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Archives of Virology

, Volume 155, Issue 2, pp 159–167 | Cite as

Molecular characterization of the VP1, VP2, VP4, VP6, NSP1 and NSP2 genes of bovine group B rotaviruses: identification of a novel VP4 genotype

  • Souvik GhoshEmail author
  • N. Kobayashi
  • S. Nagashima
  • M. Chawla-Sarkar
  • T. Krishnan
  • B. Ganesh
  • T. N. Naik
Original Article

Abstract

Studies on bovine group B rotaviruses (GBRs) are limited. To date, only the VP6 gene of a single bovine GBR strain and the VP7 and NSP5 genes of a few bovine GBR strains have been sequenced and analyzed. In the present study, using a single-primer amplification method, we have determined the full-length nucleotide sequences of the VP1, VP2, VP4, VP6, NSP1 and NSP2 genes of three bovine GBR strains from eastern India. In all six of these genes, the bovine GBR strains shared high genetic relatedness among themselves but exhibited high genetic diversity with cognate genes of human, murine and ovine GBRs. Interestingly, as with group A rotaviruses, the bovine GBR VP1, VP2, VP6 and NSP2 genes appeared to be more conserved than the VP4 and NSP1 genes among strains of different species. The present study provides important insights into the genetic makeup and diversity of bovine GBRs, and also identifies a novel GBR VP4 genotype.

Keywords

NSP2 Gene Strain DB176 Sequence Identity Cutoff Strain KB63 High Genetic Relatedness 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The study was supported in part by a Grant-in-aid for scientific research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grant number 20-08463) and the Program of Founding Research Centers for Emerging and Reemerging Infectious Diseases (Okayama University-National Institute of Cholera and Enteric Diseases, India).

Supplementary material

705_2009_555_MOESM1_ESM.pdf (280 kb)
Supplementary material 1 (PDF 280 kb)

