1887

Journal of General Virology header logo

Volume 94, Issue 1

Whole-genome analysis of two bovine rotavirus C strains: Shintoku and Toyama Free

Abstract

Rotavirus C (RVC) has been detected frequently in epidemic cases and/or outbreaks of diarrhoea in humans and animals worldwide. Because it is difficult to cultivate RVCs serially in cell culture, the sequence data available for RVCs are limited, despite their potential economical and epidemiological impact. Although whole-genome sequences of one porcine RVC and seven human RVC strains have been analysed, this has not yet been done for a bovine RVC strain. In the present study, we first determined the nucleotide sequences for five as-yet underresearched genes, including the NSP4 gene, from a cultivable bovine RVC, the Shintoku strain, identified in Hokkaido Prefecture, Japan, in 1991. In addition, we elucidated the ORF sequences of all segments from another bovine RVC, the Toyama strain, detected in Toyama Prefecture, Japan, in 2010, in order to investigate genetic divergence among bovine RVCs. Comparison of segmental nucleotide and deduced amino acid sequences among RVCs indicates high identity among bovine RVCs and low identity between human and porcine RVCs. Phylogenetic analysis of each gene showed that the two bovine RVCs belong to a cluster distinct from human and porcine RVCs. These data demonstrate that RVCs can be classified into different genotypes according to host species. Moreover, RVC NSP1, NSP2 and VP1 amino acid sequences contain a unique motif that is highly conserved among rotavirus A (RVA) strains and, hence, several proteins from bovine RVCs are suggested to play important roles that are similar to those of RVAs.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.046763-0
2013-01-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/1/128.html?itemId=/content/journal/jgv/10.1099/vir.0.046763-0&mimeType=html&fmt=ahah

