1887

Abstract

To date, full-genome sequences of only seven human group B rotavirus (RVBs) strains have been described. Such data on more RVBs are necessary to establish the evolutionary relationship and ecological features of RVBs from different geographical regions. The present study was aimed at determining the full-length sequences of all 11 genes of 13 human RVB strains detected during 1995–2010 in sporadic and outbreak cases of acute gastroenteritis from four different cities of western India. This study also included estimation of evolutionary rates and site-specific selection pressure analysis for all gene segments. Nucleotide/deduced amino acid sequence analyses of structural and non-structural genes showed 95.1–99.8/94.1–100 % identity with the counterparts of RVB strains isolated in India, Bangladesh and Myanmar. Phylogenetic analyses of all gene segments revealed formation of a monophyletic clade of the western Indian RVB strains, reflecting their highly conserved nature. All gene segments were also found to be under negative/purifying selection pressure. These data suggest that RVB is circulating in the natural host as a series of stable viral clones. Estimates of rates of nucleotide substitution in all RVBs ranged from 1.36–4.78×10 substitutions per site per year. The rate for human RVB VP7 and NSP2 genes were comparable, respectively, with the evolution kinetics of genotype G9/G12 and N1 group A rotavirus strains. The time of the most recent common ancestor of the extant human RVBs was estimated to be during 1915–1974. Evolutionary and genetic analyses carried out in this study provide data that is useful for the elucidation of evolutionary relationship/timescale, stasis or dynamics existing in the RVB population.

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2012-10-01
2024-03-28
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References

  1. Ahmed M. U., Kobayashi N., Wakuda M., Sanekata T., Taniguchi K., Kader A., Naik T. N., Ishino M., Alam M. M. other authors 2004; Genetic analysis of group B human rotaviruses detected in Bangladesh in 2000 and 2001. J Med Virol 72:149–155[PubMed] [CrossRef]
    [Google Scholar]
  2. Aung T. S., Kobayashi N., Nagashima S., Ghosh S., Aung M. S., Oo K. Y., Win N. 2009; Detection of group B rotavirus in an adult with acute gastroenteritis in Yangon, Myanmar. J Med Virol 81:1968–1974 [View Article][PubMed]
    [Google Scholar]
  3. Barman P., Ghosh S., Das S., Varghese V., Chaudhuri S., Sarkar S., Krishnan T., Bhattacharya S. K., Chakrabarti A. other authors 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 42:2816–2818 [View Article][PubMed]
    [Google Scholar]
  4. Brown D. W., Beards G. M., Chen G. M., Flewett T. H. 1987; Prevalence of antibody to group B (atypical) rotavirus in humans and animals. J Clin Microbiol 25:316–319[PubMed]
    [Google Scholar]
  5. Chasey D., Banks J. 1984; The commonest rotaviruses from neonatal lamb diarrhoea in England and Wales have atypical electropherotypes. Vet Rec 115:326–327 [View Article][PubMed]
    [Google Scholar]
  6. Chen G. M., Hung T., Mackow E. R. 1990; Identification of the gene encoding the major outer capsid protein of ADRV: primary characterisation of RNA segment 9. Virology 178:311–315[PubMed] [CrossRef]
    [Google Scholar]
  7. Chen G. M., Werner-Eckert R., Tao H., Mackow E. R. 1991; Expression of the major inner capsid protein of the group B rotavirus ADRV: primary characterization of genome segment 5. Virology 182:820–829[PubMed] [CrossRef]
    [Google Scholar]
  8. Chitambar S. D., Lahon A., Tatte V. S., Maniya N. H., Tambe G. U., Khatri K. I., Desai H. S., Ugare M. R., Kulkarni S. V., Waghmare A. P. 2011; Occurrence of group B rotavirus infections in the outbreaks of acute gastroenteritis from western India. Indian J Med Res 134:399–400[PubMed]
    [Google Scholar]
