1887

Journal of General Virology header logo

Volume 98, Issue 11

A provisional complete genome-based genotyping system for rotavirus species C from terrestrial mammals Free

Abstract

Rotaviruses C (RVCs) have been detected in pigs, humans, cows, ferrets and dogs. Despite their zoonotic impact and pathogenicity, the genetic characterization of RVCs is incomplete, unlike rotaviruses A (RVAs), whose genetics are well studied. Several studies reported partial and complete genomic sequences for multiple porcine and canine RVCs. We aimed to establish a complete genome-based genotyping system for RVCs, by analysing complete genome data from 22 porcine RVCs identified in Japan from 2002 to 2010, along with those from multiple human, bovine, porcine, canine and ferret RVCs reported in several previous studies. Comparative sequence analyses among RVCs from various host species demonstrated that porcine RVCs had a high level of genetic diversity. In addition, phylogenetic analyses of all 11 RNA segments indicated that porcine RVCs could be classified into multiple genotypes. Notably, the VP4 dendrogram divided bovine RVCs into multiple genotypes. Consequently, the provisional genotype classification for RVCs from terrestrial mammals revealed the existence of genotypes 18G, 21P, 13I, 4R, 6C, 6M, 9A, 8N, 6T, 5E and 4H for the genes VP7, VP4, VP6, VP1, VP2, VP3, NSP1, NSP2, NSP3, NSP4 and NSP5, respectively, based on the cut-off values as defined by the Rotavirus Classification Working Group. The system established in this study deepens our understanding of RVC evolution and facilitates the discovery of genetic events (gene reassortment and interspecies transmission) among RVCs.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): complete genome , genetic diversity , genotype classification , phylogenetic analysis and rotavirus C
© 2017 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000953
2017-11-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/11/2647.html?itemId=/content/journal/jgv/10.1099/jgv.0.000953&mimeType=html&fmt=ahah

