1887

Abstract

RNA recombination is a significant driving force in viral evolution. Increased awareness of recombination within the genus of the family has led to a rise in the identification of norovirus (NoV) recombinants and they are now reported at high frequency. Currently, there is no classification system for recombinant NoVs and a widely accepted recombinant genotyping system is still needed. Consequently, there is duplication in reporting of novel recombinants. This has led to difficulties in defining the number and types of recombinants in circulation. In this study, 120 NoV nucleotide sequences were compiled from the current GenBank database and published literature. NoV recombinants and their recombination breakpoints were identified using three methods: phylogenetic analysis, SimPlot analysis and the maximum method. A total of 20 NoV recombinant types were identified in circulation worldwide. The recombination point is the ORF1/2 overlap in all isolates except one, which demonstrated a double recombination event within the polymerase region.

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2007-12-01
2024-04-16
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References

  1. Ambert-Balay K., Bon F., Le Guyader F., Pothier P., Kohli E. 2005; Characterization of new recombinant noroviruses. J Clin Microbiol 43:5179–5186 [CrossRef]
    [Google Scholar]
  2. Armah G. E., Gallimore C. I., Binka F. N., Asmah R. H., Green J., Ugoji U., Anto F., Brown D. W., Gray J. J. 2006; Characterisation of norovirus strains in rural Ghanaian children with acute diarrhoea. J Med Virol 78:1480–1485 [CrossRef]
    [Google Scholar]
  3. Asanaka M., Atmar R. L., Ruvolo V., Crawford S. E., Neill F. H., Estes M. K. 2005; Replication and packaging of Norwalk virus RNA in cultured mammalian cells. Proc Natl Acad Sci U S A 102:10327–10332 [CrossRef]
    [Google Scholar]
  4. Atmar R. L., Estes M. K. 2006; The epidemiologic and clinical importance of norovirus infection. Gastroenterol Clin North Am 35:275–290 [CrossRef]
    [Google Scholar]
  5. Bon F., Ambert-Balay K., Giraudon H., Kaplon J., Le Guyader S., Pommepuy M., Gallay A., Vaillant V., de Valk H. other authors 2005; Molecular epidemiology of caliciviruses detected in sporadic and outbreak cases of gastroenteritis in France from December 1998 to February 2004. J Clin Microbiol 43:4659–4664 [CrossRef]
    [Google Scholar]
  6. Buesa J., Collado B., Lopez-Andujar P., Abu-Mallouh R., Rodriguez Diaz J., Garcia Diaz A., Prat J., Guix S., Llovet T. other authors 2002; Molecular epidemiology of caliciviruses causing outbreaks and sporadic cases of acute gastroenteritis in Spain. J Clin Microbiol 40:2854–2859 [CrossRef]
    [Google Scholar]
  7. Bull R. A., Hansman G. S., Clancy L. E., Tanaka M. M., Rawlinson W. D., White P. A. 2005; Norovirus recombination in ORF1/ORF2 overlap. Emerg Infect Dis 11:1079–1085 [CrossRef]
    [Google Scholar]
  8. Bull R. A., Tu E. T., McIver C. J., Rawlinson W. D., White P. A. 2006; Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. J Clin Microbiol 44:327–333 [CrossRef]
    [Google Scholar]
  9. Coyne K. P., Reed F. C., Porter C. J., Dawson S., Gaskell R. M., Radford A. D. 2006; Recombination of Feline calicivirus within an endemically infected cat colony. J Gen Virol 87:921–926 [CrossRef]
    [Google Scholar]
  10. de Jong J. C., Claas E. C., Osterhaus A. D., Webster R. G., Lim W. L. 1997; A pandemic warning?. Nature 389:554
    [Google Scholar]
  11. Etherington G. J., Dicks J., Roberts I. N. 2006; High throughput sequence analysis reveals hitherto unreported recombination in the genus Norovirus . Virology 345:88–95 [CrossRef]
    [Google Scholar]
  12. Fankhauser R. L., Monroe S. S., Noel J. S., Humphrey C. D., Bresee J. S., Parashar U. D., Ando T., Glass R. I. 2002; Epidemiologic and molecular trends of “Norwalk-like viruses” associated with outbreaks of gastroenteritis in the United States. J Infect Dis 186:1–7 [CrossRef]