References

  1. Abid I., Guix S., Aouni M., Pintó R., Bosch A. 2007; Detection and characterization of human group C rotavirus in the pediatric population of Barcelona, Spain. J Clin Virol 38:78–82 [View Article][PubMed]
     [Google Scholar]
  2. Adah M. I., Wade A., Oseto M., Kuzuya M., Taniguchi K. 2002; Detection of human group C rotaviruses in Nigeria and sequence analysis of their genes encoding VP4, VP6, and VP7 proteins. J Med Virol 66:269–275 [View Article][PubMed]
     [Google Scholar]
  3. Bohl E. H., Saif L. J., Theil K. W., Agnes A. G., Cross R. F. 1982; Porcine pararotavirus: detection, differentiation from rotavirus, and pathogenesis in gnotobiotic pigs. J Clin Microbiol 15:312–319[PubMed]
     [Google Scholar]
  4. Carpio R. V., González-Nilo F. D., Jayaram H., Spencer E., Prasad B. V., Patton J. T., Taraporewala Z. F. 2004; Role of the histidine triad-like motif in nucleotide hydrolysis by the rotavirus RNA-packaging protein NSP2. J Biol Chem 279:10624–10633 [View Article][PubMed]
     [Google Scholar]
  5. Castello A. A., Argüelles M. H., Villegas G. A., Olthoff A., Glikmann G. 2002; Incidence and prevalence of human group C rotavirus infections in Argentina. J Med Virol 67:106–112 [View Article][PubMed]
     [Google Scholar]
  6. Chang K. O., Nielsen P. R., Ward L. A., Saif L. J. 1999; Dual infection of gnotobiotic calves with bovine strains of group A and porcine-like group C rotaviruses influences pathogenesis of the group C rotavirus. J Virol 73:9284–9293[PubMed]
     [Google Scholar]
  7. Chen Z., Lambden P. R., Lau J., Caul E. O., Clarke I. N. 2002; Human group C rotavirus: completion of the genome sequence and gene coding assignments of a non-cultivatable rotavirus. Virus Res 83:179–187 [View Article][PubMed]
     [Google Scholar]
  8. Cohen J., Charpilienne A., Chilmonczyk S., Estes M. K. 1989; Nucleotide sequence of bovine rotavirus gene 1 and expression of the gene product in baculovirus. Virology 171:131–140 [View Article][PubMed]
     [Google Scholar]
  9. Esona M. D., Humphrey C. D., Dennehy P. H., Jiang B. 2008; Prevalence of group C rotavirus among children in Rhode Island, United States. J Clin Virol 42:221–224 [View Article][PubMed]
     [Google Scholar]
  10. Estes M. K., Kapikian A. Z. 2007; Rotaviruses. In Fields Virology, 5th edn. pp. 1917–1974 Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Roizman B., Straus S. E. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins;
     [Google Scholar]
  11. Gabbay Y. B., Borges A. A., Oliveira D. S., Linhares A. C., Mascarenhas J. D., Barardi C. R., Simões C. M., Wang Y., Glass R. I., Jiang B. 2008; Evidence for zoonotic transmission of group C rotaviruses among children in Belém, Brazil. J Med Virol 80:1666–1674 [View Article][PubMed]
     [Google Scholar]
  12. Graff J. W., Mitzel D. N., Weisend C. M., Flenniken M. L., Hardy M. E. 2002; Interferon regulatory factor 3 is a cellular partner of rotavirus NSP1. J Virol 76:9545–9550 [View Article][PubMed]
     [Google Scholar]
  13. Jiang B., Tsunemitsu H., Gentsch J. R., Glass R. I., Green K. Y., Qian Y., Saif L. J. 1992; Nucleotide sequence of gene 5 encoding the inner capsid protein (VP6) of bovine group C rotavirus: comparison with corresponding genes of group C, A, and B rotaviruses. Virology 190:542–547 [View Article][PubMed]
     [Google Scholar]
  14. Jiang B., Tsunemitsu H., Gentsch J. R., Saif L. J., Glass R. I. 1993; Nucleotide sequences of genes 6 and 10 of a bovine group C rotavirus. Nucleic Acids Res 21:2250 [View Article][PubMed]
     [Google Scholar]
  15. Jiang B., Tsunemitsu H., Dennehy P. H., Oishi I., Brown D., Schnagl R. D., Oseto M., Fang Z. Y., Avendano L. F.other authors 1996; Sequence conservation and expression of the gene encoding the outer capsid glycoprotein among human group C rotaviruses of global distribution. Arch Virol 141:381–390 [View Article][PubMed]
     [Google Scholar]
  16. Kim Y., Chang K. O., Straw B., Saif L. J. 1999; Characterization of group C rotaviruses associated with diarrhea outbreaks in feeder pigs. J Clin Microbiol 37:1484–1488[PubMed]
     [Google Scholar]
  17. Kobayashi N., Alam M., Kojima K., Mise K., Ishino M., Sumi A. 2003; Genomic diversity and evolution of rotaviruses: an overview. In Genomic Diversity and Molecular Epidemiology of Rotaviruses pp. 75–90 Edited by Kobayashi N. Trivandrum, India: Research Signpost;
     [Google Scholar]
  18. Kusanagi K., Kuwahara H., Katoh T., Nunoya T., Ishikawa Y., Samejima T., Tajima M. 1992; Isolation and serial propagation of porcine epidemic diarrhea virus in cell cultures and partial characterization of the isolate. J Vet Med Sci 54:313–318 [View Article][PubMed]
     [Google Scholar]
