Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1991 Mar 2;112(6):1143–1150. doi: 10.1083/jcb.112.6.1143

Differences between the lateral organization of conventional and inositol phospholipid-anchored membrane proteins. A further definition of micrometer scale membrane domains

PMCID: PMC2288893  PMID: 1825659

Abstract

Plasma membranes of many cells appear to be divided into domains, areas whose composition and function differ from the average for an entire membrane. We have previously used fluorescence photo-bleaching and recovery to demonstrate one type of membrane domain, with dimensions of micrometers (Yechiel, E., and M. Edidin. 1987, J. Cell Biol. 105: 755- 760). The presence of membrane domains is inferred from the dependence of the apparent mobile fraction of labeled molecules on the size of the membrane area probed. We now find that by this definition classical class I MHC molecules, H-2Db, are concentrated in domains in the membranes of K78-2 hepatoma cells, while the nonclassical class I- related molecules, Qa-2, are free to pass the boundaries of these domains. The two proteins are highly homologous but differ in their mode of anchorage to the membrane lipid bilayer. H-2Db is anchored by a transmembrane peptide, while Qa-2 is anchored by a glycosylphosphatidylinositol (GPI) anchor. A mutant class I protein with its external portion derived from Qa-2 but with transmembrane and cytoplasmic sequences from a classical class I molecule shows a dependence of its mobile fraction on the area of membrane probed, while a mutant whose external portions are a mixture of classical and nonclassical class I sequences, GPI-linked to the bilayer, does not show this dependence and hence by our definition is not restricted to membrane domains.

