1887

Journal of General Virology header logo

Volume 92, Issue 4

Whole genome characterization of new bovine rotavirus G21P[29] and G24P[33] strains provides evidence for interspecies transmission Free

Abstract

We have reported a novel bovine rotavirus, the AzuK-1 (G21P[29]) strain, isolated from an asymptomatic calf. We isolated another bovine rotavirus, the Dai-10 strain, bearing new G24P[33] genotypes, assigned by the Rotavirus Classification Working Group (RCWG), from an asymptomatic cow in Hyogo Prefecture, Japan in 2007. To gain an insight into the origins and evolution of these strains, we determined the complete ORF sequences of all 11 genes of the two strains. The NSP3 genes of both strains were confirmed to belong to a new NSP3 genotype, T9, by the RCWG. Genotype determination of AzuK-1 and Dai-10 strains revealed that eight gene segments of both strains possessed genotypes typically observed in bovine rotaviruses, with the exception of VP4, VP7 and NSP3 gene segments. Unexpectedly, phylogenetic analyses showed that VP6 and NSP2 gene segments of the AzuK-1 and Dai-10 strains were clustered with those of simian or canine/feline rotaviruses, rather than with those of bovine rotaviruses. These findings indicate the possibility that both strains originated by interspecies transmission and multiple reassortment events involving bovine, simian and canine/feline rotaviruses, resulting in the introduction of some genes into the genetic background of bovine rotaviruses.

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

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.028175-0
2011-04-01
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/4/952.html?itemId=/content/journal/jgv/10.1099/vir.0.028175-0&mimeType=html&fmt=ahah