References

  1. 1.
    Alam MM, Kobayashi N, Ishino M, Ahmed MS, Ahmed MU, Paul SK, Muzumdar BK, Hussain Z, Wang YH, Naik TN (2007) Genetic analysis of an ADRV-N-like novel rotavirus strain B219 detected in a sporadic case of adult diarrhea in Bangladesh. Arch Virol 152:199–208CrossRefPubMedGoogle Scholar
  2. 2.
    Barman P, Ghosh S, Das S, Varghese V, Chaudhuri S, Sarkar S, Krishnan T, Bhattacharya SK, Chakrabarti A, Naik TN (2004) Sequencing and sequence analysis of VP7 and NSP5 genes reveal emergence of a new genotype of bovine group B rotaviruses in India. J Clin Microbiol 42:2816–2818CrossRefPubMedGoogle Scholar
  3. 3.
    Barman P, Ghosh S, Samajdar S, Mitra U, Dutta P, Bhattacharya SK, Krishnan T, Kobayashi N, Naik TN (2006) RT-PCR based diagnosis revealed importance of human group B rotavirus infection in childhood diarrhoea. J Clin Virol 36:222–227CrossRefPubMedGoogle Scholar
  4. 4.
    Brown DW, Beards GM, Chen GM, Flewett TH (1987) Prevalence of antibody to group B (atypical) rotavirus in humans and animals. J Clin Microbiol 25:316–319PubMedGoogle Scholar
  5. 5.
    Chang KO, Parwani AV, Smith D, Saif LJ (1997) Detection of group B rotaviruses in fecal samples from diarrheic calves and adult cows and characterization of their VP7 genes. J Clin Microbiol 35:2107–2110PubMedGoogle Scholar
  6. 6.
    Cohen J, Charpilienne A, Chilmonczyk S, Estes MK (1989) Nucleotide sequence of bovine rotavirus gene 1 and expression of the gene product in baculovirus. Virology 171:131–140CrossRefPubMedGoogle Scholar
  7. 7.
    Dunn SJ, Cross TL, Greenberg HB (1994) Comparison of the rotavirus nonstructural protein NSP1 (NS53) from different species by sequence analysis and northern blot hybridization. Virology 203:178–183CrossRefPubMedGoogle Scholar
  8. 8.
    Estes MK, Kapikian AZ (2007) Rotaviruses and their replication. In: Fields BN, Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (eds) Fields virology, 5th edn. Lippincott, Williams & Wilkins, Philadelphia, pp 1917–1974Google Scholar
  9. 9.
    Gabbay YB, Borges AA, Oliveira DS, Linhares AC, Mascarenhas JD, Barardi CR, Simões CM, Wang Y, Glass RI, Jiang B (2008) Evidence for zoonotic transmission of group C rotaviruses among children in Belém, Brazil. J Med Virol 80:1666–1674CrossRefPubMedGoogle Scholar
  10. 10.
    Ghosh S, Varghese V, Sinha M, Kobayashi N, Naik TN (2007) Evidence for interstate transmission and increase in prevalence of bovine group B rotavirus strains with a novel VP7 genotype among diarrhoeic calves in Eastern and Northern states of India. Epidemiol Infect 135:1324–1330CrossRefPubMedGoogle Scholar
  11. 11.
    Gorziglia M, Green K, Nishikawa K, Taniguchi K, Jones R, Kapikian AZ, Chanock RM (1988) Sequence of the fourth gene of human rotaviruses recovered from asymptomatic or symptomatic infections. J Virol 62:2978–2984PubMedGoogle Scholar
  12. 12.
    Heiman EM, McDonald SM, Barro M, Taraporewala ZF, Bar-Magen T, Patton JT (2008) Group A human rotavirus genomics: evidence that gene constellations are influenced by viral protein interactions. J Virol 82:11106–11116CrossRefPubMedGoogle Scholar
  13. 13.
    Hua J, Mansell EA, Patton JT (1993) Comparative analysis of the rotavirus NS53 gene: conservation of basic and cysteine-rich regions in the protein and possible stem-loop structures in the RNA. Virology 196:372–378CrossRefPubMedGoogle Scholar
  14. 14.
    Jiang B, Gentsch JR, Tsunemitsu H, Saif LJ, Glass RI (1999) Sequence analysis of the gene encoding VP4 of a bovine group C rotavirus: molecular evidence for a new P genotype. Virus Genes 19:85–88CrossRefPubMedGoogle Scholar
  15. 15.
    Jiang S, Ji S, Tang Q, Cui X, Yang H, Kan B, Gao S (2008) Molecular characterization of a novel adult diarrhoea rotavirus strain J19 isolated in China and its significance for the evolution and origin of group B rotaviruses. J Gen Virol 89:2622–2629CrossRefPubMedGoogle Scholar
  16. 16.
    Kobayashi N, Alam M, Kojima K, Mise K, Ishino M, Sumi A (2003) Genomic diversity and evolution of rotaviruses: an overview. In: Kobayashi N (ed) Genomic diversity and molecular epidemiology of rotaviruses. Research Signpost, Trivandrum, pp 75–90Google Scholar
  17. 17.
    Kobayashi N, Naik TN, Ahmed MU (2003) Genomic diversity and molecular evolution of group B human rotaviruses. In: Kobayashi N (ed) Genomic diversity and molecular epidemiology of rotaviruses. Research Signpost, Trivandrum, pp 91–104Google Scholar
  18. 18.
    Kobayashi N, Naik TN, Kusuhara Y, Krishnan T, Sen A, Bhattacharya SK, Taniguchi K, Alam MM, Urasawa T, Urasawa S (2001) Sequence analysis of genes encoding structural and nonstructural proteins of a human group B rotavirus detected in Calcutta, India. J Med Virol 64:583–588CrossRefPubMedGoogle Scholar
