Europe PMC

This website requires cookies, and the limited processing of your personal data in order to function. By using the site you are agreeing to this as outlined in our privacy notice and cookie policy.

Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior.

Author information

Affiliations

  • 1. Department of Biochemistry and Cell Biology, State University of New York at Stony Brook 11794.
      Authors
    • Schroeder R 1
    (1 author)

Proceedings of the National Academy of Sciences of the United States of America, 01 Dec 1994, 91(25):12130-12134
https://doi.org/10.1073/pnas.91.25.12130 PMID: 7991596 PMCID: PMC45390

Free full text in Europe PMC

Abstract 

Proteins anchored by GPI are poorly solubilized from cell membranes by cold nonionic detergents because they associate with detergent-resistant membranes rich in cholesterol and sphingolipids. In this study, we demonstrated that cholesterol and sphingolipid-rich liposomes were incompletely solubilized by Triton X-100. GPI-anchored placental alkaline phosphatase incorporated in these liposomes was also not solubilized by cold Triton X-100. As sphingolipids have much higher melting temperatures (Tm) than cellular phospholipids, a property correlated with Tm might cause detergent inextractability. In support of this idea, we found that the low-Tm lipid dioleoyl phosphatidylcholine (DOPC) was efficiently extracted from detergent-resistant liposomes by Triton X-100, whereas the high-Tm lipid dipalmitoyl phosphatidylcholine (DPPC) was not. The fluorescence polarization of liposome-incorporated diphenylhexatriene was measured to determine the "fluidity" of the detergent-resistant liposomes. We found that these liposomes were about as fluid as DPPC/cholesterol liposomes, which were present in the liquid-ordered phase, and much less fluid than DOPC or DOPC/cholesterol liposomes. These findings may explain the behavior of GPI-anchored proteins, which often have saturated fatty acyl chains and should prefer a less-fluid membrane. Therefore, we propose that acyl chain interactions can influence the association of GPI-anchored proteins with detergent-resistant membrane lipids. The affinity of GPI-anchored proteins for a sphingolipid-rich membrane phase that is not in the liquid crystalline state may be important in determining their cellular localization.

Free full text 

Logo of pnasLink to Publisher's site
Proc Natl Acad Sci U S A. 1994 Dec 6; 91(25): 12130–12134.
PMCID: PMC45390
PMID: 7991596

Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior.

R Schroeder, E London, and D Brown
Author information Copyright and License information Disclaimer

Abstract

Proteins anchored by GPI are poorly solubilized from cell membranes by cold nonionic detergents because they associate with detergent-resistant membranes rich in cholesterol and sphingolipids. In this study, we demonstrated that cholesterol and sphingolipid-rich liposomes were incompletely solubilized by Triton X-100. GPI-anchored placental alkaline phosphatase incorporated in these liposomes was also not solubilized by cold Triton X-100. As sphingolipids have much higher melting temperatures (Tm) than cellular phospholipids, a property correlated with Tm might cause detergent inextractability. In support of this idea, we found that the low-Tm lipid dioleoyl phosphatidylcholine (DOPC) was efficiently extracted from detergent-resistant liposomes by Triton X-100, whereas the high-Tm lipid dipalmitoyl phosphatidylcholine (DPPC) was not. The fluorescence polarization of liposome-incorporated diphenylhexatriene was measured to determine the "fluidity" of the detergent-resistant liposomes. We found that these liposomes were about as fluid as DPPC/cholesterol liposomes, which were present in the liquid-ordered phase, and much less fluid than DOPC or DOPC/cholesterol liposomes. These findings may explain the behavior of GPI-anchored proteins, which often have saturated fatty acyl chains and should prefer a less-fluid membrane. Therefore, we propose that acyl chain interactions can influence the association of GPI-anchored proteins with detergent-resistant membrane lipids. The affinity of GPI-anchored proteins for a sphingolipid-rich membrane phase that is not in the liquid crystalline state may be important in determining their cellular localization.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.1M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.
 
icon of scanned page 12130
12130
icon of scanned page 12131
12131
icon of scanned page 12132
12132
icon of scanned page 12133
12133
icon of scanned page 12134
12134
 