References

  1. Abe, M., Ito, N., Morikawa, S., Takasu, M., Murase, T., Kawashima, T., Kawai, Y., Kohara, J. & Sugiyama, M.(2009). Molecular epidemiology of rotaviruses among healthy calves in Japan: isolation of a novel bovine rotavirus bearing new P and G genotypes. Virus Res 144, 250–257.[CrossRef] [Google Scholar]
  2. Abe, M., Yamasaki, A., Ito, N., Mizoguchi, T., Asano, M., Okano, T. & Sugiyama, M.(2010). Molecular characterization of rotaviruses in a Japanese raccoon dog (Nyctereutes procyonoides) and a masked palm civet (Paguma larvata) in Japan. Vet Microbiol 146, 253–259.[CrossRef] [Google Scholar]
  3. Bányai, K., Esona, M. D., Kerin, T. K., Hull, J. J., Mijatovic, S., Vásconez, N., Torres, C., de Filippis, A. M., Foytich, K. R. & Gentsch, J. R.(2009). Molecular characterization of a rare, human-porcine reassortant rotavirus strain, G11P[6], from Ecuador. Arch Virol 154, 1823–1829.[CrossRef] [Google Scholar]
  4. Blackhall, J., Bellinzoni, R., Mattion, N., Estes, M. K., La Torre, J. L. & Magnusson, G.(1992). A bovine rotavirus serotype 1: serologic characterization of the virus and nucleotide sequence determination of the structural glycoprotein VP7 gene. Virology 189, 833–837.[CrossRef] [Google Scholar]
  5. Collins, P. J., Martella, V., Buonavoglia, C. & O'Shea, H.(2010). Identification of a G2-like porcine rotavirus bearing a novel VP4 type, P[32]. Vet Res 41, 73.[CrossRef] [Google Scholar]
  6. Dhama, K., Chauhan, R. S., Mahendran, M. & Malik, S. V.(2009). Rotavirus diarrhea in bovines and other domestic animals. Vet Res Commun 33, 1–23. [Google Scholar]
  7. El-Attar, L., Dhaliwal, W., Iturriza-Gómara, M. & Bridger, J. C.(2002). Identification and molecular characterization of a bovine G3 rotavirus which causes age-independent diarrhea in cattle. J Clin Microbiol 40, 937–942.[CrossRef] [Google Scholar]
  8. Esona, M. D., Geyer, A., Banyai, K., Page, N., Aminu, M., Armah, G. E., Hull, J., Steele, D. A., Glass, R. I. & Gentsch, J. R.(2009). Novel human rotavirus genotype G5P[7] from child with diarrhea, Cameroon. Emerg Infect Dis 15, 83–86.[CrossRef] [Google Scholar]
  9. Esona, M. D., Mijatovic-Rustempasic, S., Conrardy, C., Tong, S., Kuzmin, I. V., Agwanda, B., Breiman, R. F., Banyai, K., Niezgoda, M. & other authors(2010). Reassortant group A rotavirus from straw-colored fruit bat (Eidolon helvum). Emerg Infect Dis 16, 1844–1852.[CrossRef] [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. : Lippincott, Williams & Wilkins. [Google Scholar]
  11. Fukai, K., Saito, T., Inoue, K. & Sato, M.(2004). Molecular characterization of novel P[14],G8 bovine group A rotavirus, Sun9, isolated in Japan. Virus Res 105, 101–106.[CrossRef] [Google Scholar]
  12. Ghosh, S., Varghese, V., Samajdar, S., Sinha, M., Naik, T. N. & Kobayashi, N.(2007). Evidence for bovine origin of VP4 and VP7 genes of human group A rotavirus G6P[14] and G10P[14] strains. J Clin Microbiol 45, 2751–2753.[CrossRef] [Google Scholar]
  13. Ghosh, S., Samajdar, S., Sinha, M., Kobayashi, N., Taniguchi, K. & Naik, T. N.(2008). Molecular characterization of rare bovine group A rotavirus G15P[11] and G15P[21] strains from eastern India: identification of simian SA11-like VP6 genes in G15P[21] strains. Virus Genes 37, 241–249.[CrossRef] [Google Scholar]
  14. Ghosh, S., Kobayashi, N., Nagashima, S., Chawla-Sarkar, M., Krishnan, T., Ganesh, B. & Naik, T. N.(2010). Full genomic analysis and possible origin of a porcine G12 rotavirus strain RU172. Virus Genes 40, 382–388.[CrossRef] [Google Scholar]
  15. Graham, K. L., Halasz, P., Tan, Y., Hewish, M. J., Takada, Y., Mackow, E. R., Robinson, M. K. & Coulson, B. S.(2003). Integrin-using rotaviruses bind α2β1 integrin α2 I domain via VP4 DGE sequence and recognize αXβ2 and αVβ3 by using VP7 during cell entry. J Virol 77, 9969–9978.[CrossRef] [Google Scholar]
  16. Hussein, H. A., Parwani, A. V., Rosen, B. I., Lucchelli, A. & Saif, L. J.(1993). Detection of rotavirus serotypes G1, G2, G3, and G11 in feces of diarrheic calves by using polymerase chain reaction-derived cDNA probes. J Clin Microbiol 31, 2491–2496. [Google Scholar]
