DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Cholesterol is enriched in the sphingolipid patches on the substrate near nonpolarized MDCK cells, but not in the sphingolipid domains in their plasma membranes

Abstract

In this paper, information about the distributions of cholesterol and sphingolipids within the plasma membranes of mammalian cells provides insight into the roles of these molecules in membrane function. In this report, high-resolution secondary ion mass spectrometry was used to image the distributions of metabolically incorporated rare isotope-labeled sphingolipids and cholesterol on the surfaces of nonpolarized epithelial cells. Sphingolipid domains that were not enriched with cholesterol were detected in the plasma membranes of subconfluent Madin-Darby canine kidney cells. Surprisingly, cholesterol-enriched sphingolipid patches were observed on the substrate adjacent to these cells. Based on the shapes of these cholesterol-enriched sphingolipid patches on the substrate and their proximity to cellular projections, we hypothesize that they are deposits of membranous particles released by the cell.

Authors:
; ;
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1567872
Alternate Identifier(s):
OSTI ID: 1476856
Report Number(s):
LLNL-JRNL-745101
Journal ID: ISSN 0005-2736; S0005273618301263; PII: S0005273618301263
Grant/Contract Number:  
08-LW-015; AC52-07NA27344
Resource Type:
Published Article
Journal Name:
Biochimica et Biophysica Acta. Biomembranes
Additional Journal Information:
Journal Name: Biochimica et Biophysica Acta. Biomembranes Journal Volume: 1860 Journal Issue: 10; Journal ID: ISSN 0005-2736
Publisher:
Elsevier
Country of Publication:
Netherlands
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Sphingolipids; Cholesterol; Madin-Darby canine kidney cells; Lipid domains; Secondary ion mass spectrometry imaging; Stable isotope labeling

Citation Formats

Yeager, Ashley N., Weber, Peter K., and Kraft, Mary L. Cholesterol is enriched in the sphingolipid patches on the substrate near nonpolarized MDCK cells, but not in the sphingolipid domains in their plasma membranes. Netherlands: N. p., 2018. Web. doi:10.1016/j.bbamem.2018.04.008.
Yeager, Ashley N., Weber, Peter K., & Kraft, Mary L. Cholesterol is enriched in the sphingolipid patches on the substrate near nonpolarized MDCK cells, but not in the sphingolipid domains in their plasma membranes. Netherlands. https://doi.org/10.1016/j.bbamem.2018.04.008
Yeager, Ashley N., Weber, Peter K., and Kraft, Mary L. Mon . "Cholesterol is enriched in the sphingolipid patches on the substrate near nonpolarized MDCK cells, but not in the sphingolipid domains in their plasma membranes". Netherlands. https://doi.org/10.1016/j.bbamem.2018.04.008.
@article{osti_1567872,
title = {Cholesterol is enriched in the sphingolipid patches on the substrate near nonpolarized MDCK cells, but not in the sphingolipid domains in their plasma membranes},
author = {Yeager, Ashley N. and Weber, Peter K. and Kraft, Mary L.},
abstractNote = {In this paper, information about the distributions of cholesterol and sphingolipids within the plasma membranes of mammalian cells provides insight into the roles of these molecules in membrane function. In this report, high-resolution secondary ion mass spectrometry was used to image the distributions of metabolically incorporated rare isotope-labeled sphingolipids and cholesterol on the surfaces of nonpolarized epithelial cells. Sphingolipid domains that were not enriched with cholesterol were detected in the plasma membranes of subconfluent Madin-Darby canine kidney cells. Surprisingly, cholesterol-enriched sphingolipid patches were observed on the substrate adjacent to these cells. Based on the shapes of these cholesterol-enriched sphingolipid patches on the substrate and their proximity to cellular projections, we hypothesize that they are deposits of membranous particles released by the cell.},
doi = {10.1016/j.bbamem.2018.04.008},
journal = {Biochimica et Biophysica Acta. Biomembranes},
number = 10,
volume = 1860,
place = {Netherlands},
year = {Mon Oct 01 00:00:00 EDT 2018},
month = {Mon Oct 01 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.bbamem.2018.04.008