  9. Chitambar S. D., Gopalkrishna V., Chhabra P., Patil P., Verma H., Lahon A., Arora R., Tatte V., Ranshing S. other authors 2012; Diversity in the enteric viruses detected in outbreaks of gastroenteritis from mumbai, Western India. Int J Environ Res Public Health 9:895–915 [View Article][PubMed]
    [Google Scholar]
  10. 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]
  11. Cook J. P., McCrae M. A. 2004; Sequence analysis of the guanylyltransferase (VP3) of group A rotaviruses. J Gen Virol 85:929–932 [View Article][PubMed]
    [Google Scholar]
  12. Deo R. C., Groft C. M., Rajashankar K. R., Burley S. K. 2002; Recognition of the rotavirus mRNA 3′ consensus by an asymmetric NSP3 homodimer. Cell 108:71–81 [View Article][PubMed]
    [Google Scholar]
  13. Domingo E., Holland J. J. 1997; RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178 [View Article][PubMed]
    [Google Scholar]
  14. Donker N. C., Kirkwood C. D. 2012; Selection and evolutionary analysis in the nonstructural protein NSP2 of rotavirus A. Infect Genet Evol 12:1355–1361 [View Article][PubMed]
    [Google Scholar]
  15. Drummond A. J., Rambaut A. 2007; BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214 [View Article][PubMed]
    [Google Scholar]
  16. Drummond A. J., Ho S. Y. W., Phillips M. J., Rambaut A. 2006; Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88 [View Article][PubMed]
    [Google Scholar]
  17. Eiden J. J., Wilde J., Firoozmand F., Yolken R. 1991; Detection of animal and human group B rotaviruses in fecal specimens by polymerase chain reaction. J Clin Microbiol 29:539–543[PubMed]
    [Google Scholar]
  18. Estes M. K., Kapikian A. Z. 2007; Rotaviruses. In Fields Virology, 5th edn. pp. 1917–1974 Edited by Knipe D. M., Howley P. M. et al. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  19. Fang Z.-Y., Ye Q., Ho M.-S., Dong H., Qing S., Penaranda M. E., Hung T., Wen L., Glass R. I. 1989; Investigation of an outbreak of adult diarrhea rotavirus in China. J Infect Dis 160:948–953 [View Article][PubMed]
    [Google Scholar]
  20. Ghosh S., Kobayashi N. 2011; Whole-genomic analysis of rotavirus strains: current status and future prospects. Future Microbiol 6:1049–1065 [View Article][PubMed]
    [Google Scholar]
  21. Gorziglia M., Green K., Nishikawa K., Taniguchi K., Jones R., Kapikian A. Z., Chanock R. M. 1988; Sequence of the fourth gene of human rotaviruses recovered from asymptomatic or symptomatic infections. J Virol 62:2978–2984[PubMed]
    [Google Scholar]
  22. Holmes E. C. 2003; Error thresholds and the constraints to RNA virus evolution. Trends Microbiol 11:543–546 [View Article][PubMed]
    [Google Scholar]
  23. 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. other authors 1984; Waterborne outbreak of rotavirus diarrhoea in adults in China caused by a novel rotavirus. Lancet 1:1139–1142[PubMed]
    [Google Scholar]
  24. Ishino M., Mise K., Takemura H., Ahmed M. U., Alam M. M., Naik T. N., Kobayashi N. 2006; Comparison of NSP4 protein between group A and B human rotaviruses: detection of novel diarrhea-causing sequences in group B NSP4. Arch Virol 151:173–182 [View Article][PubMed]
    [Google Scholar]
  25. Ito H., Sugiyama M., Masubuchi K., Mori Y., Minamoto N. 2001; Complete nucleotide sequence of a group A avian rotavirus genome and a comparison with its counterparts of mammalian rotaviruses. Virus Res 75:123–138 [View Article][PubMed]
    [Google Scholar]
  26. Jenkins G. M., Rambaut A., Pybus O. G., Holmes E. C. 2002; Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54:156–165 [View Article][PubMed]
    [Google Scholar]
  27. 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 89:2622–2629 [View Article][PubMed]
    [Google Scholar]
