Home LiteratureArticle Details
PMID: 9585412 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Lipid domain structure of the plasma membrane revealed by patching of membrane components.

The Journal of cell biology ·Vol. 141 ·No. 4 ·1998-05-18 ·Pages 929-42

Harder T, Scheiffele P, Verkade P, Simons K

Abstract

Lateral assemblies of glycolipids and cholesterol, "rafts," have been implicated to play a role in cellular processes like membrane sorting, signal transduction, and cell adhesion. We studied the structure of raft domains in the plasma membrane of non-polarized cells. Overexpressed plasma membrane markers were evenly distributed in the plasma membrane. We compared the patching behavior of pairs of raft markers (defined by insolubility in Triton X-100) with pairs of raft/non-raft markers. For this purpose we cross-linked glycosyl-phosphatidylinositol (GPI)-anchored proteins placental alkaline phosphatase (PLAP), Thy-1, influenza virus hemagglutinin (HA), and the raft lipid ganglioside GM1 using antibodies and/or cholera toxin. The patches of these raft markers overlapped extensively in BHK cells as well as in Jurkat T-lymphoma cells. Importantly, patches of GPI-anchored PLAP accumulated src-like protein tyrosine kinase fyn, which is thought to be anchored in the cytoplasmic leaflet of raft domains. In contrast patched raft components and patches of transferrin receptor as a non-raft marker were sharply separated. Taken together, our data strongly suggest that coalescence of cross-linked raft elements is mediated by their common lipid environments, whereas separation of raft and non-raft patches is caused by the immiscibility of different lipid phases. This view is supported by the finding that cholesterol depletion abrogated segregation. Our results are consistent with the view that raft domains in the plasma membrane of non-polarized cells are normally small and highly dispersed but that raft size can be modulated by oligomerization of raft components.

