Evolution of a persistent aphthovirus in cytolytic infections: Partial reversion of phenotypic traits accompanied by genetic diversification

Journal of Virology

Volumn 70, Issue 10, 1996, Pages 6617-6624

  Sevilla, Noemi ^a   Domingo, Esteban ^a,b  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CYTOLYSIS; EVOLUTION; FOOT AND MOUTH DISEASE VIRUS; GENOTYPE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA VIRUS INFECTION; VIRAL GENETICS; VIRUS MUTATION; VIRUS REPLICATION;

EID: 0029794374     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.10.6617-6624.1996     Document Type: Article

References (54)

1. 3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells. J. Virol. 69:2664-2666.
2. Borrego, B., I. S. Novella, E. Giralt, D. Andreu, and E. Domingo. 1993. Distinct repertoire of antigenic variants of foot-and-mouth disease virus in the presence or absence of immune selection. J. Virol. 67:6071-6079.
3. Burrows, R., J. A. Mann, A. J. M. Garland, A. Greig, and D. Groodridge. 1981. The pathogenesis of natural and simulated natural foot-and-mouth-disease infection in cattle. J. Comp. Pathol. 91:599-609.
4. Carrillo, C., J. Plana, R. Mascarella, J. Bergadá, and F. Sobrino. 1990. Genetic and phenotypic variability during replication of foot-and-mouth disease virus in swine. Virology 179:890-892.
5. Clarke, D. K., E. A. Duarte, A. Moya, S. F. Elena, E. Domingo, and J. J. Holland. 1993. Genetic bottlenecks and population passages cause profound fitness differences in RNA viruses. J. Virol. 67:222-228.
6. Couderc, T., N. Guédo, V. Calvez, I. Pelletier, J. Hogle, F. Colbère-Garapin, and B. Blondel. 1994. Substitutions in the capsids of poliovirus mutants selected in human neuroblastoma cells confer on the Mahoney type 1 strain a phenotype neurovirulent in mice. J. Virol. 68:8386-8391.
7. Chao, L. 1990. Fitness of RNA virus decreased by Muller's ratchet. Nature (London) 348:454-455.
8. Chumakov, K. M., E. M. Dragunsky, L. P. Norwood, M. P. Douthilt, Y. Ran, R. E. Taffs, J. Ridge, and I. S. Levenbook. 1994. Consistent selection of mutations in the 5′-untranslated region of oral poliovirus vaccine upon passaging in vitro. J. Med. Virol. 42:79-85.
9. de la Torre, J. C., M. Dávila, F. Sobrino, J. Ortín, and E. Domingo. 1985. Establishment of cell lines persistently infected with foot-and-mouth disease virus. Virology 145:24-35.
10. de la Torre, J. C., S. de la Luna, J. Díez, and E. Domingo. 1989. Resistance to foot-and-mouth disease virus mediated by trans-acting cellular products. J. Virol. 63:2385-2387.
11. de la Torre, J. C., C. Giachetti, B. L. Semler, and J. J. Holland. 1992. High frequency of single-base transitions and extreme frequency of precise multiple-base reversion mutations in poliovirus. Proc. Natl. Acad. Sci. USA 89:2531-2535.
12. de la Torre, J. C., E. Martínez-Salas, J. Díez, and E. Domingo. 1989. Extensive cell heterogeneity during a persistent infection with foot-and-mouth disease virus. J. Virol. 63:59-63.
13. de la Torre, J. C., E. Martínez-Salas, J. Díez, D. Villaverde, F. Gebauer, E. Rocha, M. Dávila, and E. Domingo. 1988. Coevolution of cells and viruses in a persistent infection of foot-and-mouth disease virus in cell culture. J. Virol. 62:2050-2058.
14. Díez, J., M. Dávila, C. Escarmís, M. G. Mateu, J. Domínguez, J. J. Pérez, E. Giralt, J. A. Melero, and E. Domingo. 1990. Unique amino acid substitutions in the capsid proteins of foot-and-mouth disease virus from a persistent infection in cell culture. J. Virol. 64:5519-5528.