  28. Kapikian A. Z., Hoshino Y., Chanock R. M. 2001; Rotaviruses. In Fields Virology, 4th edn. pp. 1787–1833 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  29. Kelkar S. D., Zade J. K. 2004; Group B rotaviruses similar to strain CAL-1, have been circulating in Western India since 1993. Epidemiol Infect 132:745–749 [View Article][PubMed]
    [Google Scholar]
  30. Kelkar S. D., Zade J. K., Dindokar A. R., Dhale G. S., Vaishya S. S. 2007; Outbreak of diarrhoea in Daman and detection of group B rotavirus from three adult cases. Natl Med J India 20:47[PubMed]
    [Google Scholar]
  31. Kobayashi N., Naik T. N., Kusuhara Y., Krishnan T., Sen A., Bhattacharya S. K., Taniguchi K., Alam M. M., 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 64:583–588 [View Article][PubMed]
    [Google Scholar]
  32. Krishnan T., Sen A., Choudhury J. S., Das S., Naik T. N., Bhattacharya S. K. 1999; Emergence of adult diarrhoea rotavirus in Calcutta, India. Lancet 353:380–381 [View Article][PubMed]
    [Google Scholar]
  33. Kuga K., Miyazaki A., Suzuki T., Takagi M., Hattori N., Katsuda K., Mase M., Sugiyama M., Tsunemitsu H. 2009; Genetic diversity and classification of the outer capsid glycoprotein VP7 of porcine group B rotaviruses. Arch Virol 154:1785–1795 [View Article][PubMed]
    [Google Scholar]
  34. Lahon A., Chitambar S. D. 2011; Molecular characterization of VP4, VP6, VP7 and NSP4 genes of group B rotavirus strains from outbreaks of gastroenteritis. Asian Pac J Trop Med 4:846–849 [View Article][PubMed]
    [Google Scholar]
  35. Lahon A., Maniya N. H., Tambe G. U., Chinchole P. R., Purwar S., Jacob G., Chitambar S. D. 2012; Group B rotavirus infection in patients with acute gastroenteritis from India: 1994-1995 and 2004-2010. Epidemiol Infect [View Article] [View Article][PubMed]
    [Google Scholar]
  36. Marthaler D., Rossow K., Collins J., Goyal S., Tsunemitsu H., Kuga K., Suzuki T., Ciarlet M., Matthijnssens J. 2012; Detection of substantial porcine group B rotavirus genetic diversity in the United States, resulting in a modified classification proposal for G genotypes. Virology (in press)
    [Google Scholar]
  37. Matthijnssens J., Ciarlet M., Heiman E., Arijs I., Delbeke T., McDonald S. M., Palombo E. A., Iturriza-Gómara M., Maes P. other authors 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 82:3204–3219 [View Article][PubMed]
    [Google Scholar]
  38. Matthijnssens J., Heylen E., Zeller M., Rahman M., Lemey P., Van Ranst M. 2010; Phylodynamic analyses of rotavirus genotypes G9 and G12 underscore their potential for swift global spread. Mol Biol Evol 27:2431–2436 [View Article][PubMed]
    [Google Scholar]
  39. 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]
  40. McDonald S. M., Patton J. T. 2008; Molecular characterization of a subgroup specificity associated with the rotavirus inner capsid protein VP2. J Virol 82:2752–2764 [View Article][PubMed]
    [Google Scholar]
  41. McDonald S. M., Aguayo D., Gonzalez-Nilo F. D., Patton J. T. 2009; Shared and group-specific features of the rotavirus RNA polymerase reveal potential determinants of gene reassortment restriction. J Virol 83:6135–6148 [View Article][PubMed]
    [Google Scholar]
  42. Mohd Jaafar F., Attoui H., Mertens P. P., de Micco P., de Lamballerie X. 2005; Identification and functional analysis of VP3, the guanylyltransferase of Banna virus (genus Seadornavirus, family Reoviridae). J Gen Virol 86:1141–1146 [View Article][PubMed]
    [Google Scholar]
  43. 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]
  44. Nakata S., Estes M. K., Graham D. Y., Wang S. S., Gary G. W., Melnick J. L. 1987; Detection of antibody to group B adult diarrhea rotaviruses in humans. J Clin Microbiol 25:812–818[PubMed]
    [Google Scholar]
  45. Ogden K. M., Ramanathan H. N., Patton J. T. 2012; Mutational analysis of residues involved in nucleotide and divalent cation stabilization in the rotavirus RNA-dependent RNA polymerase catalytic pocket. Virology 431:12–20 [View Article][PubMed]
    [Google Scholar]
