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. 2007 May 29;152(9):1709–1719. doi: 10.1007/s00705-007-0989-y

Genetic diversity and recombination of murine noroviruses in immunocompromised mice

B Müller 1, U Klemm 2, A Mas Marques 1, E Schreier 1
PMCID: PMC7086864  PMID: 17533553

Summary

Murine noroviruses (MNV) are newly identified pathogens which infect laboratory mice. In this study, we found a high prevalence (64.3%) of MNV in various breeding colonies of immunocompromised, transgenic and wild-type mouse lines. All mice survived infection with no signs of clinical disease. Faeces samples were collected from animals housed in two separate laboratory mouse colonies in Berlin, Germany, and screened using quantitative reverse transcription (RT)-PCR. We have determined the complete nucleotide sequences of 3 novel MNV strains. Furthermore, we sequenced two subgenomic regions within open reading frames (ORFs) 1 and 2 that are suitable for genotyping. Sequence analysis of the full-length and partial genomes obtained from naturally infected mice yielded valuable data on genetic diversity of murine noroviruses. The discordance of genotype affiliation of some MNVs shown in ORF1 and ORF2 suggests intertypic recombination events in vivo.

Keywords: Mouse Line, Complete Nucleotide Sequence, Human Noroviruses, Subgenomic Region, SimPlot Analysis