References

  1. Estes MK, Kapikian AZ. Rotaviruses. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al. (editors) Fields Virology, 5th ed. Philadelphia: Lippincott, Williams & Wilkins; 2007 pp. 1917–1974
     [Google Scholar]
  2. Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, van Ranst M et al. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 2012; 157:1177–1182 [View Article][PubMed]
     [Google Scholar]
  3. Mihalov-Kovács E, Gellért Á, Marton S, Farkas SL, Fehér E et al. Candidate new rotavirus species in sheltered dogs, Hungary. Emerg Infect Dis 2015; 21:660–663 [View Article][PubMed]
     [Google Scholar]
  4. Saif LJ, Bohl EH, Theil KW, Cross RF, House JA. Rotavirus-like, calicivirus-like, and 23-nm virus-like particles associated with diarrhea in young pigs. J Clin Microbiol 1980; 12:105–111[PubMed]
     [Google Scholar]
  5. Bohl EH, Saif LJ, Theil KW, Agnes AG, Cross RF. Porcine pararotavirus: detection, differentiation from rotavirus, and pathogenesis in gnotobiotic pigs. J Clin Microbiol 1982; 15:312–319[PubMed]
     [Google Scholar]
  6. Rodger SM, Bishop RF, Holmes IH. Detection of a rotavirus-like agent associated with diarrhea in an infant. J Clin Microbiol 1982; 16:724–726[PubMed]
     [Google Scholar]
  7. Torres-Medina A. Isolation of an atypical rotavirus causing diarrhea in neonatal ferrets. Lab Anim Sci 1987; 37:167–171[PubMed]
     [Google Scholar]
  8. Chang KO, Nielsen PR, Ward LA, Saif LJ. 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 1999; 73:9284–9293[PubMed]
     [Google Scholar]
  9. Otto P, Schulze P, Herbst W. Demonstration of group C rotaviruses in fecal samples of diarrheic dogs in Germany. Arch Virol 1999; 144:2467–2473 [View Article][PubMed]
     [Google Scholar]
  10. Tsunemitsu H, Saif LJ, Jiang BM, Shimizu M, Hiro M et al. Isolation, characterization, and serial propagation of a bovine group C rotavirus in a monkey kidney cell line (MA104). J Clin Microbiol 1991; 29:2609–2613[PubMed]
     [Google Scholar]
  11. Matsumoto K, Hatano M, Kobayashi K, Hasegawa A, Yamazaki S et al. An outbreak of gastroenteritis associated with acute rotaviral infection in schoolchildren. J Infect Dis 1989; 160:611–615 [View Article][PubMed]
     [Google Scholar]
  12. Caul EO, Ashley CR, Darville JM, Bridger JC. Group C rotavirus associated with fatal enteritis in a family outbreak. J Med Virol 1990; 30:201–205 [View Article][PubMed]
     [Google Scholar]
  13. Jiang B, Dennehy PH, Spangenberger S, Gentsch JR, Glass RI. First detection of group C rotavirus in fecal specimens of children with diarrhea in the United States. J Infect Dis 1995; 172:45–50 [View Article][PubMed]
     [Google Scholar]
  14. Kuzuya M, Fujii R, Hamano M, Yamada M, Shinozaki K et al. Survey of human group C rotaviruses in Japan during the winter of 1992 to 1993. J Clin Microbiol 1998; 36:6–10[PubMed]
     [Google Scholar]
  15. Nilsson M, Svenungsson B, Hedlund KO, Uhnoo I, Lagergren A et al. Incidence and genetic diversity of group C rotavirus among adults. J Infect Dis 2000; 182:678–684 [View Article][PubMed]
     [Google Scholar]
  16. Peñaranda ME, Cubitt WD, Sinarachatanant P, Taylor DN, Likanonsakul S et al. Group C rotavirus infections in patients with diarrhea in Thailand, Nepal, and England. J Infect Dis 1989; 160:392–397 [View Article][PubMed]
     [Google Scholar]
  17. Oishi I, Yamazaki K, Minekawa Y. An occurrence of diarrheal cases associated with group C rotavirus in adults. Microbiol Immunol 1993; 37:505–509 [View Article][PubMed]
     [Google Scholar]
  18. Hamano M, Kuzuya M, Fujii R, Ogura H, Mori T et al. Outbreak of acute gastroenteritis caused by human group C rotavirus in a primary school. Jpn J Infect Dis 1999; 52:170–171[PubMed]
     [Google Scholar]
  19. Qiao H, Nilsson M, Abreu ER, Hedlund KO, Johansen K et al. Viral diarrhea in children in Beijing, China. J Med Virol 1999; 57:390–396 [View Article][PubMed]
     [Google Scholar]
  20. Sebata T, Steele AD. Human group C rotavirus identified in South Africa. S Afr Med J 1999; 89:1073–1074[PubMed]
     [Google Scholar]
  21. Kuzuya M, Fujii R, Hamano M, Ohata R, Ogura H et al. Seroepidemiology of human group C rotavirus in Japan based on a blocking enzyme-linked immunosorbent assay. Clin Diagn Lab Immunol 2001; 8:161–165 [View Article][PubMed]
     [Google Scholar]
  22. Adah MI, Wade A, Oseto M, Kuzuya M, Taniguchi K. Detection of human group C rotaviruses in Nigeria and sequence analysis of their genes encoding VP4, VP6, and VP7 proteins. J Med Virol 2002; 66:269–275 [View Article][PubMed]
     [Google Scholar]
  23. Castello AA, Argüelles MH, Villegas GA, Olthoff A, Glikmann G. Incidence and prevalence of human group C rotavirus infections in Argentina. J Med Virol 2002; 67:106–112 [View Article][PubMed]
