1887

Abstract

Perhaps the most important factor to limit the effectiveness of vaccines against virus infections is that of virus variation. Successful vaccines have been developed against viruses such as those causing smallpox, measles, yellow fever and poliomyelitis, and they are effective against most circulating virus strains. However, with some viruses vaccination has been much less successful either because numerous antigenically distinct strains co-circulate, as is the case for rhinoviruses, or because new strains are continually emerging, as in the case of influenza virus. Despite the importance of virus variability, little is known about the factors that influence it and that are responsible for the dramatically different patterns of variation displayed by different viruses. The primary source of variation is obviously mutation, and it has been suggested in several recent papers that the extreme variability of some viruses may be a consequence of an unusually high rate of mutation (Holland ., 1982; Reanney, 1984; Domingo ., 1985; Saitou & Nei, 1986). The purpose of this analytical review is to summarize recent information about the mutation rates of eukaryotic viruses, and to discuss the relationship between such rates and virus variability in the field.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-68-11-2729
1987-11-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/68/11/JV0680112729.html?itemId=/content/journal/jgv/10.1099/0022-1317-68-11-2729&mimeType=html&fmt=ahah

References

  1. Battula N., Loeb L. A. 1974; The infidelity of avian myeloblastosis virus deoxyribonucleic acid polymerase in polynucleotide replication. Journal of Biological Chemistry 249:4086–4093
    [Google Scholar]
  2. Birrer M. J., Udem S., Nathenson S., Bloom B. R. 1981; Antigenic variants of measles virus. Nature; London: 29367–69
    [Google Scholar]
  3. Blondel B., Crainic R., Fichot O., Dufraisse G., Candrea A., Diamond D., Girard M., Horaud F. 1986; Mutations conferring resistance to neutralization with monoclonal antibodies in type 1 poliovirus can be located outside or inside the antibody-binding site. Journal of Virology 57:81–90
    [Google Scholar]
  4. Bos T. J., Nayak D. P. 1986; Identification of defects in the neuraminidase gene of four temperature-sensitive mutants of A/WSN/33 influenza virus. Virology 154:85–96
    [Google Scholar]
  5. Both G. W., Sleigh M. J., Cox N. J., Kendal A. P. 1983; Antigenic drift in influenza virus H3 hemagglutinin from 1968 to 1980: multiple evolutionary pathways and sequential amino acid changes at key antigenic sites. Journal of Virology 48:52–60
    [Google Scholar]
  6. Brand C., Palese P. 1980; Sequential passage of influenza virus in embryonated eggs or tissue culture: emergence of mutants. Virology 107:424–433
    [Google Scholar]
  7. Buonagurio D. A., Nakada S., Desselberger U., Krystal M., Palese P. 1985; Noncumulative sequence changes in the hemagglutinin genes of influenza C virus isolates. Virology 146:221–232
    [Google Scholar]
  8. Buonagurio D. A., Nakada S., Fitch W. M., Palese P. 1986a; Epidemiology of influenza C virus in man: multiple evolutionary lineages and low rate of change. Virology 153:12–21
    [Google Scholar]
  9. Buonagurio D. A., Nakada S., Parvin J. D., Krystal M., Palese P., Fitch W. M. 1986b; Evolution of human influenza A viruses over 50 years: rapid uniform rate of change in NS gene. Science 232:980–982
    [Google Scholar]
  10. Campione-Piccardo J., Rawlins W. E., Bacchetti S. 1979; Selective assay for herpes simplex viruses expressing thymidine kinase. Journal of Virology 31:281–287
    [Google Scholar]
  11. Caton A. J., Brownlee G. G., Yewdell J. W., Gerhard W. 1982; The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (HI subtype). Cell 31:417–427
    [Google Scholar]
  12. Coelingh K. L., Winter C., Murphy B. R. 1985; Antigenic variation in the hemagglutinin-neuraminidase protein of human parainfluenza type 3 virus. Virology 143:569–582
    [Google Scholar]
  13. Coelingh K. L., Winter C. C., Murphy B. R., Rice J. M., Kemball P. C., Olmsted R. A., Collins P. L. 1986; Conserved epitopes on the hemagglutinin-neuraminidase proteins of human and bovine parainfluenza virus type 3 viruses: nucleotide sequence analysis of variants selected with monoclonal antibodies. Journal of Virology 60:90–96
    [Google Scholar]
  14. Coffin J. M. 1986; Genetic variation in AIDS viruses. Cell 46:1–4
    [Google Scholar]
  15. Coffin J. M., Tsichlis P. N., Barker C. s., Voynow S., Robinson H. L. 1980; Variation in avian retrovirus genomes. Annals of the New York Academy of Sciences 354:410–425
    [Google Scholar]
  16. Coulon P., Rollin P. E., Flamand A. 1983; Molecular basis of rabies virus virulence. II. Identification of a site on the CVS glycoprotein associated with virulence. Journal of General Virology 64:693–696
    [Google Scholar]
  17. Derse D., Cheng Y-C. 1981; Herpes simplex virus type IDNA polymerase.Kinetic properties of the associated 3′-5′ exonuclease activity and its role in araAMP incorporation. Journal of Biological Chemistry 256:8525–8530
    [Google Scholar]
  18. Diamond D. C., Jameson B. A., Bonin J., Kohara M., Abe S., Itoh H., Komatsu T., Arita M., Kuge S., Nomoto A., Osterhaus A. D. M. E., Crainic R., Wimmer E. 1985; Antigenic variation and resistance to neutralization in poliovirus type 1. Science 229:1090–1093
    [Google Scholar]
  19. 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]
  20. Domingo E., Martinez-Salas E., Sobrino F., Carlos De La Torre J., Portela A., Ortin J., Lopez-Galindez C., Perez-Brena P., Villanueva N., Najera R., Van De Pol S., Steinhauer D., De Polo N., Holland 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. 1969; Comparative rates of spontaneous mutation. Nature; London: 2211132
    [Google Scholar]
  22. Durbin R. K., Stollar V. 1986; Sequence analysis of the E2 gene of a hyperglycosylated, host restricted mutant of Sindbis virus and estimation of mutation rate from frequency of revertants. Virology 154:135–143
    [Google Scholar]
  23. Dyall-Smith M. L., Lazdins I., Tregear G. W., Holmes I. H. 1986; Location of the major antigenic sites involved in rotavirus serotype-specific neutralization. Proceedings of the National Academy of Sciences, U.S.A 83:3465–3468
    [Google Scholar]
  24. Emini E. A., Kao S., Lewis A. J., Crainic R., Wimmer E. 1983; Functional basis of poliovirus neutralization determined with monospecific neutralizing antibodies. Journal of Virology 46:466–474
    [Google Scholar]
  25. Evans D. M. A., Minor P. D., Schild G. C., Almond J. W. 1983; Critical role of an eight amino acid sequence of VP1 in neutralization of poliovirus type 3. Nature; London: 304459–462
    [Google Scholar]
  26. Fields S., Winter G. 1981; Nucleotide sequence heterogeneity and sequence rearrangements in influenza virus cDNA. Gene 15:207–214
    [Google Scholar]
  27. Gerhard W., Yewdell J., Frankel M. E., Webster R. 1981; Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature; London: 290713–717
    [Google Scholar]
  28. Hahn B. H., Shaw G. M., Taylor M. E., Redfield R. R., Markham P. D., Salahuddin S. Z., Wong-Staal F., Gallo R. C., Parks E. S., Parks W. P. 1986; Genetic variation in HTLV-III/LAV over time in patients with AIDS or at risk for AIDS. Science 232:1548–1553
    [Google Scholar]
  29. Hall J. D., Coen D. M., Fisher B. L., Weisslitz M., Randall S., Almy R. E., Gelep P. T., Schaffer P. A. 1984; Generation of genetic diversity in herpex simplex virus: an antimutator phenotype maps to the DNA polymerase locus. Virology 132:26–37
    [Google Scholar]
  30. Hayashida H., Toh H., Kikuno R., Miyata T. 1985; Evolution of influenza virus genes. Molecular Biology and Evolution 2:289–303
    [Google Scholar]
  31. Holland J., Spindler K., Horodyski F., Grabau E., Nichol S., Van De Pol S. 1982; Rapid evolution of RNA genomes. Science 215:1577–1585
    [Google Scholar]
  32. Holland T. C., Marlin S. D., Levine M., Glorioso J. 1983; Antigenic variants of herpes simplex virus selected with glycoprotein-specific monoclonal antibodies. Journal of Virology 45:672–682
