A multiply substituted G-H loop from foot-and-mouth disease virus in complex with a neutralizing antibody: A role for water molecules

Journal of General Virology

Volumn 81, Issue 6, 2000, Pages 1495-1505

  Ochoa, Wendy F ^a   Kalko, Susana G ^a   Mateu, Mauricio G ^b   Gomes, Paula ^c   Andreu, David ^c   Domingo, Esteban ^b   Fita, Ignasi ^a   Verdaguer, Nuria ^a  

^a INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARGININE; ASPARTIC ACID; GLYCINE; IMMUNOGLOBULIN F(AB) FRAGMENT; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; SOLVENT; SYNTHETIC PEPTIDE; VIRUS ANTIGEN; VIRUS VACCINE; WATER;

AMINO ACID SUBSTITUTION; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; FOOT AND MOUTH DISEASE VIRUS; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; STEREOSPECIFICITY; VIRION; VIRUS ISOLATION; VIRUS TYPING;

FOOT-AND-MOUTH DISEASE VIRUS; FOOT-AND-MOUTH DISEASE VIRUS C; RNA VIRUSES;

EID: 0034120516     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/0022-1317-81-6-1495     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. Bachrach, H. L (1968). Foot and mouth disease virus. Annual Review of Microbiology 22, 201-244.
3. Beck, E. & Strohmaier, K. (1987). Subtyping of European foot-and-mouth disease virus strains by nucleotide sequence determination. Journal of Virology 61, 1621-1629.
4. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A. & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. Journal of Chemical Physics 81, 3684-3690.
5. Berendsen, H. J., Van Gunsteren, W. F., Zwinderman, H. R. & Geurtsen, R. G. (1986). Simulations of proteins in water. Annals of the New York Academy of Sciences 482, 269-286.
6. Berinstein, A., Roivainen, M., Hovi, T., Mason, P. W. & Baxt, B. (1995). Antibodies to the vitronectin receptor (integrin alpha V beta 3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells. Journal of Virology 69, 2664-2666.
7. Bittle, J. L., Houghten, R. A., Alexander, H., Shinnick, T. M., Sutcliffe, J. G., Lerner, R. A., Rowlands, D. J. & Brown, F. (1982). Protection against foot-and-mouth disease by immunization with a chemically synthesized peptide predicted from the viral nucleotide sequence. Nature 298, 30-33.
8. Brown, F. (1994). Foot-and-mouth disease. In Synthetic Vaccines, pp. 416-432. Edited by B. H. Nicholson. Oxford: Blackwell Scientific.
9. Brünger, A. T. (1992). XPLOR manual, version 3.0. Yale University, New Haven, CT, USA.
10. Carreño, C., Roig, X., Cairo, J., Camarero, J., Mateu, M. G., Domingo, E., Giralt, E. & Andreu, D. (1992). Studies on antigenic variability of C strains of foot-and-mouth disease virus by means of synthetic peptides and monoclonal antibodies. International Journal of Peptide and Protein Research 39, 41-47.
11. Clarke, B. E., Carroll, A. R., Rowlands, D. J., Nicholson, B. H., Houghten, R. A., Lerner, R. A. & Brown, F. (1983). Synthetic peptides mimic subtype specificity of foot-and-mouth disease virus. FEBS Letters 157, 261-264.
12. 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.
13. Domingo, E. & Holland, J. J. (1992). Complications of RNA heterogeneity for the engineering of virus vaccines and antiviral agents. In Genetic Engineering, Principles and Methods, vol. 14, pp. 13-32. Edited by J. K. Setlow. New York: Plenum.
14. Domingo, E., Mateu, M. G., Martínez, M. A., Dopazo, J., Moya, A. & Sobrino, F. (1990). Genetic variability and antigenic diversity of foot-and-mouth disease virus. In Applied Virology Research, pp. 233-266. Edited by E. Kurkstak, R. C. Marusyk, S. A. Murphy & M. H. V. Van Regenmortel. New York: Plenum.
15. Domingo, E., Verdaguer, N., Ochoa, W. F., Ruiz-Jarabo, C. M., Sevilla, N., Baranowski, E., Mateu, M. G. & Fita, I. (1999). Biochemical and structural studies with neutralizing antibodies raised against foot-and-mouth disease virus. Virus Research 62, 169-175.
16. 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). Journal of General Virology 70, 625-637.
17. Freire, E. (1999). The propagation of binding interactions to remote sites in proteins: analysis of the binding of the monoclonal antibody D1.3 to lysozyme. Proceedings of the National Academy of Sciences, USA 96, 10118-10122.
18. Hernández, J., Valero, M. L., Andreu, D., Domingo, E. & Mateu, M. G. (1996). Antibody and host cell recognition of foot-and-mouth disease virus (serotype C) cleaved at the Arg-Gly-Asp (RGD) motif: a structural interpretation. Journal of General Virology 77, 257-264.
