Structure of Foot-and-mouth disease virus serotype A1061 alone and complexed with oligosaccharide receptor: Receptor conservation in the face of antigenic variation

Journal of General Virology

Volumn 86, Issue 7, 2005, Pages 1909-1920

  Fry, Elizabeth E ^a   Newman, John W I ^b   Curry, Stephen ^b,c   Najjam, Saloua ^b   Jackson, Terry ^b   Blakemore, Wendy ^b,e   Lea, Susan M ^d   Miller, Laura ^b,f   Burman, Alison ^b   King, Andrew M Q ^b   Stuart, David I ^a  

^a Division of Structural Biology   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e ASTEX PHARMACEUTICALS   (United Kingdom)

^f U S MEAT ANIMAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; FOOT AND MOUTH DISEASE VACCINE; HEPARAN SULFATE; HEPARIN; INTEGRIN; INTEGRIN RECEPTOR; OLIGOSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGENIC VARIATION; ARTICLE; BINDING AFFINITY; CELL CULTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EPITHELIUM CELL; FOOT AND MOUTH DISEASE VIRUS; GENE SEQUENCE; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MOTIF; SEQUENCE ANALYSIS; SEROTYPE; STRAIN DIFFERENCE; TARGET CELL; VIRUS MORPHOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENIC VARIATION; BINDING SITES; CHO CELLS; CRICETINAE; CRYSTALLOGRAPHY, X-RAY; FOOT-AND-MOUTH DISEASE VIRUS; HEPARITIN SULFATE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; RECEPTORS, VIRUS; SEROTYPING; SURFACE PLASMON RESONANCE;

FOOT-AND-MOUTH DISEASE VIRUS;

EID: 21444433508     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.80730-0     Document Type: Article

References (62)

