1887

Abstract

Field isolates of foot-and-mouth disease virus (FMDV) use RGD-dependent integrins as receptors for internalization, whereas strains that are adapted for growth in cultured cell lines appear to be able to use alternative receptors like heparan sulphate proteoglycans (HSPG). The ligand-binding potential of integrins is regulated by changes in the conformation of their ectodomains and the ligand-binding state would be expected to be an important determinant of tropism for viruses that use integrins as cellular receptors. Currently, αvβ3 is the only integrin that has been shown to act as a receptor for FMDV. In this study, a solid-phase receptor-binding assay has been used to characterize the binding of FMDV to purified preparations of the human integrin α5β1, in the absence of HSPG and other RGD-binding integrins. In this assay, binding of FMDV resembled authentic ligand binding to α5β1 in its dependence on divalent cations and specific inhibition by RGD peptides. Most importantly, binding was found to be critically dependent on the conformation of the integrin, as virus bound only after induction of the high-affinity ligand-binding state. In addition, the identity of the amino acid residue immediately following the RGD motif is shown to influence differentially the ability of FMDV to bind integrins α5β1 and αvβ3 and evidence is provided that α5β1 might be an important FMDV receptor.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-5-1383
2000-05-01
2024-12-07
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/5/0811383a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-5-1383&mimeType=html&fmt=ahah

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. Baranowski, E., Sevilla, N., Verdaguer, N., Ruiz-Jarabo, C. M., Beck, E. & Domingo, E. (1998). Multiple virulence determinants of foot-and-mouth disease virus in cell culture.Journal of Virology 72, 6362-6372. [Google Scholar]
  3. Bazzoni, G., Shih, D. T., Buck, C. A. & Hemler, M. E. (1995). Monoclonal antibody 9EG7 defines a novel β1 integrin epitope induced by soluble ligand and manganese, but inhibited by calcium.Journal of Biological Chemistry 270, 25570-25577.[CrossRef] [Google Scholar]
  4. Belsham, G. J. (1993). Distinctive features of foot-and-mouth disease virus, a member of the picornavirus family: aspects of virus protein synthesis, protein processing and structure.Progress in Biophysics and Molecular Biology 60, 241-260.[CrossRef] [Google Scholar]
  5. Berinstein, A., Roivainen, M., Hovi, T., Mason, P. W. & Baxt, B. (1995). Antibodies to the vitronectin receptor (integrin αvβ3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells.Journal of Virology 69, 2664-2666. [Google Scholar]
  6. Chambers, M. A., Dougan, G., Newman, J., Brown, F., Crowther, J., Mould, A. P., Humphries, M. J., Francis, M. J., Clarke, B., Brown, A. L. & Rowlands, D. (1996). Chimeric hepatitis B virus core particles as probes for studying peptide–integrin interactions.Journal of Virology 70, 4045-4052. [Google Scholar]
  7. Chang, K. H., Day, C., Walker, J., Hyypiä, T. & Stanway, G. (1992). The nucleotide sequences of wild-type coxsackievirus A9 strains imply that an RGD motif in VP1 is functionally significant.Journal of General Virology 73, 621-626.[CrossRef] [Google Scholar]
  8. Crowther, J. R., Farias, S., Carpenter, W. C. & Samuel, A. R. (1993). Identification of a fifth neutralizable site on type O foot-and-mouth disease virus following characterization of single and quintuple monoclonal antibody escape mutants.Journal of General Virology 74, 1547-1553.[CrossRef] [Google Scholar]