  46. Parwani A. V., Lucchelli A., Saif L. J. 1996; Identification of group B rotaviruses with short genome electropherotypes from adult cows with diarrhea. J Clin Microbiol 34:1303–1305[PubMed]
    [Google Scholar]
  47. Pitzer V. E., Patel M. M., Lopman B. A., Viboud C., Parashar U. D., Grenfell B. T. 2011; Modeling rotavirus strain dynamics in developed countries to understand the potential impact of vaccination on genotype distributions. Proc Natl Acad Sci U S A 108:19353–19358 [View Article][PubMed]
    [Google Scholar]
  48. Rahman M., Hassan Z. M., Zafrul H., Saiada F., Banik S., Faruque A. S., Delbeke T., Matthijnssens J., Van Ranst M., Azim T. 2007; Sequence analysis and evolution of group B rotaviruses. Virus Res 125:219–225 [View Article][PubMed]
    [Google Scholar]
  49. Saiada F., Rahman H. N., Moni S., Karim M. M., Pourkarim M. R., Azim T., Rahman M. 2011; Clinical presentation and molecular characterization of group B rotaviruses in diarrhoea patients in Bangladesh. J Med Microbiol 60:529–536 [View Article][PubMed]
    [Google Scholar]
  50. Sanekata T., Ahmed M. U., Kader A., Taniguchi K., Kobayashi N. 2003; Human group B rotavirus infections cause severe diarrhea in children and adults in Bangladesh. J Clin Microbiol 41:2187–2190 [View Article][PubMed]
    [Google Scholar]
  51. Sereno M. M., Gorziglia M. I. 1994; The outer capsid protein VP4 of murine rotavirus strain Eb represents a tentative new P type. Virology 199:500–504 [View Article][PubMed]
    [Google Scholar]
  52. Suchard M. A., Weiss R. E., Sinsheimer J. S. 2001; Bayesian selection of continuous-time Markov chain evolutionary models. Mol Biol Evol 18:1001–1013 [View Article][PubMed]
    [Google Scholar]
  53. Suzuki T., Kuga K., Miyazaki A., Tsunemitsu H. 2011; Genetic divergence and classification of non-structural protein 1 among porcine rotaviruses of species B. J Gen Virol 92:2922–2929 [View Article][PubMed]
    [Google Scholar]
  54. 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]
  55. Tamura K., Nei M. 1993; Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
    [Google Scholar]
  56. 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]
  57. Theil K. W., Saif L. J., Moorhead P. D., Whitmoyer R. E. 1985; Porcine rotavirus-like virus (group B rotavirus): characterization and pathogenicity for gnotobiotic pigs. J Clin Microbiol 21:340–345[PubMed]
    [Google Scholar]
  58. Thompson J. D., Higgins D. G., Gibson T. J. 1994; CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [View Article][PubMed]
    [Google Scholar]
  59. Tsunemitsu H., Morita D., Takaku H., Nishimori T., Imai K., Saif L. J. 1999; First detection of bovine group B rotavirus in Japan and sequence of its VP7 gene. Arch Virol 144:805–815 [View Article][PubMed]
    [Google Scholar]
  60. Vende P., Piron M., Castagné N., Poncet D. 2000; Efficient translation of rotavirus mRNA requires simultaneous interaction of NSP3 with the eukaryotic translation initiation factor eIF4G and the mRNA 3′ end. J Virol 74:7064–7071 [View Article][PubMed]
    [Google Scholar]
  61. Vonderfecht S. L., Huber A. C., Eiden J., Mader L. C., Yolken R. H. 1984; Infectious diarrhea of infant rats produced by a rotavirus-like agent. J Virol 52:94–98[PubMed]
    [Google Scholar]
  62. Yamamoto D., Ghosh S., Ganesh B., Krishnan T., Chawla-Sarkar M., Alam M. M., Aung T. S., Kobayashi N. 2010; Analysis of genetic diversity and molecular evolution of human group B rotaviruses based on whole genome segments. J Gen Virol 91:1772–1781 [View Article][PubMed]
    [Google Scholar]
  63. Yang J. H., Kobayashi N., Wang Y. H., Zhou X., Li Y., Zhou D. J., Hu Z. H., Ishino M., Alam M. M. other authors 2004; Phylogenetic analysis of a human group B rotavirus WH-1 detected in China in 2002. J Med Virol 74:662–667 [View Article][PubMed]
    [Google Scholar]
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