  19. Kuzuya M., Fujii R., Hamano M., Yamada M., Shinozaki K., Sasagawa A., Hasegawa S., Kawamoto H., Matsumoto K.other authors 1998; Survey of human group C rotaviruses in Japan during the winter of 1992 to 1993. J Clin Microbiol 36:6–10[PubMed]
     [Google Scholar]
  20. Luchs A., Morillo S. G., de Oliveira C. M., Timenetsky M. C. 2011; Monitoring of group C rotavirus in children with acute gastroenteritis in Brazil: an emergent epidemiological issue after rotavirus vaccine?. J Med Virol 83:1631–1636 [View Article][PubMed]
     [Google Scholar]
  21. Mackow E. R. 1995; Group B and C rotaviruses. In Infections of the Gastrointestinal Tract pp. 983–1008 Edited by Blaser M. J., Smith P. D., Ravdin J. I., Greenberg H. B., Guerrant R. L. New York: Raven Press;
     [Google Scholar]
  22. Martella V., Bányai K., Lorusso E., Decaro N., Bellacicco A., Desario C., Corrente M., Greco G., Moschidou P.other authors 2007; Genetic heterogeneity in the VP7 of group C rotaviruses. Virology 367:358–366 [View Article][PubMed]
     [Google Scholar]
  23. Matsumoto K., Hatano M., Kobayashi K., Hasegawa A., Yamazaki S., Nakata S., Chiba S., Kimura Y. 1989; An outbreak of gastroenteritis associated with acute rotaviral infection in schoolchildren. J Infect Dis 160:611–615 [View Article][PubMed]
     [Google Scholar]
  24. Matthijnssens J., Ciarlet M., Rahman M., Attoui H., Bányai K., Estes M. K., Gentsch J. R., Iturriza-Gómara M., Kirkwood C. D.other authors 2008a; Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 153:1621–1629 [View Article][PubMed]
     [Google Scholar]
  25. Matthijnssens J., Ciarlet M., Heiman E., Arijs I., Delbeke T., McDonald S. M., Palombo E. A., Iturriza-Gómara M., Maes P.other authors 2008b; Full genome-based classification of rotaviruses reveals a common origin between human Wa-like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 82:3204–3219 [View Article][PubMed]
     [Google Scholar]
  26. Matthijnssens J., Taraporewala Z. F., Yang H., Rao S., Yuan L., Cao D., Hoshino Y., Mertens P. P., Carner G. R.other authors 2010; Simian rotaviruses possess divergent gene constellations that originated from interspecies transmission and reassortment. J Virol 84:2013–2026 [View Article][PubMed]
     [Google Scholar]
  27. Matthijnssens J., Otto P. H., Ciarlet M., Desselberger U., Van Ranst M., Johne R. 2012; VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 157:1177–1182 [View Article][PubMed]
     [Google Scholar]
  28. Mawatari T., Taneichi A., Kawagoe T., Hosokawa M., Togashi K., Tsunemitsu H. 2004; Detection of a bovine group C rotavirus from adult cows with diarrhea and reduced milk production. J Vet Med Sci 66:887–890 [View Article][PubMed]
     [Google Scholar]
  29. McDonald S. M., Matthijnssens J., McAllen J. K., Hine E., Overton L., Wang S., Lemey P., Zeller M., Van Ranst M.other authors 2009; Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog 5:e1000634 [View Article][PubMed]
     [Google Scholar]
  30. Medici M. C., Abelli L. A., Martinelli M., Martella V., Dettori G., Chezzi C. 2009; Molecular characterization of group C rotaviruses detected in children in Italy. J Clin Virol 44:62–65 [View Article][PubMed]
     [Google Scholar]
  31. Mitui M. T., Bozdayi G., Dalgic B., Bostanci I., Nishizono A., Ahmed K. 2009; Molecular characterization of a human group C rotavirus detected first in Turkey. Virus Genes 39:157–164 [View Article][PubMed]
     [Google Scholar]
  32. Moon S., Humphrey C. D., Kim J. S., Baek L. J., Song J. W., Song K. J., Jiang B. 2011; First detection of group C rotavirus in children with acute gastroenteritis in South Korea. Clin Microbiol Infect 17:244–247 [View Article][PubMed]
     [Google Scholar]
  33. Morin M., Magar R., Robinson Y. 1990; Porcine group C rotavirus as a cause of neonatal diarrhea in a Quebec swine herd. Can J Vet Res 54:385–389[PubMed]
     [Google Scholar]
  34. Mwenda J. M., Peenze I., Omollo E., Galo M., Steele A. D. 2003; Human group C rotaviruses identified in Kenya. East Afr Med J 80:73–76[PubMed]
     [Google Scholar]
  35. Nagashima S., Kobayashi N., Ishino M., Alam M. M., Ahmed M. U., Paul S. K., Ganesh B., Chawla-Sarkar M., Krishnan T.other authors 2008; Whole genomic characterization of a human rotavirus strain B219 belonging to a novel group of the genus Rotavirus. J Med Virol 80:2023–2033 [View Article][PubMed]
     [Google Scholar]
  36. Nilsson M., Svenungsson B., Hedlund K. O., Uhnoo I., Lagergren A., Akre T., Svensson L. 2000; Incidence and genetic diversity of group C rotavirus among adults. J Infect Dis 182:678–684 [View Article][PubMed]
     [Google Scholar]
  37. Otto P., Schulze P., Herbst W. 1999; Demonstration of group C rotaviruses in fecal samples of diarrheic dogs in Germany. Arch Virol 144:2467–2473 [View Article][PubMed]