Images in this article

Image
Image
on p.12131
Image
Image
on p.12133
Image
Image
on p.12133
Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Brown DA, Rose JK. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 1992 Feb 7;68(3):533–544. [Abstract] [Google Scholar]
  • Sargiacomo M, Sudol M, Tang Z, Lisanti MP. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol. 1993 Aug;122(4):789–807. [Europe PMC free article] [Abstract] [Google Scholar]
  • Cinek T, Horejsí V. The nature of large noncovalent complexes containing glycosyl-phosphatidylinositol-anchored membrane glycoproteins and protein tyrosine kinases. J Immunol. 1992 Oct 1;149(7):2262–2270. [Abstract] [Google Scholar]
  • Kurzchalia TV, Dupree P, Parton RG, Kellner R, Virta H, Lehnert M, Simons K. VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J Cell Biol. 1992 Sep;118(5):1003–1014. [Europe PMC free article] [Abstract] [Google Scholar]
  • Arreaza G, Melkonian KA, LaFevre-Bernt M, Brown DA. Triton X-100-resistant membrane complexes from cultured kidney epithelial cells contain the Src family protein tyrosine kinase p62yes. J Biol Chem. 1994 Jul 22;269(29):19123–19127. [Abstract] [Google Scholar]
  • Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell. 1992 Feb 21;68(4):673–682. [Abstract] [Google Scholar]
  • Lisanti MP, Tang ZL, Sargiacomo M. Caveolin forms a hetero-oligomeric protein complex that interacts with an apical GPI-linked protein: implications for the biogenesis of caveolae. J Cell Biol. 1993 Nov;123(3):595–604. [Europe PMC free article] [Abstract] [Google Scholar]
  • Chang WJ, Ying YS, Rothberg KG, Hooper NM, Turner AJ, Gambliel HA, De Gunzburg J, Mumby SM, Gilman AG, Anderson RG. Purification and characterization of smooth muscle cell caveolae. J Cell Biol. 1994 Jul;126(1):127–138. [Europe PMC free article] [Abstract] [Google Scholar]
  • Thompson TE, Tillack TW. Organization of glycosphingolipids in bilayers and plasma membranes of mammalian cells. Annu Rev Biophys Biophys Chem. 1985;14:361–386. [Abstract] [Google Scholar]
  • Skibbens JE, Roth MG, Matlin KS. Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and nonpolar fibroblasts. J Cell Biol. 1989 Mar;108(3):821–832. [Europe PMC free article] [Abstract] [Google Scholar]
  • Simons K, van Meer G. Lipid sorting in epithelial cells. Biochemistry. 1988 Aug 23;27(17):6197–6202. [Abstract] [Google Scholar]
  • Macala LJ, Yu RK, Ando S. Analysis of brain lipids by high performance thin-layer chromatography and densitometry. J Lipid Res. 1983 Sep;24(9):1243–1250. [Abstract] [Google Scholar]
  • Micanovic R, Bailey CA, Brink L, Gerber L, Pan YC, Hulmes JD, Udenfriend S. Aspartic acid-484 of nascent placental alkaline phosphatase condenses with a phosphatidylinositol glycan to become the carboxyl terminus of the mature enzyme. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1398–1402. [Europe PMC free article] [Abstract] [Google Scholar]
  • Koke JA, Yang M, Henner DJ, Volwerk JJ, Griffith OH. High-level expression in Escherichia coli and rapid purification of phosphatidylinositol-specific phospholipase C from Bacillus cereus and Bacillus thuringiensis. Protein Expr Purif. 1991 Feb;2(1):51–58. [Abstract] [Google Scholar]
  • Reiss-Husson F. Structure des phases liquide-cristallines de différents phospholipides, monoglycérides, sphingolipides, anhydres ou en présence d'eau. J Mol Biol. 1967 May 14;25(3):363–382. [Abstract] [Google Scholar]
  • Clowes AW, Cherry RJ, Chapman D. Physical properties of lecithin-cerebroside bilayers. Biochim Biophys Acta. 1971 Oct 12;249(1):301–317. [Abstract] [Google Scholar]
  • Barenholz Y, Suurkuusk J, Mountcastle D, Thompson TE, Biltonen RL. A calorimetric study of the thermotropic behavior of aqueous dispersions of natural and synthetic sphingomyelins. Biochemistry. 1976 Jun 1;15(11):2441–2447. [Abstract] [Google Scholar]
  • Schreier H, Moran P, Caras IW. Targeting of liposomes to cells expressing CD4 using glycosylphosphatidylinositol-anchored gp120. Influence of liposome composition on intracellular trafficking. J Biol Chem. 1994 Mar 25;269(12):9090–9098. [Abstract] [Google Scholar]
  • McConville MJ, Ferguson MA. The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochem J. 1993 Sep 1;294(Pt 2):305–324. [Europe PMC free article] [Abstract] [Google Scholar]
  • Sankaram MB, Thompson TE. Cholesterol-induced fluid-phase immiscibility in membranes. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8686–8690. [Europe PMC free article] [Abstract] [Google Scholar]
  • Montesano R, Roth J, Robert A, Orci L. Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature. 1982 Apr 15;296(5858):651–653. [Abstract] [Google Scholar]
  • Parton RG. Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J Histochem Cytochem. 1994 Feb;42(2):155–166. [Abstract] [Google Scholar]
  • Mayor S, Rothberg KG, Maxfield FR. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 1994 Jun 24;264(5167):1948–1951. [Abstract] [Google Scholar]
Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

Full text links 

Read article at publisher's site: https://doi.org/10.1073/pnas.91.25.12130

Read article for free, from open access legal sources, via Unpaywall: https://europepmc.org/articles/pmc45390?pdf=renderUnpaywall

Citations & impact 

Impact metrics

401
Citations
Jump to Citations

Citations of article over time

Alternative metrics

Altmetric item for https://www.altmetric.com/details/3296603
Altmetric
Discover the attention surrounding your research
https://www.altmetric.com/details/3296603

Smart citations by scite.ai
Smart citations by scite.ai include citation statements extracted from the full text of the citing article. The number of the statements may be higher than the number of citations provided by EuropePMC if one paper cites another multiple times or lower if scite has not yet processed some of the citing articles.
Explore citation contexts and check if this article has been supported or disputed.
https://scite.ai/reports/10.1073/pnas.91.25.12130

Supporting
Mentioning
Contrasting
41
568
1

Article citations

Go to all (401) article citations

Other citations

Similar Articles 

To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.

Funding 

Funders who supported this work.

NIGMS NIH HHS (2)