1887

Abstract

Murine polyomavirus (MPyV) infection occurs through recognition of sialic acid (SA) residues present on the host cell membrane, but the nature of the molecules involved and the exact role of this interaction in virus cell entry still need to be clarified. In this work, mutations at residues R or H of the MPyV VP1 protein were shown to lead to a complete loss of virus infectivity, which, however, could be restored by lipofection of virus particles into the cytoplasm of the host cells. Using virus-like particles (VLPs), it was demonstrated that the non-infectivity of these mutants was due to impaired cell entry caused by total abrogation of SA-dependent cell binding. This indicates that SA residues are essential primary cell receptors for MPyV. As the 41 integrin has been identified recently as a cell receptor for MPyV, the relationship, if any, was investigated between SA-containing and 41 integrin receptors. The ability of mutants RQ and HQ and wt VLPs to bind to cells overexpressing the 41 integrin was studied in SA-positive (BALB/c 3T3 cells and Pro-5 cells) and SA-deficient (Pro5-derived Lec-2 cells) backgrounds. Overexpression of 41 integrin did not restore binding of mutant VLPs in any of these cell lines or, indeed, that of wt VLPs in a SA-deficient background. Moreover, evidence is provided that overexpression of the sialylated 41 integrin enhances wt VLP cell binding, suggesting that, in addition to its function at a post-attachment level, 41 integrin acts also as one of the SA-containing receptors for initial cell binding.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.19369-0
2003-11-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/11/vir842927.html?itemId=/content/journal/jgv/10.1099/vir.0.19369-0&mimeType=html&fmt=ahah