     [Google Scholar]
  24. Mwenda JM, Peenze I, Omollo E, Galo M, Steele AD. Human group C rotaviruses identified in Kenya. East Afr Med J 2003; 80:73–76[PubMed]
     [Google Scholar]
  25. Schnagl RD, Boniface K, Cardwell P, McCarthy D, Ondracek C et al. Incidence of group C human rotavirus in central Australia and sequence variation of the VP7 and VP4 genes. J Clin Microbiol 2004; 42:2127–2133 [View Article][PubMed]
     [Google Scholar]
  26. Rahman M, Banik S, Faruque AS, Taniguchi K, Sack DA et al. Detection and characterization of human group C rotaviruses in Bangladesh. J Clin Microbiol 2005; 43:4460–4465 [View Article][PubMed]
     [Google Scholar]
  27. Yee EL, Jiang B, Kendall RS, Humphrey C, Glass RI. Group C rotavirus in a pediatric kidney transplant patient with diarrhea. J Clin Virol 2006; 36:306–308 [View Article][PubMed]
     [Google Scholar]
  28. Tsunemitsu H, Jiang B, Saif LJ. Sequence comparison of the VP7 gene encoding the outer capsid glycoprotein among animal and human group C rotaviruses. Arch Virol 1996; 141:705–713 [View Article][PubMed]
     [Google Scholar]
  29. Mawatari T, Taneichi A, Kawagoe T, Hosokawa M, Togashi K et al. Detection of a bovine group C rotavirus from adult cows with diarrhea and reduced milk production. J Vet Med Sci 2004; 66:887–890 [View Article][PubMed]
     [Google Scholar]
  30. Soma J, Tsunemitsu H, Miyamoto T, Suzuki G, Sasaki T et al. Whole-genome analysis of two bovine rotavirus C strains: Shintoku and Toyama. J Gen Virol 2013; 94:128–135 [View Article][PubMed]
     [Google Scholar]
  31. Mawatari T, Hirano K, Tsunemitsu H, Suzuki T. Whole-genome analysis of bovine rotavirus species C isolates obtained in Yamagata, Japan, 2003-2010. J Gen Virol 2014; 95:1117–1125 [View Article][PubMed]
     [Google Scholar]
  32. Tsunemitsu H, Jiang B, Saif LJ. Detection of group C rotavirus antigens and antibodies in animals and humans by enzyme-linked immunosorbent assays. J Clin Microbiol 1992; 30:2129–2134[PubMed]
     [Google Scholar]
  33. Sigolo de San Juan C, Bellinzoni RC, Mattion N, La Torre J, Scodeller EA. Incidence of group A and atypical rotaviruses in Brazilian pig herds. Res Vet Sci 1986; 41:270–272[PubMed]
     [Google Scholar]
  34. Saif LJ, Jiang B. Nongroup A rotaviruses of humans and animals. Curr Top Microbiol Immunol 1994; 185:339–371[PubMed]
     [Google Scholar]
  35. Kim Y, Chang KO, Straw B, Saif LJ. Characterization of group C rotaviruses associated with diarrhea outbreaks in feeder pigs. J Clin Microbiol 1999; 37:1484–1488[PubMed]
     [Google Scholar]
  36. Martella V, Bányai K, Lorusso E, Bellacicco AL, Decaro N et al. Prevalence of group C rotaviruses in weaning and post-weaning pigs with enteritis. Vet Microbiol 2007; 123:26–33 [View Article][PubMed]
     [Google Scholar]
  37. Marthaler D, Rossow K, Culhane M, Collins J, Goyal S et al. Identification, phylogenetic analysis and classification of porcine group C rotavirus VP7 sequences from the United States and Canada. Virology 2013; 446:189–198 [View Article][PubMed]
     [Google Scholar]
  38. Amimo JO, Vlasova AN, Saif LJ. Prevalence and genetic heterogeneity of porcine group C rotaviruses in nursing and weaned piglets in Ohio, USA and identification of a potential new VP4 genotype. Vet Microbiol 2013; 164:27–38 [View Article][PubMed]
     [Google Scholar]
  39. Suzuki T, Hasebe A, Miyazaki A, Tsunemitsu H. Phylogenetic characterization of VP6 gene (inner capsid) of porcine rotavirus C collected in Japan. Infect Genet Evol 2014; 26:223–227 [View Article][PubMed]
     [Google Scholar]
  40. Suzuki T, Hasebe A, Miyazaki A, Tsunemitsu H. Analysis of genetic divergence among strains of porcine rotavirus C, with focus on VP4 and VP7 genotypes in Japan. Virus Res 2015; 197:26–34 [View Article][PubMed]
     [Google Scholar]
  41. Martella V, Bányai K, Lorusso E, Decaro N, Bellacicco A et al. Genetic heterogeneity in the VP7 of group C rotaviruses. Virology 2007; 367:358–366 [View Article][PubMed]
     [Google Scholar]
  42. Collins PJ, Martella V, O'Shea H. Detection and characterization of group C rotaviruses in asymptomatic piglets in Ireland. J Clin Microbiol 2008; 46:2973–2979 [View Article][PubMed]
     [Google Scholar]
  43. Kuga K, Miyazaki A, Suzuki T, Takagi M, Hattori N et al. Genetic diversity and classification of the outer capsid glycoprotein VP7 of porcine group B rotaviruses. Arch Virol 2009; 154:1785–1795 [View Article][PubMed]
     [Google Scholar]
  44. Jeong YJ, Matthijnssens J, Kim DS, Kim JY, Alfajaro MM et al. Genetic diversity of the VP7, VP4 and VP6 genes of Korean porcine group C rotaviruses. Vet Microbiol 2015; 176:61–69 [View Article][PubMed]
