1887

Journal of General Virology header logo

Volume 97, Issue 12

Molecular characterization of emerging G9P[4] rotavirus strains possessing a rare E6 NSP4 or T1 NSP3 genotype on a genogroup-2 backbone using a refined classification framework Free

Abstract

Rotavirus infections associated with unusual strains are an emerging concern in rotavirus vaccination programmes. Recently, an increase in circulation of unusual G9P[4] strains was reported from different regions of India, placing this genotype in third position, after G1P[8] and G2P[4], of the most common rotavirus strains. The aim of the present study was to analyse the complete genomic constellation of three G9P[4] strains (RV09, RV10 and RV11), determine their genetic relatedness to other genogroup-2 strains and understand the evolution of a rare E6 and other NSP4 genotypes. All strains revealed the presence of a genogroup-2 backbone, with RV09 constituting the NSP3 T1 genotype and RV10 and RV11 bearing the NSP4 E6 genotype. A refined criterion adopted to classify the nine internal gene segments of G2P[4] and non-G2P[4] strains with the genogroup-2 backbone into lineages and sub-lineages indicated divergence of >8 % (except NSP1: >5.5 %) for lineages and >3 % for sub-lineages. The VP1 and/or VP3 genes of study strains showed close relationships with animal-like human rotaviruses. The estimated evolutionary rate for the NSP4 E6 genotype was marginally higher (3.78×10 substitutions per site per year) than that of genotypes E1 (2.6×10 substitutions per site per year) and E2 (3.06×10 substitutions per site per year), suggesting a step towards adaptation of E6 on a genogroup-2 backbone. The time and origin of the most recent common ancestor of E6 genotype were estimated to be 1981 and South Asia, respectively. Full-genome and evolutionary analyses performed in this study for G9P[4] strains will help better understand the extent of gene reassortment and origin in unusual rotavirus strains that may remain viable and cause infections in humans.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): genogroup-2 , India , inter-genogroup reassortment , NSP4 E6 and rotavirus
© 2016 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000650
2016-12-16
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/12/3139.html?itemId=/content/journal/jgv/10.1099/jgv.0.000650&mimeType=html&fmt=ahah