References

  1. Amati P. 1985; Polyoma regulatory region: a potential probe for mouse cell differentiation. Cell 43:561–562
    [Google Scholar]
  2. Arias C. F., Isa P., Guerrero C. A., Mèndez E., Zàrate S., Lopez T., Espinosa R., Romero P., Lopez S. 2002; Molecular biology of rotavirus cell entry. Arch Med Res 33:356–361
    [Google Scholar]
  3. Arnberg N., Edlund K., Kidd A. H., Wadell G. 2000a; Adenovirus type 37 uses sialic acid as a cellular receptor. J Virol 74:42–48
    [Google Scholar]
  4. Arnberg N., Kidd A. H., Edlund K., Olfat F., Wadell G. 2000b; Initial interactions of subgenus D adenoviruses with A549 cellular receptors: sialic acid versus α v integrins. J Virol 74:7691–7693
    [Google Scholar]
  5. Barton E. S., Chappell J. D., Connolly J. L., Forrest J. C., Dermody T. S. 2001a; Reovirus receptors and apoptosis. Virology 290:173–180
    [Google Scholar]
  6. Barton E. S., Connolly J. L., Forrest J. C., Chappell J. D., Dermody T. S. 2001b; Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening. J Biol Chem 276:2200–2211
    [Google Scholar]
  7. Bauer P. H., Cui C., Liu R., Stehle T., Harrison S. C., DeCaprio J. A., Benjamin T. L. 1999; Discrimination between sialic acid-containing receptors and pseudoreceptors regulates polyomavirus spread in the mouse. J Virol 73:5826–5832 erratum 74, 5746
    [Google Scholar]
  8. Cahan L. D., Singh R., Paulson J. C. 1983; Sialyloligosaccharide receptors of binding variants of polyoma virus. Virology 130:281–289
    [Google Scholar]
  9. Caruso M., Iacobini C., Passananti C., Felsani A., Amati P. 1990; Protein recognition sites in polyomavirus enhancer: formation of a novel site for NF-1 factor in an enhancer mutant and characterization of a site in the enhancer D domain. EMBO J 9:947–955 erratum 9, 3806
    [Google Scholar]
  10. Caruso M., Belloni L., Sthandier O., Amati P., Garcia M. I. 2003; α 4 β 1 integrin acts as a cell receptor for murine polyomavirus at the postattachment level. J Virol 77:3913–3921
    [Google Scholar]
  11. Chen M. H., Benjamin T. 1997; Roles of N -glycans with α 2,6 as well as α 2,3 linked sialic acid in infection by polyoma virus. Virology 233:440–442
    [Google Scholar]
  12. Chomczynski P., Sacchi N. 1987; Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159
    [Google Scholar]
  13. Eckhart W. 1990; Polyomavirinae and their replication. In Virology , 2nd edn. pp  1593–1607 Edited by Fields B. N., Knipe D. M., Howley P. M. New York: Lippincott–Raven;
    [Google Scholar]
  14. Fasbender A., Zabner J., Chillon M., Moninger T. O., Puga A. P., Davidson B. L., Welsh M. J. 1997; Complexes of adenovirus with polycationic polymers and cationic lipids increase the efficiency of gene transfer in vitro and in vivo . J Biol Chem 272:6479–6489
    [Google Scholar]
  15. Forstovà J., Krauzewicz N., Sandig V., Elliott J., Palkovà Z., Strauss M., Griffin B. E. 1995; Polyoma virus pseudocapsids as efficient carriers of heterologous DNA into mammalian cells. Hum Gene Ther 6:297–306
    [Google Scholar]
  16. Freund R., Calderone A., Dawe C. J., Benjamin T. L. 1991a; Polyomavirus tumor induction in mice: effects of polymorphisms of VP1 and large T antigen. J Virol 65:335–341
    [Google Scholar]
  17. Freund R., Garcea R. L., Sahli R., Benjamin T. L. 1991b; A single-amino-acid substitution in polyomavirus VP1 correlates with plaque size and hemagglutination behavior. J Virol 65:350–355
    [Google Scholar]
  18. Fried H., Cahan L. D., Paulson J. C. 1981; Polyoma virus recognizes specific sialyligosaccharide receptors on host cells. Virology 109:188–192
    [Google Scholar]
  19. Garcia M. I., Perez M., Caruso M., Sthandier O., Ferreira R., Cermola M., Macchia C., Amati P. 2000; A mutation in the DE loop of the VP1 protein that prevents polyomavirus transcription and replication. Virology 272:293–301
    [Google Scholar]
  20. Griffith G. R., Consigli R. A. 1986; Cross-linking of a polyomavirus attachment protein to its mouse kidney cell receptor. J Virol 58:773–781
    [Google Scholar]
  21. Herrmann M., von der Lieth C. W., Stehling P., Reutter W., Pawlita M. 1997; Consequences of a subtle sialic acid modification on the murine polyomavirus receptor. J Virol 71:5922–5931
    [Google Scholar]
  22. Irie A., Kamata T., Puzon-McLaughlin W., Takada Y. 1995; Critical amino acid residues for ligand binding are clustered in a predicted β -turn of the third N-terminal repeat in the integrin α 4 and α 5 subunits. EMBO J 14:5550–5556