15. Díez, J., M. Hofner, E. Domingo, and A. I. Donaldson. 1990. Foot-and-mouth disease virus strains isolated from persistently infected cell cultures are attenuated for mice and cattle. Virus Res. 18:3-8.
16. Díez, J., M. G. Mateu, and E. Domingo. 1989. 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. 70:3281-3289.
17. Di Girolamo, W., M. Salas, and R. P. Laguens. 1985. Role of Langerhans cells in the infection of the guinea-pig epidermis with foot-and-mouth disease virus. Arch. Virol. 83:331-336.
18. Domingo, E., M. Dávila, and J. Ortín. 1980. Nucleotide sequence heterogeneity of the RNA from a natural population of foot-and-mouth disease virus. Gene 11:333-346.
19. Domingo, E., C. Escarmís, M. A. Martínez, E. Martínez-Salas, and M. G. Mateu. 1992. Foot-and-mouth disease virus populations are quasispecies. Curr. Top. Microbiol. Immunol. 176:33-47.
20. Domingo, E., and J. J. Holland. 1994. Mutation rates and rapid evolution of RNA viruses, p. 161-184. In S. S. Morse (ed.), Evolutionary biology of viruses. Raven Press, New York.
21. Domingo, E., M. G. Mateu, C. Escarmís, E. Martínez-Salas, D. Andreu, E. Giralt, N. Verdaguer, and I. Fita. 1996. Molecular evolution of aphthoviruses. Virus Genes 11:197-207.
22. Domingo, E., D. L. Sabo, T. Taniguchi, and C. Weissmann. 1978. Nucleotide sequence heterogeneity of an RNA phage population. Cell 13:735-744.
23. Donn, A., M. Castagnaro, and A. I. Donaldson. 1995. Ultrastructural and replicative features of foot-and-mouth disease virus in persistently infected BHK-21 cells. Arch. Virol. 140:13-25.
24. Drake, J. W. 1993. Rates of spontaneous mutations among RNA viruses. Proc. Natl. Acad. Sci. USA 90:4171-4175.
25. Duarte, E., D. Clarke, A. Moya, E. Domingo, and J. J. Holland. 1992. Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet. Proc. Natl. Acad. Sci. USA 89:6015-6019.
26. Eigen, M., and C. K. Biebricher. 1988. Sequence space and quasispecies distribution, p. 211-245. In E. Domingo, J. J. Holland, and P. Ahlquist (ed.), RNA genetics, vol. 3. CRC Press, Inc. Boca Raton, Fla.
27. Escarmís, C., M. Toja, M. Medina, and E. Domingo. 1992. Modifications of the 5′ untranslated region of foot-and-mouth disease virus after prolonged persistence in cell culture. Virus Res. 26:113-125.
28. Feng, D. F., M. S. Johnson, and R. F. Doolittle. 1985. Aligning amino acid sequences: comparison of commonly used methods. J. Mol. Evol. 21:112-125.
29. Fox, G., N. Parry, P. V. Barnett, B. McGinn, D. J. Rowlands, and F. Brown. 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.
30. Gebauer, F., J. C. de la Torre, I. Gomes, M. G. Mateu de Mello, and E. Domingo. 1988. Rapid selection of genetic and antigenic variants of foot-and-mouth disease virus during persistence in cattle. J. Virol. 62:2041-2049.
31. Harris, T. J. R., and F. Brown. 1977. Biochemical analysis of a virulent and an avirulent strain of foot-and-mouth disease virus. J. Gen. Virol. 34:87-105.
32. Hernández, J., M. L. Valero, D. Andreu, E. Domingo, and M. G. Mateu. 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. J. Gen. Virol. 77:257-264.
33. 32a.Holguín, A., et al. Unpublished results.
34. Kimura, M. 1980. A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
35. Lea, S., J. Hernández, W. Blakemore, E. Brocchi, S. Curry, E. Domingo, E. Fry, R. Abu-Ghazaleh, A. King, J. Newman, D. Stuart, and M. G. Mateu. 1994. The structure and antigenicity of type C foot-and-mouth disease virus. Structure 2:123-139.