19. Hewat, E. A., Verdaguer, N., Fita, I., Blakemore, W., Brookes, S., King, A., Newman, J., Domingo, E., Mateu, M. G. & Stuart, D. I. (1997). Structure of the complex of an Fab fragment of a neutralizing antibody with foot-and-mouth disease virus: positioning of a highly mobile antigenic loop. EMBO Journal 16, 1492-1500.
20. vβ3 in vitro. Journal of Virology 71, 8357-8361.
21. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallographica A47, 110-119.
22. 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. (1993). Structure of a major immunogenic site on foot-and-mouth disease virus. Nature 362, 566-568.
23. 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.
24. 1 and a laboratory antigenic variant, G67. Structure 3, 571-580.
25. 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.
26. McCullough, K. C., De Simone, F., Brocchi, E., Capucci, L., Crowther, J. R. & Kihm, U. (1992). Protective immune response against foot-and-mouth disease. Journal of Virology 66, 1835-1840.
27. Martínez, M. A., Hernández, J., Piccone, M. E., Palma, E. L., Domingo, E., Knowles, N. & Mateu, M. G. (1991). Two mechanisms of antigenic diversification of foot-and-mouth disease virus. Virology 184, 695-706.
28. Martínez, M. A., Verdaguer, N., Mateu, M. G. & Domingo, E. (1997). Evolution subverting essentiality: dispensability of the cell attachment Arg-Gly-Asp motif in multiply passaged foot-and-mouth disease virus . Proceedings of the National Academy of Sciences, USA 94, 6798-6802.
29. 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-dependent enhancement pathway. Proceedings of the National Academy of Sciences, USA 91, 1932-1936.
30. Mateu, M. G. (1995). Antibody recognition of picornaviruses and escape from neutralization: a structural view. Virus Research 38, 1-24.
31. Mateu, M. G., Rocha, E., Vicente, O., Vayreda, F., Navalpotro, C., Andreu, D., Pedroso, E., Giralt, E., Enjuanes, L. & Domingo, E. (1987). Reactivity with monoclonal antibodies of viruses from an episode of foot-and-mouth disease. Virus Research 8, 261-274.
32. Mateu, M. G., Da Silva, J. L., Rocha, E., De Brum, D. L., Alonso, A., Enjuanes, L., Domingo, E. & Barahona, H. (1988). Extensive antigenic heterogeneity of foot-and-mouth disease virus of serotype C. Virology 167, 113-124.
33. Mateu, M. G., Martínez, M. A., Rocha, E., Andreu, D., Parejo, J., Giralt, E., Sobrino, F. & Domingo, E. (1989). Implications of a quasispecies genome structure: effect of frequent, naturally occurring amino acid substitutions on the antigenicity of foot-and-mouth disease virus. Proceedings of the National Academy of Sciences, USA 86, 5883-5887.
34. Mateu, M. G., Martínez, M. A., Capucci, L., Andreu, D., Giralt, E., Sobrino, F., Brocchi, E. & Domingo, E. (1990). A single amino acid substitution affects multiple overlapping epitopes in the major antigenic site of foot-and-mouth disease virus of serotype C. Journal of General Virology 71, 629-637.
35. Mateu, M. G., Andreu, D., Carreño, C., Roig, X., Cairó, J. J., Camarero, J. A., Giralt, E. & Domingo, E. (1992). Non-additive effects of multiple amino acid substitutions on antigen-antibody recognition. European Journal of Immunology 22, 1385-1389.
36. 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.
37. Misbah, S. A., Spickett, G. P., Ryba, P. C., Hockaday, J. M., Kroll, J. S., Sherwood, C., Kurtz, J. B., Moxon, E. R. & Chapel, H. M. (1992). Chronic enteroviral meningoencephalitis in agammaglobulinemia: case report and literature review. Journal of Clinical Immunology 12, 266-270.
38. Navaza, J. (1994). AMoRe: an automated package for molecular replacement. Acta Crystallographica A50, 157-163.
39. vβ3 as its receptor. Journal of Virology 72, 3587-3594.
40. Novella, I. S., Borrego, B., Mateu, M. G., Domingo, E., Giralt, E. & Andreu, D. (1993). Use of substituted and tandem-repeated peptides to probe the relevance of the highly conserved RGD tripeptide in the immune response against foot-and-mouth disease virus. FEBS Letters 330, 253-259.
41. Otwinowski, Z. & Minor, W. (1996). Processing of X-ray diffraction data collected in an oscillation mode. Methods in Enzymology 35, 307-326.
42. 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.