    [Google Scholar]
  23. Irie A., Kamata T., Takada Y. 1997; Multiple loop structures critical for ligand binding of the integrin α 4 subunit in the upper face of the β -propeller mode 1. Proc Natl Acad Sci U S A 94:7198–7203
    [Google Scholar]
  24. Kelm S., Schauer R. 1997; Sialic acids in molecular and cellular interactions. Int Rev Cytol 175:137–240
    [Google Scholar]
  25. Krauzewicz N., Griffin B. E. 2000; Polyoma and papilloma virus vectors for cancer gene therapy. Adv Exp Med Biol 465:73–82
    [Google Scholar]
  26. Maione R., Passananti C., De Simone V., Delli-Bovi P., Augusti-Tocco G., Amati P. 1985; Selection of mouse neuroblastoma cell-specific polyoma virus mutants with stage differentiative advantages of replication. EMBO J 4:3215–3221
    [Google Scholar]
  27. Marriott S. J., Griffith G. R., Consigli R. A. 1987a; Octyl- β -d-glucopyranoside extracts polyomavirus receptor moieties from the surfaces of mouse kidney cells. J Virol 61:375–382
    [Google Scholar]
  28. Marriott S. J., Roeder D. J., Consigli R. A. 1987b; Anti-idiotypic antibodies to a polyomavirus monoclonal antibody recognize cell surface components of mouse kidney cells and prevent polyomavirus infection. J Virol 61:2747–2753
    [Google Scholar]
  29. McCutchan J. H., Pagano J. S. 1968; Enhancement of the infectivity of simian virus 40 deoxyribonucleic acid with diethylaminoethyl-dextran. J Natl Cancer Inst 41:351–357
    [Google Scholar]
  30. Morgenstern J. P., Land H. 1990; A series of mammalian expression vectors and characterisation of their expression of reported gene in stably and transiently transfected cells. Nucleic Acids Res 18:1068
    [Google Scholar]
  31. Pretzlaff R. K., Xue V. W., Rowin M. E. 2000; Sialidase treatment exposes the β 1-integrin active ligand binding site on HL60 cells and increases binding to fibronectin. Cell Adhes Commun 7:491–500
    [Google Scholar]
  32. Rietzler M., Bittner M., Kolanus W., Schuster A., Holzmann B. 1998; The human WD repeat protein WAIT-1 specifically interacts with the cytoplasmic tails of β 7-integrins. J Biol Chem 273:27459–27466
    [Google Scholar]
  33. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  34. Semel A. C., Seales E. C., Singhal A., Eklund E. A., Colley K. J., Bellis S. L. 2002; Hyposialylation of integrins stimulates the activity of myeloid fibronectin receptors. J Biol Chem 277:32830–32836
    [Google Scholar]
  35. Shih D. T., Edelman J. M., Horwitz A. F., Grunwald G. B., Buck C. A. 1993; Structure/function analysis of the integrin β1 subunit by epitope mapping. J Cell Biol 122:1361–1371
    [Google Scholar]
  36. Soeda E., Krauzewicz N., Cox C., Stokrovà J., Forstovà J., Griffin B. E. 1998; Enhancement by polylysine of transient, but not stable, expression of genes carried into cells by polyoma VP1 pseudocapsids. Gene Ther 5:1410–1419
    [Google Scholar]
  37. Stanley P., Siminovitch L. 1977; Complementation between mutants of CHO cells resistant to a variety of plant lectins. Somatic Cell Genet 3:391–405
    [Google Scholar]
  38. Stanley P., Callibot V., Siminovitch L. 1975; Selection and characterization of eight phenotypically distinct lines of lectin-resistant Chinese hamster ovary cells. Cell 6:121–128
    [Google Scholar]
  39. Stehle T., Harrison S. C. 1996; Crystal structures of murine polyomavirus in complex with straight-chain and branched-chain sialyloligosaccharide receptor fragments. Structure 4:183–194
    [Google Scholar]
  40. Stehle T., Harrison S. C. 1997; High-resolution structure of a polyomavirus VP1-oligosaccharide complex: implications for assembly and receptor binding. EMBO J 16:5139–5148
    [Google Scholar]
  41. Stehle T., Yan Y., Benjamin T. L., Harrison S. C. 1994; Structure of polyomavirus complexed with an oligosaccharide receptor fragment. Nature 369:160–163
    [Google Scholar]
  42. Stray S. J., Cummings R. D., Air G. M. 2000; Influenza virus infection of desialylated cells. Glycobiology 10:649–658
    [Google Scholar]
  43. Twigg A. J., Sherratt D. 1980; Trans-complementable copy-number mutants of plasmid ColE1. Nature 283:216–218
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.19369-0
Loading
/content/journal/jgv/10.1099/vir.0.19369-0
Loading

Data & Media loading...

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