Detection of substantial porcine group B rotavirus genetic diversity in the United States, resulting in a modified classification proposal for G genotypes

Virology

Volumn 433, Issue 1, 2012, Pages 85-96

  Marthaler, Douglas ^a   Rossow, Kurt ^a   Gramer, Marie ^a   Collins, James ^a   Goyal, Sagar ^a   Tsunemitsu, Hiroshi ^b   Kuga, Kazufumi ^b   Suzuki, Tohru ^b   Ciarlet, Max ^c   Matthijnssens, Jelle ^d  

^a UNIVERSITY OF MINNESOTA   (United States)

^b NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^c Novartis Vaccines and Diagnostics Inc   (United States)

^d REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

Classification; Gastrointestinal disease; Genotype; Phylogenetic analysis; Porcine enteric disease; Rotavirus group A; Rotavirus group B; Rotavirus group C; VP7

Indexed keywords

NUCLEOTIDE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; HISTOPATHOLOGY; MIXED INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PORCINE GROUP A ROTAVIRUS; PORCINE GROUP B ROTAVIRUS; PORCINE GROUP C ROTAVIRUS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAVIRUS; ROTAVIRUS INFECTION; UNITED STATES; VIRUS DETECTION; VIRUS GENE; VIRUS IDENTIFICATION; VIRUS STRAIN; VP7 GENE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, VIRAL; CAPSID PROTEINS; COINFECTION; DIARRHEA; GENETIC VARIATION; GENOTYPE; HUMANS; INTESTINE, SMALL; MOLECULAR SEQUENCE DATA; MOLECULAR TYPING; PHYLOGENY; ROTAVIRUS; ROTAVIRUS INFECTIONS; SWINE; SWINE DISEASES; UNITED STATES;

ANIMALIA; ROTAVIRUS; ROTAVIRUS A; ROTAVIRUS B; ROTAVIRUS C; SUIDAE; SUS;

EID: 84866160788     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.07.006     Document Type: Article

References (56)

