1887

Abstract

To understand the mutations and genetic rearrangements that allow rabies virus infections of new hosts and adaptation in nature, the quasispecies structure of the nucleoprotein and glycoprotein genes as well as two noncoding sequences of a rabies virus genome were determined. Gene sequences were obtained from the brain and from the salivary glands of the original host, a naturally infected European fox, and after serial passages in mice, dogs, cats and cell culture. A relative genetic stasis of the consensus sequences confirmed previous results about the stability of rabies virus. At the quasispecies level, the mutation frequency varies, in the following order: glycoprotein region (21·9×10 mutations per bp), noncoding sequence nucleoprotein–phosphoprotein region (7·2–7·9×10 mutations per bp) and nucleoprotein gene region (2·9–3·7×10 mutations per bp). These frequencies varied according to the number, type of heterologous passages and the genomic region considered. The shape of the quasispecies structure was dramatically modified by passages in mice, in which the mutation frequencies increased by 12–31×10 mutations per bp, depending on the region considered. Nonsynonymous mutations were preponderant particularly in the glycoprotein gene, stressing the importance of positive selection in the maintenance and fixation of substitutions. Two mechanisms of genomic evolution of the rabies virus quasispecies, while adapting to environmental changes, have been identified: a limited accumulation of mutations with no replacement of the original master sequence and a less frequent but rapid selective overgrowth of favoured variants.

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1999-08-01
2019-12-06
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References

  1. Adami, C., Pooley, J., Glomb, J., Stecker, E., Fazal, F., Fleming, J. O. & Baker, S. C. ( 1995; ). Evolution of mouse hepatitis virus (MHV) during chronic infection: quasispecies nature of the persisting MHV RNA. Virology 209, 337-346.[CrossRef]
    [Google Scholar]
  2. Amengual, B., Whitby, J. E., King, A., Serra Cobo, J. & Bourhy, H. ( 1997; ). Evolution of European bat lyssavirus. Journal of General Virology 78, 2319-2328.
    [Google Scholar]
  3. Barnes, W. M. ( 1992; ). The fidelity of Taq polymerase catalysing PCR is improved by an N-terminal deletion. Gene 112, 29-35.[CrossRef]
    [Google Scholar]
  4. Bass, B. L., Weintraub, H., Cattaneo, R. & Billeter, M. A. ( 1989; ). Biased hypermutation of viral RNA genome could be due to unwinding/modification of double-stranded RNA. Cell 56, 331.[CrossRef]
    [Google Scholar]
  5. Benmansour, A., Leblois, H., Coulon, P., Tuffereau, C., Lafay, F. & Flamand, A. ( 1991; ). Antigenicity of rabies virus glycoprotein. Journal of Virology 65, 4198-4203.
    [Google Scholar]
  6. Benmansour, A., Brahimi, M., Tuffereau, C., Coulon, P., Lafay, F. & Flamand, A. ( 1992; ). Rapid sequence evolution of street rabies glycoprotein is related to the highly heterogeneous nature of the viral population. Virology 187, 33-45.[CrossRef]
    [Google Scholar]
  7. Bourhy, H. & Sureau, P. (1991). Laboratory Methods for Rabies Diagnosis, p. 197. Paris: Institut Pasteur.
  8. Bourhy, H., Rollin, P. E., Vincent, J. & Sureau, P. ( 1989; ). Comparative field evaluation of the fluorescent-antibody test, virus isolation from tissue culture, and enzyme immunodiagnosis for rapid laboratory diagnosis of rabies. Journal of Clinical Microbiology 27, 519-523.
    [Google Scholar]
  9. Bourhy, H., Kissi, B. & Tordo, N. ( 1993; ). Molecular diversity of the Lyssavirus genus. Virology 194, 70-81.[CrossRef]
    [Google Scholar]
  10. Bracho, M. A., Moya, A. & Barrio, E. ( 1998; ). Contribution of Taq polymerase-induced errors to the estimation of RNA virus diversity. Journal of General Virology 79, 2921-2928.
    [Google Scholar]
  11. Britten, J. R. ( 1993; ). Forbidden synonymous substitutions in coding regions. Molecular Biology and Evolution 10, 205-220.