  9. Curry, S., Abu-Ghazaleh, R., Blakemore, W., Fry, E., Jackson, T., King, A., Lea, S., Logan, D., Newman, J. & Stuart, D. (1992). Crystallization and preliminary X-ray analysis of three serotypes of foot-and-mouth disease virus.Journal of Molecular Biology 228, 1263-1268.[CrossRef] [Google Scholar]
  10. Curry, S., Fry, E., Blakemore, W., Abu-Ghazaleh, R., Jackson, T., King, A., Lea, S., Newman, J., Rowlands, D. & Stuart, D. (1996). Perturbations in the surface structure of A22 Iraq foot-and-mouth disease virus accompanying coupled changes in host cell specificity and antigenicity.Structure 4, 135-145.[CrossRef] [Google Scholar]
  11. Damjanovich, L., Albelda, S. M., Mette, S. A. & Buck, C. A. (1992). Distribution of integrin cell adhesion receptors in normal and malignant lung tissue.American Journal of Respiratory Cell and Molecular Biology 6, 197-206.[CrossRef] [Google Scholar]
  12. Dedhar, S. & Hannigan, G. E. (1996). Integrin cytoplasmic interactions and bidirectional transmembrane signalling.Current Opinion in Cell Biology 8, 657-669.[CrossRef] [Google Scholar]
  13. 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 Journal 18, 543-554.[CrossRef] [Google Scholar]
  14. Ghazi, F., Hughes, P. J., Hyypiä, T. & Stanway, G. (1998). Molecular analysis of human parechovirus type 2 (formerly echovirus 23).Journal of General Virology 79, 2641-2650. [Google Scholar]
  15. Healy, J. M., Murayama, O., Maeda, T., Yoshino, K., Sekiguchi, K. & Kikuchi, M. (1995). Peptide ligands for integrin αvβ3 selected from random phage display libraries.Biochemistry 34, 3948-3955.[CrossRef] [Google Scholar]
  16. Hughes, P. E., Renshaw, M. W., Pfaff, M., Forsyth, J., Keivens, V. M., Schwartz, M. A. & Ginsberg, M. H. (1997). Suppression of integrin activation: a novel function of a Ras/Raf-initiated MAP kinase pathway.Cell 88, 521-530.[CrossRef] [Google Scholar]
  17. Hynes, R. O. (1992). Integrins: versatility, modulation, and signaling in cell adhesion.Cell 69, 11-25.[CrossRef] [Google Scholar]
  18. Hyypiä, T., Horsnell, C., Maaronen, M., Khan, M., Kalkkinen, N., Auvinen, P., Kinnunen, L. & Stanway, G. (1992). A distinct picornavirus group identified by sequence analysis.Proceedings of the National Academy of Sciences, USA 89, 8847-8851.[CrossRef] [Google Scholar]
  19. 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.Journal of Virology 70, 5282-5287. [Google Scholar]
  20. Jackson, T., Sharma, A., Abu Ghazaleh, R., Blakemore, W. E., Ellard, F. M., Simmons, D. L., Newman, J. W. I., Stuart, D. I. & King, A. M. Q. (1997). Arginine–glycine–aspartic acid-specific binding by foot-and mouth disease virus to the purified integrin αvβ3 in vitro.Journal of Virology 71, 8357-8361. [Google Scholar]
  21. Jung, Y.-T., Kim, G.-R. & Paik, S.-Y. (1998). Molecular biological characterization of enterovirus variant isolates from patients with aseptic meningitis.Experimental & Molecular Medicine 30, 101-107.[CrossRef] [Google Scholar]
  22. Kashiwagi, H., Schwartz, M. A., Eigenthaler, M., Davis, K. A., Ginsberg, M. H. & Shattil, S. J. (1997). Affinity modulation of platelet integrin αIIbβ3 by β3-endonexin, a selective binding partner of the β3 integrin cytoplasmic tail.Journal of Cell Biology 137, 1433-1443.[CrossRef] [Google Scholar]
  23. Kitson, J. D. A., McCahon, D. & Belsham, G. J. (1990). Sequence analysis of monoclonal antibody resistant mutants of type O foot and mouth disease virus: evidence for the involvement of the three surface exposed capsid proteins in four antigenic sites.Virology 179, 26-34.[CrossRef] [Google Scholar]
  24. Knowles, N. J. & Samuel, A. R. (1994).Report of the Session of the Research Group of the Standing Technical Committee of the European Commission for the Control of Foot-and-Mouth Disease. Vienna, Austria, 19–22 September 1994.