43. Pereira, H. G. (1977). Subtyping foot-and-mouth disease virus. Developments in Biological Standardization 35, 167-174.
44. Pereira, H. G. (1981). Foot-and-mouth disease virus. In Virus Diseases of Food Animals, pp. 333-363. Edited by R. P. G. Gibbs. New York: Academic Press.
45. Pfaff, E. (1997). Recognition sites of RGD-dependent integrins. In Integrin Ligand Interactions, pp. 101-121. Edited by J. A. Eble & K. Kühn. Austin, TX: R. G. Landes.
46. Pfaff, E., Mussgay, M., Bohm, H. O., Schulz, G. E. & Schaller, H. (1982). Antibodies against a preselected peptide recognize and neutralize foot and mouth disease virus. EMBO Journal 1, 869-874.
47. Rickaert, J. P., Ciccotti, G. & Berendsen, H. J. C. (1977). Numerical integration of cartesian equations of motions of a system with constraints: molecular dynamics of n-alkanes. Journal of Computational Physics 23, 327-341.
48. Rousel, A. & Cambillau, C. (1989). TURBO-Frodo. In Silicon Graphics Geometry Partners Directory, pp. 77-79. Mountain View, CA: Silicon Graphics.
49. Rowlands, D. J., Clarke, B. E., Carroll, A. R., Brown, F., Nicholson, B. H., Bittle, J. L., Houghten, R. A. & Lerner, R. A. (1983). Chemical basis of antigenic variation in foot-and-mouth disease virus. Nature 306, 694-697.
50. Rueckert, R. R. (1996). Picornaviridae: the viruses and their replication. In Fields Virology, 3rd edn, pp. 609-654. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: Lippincott-Raven.
51. Sobrino, F., Dávila, M., Ortín, J. & Domingo, E. (1983). Multiple genetic variants arise in the course of replication of foot- and-mouth disease virus in cell culture. Virology 128, 310-318.
52. Strohmaier, K., Franze, R. & Adam, K.-H. (1982). Location and characterization of the antigenic portion of the FMDV immunizing protein. Journal of General Virology 59, 295-306.
53. Stura, E. A. & Wilson, I. A. (1992). Seeding techniques. In Crystallization of Nucleic Acids and Proteins. A Practical Approach, pp. 99-126. Edited by A. Ducruix & R. Giege. Oxford: IRL Press.
54. Taboga, O., Tami, C., Carrillo, E., Núñez, J. I., Rodríguez, A., Saíz, J. C., Blanco, E., Valero, M. L., Roig, X., Camarero, J. A., Andreu, D., Mateu, M. G., Giralt, E., Domingo, E., Sobrino, F. & Palma, E. L. (1997). A large-scale evaluation of peptide vaccines against foot-and-mouth disease: lack of solid protection in cattle and isolation of escape mutants. Journal of Virology 71, 2606-2614.
55. Timoney, J. F., Gillespie, J. H., Scott, F. N. & Barlough, J. E. (1992). Foot-and-mouth disease. In Hagan and Bruner's Microbiology and Infectious Diseases of Domestic Animals, pp. 647-667. Ithaca, NY : Cornell University Press.
56. van Gunsteren, W. F., Billeter, S. R., Eising, A. A., Hünenberg, P. H., Krüger, P., Mark, A. E., Scott, W. R. P. & Tironi, I. G. (1996). Biomolecular simulation. In GROMOS96 Manual and User Guide, Zürich: Biomolecular Software.
57. 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 Journal 14, 1690-1696.
58. Verdaguer, N., Mateu, M. G., Bravo, J., Domingo, E. & Fita, I. (1996). Induced pocket to accommodate the cell attachment Arg-Gly-Asp motif in a neutralizing antibody against foot-and-mouth disease virus. Journal of Molecular Biology 256, 364-376.
59. Verdaguer, N., Fita, I., Domingo, E. & Mateu, M. G. (1997). Efficient neutralization of foot-and-mouth disease virus by monovalent antibody binding. Journal of Virology 71, 9813-9816.
60. Verdaguer, N., Sevilla, N., Valero, M. L., Stuart, D., Brocchi, E., Andreu, D., Giralt, E., Domingo, E., Mateu, M. G. & Fita, I. (1998). A similar pattern of interaction for different antibodies with a major antigenic site of foot-and-mouth disease virus : implications for intratypic antigenic variation. Journal of Virology 72, 739-748.
61. Verdaguer, N., Schoehn, G., Ochoa, W. F., Fita, I., Brookes, S., King, A., Domingo, E., Mateu, M. G., Stuart, D. & Hewat, E. A. (1999). Flexibility of the major antigenic loop of foot-and-mouth disease virus bound to a Fab fragment of a neutralizing antibody: structure and neutralization. Virology 255, 260-268.
62. Villaverde, A., Martínez, M. A., Sobrino, F., Dopazo, J., Moya, A. & Domingo, E. (1991). Fixation of mutations at the VP1 gene of foot-and-mouth disease virus. Can quasispecies define a transient molecular clock? Gene 103, 147-153.