1887

Abstract

Annexin II has been identified as a human cytomegalovirus (HCMV)-binding protein, shown to be a component of purified virions and proposed as a cellular receptor for the virus. In addition, annexin II is capable of associating with the major HCMV envelope glycoprotein, gB (gpUL55). As one approach to examine the role of annexin II in virus entry, a high-titre polyclonal annexin II-specific antibody was produced and its effects in virus entry and cell-to-cell spread assays were tested. This anti-annexin II serum recognized virion and cell surface annexin II and annexin II-derived peptides. Recombinant annexin II, with characteristic calcium- and phospholipid-binding activities, was also examined. Pretreatment of cells, virions or both with polyclonal anti-annexin II serum, affinity-purified anti-annexin II antibodies or recombinant annexin II protein prior to infection was inconsequential to the entry of HCMV into fibroblasts. HCMV was also able to dose-dependently penetrate annexin II-deficient 293 cells. Furthermore, the spread of HCMV from cell to cell was not inhibited in the presence of polyclonal anti-annexin II antibodies or exogenous annexin II protein. These experiments do not support a direct role of annexin II in virus entry or spread. Alternative roles for the gB-annexin II interaction are proposed.

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1999-07-01
2024-03-28
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References

  1. Adlish J. D., Lahijani R. S., St Jeor S. C. 1990; Identification of a putative cell receptor for human cytomegalovirus. Virology 176:337–345
    [Google Scholar]
  2. Blackwood R. A., Ernst J. D. 1990; Characterization of Ca2(+)-dependent phospholipid binding, vesicle aggregation and membrane fusion by annexins. Biochemical Journal 266:195–200
    [Google Scholar]
  3. Bold S., Ohlin M., Garten W., Radsak K. 1996; Structural domains involved in human cytomegalovirus glycoprotein B-mediated cell-cell fusion. Journal of General Virology 77:2297–2302
    [Google Scholar]
  4. Boyle K. A., Compton T. 1998; Receptor-binding properties of a soluble form of human cytomegalovirus glycoprotein B. Journal of Virology 72:1826–1833
    [Google Scholar]
  5. Boyle K. A., Pietropaolo R. L., Compton T. 1999; Engagement of the cellular receptor for glycoprotein B of human cytomegalovirus activates the interferon-responsive pathway. Molecular and Cellular Biology 19:3607–3613
    [Google Scholar]
  6. Britt W. J. 1984; Neutralizing antibodies detect a disulfide-linked glycoprotein complex within the envelope of human cytomegalovirus. Virology 135:369–378
    [Google Scholar]
  7. Britt W. J., Vugler L., Butfiloski E. J., Stephens E. B. 1990; Cell surface expression of human cytomegalovirus (HCMV) gp55-116 (gB): use of HCMV-recombinant vaccinia virus-infected cells in analysis of the human neutralizing antibodyresponse. JournalofVirology 64:1079–1085
    [Google Scholar]
  8. Burgoyne R. D. 1988; Calpactin in exocytosis. Nature 331:20
    [Google Scholar]
  9. Cesarman G. M., Guevara C. A., Hajjar K. A. 1994; An endothelial cell receptor for plasminogen/tissue plasminogen activator (t-PA). II. Annexin II-mediated enhancement of t-PA-dependent plasminogen activation. Journal of Biological Chemistry 269:21198–21203
    [Google Scholar]
  10. Chung C. Y., Erickson H. P. 1994; Cell surface annexin II is a high affinity receptor for the alternatively spliced segment of tenascin-C. Journal of Cell Biology 126:539–548
    [Google Scholar]
  11. Compton T. 1993; An immortalized human fibroblast cell line is permissive for human cytomegalovirus infection. Journal of Virology 67:3644–3648
    [Google Scholar]