  19. 19.
    Kojima K, Taniguchi K, Kobayashi N (1996) Species-specific and interspecies relatedness of NSP1 sequences in human, porcine, bovine, feline, and equine rotavirus strains. Arch Virol 141:1–12CrossRefPubMedGoogle Scholar
  20. 20.
    Lawton JA, Zeng CQ, Mukherjee SK, Cohen J, Estes MK, Prasad BV (1997) Three-dimensional structural analysis of recombinant rotavirus-like particles with intact and amino-terminal-deleted VP2: implications for the architecture of the VP2 capsid layer. J Virol 71:7353–7360PubMedGoogle Scholar
  21. 21.
    Mackow ER (1995) Group B and C rotaviruses. In: Blaser MJ, Smith PD, Ravdin JI, Greenberg HB, Guerrant RL (eds) Infections of the gastrointestinal tract. Raven Press Ltd, New York, pp 983–1008Google Scholar
  22. 22.
    Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gómara M, Maes P, Patton JT, Rahman M, Van Ranst M (2008) 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 82:3204–3219CrossRefPubMedGoogle Scholar
  23. 23.
    McDonald SM, Patton JT (2008) Molecular characterization of a subgroup specificity associated with the rotavirus inner capsid protein VP2. J Virol 82:2752–2764CrossRefPubMedGoogle Scholar
  24. 24.
    McDonald SM, Aguayo D, Gonzalez-Nilo FD, Patton JT (2009) Shared and group-specific features of the rotavirus RNA polymerase reveal potential determinants of gene reassortment restriction. J Virol 83:6135–6148CrossRefPubMedGoogle Scholar
  25. 25.
    Nagashima S, Kobayashi N, Ishino M, Alam MM, Ahmed MU, Paul SK, Ganesh B, Chawla-Sarkar M, Krishnan T, Naik TN, Wang YH (2008) Whole genomic characterization of a human rotavirus strain B219 belonging to a novel group of the genus Rotavirus. J Med Virol 80:2023–2033CrossRefPubMedGoogle Scholar
  26. 26.
    Prasad BV, Rothnagel R, Zeng CQ, Jakana J, Lawton JA, Chiu W, Estes MK (1996) Visualization of ordered genomic RNA and localization of transcriptional complexes in rotavirus. Nature 382:471–473CrossRefPubMedGoogle Scholar
  27. 27.
    Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  28. 28.
    Sanekata T, Kuwamoto Y, Akamatsu S, Sakon N, Oseto M, Taniguchi K, Nakata S, Estes MK (1996) Isolation of group B porcine rotavirus in cell culture. J Clin Microbiol 34:759–761PubMedGoogle Scholar
  29. 29.
    Schumann T, Hotzel H, Otto P, Johne R (2009) Evidence of interspecies transmission and reassortment among avian group A rotaviruses. Virology 386:334–343CrossRefPubMedGoogle Scholar
  30. 30.
    Sereno MM, Gorziglia M (1994) The outer capsid protein VP4 of murine rotavirus strain Eb represents a tentative new P type. Virology 199:500–504CrossRefPubMedGoogle Scholar
  31. 31.
    Shen S, McKee TA, Wang ZD, Desselberger U, Liu DX (1999) Sequence analysis and in vitro expression of genes 6 and 11 of an ovine group B rotavirus isolate, KB63: evidence for a non-defective, C-terminally truncated NSP1 and a phosphorylated NSP5. J Gen Virol 80:2077–2085PubMedGoogle Scholar
  32. 32.
    Snodgrass DR, Herring AJ, Campbell I, Inglis JM, Hargreaves FD (1984) Comparison of atypical rotaviruses from calves, piglets, lambs and man. J Gen Virol 65:909–914CrossRefPubMedGoogle Scholar
  33. 33.
    Tsunemitsu H, Kamiyama M, Kawashima K, Katsuda K, Kohmoto M, Saif LJ, Shouji T, Onodera T (2005) Molecular characterization of the major capsid protein VP6 of bovine group B rotavirus and its use in seroepidemiology. J Gen Virol 86:2569–2575CrossRefPubMedGoogle Scholar
  34. 34.
    Tsunemitsu H, Morita D, Takaku H, Nishimori T, Imai K, Saif LJ (1999) First detection of bovine group B rotavirus in Japan and sequence of its VP7 gene. Arch Virol 144:805–815CrossRefPubMedGoogle Scholar
  35. 35.
    Vonderfecht SL, Lindsay DA, Eiden JJ (1994) Detection of rat, porcine, and bovine group B rotavirus in fecal specimens by solid-phase enzyme immunoassay. J Clin Microbiol 32:1107–1108PubMedGoogle Scholar
  36. 36.
    Wakuda M, Pongsuwanna Y, Taniguchi K (2005) Complete nucleotide sequences of two RNA segments of human picobirnavirus. J Virol Methods 126:165–169CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Souvik Ghosh
    • 1
    Email author
  • N. Kobayashi
    • 1
  • S. Nagashima
    • 2
  • M. Chawla-Sarkar
    • 3
  • T. Krishnan
    • 3
  • B. Ganesh
    • 3
  • T. N. Naik
    • 4
  1. 1.Department of HygieneSapporo Medical University School of MedicineSapporoJapan
  2. 2.Division of Virology, Department of Infection and ImmunityJichi Medical University School of MedicineTochigiJapan
  3. 3.Division of VirologyNational Institute of Cholera and Enteric DiseasesKolkataIndia
  4. 4.School of BiologyNational Institute of Science Education and ResearchBhubaneswarIndia

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