Full Text

The Full Text of this article is available as a PDF (880.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bierer B. E., Herrmann S. H., Brown C. S., Burakoff S. J., Golan D. E. Lateral mobility of class I histocompatibility antigens in B lymphoblastoid cell membranes: modulation by cross-linking and effect of cell density. J Cell Biol. 1987 Sep;105(3):1147–1152. doi: 10.1083/jcb.105.3.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bjorkman P. J., Saper M. A., Samraoui B., Bennett W. S., Strominger J. L., Wiley D. C. Structure of the human class I histocompatibility antigen, HLA-A2. Nature. 1987 Oct 8;329(6139):506–512. doi: 10.1038/329506a0. [DOI] [PubMed] [Google Scholar]
  3. Cowan A. E., Myles D. G., Koppel D. E. Lateral diffusion of the PH-20 protein on guinea pig sperm: evidence that barriers to diffusion maintain plasma membrane domains in mammalian sperm. J Cell Biol. 1987 Apr;104(4):917–923. doi: 10.1083/jcb.104.4.917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Darlington G. J., Bernhard H. P., Miller R. A., Ruddle F. H. Expression of liver phenotypes in cultured mouse hepatoma cells. J Natl Cancer Inst. 1980 Apr;64(4):809–819. [PubMed] [Google Scholar]
  5. Dubinsky J. M., Loftus D. J., Fischbach G. D., Elson E. L. Formation of acetylcholine receptor clusters in chick myotubes: migration or new insertion? J Cell Biol. 1989 Oct;109(4 Pt 1):1733–1743. doi: 10.1083/jcb.109.4.1733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hiraoka Y., Sedat J. W., Agard D. A. Determination of three-dimensional imaging properties of a light microscope system. Partial confocal behavior in epifluorescence microscopy. Biophys J. 1990 Feb;57(2):325–333. doi: 10.1016/S0006-3495(90)82534-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ishihara A., Hou Y., Jacobson K. The Thy-1 antigen exhibits rapid lateral diffusion in the plasma membrane of rodent lymphoid cells and fibroblasts. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1290–1293. doi: 10.1073/pnas.84.5.1290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Karnovsky M. J., Kleinfeld A. M., Hoover R. L., Klausner R. D. The concept of lipid domains in membranes. J Cell Biol. 1982 Jul;94(1):1–6. doi: 10.1083/jcb.94.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Klausner R. D., Kleinfeld A. M., Hoover R. L., Karnovsky M. J. Lipid domains in membranes. Evidence derived from structural perturbations induced by free fatty acids and lifetime heterogeneity analysis. J Biol Chem. 1980 Feb 25;255(4):1286–1295. [PubMed] [Google Scholar]
  10. Klausner R. D., Wolf D. E. Selectivity of fluorescent lipid analogues for lipid domains. Biochemistry. 1980 Dec 23;19(26):6199–6203. doi: 10.1021/bi00567a039. [DOI] [PubMed] [Google Scholar]
  11. Liu S. C., Derick L. H., Palek J. Visualization of the hexagonal lattice in the erythrocyte membrane skeleton. J Cell Biol. 1987 Mar;104(3):527–536. doi: 10.1083/jcb.104.3.527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ozato K., Sachs D. H. Monoclonal antibodies to mouse MHC antigens. III. Hybridoma antibodies reacting to antigens of the H-2b haplotype reveal genetic control of isotype expression. J Immunol. 1981 Jan;126(1):317–321. [PubMed] [Google Scholar]
  13. Phelps B. M., Primakoff P., Koppel D. E., Low M. G., Myles D. G. Restricted lateral diffusion of PH-20, a PI-anchored sperm membrane protein. Science. 1988 Jun 24;240(4860):1780–1782. doi: 10.1126/science.3381102. [DOI] [PubMed] [Google Scholar]
  14. Rodriguez-Boulan E., Nelson W. J. Morphogenesis of the polarized epithelial cell phenotype. Science. 1989 Aug 18;245(4919):718–725. doi: 10.1126/science.2672330. [DOI] [PubMed] [Google Scholar]
  15. Saxton M. J. The membrane skeleton of erythrocytes. A percolation model. Biophys J. 1990 Jun;57(6):1167–1177. doi: 10.1016/S0006-3495(90)82636-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Schroit A. J., Pagano R. E. Capping of a phospholipid analog in the plasma membrane of lymphocytes. Cell. 1981 Jan;23(1):105–112. doi: 10.1016/0092-8674(81)90275-0. [DOI] [PubMed] [Google Scholar]
  17. Shen B. W., Josephs R., Steck T. L. Ultrastructure of the intact skeleton of the human erythrocyte membrane. J Cell Biol. 1986 Mar;102(3):997–1006. doi: 10.1083/jcb.102.3.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Stroynowski I. Molecules related to class-I major histocompatibility complex antigens. Annu Rev Immunol. 1990;8:501–530. doi: 10.1146/annurev.iy.08.040190.002441. [DOI] [PubMed] [Google Scholar]
  19. Stroynowski I., Soloski M., Low M. G., Hood L. A single gene encodes soluble and membrane-bound forms of the major histocompatibility Qa-2 antigen: anchoring of the product by a phospholipid tail. Cell. 1987 Aug 28;50(5):759–768. doi: 10.1016/0092-8674(87)90334-5. [DOI] [PubMed] [Google Scholar]
  20. Thompson T. E., Tillack T. W. Organization of glycosphingolipids in bilayers and plasma membranes of mammalian cells. Annu Rev Biophys Biophys Chem. 1985;14:361–386. doi: 10.1146/annurev.bb.14.060185.002045. [DOI] [PubMed] [Google Scholar]
  21. Ulker N., Hood L. E., Stroynowski I. Molecular signals for phosphatidylinositol modification of the Qa-2 antigen. J Immunol. 1990 Oct 1;145(7):2214–2219. [PubMed] [Google Scholar]
  22. Wier M., Edidin M. Constraint of the translational diffusion of a membrane glycoprotein by its external domains. Science. 1988 Oct 21;242(4877):412–414. doi: 10.1126/science.3175663. [DOI] [PubMed] [Google Scholar]
  23. Wolf D. E., Edidin M., Handyside A. H. Changes in the organization of the mouse egg plasma membrane upon fertilization and first cleavage: indications from the lateral diffusion rates of fluorescent lipid analogs. Dev Biol. 1981 Jul 15;85(1):195–198. doi: 10.1016/0012-1606(81)90250-5. [DOI] [PubMed] [Google Scholar]
  24. Wolf D. E., Kinsey W., Lennarz W., Edidin M. Changes in the organization of the sea urchin egg plasma membrane upon fertilization: indications from the lateral diffusion rates of lipid-soluble fluorescent dyes. Dev Biol. 1981 Jan 15;81(1):133–138. doi: 10.1016/0012-1606(81)90355-9. [DOI] [PubMed] [Google Scholar]
  25. Wolf D. E., Lipscomb A. C., Maynard V. M. Causes of nondiffusing lipid in the plasma membrane of mammalian spermatozoa. Biochemistry. 1988 Feb 9;27(3):860–865. doi: 10.1021/bi00403a004. [DOI] [PubMed] [Google Scholar]
  26. Yechiel E., Edidin M. Micrometer-scale domains in fibroblast plasma membranes. J Cell Biol. 1987 Aug;105(2):755–760. doi: 10.1083/jcb.105.2.755. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES