1887

Abstract

This study analysed phylogenetic evidence of recombination in sequences of hepatitis A virus (HAV) available in international databases. Isolation of distinct recombinant HAV strains has been reported previously; however, the prevalence of natural recombination and its role in HAV genetics remains obscure. Analysis of full genome sequences revealed evidence of common intratypic recombination among the most prevalent subtypes, IA and IIIA. Many of the available complete sequences of these genotypes carried phylogenetic signs of recombination in all genomic regions without obvious hotspots. In addition, and in line with previous reports, recombination between subtypes IA and IB was detected. A dataset of 104 published HAV sequences for the VP1–2A and 3CD genomic regions was also analysed. Multiple instances of phylogenetic incompatibility were found among subtypes IA and IIIA. Three cases of recombination disrupted the phylogenetic grouping of subtype IA HAV strains isolated in Japan within less than 4 years, indicating common intratypic recombination in HAV. There were no signs of recombination between different HAV genotypes, despite the fact that co-circulation of genotypes IA and IIIA has commonly been reported in different parts of the world and many sequences in the sampling in this study originated from the same geographical region. These results indicate that there is reproductive isolation between genotypes of HAV, as exists between enterovirus species, and suggest that common intratypic recombination constrains the diversity within a genotype and maintains HAV genotypes as global gene pools.

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2011-04-01
2019-11-21
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References

  1. Benschop, K. S., de Vries, M., Minnaar, R. P., Stanway, G., van der Hoek, L., Wolthers, K. C. & Simmonds, P. ( 2010; ). Comprehensive full-length sequence analyses of human parechoviruses: diversity and recombination. J Gen Virol 91, 145–154. [CrossRef]
    [Google Scholar]
  2. Boni, M. F., de Jong, M. D., van Doorn, H. R. & Holmes, E. C. ( 2010; ). Guidelines for identifying homologous recombination events in influenza A virus. PLoS ONE 5, e10434. [CrossRef]
    [Google Scholar]
  3. Brown, B., Oberste, M. S., Maher, K. & Pallansch, M. A. ( 2003; ). Complete genomic sequencing shows that polioviruses and members of human enterovirus species C are closely related in the noncapsid coding region. J Virol 77, 8973–8984. [CrossRef]
    [Google Scholar]
  4. Ching, K. Z., Nakano, T., Chapman, L. E., Demby, A. & Robertson, B. H. ( 2002; ). Genetic characterization of wild-type genotype VII hepatitis A virus. J Gen Virol 83, 53–60.
    [Google Scholar]
  5. Chironna, M., Grottola, A., Lanave, C., Villa, E., Barbuti, S. & Quarto, M. ( 2003; ). Genetic analysis of HAV strains recovered from patients with acute hepatitis from Southern Italy. J Med Virol 70, 343–349. [CrossRef]
    [Google Scholar]
  6. Chitambar, S., Joshi, M., Lole, K., Walimbe, A. & Vaidya, S. ( 2007; ). Cocirculation of and coinfections with hepatitis A virus subgenotypes IIIA and IB in patients from Pune, western India. Hepatol Res 37, 85–93. [CrossRef]
    [Google Scholar]
  7. Cohen, J. I., Ticehurst, J. R., Purcell, R. H., Buckler-White, A. & Baroudy, B. M. ( 1987; ). Complete nucleotide sequence of wild-type hepatitis A virus: comparison with different strains of hepatitis A virus and other picornaviruses. J Virol 61, 50–59.
