.5b08894

Full Text Available
Preferential interactions of primary amine-terminated quantum dots with membrane domain boundaries and lipid rafts revealed with nanometer resolution

Journal Article Mensch, Arielle C. ; Melby, Eric S. ; Laudadio, Elizabeth D. ; ... - Environmental Science: Nano

The initial interactions of engineered nanoparticles (NPs) with living cells are governed by physicochemical properties of the NP and the molecular composition and structure of the cell membrane. Eukaryotic cell membranes contain lipid rafts – liquid-ordered nanodomains involved in membrane trafficking and molecular signaling. However, the impact of these membrane structures on cellular interactions of NPs remains unclear. Here we investigate the role of membrane domains in the interactions of primary amine-terminated quantum dots (Qdots) with liquid-ordered domains or lipid rafts in model membranes and intact cells, respectively. Using correlative atomic force and fluorescence microscopy, we found that the Qdotsmore »« less
Cited by 1
DOI: 10.1039/C9EN00996E

Full Text Available
Linking lipid architecture to bilayer structure and mechanics using self-consistent field modelling

Journal Article Pera, H. ; Kleijn, J. M. ; Leermakers, F. A. M., - Journal of Chemical Physics

To understand how lipid architecture determines the lipid bilayer structure and its mechanics, we implement a molecularly detailed model that uses the self-consistent field theory. This numerical model accurately predicts parameters such as Helfrichs mean and Gaussian bending modulus k{sub c} and k{sup ¯} and the preferred monolayer curvature J{sub 0}{sup m}, and also delivers structural membrane properties like the core thickness, and head group position and orientation. We studied how these mechanical parameters vary with system variations, such as lipid tail length, membrane composition, and those parameters that control the lipid tail and head group solvent quality. For themore »« less
DOI: 10.1063/1.4863994
Lipid raft facilitated ligation of K-{alpha}1-tubulin by specific antibodies on epithelial cells: Role in pathogenesis of chronic rejection following human lung transplantation

Journal Article Tiriveedhi, Venkataswarup ; Angaswamy, Nataraju ; Weber, Joseph ; ... - Biochemical and Biophysical Research Communications

Research highlights: {yields} Addition of KAT Abs (+) sera to NHBE culture causes upregulation of growth factors. {yields} Cholesterol depletion causes down regulation of growth factor expression. {yields} Cholesterol depletion is accompanied by loss of membrane bound caveolin. {yields} Thus, we demonstrate lipid raft are critical for efficient ligation of the KAT Abs. -- Abstract: Long term function of human lung allografts is hindered by development of chronic rejection manifested as Bronchiolitis Obliterans Syndrome (BOS). We have previously identified the development of antibodies (Abs) following lung transplantation to K-{alpha}1-tubulin (KAT), an epithelial surface gap junction cytoskeletal protein, in patients whomore »« less
DOI: 10.1016/J.BBRC.2010.07.063
Scaling relationships for the elastic moduli and viscosity of mixed lipid membranes

Journal Article Kelley, Elizabeth G. ; Butler, Paul D. ; Ashkar, Rana ; ... - Proceedings of the National Academy of Sciences of the United States of America

The elastic and viscous properties of biological membranes play a vital role in controlling cell functions that require local reorganization of the membrane components as well as dramatic shape changes such as endocytosis, vesicular trafficking, and cell division. These properties are widely acknowledged to depend on the unique composition of lipids within the membrane, yet the effects of lipid mixing on the membrane biophysical properties remain poorly understood. Here, we present a comprehensive characterization of the structural, elastic, and viscous properties of fluid membranes composed of binary mixtures of lipids with different tail lengths. We show that the mixed lipidmore »« less
DOI: 10.1073/pnas.2008789117

Similar Records

Title: Lipid Rafts: Buffers of Cell Membrane Physical Properties

Abstract

Citation Formats

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

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

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