References

  1. Ambert-Balay K, Bon F, Le Guyader F, Pothier P, Kohli E. Characterization of new recombinant noroviruses. J Clin Microbiol. 2005;43:5179–5186. doi: 10.1128/JCM.43.10.5179-5186.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ando T, Noel JS, Fankhauser RL. Genetic classification of “Norwalk-like viruses”. J Infect Dis. 2000;181(Suppl 2):S336–S348. doi: 10.1086/315589. [DOI] [PubMed] [Google Scholar]
  3. Belliot G, Sosnovtsev SV, Mitra T, Hammer C, Garfield M, Green KY. In vitro proteolytic processing of the MD145 norovirus ORF1 nonstructural polyprotein yields stable precursors and products similar to those detected in calicivirus-infected cells. J Virol. 2003;77:10957–10974. doi: 10.1128/JVI.77.20.10957-10974.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bertolotti-Ciarlet A, White LJ, Chen R, Prasad BV, Estes MK. Structural requirements for the assembly of Norwalk virus-like particles. J Virol. 2002;76:4044–4055. doi: 10.1128/JVI.76.8.4044-4055.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bull RA, Hansman GS, Clancy LE, Tanaka MM, Rawlinson WD, White PA. Norovirus recombination in ORF1/ORF2 overlap. Emerg Infect Dis. 2005;11:1079–1085. doi: 10.3201/eid1107.041273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA, Vinje J. Surrogates for the study of norovirus stability and inactivation in the environment: a comparison of murine norovirus and feline calicivirus. J Food Prot. 2006;69:2761–2765. doi: 10.4315/0362-028x-69.11.2761. [DOI] [PubMed] [Google Scholar]
  7. Chakravarty S, Hutson AM, Estes MK, Prasad BV. Evolutionary trace residues in noroviruses: importance in receptor binding, antigenicity, virion assembly, and strain diversity. J Virol. 2005;79:554–568. doi: 10.1128/JVI.79.1.554-568.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Felsenstein J. PHYLIP-Phylogeny Inference Package (Version 3.2) Cladistics. 1989;5:164–166. [Google Scholar]
  9. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999;41:95–98. [Google Scholar]
  10. Han MG, Smiley JR, Thomas C, Saif LJ. 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. 2004;42:5214–5224. doi: 10.1128/JCM.42.11.5214-5224.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hansman GS, Oka T, Katayama K, Takeda N. Human sapoviruses: genetic diversity, recombination, and classification. Rev Med Virol. 2007;17:133–141. doi: 10.1002/rmv.533. [DOI] [PubMed] [Google Scholar]
  12. Hardy ME. Norovirus protein structure and function. FEMS Microbiol Lett. 2005;253:1–8. doi: 10.1016/j.femsle.2005.08.031. [DOI] [PubMed] [Google Scholar]
  13. Hsu CC, Wobus CE, Steffen EK, Riley LK, Livingston RS. Development of a microsphere-based serologic multiplexed fluorescent immunoassay and a reverse transcriptase PCR assay to detect murine norovirus 1 infection in mice. Clin Diagn Lab Immunol. 2005;12:1145–1151. doi: 10.1128/CDLI.12.10.1145-1151.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hsu CC, Riley LK, Wills HM, Livingston RS. Persistent infection with and serologic cross-reactivity of three novel murine noroviruses. Comp Med. 2006;56:247–251. [PubMed] [Google Scholar]
  15. Hsu CC, Riley LK, Livingston RS. Molecular characterization of three novel murine noroviruses. Virus Genes. 2007;34:147–155. doi: 10.1007/s11262-006-0060-1. [DOI] [PubMed] [Google Scholar]
  16. Kao CC, Singh P, Ecker DJ. De novo initiation of viral RNA-dependent RNA synthesis. Virology. 2001;287:251–260. doi: 10.1006/viro.2001.1039. [DOI] [PubMed] [Google Scholar]
  17. Karst SM, Wobus CE, Lay M, Davidson J, Virgin HWt. STAT1-dependent innate immunity to a Norwalk-like virus. Science. 2003;299:1575–1578. doi: 10.1126/science.1077905. [DOI] [PubMed] [Google Scholar]
  18. Katayama K, Shirato-Horikoshi H, Kojima S, Kageyama T, Oka T, Hoshino F, Fukushi S, Shinohara M, Uchida K, Suzuki Y, Gojobori T, Takeda N. Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses. Virology. 2002;299:225–239. doi: 10.1006/viro.2002.1568. [DOI] [PubMed] [Google Scholar]
  19. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
  20. Kirkegaard K, Baltimore D. The mechanism of RNA recombination in poliovirus. Cell. 1986;47:433–443. doi: 10.1016/0092-8674(86)90600-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol. 1999;73:152–160. doi: 10.1128/jvi.73.1.152-160.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Makino S, Keck JG, Stohlman SA, Lai MM. High-frequency RNA recombination of murine coronaviruses. J Virol. 1986;57:729–737. doi: 10.1128/jvi.57.3.729-737.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Matsui SM, Greenberg HB. Immunity to calicivirus infection. J Infect Dis. 2000;181(Suppl 2):S331–S335. doi: 10.1086/315587. [DOI] [PubMed] [Google Scholar]
  24. Page RD. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 1996;12:357–358. doi: 10.1093/bioinformatics/12.4.357. [DOI] [PubMed] [Google Scholar]
  25. Parrino TA, Schreiber DS, Trier JS, Kapikian AZ, Blacklow NR. Clinical immunity in acute gastroenteritis caused by Norwalk agent. N Engl J Med. 1977;297:86–89. doi: 10.1056/NEJM197707142970204. [DOI] [PubMed] [Google Scholar]
  26. Pfister T, Wimmer E. Polypeptide p41 of a Norwalk-like virus is a nucleic acid-independent nucleoside triphosphatase. J Virol. 2001;75:1611–1619. doi: 10.1128/JVI.75.4.1611-1619.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. X-ray crystallographic structure of the Norwalk virus capsid. Science. 1999;286:287–290. doi: 10.1126/science.286.5438.287. [DOI] [PubMed] [Google Scholar]
  28. Schreier E, Doring F, Kunkel U. Molecular epidemiology of outbreaks of gastroenteritis associated with small round structured viruses in Germany in 1997/98. Arch Virol. 2000;145:443–453. doi: 10.1007/s007050050038. [DOI] [PubMed] [Google Scholar]
  29. Schuffenecker I, Ando T, Thouvenot D, Lina B, Aymard M. Genetic classification of “Sapporo-like viruses”. Arch Virol. 2001;146:2115–2132. doi: 10.1007/s007050170024. [DOI] [PubMed] [Google Scholar]
  30. Sosnovtsev SV, Belliot G, Chang KO, Prikhodko VG, Thackray LB, Wobus CE, Karst SM, Virgin HW, Green KY. Cleavage map and proteolytic processing of the murine norovirus nonstructural polyprotein in infected cells. J Virol. 2006;80:7816–7831. doi: 10.1128/JVI.00532-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ward JM, Wobus CE, Thackray LB, Erexson CR, Faucette LJ, Belliot G, Barron EL, Sosnovtsev SV, Green KY. Pathology of immunodeficient mice with naturally occurring murine norovirus infection. Toxicol Pathol. 2006;34:708–715. doi: 10.1080/01926230600918876. [DOI] [PubMed] [Google Scholar]
  32. Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV, Belliot G, Krug A, Mackenzie JM, Green KY, Virgin HW. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2004;2:e432. doi: 10.1371/journal.pbio.0020432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wobus CE, Thackray LB, Virgin HWt. Murine norovirus: a model system to study norovirus biology and pathogenesis. J Virol. 2006;80:5104–5112. doi: 10.1128/JVI.02346-05. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Worobey M, Holmes EC. Evolutionary aspects of recombination in RNA viruses. J Gen Virol. 1999;80(Pt 10):2535–2543. doi: 10.1099/0022-1317-80-10-2535. [DOI] [PubMed] [Google Scholar]
  35. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. Norovirus classification and proposed strain nomenclature. Virology. 2006;346:312–323. doi: 10.1016/j.virol.2005.11.015. [DOI] [PubMed] [Google Scholar]

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