MeSH Terms
Alkaline Phosphatase/metabolism Animals Antibodies Biomarkers Cell Line Cell Membrane/chemistry,physiology,ultrastructure Cholera Toxin/pharmacology Cricetinae Cross-Linking Reagents G(M1) Ganglioside/metabolism Glycosylphosphatidylinositols/metabolism Hemagglutinin Glycoproteins, Influenza Virus/metabolism Humans Jurkat Cells Kidney Membrane Lipids/analysis,metabolism Microscopy, Immunoelectron Patch-Clamp Techniques Placenta/enzymology Proto-Oncogene Proteins/biosynthesis Proto-Oncogene Proteins c-fyn Recombinant Proteins/biosynthesis,metabolism Signal Transduction Solubility Thy-1 Antigens/metabolism Transfection
Chemicals
Antibodies Biomarkers Cross-Linking Reagents Glycosylphosphatidylinositols Hemagglutinin Glycoproteins, Influenza Virus Membrane Lipids Proto-Oncogene Proteins Recombinant Proteins Thy-1 Antigens G(M1) Ganglioside Cholera Toxin FYN protein, human Proto-Oncogene Proteins c-fyn Alkaline Phosphatase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Harder T
European Molecular Biology Laboratory, Cell Biology Programme, 69117 Heidelberg, Germany.
Scheiffele P
Verkade P
Simons K
References (64)
64 references, click to expand
  1. A single amino acid change in the cytoplasmic domain allows the influenza virus hemagglutinin to be endocytosed through coated pits.
    Cell. 1988 Jun 3;53(5):743-52 PMID: 2897244
  2. Alteration of the myometrial plasma membrane cholesterol content with beta-cyclodextrin modulates the binding affinity of the oxytocin receptor.
    Biochemistry. 1995 Oct 24;34(42):13784-93 PMID: 7577971
  3. Structural requirements for basolateral sorting of the human transferrin receptor in the biosynthetic and endocytic pathways of Madin-Darby canine kidney cells.
    J Cell Biol. 1997 Jun 16;137(6):1255-64 PMID: 9182660
  4. Guilty by insolubility--does a protein's detergent insolubility reflect a caveolar location?
    Trends Cell Biol. 1995 May;5(5):187-9 PMID: 14731445
  5. Caveolae and caveolins.
    Curr Opin Cell Biol. 1996 Aug;8(4):542-8 PMID: 8791446
  6. Sphingolipid organization in biomembranes: what physical studies of model membranes reveal.
    J Cell Sci. 1998 Jan;111 ( Pt 1):1-9 PMID: 9394007
  7. Bone-resorbing osteoclasts reveal a dynamic division of basal plasma membrane into two different domains.
    J Cell Sci. 1996 Feb;109 ( Pt 2):301-7 PMID: 8838653
  8. Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide.
    Protein Sci. 1994 Feb;3(2):166-75 PMID: 8003954
  9. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment.
    Mol Biol Cell. 1995 Jul;6(7):929-44 PMID: 7579703
  10. Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants.
    Cell. 1992 Nov 27;71(5):741-53 PMID: 1423629
  11. Antigen-mediated IGE receptor aggregation and signaling: a window on cell surface structure and dynamics.
    Annu Rev Biophys Biomol Struct. 1996;25:79-112 PMID: 8800465
  12. Lipid domains in model and biological membranes.
    Chem Phys Lipids. 1994 Sep 6;73(1-2):121-37 PMID: 8001178
  13. Interactions between GPI-anchored proteins and membrane lipids.
    Trends Cell Biol. 1992 Nov;2(11):338-43 PMID: 14731512
  14. Cholesterol-induced fluid-phase immiscibility in membranes.
    Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8686-90 PMID: 1656453
  15. Detergent insolubility of alkaline phosphatase during biosynthetic transport and endocytosis. Role of cholesterol.
    J Biol Chem. 1993 Feb 15;268(5):3150-5 PMID: 8428991
  16. Evidence for transbilayer, tail-to-tail cholesterol dimers in dipalmitoylglycerophosphocholine liposomes.
    Biochemistry. 1995 Mar 21;34(11):3851-7 PMID: 7893682
  17. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking.
    Science. 1994 Jun 24;264(5167):1948-51 PMID: 7516582
  18. Fc epsilon RI-mediated association of 6-micron beads with RBL-2H3 mast cells results in exclusion of signaling proteins from the forming phagosome and abrogation of normal downstream signaling.
    J Cell Biol. 1996 Sep;134(6):1427-39 PMID: 8830772
  19. The tyrosine kinase connection: how GPI-anchored proteins activate T cells.
    Curr Opin Immunol. 1993 Jun;5(3):349-54 PMID: 8347297
  20. The concept of lipid domains in membranes.
    J Cell Biol. 1982 Jul;94(1):1-6 PMID: 6889603
  21. Mechanisms of cell polarity: sorting and transport in epithelial cells.
    Curr Opin Cell Biol. 1994 Aug;6(4):545-54 PMID: 7986532
  22. A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin.
    J Cell Biol. 1991 Aug;114(3):413-21 PMID: 1860878
  23. On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes.
    Biochemistry. 1997 Sep 9;36(36):10944-53 PMID: 9283086
  24. Specific selection of host cell glycoproteins during assembly of murine leukaemia virus and vesicular stomatitis virus: presence of Thy-1 glycoprotein and absence of H-2, Pgp-1 and T-200 glycoproteins on the envelopes of these virus particles.
    J Gen Virol. 1983 Jun;64 (Pt 6):1241-53 PMID: 6133909
  25. Different requirements for NSF, SNAP, and Rab proteins in apical and basolateral transport in MDCK cells.
    Cell. 1995 May 19;81(4):571-80 PMID: 7758111
  26. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain.
    EMBO J. 1997 Sep 15;16(18):5501-8 PMID: 9312009
  27. Oligomerization of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol.
    FEBS Lett. 1996 Jun 17;388(2-3):143-9 PMID: 8690074
  28. Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and nonpolar fibroblasts.
    J Cell Biol. 1989 Mar;108(3):821-32 PMID: 2522097
