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. 1991 Jul;65(7):3954–3957. doi: 10.1128/jvi.65.7.3954-3957.1991

Fitness alteration of foot-and-mouth disease virus mutants: measurement of adaptability of viral quasispecies.

M A Martínez 1, C Carrillo 1, F González-Candelas 1, A Moya 1, E Domingo 1, F Sobrino 1
PMCID: PMC241436  PMID: 1645804

Abstract

We document the rapid alteration of fitness of two foot-and-mouth disease virus (FMDV) mutants resistant to a neutralizing monoclonal antibody. Both mutants showed a selective disadvantage in BHK-21 cells when passaged in competition with their parental FMDV. Upon repeated replication of the mutants alone, they acquired a selective advantage over the parental FMDV and fixed additional genomic substitutions without reversion of the monoclonal antibody-resistant phenotype. Thus, variants that were previously kept at low frequency in the mutant spectrum of a viral quasispecies rapidly became the master sequence of a new genomic distribution and dominated the viral population.

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Selected References

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  1. Batschelet E., Domingo E., Weissmann C. The proportion of revertant and mutant phage in a growing population, as a function of mutation and growth rate. Gene. 1976;1(1):27–32. doi: 10.1016/0378-1119(76)90004-4. [DOI] [PubMed] [Google Scholar]
  2. Carman W. F., Zanetti A. R., Karayiannis P., Waters J., Manzillo G., Tanzi E., Zuckerman A. J., Thomas H. C. Vaccine-induced escape mutant of hepatitis B virus. Lancet. 1990 Aug 11;336(8711):325–329. doi: 10.1016/0140-6736(90)91874-a. [DOI] [PubMed] [Google Scholar]
  3. Domingo E., Dávila M., Ortín J. Nucleotide sequence heterogeneity of the RNA from a natural population of foot-and-mouth-disease virus. Gene. 1980 Nov;11(3-4):333–346. doi: 10.1016/0378-1119(80)90073-6. [DOI] [PubMed] [Google Scholar]
  4. Domingo E. RNA virus evolution and the control of viral disease. Prog Drug Res. 1989;33:93–133. doi: 10.1007/978-3-0348-9146-2_5. [DOI] [PubMed] [Google Scholar]
  5. Domingo E., Sabo D., Taniguchi T., Weissmann C. Nucleotide sequence heterogeneity of an RNA phage population. Cell. 1978 Apr;13(4):735–744. doi: 10.1016/0092-8674(78)90223-4. [DOI] [PubMed] [Google Scholar]
  6. Dykhuizen D., Hartl D. L. Selective neutrality of 6PGD allozymes in E. coli and the effects of genetic background. Genetics. 1980 Dec;96(4):801–817. doi: 10.1093/genetics/96.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eigen M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften. 1971 Oct;58(10):465–523. doi: 10.1007/BF00623322. [DOI] [PubMed] [Google Scholar]
  8. Gonzalez M. J., Saiz J. C., Laor O., Moore D. M. Antigenic stability of foot-and-mouth disease virus variants on serial passage in cell culture. J Virol. 1991 Jul;65(7):3949–3953. doi: 10.1128/jvi.65.7.3949-3953.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Holland J. J., de la Torre J. C., Clarke D. K., Duarte E. Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol. 1991 Jun;65(6):2960–2967. doi: 10.1128/jvi.65.6.2960-2967.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Holland J. J., de la Torre J. C., Steinhauer D. A., Clarke D., Duarte E., Domingo E. Virus mutation frequencies can be greatly underestimated by monoclonal antibody neutralization of virions. J Virol. 1989 Dec;63(12):5030–5036. doi: 10.1128/jvi.63.12.5030-5036.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Holland J., Spindler K., Horodyski F., Grabau E., Nichol S., VandePol S. Rapid evolution of RNA genomes. Science. 1982 Mar 26;215(4540):1577–1585. doi: 10.1126/science.7041255. [DOI] [PubMed] [Google Scholar]