1. Ahmed M.U., Kobayashi N., Wakuda M., Sanekata T., Taniguchi K., Kader A., Naik T.N., Ishino M., Alam M.M., Kojima K., Mise K., Sumi A. Genetic analysis of group B human rotaviruses detected in Bangladesh in 2000 and 2001. J. Med. Virol. 2004, 72:149-155.
2. Ball L. The universal taxonomy of viruses in theory and practice. Virus Taxonomy: Classification and Nomenclature of Viruses: Eighth Report of the International Committee on the Taxonomy of Viruses 2005, 3-8. Elsevier, Academic Press, Amsterdam; Boston. C. Fauquet, M. Mayo, J. Maniloff, U. Desselberger, L. Ball (Eds.).
3. Barman P., Ghosh S., Das S., Varghese V., Chaudhuri S., Sarkar S., Krishnan T., Bhattacharya S.K., Chakrabarti A., Kobayashi N., Naik T.N. 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. 2004, 42:2816-2818.
4. Both G.W., Bellamy A.R., Mitchell D.B. Rotavirus protein structure and function. Curr. Top. Microbiol. Immunol. 1994, 185:67-105.
5. Bridger J.C. Non-group A rotaviruses. Viral Infections of the Gastrointestinal Tract 1994, 369-407. Marcel Dekker, New York. 2nd edn. A.Z. Kapikian (Ed.).
6. Bridger J.C., Brown J.F. Prevalence of antibody to typical and atypical rotaviruses in pigs. Vet. Rec. 1985, 116:50.
7. Chang K.O., Parwani A.V., Smith D., Saif L.J. Detection of group B rotaviruses in fecal samples from diarrheic calves and adult cows and characterization of their VP7 genes. J. Clin. Microbiol. 1997, 35:2107-2110.
8. Chasey D., Bridger J.C., McCrae M.A. A new type of atypical rotavirus in pigs. Arch. Virol. 1986, 89:235-243.
9. Chen G.M., Hung T., Mackow E.R. Identification of the gene encoding the group B rotavirus VP7 equivalent: primary characterization of the ADRV segment 9 RNA. Virology 1990, 178:311-315.
10. Collins P.J., Martella V., O'Shea H. Detection and characterization of group C rotaviruses in asymptomatic piglets in Ireland. J. Clin. Microbiol. 2008, 46:2973-2979.
11. Dai G.Z., Sun M.S., Liu S.Q., Ding X.F., Chen Y.D., Wang L.C., Du D.P., Zhao G., Su Y., Li J. First report of an epidemic of diarrhoea in human neonates involving the new rotavirus and biological characteristics of the epidemic virus strain (KMB/R85). J. Med. Virol. 1987, 22:365-373.
12. de Villiers E.M., Fauquet C., Broker T.R., Bernard H.U., zur Hausen H. Classification of papillomaviruses. Virology 2004, 324:17-27.
13. Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., Wilson, A., 2011. Geneious v5.4, Available from: http://www.geneious.com/.
14. Eiden J.J., Nataro J., Vonderfecht S., Petric M. Molecular cloning, sequence analysis, in vitro expression, and immunoprecipitation of the major inner capsid protein of the IDIR strain of group B rotavirus (GBR). Virology 1992, 188:580-589.
15. Estes M.K. Rotaviruses. Fields' virology 2007, 1917-1974. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia. D. Knipe, P. Howley, D. Griffin, R. Lamb, M. Martin, B. Roizman, S. Straus (Eds.).
16. Fang Z.Y., Ye Q., Ho M.S., Dong H., Qing S., Penaranda M.E., Hung T., Wen L., Glass R.I. Investigation of an outbreak of adult diarrhea rotavirus in China. J. Infect. Dis. 1989, 160:948-953.
17. Ghosh S., Varghese V., Sinha M., Kobayashi N., Naik T.N. 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. 2007, 135:1324-1330.
18. Green K.Y., Sears J.F., Taniguchi K., Midthun K., Hoshino Y., Gorziglia M., Nishikawa K., Urasawa S., Kapikian A.Z., Chanock R.M. Prediction of human rotavirus serotype by nucleotide sequence analysis of the VP7 protein gene. J. Virol. 1988, 62:1819-1823.
19. Hoshino Y., Saif L.J., Sereno M.M., Chanock R.M., Kapikian A.Z. Infection immunity of piglets to either VP3 or VP7 outer capsid protein confers resistance to challenge with a virulent rotavirus bearing the corresponding antigen. J. Virol. 1988, 62:744-748.
