Skip to main content
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1992 May 1;175(5):1317–1326. doi: 10.1084/jem.175.5.1317

Membrane sorting during phagocytosis: selective exclusion of major histocompatibility complex molecules but not complement receptor CR3 during conventional and coiling phagocytosis

PMCID: PMC2119207  PMID: 1569400

Abstract

We have used immunocytochemical techniques and enzyme cytochemistry to examine the distribution of plasma membrane proteins during coiling phagocytosis of Legionella pneumophila and conventional phagocytosis of Escherichia coli. Whereas class I and class II major histocompatibility complex (MHC) molecules are relatively excluded from nascent phagosomes during conventional and coiling phagocytosis, the CR3 complement receptor persists in nascent phagosomes. The staining pattern for alkaline phosphatase activity resembles that of MHC molecules, with a marked exclusion of phosphatase activity from L. pneumophila coils and nascent phagosomes. The staining pattern for 5'-nucleotidase activity, on the other hand, resembles that of CR3 with intense staining in the inner layers of L. pneumophila coils. These results demonstrate that the cell has the ability to exclude selectively certain membrane proteins from the nascent phagosome during phagocytosis, thereby producing a phagosomal membrane markedly different from the plasma membrane from which it is derived.

Full Text

The Full Text of this article is available as a PDF (3.6 MB).

Selected References

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

  1. Antoine J. C., Jouanne C., Lang T., Prina E., de Chastellier C., Frehel C. Localization of major histocompatibility complex class II molecules in phagolysosomes of murine macrophages infected with Leishmania amazonensis. Infect Immun. 1991 Mar;59(3):764–775. doi: 10.1128/iai.59.3.764-775.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Antoine J. C., Prina E., Jouanne C., Bongrand P. Parasitophorous vacuoles of Leishmania amazonensis-infected macrophages maintain an acidic pH. Infect Immun. 1990 Mar;58(3):779–787. doi: 10.1128/iai.58.3.779-787.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Borgers M., Thoné F. Further characterization of phosphatase activities using non-specific substrates. Histochem J. 1976 May;8(3):301–317. doi: 10.1007/BF01003819. [DOI] [PubMed] [Google Scholar]
  4. Chang K. P. Cellular and molecular mechanisms of intracellular symbiosis in leishmaniasis. Int Rev Cytol Suppl. 1983;14:267–305. [PubMed] [Google Scholar]
  5. Chang K. P. Leishmania donovani: promastigote--macrophage surface interactions in vitro. Exp Parasitol. 1979 Oct;48(2):175–189. doi: 10.1016/0014-4894(79)90097-3. [DOI] [PubMed] [Google Scholar]
  6. Horwitz M. A., Maxfield F. R. Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J Cell Biol. 1984 Dec;99(6):1936–1943. doi: 10.1083/jcb.99.6.1936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Horwitz M. A. Phagocytosis of the Legionnaires' disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell. 1984 Jan;36(1):27–33. doi: 10.1016/0092-8674(84)90070-9. [DOI] [PubMed] [Google Scholar]
  8. Horwitz M. A., Silverstein S. C. Influence of the Escherichia coli capsule on complement fixation and on phagocytosis and killing by human phagocytes. J Clin Invest. 1980 Jan;65(1):82–94. doi: 10.1172/JCI109663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Horwitz M. A., Silverstein S. C. Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest. 1980 Sep;66(3):441–450. doi: 10.1172/JCI109874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Horwitz M. A. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med. 1983 Dec 1;158(6):2108–2126. doi: 10.1084/jem.158.6.2108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hubbard A. L., Cohn Z. A. Externally disposed plasma membrane proteins. II. Metabolic fate of iodinated polypeptides of mouse L cells. J Cell Biol. 1975 Feb;64(2):461–479. doi: 10.1083/jcb.64.2.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Mellman I. S., Plutner H., Steinman R. M., Unkeless J. C., Cohn Z. A. Internalization and degradation of macrophage Fc receptors during receptor-mediated phagocytosis. J Cell Biol. 1983 Mar;96(3):887–895. doi: 10.1083/jcb.96.3.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Muller W. A., Steinman R. M., Cohn Z. A. Membrane proteins of the vacuolar system. III. Further studies on the composition and recycling of endocytic vacuole membrane in cultured macrophages. J Cell Biol. 1983 Jan;96(1):29–36. doi: 10.1083/jcb.96.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. North R. J. The localization by electron microscopy of acid phosphatase activity in guinea pig macrophages. J Ultrastruct Res. 1966 Sep;16(1):96–108. doi: 10.1016/s0022-5320(66)80025-4. [DOI] [PubMed] [Google Scholar]
  15. Payne N. R., Horwitz M. A. Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J Exp Med. 1987 Nov 1;166(5):1377–1389. doi: 10.1084/jem.166.5.1377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pimenta P. F., De Souza W. Freeze-fracture and cytochemistry study of the interaction between Leishmania mexicana amazonensis and macrophages. J Submicrosc Cytol Pathol. 1988 Jan;20(1):89–99. [PubMed] [Google Scholar]
  17. Rollins T. E., Smith W. L. Subcellular localization of prostaglandin-forming cyclooxygenase in Swiss mouse 3T3 fibroblasts by electron microscopic immunocytochemistry. J Biol Chem. 1980 May 25;255(10):4872–4875. [PubMed] [Google Scholar]
  18. Shukla S. D., Coleman R., Finean J. B., Michell R. H. Selective release of plasma-membrane enzymes from rat hepatocytes by a phosphatidylinositol-specific phospholipase C. Biochem J. 1980 Apr 1;187(1):277–280. doi: 10.1042/bj1870277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Stochaj U., Flocke K., Mathes W., Mannherz H. G. 5'-Nucleotidases of chicken gizzard and human pancreatic adenocarcinoma cells are anchored to the plasma membrane via a phosphatidylinositol-glycan. Biochem J. 1989 Aug 15;262(1):33–40. doi: 10.1042/bj2620033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tsan M. F., Berlin R. D. Effect of phagocytosis on membrane transport of nonelectrolytes. J Exp Med. 1971 Oct 1;134(4):1016–1035. doi: 10.1084/jem.134.4.1016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wyrick P. B., Brownridge E. A. Growth of Chlamydia psittaci in macrophages. Infect Immun. 1978 Mar;19(3):1054–1060. doi: 10.1128/iai.19.3.1054-1060.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES