1887

Abstract

Equine rhinitis A virus (ERAV) shares many features with foot-and-mouth disease virus (FMDV) and both are classified within the genus of the family . ERAV is used as a surrogate for FMDV research as it does not require high-level biosecurity. In contrast to FMDV, which uses integrins as cellular receptors, the receptor for ERAV has been reported to involve the sugar moiety sialic acid. This study confirmed the importance of sialic acid for cell entry by ERAV and reports the crystal structure of ERAV particles complexed with the receptor analogue 3′-sialyllactose. The receptor is attached to the rim of a capsid pit adjacent to the major immunogenic site and distinct from the sialic acid binding site used by a related picornavirus, the cardiovirus Theiler's murine encephalitis virus. The structure of the major antigenic determinant of the virus, previously identified from antibody escape mutations, is also described as the EF loop of VP1, which forms a hairpin stretching across the capsid surface close to the icosahedral fivefold axis, neighbouring the receptor-binding site, and spanning two protomeric units.

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2010-08-01
2019-11-21
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References

  1. Acharya, R., Fry, E., Stuart, D., Fox, G., Rowlands, D. & Brown, F. ( 1989; ). The three-dimensional structure of foot-and-mouth disease virus at 2.9 Å resolution. Nature 337, 709–716.[CrossRef]
    [Google Scholar]
  2. Alexander, D. A. & Dimock, K. ( 2002; ). Sialic acid functions in enterovirus 70 binding and infection. J Virol 76, 11265–11272.[CrossRef]
    [Google Scholar]
  3. Baranowski, E., Ruiz-Jarabo, C. M., Sevilla, N., Andreu, D., Beck, E. & Domingo, E. ( 2000; ). Cell recognition by foot-and-mouth disease virus that lacks the RGD integrin-binding motif: flexibility in aphthovirus receptor usage. J Virol 74, 1641–1647.[CrossRef]
    [Google Scholar]
  4. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N. & Bourne, P. E. ( 2000; ). The Protein Data Bank. Nucleic Acids Res 28, 235–242.[CrossRef]
    [Google Scholar]
  5. Brunger, A. T. ( 1992; ). XPLOR Version 3.1. New Haven and London.: Yale University Press.
  6. Burmeister, W. P., Ruigrok, R. W. H. & Cusack, S. ( 1992; ). The 2.2A resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. EMBO J 11, 49–56.
    [Google Scholar]
  7. De Lano,W. L. (2002). The pyMOL Molecular Graphics System. http://pymol.sourceforge.net/overview/index.htm.
  8. Fox, G., Parry, N. R., Barnett, P. V., McGinn, B., Rowlands, D. J. & Brown, F. ( 1989; ). Cell attachment site on foot-and-mouth disease virus includes the amino acid sequence RGD (arginine-glycine-aspartic acid). J Gen Virol 70, 625–637.[CrossRef]
    [Google Scholar]
  9. Fry, E. E., Lea, S. M., Jackson, T., Newman, J. W. I., Ellard, F. M., Blakemore, W. E., Abu-Ghazaleh, R., Samuel, A., King, A. M. Q. & Stuart, D. I. ( 1999; ). The structure and function of a foot-and-mouth disease virus–oligosaccharide receptor complex. EMBO J 18, 543–554.[CrossRef]
    [Google Scholar]
  10. Fry, E. E., Newman, J. W. & Curry, S. ( 2005; ). Structure of Foot-and-mouth disease virus serotype A1061 alone and complexed with oligosaccharide receptor: receptor conservation in the face of antigenic variation. J Gen Virol 86, 1909–1920.[CrossRef]
    [Google Scholar]
  11. Jackson, T., Ellard, F. M., Abu Ghazaleh, R., Brookes, S. M., Blakemore, W. E., Corteyn, A. H., Stuart, D. I., Newman, J. W. I. & King, A. M. Q. ( 1996; ). Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J Virol 70, 5282–5287.
    [Google Scholar]
  12. Jackson, T., King, A. M. Q., Stuart, D. I. & Fry, E. ( 2003; ). Structure and receptor binding. Virus Res 91, 33–46.[CrossRef]
    [Google Scholar]
  13. Kriegshäuser, G., Wutz, G., Lea, S., Stuart, D. I., Skern, T. & Kuechler, E. ( 2003; ). Model of the equine rhinitis A virus capsid: identification of a major neutralizing immunogenic site. J Gen Virol 84, 2365–2373.[CrossRef]
    [Google Scholar]
  14. Li, F., Stevenson, R. A., Crabb, B. S., Studdert, M. J. & Hartley, C. A. ( 2005; ). Several recombinant capsid proteins of equine rhinitis A virus show potential as diagnostic antigens. Clin Diagn Lab Immunol 12, 778–785.
    [Google Scholar]
  15. Mason, P., Baxt, B., Brown, F., Harber, J., Murdis, A. & Wimmer, E. ( 1993; ). Antibody-complexed foot-and-mouth disease virus, but not poliovirus, can infect normally insusceptible cells via the Fc receptor. Virology 192, 568–577.[CrossRef]
    [Google Scholar]
  16. Otwinoski, Z. ( 1993; ). Oscillation data reduction program. In Data Collection and Processing. Warrington, UK: Daresbury Laboratory/SERC.
  17. Sa-Carvalho, D., Rieder, E., Baxt, B., Rodarte, R., Tanuri, A. & Mason, P. W. ( 1997; ). Tissue culture adaptation of foot-and-mouth disease virus selects viruses that bind to heparin and are attenuated in cattle. J Virol 71, 5115–5123.
    [Google Scholar]
  18. Shah, A. H. & Lipton, H. L. ( 2002; ). Low-neurovirulence Theiler's viruses use sialic acid moieties on N-linked oligosaccharide structures for attachment. Virology 304, 443–450.[CrossRef]
    [Google Scholar]
  19. 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.[CrossRef]
    [Google Scholar]
  20. Stevenson, R. A., Hartley, C. A., Huang, J. A., Studdert, M. J., Crabb, B. S. & Warner, S. ( 2003; ). Mapping epitopes in equine rhinitis A virus VP1 recognized by antibodies elicited in response to infection of the natural host. J Gen Virol 84, 1607–1612.[CrossRef]
    [Google Scholar]
  21. Stevenson, R. A., Huang, J. A., Studdert, M. J. & Hartley, C. A. ( 2004a; ). Identification of a neutralizing epitope in the βE–βF loop of VP1 of equine rhinitis A virus, defined by a neutralization-resistant variant. J Gen Virol 85, 2545–2553.[CrossRef]
    [Google Scholar]
  22. Stevenson, R. A., Huang, J. A., Studdert, M. J. & Hartley, C. A. ( 2004b; ). Sialic acid acts as a receptor for equine rhinitis A virus binding and infection. J Gen Virol 85, 2535–2543.[CrossRef]
    [Google Scholar]
  23. Strohmaier, K., Franze, R. & Adam, K.-H. ( 1982; ). Location and characterization of the antigenic portion of the FMDV immunizing protein. J Gen Virol 59, 295–306.[CrossRef]
    [Google Scholar]
  24. Tuthill, T. J., Harlos, K., Walter, T. S., Knowles, N. J., Groppelli, E., Rowlands, D. J., Stuart, D. I. & Fry, E. E. ( 2009; ). Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism? PLoS Pathog 5, e1000620 [CrossRef]
    [Google Scholar]
  25. Varrasso, A., Drummer, H. E., Huang, J. A., Stevenson, R. A., Ficorilli, N., Studdert, M. J. & Hartley, C. A. ( 2001; ). Sequence conservation and antigenic variation of the structural proteins of equine rhinitis A virus. J Virol 75, 10550–10556.[CrossRef]
    [Google Scholar]
  26. Wallace, A. C., Lakowski, R. A. & Thornton, J. M. ( 1995; ). ligplot: A program to generate schematic diagrams of protein–ligand interactions. Protein Eng 8, 127–134.[CrossRef]
    [Google Scholar]
  27. Zhao, Q., Pacheco, J. M. & Mason, P. W. ( 2003; ). Evaluation of genetically engineered derivatives of a Chinese strain of foot-and-mouth disease virus reveals a novel cell-binding site which functions in cell culture and in animals. J Virol 77, 3269–3280.[CrossRef]
    [Google Scholar]
  28. Zhou, L., Luo, Y., Wu, Y., Tsao, J. & Luo, M. ( 2000; ). Sialylation of the host receptor may modulate entry of demyelinating persistent Theiler's virus. J Virol 74, 1477–1485.[CrossRef]
    [Google Scholar]
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vol. , part 8, pp. 1971–1977

Icosahedrally averaged omit map for sialyllactose bound to ERAV. The sialic acid moiety is to the left.



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