     [Google Scholar]
  38. Park S. I., Jeong Y. J., Kim H. J., Park J. G., Kang S. Y., Woo S. K., Kim C. H., Jung C. H., Kang M. I., Cho K. O. 2011; Genetically diverse group C rotaviruses cause sporadic infection in Korean calves. J Vet Med Sci 73:479–482 [View Article][PubMed]
     [Google Scholar]
  39. Peñaranda M. E., Cubitt W. D., Sinarachatanant P., Taylor D. N., Likanonsakul S., Saif L., Glass R. I. 1989; Group C rotavirus infections in patients with diarrhea in Thailand, Nepal, and England. J Infect Dis 160:392–397 [View Article][PubMed]
     [Google Scholar]
  40. Phan T. G., Nishimura S., Okame M., Nguyen T. A., Khamrin P., Okitsu S., Maneekarn N., Ushijima H. 2004; Virus diversity and an outbreak of group C rotavirus among infants and children with diarrhea in Maizuru city, Japan during 2002–2003. J Med Virol 74:173–179 [View Article][PubMed]
     [Google Scholar]
  41. Qiao H., Nilsson M., Abreu E. R., Hedlund K. O., Johansen K., Zaori G., Svensson L. 1999; Viral diarrhea in children in Beijing, China. J Med Virol 57:390–396 [View Article][PubMed]
     [Google Scholar]
  42. Rahman M., Banik S., Faruque A. S., Taniguchi K., Sack D. A., Van Ranst M., Azim T. 2005; Detection and characterization of human group C rotaviruses in Bangladesh. J Clin Microbiol 43:4460–4465 [View Article][PubMed]
     [Google Scholar]
  43. Rodger S. M., Bishop R. F., Holmes I. H. 1982; Detection of a rotavirus-like agent associated with diarrhea in an infant. J Clin Microbiol 16:724–726[PubMed]
     [Google Scholar]
  44. Saif L. J., Jiang B. 1994; Nongroup A rotaviruses of humans and animals. Curr Top Microbiol Immunol 185:339–371 [View Article][PubMed]
     [Google Scholar]
  45. Saif L. J., Bohl E. H., Theil K. W., Cross R. F., House J. A. 1980; Rotavirus-like, calicivirus-like, and 23-nm virus-like particles associated with diarrhea in young pigs. J Clin Microbiol 12:105–111[PubMed]
     [Google Scholar]
  46. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
     [Google Scholar]
  47. Sánchez-Fauquier A., Roman E., Colomina J., Wilhelmi I., Glass R. I., Jiang B. 2003; First detection of group C rotavirus in children with acute diarrhea in Spain. Arch Virol 148:399–404 [View Article][PubMed]
     [Google Scholar]
  48. Schnagl R. D., Boniface K., Cardwell P., McCarthy D., Ondracek C., Coulson B., Erlich J., Morey F. 2004; Incidence of group C human rotavirus in central Australia and sequence variation of the VP7 and VP4 genes. J Clin Microbiol 42:2127–2133 [View Article][PubMed]
     [Google Scholar]
  49. Sigolo de San Juan C., Bellinzoni R. C., Mattion N., La Torre J., Scodeller E. A. 1986; Incidence of group A and atypical rotaviruses in Brazilian pig herds. Res Vet Sci 41:270–272[PubMed]
     [Google Scholar]
  50. Suzuki T., Soma J., Kuga K., Miyazaki A., Tsunemitsu H. 2012; Sequence and phylogenetic analyses of nonstructural protein 2 genes of species B porcine rotaviruses detected in Japan during 2001–2009. Virus Res 165:46–51 [View Article][PubMed]
     [Google Scholar]
  51. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
     [Google Scholar]
  52. Torres-Medina A. 1987; Isolation of an atypical rotavirus causing diarrhea in neonatal ferrets. Lab Anim Sci 37:167–171[PubMed]
     [Google Scholar]
  53. Tsunemitsu H., Saif L. J., Jiang B. M., Shimizu M., Hiro M., Yamaguchi H., Ishiyama T., Hirai T. 1991; Isolation, characterization, and serial propagation of a bovine group C rotavirus in a monkey kidney cell line (MA104). J Clin Microbiol 29:2609–2613[PubMed]
     [Google Scholar]
  54. Tsunemitsu H., Jiang B., Saif L. J. 1992; Detection of group C rotavirus antigens and antibodies in animals and humans by enzyme-linked immunosorbent assays. J Clin Microbiol 30:2129–2134[PubMed]
     [Google Scholar]
  55. Tsunemitsu H., Jiang B., Saif L. J. 1996; Sequence comparison of the VP7 gene encoding the outer capsid glycoprotein among animal and human group C rotaviruses. Arch Virol 141:705–713 [View Article][PubMed]
     [Google Scholar]
  56. Yamamoto D., Ghosh S., Kuzuya M., Wang Y. H., Zhou X., Chawla-Sarkar M., Paul S. K., Ishino M., Kobayashi N. 2011; Whole-genome characterization of human group C rotaviruses: identification of two lineages in the VP3 gene. J Gen Virol 92:361–369 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.046763-0
Loading
Whole-genome analysis of two bovine rotavirus C strains: Shintoku and Toyama
J. Gen. Virol. 94, 128 (2013); https://doi.org/10.1099/vir.0.046763-0
/content/journal/jgv/10.1099/vir.0.046763-0
/content/journal/jgv/10.1099/vir.0.046763-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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