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. 1984 Jan 1;159(1):193–207. doi: 10.1084/jem.159.1.193

Spontaneous internalization of Class I major histocompatibility complex molecules in T lymphoid cells

PMCID: PMC2187213  PMID: 6363594

Abstract

A low proportion of T lymphocytes in normal mouse spleen contains small intracytoplasmic vesicles showing Class I MHC molecules. After stimulation in vitro in a mixed lymphocyte reaction or by addition of Con A, the proportion of T cells with such intracytoplasmic vesicles increases progressively and becomes the majority. Labeling with fluorochrome-conjugated antibodies has shown that the vesicles are formed by internalization of molecules from the plasma membrane. The process is spontaneous and does not require cross-linking by antibodies or other ligands; it is selective inasmuch as other molecules (Thy-1 and T200 antigens) are not included and it is specific since it is not performed by other cells such as B lymphoid cells or fibroblasts. On the whole the process shows similarities with the internalization and recycling of other receptors, such as the receptors for different macromolecules of metabolic or informational significance, as seen in other cells. On the other hand, the specificity of Class I MHC mobilization in T lymphoid cells suggest a role for this process which is related to the immune function of these molecules.

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Selected References

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  1. Anderson R. G., Brown M. S., Beisiegel U., Goldstein J. L. Surface distribution and recycling of the low density lipoprotein receptor as visualized with antireceptor antibodies. J Cell Biol. 1982 Jun;93(3):523–531. doi: 10.1083/jcb.93.3.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Basu S. K., Goldstein J. L., Anderson R. G., Brown M. S. Monensin interrupts the recycling of low density lipoprotein receptors in human fibroblasts. Cell. 1981 May;24(2):493–502. doi: 10.1016/0092-8674(81)90340-8. [DOI] [PubMed] [Google Scholar]
  3. Benacerraf B. Role of MHC gene products in immune regulation. Science. 1981 Jun 12;212(4500):1229–1238. doi: 10.1126/science.6165083. [DOI] [PubMed] [Google Scholar]
  4. Bleil J. D., Bretscher M. S. Transferrin receptor and its recycling in HeLa cells. EMBO J. 1982;1(3):351–355. doi: 10.1002/j.1460-2075.1982.tb01173.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown M. S., Anderson R. G., Basu S. K., Goldstein J. L. Recycling of cell-surface receptors: observations from the LDL receptor system. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 2):713–721. doi: 10.1101/sqb.1982.046.01.068. [DOI] [PubMed] [Google Scholar]
  6. Brown M. S., Anderson R. G., Goldstein J. L. Recycling receptors: the round-trip itinerary of migrant membrane proteins. Cell. 1983 Mar;32(3):663–667. doi: 10.1016/0092-8674(83)90052-1. [DOI] [PubMed] [Google Scholar]
  7. Ciechanover A., Schwartz A. L., Lodish H. F. The asialoglycoprotein receptor internalizes and recycles independently of the transferrin and insulin receptors. Cell. 1983 Jan;32(1):267–275. doi: 10.1016/0092-8674(83)90517-2. [DOI] [PubMed] [Google Scholar]
  8. Emerson S. G., Murphy D. B., Cone R. E. Selective turnover and shedding of H-2K and H-2D antigens is controlled by the major histocompatibility complex. Implications for H-2-restricted recognition. J Exp Med. 1980 Oct 1;152(4):783–795. doi: 10.1084/jem.152.4.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Glimcher L. H., Longo D. L., Green I., Schwartz R. H. Murine syngeneic mixed lymphocyte response. I. Target antigens are self Ia molecules. J Exp Med. 1981 Nov 1;154(5):1652–1670. doi: 10.1084/jem.154.5.1652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grey H. M., Colon S. M., Chesnut R. W. Requirements for the processing of antigen by antigen-presenting B cells. II. Biochemical comparison of the fate of antigen in B cell tumors and macrophages. J Immunol. 1982 Dec;129(6):2389–2395. [PubMed] [Google Scholar]
  11. Guesdon J. L., Ternynck T., Avrameas S. The use of avidin-biotin interaction in immunoenzymatic techniques. J Histochem Cytochem. 1979 Aug;27(8):1131–1139. doi: 10.1177/27.8.90074. [DOI] [PubMed] [Google Scholar]
