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
2020-07-15
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. Cell43:561–562
    [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 Res33:356–361
    [Google Scholar]
  3. Arnberg N., Edlund K., Kidd A. H., Wadell G.. 2000a; Adenovirus type 37 uses sialic acid as a cellular receptor. J Virol74:42–48
    [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 Virol74:7691–7693
    [Google Scholar]
  5. Barton E. S., Chappell J. D., Connolly J. L., Forrest J. C., Dermody T. S.. 2001a; Reovirus receptors and apoptosis. Virology290:173–180
    [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 Chem276:2200–2211
    [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 Virol73:5826–5832 erratum 74, 5746
    [Google Scholar]
  8. Cahan L. D., Singh R., Paulson J. C.. 1983; Sialyloligosaccharide receptors of binding variants of polyoma virus. Virology130:281–289
    [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 J9:947–955 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 Virol77:3913–3921
    [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. Virology233:440–442
    [Google Scholar]
  12. Chomczynski P., Sacchi N.. 1987; Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem162:156–159
    [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 Chem272:6479–6489
    [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 Ther6:297–306
    [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 Virol65:335–341
    [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 Virol65:350–355
    [Google Scholar]
  18. Fried H., Cahan L. D., Paulson J. C.. 1981; Polyoma virus recognizes specific sialyligosaccharide receptors on host cells. Virology109:188–192
    [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. Virology272:293–301
    [Google Scholar]
  20. Griffith G. R., Consigli R. A.. 1986; Cross-linking of a polyomavirus attachment protein to its mouse kidney cell receptor. J Virol58:773–781
    [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 Virol71:5922–5931
    [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 J14:5550–5556
    [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 A94:7198–7203
    [Google Scholar]
  24. Kelm S., Schauer R.. 1997; Sialic acids in molecular and cellular interactions. Int Rev Cytol175:137–240
    [Google Scholar]
  25. Krauzewicz N., Griffin B. E.. 2000; Polyoma and papilloma virus vectors for cancer gene therapy. Adv Exp Med Biol465:73–82
    [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 J4:3215–3221
    [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 Virol61:375–382
    [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 Virol61:2747–2753
    [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 Inst41:351–357
    [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 Res18:1068
    [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 Commun7:491–500
    [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 Chem273:27459–27466
    [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 Chem277:32830–32836
    [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 Biol122:1361–1371
    [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 Ther5:1410–1419
    [Google Scholar]
  37. Stanley P., Siminovitch L.. 1977; Complementation between mutants of CHO cells resistant to a variety of plant lectins. Somatic Cell Genet3:391–405
    [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. Cell6:121–128
    [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. Structure4:183–194
    [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 J16:5139–5148
    [Google Scholar]
  41. Stehle T., Yan Y., Benjamin T. L., Harrison S. C.. 1994; Structure of polyomavirus complexed with an oligosaccharide receptor fragment. Nature369:160–163
    [Google Scholar]
  42. Stray S. J., Cummings R. D., Air G. M.. 2000; Influenza virus infection of desialylated cells. Glycobiology10:649–658
    [Google Scholar]
  43. Twigg A. J., Sherratt D.. 1980; Trans-complementable copy-number mutants of plasmid ColE1. Nature283:216–218
    [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...

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