    [Google Scholar]
  12. Cattaneo, R., Schmid, A., Eschle, D., Baczko, K., Meulen, V. & Billeter, M. A. ( 1988; ). Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell 55, 255-265.[CrossRef]
    [Google Scholar]
  13. Clarke, D. K., Duarte, E. A., Elena, S. F., Moya, A., Domingo, E. & Holland, J. J. ( 1994; ). The red queen reigns in the kingdom of RNA viruses. Proceedings of the National Academy of Sciences, USA 91, 4821-4824.[CrossRef]
    [Google Scholar]
  14. de la Torre, J. C. & Holland, J. J. ( 1990; ). RNA virus quasispecies populations can suppress vastly superior mutant progeny. Journal of Virology 64, 6278-6281.
    [Google Scholar]
  15. Dietzschold, B., Wunner, W. H., Wiktor, T. J., Lopes, A. D., Lafon, M., Smith, C. L. & Koprowski, H. ( 1983; ). Characterization of an antigenic determinant of the glycoprotein that correlates with pathogenicity of rabies virus. Proceedings of the National Academy of Sciences, USA 80, 70-74.[CrossRef]
    [Google Scholar]
  16. Domingo, E. & Holland, J. J. ( 1994; ). Mutation rates and rapid evolution of RNA viruses. In The Evolutionary Biology of Viruses, pp. 161-184. Edited by S. S. Morse. New York: Raven Press.
  17. Domingo, E. & Holland, J. J. ( 1997; ). RNA virus mutations and fitness for survival. Annual Review of Microbiology 51, 151-178.[CrossRef]
    [Google Scholar]
  18. Domingo, E., Sabo, D., Taniguchi, T. & Weissmann, C. ( 1978; ). Nucleotide sequence heterogeneity of an RNA phage population. Cell 13, 735-744.[CrossRef]
    [Google Scholar]
  19. Domingo, E., Davilla, M. & Ortin, J. ( 1980; ). Nucleotide sequence heterogeneity of the RNA from a natural population of foot-and-mouth disease virus. Gene 11, 333-346.[CrossRef]
    [Google Scholar]
  20. Domingo, E., Martinez-Salas, E., Sobrino, F., de la Torre, J. C., Portela, A., Ortin, J., Lopez-Galindez, C., Pérez-Brena, P., Villanueva, N., Najera, R., Van de Pol, S., Steinhauer, D., De Polo, N. & Holland, J. J. ( 1985; ). The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance – a review. Gene 40, 1-8.
    [Google Scholar]
  21. Drake, J. W. ( 1993; ). Rates of spontaneous mutations among RNA viruses. Proceedings of the National Academy of Sciences, USA 90, 4171-4175.[CrossRef]
    [Google Scholar]
  22. Flamand, A., Raux, H. & Ruigrok, R. W. H. ( 1993; ). Mechanisms of rabies virus neutralization. Virology 194, 302-313.[CrossRef]
    [Google Scholar]
  23. Goodenow, M., Huet, T., Saurin, W., Kwok, S., Sninsky, J. & Wain-Hobson, S. ( 1989; ). HIV-1 isolates are rapidly evolving quasispecies: evidence for viral mixtures and preferred nucleotide substitutions. Journal of Acquired Immune Deficiency Syndromes 2, 344-352.
    [Google Scholar]
  24. Holland, J. J., De la Torre, J. C. & Steinhauer, D. A. ( 1992; ). RNA virus populations as quasispecies. Current Topics in Microbiology and Immunology 176, 1-21.
    [Google Scholar]
  25. Kissi, B., Tordo, N. & Bourhy, H. ( 1995; ). Genetic polymorphism in the rabies virus nucleoprotein gene. Virology 209, 526-537.[CrossRef]
    [Google Scholar]
  26. Kumar, S., Tamura, K. & Nei, M. (1995). MEGA: Molecular evolutionary genetic analysis, version 1.0. The Pennsylvania State University, University Park, PA 16802, USA.
  27. Lafay, F., Benejean, J., Flamand, A., Tuffereau, C. & Coulon, P. ( 1994; ). Vaccination against rabies: construction and characterization of SAG2, a double avirulent derivative of SADbern. Vaccine 12, 317-319.[CrossRef]
    [Google Scholar]
  28. Li, W.-H. (1997). Molecular Evolution. Sunderland, MA: Sinauer Associates.
  29. Martinez, M. A., Vartanian, J.-P. & Wain Hobson, S. ( 1994; ). Hypermutagenesis of RNA using human immunodeficiency virus type 1 reverse transcriptase and biased dNTP concentration. Proceedings of the National Academy of Sciences, USA 91, 11787-11791.[CrossRef]
    [Google Scholar]
  30. Martínez, I., Dopazo, J. & Melero, J. A. ( 1997; ). Antigenic structure of the human respiratory syncytial virus glycoprotein and relevance of hypermutation events for the generation of antigenic variants. Journal of General Virology 78, 2419-2429.