  12. Huet C., Ash J. F., Singer S. J. The antibody-induced clustering and endocytosis of HLA antigens on cultured human fibroblasts. Cell. 1980 Sep;21(2):429–438. doi: 10.1016/0092-8674(80)90479-1. [DOI] [PubMed] [Google Scholar]
  13. Hütteroth T. H., Cleve H., Litwin S. D., Poulik M. D. The relationship between 2 -microglobulin and immunoglobulin in cultured human lymphoid cell lines. J Exp Med. 1973 Mar 1;137(3):838–843. doi: 10.1084/jem.137.3.838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kearney J. F., Lawton A. R. B lymphocyte differentiation induced by lipopolysaccharide. I. Generation of cells synthesizing four major immunoglobulin classes. J Immunol. 1975 Sep;115(3):671–676. [PubMed] [Google Scholar]
  15. Klein J., Juretic A., Baxevanis C. N., Nagy Z. A. The traditional and a new version of the mouse H-2 complex. Nature. 1981 Jun 11;291(5815):455–460. doi: 10.1038/291455a0. [DOI] [PubMed] [Google Scholar]
  16. Klein J., Widmer M. B., Segall M., Bach F. H. Mixed lymphocyte culture reactivity and H-2 histocompatibility loci differences. Cell Immunol. 1972 Aug;4(4):442–446. doi: 10.1016/0008-8749(72)90045-7. [DOI] [PubMed] [Google Scholar]
  17. Larrick J. W., Cresswell P. Transferrin receptors on human B and T lymphoblastoid cell lines. Biochim Biophys Acta. 1979 Apr 3;583(4):483–490. doi: 10.1016/0304-4165(79)90065-5. [DOI] [PubMed] [Google Scholar]
  18. Ledbetter J. A., Herzenberg L. A. Xenogeneic monoclonal antibodies to mouse lymphoid differentiation antigens. Immunol Rev. 1979;47:63–90. doi: 10.1111/j.1600-065x.1979.tb00289.x. [DOI] [PubMed] [Google Scholar]
  19. Letarte M., Meghji G. An Ia+ subpopulation of activated spleen T cells is generated by concanavalin A stimulation. J Immunol. 1980 Jul;125(1):378–383. [PubMed] [Google Scholar]
  20. Marshak-Rothstein A., Fink P., Gridley T., Raulet D. H., Bevan M. J., Gefter M. L. Properties and applications of monoclonal antibodies directed against determinants of the Thy-1 locus. J Immunol. 1979 Jun;122(6):2491–2497. [PubMed] [Google Scholar]
  21. Monos D. S., Cooper H. L. Rapid turnover of HLA proteins in quiescent lymphocytes: proposed connection with immunologic surveillance. J Immunol. 1983 Jul;131(1):341–346. [PubMed] [Google Scholar]
  22. Nussenzweig M. C., Steinman R. M. Contribution of dendritic cells to stimulation of the murine syngeneic mixed leukocyte reaction. J Exp Med. 1980 May 1;151(5):1196–1212. doi: 10.1084/jem.151.5.1196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ozato K., Ebert J. D. Retention of intact concanavalin A and Lens culinaris lectin in transformed lymphoblasts during mitogenic response. Cell Immunol. 1978 May;37(2):273–284. doi: 10.1016/0008-8749(78)90196-x. [DOI] [PubMed] [Google Scholar]
  24. Ozato K., Mayer N., Sachs D. H. Hybridoma cell lines secreting monoclonal antibodies to mouse H-2 and Ia antigens. J Immunol. 1980 Feb;124(2):533–540. [PubMed] [Google Scholar]
  25. 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]
  26. Pearse B. M., Bretscher M. S. Membrane recycling by coated vesicles. Annu Rev Biochem. 1981;50:85–101. doi: 10.1146/annurev.bi.50.070181.000505. [DOI] [PubMed] [Google Scholar]
  27. Steinman R. M., Mellman I. S., Muller W. A., Cohn Z. A. Endocytosis and the recycling of plasma membrane. J Cell Biol. 1983 Jan;96(1):1–27. doi: 10.1083/jcb.96.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tartakoff A. M. Perturbation of vesicular traffic with the carboxylic ionophore monensin. Cell. 1983 Apr;32(4):1026–1028. doi: 10.1016/0092-8674(83)90286-6. [DOI] [PubMed] [Google Scholar]
  29. Victor C., Bona C., Pernis B. Idiotypes on B lymphocytes: association with immunoglobulins. J Immunol. 1983 Apr;130(4):1819–1825. [PubMed] [Google Scholar]
  30. Yahara I., Edelman G. M. Modulation of lymphocyte receptor mobility by locally bound concanavalin A. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1579–1583. doi: 10.1073/pnas.72.4.1579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]

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