  25. Koivunen, E., Gay, D. A. & Ruoslahti, E. (1993). Selection of peptides binding to the α5β1 integrin from phage display libraries.Journal of Biological Chemistry 268, 20205-20210. [Google Scholar]
  26. Lea, S., Hernández, J., Blakemore, W., Brocchi, E., Curry, S., Domingo, E., Fry, E., Abu-Ghazaleh, R., King, A., Newman, J., Stuart, D. & Mateu, M. G. (1994). The structure and antigenicity of a type C foot-and-mouth disease virus.Structure 2, 123-139.[CrossRef] [Google Scholar]
  27. Lee, J. O., Bankston, L. A., Arnaout, M. A. & Liddington, R. C. (1995). Two conformations of the integrin A-domain (I-domain): a pathway for activation?Structure 3, 1333-1340.[CrossRef] [Google Scholar]
  28. Li, R., Rieu, P., Griffith, D. L., Scott, D. & Arnaout, M. A. (1998). Two functional states of the CD11b A-domain: correlations with key features of two Mn2+-complexed crystal structures.Journal of Cell Biology 143, 1523-1534.[CrossRef] [Google Scholar]
  29. Logan, D., Abu-Ghazaleh, R., Blakemore, W., Curry, S., Jackson, T., King, A., Lea, S., Lewis, R., Newman, J., Parry, N., Rowlands, D., Stuart, D. & Fry, E. (1993). Structure of a major immunogenic site on foot-and-mouth disease virus.Nature 362, 566-568.[CrossRef] [Google Scholar]
  30. Mason, P. W., Rieder, E. & Baxt, B. (1994). RGD sequence of foot-and-mouth disease virus is essential for infecting cells via the natural receptor but can be bypassed by an antibody-dependant enhancement pathway.Proceedings of the National Academy of Sciences, USA 91, 1932-1936.[CrossRef] [Google Scholar]
  31. Mateu, M. G., Valero, M. L., Andreu, D. & Domingo, E. (1996). Systematic replacement of amino acid residues within an Arg–Gly–Asp-containing loop of foot-and-mouth disease virus and effect on cell recognition.Journal of Biological Chemistry 271, 12814-12819.[CrossRef] [Google Scholar]
  32. Mette, S. A., Pilewski, J., Buck, C. A. & Albelda, S. M. (1993). Distribution of integrin cell adhesion receptors on normal bronchial epithelial cells and lung cancer cells in vitro and in vivo.American Journal of Respiratory Cell and Molecular Biology 8, 562-572.[CrossRef] [Google Scholar]
  33. Montgomery, A. M. P., Reisfeld, R. A. & Cheresh, D. A. (1994). Integrin αvβ3 rescues melanoma cells from apoptosis in three-dimensional dermal collagen.Proceedings of the National Academy of Sciences, USA 91, 8856-8860.[CrossRef] [Google Scholar]
  34. Mould, A. P., Garratt, A. N., Askari, J. A., Akiyama, S. K. & Humphries, M. J. (1995a). Identification of a novel anti-integrin monoclonal antibody that recognises a ligand-induced binding site epitope on the β1 subunit.FEBS Letters 363, 118-122.[CrossRef] [Google Scholar]
  35. Mould, A. P., Akiyama, S. K. & Humphries, M. J. (1995b). Regulation of integrin α5β1–fibronectin interactions by divalent cations. Evidence for distinct classes of binding sites for Mn2+, Mg2+, and Ca2+.Journal of Biological Chemistry 270, 26270-26277.[CrossRef] [Google Scholar]
  36. Mould, A. P., Akiyama, S. K. & Humphries, M. J. (1996). The inhibitory anti-β1 integrin monoclonal antibody 13 recognizes an epitope that is attenuated by ligand occupancy. Evidence for allosteric inhibition of integrin function.Journal of Biological Chemistry 271, 20365-20374.[CrossRef] [Google Scholar]
  37. Neff, S., Sa-Carvalho, D., Rieder, E., Mason, P. W., Blystone, S. D., Brown, E. J. & Baxt, B. (1998). Foot-and-mouth disease virus virulent for cattle utilizes the integrin αvβ3 as its receptor.Journal of Virology 72, 3587-3594. [Google Scholar]
  38. Nelsen-Salz, B., Eggers, H. J. & Zimmermann, H. (1999). Integrin αvβ3 (vitronectin receptor) is a candidate receptor for the virulent echovirus 9 strain Barty.Journal of General Virology 80, 2311-2313. [Google Scholar]
