1887

Journal of General Virology header logo

Volume 84, Issue 11

Cellular receptor interactions of C-cluster human group A coxsackieviruses Free

Abstract

The cellular receptor complex of coxsackievirus A21 (CVA21), a C-cluster human enterovirus, is formed by the subtle interaction of individual cellular receptors, decay accelerating factor (DAF) and intercellular adhesion molecule-1 (ICAM-1). In this receptor complex, DAF functions in the membrane sequestration of the virus, while the role of ICAM-1 is as the functional cellular internalization receptor. However, despite the elucidation of the CVA21–cell receptor interactions, there have been few definite investigations into cellular receptor usage of other coxsackie A viruses (CVAs) belonging to the C-cluster. In the present study, radiolabelled virus-binding assays demonstrated that CVA13, -15, -18 and -20, a subset of the human enterovirus C-cluster, bind directly to surface-expressed ICAM-1, but not to surface-expressed DAF. Furthermore, lytic infection of ICAM-1-expressing rhabdomyosarcoma (RD) cells by this C-cluster subset of viruses was inhibited by specific ICAM-1 monoclonal antibody blockade, except for that of CVA20. Despite possessing ICAM-1-binding capabilities, CVA20 employed an as yet unidentified internalization receptor for cell entry and subsequent productive lytic infection of ICAM-1-negative RD cells. In a further example of C-cluster cellular receptor heterogeneity, CVA13 exhibited significant binding to the surface of CHO cells expressing neither DAF nor ICAM-1. Despite a common receptor usage of ICAM-1 by this subset of C-cluster CVAs, the amino acid residues postulated to represent the ICAM-1-receptor footprint were not conserved.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.19329-0
2003-11-01
2023-06-09
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/11/vir843041.html?itemId=/content/journal/jgv/10.1099/vir.0.19329-0&mimeType=html&fmt=ahah

References

  1. Belnap D. M., McDermott B. M., Filman D. J., Cheng N., Trus B. L., Zuccola H. J., Racaniello V. R., Hogle J. M., Steven A. C. 2000; Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc Natl Acad Sci U S A 97:73–78
     [Google Scholar]
  2. Berendt A. R., McDowell A., Craig A. G., Bates P. A., Sternberg M. J. E., Marsh K., Newbold C. I., Hogg N. 1992; The binding site on ICAM-1 for Plasmodium falciparum -infected erythrocytes overlaps, but is distinct from the LFA-1 binding site. Cell 68:71–81
     [Google Scholar]
  3. Bergelson J. M., Chan M., Solomon K. R., St John N. F., Lin H., Finberg R. W. 1994; Decay-accelerating factor (CD55), a glycosylphosphatidylinositol-anchored complement regulatory protein, is a receptor for several echoviruses. Proc Natl Acad Sci U S A 91:6245–6248
     [Google Scholar]
  4. Colonno R. J., Callahan P. L., Long W. J. 1986; Isolation of a monoclonal antibody that blocks attachment of the major group of human rhinoviruses. J Virol 57:7–12
     [Google Scholar]
  5. Colonno R. J., Condra J. H., Mizutani S., Callahan P. C., Davies M. E., Murcko M. A. 1988; Evidence for the direct involvement of the rhinovirus canyon in receptor binding. Proc Natl Acad Sci U S A 85:5449–5453
     [Google Scholar]
  6. Couch R. B., Cate T. R., Gerone P. J., Fleet W. F., Lang D. J., Griffith W. R., Knight V. 1965; Production of illness with a small-particle aerosol of coxsackie A21. J Clin Invest 44:535–542
     [Google Scholar]
  7. Coyne K. E., Hall E. S., Thompson M. A., Arce M. A., Kinoshoita T., Fujita T., Anstee D. J., Rosse W., Lublin D. M. 1992; Mapping of epitopes, glycosylation sites, and complement regulatory domains in human decay accelerating factor. J Immunol 149:2906–2913
     [Google Scholar]
  8. Filman D. J., Wien M. W., Cunningham J. A., Bergelson J. M., Hogle J. M. 1998; Structure determination of echovirus 1. Acta Crystallogr D Biol Crystallogr 54:1261–1272
     [Google Scholar]
  9. Goodfellow I. G., Sioofy A. B., Powell R. M., Evans D. J. 2001; Echoviruses bind heparan sulfate at the cell surface. J Virol 75:4918–4921
     [Google Scholar]
  10. Greve J. M., Davis G., Meyer A. M., Forte C. P., Yost S. C., Marlor C. W., Kamarck M. E., McClelland A. 1989; The major human rhinovirus receptor is ICAM-1. Cell 56:839–847
     [Google Scholar]
  11. He Y., Chipman P. R., Howitt J. 7 other authors 2001; Interaction of coxsackievirus B3 with the full length coxsackievirus–adenovirus receptor. Nat Struct Biol 8:874–878
     [Google Scholar]
  12. He Y., Lin F., Chipman P., Bator C. M., Baker T. S., Shoham M., Kuhn R. J., Medof E. M., Rossmann M. G. 2002; Structure of decay-accelerating factor bound to echovirus 7: a virus receptor complex. Proc Natl Acad Sci U S A 99:10325–10329
     [Google Scholar]
  13. Hughes P. J., North C., Minor P. D., Stanway G. 1989; The complete nucleotide sequence of coxsackievirus A21. J Gen Virol 70:2943–2952
     [Google Scholar]
  14. Karnauchow T. M., Dawe S., Lublin D. M., Dimock K. 1998; Short consensus repeat domain 1 of decay-accelerating factor is required for enterovirus 70 binding. J Virol 72:9380–9383
     [Google Scholar]
  15. Kolatkar P. R., Bella J., Olson N. H., Bator C. M., Baker T. S., Rossman M. G. 1999; Structural studies of two rhinovirus serotypes complexed with fragments of their cellular receptor. EMBO J 18:6249–6259
     [Google Scholar]
  16. Lindberg A. M., Crowell R. L., Zell R., Kandolf R., Pettersson U. 1992; Mapping the RD phenotype of the Nancy strain of coxsackievirus B3. Virus Res 24:187–196
     [Google Scholar]
  17. Lindberg A. M., Polacek C., Johansson S. 1997; Amplification and cloning of complete enterovirus genomes by long distance PCR. J Virol Methods 65:191–199
     [Google Scholar]
  18. Lublin D. M., Atkinson J. P. 1989; Decay-accelerating factor: biochemistry, molecular biology, and function. Annu Rev Immunol 7:35–58
     [Google Scholar]
  19. McKinlay M. A., Pevear D. C., Rossmann M. G. 1992; Treatment of the picornavirus common cold by inhibitors of viral uncoating and attachment. Annu Rev Microbiol 46:635–654
     [Google Scholar]
  20. Mizushima S., Nagata S. 1990; pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res 18:5322
     [Google Scholar]
  21. Muckelbauer J. K., Kremer I., Minor I., Diana G., Dutko F. J., Groarke J., Pevear P. C., Rossman M. G. 1995; The structure of coxsackievirus B3 at 3·5 Å resolution. Structure 3:653–667
     [Google Scholar]
  22. Oberste M. S., Maher K., Kilpatrick D. R., Pallansch M. A. 1999; Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73:1941–1948
     [Google Scholar]
  23. Plummer G. 1965; The picornaviruses of man and animals: a comparative review. Progr Med Virol 7:326–361
     [Google Scholar]
  24. Pöyry T., Kinnunen L., Hyypiä T., Brown B., Horsnell C., Hovi T., Stanway G. 1996; Genetic and phylogenetic clustering of enteroviruses. J Gen Virol 77:1699–1717
     [Google Scholar]
  25. Pulli T., Koskimies P., Hyypiä T. 1995; Molecular comparison of Coxsackie A virus serotypes. Virology 212:30–38
     [Google Scholar]
  26. Reed L. J., Muench H. A. 1938; A simple method of estimating fifty per cent endpoints. Am J Hyg 27:493–497
     [Google Scholar]
  27. Rossmann M. G., Arnold E., Erickson J. W. 10 other authors 1985; Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317:145–153
     [Google Scholar]
  28. Shafren D. R. 1998; Viral cell entry induced by cross-linked decay-accelerating factor. J Virol 72:9407–9412
     [Google Scholar]
  29. Shafren D. R., Bates R. C., Agrez M. V., Herd R. L., Burns G. F., Barry R. D. 1995; Coxsackieviruses B1, B3 and B5 use decay accelerating factor as a receptor for cell attachment. J Virol 69:3873–3877
     [Google Scholar]
  30. Shafren D. R., Dorahy D. J., Greive S. J., Burns G. F., Barry R. D. 1997a; Mouse cells expressing human intercellular adhesion molecule-1 are susceptible to infection by coxsackievirus A21. J Virol 71:785–789
     [Google Scholar]
  31. Shafren D. R., Dorahy D. J., Ingham R. A., Burns G. F., Barry R. D. 1997b; Coxsackievirus A21 binds to decay-accelerating factor but requires intercellular adhesion molecule 1 for cell entry. J Virol 71:4736–4743
     [Google Scholar]
  32. Shafren D. R., Dorahy D. J., Thorne R. F., Kinoshita T., Barry R. D., Burns G. F. 1998; Antibody binding to individual short consensus repeats of decay-accelerating factor enhances enterovirus cell attachment and infectivity. J Immunol 160:2318–2323
     [Google Scholar]
  33. Shepley M. P., Racaniello V. R. 1994; A monoclonal antibody that blocks poliovirus attachment recognizes the lymphocyte homing receptor CD44. J Virol 68:1301–1308
     [Google Scholar]
  34. Stuart A. D., McKee T. A., Williams P. A., Harley C., Shen S., Stuart D. I., Brown T. D. K., Lea S. M. 2002; Determination of the structure of a decay-accelerating factor-binding clinical isolate of echovirus 11 allows mapping of mutants with altered receptor requirements for infection. J Virol 76:7694–7704
     [Google Scholar]
  35. Supanaranond K., Takeda N., Yamaki S. 1992; The complete nucleotide sequence of a variant of coxsackievirus A24, an agent causing acute hemorrhagic conjunctivitis. Virus Genes 6:149–158
     [Google Scholar]
  36. Thompson J. D., Higgins D. G., Gobson T. J. 1994; ClustalW – improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
     [Google Scholar]
  37. Xiao C., Bator C. M., Bowman V. D. 8 other authors 2001; Interaction of coxsackievirus A21 with its cellular receptor, ICAM-1. J Virol 75:2444–2451
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.19329-0
Loading
Cellular receptor interactions of C-cluster human group A coxsackieviruses
J. Gen. Virol. 84, 3041 (2003); https://doi.org/10.1099/vir.0.19329-0
/content/journal/jgv/10.1099/vir.0.19329-0
/content/journal/jgv/10.1099/vir.0.19329-0
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