    [Google Scholar]
  31. Morimoto, K., Hooper, D. C., Carbaugh, H., Fu, Z. F., Koprowski, H. & Dietzschold, B. ( 1998; ). Rabies virus quasispecies: implication for pathogenesis. Proceedings of the National Academy of Sciences, USA 95, 3152-3156.[CrossRef]
    [Google Scholar]
  32. Nadin-Davis, S. A., Casey, G. A. & Wandeler, A. ( 1993; ). Identification of regional variants of the rabies virus within the Canadian province of Ontario. Journal of General Virology 74, 829-837.[CrossRef]
    [Google Scholar]
  33. Nadin-Davis, S. A., Casey, G. A. & Wandeler, A. I. ( 1994; ). A molecular epidemiological study of rabies virus in central Ontario and western Quebec. Journal of General Virology 75, 2575-2583.[CrossRef]
    [Google Scholar]
  34. Plyusnin, A., Vapalahti, O., Lehväslaiho, H., Apekina, N., Mikhailova, T., Gavrilovskaya, I., Laakkonen, J., Niemimaa, J., Henttonen, H., Brummer-Korvenkontio, M. & Vaheri, H. ( 1995; ). Genetic variation of wild Puumala viruses within the serotype, local rodent populations and individual animals. Virus Research 38, 25-41.[CrossRef]
    [Google Scholar]
  35. Rima, B. K., Earle, J. A. P., Baczko, K., Rota, P. A. & Bellini, W. J. ( 1995; ). Measles virus strain variations. Current Topics in Microbiology and Immunology 191, 65-83.
    [Google Scholar]
  36. Sacramento, D., Bourhy, H. & Tordo, N. ( 1991; ). PCR technique as an alternative method for diagnosis and molecular epidemiology of rabies virus. Molecular and Cellular Probes 6, 229-240.
    [Google Scholar]
  37. Sacramento, D., Badrane, H., Bourhy, H. & Tordo, N. ( 1992; ). Molecular epidemiology of rabies virus in France: comparison with vaccine strains. Journal of General Virology 73, 1149-1158.[CrossRef]
    [Google Scholar]
  38. Seif, I., Coulon, P., Rollin, P. E. & Flamand, A. ( 1985; ). Rabies virulence: effect on pathogenicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. Journal of Virology 53, 926-934.
    [Google Scholar]
  39. Sevilla, N., Ruiz-Jarabo, C. M., Gómez-Mariano, G., Baranowski, E. & Domingo, E. ( 1998; ). An RNA virus can adapt to the multiplicity of infection. Journal of General Virology 79, 2971-2980.
    [Google Scholar]
  40. Smith, J. S., Yager, P. A. & Baer, G. M. ( 1973; ). A rapid tissue culture test for determining rabies neutralizing antibody. In Laboratory Techniques in Rabies, pp. 354-357. Edited by M. M. Kaplan & H. Koprowski. Geneva: World Health Organization.
  41. Smith, J. S., Orciari, L. A., Yager, P., Seidel, H. D. & Warner, C. K. ( 1992; ). Epidemiologic and historical relationships among 87 rabies virus isolates as determined by limited sequence analysis. Journal of Infectious Diseases 166, 296-307.[CrossRef]
    [Google Scholar]
  42. Smith, D. B., McAllister, J., Casino, C. & Simmonds, P. ( 1997; ). Virus ‘quasispecies’: making a mountain out of a molehill? Journal of General Virology 78, 1511-1519.
    [Google Scholar]
  43. Spindler, K. R., Horodyski, F. M. & Holland, J. J. ( 1982; ). High multiplicities of infection favor rapid and random evolution of vesicular stomatitis virus. Virology 119, 96-108.[CrossRef]
    [Google Scholar]
  44. Steinhauer, D. A. & Holland, J. J. ( 1987; ). Rapid evolution of RNA viruses. Annual Review of Microbiology 41, 409-433.[CrossRef]
    [Google Scholar]
  45. Steinhauer, D. A., de la Torre, J. C., Meier, E. & Holland, J. J. ( 1989; ). Extreme heterogeneity in populations of vesicular stomatitis virus. Journal of Virology 63, 2072-2080.