Citation Metrics:
Cited by: 9 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Physical and biochemical regulation of integrin release during rear detachment of migrating cells
journal, April 1998

  • Palecek, S. P.; Huttenlocher, A.; Horwitz, A. F.
  • Journal of Cell Science, Vol. 111, Issue 7
  • DOI: 10.1242/jcs.111.7.929

Golgi sorting regulates organization and activity of GPI proteins at apical membranes
journal, March 2014

  • Paladino, Simona; Lebreton, Stéphanie; Tivodar, Simona
  • Nature Chemical Biology, Vol. 10, Issue 5
  • DOI: 10.1038/nchembio.1495

Gangliosides GM1 and GM3 in the Living Cell Membrane Form Clusters Susceptible to Cholesterol Depletion and Chilling
journal, June 2007

  • Fujita, Akikazu; Cheng, Jinglei; Hirakawa, Minako
  • Molecular Biology of the Cell, Vol. 18, Issue 6
  • DOI: 10.1091/mbc.e07-01-0071

The fence and picket structure of the plasma membrane of live cells as revealed by single molecule techniques (Review)
journal, January 2003


Fluorescent probe partitioning in GUVs of binary phospholipid mixtures: Implications for interpreting phase behavior
journal, January 2012

  • Juhasz, Janos; Davis, James H.; Sharom, Frances J.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1818, Issue 1
  • DOI: 10.1016/j.bbamem.2011.09.006

Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization
journal, June 2003

  • Nakada, Chieko; Ritchie, Kenneth; Oba, Yuichi
  • Nature Cell Biology, Vol. 5, Issue 7
  • DOI: 10.1038/ncb1009

Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts
journal, January 2013

  • Frisz, J. F.; Lou, K.; Klitzing, H. A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 8
  • DOI: 10.1073/pnas.1216585110

The reactions between glutaraldehyde and various proteins. An investigation of their kinetics
journal, March 1970

  • Hopwood, D.; Allen, C. R.; McCabe, M.
  • The Histochemical Journal, Vol. 2, Issue 2
  • DOI: 10.1007/BF01003541

Paradigm Shift of the Plasma Membrane Concept from the Two-Dimensional Continuum Fluid to the Partitioned Fluid: High-Speed Single-Molecule Tracking of Membrane Molecules
journal, June 2005


Theoretical and practical aspects of glutaraldehyde fixation
journal, July 1972


Membrane lipidome of an epithelial cell line
journal, January 2011

  • Sampaio, Julio L.; Gerl, Mathias J.; Klose, Christian
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 5
  • DOI: 10.1073/pnas.1019267108

Correlated Fluorescence-Atomic Force Microscopy of Membrane Domains: Structure of Fluorescence Probes Determines Lipid Localization
journal, March 2006


Investigation on lipid asymmetry using lipid probes
journal, June 2002

  • Devaux, Philippe F.; Fellmann, Pierre; Hervé, Paulette
  • Chemistry and Physics of Lipids, Vol. 116, Issue 1-2
  • DOI: 10.1016/S0009-3084(02)00023-3

Lipids on the frontier: a century of cell-membrane bilayers
journal, May 2003

  • Edidin, Michael
  • Nature Reviews Molecular Cell Biology, Vol. 4, Issue 5
  • DOI: 10.1038/nrm1102

Studies on the development and maintenance of epithelial cell surface polarity with monoclonal antibodies.
journal, May 1984


Sphingolipid Organization in the Plasma Membrane and the Mechanisms That Influence It
journal, January 2017


Expression of the Longin domain of TI-VAMP impairs lysosomal secretion and epithelial cell migration
journal, May 2007

  • Proux-Gillardeaux, Véronique; Raposo, Graça; Irinopoulou, Theano
  • Biology of the Cell, Vol. 99, Issue 5
  • DOI: 10.1042/BC20060097