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.
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. J Virol 72, 6362-6372.
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.
4. 12 foot-and-mouth disease virus. J Virol 63, 2143-2151.
5. 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.
6. Bernard, K. A., Klimstra, W. B. & Johnston, R. E. (2000). Mutations in the E2 glycoprotein of Venezuelan equine encephalitis virus confer heparan sulfate interaction, low morbidity, and rapid clearance from blood of mice. Virology 276, 93-103.
7. Bernfield, M., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J. & Zako, M. (1999). Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68, 729-777.
8. Boothroyd, J. C., Harris, T. J. R., Rowlands, D. J. & Lowe, P. A. (1982). The nucleotide sequence of cDNA coding for the structural proteins of foot-and-mouth disease virus. Gene 17, 153-161.
9. Brunger, A. T. (1992). XPLOR Version 3.1. New Haven, CT: Yale University Press.
10. Byrnes, A. P. & Griffin, D. E. (2000). Large-plaque mutants of Sindbis virus show reduced binding to heparan sulfate, heightened viremia, and slower clearance from the circulation. J Virol 74, 644-651.
11. Cardin, A. D. & Weintraub, H. J. (1989). Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9, 21-32.
12. Collaborative Computational Project, Number 4 (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760-763.
13. 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. J Gen Virol 74, 1547-1553.
14. Curry, S., Abu-Ghazaleh, R., Blakemore, W. & 7 other authors (1992). Crystallization and preliminary X-ray analysis of three sero-types of foot-and-mouth disease virus. J Mol Biol 228, 1263-1268.
15. Curry, S., Fry, E., Blakemore, W. & 7 other authors (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.
16. Escribano-Romero, E., Jimenez-Clavero, M. A., Gomes, P., García-Ranea, J. A. & Ley, V. (2004). Heparan sulphate mediates swine vesicular disease virus attachment to the host cell. J Gen Virol 85, 653-663.
17. Esko, J. D., Weinke, J. L., Taylor, W. H., Ekborg, G., Rodén, L., Anantharamaiah, G. & Gawish, A. (1987). Inhibition of chondroitin and heparan sulfate biosynthesis in Chinese hamster ovary cell mutants defective in galactosyltransferase I. J Biol Chem 262, 12189-12195.
18. Esnouf, R. M. (1997). An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J Mol Graph Model 15, 132-134.
19. Esnouf, R. M. (1999). Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr D Biol Crystallogr 55, 938-940.
20. Faham, S., Hileman, R. E., Fromm, J. R., Linhardt, R. J. & Rees, D. C. (1996). Heparin structure and interactions with basic fibroblast growth factor. Science 271, 1116-1120.
21. Filman, D. J., Syed, R., Chow, M., Macadam, A. J., Minor, P. D. & Hogle, J. M. (1989). Structural factors that control conformational transitions and serotype specificity in type 3 poliovirus. EMBO J 8, 1567-1579.
22. Fox, G., Parry, N. R., Barnett, P. V., McGinn, B., Rowlands, D. J. & Brown, F. (1989). The 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.
23. Fry, E., Acharya, R. & Stuart, D. (1993). Methods used in the structure determination of foot-and-mouth disease virus. Acta Crystallogr A 49, 45-55.
24. Fry, E. E., Lea, S. M., Jackson, T. & 7 other authors (1999). The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J 18, 543-554.
25. Ganesh, V. K., Smith, S. A., Kotwal, G. J. & Murthy, K. H. M. (2004). Structure of vaccinia complement protein in complex with heparin and potential implications for complement regulation. Proc Natl Acad Sci U S A 101, 8924-8929.
26. 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.
27. Harlos, K. (1992). Micro-bridges for sitting-drop crystallizations. J Appl Crystallogr 25, 536-538.
28. 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.
29. 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 viruses to the purified integrin αvβ3 in vitro. J Virol 71, 8357-8361.
30. Jackson, T., Sheppard, D., Denyer, M., Blakemore, W. & King, A. M. Q. (2000). The epithelial integrin αvβ6 is a receptor for foot-and-mouth disease virus. J Virol 74, 4949-4956.
31. Jackson, T., Mould, A. P., Sheppard, D. & King, A. M. Q. (2002). Integrin αvβ1 is a receptor for foot-and-mouth disease virus. J Virol 76, 935-941.
32. Jackson, T., King, A. M. Q., Stuart, D. I. & Fry, E. (2003). Structure and receptor binding. Virus Res 91, 33-46.
33. Jackson, T., Clark, S., Berryman, S., Burman, A., Cambier, S., Mu, D., Nishimura, S. & King, A. M. Q. (2004). Integrin αvβ8 functions as a receptor for foot-and-mouth disease virus: role of the β-chain cytodomain in integrin-mediated infection. J Virol 78, 4533-4540.
34. Jones, T. A. (1985). Interactive computer graphics: FRODO. Methods Enzymol 115, 157-171.
35. Kim, S. S., Smith, T. J., Chapman, M. S., Rossmann, M. C., Pevear, D. C., Dutko, F. J., Felock, P. J., Diana, G. D. & McKinlay, M. A. (1989). Crystal structure of human rhinovirus serotype 1A (HRV1A). J Mol Biol 210, 91-111.
36. 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.
37. Klimstra, W. B., Ryman, K. D. & Johnston, R. E. (1998). Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J Virol 72, 7357-7366.
38. Kraulis, P. J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24, 946-950.
39. Lea, S., Hernandez, J., Blakemore, W. & 9 other authors (1994). The structure and antigenicity of a type C foot-and-mouth disease virus. Structure 2, 123-139.
40. 1 and a laboratory antigenic variant, G67. Structure 3, 571-580.
41. Lee, E. & Lobigs, M. (2002). Mechanism of virulence attenuation of glycosaminoglycan-binding variants of Japanese encephalitis virus and Murray Valley encephalitis virus. J Virol 76, 4901-4911.
42. Logan, D., Abu-Ghazaleh, R., Blakemore, W. & 10 other authors (1993). Structure of a major immunogenic site on foot-and-mouth disease virus. Nature 362, 566-568.
43. Mandl, C. W., Kroschewski, H., Allison, S. L., Kofler, R., Holzmann, H., Meixner, T. & Heinz, F. X. (2001). Adaptation of tick-borne encephalitis virus to BHK-21 cells results in the formation of multiple heparan sulfate binding sites in the envelope protein and attenuation in vivo. J Virol 75, 5627-5637.
44. Mason, P. W., Baxt, B., Brown, F., Harber, J., Murdin, 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.
45. Merritt, E. A. & Murphy, M. E. P. (1994). Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr D Biol Crystallogr 50, 869-873.
46. Mulloy, B. & Linhardt, R. J. (2001). Order out of complexity - protein structures that interact with heparin. Curr Opin Struct Biol 11, 623-628.
47. 3 as its receptor. J Virol 72, 3587-3594.
48. Nicholls, A., Sharp, K. A. & Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296.
49. Otwinoski, Z. (1993). Oscillation data reduction program. In Proceedings of the CCP4 Study Weekend: Data Collection and Processing, 29-30 January, 1993, pp. 56-62. Warrington, UK: Daresbury Laboratory, SERC.
50. Parry, N., Fox, G., Rowlands, D., Brown, F., Fry, E., Acharya, R., Logan, D. & Stuart, D. (1990). Structural and serological evidence for a novel mechanism of antigenic variation in foot-and-mouth disease virus. Nature 347, 569-572.
51. Reddi, H. V., Kumar, A. S. M., Kung, A. Y., Kallio, P. D., Schlitt, B. P. & Lipton, H. L. (2004). Heparan sulfate-independent infection attenuates high-neurovirulence GDVII virus-induced encephalitis. J Virol 78, 8909-8916.
52. 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.
53. Spillmann, D. (2001). Heparan sulfate: anchor for viral intruders? Biochimie 83, 811-817.
54. Stehle, T., Yan, Y., Benjamin, T. L. & Harrison, S. C. (1994). Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature 369, 160-163.
55. 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.
56. Stuart, D. I., Levine, M., Muirhead, H. & Stammers, D. K. (1979). Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6 Å. J Mol Biol 134, 109-142.
57. Thomas, A. A. M., Woortmeijer, R. J., Puijk, W. & Barteling, S. J. (1988). Antigenic sites on foot-and-mouth disease virus type A10. J Virol 62, 2782-2789.
58. Verdaguer, N., Mateu, M. G., Andreu, D., Giralt, E., Domingo, E. & Fita, I. (1995). Structure of the major antigenic loop of foot-and-mouth disease virus complexed with a neutralizing antibody: direct involvement of the Arg-Gly-Asp motif in the interaction. EMBO J 14, 1690-1696.
59. Verdaguer, N., Fita, I., Domingo, E. & Mateu, M. G. (1997). Efficient neutralization of foot-and-mouth disease virus by monovalent antibody binding. J Virol 71, 9813-9816.
60. Wallace, A. C., Laskowski, R. A. & Thornton, J. M. (1995). LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8, 127-134.
61. Zautner, A. E., Körner, U., Henke, A., Badorff, C. & Schmidtke, M. (2003). Heparan sulfates and coxsackievirus-adenovirus receptor: each one mediates coxsackievirus B3 PD infection. J Virol 77, 10071-10077.
62. 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.