    [Google Scholar]
  13. Gallimore C. I., Cubitt D., du Plessis N., Gray J. J. 2004a; Asymptomatic and symptomatic excretion of noroviruses during a hospital outbreak of gastroenteritis. J Clin Microbiol 42:2271–2274 [CrossRef]
    [Google Scholar]
  14. Gallimore C. I., Lewis D., Taylor C., Cant A., Gennery A., Gray J. J. 2004b; Chronic excretion of a norovirus in a child with cartilage hair hypoplasia (CHH). J Clin Virol 30:196–204 [CrossRef]
    [Google Scholar]
  15. Gallimore C. I., Cheesbrough J. S., Lamden K., Bingham C., Gray J. J. 2005; Multiple norovirus genotypes characterised from an oyster-associated outbreak of gastroenteritis. Int J Food Microbiol 103:323–330 [CrossRef]
    [Google Scholar]
  16. Glass P. J., White L. J., Ball J. M., Leparc-Goffart I., Hardy M. E., Estes M. K. 2000; Norwalk virus open reading frame 3 encodes a minor structural protein. J Virol 74:6581–6591 [CrossRef]
    [Google Scholar]
  17. Han M. G., Smiley J. R., Thomas C., Saif L. J. 2004; Genetic recombination between two genotypes of genogroup III bovine noroviruses (BoNVs) and capsid sequence diversity among BoNVs and Nebraska-like bovine enteric caliciviruses. J Clin Microbiol 42:5214–5224 [CrossRef]
    [Google Scholar]
  18. Hansman G. S., Doan L. T., Kguyen T. A., Okitsu S., Katayama K., Ogawa S., Natori K., Takeda N., Kato Y. & other authors (2004a). Detection of norovirus and sapovirus infection among children with gastroenteritis in Ho Chi Minh City. Vietnam. Arch Virol 149:1673–1688
    [Google Scholar]
  19. Hansman G. S., Katayama K., Maneekarn N., Peerakome S., Khamrin P., Tonusin S., Okitsu S., Nishio O., Takeda N., Ushijima H. 2004b; Genetic diversity of norovirus and sapovirus in hospitalized infants with sporadic cases of acute gastroenteritis in Chiang Mai, Thailand. J Clin Microbiol 42:1305–1307 [CrossRef]
    [Google Scholar]
  20. Hansman G. S., Takeda N., Oka T., Oseto M., Hedlund K. O., Katayama K. 2005; Intergenogroup recombination in sapoviruses. Emerg Infect Dis 11:1916–1920
    [Google Scholar]
  21. Hardy M. E. 2005; Norovirus protein structure and function. FEMS Microbiol Lett 253:1–8 [CrossRef]
    [Google Scholar]
  22. Hardy M. E., Kramer S. F., Treanor J. J., Estes M. K. 1997; Human calicivirus genogroup II capsid sequence diversity revealed by analyses of the prototype Snow Mountain agent. Arch Virol 142:1469–1479 [CrossRef]
    [Google Scholar]
  23. Iritani N., Seto Y., Kubo H., Murakami T., Haruki K., Ayata M., Ogura H. 2003; Prevalence of Norwalk-like virus infections in cases of viral gastroenteritis among children in Osaka City, Japan. J Clin Microbiol 41:1756–1759 [CrossRef]
    [Google Scholar]
  24. Jiang X., Espul C., Zhong W. M., Cuello H., Matson D. O. 1999; Characterization of a novel human calicivirus that may be a naturally occurring recombinant. Arch Virol 144:2377–2387 [CrossRef]
    [Google Scholar]
  25. Katayama K., Horikoshi-Shirato H., Takeda N. 2002a; Phylogenetic analysis of 14 strains of Norwalk-like viruses: identification of the region in the genome for genotyping. Nippon Rinsho 60:1165–1174 (in Japanese
    [Google Scholar]
  26. Katayama K., Shirato-Horikoshi H., Kojima S., Kageyama T., Oka T., Hoshino F., Fukushi S., Shinohara M., Uchida K. other authors 2002b; Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses. Virology 299:225–239 [CrossRef]
    [Google Scholar]
  27. Kim M. J., Kao C. 2001; Factors regulating template switch in vitro by viral RNA-dependent RNA polymerases: implications for RNA-RNA recombination. Proc Natl Acad Sci U S A 98:4972–4977 [CrossRef]
    [Google Scholar]
  28. Kumar S., Tamura K., Nei M. 2004; mega3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163 [CrossRef]
    [Google Scholar]
  29. Lai M. M. 1992; RNA recombination in animal and plant viruses. Microbiol Rev 56:61–79
