1887

Abstract

Simian virus 40 (SV40) binds to MHC class I molecules anywhere on the cell surface and then enters through caveolae. The fate of class I molecules after SV40 binding is not known. Sensitivity of I-surface-labelled class I molecules to papain cleavage was used to distinguish internalized class I molecules from class I molecules remaining at the cell surface. Whereas the caveolae-enriched membrane microdomain was found to also be enriched for class I molecules, no internalized papain-resistant I-surface-labelled class I molecules could be detected at any time in either control cells or in cells preadsorbed with saturating amounts of SV40. Instead, I-surface-labelled class I molecules, as well as preadsorbed I-labelled anti-class I antibodies, accumulated in the medium, coincident with the turnover of class I molecules at the cell surface. The class I heavy chains that accumulated in the medium were truncated and their release was specifically prevented by the metalloprotease inhibitor 1,10-phenanthroline. Thus, whereas class I molecules mediate SV40 binding, they do not appear to mediate SV40 entry.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-79-6-1469
1998-06-01
2022-09-30
Loading full text...

Full text loading...

/deliver/fulltext/jgv/79/6/9634090.html?itemId=/content/journal/jgv/10.1099/0022-1317-79-6-1469&mimeType=html&fmt=ahah

References

  1. Abdel Motal U. M., Zhou X., Joki A., Siddiqi A. R., Srinivasa B. R., Stenvall K., Dahmen J., Jondal M. 1993; Major histocompatibility complex class I-binding peptides are recycled to the cell surface after internalization. European Journal of Immunology 23:3224–3229
    [Google Scholar]
  2. Anderson H. A., Chen Y., Norkin L. C. 1996; Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Molecular Biology of the Cell 7:1825–1834
    [Google Scholar]
  3. Anderson R. G. W. 1993a; Caveolae: where incoming and outgoing messengers meet. Proceedings of the National Academy of Sciences, USA 90:10909–10913
    [Google Scholar]
  4. Anderson R. G. W. 1993b; Potocytosis of small molecules and ions by caveolae. Trends in Cell Biology 3:69–72
    [Google Scholar]
  5. Aragnol D., Malissen B., Schiff C., Piron M. A., Leserman L. D. 1986; Endocytosis of class I molecules studied using B cell-B lymphoma and B cell-T lymphoma hybrids. Journal of Immunology 137:3347–3353
    [Google Scholar]
  6. Atwood W. J., Norkin L. C. 1989; Class I major histocompatibility proteins as cell surface receptors for simian virus 40. Journal of Virology 63:4474–4477
    [Google Scholar]
  7. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248–254
    [Google Scholar]
  8. Breau W. C., Atwood W. J., Norkin L. C. 1992; Class I major histocompatibility proteins are an essential component of the simian virus 40 receptor. Journal of Virology 66:2037–2045
    [Google Scholar]
  9. Brown D. A., Rose J. K. 1992; Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533–544
    [Google Scholar]
  10. Capps G. G., VanKampen M., Ward C. L., Zuniga M. C. 1989; Endocytosis of the class I major histocompatibility antigen via a phorbol myristate acetate-inducible pathway is a cell-specific phenomenon and requires the cytoplasmic domain. Journal of Cell Biology 108:1317–1329
    [Google Scholar]
  11. Cox J. H., Yewdell J. W., Eisenlohr L. C., Johnson P. R., Bennink J. R. 1990; Antigen presentation requires transport of MHC class I molecules from the endoplasmic reticulum. Science 247:715–718
    [Google Scholar]
  12. Dangoria N. S., Breau W. C., Anderson H. A., Cishek D. M., Norkin L. C. 1996; Extracellular simian virus 40 induces an ERK/MAPK-independent signaling pathway that activates primary response genes and promotes virus entry. Journal of General Virology 77:2173–2182
    [Google Scholar]
  13. Dasgupta J. S., Watkins S., Slayter H., Yunis E. J. 1988; Receptor like nature of class I HLA: endocytosis via coated pits. Journal of Immunology 141:2577–2580
    [Google Scholar]
  14. Demaria S., Schwab R., Bushkin Y. 1992; The origin and fate of β 2m-free MHC class I molecules induced on activated T cells. Cellular Immunology 142:103–113
    [Google Scholar]
  15. Demaria S., Schwab R., Gottesman S. R. S., Bushkin Y. 1994; Soluble β 2-microglobulin-free class I heavy chains are released from the surface of activated and leukemia cells by a metalloprotease. Journal of Biological Chemistry 269:6689–6694