  17. Isegawa, Y., Nakagomi, O., Brüssow, H., Minamoto, N., Nakagomi, T. & Ueda, S.(1994). A unique VP4 gene allele carried by an unusual bovine rotavirus strain, 993/83. Virology 198, 366–369.[CrossRef] [Google Scholar]
  18. Lamhoujeb, S., Cook, A., Pollari, F., Bidawid, S., Farber, J. & Mattison, K.(2010). Rotaviruses from Canadian farm samples. Arch Virol 155, 1127–1137.[CrossRef] [Google Scholar]
  19. López, S. & Arias, C. F.(2004). Multistep entry of rotavirus into cells: a Versaillesque dance. Trends Microbiol 12, 271–278.[CrossRef] [Google Scholar]
  20. Maes, P., Matthijnssens, J., Rahman, M. & Van Ranst, M.(2009). RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol 9, 238.[CrossRef] [Google Scholar]
  21. Martella, V., Ciarlet, M., Bányai, K., Lorusso, E., Cavalli, A., Corrente, M., Elia, G., Arista, S., Camero, M. & Desario, C.(2006). Identification of a novel VP4 genotype carried by a serotype G5 porcine rotavirus strain. Virology 346, 301–311.[CrossRef] [Google Scholar]
  22. Martella, V., Ciarlet, M., Bányai, K., Lorusso, E., Arista, S., Lavazza, A., Pezzotti, G., Decaro, N., Cavalli, A. & other authors(2007). Identification of group A porcine rotavirus strains bearing a novel VP4 (P) genotype in Italian swine herds. J Clin Microbiol 45, 577–580.[CrossRef] [Google Scholar]
  23. Martella, V., Bányai, K., Matthijnssens, J., Buonavoglia, C. & Ciarlet, M.(2010). Zoonotic aspects of rotaviruses. Vet Microbiol 140, 246–255.[CrossRef] [Google Scholar]
  24. Matthijnssens, J., Rahman, M., Martella, V., Xuelei, Y., De Vos, S., De Leener, K., Ciarlet, M., Buonavoglia, C. & Van Ranst, M.(2006). Full genomic analysis of human rotavirus strain B4106 and lapine rotavirus strain 30/96 provides evidence for interspecies transmission. J Virol 80, 3801–3810.[CrossRef] [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(2008a). 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.[CrossRef] [Google Scholar]
  26. Matthijnssens, J., Ciarlet, M., Rahman, M., Attoui, H., Bányai, K., Estes, M. K., Gentsch, J. R., Iturriza-Gómara, M., Kirkwood, C. D. & other authors(2008b). Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 153, 1621–1629.[CrossRef] [Google Scholar]
  27. Matthijnssens, J., Rahman, M. & Van Ranst, M.(2008c). Two out of the 11 genes of an unusual human G6P[6] rotavirus isolate are of bovine origin. J Gen Virol 89, 2630–2635.[CrossRef] [Google Scholar]
  28. Matthijnssens, J., Potgieter, C. A., Ciarlet, M., Parreño, V., Martella, V., Bányai, K., Garaicoechea, L., Palombo, E. A., Novo, L. & other authors(2009). Are human P[14] rotavirus strains the result of interspecies transmissions from sheep or other ungulates that belong to the mammalian order Artiodactyla? J Virol 83, 2917–2929.[CrossRef] [Google Scholar]
  29. Matthijnssens, J., Rahman, M., Ciarlet, M., Zeller, M., Heylen, E., Nakagomi, T., Uchida, R., Hassan, Z., Azim, T. & other authors(2010a). Reassortment of human rotavirus gene segments into G11 rotavirus strains. Emerg Infect Dis 16, 625–630.[CrossRef] [Google Scholar]
  30. Matthijnssens, J., Taraporewala, Z. F., Yang, H., Rao, S., Yuan, L., Cao, D., Hoshino, Y., Mertens, P. P., Carner, G. R. & other authors(2010b). Simian rotaviruses possess divergent gene constellations that originated from interspecies transmission and reassortment. J Virol 84, 2013–2026.[CrossRef] [Google Scholar]
  31. McNeal, M. M., Sestak, K., Choi, A. H., Basu, M., Cole, M. J., Aye, P. P., Bohm, R. P. & Ward, R. L.(2005). Development of a rotavirus-shedding model in rhesus macaques, using a homologous wild-type rotavirus of a new P genotype. J Virol 79, 944–954.[CrossRef] [Google Scholar]
  32. McNulty, M. S. & Logan, E. F.(1983). Longitudinal survey of rotavirus infection in calves. Vet Rec 113, 333–335.[CrossRef] [Google Scholar]
  33. Mukherjee, A., Dutta, D., Ghosh, S., Bagchi, P., Chattopadhyay, S., Nagashima, S., Kobayashi, N., Dutta, P., Krishnan, T. & other authors(2009). Full genomic analysis of a human group A rotavirus G9P[6] strain from Eastern India provides evidence for porcine-to-human interspecies transmission. Arch Virol 154, 733–746.[CrossRef] [Google Scholar]