Fluorinated Colloidal Gold Immunolabels for Imaging Select Proteins in Parallel with Lipids Using High-Resolution Secondary Ion Mass Spectrometry
journal, February 2012

  • Wilson, Robert L.; Frisz, Jessica F.; Hanafin, William P.
  • Bioconjugate Chemistry, Vol. 23, Issue 3
  • DOI: 10.1021/bc200482z

Sorting of sphingolipids in epithelial (Madin-Darby canine kidney) cells.
journal, October 1987

  • van Meer, G.; Stelzer, E. H.; Wijnaendts-van-Resandt, R. W.
  • The Journal of Cell Biology, Vol. 105, Issue 4
  • DOI: 10.1083/jcb.105.4.1623

Gold-Enhanced Biomolecular Surface Imaging of Cells and Tissue by SIMS and MALDI Mass Spectrometry
journal, February 2006

  • Altelaar, A. F. Maarten; Klinkert, Ivo; Jalink, Kees
  • Analytical Chemistry, Vol. 78, Issue 3
  • DOI: 10.1021/ac0513111

Development of cell surface polarity in the epithelial Madin-Darby canine kidney (MDCK) cell line.
journal, November 1984


Synthesis of Borondipyrromethene (BODIPY)-Labeled Sphingosine Derivatives by Cross-metathesis Reaction
journal, March 2007

  • Peters, Carsten; Billich, Andreas; Ghobrial, Michael
  • The Journal of Organic Chemistry, Vol. 72, Issue 5
  • DOI: 10.1021/jo062347b

Ceramide-orchestrated signalling in cancer cells
journal, December 2012

  • Morad, Samy A. F.; Cabot, Myles C.
  • Nature Reviews Cancer, Vol. 13, Issue 1
  • DOI: 10.1038/nrc3398

Phospholipids undergo hop diffusion in compartmentalized cell membrane
journal, June 2002

  • Fujiwara, Takahiro; Ritchie, Ken; Murakoshi, Hideji
  • The Journal of Cell Biology, Vol. 157, Issue 6
  • DOI: 10.1083/jcb.200202050

Sphingolipid Domains in the Plasma Membranes of Fibroblasts Are Not Enriched with Cholesterol
journal, April 2013

  • Frisz, Jessica F.; Klitzing, Haley A.; Lou, Kaiyan
  • Journal of Biological Chemistry, Vol. 288, Issue 23
  • DOI: 10.1074/jbc.M113.473207

Lipid sorting in epithelial cells
journal, August 1988


Hyaluronan production enhances shedding of plasma membrane-derived microvesicles
journal, August 2013

  • Rilla, Kirsi; Pasonen-Seppänen, Sanna; Deen, Ashik J.
  • Experimental Cell Research, Vol. 319, Issue 13
  • DOI: 10.1016/j.yexcr.2013.05.021

Influenza Viruses Select Ordered Lipid Domains during Budding from the Plasma Membrane
journal, January 1999

  • Scheiffele, Peter; Rietveld, Anton; Wilk, Thomas
  • Journal of Biological Chemistry, Vol. 274, Issue 4
  • DOI: 10.1074/jbc.274.4.2038

Dynamics of beta 1 integrin-mediated adhesive contacts in motile fibroblasts
journal, December 1992


Miscibility Phase Diagrams of Giant Vesicles Containing Sphingomyelin
journal, April 2005


Discovery of the migrasome, an organelle mediating release of cytoplasmic contents during cell migration
journal, October 2014


Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes
journal, February 2008


Segregation of GM1 and GM3 clusters in the cell membrane depends on the intact actin cytoskeleton
journal, May 2009

  • Fujita, Akikazu; Cheng, Jinglei; Fujimoto, Toyoshi
  • Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1791, Issue 5
  • DOI: 10.1016/j.bbalip.2009.01.008

Glycosphingolipid-enriched, detergent-insoluble complexes in protein sorting in epithelial cells
journal, June 1993