    [Google Scholar]
  33. Holland T. C., Homa F. L., Marlin S. D., Levine M., Glorioso J. 1984; Herpes simplex virus type 1 glycoprotein C-negative mutants exhibit multiple phenotypes, including secretion of truncated glycoproteins. Journal of Virology 52:566–574
    [Google Scholar]
  34. Ishihama A., Mizumoto K., Kawakami K., Kato A., Honda A. 1986; Proofreading function associated with the RNA-dependent RNA polymerase from influenza virus. Journal of Biological Chemistry 261:10417–10421
    [Google Scholar]
  35. Jimenez G., Correa I., Melgosa M. p., Bullido M. J., Enjvanes L. 1986; Critical epitopes in transmissible gastroenteritis virus neutralization. Journal of Virology 60:131–139
    [Google Scholar]
  36. Joklik W. K. 1985; Recent progress in reovirus research. Annual Review of Genetics 19:537–575
    [Google Scholar]
  37. Kew O. M., Nottay B. K., Hatch M. H., Nakano J. H., Obijeski J. F. 1981; Multiple genetic changes can occur in the oral poliovaccines upon replication in humans. Journal of General Virology 56:337–347
    [Google Scholar]
  38. Kousoulas K. G., Pellett P. E., Pereira L., Roizman B. 1984; Mutations affecting conformation or sequence of neutralizing epitopes identified by reactivity of viable plaques segregate from syn and ts domains of HSV-1 (F) gB gene. Virology 135:379–394
    [Google Scholar]
  39. Krystal M., Young J. F., Palese P., Wilson I. A., Skehel J. J., Wiley D. C. 1983; Sequential mutations in hemagglutinins of influenza B virus isolates: definition of antigenic domains. Proceedings of the National Academy of Sciences, U.S.A 80:4527–4531
    [Google Scholar]
  40. Lazdins I., Sonza S., Dyall-Smith M. L., Coulson B. S., Holmes I. H. 1985; Demonstration of an immunodominant neutralization site by analysis of antigenic variants of SA11 rotavirus. Journal of Virology 56:317–319
    [Google Scholar]
  41. Lefrancois L., Lyles D. S. 1983; Antigenic determinants of vesicular stomatitis virus: analysis with antigenic variants. Journal of Immunology 130:394–398
    [Google Scholar]
  42. Lentz M. R., Air G. M., Laver W. G., Webster R. G. 1984; Sequence of the neuraminidase gene of influenza virus A/Tokyo/3/67 and previously uncharacterised monoclonal variants. Virology 135:257–265
    [Google Scholar]
  43. Li W. H., Tanimura M. 1987; The molecular clock runs more slowly in man than in apes and monkeys. Nature; London: 32693–96
    [Google Scholar]
  44. Li W. H., Gojobori T., Nei M. 1981; Pseudogenes as a paradigm of neutral evolution. Nature; London: 292237–239
    [Google Scholar]
  45. Loeb L. A., Kunkel T. A. 1982; Fidelity of DNA synthesis. Annual Review of Biochemistry 51:429–457
    [Google Scholar]
  46. Lubeck M. D., Schulman J. L., Palese P. 1980; Antigenic variants of influenza viruses: marked differences in the frequencies of variants selected with different monoclonal antibodies. Virology 102:458–462
    [Google Scholar]
  47. Marlin S. D., Holland T. C., Levine M., Glorioso J. C. 1985; Epitopes of herpes simplex virus type 1 glycoprotein gC are clustered in two distinct antigenic sites. Journal of Virology 53:128–136
    [Google Scholar]
  48. Marlin S. D., Highlander S. L., Holland T. C., Levine M., Glorioso J. C. 1986; Antigenic variation (mar mutations) in herpes simplex virus glycoprotein B can induce temperature-dependent alterations in gB processing and virus production. Journal of Virology 59:142–153
    [Google Scholar]
  49. Martinez C., Del Rio L., Portela A., Domingo E., Ortin J. 1983; Evolution of the influenza virus neuraminidase gene during drift of the N2 subtype. Virology 130:539–545
    [Google Scholar]
  50. Minor P. D., Schild G. C., Bootman J., Evans D. M. A., Ferguson M., Reeve P., Spitz M., Stanway G., Cann A. J., Hauptmann R., Clarke C. D., Mountford R. C., Almond J. W. 1983; Location and primary structure of a major antigenic site for poliovirus neutralization. Nature; London: 301674–679
    [Google Scholar]
  51. Morita K., Vanderoef R., Lenard J. 1987; Phenotypic revertants of temperature-sensitive M protein mutants of vesicular stomatitis virus: sequence analysis and functional characterization. Journal of Virology 61:256–263
    [Google Scholar]
  52. Mukai T., Cockerham C. C. 1977; Spontaneous mutation rates at enzyme loci in Drosophila melanogaster. Proceedings of the National Academy of Sciences, U.S.A 74:2514–2517
    [Google Scholar]
  53. Nakajima S., Kendal A. P. 1981; Antigenic drift in influenza A/USSR/90/77 (H1N1) variants selected in vitro with monoclonal antibodies. Virology 113:656–662
    [Google Scholar]
  54. Nottay B. K., Kew O. M., Hatch M. H., Heyward J. T., Obijeski J. F. 1981; Molecular variation of type 1 vaccine-related and wild poliovirus during replication in humans. Virology 108:405–423
    [Google Scholar]
  55. Ortin J., Martinez C., Del Rio L., Davila M., Lopez-Galindez C., Villanueva N., Domingo E. 1983; Evolution of the nucleotide sequence of influenza virus RNA segment 7 during drift of the H3N2 subtype. Gene 23:233–239
    [Google Scholar]
  56. Palese P., Young J. F. 1982; Variation of influenza A, B and C viruses. Science 215:1468–1474
    [Google Scholar]
  57. Parrish C. R., Carmichael L. E. 1983; Antigenic structure and variation of canine parvovirus type-2, feline panleukopenia virus and mink enteritis virus. Virology 129:401–414
    [Google Scholar]
  58. Parvin J. D., Moscona A., Pan W. T., Leider J. M., Palese P. 1986; Measurement of the mutation rates of animal viruses: influenza A virus and poliovirus type 1. Journal of Virology 59:377–383
    [Google Scholar]
  59. Pellett P. E., Kousoulas K. G., Pereira L., Roizman B. 1985; Anatomy of the herpes simplex virus 1 strain F glycoprotein B gene: primary sequence and predicted protein structure of the wild type and of monoclonal antibody-resistant mutants. Journal of Virology 53:243–253
    [Google Scholar]
  60. Pincus S. E., Diamond D. C., Emini E. A., Wimmer E. 1986; Guanidine-selected mutants of poliovirus: mapping of point mutations to polypeptide 2C. Journal of Virology 57:638–646
    [Google Scholar]
  61. Portner A., Webster R. G., Bean W. H. 1980; Similar frequencies of antigenic variation in Sendai, vesicular stomatitis and influenza A viruses. Virology 104:235–238
    [Google Scholar]
  62. Prabhakar B. S., Haspel M. U., Mcclintock P. R., Notkins A. L. 1982; High frequency of antigenic variants among naturally occurring human coxsackie B4 virus isolates identified by monoclonal antibodies. Nature; London: 300374–376
    [Google Scholar]
  63. Pringle C. R., Devine V., Wilkie M., Preston C. M., Dolan A., Mcgeoch D. J. 1981; Enhanced mutability associated with a temperature-sensitive mutant of vesicular stomatitis virus. Journal of Virology 39:377–389
    [Google Scholar]
  64. Rawlins D. R., Collis P., Muzyczka N. 1983; Characterization of am404, an amber mutation in the simian virus 40 T antigen gene. Journal of Virology 47:202–216
    [Google Scholar]
  65. Raymond F. L., Caton A. J., Cox N. J., Kendal A. P., Brownlee G. G. 1983; Antigenicity and evolution amongst recent influenza viruses of H1N1 subtype. Nucleic Acids Research 11:7191–7203
    [Google Scholar]
  66. Reanney D. 1984; The molecular evolution of viruses. In The Microbe 1984, Part I: Viruses pp. 175–196 Mahy B. W. J., Pattison J. R. Edited by Cambridge: Cambridge University Press;
    [Google Scholar]
  67. Russell P. H. 1984; Newcastle disease virus: the effect of monoclonal antibody in the overlay on virus penetration and the immunoselection of variants. Journal of General Virology 65:795–798
    [Google Scholar]
  68. Saitou N., Nei M. 1986; Polymorphism and evolution of influenza A virus genes. Molecular Biology and Evolution 3:57–74
    [Google Scholar]
  69. Samson A. C. R., Russell P. H., Hallam S. E. 1985; Isolation and characterization of monoclonal antibody-resistant mutants of Newcastle disease virus. Journal of General Virology 66:357–361
    [Google Scholar]
  70. Scholtissek C., Spring S. B. 1981; Suppressor recombinants and suppressor mutants. In Genetic Variation among Influenza Viruses pp. 399–413 Nayak D. P. Edited by New York: Academic Press;
    [Google Scholar]
  71. Schubert M., Harrison G. G., Meier E. 1984; Primary structure of the vesicular stomatitis virus polymerase (L) gene: evidence for a high frequency of mutations. Journal of Virology 51:505–514
    [Google Scholar]
  72. 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]
  73. Sherry B., Rueckert R. 1985; Evidence for at least two dominant neutralization antigens on human rhinovirus 14. Journal of Virology 53:137–143
    [Google Scholar]
  74. 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]
  75. 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]
  76. 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]
  77. Soeda E., Maruyama T. 1982; Molecular evolution in papova viruses and in bacteriophages. Advances in Biophysics 15:1–17
    [Google Scholar]
  78. 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
    [Google Scholar]
  79. Steinhauer D. A., Holland I. J. 1986; Direct method for quantitation of extreme polymerase error frequencies at selected base sites in viral RNA. Journal of Virology 57:219–228
    [Google Scholar]
  80. Sugiura A., Tobita K., Kilbourne E. D. 1972; Isolation and preliminary characterization of temperature-sensitive mutants of influenza virus. Journal of Virology 10:639–647
    [Google Scholar]
  81. Takeda N., Miyamura K., Ogino T., Natori K., Yamazaki S., Sakurai N., Nakazono N., Ishii K., Kono R. 1984; Evolution of enterovirus type 70: oligonucleotide mapping analysis of RNA genome. Virology 134:375–388
    [Google Scholar]
  82. Verhoeyen M., Fang R., Min Jou W., Devos R., Huglebroeck D., Saman E., Fiers W. 1980; Antigenic drift between the haemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75. Nature; London: 286771–776
    [Google Scholar]
  83. Verhoeyen M., Van Rompuy L., Min Jou W., Huylebroeck D., Fiers W. 1983; Complete nucleotide sequence of the influenza B/Singapore/222/79 virus haemagglutinin gene and comparison with the B/Lee/40 hemagglutinin. Nucleic Acids Research 11:4703–4712
    [Google Scholar]
  84. Vogel F., Motulsky A. G. 1982 Human Genetics pp 311–313 Berlin: Springer-Verlag;
    [Google Scholar]
  85. Webster R. G., Laver W. G. 1980; Determination of the number of non-overlapping antigenic areas on Hong Kong (H3N2) influenza virus hemagglutinin with monoclonal antibodies and the selection of variants with potential epidemiological significance. Virology 104:139–148
    [Google Scholar]
  86. Webster R. G., Hinshaw V. S., Laver W. G. 1982; Selection and analysis of antigenic variants of the neuraminidase of N2 influenza viruses with monoclonal antibodies. Virology 117:93–104
    [Google Scholar]
  87. Weddell G. N., Yansura D. G., Dowbenko D. J., Hoatlin M. E., Grubman M. J., Moore D. M., Kleid D. G. 1985; Sequence variation in the gene for the immunogenic capsid protein VP1 of foot-and-mouth disease virus type A. Proceedings of the National Academy of Sciences, U.S.A 82:2618–2622
    [Google Scholar]
  88. Wiktor T. J., Koprowski H. 1980; Antigenic variants of rabies virus. Journal of Experimental Medicine 152:99–112
    [Google Scholar]
  89. Wilson J. B., Hayday A., Courtneidge S., Fried M. 1986; A frameshift at a mutational hotspot in the polyoma virus early region generates two new proteins that define T-antigen functional domains. Cell 44:477–487
    [Google Scholar]
  90. Yewdell J., Gerhard W. 1982; Delineation of four antigenic sites on a paramyxovirus glycoprotein via which monoclonal antibodies mediate distinct antiviral activities. Journal of Immunology 128:2670–2675
    [Google Scholar]
  91. Yewdell J. W., Webster R. G., Gerhard W. 1979; Antigenic variation in three distinct determinants of an influenza type Ahaemagglutinin molecule. Nature; London: 279246–248
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-68-11-2729
Loading
/content/journal/jgv/10.1099/0022-1317-68-11-2729
Loading

Data & Media loading...

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