    [Google Scholar]
  8. Costa-Mattioli, M., Di Napoli, A., Ferré, V., Billaudel, S., Perez-Bercoff, R. & Cristina, J. ( 2003a; ). Genetic variability of hepatitis A virus. J Gen Virol 84, 3191–3201. [CrossRef]
    [Google Scholar]
  9. Costa-Mattioli, M., Ferré, V., Casane, D., Perez-Bercoff, R., Coste-Burel, M., Imbert-Marcille, B. M., Andre, E. C., Bressollette-Bodin, C., Billaudel, S. & Cristina, J. ( 2003b; ). Evidence of recombination in natural populations of hepatitis A virus. Virology 311, 51–59. [CrossRef]
    [Google Scholar]
  10. Drexler, J. F., Baumgarte, S., de Souza Luna, L. K., Stöcker, A., Almeida, P. S., Ribeiro, T. C., Petersen, N., Herzog, P., Pedroso, C. & other authors ( 2010; ). Genomic features and evolutionary constraints in Saffold-like cardioviruses. J Gen Virol 91, 1418–1427. [CrossRef]
    [Google Scholar]
  11. Drummond, A. J. & Rambaut, A. ( 2007; ). beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7, 214. [CrossRef]
    [Google Scholar]
  12. Edgar, R. C. ( 2004; ). muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797. [CrossRef]
    [Google Scholar]
  13. Endo, K., Inoue, J., Takahashi, M., Mitsui, T., Masuko, K., Akahane, Y. & Okamoto, H. ( 2007a; ). Analysis of the full-length genome of a subgenotype IIIB hepatitis A virus isolate: primers for broadly reactive PCR and genotypic analysis. J Med Virol 79, 8–17. [CrossRef]
    [Google Scholar]
  14. Endo, K., Takahashi, M., Masuko, K., Inoue, K., Akahane, Y. & Okamoto, H. ( 2007b; ). Full-length sequences of subgenotype IIIA and IIIB hepatitis A virus isolates: characterization of genotype III HAV genomes. Virus Res 126, 116–127. [CrossRef]
    [Google Scholar]
  15. Felsenstein, J. ( 1989; ). phylip – phylogeny inference package (version 3.2). Cladistics 5, 164–166.
    [Google Scholar]
  16. Fujiwara, K., Yokosuka, O., Fukai, K., Imazeki, F., Saisho, H. & Omata, M. ( 2001; ). Analysis of full-length hepatitis A virus genome in sera from patients with fulminant and self-limited acute type A hepatitis. J Hepatol 35, 112–119. [CrossRef]
    [Google Scholar]
  17. García-Aguirre, L. & Cristina, J. ( 2008; ). Analysis of the full-length genome of hepatitis A virus isolated in South America: heterogeneity and evolutionary constraints. Arch Virol 153, 1473–1478. [CrossRef]
    [Google Scholar]
  18. Graff, J., Normann, A., Feinstone, S. M. & Flehmig, B. ( 1994; ). Nucleotide sequence of wild-type hepatitis A virus GBM in comparison with two cell culture-adapted variants. J Virol 68, 548–554.
    [Google Scholar]
  19. Hall, T. A. ( 1999; ). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 95–98.
    [Google Scholar]
  20. Heath, L., van der Walt, E., Varsani, A. & Martin, D. P. ( 2006; ). Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J Virol 80, 11827–11832. [CrossRef]
    [Google Scholar]
  21. Hollinger, F. B. & Emerson, S. U. ( 2007; ). Hepatitis A Virus. In Fields Virology, 5th edn, pp. 911–940. Edited by Knipe, D. M. & Howley, P. M.. Philadelphia. : Lippincott Williams & Wilkins.
    [Google Scholar]
  22. Hu, Y., Hu, N. & Liu, G. ( 2002; ). Complete genomes of two human hepatitis A virus isolates from China: analysis and comparison with other isolates. Acta Virol 46, 153–157.
    [Google Scholar]
  23. Huang, S.-C., Hsu, Y.-W., Wang, H.-C., Huang, S.-W., Kiang, D., Tsai, H.-P., Wang, S.-M., Liu, C.-C., Lin, K.-H. & Su, I.-J. ( 2008; ). Appearance of intratypic recombination of enterovirus 71 in Taiwan from 2002 to 2005. Virus Res 131, 250–259. [CrossRef]
    [Google Scholar]
  24. Jansen, R. W., Siegl, G. & Lemon, S. M. ( 1990; ). Molecular epidemiology of human hepatitis A virus defined by an antigen-capture polymerase chain reaction method. Proc Natl Acad Sci U S A 87, 2867–2871. [CrossRef]
    [Google Scholar]
  25. Joshi, M. S., Walimbe, A. M. & Chitambar, S. D. ( 2008; ). Evaluation of genomic regions of hepatitis A virus for phylogenetic analysis: suitability of the 2C region for genotyping. J Virol Methods 153, 36–42. [CrossRef]
    [Google Scholar]
  26. Kulkarni, M. A., Walimbe, A. M., Cherian, S. & Arankalle, V. A. ( 2009; ). Full length genomes of genotype IIIA Hepatitis A virus strains (1995–2008) from India and estimates of the evolutionary rates and ages. Infect Genet Evol 9, 1287–1294. [CrossRef]
    [Google Scholar]
  27. Leitch, E. C., Harvala, H., Robertson, I., Ubillos, I., Templeton, K. & Simmonds, P. ( 2009; ). Direct identification of human enterovirus serotypes in cerebrospinal fluid by amplification and sequencing of the VP1 region. J Clin Virol 44, 119–124. [CrossRef]
    [Google Scholar]
  28. Lemon, S. M., Murphy, P. C., Shields, P. A., Ping, L.-H., Feinstone, S. M., Cromeans, T. & Jansen, R. W. ( 1991; ). Antigenic and genetic variation in cytopathic hepatitis A virus variants arising during persistent infection: evidence for genetic recombination. J Virol 65, 2056–2065.
    [Google Scholar]
  29. Lenfant, C. ( 1994; ). From the National Institutes of Health. JAMA 272, 842. [CrossRef]
    [Google Scholar]
  30. Liu, W., Zhai, J., Liu, J. & Xie, Y. ( 2010a; ). Identification of recombination between subgenotypes IA and IB of hepatitis A virus. Virus Genes 40, 222–224. [CrossRef]
    [Google Scholar]
  31. Liu, Y., Wang, C., Mueller, S., Paul, A. V., Wimmer, E. & Jiang, P. ( 2010b; ). Direct interaction between two viral proteins, the nonstructural protein 2CATPase and the capsid protein VP3, is required for enterovirus morphogenesis. PLoS Pathog 6, e1001066. [CrossRef]
    [Google Scholar]
  32. Lole, K. S., Bollinger, R. C., Paranjape, R. S., Gadkari, D., Kulkarni, S. S., Novak, N. G., Ingersoll, R., Sheppard, H. W. & Ray, S. C. ( 1999; ). Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73, 152–160.
    [Google Scholar]
  33. Lu, L., Ching, K. Z., de Paula, V. S., Nakano, T., Siegl, G., Weitz, M. & Robertson, B. H. ( 2004; ). Characterization of the complete genomic sequence of genotype II hepatitis A virus (CF53/Berne isolate). J Gen Virol 85, 2943–2952. [CrossRef]
    [Google Scholar]
  34. Lukashev, A. N. ( 2010; ). Recombination among picornaviruses. Rev Med Virol 20, 327–337. [CrossRef]
    [Google Scholar]
  35. Lukashev, A. N., Lashkevich, V. A., Ivanova, O. E., Koroleva, G. A., Hinkkanen, A. E. & Ilonen, J. ( 2003; ). Recombination in circulating enteroviruses. J Virol 77, 10423–10431. [CrossRef]
    [Google Scholar]
  36. Lukashev, A. N., Lashkevich, V. A., Ivanova, O. E., Koroleva, G. A., Hinkkanen, A. E. & Ilonen, J. ( 2005; ). Recombination in circulating Human enterovirus B: independent evolution of structural and non-structural genome regions. J Gen Virol 86, 3281–3290. [CrossRef]
    [Google Scholar]
  37. Madaniuk, A. G., Tiunnikov, G. I., Konakova, V. E., Bondarenko, E. P., Nemtsov, Iu. V., Karpovich, L. G., Kalashnikova, T. V., Mamaeva, N. V., Sosnovtsev, S. V. & Chizhikov, V. E. ( 1993; ). The isolation and study of the characteristics of a cytopathic strain of the hepatitis A virus. Vopr Virusol 38, 101–105 (in Russian ).
    [Google Scholar]
  38. Moratorio, G., Costa-Mattioli, M., Piovani, R., Romero, H., Musto, H. & Cristina, J. ( 2007; ). Bayesian coalescent inference of hepatitis A virus populations: evolutionary rates and patterns. J Gen Virol 88, 3039–3042. [CrossRef]
    [Google Scholar]
  39. Najarian, R., Caput, D., Gee, W., Potter, S. J., Renard, A., Merryweather, J., Van Nest, G. & Dina, D. ( 1985; ). Primary structure and gene organization of human hepatitis A virus. Proc Natl Acad Sci U S A 82, 2627–2631. [CrossRef]
    [Google Scholar]
  40. Oberste, M. S., Peñaranda, S. & Pallansch, M. A. ( 2004; ). RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J Virol 78, 2948–2955. [CrossRef]
    [Google Scholar]
  41. Paul, A. V., Tada, H., von der Helm, K., Wissel, T., Kiehn, R., Wimmer, E. & Deinhardt, F. ( 1987; ). The entire nucleotide sequence of the genome of human hepatitis A virus (isolate MBB). Virus Res 8, 153–171. [CrossRef]
    [Google Scholar]
  42. Pina, S., Buti, M., Jardí, R., Clemente-Casares, P., Jofre, J. & Girones, R. ( 2001; ). Genetic analysis of hepatitis A virus strains recovered from the environment and from patients with acute hepatitis. J Gen Virol 82, 2955–2963.
    [Google Scholar]
  43. Pintó, R. M., Aragonès, L., Costafreda, M. I., Ribes, E. & Bosch, A. ( 2007; ). Codon usage and replicative strategies of hepatitis A virus. Virus Res 127, 158–163. [CrossRef]
    [Google Scholar]
  44. Robertson, B. H., Khanna, B., Nainan, O. V. & Margolis, H. S. ( 1991; ). Epidemiologic patterns of wild-type hepatitis A virus determined by genetic variation. J Infect Dis 163, 286–292.[CrossRef]
    [Google Scholar]
  45. Robertson, B. H., Jansen, R. W., Khanna, B., Totsuka, A., Nainan, O. V., Siegl, G., Widell, A., Margolis, H. S., Isomura, S. & other authors ( 1992; ). Genetic relatedness of hepatitis A virus strains recovered from different geographical regions. J Gen Virol 73, 1365–1377. [CrossRef]
    [Google Scholar]
  46. Shapiro, B., Rambaut, A. & Drummond, A. J. ( 2006; ). Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23, 7–9.
    [Google Scholar]
  47. Simmonds, P. & Smith, D. B. ( 1999; ). Structural constraints on RNA virus evolution. J Virol 73, 5787–5794.
    [Google Scholar]
  48. Simmonds, P. & Welch, J. ( 2006; ). Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80, 483–493. [CrossRef]
    [Google Scholar]
  49. Stanway, G., Brown, F., Christian, P., Hovi, T., Hyypiä, T., King, A. M. Q., Knowles, N. J., Lemon, S. M., Minor, P. D. & other authors ( 2005; ). Family Picornaviridae. In Virus Taxonomy Eighth Report of the International Committee on Taxonomy of Viruses, pp. 757–778. Edited by Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U. & Ball, L. A.. London. : Elsevier/Academic Press.
    [Google Scholar]
  50. Stene-Johansen, K., Skaug, K. & Blystad, H. ( 1999; ). Surveillance of hepatitis A by molecular epidemiologic studies. Tidsskr Nor Laegeforen 119, 3725–3729 (in Norwegian ).
    [Google Scholar]
  51. Tallo, T., Norder, H., Tefanova, V., Ott, K., Ustina, V., Prukk, T., Solomonova, O., Schmidt, J., Zilmer, K. & other authors ( 2003; ). Sequential changes in hepatitis A virus genotype distribution in Estonia during 1994 to 2001. J Med Virol 70, 187–193. [CrossRef]
    [Google Scholar]
  52. Tamura, K., Dudley, J., Nei, M. & Kumar, S. ( 2007; ). mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599. [CrossRef]
    [Google Scholar]
  53. Tsarev, S. A., Emerson, S. U., Balayan, M. S., Ticehurst, J. & Purcell, R. H. ( 1991; ). Simian hepatitis A virus (HAV) strain AGM-27: comparison of genome structure and growth in cell culture with other HAV strains. J Gen Virol 72, 1677–1683. [CrossRef]
    [Google Scholar]
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