  39. Oberste, M. S., Maher, K. & Pallansch, M. A. (1998). Complete sequence of echovirus 23 and its relationship to echovirus 22 and other human enteroviruses.Virus Research 56, 217-223.[CrossRef] [Google Scholar]
  40. O’Toole, T. E., Katagiri, Y., Faull, R. J., Peter, K., Tamura, R., Quaranta, V., Loftus, J. C., Shattil, S. J. & Ginsberg, M. H. (1994). Integrin cytoplasmic domains mediate inside-out signal transduction.Journal of Cell Biology 124, 1047-1059.[CrossRef] [Google Scholar]
  41. O’Toole, T. E., Ylanne, J. & Culley, B. M. (1995). Regulation of integrin affinity states through an NPXY motif in the β subunit cytoplasmic domain.Journal of Biology Chemistry 270, 8553-8558.[CrossRef] [Google Scholar]
  42. Pierschbacher, M. D. & Ruoslahti, E. (1984). Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule.Nature 309, 30-33.[CrossRef] [Google Scholar]
  43. Pytela, R., Pierschbacher, M. D. & Ruoslahti, E. (1985). Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor.Cell 40, 191-198.[CrossRef] [Google Scholar]
  44. Pytela, R., Pierschbacher, M. D., Ginsberg, M. H., Plow, E. F. & Ruoslahti, E. (1986). Platelet membrane glycoprotein IIb/IIIa: member of a family of Arg–Gly–Asp-specific adhesion receptors.Science 231, 1559-1562.[CrossRef] [Google Scholar]
  45. Rieder, E., Baxt, B. & Mason, P. W. (1994). Animal-derived antigenic variants of foot-and-mouth disease virus type A12 have low affinity for cells in culture.Journal of Virology 68, 5296-5299. [Google Scholar]
  46. Roivainen, M., Piirainen, L., Hovi, T., Virtanen, I., Riikonen, T., Heino, J. & Hyypiä, T. (1994). Entry of coxsackievirus A9 into host cells: specific interactions with αvβ3 integrin, the vitronectin receptor.Virology 203, 357-365.[CrossRef] [Google Scholar]
  47. Rowe, C. A. (1993).Molecular and serological characterisation of a type SAT 2 foot-and-mouth disease virus. PhD thesis, University of Reading, UK.
  48. 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.Journal of Virology 71, 5115-5123. [Google Scholar]
  49. Salt, J. S. (1998). Persistent infection with foot-and-mouth disease virus.Topics in Tropical Virology 1, 77-129. [Google Scholar]
  50. Springer, T. A. (1990). Adhesion receptors of the immune system.Nature 346, 425-434.[CrossRef] [Google Scholar]
  51. Strohmaier, K., Franze, R. & Adam, K.-H. (1982). Location and characterization of the antigenic protein of the FMDV immunizing protein.Journal of General Virology 59, 295-306.[CrossRef] [Google Scholar]
  52. Veiga, S. S., Elias, M. C. Q. B., Gremski, W., Porcionatto, M. A., da Silva, R., Nader, H. B. & Brentani, R. R. (1997). Post-translational modifications of α5β1 integrin by glycosaminoglycan chains. The α5β1 integrin is a facultative proteoglycan.Journal of Biological Chemistry 272, 12529-12535.[CrossRef] [Google Scholar]
  53. Villaverde, A., Feliu, J. X., Harbottle, R. P., Benito, A. & Coutelle, C. (1996). A recombinant, arginine–glycine–aspartic acid (RGD) motif from foot-and-mouth disease virus binds mammalian cells through vitronectin and, to a lower extent, fibronectin receptors.Gene 180, 101-106.[CrossRef] [Google Scholar]
  54. Xie, Q.-C., McCahon, D., Crowther, J. R., Belsham, G. J. & McCullough, K. C. (1987). Neutralization of foot-and-mouth disease virus can be mediated through any of at least three antigenic sites.Journal of General Virology 68, 1637-1647.[CrossRef] [Google Scholar]
  55. Zhang, Z., Vuori, K., Wang, H., Reed, J. C. & Ruoslahti, E. (1996). Integrin activation by R-ras.Cell 85, 61-69.[CrossRef] [Google Scholar]
  56. Zimmermann, H., Eggers, H. J. & Nelsen-Salz, B. (1996). Molecular cloning and sequence determination of the complete genome of the virulent echovirus 9 strain barty.Virus Genes 12, 149-154.[CrossRef] [Google Scholar]
/content/journal/jgv/10.1099/0022-1317-81-5-1383
Loading
/content/journal/jgv/10.1099/0022-1317-81-5-1383
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