36. Lu, Z., G. V. Rezapkin, M. P. Douthitt, Y. Ran, D. M. Asher, I. S. Levenbook, and K. M. Chumakov. 1996. Limited genetic changes in the Sabin 1 strain poliovirus occurring in the central nervous system of monkeys. J. Gen. Virol. 77:273-280.
37. Malirat, V., P. Augé de Mello, B. Tiraboschi, E. Beck, I. Gomes, and I. E. Bergmann. 1994. Genetic variation of foot-and-mouth disease virus during persistent infection in cattle. Virus Res. 34:31-48.
38. 36a.Martínez, M. A. Unpublished results.
39. Martínez, M. A., C. Carrillo, F. González-Candelas, A. Moya, E. Domingo, and F. Sobrino. 1991. Fitness alteration of foot-and-mouth disease virus mutants: measurement of adaptability of viral quasispecics. J. Virol. 65: 3954-3957.
40. Martíhez-Salas, E., M. P. Regalado, and E. Domingo. 1996. Identification of an essential region for internal initiation of translation in the aphthovirus internal ribosome entry site and implications for viral evolution. J. Virol. 70:992-998.
41. Martínez-Salas, E., J. C. Sáiz. M. Dávila, G. J. Belsham, and E. Domingo. 1993. A single nucleotide substitution in the internal ribosome entry site of foot-and-mouth disease virus leads to enhanced cap-independent translation in vivo. J. Virol. 67:3748-3755.
42. Martín-Hernández, A. M., E. C. Carrillo, N. Sevilla, and E. Domingo. 1994. Rapid cell variation can determine the establishment of a persistent viral infection. Proc. Natl. Acad. Sci. USA 91:3705-3709.
43. Mason, M. W., E. Rieder, and B. Baxt. 1994. ROD 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. Proc. Natl. Acad. Sci. USA 91:1932-1936.
44. Mateu, M. G., J. Hernández, M. A. Martínez, D. Feigelstock, S. Lea, J. J. Pérez, E. Giralt, D. Stuart, E. L. Palma, and E. Domingo. 1994. Antigenic heterogeneity of a foot-and-mouth disease virus serotype in the field is mediated by very limited sequence variation at several antigenic sites. J. Virol. 68:1407-1417.
45. Mateu, M. G., M. L. Valero, D. Andreu, and E. Domingo. 1996. Systematic replacement of amino acid residues within the Arg-Gly-Asp-containing loop of foot-and-moulh disease virus: effect on cell recognition. J. Biol. Chem. 271:12814-12819.
46. Nei, M. 1987. Molecular evolutionary genetics. Columbia University Press, New York.
47. Novella, I. S., E. A. Duarte, S. F. Elena, A. Moya, E. Domingo, and J. J. Holland. 1995. Exponential increases of RNA virus fitness during large population transmissions. Proc. Natl. Acad. Sci. USA 92:5841-5844.
48. Rueckert, R. R. 1996. Picornaviridae: the viruses and their replication, p. 609-654. In B. N. Fields et al. (ed.), Virology. Lippincott-Raven Publishers, Philadelphia.
49. Salt, J. S. 1993. The carrier state in foot-and-mouth disease - an immunological review. Br. Vet. J. 149:207-223.
50. Sobrino, F., M. Dávila, J. Ortín, and E. Domingo. 1983. Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology 128:310-318.
51. van Bekkum, J. G., H. S. Frenkel, H. H. J. Frederiks, and S. Frenkel. 1959. Observations on the carrier state of cattle exposed to foot-and-mouth disease virus. Tijdschr. Diergeneeskd. 84:1159-1164.
52. Wimmer, E., C. U. T. Hellen, and X. Cao. 1993. Poliovirus genetics. Annu. Rev. Genet. 27:353-436.
53. Woodbury, E. L. 1995. A review of the possible mechanisms for the persistence of foot-and-mouth disease virus. Epidemiol. Infect. 114:1-13.
54. Yilma, T. 1980. Morphogenesis of vesiculation in foot-and-mouth disease. Am. J. Vet. Res. 41:1537-1542.