  12. Kinnunen L., Huovilainen A., Pöyry T., Hovi T. Rapid molecular evolution of wild type 3 poliovirus during infection in individual hosts. J Gen Virol. 1990 Feb;71(Pt 2):317–324. doi: 10.1099/0022-1317-71-2-317. [DOI] [PubMed] [Google Scholar]
  13. Mateu M. G., Da Silva J. L., Rocha E., De Brum D. L., Alonso A., Enjuanes L., Domingo E., Barahona H. Extensive antigenic heterogeneity of foot-and-mouth disease virus of serotype C. Virology. 1988 Nov;167(1):113–124. doi: 10.1016/0042-6822(88)90060-8. [DOI] [PubMed] [Google Scholar]
  14. Mateu M. G., Martínez M. A., Capucci L., Andreu D., Giralt E., Sobrino F., Brocchi E., Domingo E. A single amino acid substitution affects multiple overlapping epitopes in the major antigenic site of foot-and-mouth disease virus of serotype C. J Gen Virol. 1990 Mar;71(Pt 3):629–637. doi: 10.1099/0022-1317-71-3-629. [DOI] [PubMed] [Google Scholar]
  15. Mateu M. G., Martínez M. A., Rocha E., Andreu D., Parejo J., Giralt E., Sobrino F., Domingo E. Implications of a quasispecies genome structure: effect of frequent, naturally occurring amino acid substitutions on the antigenicity of foot-and-mouth disease virus. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5883–5887. doi: 10.1073/pnas.86.15.5883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mateu M. G., Rocha E., Vicente O., Vayreda F., Navalpotro C., Andreu D., Pedroso E., Giralt E., Enjuanes L., Domingo E. Reactivity with monoclonal antibodies of viruses from an episode of foot-and-mouth disease. Virus Res. 1987 Sep;8(3):261–274. doi: 10.1016/0168-1702(87)90020-7. [DOI] [PubMed] [Google Scholar]
  17. Meyerhans A., Cheynier R., Albert J., Seth M., Kwok S., Sninsky J., Morfeldt-Månson L., Asjö B., Wain-Hobson S. Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell. 1989 Sep 8;58(5):901–910. doi: 10.1016/0092-8674(89)90942-2. [DOI] [PubMed] [Google Scholar]
  18. Rowlands D. J., Clarke B. E., Carroll A. R., Brown F., Nicholson B. H., Bittle J. L., Houghten R. A., Lerner R. A. Chemical basis of antigenic variation in foot-and-mouth disease virus. Nature. 1983 Dec 15;306(5944):694–697. doi: 10.1038/306694a0. [DOI] [PubMed] [Google Scholar]
  19. Sobrino F., Dávila M., Ortín J., Domingo E. Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology. 1983 Jul 30;128(2):310–318. doi: 10.1016/0042-6822(83)90258-1. [DOI] [PubMed] [Google Scholar]
  20. Sobrino F., Palma E. L., Beck E., Dávila M., de la Torre J. C., Negro P., Villanueva N., Ortín J., Domingo E. Fixation of mutations in the viral genome during an outbreak of foot-and-mouth disease: heterogeneity and rate variations. Gene. 1986;50(1-3):149–159. doi: 10.1016/0378-1119(86)90320-3. [DOI] [PubMed] [Google Scholar]
  21. Steinhauer D. A., Holland J. J. Rapid evolution of RNA viruses. Annu Rev Microbiol. 1987;41:409–433. doi: 10.1146/annurev.mi.41.100187.002205. [DOI] [PubMed] [Google Scholar]
  22. Steinhauer D. A., de la Torre J. C., Meier E., Holland J. J. Extreme heterogeneity in populations of vesicular stomatitis virus. J Virol. 1989 May;63(5):2072–2080. doi: 10.1128/jvi.63.5.2072-2080.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Valcárcel J., Ortín J. Phenotypic hiding: the carryover of mutations in RNA viruses as shown by detection of mar mutants in influenza virus. J Virol. 1989 Sep;63(9):4107–4109. doi: 10.1128/jvi.63.9.4107-4109.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. de la Torre J. C., Martínez-Salas E., Diez J., Villaverde A., Gebauer F., Rocha E., Dávila M., Domingo E. Coevolution of cells and viruses in a persistent infection of foot-and-mouth disease virus in cell culture. J Virol. 1988 Jun;62(6):2050–2058. doi: 10.1128/jvi.62.6.2050-2058.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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