    [Google Scholar]
  16. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Buckhart M., Di Marzio P., Marmon S., Sutton R. E., Hill C. M., Davis C. B., Peiper S. C., Schall T. J., Littman D. R., Landau N. R. 1996; Identification of a major co-receptor for primary isolates of HIV-1. Nature 281:661–666
    [Google Scholar]
  17. Dragic T., Litwin V., Allaway G. P., Martin S. R., Huang Y., Nagashima K. A., Cayanan C., Maddon P. J., Koup R. A., Moore J. P., Paxton W. A. 1996; HIV entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 281:667–673
    [Google Scholar]
  18. Eicholtz T., Vossebeld P., van Overveld M., Ploegh H. 1992; Activation of protein kinase C accelerates internalization of transferrin receptor but not of major histocompatibility complex class I, independent of their phosphorylation status. Journal of Biological Chemistry 267:22490–22495
    [Google Scholar]
  19. Goldstein J. L., Brown M. S., Anderson R. G. W., Russell D. W. W., Schneider W. J. 1985; Receptor mediated endocytosis: concepts emerging from the LDL receptor system. Annual Review of Cell Biology 1:1–39
    [Google Scholar]
  20. Harlow E., Lane D. 1988 Antibodies: A Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  21. Hochman J., Jiang H, Edidin M., Pernis B. 1991; Endocytosis and dissociation of class I MHC molecules with fluorescent β-2 microglobulin. Journal of Immunology 146:1862–1867
    [Google Scholar]
  22. Huet C., Ash J. F., Singer S. J. 1980; The antibody-induced clustering and endocytosis of HLA antigens on cultured human fibroblasts. Cell 21:429–438
    [Google Scholar]
  23. Kartenbeck J., Stukenbrok H., Helenius A. 1989; Endocytosis of simian virus 40 into the endoplasmic reticulum. Journal of Cell Biology 109:2721–2729
    [Google Scholar]
  24. Lisanti M. P., Scherer P. E., Tang Z., Sargiacomo M. 1994a; Caveolae, caveolin, and caveolin-rich membrane domains : a signaling hypothesis. Trends in Cell Biology 4:231–235
    [Google Scholar]
  25. Lisanti M. P., Scherer P. E., Vidugiriene J., Tang Z. L., Hermanowski-Vosatka A., Tu Y. H., Cook R. F., Sargiacomo M. 1994b; Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source : implications for human disease. Journal of Cell Biology 126:111–126
    [Google Scholar]
  26. Ljunggren H. G., Stam J. N., Öhlen C., Neefjes J. J., Häglund P., Heemels M. T., Bastin J., Schumacher T. N. M., Townsend A., Karre K., Ploegh H. L. 1990; Empty class I molecules come out in the cold. Nature 346:476–480
    [Google Scholar]
  27. McClain D., Fuller A. O. 1994; Cell-specific kinetics and efficiency of herpes simplex type 1 entry are determined by two distinct phases of attachment. Virology 19:690–702
    [Google Scholar]
  28. Machy P., Truneh A., Gennaro D., Hoffstein S. 1987; Major histocompatibility complex class I molecules internalized via coated pits in T lymphocytes. Nature 328:724–726
    [Google Scholar]
  29. Marsh M., Helenius A. 1989; Virus entry into animal cells. Advances in Virus Research 36:107–151
    [Google Scholar]
  30. Montesano R., Roth J., Robert A., Orci L. 1982; Non-coated membrane invaginations are involved in binding and internalization of tetanus toxins. Nature 296:651–653
    [Google Scholar]
  31. Neefjes J. J., Breur-Vriesendorp B. S., Van Seventer G. A., Ivanyi P., Ploegh H. L. 1986; An improved biochemical method for the analysis of HLA class I antigens. Definition of new HLA-class I subtypes. Human Immunology 16:169–181
    [Google Scholar]
  32. Neefjes J. J., Stollarz V., Peters P. J., Geuze H. J., Ploegh H. L. 1990; The biosynthetic pathway of MHC class II but not MHC class I intersects the endocytic route. Cell 61:171–183
    [Google Scholar]
  33. Neefjes J. J., Smit L., Gehrmann M., Ploegh H. L. 1992; The fate of the three subunits of major histocompatibility complex class I molecules. European Journal of Immunology 22:1609–1614
    [Google Scholar]
  34. Norkin L. C. 1995; Virus receptors : implications for pathogenesis and the design of antiviral agents. Clinical Microbiology Reviews 8:293–315
    [Google Scholar]
  35. Norkin L. C., Anderson H. A. 1996; Multiple stages of virus-receptor interactions as shown by simian virus 40. Advances in Experimental Medicine and Biology 408:159–167