     [Google Scholar]
  45. Moutelíková R, Prodělalová J, Dufková L. Diversity of VP7, VP4, VP6, NSP2, NSP4, and NSP5 genes of porcine rotavirus C: phylogenetic analysis and description of potential new VP7, VP4, VP6, and NSP4 genotypes. Arch Virol 2015; 160:1715–1727 [View Article][PubMed]
     [Google Scholar]
  46. Pesavento JB, Crawford SE, Estes MK, Prasad BV. Rotavirus proteins: structure and assembly. Curr Top Microbiol Immunol 2006; 309:189–219[PubMed]
     [Google Scholar]
  47. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T et al. 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 2008; 82:3204–3219 [View Article][PubMed]
     [Google Scholar]
  48. Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 2008; 153:1621–1629 [View Article][PubMed]
     [Google Scholar]
  49. McDonald SM, Matthijnssens J, Mcallen JK, Hine E, Overton L et al. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog 2009; 5:e1000634 [View Article][PubMed]
     [Google Scholar]
  50. Bremont M, Juste-Lesage P, Chabanne-Vautherot D, Charpilienne A, Cohen J. Sequences of the four larger proteins of a porcine group C rotavirus and comparison with the equivalent group A rotavirus proteins. Virology 1992; 186:684–692 [View Article][PubMed]
     [Google Scholar]
  51. Chen Z, Lambden PR, Lau J, Caul EO, Clarke IN. Human group C rotavirus: completion of the genome sequence and gene coding assignments of a non-cultivatable rotavirus. Virus Res 2002; 83:179–187 [View Article][PubMed]
     [Google Scholar]
  52. Wise AG, Smedley RC, Kiupel M, Maes RK. Detection of group C rotavirus in juvenile ferrets (Mustela putorius furo) with diarrhea by reverse transcription polymerase chain reaction: sequencing and analysis of the complete coding region of the VP6 gene. Vet Pathol 2009; 46:985–991 [View Article][PubMed]
     [Google Scholar]
  53. Lee SG, Youn SH, Oh MH, Rhee OJ, Oh S et al. Molecular characterization of two strains of porcine group C rotavirus. J Microbiol 2011; 49:1058–1062 [View Article][PubMed]
     [Google Scholar]
  54. Yamamoto D, Ghosh S, Kuzuya M, Wang YH, Zhou X et al. Whole-genome characterization of human group C rotaviruses: identification of two lineages in the VP3 gene. J Gen Virol 2011; 92:361–369 [View Article][PubMed]
     [Google Scholar]
  55. Marton S, Mihalov-Kovács E, Dóró R, Csata T, Fehér E et al. Canine rotavirus C strain detected in Hungary shows marked genotype diversity. J Gen Virol 2015; 96:3059–3071 [View Article][PubMed]
     [Google Scholar]
  56. Niira K, Ito M, Masuda T, Saitou T, Abe T et al. Whole genome sequences of Japanese porcine species C rotaviruses reveal a high diversity of genotypes of individual genes and will contribute to a comprehensive, generally accepted classification system. Infect Genet Evol 2016; 44:106–113 [View Article][PubMed]
     [Google Scholar]
  57. Cohen J, Charpilienne A, Chilmonczyk S, Estes MK. Nucleotide sequence of bovine rotavirus gene 1 and expression of the gene product in baculovirus. Virology 1989; 171:131–140 [View Article][PubMed]
     [Google Scholar]
  58. Nagashima S, Kobayashi N, Ishino M, Alam MM, Ahmed MU et al. Whole genomic characterization of a human rotavirus strain B219 belonging to a novel group of the genus Rotavirus. J Med Virol 2008; 80:2023–2033 [View Article][PubMed]
     [Google Scholar]
  59. Cook JP, Mccrae MA. Sequence analysis of the guanylyltransferase (VP3) of group A rotaviruses. J Gen Virol 2004; 85:929–932 [View Article][PubMed]
     [Google Scholar]
  60. Graff JW, Mitzel DN, Weisend CM, Flenniken ML, Hardy ME. Interferon regulatory factor 3 is a cellular partner of rotavirus NSP1. J Virol 2002; 76:9545–9550 [View Article][PubMed]
     [Google Scholar]
  61. Carpio RV, González-Nilo FD, Jayaram H, Spencer E, Prasad BV et al. Role of the histidine triad-like motif in nucleotide hydrolysis by the rotavirus RNA-packaging protein NSP2. J Biol Chem 2004; 279:10624–10633 [View Article][PubMed]
     [Google Scholar]
  62. Suzuki T, Soma J, Kuga K, Miyazaki A, Tsunemitsu H. Sequence and phylogenetic analyses of nonstructural protein 2 genes of species B porcine rotaviruses detected in Japan during 2001-2009. Virus Res 2012; 165:46–51 [View Article][PubMed]
     [Google Scholar]
  63. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000953
Loading
A provisional complete genome-based genotyping system for rotavirus species C from terrestrial mammals
J. Gen. Virol. 98, 2647 (2017); https://doi.org/10.1099/jgv.0.000953
/content/journal/jgv/10.1099/jgv.0.000953
/content/journal/jgv/10.1099/jgv.0.000953
Loading

Data & Media loading...

Supplements

Supplementary File 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