  12. Compton T. 1995; Towards a definition of the HCMV entry pathway. Scandinavian Journal of Infectious Diseases 99:30–32
    [Google Scholar]
  13. Crompton M. R., Moss S. E., Crumpton M. J. 1988; Diversity in the lipocortin/calpactin family. Cell 55:1–3
    [Google Scholar]
  14. Compton T., Nepomuceno R. R., Nowlin D. M. 1992; Human cytomegalovirus penetrates host cells by pH-independent fusion at the cell surface. Virology 191:387–395
    [Google Scholar]
  15. Compton T., Nowlin D. M., Cooper N. R. 1993; Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 193:834–841
    [Google Scholar]
  16. Drust D. S., Creutz C. E. 1988; Aggregation of chromaffin granules by calpactin at micromolar levels of calcium. Nature 331:88–91
    [Google Scholar]
  17. Evans T. C. Jr, Nelsestuen G. L. 1994; Calcium and membranebinding properties of monomeric and multimeric annexin II. Biochemistry 33:13231–13238
    [Google Scholar]
  18. Hajjar K. A. 1993; Homocysteine-induced modulation of tissue plasminogen activator binding to its endothelial cell membrane receptor. Journal of Clinical Investigation 91:2873–2879
    [Google Scholar]
  19. Hajjar K. A., Harpel P. C., Jaffe E. A., Nachman R. L. 1986; Binding of plasminogen to cultured human endothelial cells. Journal of Biological Chemistry 261:11656–11662
    [Google Scholar]
  20. Hajjar K. A., Jacovina A. T., Chacko J. 1994; An endothelial cell receptor for plasminogen/tissue plasminogen activator. I. Identity with annexin II. Journal of Biological Chemistry 269:21191–21197
    [Google Scholar]
  21. Harder T., Gerke V. 1993; The subcellular distribution of early endosomes is affected by the annexin II2p11(2) complex. Journal of Cell Biology 123:1119–1132
    [Google Scholar]
  22. Harder T., Gerke V. 1994; The annexin II(2)p11(2) complex is the major protein component of the Triton X-100-insoluble low-density fraction prepared from MDCK cells in the presence of Ca2 +. Biochimica et Biophysica Acta 1223:375–382
    [Google Scholar]
  23. Harlow E., Lane D. 1988; Storing and purifying antibodies. In Antibodies A Laboratory Manual pp 283–318 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  24. Jost M., Weber K., Gerke V. 1994; Annexin II contains two types of Ca(2+)-binding sites. Biochemical Journal 298:553–559
    [Google Scholar]
  25. Keay S., Baldwin B. 1992; The human fibroblast receptor for gp86 of human cytomegalovirus is a phosphorylated glycoprotein. Journal of Virology 66:4834–4838
    [Google Scholar]
  26. Keay S., Merigan T. C., Rasmussen L. 1989; Identification of cell surface receptors for the 86-kilodalton glycoprotein of human cytomegalovirus. Proceedings of the National Academy of Sciences, USA 86:10100–10103
    [Google Scholar]
  27. Ma A. S., Bell D. J., Mittal A. A., Harrison H. H. 1994; Immuno-cytochemical detection of extracellular annexin II in cultured human skin keratinocytes and isolation of annexin II isoforms enriched in the extracellular pool. Journal of Cell Science 107:1973–1984
    [Google Scholar]
  28. Marriott G., Kirk W. R., Johnsson N., Weber K. 1990; Absorption and fluorescence spectroscopic studies of the Ca2(+)-dependent lipid binding protein p36: the annexin repeat as the Ca2+ binding site. Biochemistry 29:7004–7011
    [Google Scholar]
  29. Moss S. E. 1992; The annexins. In The Annexins pp 1–10 Edited by Moss S. E. Chapel Hill, USA: Portland Press;
    [Google Scholar]
  30. Neyts J., Snoeck R., Schols D., Balzarini J., Esko J. D., Van Schepdael A., De Clercq E. 1992; Sulfated polymers inhibit the interaction of human cytomegalovirus with cell surface heparan sulfate. Virology 189:48–58
    [Google Scholar]
  31. Nowlin D. M., Cooper N. R., Compton T. 1991; Expression of a human cytomegalovirus receptor correlates with infectibility of cells. Journal of Virology 65:3114–3121