  29. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface.
    Cell. 1992 Feb 7;68(3):533-44 PMID: 1531449
  30. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains.
    J Biol Chem. 1997 Feb 14;272(7):4276-80 PMID: 9020144
  31. The role of lipid signaling in constitutive membrane traffic.
    Curr Opin Cell Biol. 1997 Aug;9(4):519-26 PMID: 9261058
  32. VIP21/caveolin is a cholesterol-binding protein.
    Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10339-43 PMID: 7479780
  33. Transport of vesicular stomatitis virus G protein to the cell surface is signal mediated in polarized and nonpolarized cells.
    J Cell Biol. 1996 May;133(3):543-58 PMID: 8636230
  34. The submembranous location of p11 and its interaction with the p36 substrate of pp60 src kinase in situ.
    Exp Cell Res. 1988 Mar;175(1):81-96 PMID: 3126079
  35. Morphogenesis of the polarized epithelial cell phenotype.
    Science. 1989 Aug 18;245(4919):718-25 PMID: 2672330
  36. Functional rafts in cell membranes.
    Nature. 1997 Jun 5;387(6633):569-72 PMID: 9177342
  37. GPI-anchored proteins, glycosphingolipids, and sphingomyelin are sequestered to caveolae only after crosslinking.
    J Histochem Cytochem. 1996 Aug;44(8):929-41 PMID: 8756764
  38. Post-Golgi biosynthetic trafficking.
    J Cell Sci. 1997 Dec;110 ( Pt 24):3001-9 PMID: 9365270
  39. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains.
    Curr Opin Cell Biol. 1997 Aug;9(4):534-42 PMID: 9261060
  40. Palmitoylation of p59fyn is reversible and sufficient for plasma membrane association.
    Mol Biol Cell. 1997 Jun;8(6):1159-73 PMID: 9201723
  41. Signals determining protein tyrosine kinase and glycosyl-phosphatidylinositol-anchored protein targeting to a glycolipid-enriched membrane fraction.
    Mol Cell Biol. 1994 Aug;14(8):5384-91 PMID: 8035816
  42. Major histocompatibility complex-restricted recognition of retroviral superantigens by V beta 17+ T cells.
    J Exp Med. 1992 Jul 1;176(1):275-80 PMID: 1535369
  43. Role of cholesterol in the capping of surface immunoglobulin receptors on murine lymphocytes.
    J Cell Biol. 1983 Jul;97(1):73-80 PMID: 6223042
  44. Endocytosis of GPI-anchored proteins in human lymphocytes: role of glycolipid-based domains, actin cytoskeleton, and protein kinases.
    J Cell Biol. 1996 May;133(4):791-9 PMID: 8666664
  45. Cholesterol is required for surface transport of influenza virus hemagglutinin.
    J Cell Biol. 1998 Mar 23;140(6):1357-67 PMID: 9508769
  46. Digging into caveolae.
    Science. 1995 Sep 8;269(5229):1398-9 PMID: 7660120
  47. Direct visualization of redistribution and capping of fluorescent gangliosides on lymphocytes.
    J Cell Biol. 1984 Nov;99(5):1575-81 PMID: 6436251
  48. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and Rho-dependent signaling pathway.
    J Cell Biol. 1996 Oct;135(1):37-51 PMID: 8858161
  49. Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein block its transport to the cell surface.
    EMBO J. 1986 May;5(5):931-41 PMID: 3013626
  50. Distinct transport vesicles mediate the delivery of plasma membrane proteins to the apical and basolateral domains of MDCK cells.
    J Cell Biol. 1990 Sep;111(3):987-1000 PMID: 2202740
  51. Apical targeting in polarized epithelial cells: There's more afloat than rafts.
    Trends Cell Biol. 1997 Oct;7(10):393-9 PMID: 17708988
  52. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8655-9 PMID: 7567992
  53. Saturation of the endocytic pathway for the transferrin receptor does not affect the endocytosis of the epidermal growth factor receptor.
    J Biol Chem. 1997 Jan 24;272(4):2116-21 PMID: 8999911
  54. Different biosynthetic transport routes to the plasma membrane in BHK and CHO cells.
    J Cell Biol. 1996 Apr;133(2):247-56 PMID: 8609159
  55. Reversible palmitoylation of signaling proteins.
    Curr Opin Cell Biol. 1997 Apr;9(2):148-54 PMID: 9069258
  56. Both sphingolipids and cholesterol participate in the detergent insolubility of alkaline phosphatase, a glycosylphosphatidylinositol-anchored protein, in mammalian membranes.
    J Biol Chem. 1995 Mar 17;270(11):6254-60 PMID: 7890763
  57. 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.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12130-4 PMID: 7991596
  58. Large-scale co-aggregation of fluorescent lipid probes with cell surface proteins.
    J Cell Biol. 1994 May;125(4):795-802 PMID: 8188747
  59. Cysteine3 of Src family protein tyrosine kinase determines palmitoylation and localization in caveolae.
    J Cell Biol. 1994 Jul;126(2):353-63 PMID: 7518463
  60. The subcellular distribution of early endosomes is affected by the annexin II2p11(2) complex.
    J Cell Biol. 1993 Dec;123(5):1119-32 PMID: 8245122
  61. Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae.
    J Histochem Cytochem. 1994 Feb;42(2):155-66 PMID: 8288861
  62. Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae.
    J Biol Chem. 1995 Mar 24;270(12):6838-42 PMID: 7896831
  63. VIP36, a novel component of glycolipid rafts and exocytic carrier vesicles in epithelial cells.
    EMBO J. 1994 Apr 1;13(7):1729-40 PMID: 8157011
  64. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells.
    Science. 1989 Sep 29;245(4925):1499-501 PMID: 2571189
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1998-05-18
Pages
929-42
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2132776
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com