    [Google Scholar]
  30. Lindell A. T., Grillner L., Svensson L., Wirgart B. Z. 2005; Molecular epidemiology of norovirus infections in Stockholm, Sweden, during the years 2000 to 2003: association of the GGIIb genetic cluster with infection in children. J Clin Microbiol 43:1086–1092 [CrossRef]
    [Google Scholar]
  31. 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]
  32. Martinez N., Espul C., Cuello H., Zhong W., Jiang X., Matson D. O., Berke T. 2002; Sequence diversity of human caliciviruses recovered from children with diarrhea in Mendoza. Argentina: 1995–1998 J Med Virol 67:289–298 [CrossRef]
    [Google Scholar]
  33. Maunula L., Von Bonsdorff C. H. 2005; Norovirus genotypes causing gastroenteritis outbreaks in Finland 1998–2002. J Clin Virol 34:186–194 [CrossRef]
    [Google Scholar]
  34. Maynard Smith J. 1992; Analyzing the mosaic structure of genes. J Mol Evol 34:126–129
    [Google Scholar]
  35. Muller H. J. 1964; The relation of recombination to mutational advance. Mutat Res 106:2–9
    [Google Scholar]
  36. Nicholas K. B., Nicholas H. B. Jr, Deerfield D. W., II. 1997; GeneDoc: analysis and visualization of genetic variation. EMBnet News 4:1–4 http://www.embnet.org/files/shared/EMBnetNews/embnet_news_4_2.pdf
    [Google Scholar]
  37. Nygard K., Torven M., Ancker C., Knauth S. B., Hedlund K. O., Giesecke J., Andersson Y., Svensson L. 2003; Emerging genotype (GGIIb) of norovirus in drinking water, Sweden. Emerg Infect Dis 9:1548–1552 [CrossRef]
    [Google Scholar]
  38. Oliver S. L., Brown D. W., Green J., Bridger J. C. 2004; A chimeric bovine enteric calicivirus: evidence for genomic recombination in genogroup III of the Norovirus genus of the Caliciviridae . Virology 326:231–239 [CrossRef]
    [Google Scholar]
  39. Oliver S. L., Batten C. A., Deng Y., Elschner M., Otto P., Charpilienne A., Clarke I. N., Bridger J. C., Lambden P. R. 2006; Genotype 1 and genotype 2 bovine noroviruses are antigenically distinct but share a cross-reactive epitope with human noroviruses. J Clin Microbiol 44:992–998 [CrossRef]
    [Google Scholar]
  40. Phan T. G., Kuroiwa T., Kaneshi K., Ueda Y., Nakaya S., Nishimura S., Yamamoto A., Sugita K., Nishimura T. other authors 2006a; Changing distribution of norovirus genotypes and genetic analysis of recombinant GIIb among infants and children with diarrhea in Japan. J Med Virol 78:971–978 [CrossRef]
    [Google Scholar]
  41. Phan T. G., Takanashi S., Kaneshi K., Ueda Y., Nakaya S., Nishimura S., Sugita K., Nishimura T., Yamamoto A. & other authors (2006b). Detection and genetic characterization of norovirus strains circulating among infants and children with acute gastroenteritis in Japan during 2004–2005. Clin Lab 52:519–525
    [Google Scholar]
  42. Phan T. G., Yagyu F., Kozlov V., Kozlov A., Okitsu S., Muller W. E., Ushijima H. 2006c; Viral gastroenteritis and genetic characterization of recombinant norovirus circulating in Eastern Russia. Clin Lab 52:247–253
    [Google Scholar]
  43. Phan T. G., Yan H., Li Y., Okitsu S., Muller W. E., Ushijima H. 2006d; Novel recombinant norovirus in China. Emerg Infect Dis 12:857–858 [CrossRef]
    [Google Scholar]
  44. Phan T. G., Kaneshi K., Ueda Y., Nakaya S., Nishimura S., Yamamoto A., Sugita K., Takanashi S., Okitsu S., Ushijima H. 2007; Genetic heterogeneity, evolution and recombination in noroviruses. J Med Virol 79:1388–1400 [CrossRef]
    [Google Scholar]
  45. Pletneva M. A., Sosnovtsev S. V., Green K. Y. 2001; The genome of Hawaii virus and its relationship with other members of the Caliciviridae . Virus Genes 23:5–16 [CrossRef]
    [Google Scholar]
  46. Posada D. 2002; Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19:708–717 [CrossRef]
    [Google Scholar]
  47. Reuter G., Krisztalovics K., Vennema H., Koopmans M., Szucs G. 2005; Evidence of the etiological predominance of norovirus in gastroenteritis outbreaks – emerging new-variant and recombinant noroviruses in Hungary. J Med Virol 76:598–607 [CrossRef]
