1887

Journal of General Virology header logo

Volume 70, Issue 12

Selection of Antigenic Variants of Foot-and-Mouth Disease Virus in the Absence of Antibodies, as Revealed by an Assay Free

Abstract

SUMMARY

Antigenic variants of foot-and-mouth disease virus (FMDV) of serotype C (isolate C-S8c1) were selected upon serial passage of the virus in cell culture in the absence of anti-FMDV antibodies. The variants rose from frequencies of < 10 in the initial plaque-purified FMDV C-S8c1 preparation, to 0·1 to 1 in three passaged populations. The proportion of antigenic variants was quantified using a new plaque immunotest. A nitrocellulose filter is applied to the agar overlay of a FMDV plaque assay, and allows recovery of infectious virus from individual plaques. A second filter is placed directly on the cell monolayer and binds enough virus to permit colorimetric visualization of plaques by an enzyme-linked assay using monoclonal antibodies (MAbs). Either all or a fraction of plaques from passaged FMDV failed to react with MAb 4G3, an antibody that recognizes an epitope located within residues 144 to 150 of capsid protein VP1. Some variants rapidly dominated the viral population, and others were maintained at low levels. RNA from unreactive viruses included mutations that resulted in amino acid substitutions at the epitope recognized by MAb 4G3. We discuss models for the selection of antigenic variants of FMDV in the absence of antibodies, and implications for the antigenic diversification of RNA viruses.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): FMDV , monoclonal antibody , mutation and RNA variability
© Society for General Microbiology 1989
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-70-12-3281
1989-12-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/70/12/JV0700123281.html?itemId=/content/journal/jgv/10.1099/0022-1317-70-12-3281&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, London 337:709–716
     [Google Scholar]
  2. Arrowsmith A. E. M. 1975; Variation among strains of type A foot-and-mouth disease virus in the Eastern Mediterranean region 1964–1972. Journal of Hygiene 75:387–397
     [Google Scholar]
  3. Arrowsmith A. E. M. 1977; A survey of foot-and-mouth disease type O strains from the Far East. Developments in Biological Standardization 35:221–230
     [Google Scholar]
  4. Bachrach H. L. 1968; Foot-and-mouth disease virus. Annual Review of Microbiology 22:201–244
     [Google Scholar]
  5. 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 FMDV by immunization with a chemically synthesized peptide predicted from the viral nucleotide sequence. Nature, London 298:30–33
     [Google Scholar]
  6. Bolwell C., Brown A. L., Barnett P. V., Campbell R. O., Clarke B. E., Parry N. R., Ouldridge E. J., Brown F., Rowlands D. J. 1989; Host cell selection of antigenic variants of foot-and-mouth disease virus. Journal of General Virology 70:45–57
     [Google Scholar]
  7. Brown F. 1979; Structure-function relationships in the picoranaviruses. In The Molecular Biology of Picornaviruses49–72 Perez-Bercoff R. New York: Plenum Press;
     [Google Scholar]
  8. De La Torre J. C., Da Vila M., Sobrino F., Ortin J., Domingo E. 1985; Establishment of cell lines persistently infected with foot-and-mouth disease virus. Virology 45:24–35
     [Google Scholar]
  9. De La Torre J. C., Martinez-Salas E., Diez J., Villaverde A., Gebauer F., Rocha E., Davila M., Domingo E. 1988; Coevolution of cells and viruses in a persistent infection of foot-and-mouth disease virus in cell culture. Journal of Virology 62:2050–2058
     [Google Scholar]
  10. Diamond D. C., Jameson B. A., Bonin J., Kohara M., Abe S., Itoh H., Komatsu T., Arita M., Kuge S., Namoto A., Osterhaus A. D. M., Criinic R., Wimmer E. 1985; Antigenic variation and resistance to neutralization in poliovirus type 1. Science 229:1090–1093
     [Google Scholar]
  11. Domingo E. 1989; RNA virus evolution and the control of viral disease. In Progress in Drug Research 3393–133 Jucker E. Basel: Birkhäuser Verlag;
     [Google Scholar]
  12. Domingo E., Holland J. 1988; High error rates, population equilibrium and evolution of RNA replication systems. In RNA Genetics III3–36 Domingo E., Holland J. J., Ahlquist P. Boca Raton: CRC Press;
     [Google Scholar]
  13. Domingo E., Flavell R. A., Weissmann C. 1976; In vitro site-directed mutagenesis: generation and properties of an infectious extracistronic mutant of bacteriophage Qβ3. Gene 1:3–25
     [Google Scholar]
  14. Domingo E., Sabo D., Taniguchi T., Weissmann C. 1978; Nucleotide sequence heterogeneity of an RNA phage population. Cell 13:735–744
     [Google Scholar]