    [Google Scholar]
  36. Ortiz-Navarret V., Hämmerling G. J. 1991; Surface appearance and instability of empty H-2 class I molecules under physiologic conditions. Proceeding of the National Academy of Sciences, USA 88:3594–3597
    [Google Scholar]
  37. Parham P., Bainstable C., Bodner W. F. 1979; Use of monoclonal antibody (W6/32) in structural studies of HLA-A, B, C antigens. Journal of Immunology 123:342–349
    [Google Scholar]
  38. Philips D. R., Morrison M. 1970; The arrangement ofproteins in the human erythrocyte membrane. Biochemical and Biophysical Research Communications 40:284–289
    [Google Scholar]
  39. Powers J., Harper J. 1986; Inhibitors of metalloproteases. In Proteinase Inhibitors pp. 219–300 Barrett A., Salveson G. Edited by Amsterdam: Elsevier;
    [Google Scholar]
  40. Reid P. A., Watts C. 1990; Cycling of cell-surface MHC glycoproteins through primaquine sensitive intracellular compartments. Nature 346:655–657
    [Google Scholar]
  41. Rock K. L., Rothstein L. E., Gamble S. R., Benacerraf B. 1990; Reassociation with β 2-microglobulin is necessary for Kb class I major histocompatibility complex binding of exogenous peptides. Proceedings of the National Academy of Sciences, USA 87:7517–7521
    [Google Scholar]
  42. Rothberg K. G., Heuser J. E., Donzell W. C., Ying Y.-S., Glenney J. R., Anderson R. G. W. 1992; Caveolin, a protein component of caveolae membrane coats. Cell 68:673–682
    [Google Scholar]
  43. Rougon G., Ceard B., Van Rietscholen J., Jordan B., Barbet J. 1984; Induction with a synthetic peptide of antibodies to HLA class I C-terminal intracytoplasmic region. Molecular Immunology 21:461–468
    [Google Scholar]
  44. Schnitzer J. E., Liu J., Oh P. 1995a; Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP,NSF,SNAP, annexins, and GTPases. Journal of Biological Chemistry 270:14399–14404
    [Google Scholar]
  45. Schnitzer J. E., McIntosh D. P., Dvorak A. M., Liu J., Oh P. 1995b; Separation of caveolae from associated microdomains of GPI-anchored proteins. Science 269:1435–1439
    [Google Scholar]
  46. Schnitzer J. E., Oh P., McIntosh D. P. 1996; Role of GTP hydrolsis in fission of caveolae directly from plasma membranes. Science 274:239–242
    [Google Scholar]
  47. Simionescu M., Simionescu N., Palade G. E. 1982; Differentiated microdomains on the luminal surface of capillary endothelium: distribution of lectin receptors. Journal of Cell Biology 94:406–413
    [Google Scholar]
  48. Song K. S., Li S., Okamoto T., Quilliam L. A., Sargiacomo M., Lisanti M. P. 1996; Co-purification and direct interaction of ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae membranes. Journal of Biological Chemistry 271:9690–9697
    [Google Scholar]
  49. Stang E., Kartenbeck J., Parton R. G. 1997; Major histo-compatibility complex class I molecules mediate association of SV40 with caveolae. Molecular Biology of the Cell 8:47–57
    [Google Scholar]
  50. Stolz D. B., Jacobson B. S. 1991; Macro- and microvascular endothelial cells in vitro; maintenance of biochemical heterogeneity despite loss of ultrastructural characteristics. In Vitro Cell and Developmental Biology 27A:169–181
    [Google Scholar]
  51. Tse D. B., Pernis B. 1984; Spontaneous internalization of class I major histocompatibility complex molecules in T lymphoid cells. Journal of Experimental Medicine 159:193–207
    [Google Scholar]
  52. Vega M. A., Strominger J. L. 1989; Constitutive endocytosis of HLA class I antigens requires a specific portion of the intracytoplasmic tail that shares structural features with other endocytosed molecules. Proceedings of the National Academy of Sciences, USA 86:2688–2692
    [Google Scholar]
  53. Wickham T., Mathins P., Cheresh P., Nimerow G. 1993; Integrins AvB3 and AvB5 promote adenovirus internalization but not virus attachment. Cell 73:309–314
    [Google Scholar]
  54. Yewdell J. W., Bennink J. R. 1992; Cell biology of antigen processing and presentation to MHC class I restricted T lymphocytes. Advances in Immunology 52:1–124
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-79-6-1469
Loading
/content/journal/jgv/10.1099/0022-1317-79-6-1469
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error