20. Hung T., Chen G.M., Wang C.G., Yao H.L., Fang Z.Y., Chao T.X., Chou Z.Y., Ye W., Chang X.J., Den S.S. Waterborne outbreak of rotavirus diarrhoea in adults in China caused by a novel rotavirus. Lancet 1984, 1:1139-1142.
21. Janke B.H., Nelson J.K., Benfield D.A., Nelson E.A. Relative prevalence of typical and atypical strains among rotaviruses from diarrheic pigs in conventional swine herds. J. Vet. Diagn. Invest. 1990, 2:308-311.
22. Kelkar S.D., Zade J.K. Group B rotaviruses similar to strain CAL-1, have been circulating in Western India since 1993. Epidemiol. Infect. 2004, 132:745-749.
23. Kobayashi N., Naik T.N., Kusuhara Y., Krishnan T., Sen A., Bhattacharya S.K., Taniguchi K., Alam M.M., Urasawa T., Urasawa S. Sequence analysis of genes encoding structural and nonstructural proteins of a human group B rotavirus detected in Calcutta, India. J. Med. Virol. 2001, 64:583-588.
24. Kuga K., Miyazaki A., Suzuki T., Takagi M., Hattori N., Katsuda K., Mase M., Sugiyama M., Tsunemitsu H. Genetic diversity and classification of the outer capsid glycoprotein VP7 of porcine group B rotaviruses. Arch.Virol. 2009, 154:1785-1795.
25. Lahon A., Chitambar S.D. Molecular characterization of VP4, VP6, VP7 and NSP4 genes of group B rotavirus strains from outbreaks of gastroenteritis. Asian Pac. J. Trop. Med. 2011, 4:846-849.
26. Lee S.G., Youn S.H., Oh M.H., Rhee O.J., Oh S., Paik S.Y. Molecular characterization of two strains of porcine group C rotavirus. J. Microbiol. 2011, 49:1058-1062.
27. Maes P., Klempa B., Clement J., Matthijnssens J., Gajdusek D.C., Kruger D.H., Van Ranst M. A proposal for new criteria for the classification of hantaviruses, based on S and M segment protein sequences. Infect. Genet. Evol. 2009, 9:813-820.
28. Martella V., Banyai K., Matthijnssens J., Buonavoglia C., Ciarlet M. Zoonotic aspects of rotaviruses. Vet. Microbiol. 2010, 140:246-255.
29. Martella V., Banyai K., Lorusso E., Bellacicco A.L., Decaro N., Camero M., Bozzo G., Moschidou P., Arista S., Pezzotti G., Lavazza A., Buonavoglia C. Prevalence of group C rotaviruses in weaning and post-weaning pigs with enteritis. Vet. Microbiol. 2007, 123:26-33.
30. Martella V., Banyai K., Lorusso E., Decaro N., Bellacicco A.L., Desario C., Corrente M., Greco G., Moschidou P., Tempesta M., Arista S., Ciarlet M., Lavazza A., Buonavoglia C. Genetic heterogeneity in the VP7 of group C rotaviruses. Virology 2007, 367:358-366.
31. Matthijnssens J., Martella V., Van Ranst M. Genomic evolution, host-species barrier, reassortment and classification of rotaviruses. Future Virol. 2010, 5:385-390.
32. Matthijnssens J., Otto P., Ciarlet M., Desselberger U., VanRanst M., Johne R. VP6 sequence-based cut-off values as a criterion for rotavirus species demarcation. Arch. Virol. 2012, 157:1177-1182.
33. Matthijnssens J., Ciarlet M., Heiman E., Arijs I., Delbeke T., McDonald S.M., Palombo E.A., Iturriza-Gomara M., Maes P., Patton J.T., Rahman M., Van Ranst M. 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.
34. Matthijnssens J., Ciarlet M., Rahman M., Attoui H., Banyai K., Estes M.K., Gentsch J.R., Iturriza-Gomara M., Kirkwood C.D., Martella V., Mertens P.P., Nakagomi O., Patton J.T., Ruggeri F.M., Saif L.J., Santos N., Steyer A., Taniguchi K., Desselberger U., Van Ranst M. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 2008, 153:1621-1629.
35. Miyazaki A., Kuga K., Suzuki T., Kohmoto M., Katsuda K., Tsunemitsu H. Genetic diversity of group A rotaviruses associated with repeated outbreaks of diarrhea in a farrow-to-finish farm: identification of a porcine rotavirus strain bearing a novel VP7 genotype G26. Vet. Res. 2011, 42:112.