  15. Domingo E., Davila M., Ortin J. 1980; Nucleotide sequence heterogeneity of the RNA from a natural population of foot-and-mouth disease virus. Gene 11:333–346
     [Google Scholar]
  16. Domingo E., Martinez-Salas E., Sobrino F., De La Torre J. C., Portela A., Ortin J., Lopez-Galindez C., Perez-Breña P., Villanueva N., Najera R., Vandepol S., Steinhauer D., De Polo N., Holland J. 1985; The quasi-species (extremely heterogeneous) nature of viral RNA genome populations: biological relevance – a review. Gene 40:1–8
     [Google Scholar]
  17. Domingo E., Mateu M. G., Martinez M. A., Dopazo J., Moya A., Sobrino F. 1989; Genetic variability and antigenic diversity of foot-and-mouth disease virus. In Applied Virology Research II Kurstak E., Marusyk R. G., Murphy F. A., Van Regenmortel M. H. V. New York: Plenum Press (in press);
     [Google Scholar]
  18. Eigen M., Biebricher C. K. 1988; Sequence space and quasispecies distribution. In RNA Genetics III211–245 Domingo E., Holland J. J., Ahlquist P. Boca Raton: CRC Press;
     [Google Scholar]
  19. Eigen M., Schuster P. 1979 The Hypercycle. A Principle of Natural Self-Organization Berlin: Springer Verlag;
     [Google Scholar]
  20. 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
     [Google Scholar]
  21. Hyslop N. S. G. 1965; Isolation of variant strains from foot-and-mouth disease virus propagated in cell cultures containing antiviral sera. Journal of General Microbiology 41:135–142
     [Google Scholar]
  22. King A. M. Q., Underwood B. O., Mccahon D., Newman J. W. I., Brown F. 1981; Biochemical identification of viruses causing the 1981 outbreaks of foot-and-mouth disease in U.K. Nature, London 293:479–480
     [Google Scholar]
  23. Martinez M. A., Carrillo C., Plana J., Mascarella R., Bergada J., Palma E. L., Domingo E., Sobrino F. 1988; Genetic and immunogenic variations among closely related isolates of foot-and-mouth disease virus. Gene 62:75–84
     [Google Scholar]
  24. 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
     [Google Scholar]
  25. 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
     [Google Scholar]
  26. Mateu M. G., Martinez 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 SciencesU.S.A 86:5883–5887
     [Google Scholar]
  27. Mosley J. W., Enders J. F. 1961; A critique on the plaque assay technique in bottle cultures. Proceedings of the Society for Experimental Biology and Medicine 108:406–408
     [Google Scholar]
  28. Pereira H. G. 1977; Subtyping of foot-and-mouth disease virus. Developments in Biological Standardization 35:167–174
     [Google Scholar]
  29. Pereira H. G. 1981; Foot-and-mouth disease. In Virus Diseases of Food Animals 2333–363 Gibbs E. P. J. New York: Academic Press;
     [Google Scholar]
  30. Pfaff E., Mussgay M., Boehm 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
     [Google Scholar]
  31. Piccone M. E., Kaplan G., Giavedoni L., Domingo E., Palma E. L. 1988; VP1 of serotype C foot-and-mouth disease viruses: long-term conservation of sequences. Journal of Virology 62:1469–1473
     [Google Scholar]
  32. Prabhakar B. S., Menegus M. A., Notkins A. L. 1985; Detection of conserved and non conserved epitopes on coxsackievirus B4: frequency of antigenic change. Virology 146:302–306
     [Google Scholar]
  33. 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, London 306:694–697
     [Google Scholar]
  34. Sherry B., Mosser A. G., Colonno R. J., Rueckert R. R. 1986; Use of monoclonal antibodies to identify four neutralization immunogens on a common cold picornavirus, human rhinovirus 14. Journal of Virology 57:246–257
     [Google Scholar]
  35. Sobrino F., Davila M., Ortin 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
     [Google Scholar]
  36. Sobrino F., Palma E. L., Beck E., Davila M., De La Torre J. C., Negro P., Villanueva N., Ortin J., Domingo E. 1986; Fixation of mutations in the viral genome during an outbreak of foot-and-mouth disease: heterogeneity and rate variations. Gene 50:149–159
     [Google Scholar]
  37. Strohmaier K., Franze R., Adam K. H. 1982; Location and characterization of the antigenic portion of the FMDV immunizing protein. Journal of General Virology 59:259–306
     [Google Scholar]
  38. 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 separate antigenic sites. Journal of General Virology 68:1637–1647
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-70-12-3281
Loading
Selection of Antigenic Variants of Foot-and-Mouth Disease Virus in the Absence of Antibodies, as Revealed by an in situ Assay
J. Gen. Virol. 70, 3281 (1989); https://doi.org/10.1099/0022-1317-70-12-3281
/content/journal/jgv/10.1099/0022-1317-70-12-3281
/content/journal/jgv/10.1099/0022-1317-70-12-3281
Loading

Data & Media loading...

Most cited 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