    [Google Scholar]
  32. Osborn M., Johnsson N., Wehland J., Weber K. 1988; The submembranous location of p11 and its interaction with the p36 substrate of pp60 src kinase in situ. Experimental Cell Research 175:81–96
    [Google Scholar]
  33. Pietropaolo R. L., Compton T. 1997; Direct interaction between human cytomegalovirus glycoprotein B and cellular annexin II. Journal of Virology 71:9803–9807
    [Google Scholar]
  34. Reutelingsperger C. P. 1994; The annexins. Lupus 3:213–216
    [Google Scholar]
  35. Soderberg C., Giugni T. D., Zaia J. A., Larsson S., Wahlberg J. M., Moller E. 1993; CD13 (human aminopeptidase-N) mediates human cytomegalovirus infection. Journal of Virology 67:6576–6585
    [Google Scholar]
  36. Spaete R. R., Thayer R. M., Probert W. S., Masiarz F. R., Chamberlain S. H., Rasmussen L., Merigan T. C., Pachl C. 1988; Human cytomegalovirus strain Towne glycoprotein B is processed by proteolytic cleavage. Virology 167:207–225
    [Google Scholar]
  37. Taylor H. P., Cooper N. R. 1990; The human cytomegalovirus receptor on fibroblasts is a 30-kilodalton membrane protein. Journal of Virology 64:2484–2490
    [Google Scholar]
  38. Thiel C., Osborn M., Gerke V. 1992; The tight association of the tyrosine kinase substrate annexin II with the submembranous cyto-skeleton depends on intact p11-and Ca(2 +)-binding sites. Journal of Cell Science 103:733–742
    [Google Scholar]
  39. Tooze J., Hollinshead M., Reis B., Radsak K., Kern H. 1993; Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. European Journal of Cell Biology 60:163–178
    [Google Scholar]
  40. Tressler R. J., Nicolson G. L. 1992; Butanol-extractable and detergent-solubilized cell surface components from murine large cell lymphoma cells associated with adhesion to organ microvessel endothelial cells. Journal of Cellular Biochemistry 48:162–171
    [Google Scholar]
  41. Tressler R. J., Updyke T. V., Yeatman T., Nicolson G. L. 1993; Extracellular annexin II is associated with divalent cation-dependent tumor cell-endothelial cell adhesion of metastatic RAW117 large-cell lymphoma cells. Journal of Cellular Biochemistry 53:265–276
    [Google Scholar]
  42. Wentworth B. B., French L. 1970; Plaque assay of cytomegalovirus strains of human origin. Proceedings of the Society for Experimental Biology and Medicine 135:253–259
    [Google Scholar]
  43. Wright J. F., Kurosky A., Wasi S. 1994; An endothelial cell-surface form of annexin II binds human cytomegalovirus. Biochemical and Biophysical Research Communications 198:983–989
    [Google Scholar]
  44. Wright J. F., Kurosky A., Pryzdial E. L., Wasi S. 1995; Host cellular annexin II is associated with cytomegalovirus particles isolated from cultured human fibroblasts. Journal of Virology 69:4784–4791
    [Google Scholar]
  45. Yeatman T. J., Updyke T. V., Kaetzel M. A., Dedman J. R., Nicolson G. L. 1993; Expression of annexins on the surfaces of non-metastatic and metastatic human and rodent tumor cells. Clinical & Experimental Metastasis 11:37–44
    [Google Scholar]
  46. Zhu H., Cong J. P., Shenk T. 1997; Use of differential display analysis to assess the effect of human cytomegalovirus infection on the accumulation of cellular RNAs: induction of interferon-responsive RNAs. Proceedings of the National Academy of Sciences, USA 94:13985–13990
    [Google Scholar]
  47. Zokas L., Glenney J. R. J. 1987; The calpactin light chain is tightly linked to the cytoskeletal form of calpactin I: studies using monoclonal antibodies to calpactin subunits. Journal of Cell Biology 105:2111–2121
    [Google Scholar]
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