36. Nishikawa K., Hoshino Y., Taniguchi K., Green K.Y., Greenberg H.B., Kapikian A.Z., Chanock R.M., Gorziglia.M. Rotavirus VP7 neutralization epitopes of serotype 3 strains. Virology 1989, 171:503-515.
37. Noel J.S., Lee T.W., Kurtz J.B., Glass R.I., Monroe S.S. Typing of human astroviruses from clinical isolates by enzyme immunoassay and nucleotide sequencing. J. Clin. Microbiol. 1995, 33:797-801.
38. Petric M., Mayur K., Vonderfecht S., Eiden J.J. Comparison of group B rotavirus genes 9 and 11. J. Gen. Virol. 1991, 72:2801-2804.
39. Rahman M., Hassan Z.M., Zafrul H., Saiada F., Banik S., Faruque A.S., Delbeke T., Matthijnssens J., Van Ranst M., Azim T. Sequence analysis and evolution of group B rotaviruses. Virus Res. 2007, 125:219-225.
40. Saiada F., Rahman H.N., Moni S., Karim M.M., Pourkarim M.R., Azim T., Rahman M. Clinical presentation and molecular characterization of group B rotaviruses in diarrhoea patients in Bangladesh. J. Med. Microbiol. 2011, 60:529-536.
41. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
42. Sanekata T., Ahmed M.U., Kader A., Taniguchi K., Kobayashi N. Human group B rotavirus infections cause severe diarrhea in children and adults in Bangladesh. J. Clin. Microbiol. 2003, 41:2187-2190.
43. Sanekata T., Kuwamoto Y., Akamatsu S., Sakon N., Oseto M., Taniguchi K., Nakata S., Estes M.K. Isolation of group B porcine rotavirus in cell culture. J. Clin. Microbiol. 1996, 34:759-761.
44. Shen S., McKee T.A., Wang Z.D., Desselberger U., Liu D.X. 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. 1999, 80:2077-2085.
45. Schuffenecker I., Ando T., Thouvenot D., Lina B., Aymard M. Genetic classification of "Sapporo-like viruses. Arch. Virol. 2001, 146:2115-2132.
46. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
47. Theil K.W., Saif L.J., Moorhead P.D., Whitmoyer R.E. Porcine rotavirus-like virus (group B rotavirus): characterization and pathogenicity for gnotobiotic pigs. J. Clin. Microbiol. 1985, 21:340-345.
48. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
49. Trojnar E., Otto P., Johne R. The first complete genome sequence of a chicken group A rotavirus indicates independent evolution of mammalian and avian strains. Virology 2009, 386:325-333.
50. Tsunemitsu H., Jiang B., Saif L.J. Sequence comparison of the VP7 gene encoding the outer capsid glycoprotein among animal and human group C rotaviruses. Arch. Virol. 1996, 141:705-713.
51. Tsunemitsu H., Morita D., Takaku H., Nishimori T., Imai K., Saif L.J. First detection of bovine group B rotavirus in Japan and sequence of its VP7 gene. Arch. Virol. 1999, 144:805-815.
52. Tsunemitsu H., Kamiyama M., Kawashima K., Katsuda K., Kohmoto M., Saif L.J., Shouji T., Onodera T. Molecular characterization of the major capsid protein VP6 of bovine group B rotavirus and its use in seroepidemiology. J. Gen. Virol. 2005, 86:2569-2575.
53. Wakuda M., Ide T., Sasaki J., Komoto S., Ishii J., Sanekata T., Taniguchi K. Porcine rotavirus closely related to novel group of human rotaviruses. Emerg. Infect. Dis. 2011, 17:1491-1493.
54. Yamamoto D., Ghosh S., Ganesh B., Krishnan T., Chawla-Sarkar M., Alam M.M., Aung T.S., Kobayashi N. Analysis of genetic diversity and molecular evolution of human group B rotaviruses based on whole genome segments. J. Gen. Virol. 2010, 91:1772-1781.
55. Yang J.H., Kobayashi N., Wang Y.H., Zhou X., Li Y., Zhou D.J., Hu Z.H., Ishino M., Alam M.M., Naik T.N., Ahmed M.U. Phylogenetic analysis of a human group B rotavirus WH-1 detected in China in 2002. J. Med. Virol. 2004, 74:662-667.
56. Zheng D.P., Ando T., Fankhauser R.L., Beard R.S., Glass R.I., Monroe S.S. Norovirus classification and proposed strain nomenclature. Virology 2006, 346:312-323.