  34. Palombo, E. A.(2002). Genetic analysis of Group A rotaviruses: evidence for interspecies transmission of rotavirus genes. Virus Genes 24, 11–20.[CrossRef] [Google Scholar]
  35. Parashar, U. D., Gibson, C. J., Bresse, J. S. & Glass, R. I.(2006). Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12, 304–306.[CrossRef] [Google Scholar]
  36. Park, S. H., Saif, L. J., Jeong, C., Lim, G. K., Park, S. I., Kim, H. H., Park, S. J., Kim, Y. J., Jeong, J. H. & other authors(2006). Molecular characterization of novel G5 bovine rotavirus strains. J Clin Microbiol 44, 4101–4112.[CrossRef] [Google Scholar]
  37. Parra, G. I., Galeano, M. E. & Arbiza, J.(2007). Genetic relationship between porcine rotavirus strains bearing a new P-type. Vet Microbiol 125, 193–195.[CrossRef] [Google Scholar]
  38. Parra, G. I., Vidales, G., Gomez, J. A., Fernandez, F. M., Parreño, V. & Bok, K.(2008). Phylogenetic analysis of porcine rotavirus in Argentina: increasing diversity of G4 strains and evidence of interspecies transmission. Vet Microbiol 126, 243–250.[CrossRef] [Google Scholar]
  39. Rahman, M., Matthijnssens, J., Nahar, S., Podder, G., Sack, D. A., Azim, T. & Van Ranst, M.(2005). Characterization of a novel P[25],G11 human group a rotavirus. J Clin Microbiol 43, 3208–3212.[CrossRef] [Google Scholar]
  40. Ramig, R. F.(1997). Genetics of the rotaviruses. Annu Rev Microbiol 51, 225–255.[CrossRef] [Google Scholar]
  41. Rao, C. D., Gowda, K. & Reddy, B. S.(2000). Sequence analysis of VP4 and VP7 genes of nontypeable strains identifies a new pair of outer capsid proteins representing novel P and G genotypes in bovine rotaviruses. Virology 276, 104–113.[CrossRef] [Google Scholar]
  42. Reynolds, D. J., Hall, G. A., Debney, T. G. & Parsons, K. R.(1985). Pathology of natural rotavirus infection in clinically normal calves. Res Vet Sci 38, 264–269. [Google Scholar]
  43. Schumann, T., Hotzel, H., Otto, P. & Johne, R.(2009). Evidence of interspecies transmission and reassortment among avian group A rotaviruses. Virology 386, 334–343.[CrossRef] [Google Scholar]
  44. Solberg, O. D., Hasing, M. E., Trueba, G. & Eisenberg, J. N.(2009). Characterization of novel VP7, VP4, and VP6 genotypes of a previously untypeable group A rotavirus. Virology 385, 58–67.[CrossRef] [Google Scholar]
  45. Steyer, A., Poljsak-Prijatelj, M., Barlic-Maganja, D. & Marin, J.(2008). Human, porcine and bovine rotaviruses in Slovenia: evidence of interspecies transmission and genome reassortment. J Gen Virol 89, 1690–1698.[CrossRef] [Google Scholar]
  46. Swiatek, D. L., Palombo, E. A., Lee, A., Coventry, M. J., Britz, M. L. & Kirkwood, C. D.(2010). Detection and analysis of bovine rotavirus strains circulating in Australian calves during 2004 and 2005. Vet Microbiol 140, 56–62.[CrossRef] [Google Scholar]
  47. Tamura, K., Dudley, J., Nei, M. & Kumar, S.(2007).mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef] [Google Scholar]
  48. Tsugawa, T. & Hoshino, Y.(2008). Whole genome sequence and phylogenetic analyses reveal human rotavirus G3P[3] strains Ro1845 and HCR3A are examples of direct virion transmission of canine/feline rotaviruses to humans. Virology 380, 344–353.[CrossRef] [Google Scholar]
  49. Ursu, K., Kisfali, P., Rigó, D., Ivanics, E., Erdélyi, K., Dán, A., Melegh, B., Martella, V. & Bányai, K.(2009). Molecular analysis of the VP7 gene of pheasant rotaviruses identifies a new genotype, designated G23. Arch Virol 154, 1365–1369.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.028175-0
Loading
Whole genome characterization of new bovine rotavirus G21P[29] and G24P[33] strains provides evidence for interspecies transmission
J. Gen. Virol. 92, 952 (2011); https://doi.org/10.1099/vir.0.028175-0
/content/journal/jgv/10.1099/vir.0.028175-0
/content/journal/jgv/10.1099/vir.0.028175-0
Loading

Data & Media loading...

Supplements

vol. , part 4, pp. 952 - 960

Multiple alignment of amino acid sequences of the VP6 gene of AzuK-1, Dai-10, SA11-H96 and other bovine ARV strains

Oligonucleotide primers used in this study [Single PDF file](64 KB)

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