    [Google Scholar]
  46. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). CLUSTAL W: improving the sensitivity of progressive multiple alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673-4680.[CrossRef]
    [Google Scholar]
  47. Thoulouse, M.-I., Lafage, M., Schachner, M., Hartmann, U., Cremer, H. & Lafon, M. ( 1998; ). The neural cell adhesion molecule is a receptor for rabies virus. Journal of Virology 72, 7181-7190.
    [Google Scholar]
  48. Tordo, N., Poch, O., Ermine, A., Keith, G. & Rougeon, F. ( 1986; ). Walking along the rabies genome: is the large G–L intergenic region a remnant gene? Proceedings of the National Academy of Sciences, USA 83, 3914-3918.[CrossRef]
    [Google Scholar]
  49. Tordo, N., Poch, O., Ermine, A., Keith, G. & Rougeon, F. ( 1988; ). Completion of the rabies virus genome sequence determination: highly conserved domains along the L (polymerase) proteins of unsegmented negative-strand RNA viruses. Virology 165, 565-576.[CrossRef]
    [Google Scholar]
  50. Tordo, N., Bourhy, H., Sather, S. & Ollo, R. ( 1993a; ). Structure and expression in baculovirus of the Mokola virus glycoprotein: an efficient recombinant vaccine. Virology 194, 59-69.[CrossRef]
    [Google Scholar]
  51. Tordo, N., Badrane, H., Bourhy, H. & Sacramento, D. ( 1993b; ). Molecular epidemiology of lyssaviruses: focus on the glycoprotein and pseudogenes. Onderstepoort Journal of Veterinary Research 60, 315-323.
    [Google Scholar]
  52. Tuffereau, C., Benejean, J., Roque Alfonso, A.-M., Flamand, A. & Fishman, M. C. ( 1998; ). Neuronal cell surface molecules mediate specific binding to rabies virus glycoprotein expressed by a recombinant baculovirus on the surfaces of lepidopteran cells. Journal of Virology 72, 1085-1091.
    [Google Scholar]
  53. Vodopija, I. & Clark, H. F. ( 1991; ). Human vaccination against rabies. In The Natural History of Rabies, pp. 571-595. Edited by G. M. Baer. Boca Raton: CRC Press.
  54. Wagner, R. W., Smith, J. E., Cooperman, B. S. & Nishikuro, K. ( 1989; ). A double stranded RNA unwinding activity introduces structural alterations by means of adenosine to inosine conversions in mammalian cells and Xenopus eggs. Proceedings of the National Academy of Sciences, USA 86, 2647-2651.[CrossRef]
    [Google Scholar]
  55. Wandeler, A. I., Nadin-Davis, S. A., Tinline, R. R. & Rupprecht, C. E. ( 1994; ). Rabies epidemiology: some ecological and evolutionary perspectives. In Lyssaviruses, pp. 297-324. Edited by C. E. Rupprecht, B. Dietzschold & H. Koprowski. Berlin: Springer-Verlag.
  56. Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M. & Kawaoka, Y. ( 1992; ). Evolution and ecology of influenza A viruses. Microbiological Reviews 56, 152-179.
    [Google Scholar]
  57. Whitt, M. A., Buonocore, L., Préhaud, C. & Rose, J. K. ( 1991; ). Membrane fusion activity, oligomerization, and virus assembly of the rabies virus glycoprotein. Virology 185, 681-688.[CrossRef]
    [Google Scholar]
  58. Wiktor, T. J., Dietzschold, B., Leamnson, R. N. & Koprowski, H. ( 1977; ). Induction and biological properties of defective interfering particles of rabies virus. Journal of Virology 21, 626-635.
    [Google Scholar]
  59. Wiktor, T. J., Macfarlan, R. I., Reagan, K. J., Dietzschold, B., Curtis, P. J., Wunner, W. H., Kieny, M., Lathe, P., Lecocq, J. P. & Mackett, M. ( 1984; ). Protection from rabies by a vaccinia virus recombinant containing the rabies virus glycoprotein gene. Proceedings of the National Academy of Sciences, USA 81, 7194-7198.[CrossRef]
    [Google Scholar]
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