  • Fiedler, Klaus; Kobayashi, Toshihide; Kurzchalia, Teymuras V.
  • Biochemistry, Vol. 32, Issue 25
  • DOI: 10.1021/bi00076a009

THE FORMATION OF CHOLESTEROL FROM i-CHOLESTERYL METHYL ETHER
journal, January 1948


Imaging and 3D Elemental Characterization of Intact Bacterial Spores by High-Resolution Secondary Ion Mass Spectrometry
journal, August 2008

  • Ghosal, Sutapa; Fallon, Stewart J.; Leighton, Terrance J.
  • Analytical Chemistry, Vol. 80, Issue 15
  • DOI: 10.1021/ac8006279

Plasma membrane organization and function: moving past lipid rafts
journal, September 2013


Functional rafts in cell membranes
journal, June 1997

  • Simons, Kai; Ikonen, Elina
  • Nature, Vol. 387, Issue 6633
  • DOI: 10.1038/42408

Oncogenic H-Ras Reprograms Madin-Darby Canine Kidney (MDCK) Cell-derived Exosomal Proteins Following Epithelial-Mesenchymal Transition
journal, August 2013

  • Tauro, Bow J.; Mathias, Rommel A.; Greening, David W.
  • Molecular & Cellular Proteomics, Vol. 12, Issue 8
  • DOI: 10.1074/mcp.M112.027086

Lipid membrane domains in the brain
journal, August 2015

  • Aureli, Massimo; Grassi, Sara; Prioni, Simona
  • Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1851, Issue 8
  • DOI: 10.1016/j.bbalip.2015.02.001

Plasma Membrane Sterol Distribution Resembles the Surface Topography of Living Cells
journal, January 2007


Natural ceramide is unable to escape the lysosome, in contrast to a fluorescent analogue
journal, April 1998


Reticulated Lipid Probe Fluorescence Reveals MDCK Cell Apical Membrane Topography
journal, February 2002


The structure of myelin figures and microemulsions as observed with the electron microscope
journal, March 1960

  • Stoeckenius, Walther; Schulman, Jack H.; Prince, Leon M.
  • Kolloid-Zeitschrift, Vol. 169, Issue 1-2
  • DOI: 10.1007/BF01502567

Three-dimensional imaging of cholesterol and sphingolipids within a Madin-Darby canine kidney cell
journal, January 2016

  • Yeager, Ashley N.; Weber, Peter K.; Kraft, Mary L.
  • Biointerphases, Vol. 11, Issue 2
  • DOI: 10.1116/1.4939681

Incorporation studies of clickable ceramides in Jurkat cell plasma membranes
journal, January 2017

  • Walter, T.; Schlegel, J.; Burgert, A.
  • Chemical Communications, Vol. 53, Issue 51
  • DOI: 10.1039/C7CC01220A

A stereodivergent synthesis of D-erythro-sphingosine and D-threo-sphingosine from L-serine
journal, September 1988

  • Garner, Philip; Park, Jung Min; Malecki, Elise
  • The Journal of Organic Chemistry, Vol. 53, Issue 18
  • DOI: 10.1021/jo00253a039

Hemagglutinin Clusters in the Plasma Membrane Are Not Enriched with Cholesterol and Sphingolipids
journal, April 2015

  • Wilson, Robert L.; Frisz, Jessica F.; Klitzing, Haley A.
  • Biophysical Journal, Vol. 108, Issue 7
  • DOI: 10.1016/j.bpj.2015.02.026

Different Sphingolipids Show Differential Partitioning into Sphingolipid/Cholesterol-Rich Domains in Lipid Bilayers
journal, September 2000


A new, long-wavelength borondipyrromethene sphingosine for studying sphingolipid dynamics in live cells
journal, January 2013

  • Kim, Raehyun; Lou, Kaiyan; Kraft, Mary L.
  • Journal of Lipid Research, Vol. 54, Issue 1
  • DOI: 10.1194/jlr.D029207

Role of cholesterol in lipid raft formation: lessons from lipid model systems
journal, March 2003