    [Google Scholar]
  48. Reuter G., Vennema H., Koopmans M., Szucs G. 2006; Epidemic spread of recombinant noroviruses with four capsid types in Hungary. J Clin Virol 35:84–88 [CrossRef]
    [Google Scholar]
  49. Rohayem J., Munch J., Rethwilm A. 2005; Evidence of recombination in the norovirus capsid gene. J Virol 79:4977–4990 [CrossRef]
    [Google Scholar]
  50. Sasaki Y., Kai A., Hayashi Y., Shinkai T., Noguchi Y., Hasegawa M., Sadamasu K., Mori K., Tabei Y. other authors 2006; Multiple viral infections and genomic divergence among noroviruses during an outbreak of acute gastroenteritis. J Clin Microbiol 44:790–797 [CrossRef]
    [Google Scholar]
  51. Seah E. L., Gunesekere I. C., Marshall J. A., Wright P. J. 1999; Variation in ORF3 of genogroup 2 Norwalk-like viruses. Arch Virol 144:1007–1014 [CrossRef]
    [Google Scholar]
  52. Tajima F., Nei M. 1984; Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1:269–285
    [Google Scholar]
  53. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  54. Tsugawa T., Numata-Kinoshita K., Honma S., Nakata S., Tatsumi M., Sakai Y., Natori K., Takeda N., Kobayashi S., Tsutsumi H. 2006; Virological, serological and clinical features of an outbreak of acute gastroenteritis due to recombinant genogroup II norovirus in an infant home. J Clin Microbiol 44:177–182 [CrossRef]
    [Google Scholar]
  55. Tu E. T.-V., Nguyen T., Lee P., Bull R. A., Musto J., Hansman G., White P. A., Rawlinson W. D., McIver C. J. 2007; Norovirus GII.4 strains and outbreaks, Australia. Emerg Infect Dis 13:1128–1129 [CrossRef]
    [Google Scholar]
  56. van den Berg H., Lodder W., van der Poel W., Vennema H., de Roda Husman A. M. 2005; Genetic diversity of noroviruses in raw and treated sewage water. Res Microbiol 156:532–540 [CrossRef]
    [Google Scholar]
  57. Vidal R., Roessler P., Solari V., Vollaire J., Jiang X., Matson D. O., Mamani N., Prado V., O'Ryan M. L. 2006; Novel recombinant norovirus causing outbreaks of gastroenteritis in Santiago, Chile. J Clin Microbiol 44:2271–2275 [CrossRef]
    [Google Scholar]
  58. Vinje J., Hamidjaja R. A., Sobsey M. D. 2004; Development and application of a capsid VP1 (region D) based reverse transcription PCR assay for genotyping of genogroup I and II noroviruses. J Virol Methods 116:109–117 [CrossRef]
    [Google Scholar]
  59. Wang Q. H., Han M. G., Cheetham S., Souza M., Funk J. A., Saif L. J. 2005; Porcine noroviruses related to human noroviruses. Emerg Infect Dis 11:1874–1881 [CrossRef]
    [Google Scholar]
  60. Waters A., Coughlan S., Hall W. W. 2007; Characterisation of a novel recombination event in the norovirus polymerase gene. Virology 363:11–14 [CrossRef]
    [Google Scholar]
  61. Widdowson M. A., Cramer E. H., Hadley L., Bresee J. S., Beard R. S., Bulens S. N., Charles M., Chege W., Isakbaeva E. other authors 2004; Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus –. United States: 2002 J Infect Dis 190:27–36 [CrossRef]
    [Google Scholar]
  62. Widdowson M. A., Monroe S. S., Glass R. I. 2005a; Are noroviruses emerging?. Emerg Infect Dis 11:735–737
    [Google Scholar]
  63. Widdowson M. A., Rockx B., Schepp R., van der Poel W. H., Vinje J., van Duynhoven Y. T., Koopmans M. P. 2005b; Detection of serum antibodies to bovine norovirus in veterinarians and the general population in the Netherlands. J Med Virol 76:119–128 [CrossRef]
    [Google Scholar]
  64. Worobey M., Holmes E. C. 1999; Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80:2535–2543
    [Google Scholar]
  65. Zheng D. P., Ando T., Fankhauser R. L., Beard R. S., Glass R. I., Monroe S. S. 2006; Norovirus classification and proposed strain nomenclature. Virology 346:312–323 [CrossRef]
    [Google Scholar]
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