Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1977 Nov;74(11):5031–5035. doi: 10.1073/pnas.74.11.5031

Transmembrane interactions and the mechanism of capping of surface receptors by their specific ligands.

L Y Bourguignon, S J Singer
PMCID: PMC432092  PMID: 337308

Abstract

The mechanism of capping of cell surface receptors has been examined by a double fluorescence staining procedure that permitted simultaneous observations of the distribution of a surface-bound ligand together with intracellular actin or myosin. At an early stage in the capping of the T-25 antigen or the H2 histocompatibility antigens on mouse splenic T lymphocytes, or of concanavalin A receptors on HeLa cells, when the specific receptors in question were collected into patches that were distributed over the entire cell surface, the intracellular membrane-associated actin or myosin was also accumulated into patches that were located directly under the receptor patches. These and other results have led us to propose a general molecular mechanism for the process of capping, in which actin and myosin are directly involved. It is suggested that membrane-associated actin is directly or indirectly bound to an integral protein or class of proteins, X, in the plasma membranes of eukaryotic cells. When any receptor in the membrane is aggregated by an external multivalent ligand, the aggregate binds effectively to X, whereas unaggregated receptors do not bind to X. The receptor aggregates, linked to actin (and myosin) through X, are then actively collected into a cap by an analogue of the actin--myosin sliding filament mechanism of muscle contraction.

Full text

PDF
5031

Images in this article

5032Image
on p.5032
5032Image
on p.5032

Selected References

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

  1. Albertini D. F., Anderson E. Microtubule and microfilament rearrangements during capping of concanavalin A receptors on cultured ovarian granulosa cells. J Cell Biol. 1977 Apr;73(1):111–127. doi: 10.1083/jcb.73.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ash J. F., Singer S. J. Concanavalin-A-induced transmembrane linkage of concanavalin A surface receptors to intracellular myosin-containing filaments. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4575–4579. doi: 10.1073/pnas.73.12.4575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bretscher M. S. Directed lipid flow in cell membranes. Nature. 1976 Mar 4;260(5546):21–23. doi: 10.1038/260021a0. [DOI] [PubMed] [Google Scholar]
  4. Edelman G. M., Yahara I., Wang J. L. Receptor mobility and receptor-cytoplasmic interactions in lymphocytes. Proc Natl Acad Sci U S A. 1973 May;70(5):1442–1446. doi: 10.1073/pnas.70.5.1442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Heggeness M. H., Ash J. F. Use of the avidin-biotin complex for the localization of actin and myosin with fluorescence microscopy. J Cell Biol. 1977 Jun;73(3):783–788. doi: 10.1083/jcb.73.3.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Heggeness M. H., Wang K., Singer S. J. Intracellular distributions of mechanochemical proteins in cultured fibroblasts. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3883–3887. doi: 10.1073/pnas.74.9.3883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Julius M. H., Simpson E., Herzenberg L. A. A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur J Immunol. 1973 Oct;3(10):645–649. doi: 10.1002/eji.1830031011. [DOI] [PubMed] [Google Scholar]
  8. Lazarides E., Weber K. Actin antibody: the specific visualization of actin filaments in non-muscle cells. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2268–2272. doi: 10.1073/pnas.71.6.2268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Loor F., Forni L., Pernis B. The dynamic state of the lymphocyte membrane. Factors affecting the distribution and turnover of surface immunoglobulins. Eur J Immunol. 1972 Jun;2(3):203–212. doi: 10.1002/eji.1830020304. [DOI] [PubMed] [Google Scholar]
  10. Müller-Eberhard H. J. The molecular basis of the biological activities of complement. Harvey Lect. 1971;66:75–104. [PubMed] [Google Scholar]
  11. Pollard T. D., Weihing R. R. Actin and myosin and cell movement. CRC Crit Rev Biochem. 1974 Jan;2(1):1–65. doi: 10.3109/10409237409105443. [DOI] [PubMed] [Google Scholar]
  12. Schreiner G. F., Fujiwara K., Pollard T. D., Unanue E. R. Redistribution of myosin accompanying capping of surface Ig. J Exp Med. 1977 May 1;145(5):1393–1398. doi: 10.1084/jem.145.5.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Schreiner G. F., Unanue E. R. Membrane and cytoplasmic changes in B lymphocytes induced by ligand-surface immunoglobulin interaction. Adv Immunol. 1976;24:37–165. doi: 10.1016/s0065-2776(08)60329-6. [DOI] [PubMed] [Google Scholar]
  14. Singer S. J. The molecular organization of membranes. Annu Rev Biochem. 1974;43(0):805–833. doi: 10.1146/annurev.bi.43.070174.004105. [DOI] [PubMed] [Google Scholar]
  15. Unanue E. R., Perkins W. D., Karnovsky M. J. Ligand-induced movement of lymphocyte membrane macromolecules. I. Analysis by immunofluorescence and ultrastructural radioautography. J Exp Med. 1972 Oct 1;136(4):885–906. doi: 10.1084/jem.136.4.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Vitetta E. S., Uhr J. W. Immunoglobulins and alloantigens on the surface of lymphoid cells. Biochim Biophys Acta. 1975 Jun 30;415(2):253–271. doi: 10.1016/0304-4157(75)90004-0. [DOI] [PubMed] [Google Scholar]
  17. Wang K., Ash J. F., Singer S. J. Filamin, a new high-molecular-weight protein found in smooth muscle and non-muscle cells. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4483–4486. doi: 10.1073/pnas.72.11.4483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Weber K., Groeschel-Stewart U. Antibody to myosin: the specific visualization of myosin-containing filaments in nonmuscle cells. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4561–4564. doi: 10.1073/pnas.71.11.4561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. de Petris S. Concanavalin A receptors, immunoglobulins, and theta antigen of the lymphocyte surface. Interactions with concanavalin A and with Cytoplasmic structures. J Cell Biol. 1975 Apr;65(1):123–146. doi: 10.1083/jcb.65.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. de Petris S., Raff M. C. Distribution of immunoglobulin on the surface of mouse lymphoid cells as determined by immunoferritin electron microscopy. Antibody-induced, temperature-dependent redistribution and its implications for membrane structure. Eur J Immunol. 1972 Dec;2(6):523–535. doi: 10.1002/eji.1830020611. [DOI] [PubMed] [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

RESOURCES