References

  1. Araújo I. T., Ferreira M. S., Fialho A. M., Assis R. M., Cruz C. M., Rocha M., Leite J. P. 2001; Rotavirus genotypes P[4]G9, P[6]G9, and P[8]G9 in hospitalized children with acute gastroenteritis in Rio de Janeiro, Brazil. J Clin Microbiol 39:1999–2001 [View Article][PubMed]
     [Google Scholar]
  2. Arista S., Vizzi E., Migliore M. C., Di Rosa E., Cascio A. 2003; High incidence of G9P181 rotavirus infections in Italian children during the winter season 1999-2000. Eur J Epidemiol 18:711–714 [View Article][PubMed]
     [Google Scholar]
  3. Armah G. E., Steele A. D., Binka F. N., Esona M. D., Asmah R. H., Anto F., Brown D., Green J., Cutts F., Hall A. 2003; Changing patterns of rotavirus genotypes in Ghana: emergence of human rotavirus G9 as a major cause of diarrhea in children. J Clin Microbiol 41:2317–2322 [View Article][PubMed]
     [Google Scholar]
  4. Babji S., Arumugam R., Sarvanabhavan A., Moses P. D., Simon A., Aggarwal I., Mathew A., Sr Anita, Kang G. 2014; Multi-center surveillance of rotavirus diarrhea in hospitalized children <5 years of age in India, 2009-2012. Vaccine 32: Suppl 1 A10–A12 [View Article][PubMed]
     [Google Scholar]
  5. Bányai K., László B., Duque J., Steele A. D., Nelson E. A., Gentsch J. R., Parashar U. D. 2012; Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine 30:A122–A130 [View Article][PubMed]
     [Google Scholar]
  6. Chitambar S. D., Arora R., Chhabra P. 2009; Molecular characterization of a rare G1P[19] rotavirus strain from India: evidence of reassortment between human and porcine rotavirus strains. J Med Microbiol 58:1611–1615 [View Article][PubMed]
     [Google Scholar]
  7. Chitambar S. D., Ranshing S. S., Pradhan G. N., Kalrao V. R., Dhongde R. K., Bavdekar A. R. 2014; Changing trends in circulating rotavirus strains in Pune, western India in 2009-2012: emergence of a rare G9P[4] rotavirus strain. Vaccine 32:A29–A32 [View Article][PubMed]
     [Google Scholar]
  8. Ciarlet M., Hyser J. M., Estes M. K. 2002; Sequence analysis of the VP4, VP6, VP7, and NSP4 gene products of the bovine rotavirus WC3. Virus Genes 24:107–118[PubMed] [CrossRef]
     [Google Scholar]
  9. Clark H. F., Hoshino Y., Bell L. M., Groff J., Hess G., Bachman P., Offit P. A. 1987; Rotavirus isolate WI61 representing a presumptive new human serotype. J Clin Microbiol 25:1757–1762[PubMed]
     [Google Scholar]
  10. Clark H. F., Lawley D. A., Schaffer A., Patacsil J. M., Marcello A. E., Glass R. I., Jain V., Gentsch J. 2004; Assessment of the epidemic potential of a new strain of rotavirus associated with the novel G9 serotype which caused an outbreak in the United States for the first time in the 1995-1996 season. J Clin Microbiol 42:1434–1438 [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. Das B. K., Gentsch J. R., Cicirello H. G., Woods P. A., Gupta A., Ramachandran M., Kumar R., Bhan M. K., Glass R. I. 1994; Characterization of rotavirus strains from newborns in New Delhi, India. J Clin Microbiol 32:1820–1822[PubMed]
     [Google Scholar]
  13. Dennis A. F., McDonald S. M., Payne D. C., Mijatovic-Rustempasic S., Esona M. D., Edwards K. M., Chappell J. D., Patton J. T. 2014; Molecular epidemiology of contemporary G2P[4] human rotaviruses cocirculating in a single U.S. community: footprints of a globally transitioning genotype. J Virol 88:3789–3801 [View Article][PubMed]
     [Google Scholar]
  14. Doan Y. H., Nakagomi T., Nakagomi O. 2012; Repeated circulation over 6 years of intergenogroup mono-reassortant G2P[4] rotavirus strains with genotype N1 of the NSP2 gene. Infect Genet Evol 12:1202–1212 [View Article]
     [Google Scholar]
  15. Doan Y. H., Nakagomi T., Agbemabiese C. A., Nakagomi O. 2015; Changes in the distribution of lineage constellations of G2P[4] rotavirus a strains detected in Japan over 32years (1980–2011). Infect Genet Evol 34:423–433 [View Article]
     [Google Scholar]
  16. 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]
     [Google Scholar]
  17. Dormitzer P. R., Sun Z. Y., Wagner G., Harrison S. C. 2002; The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 21:885–897 [View Article][PubMed]
     [Google Scholar]
  18. Dormitzer P. R., Nason E. B., Prasad B. V., Harrison S. C. 2004; Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430:1053–1058 [View Article][PubMed]
     [Google Scholar]
  19. Drummond A. J., Ho S. Y., Phillips M. J., Rambaut A. 2006; Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88 [View Article][PubMed]
     [Google Scholar]
  20. Drummond A. J., Rambaut A. 2007; beast: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:1 [View Article][PubMed]
     [Google Scholar]
  21. Dyall-Smith M. L., Lazdins I., Tregear G. W., Holmes I. H. 1986; Location of the major antigenic sites involved in rotavirus serotype-specific neutralization. Proc Natl Acad Sci 83:3465–3468 [View Article]
     [Google Scholar]
  22. Esona M. D., Geyer A., Banyai K., Page N., Aminu M., Armah G. E., Hull J., Steele D. A., Glass R. I. et al. 2009; Novel human rotavirus genotype G5P[7] from child with diarrhea, Cameroon. Emerg Infect Dis 15:83 [View Article][PubMed]
     [Google Scholar]
  23. Espínola E. E., Amarilla A., Arbiza J., Parra G. I. 2008; Sequence and phylogenetic analysis of the VP4 gene of human rotaviruses isolated in Paraguay. Arch Virol 153:1067–1073 [View Article][PubMed]
     [Google Scholar]
  24. Estes M. K., Kapikian A. Z. 2007; Rotaviruses. In Fields Virology, 5th edn. , pp. 1917–1974 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott, Williams, and Wilkins;
     [Google Scholar]
  25. Gouvea V., Glass R. I., Woods P., Taniguchi K., Clark H. F., Forrester B., Fang Z. Y. 1990; Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28:276–282[PubMed]
     [Google Scholar]
  26. Heiman E. M., McDonald S. M., Barro M., Taraporewala Z. F., Bar-Magen T., Patton J. T. 2008; Group a human rotavirus genomics: evidence that gene constellations are influenced by viral protein interactions. J Virol 82:11106–11116 [View Article][PubMed]
     [Google Scholar]
  27. Holmes I. H. 1983; Rotaviruses. In The Reoviridae pp. 359–423 Edited by Joklik W. New York: Plenum Press; [CrossRef]
     [Google Scholar]
  28. 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]
  29. Kang G., Arora R., Chitambar S. D., Deshpande J., Gupte M. D., Kulkarni M., Naik T. N., Mukherji D., Venkatasubramaniam S. et al. 2009; Multicenter, hospital-based surveillance of rotavirus disease and strains among indian children aged <5 years. J Infect Dis 200:S147–S153 [View Article][PubMed]
     [Google Scholar]
  30. Kang G., Desai R., Arora R., Chitamabar S., Naik T. N., Krishnan T., Deshpande J., Gupte M. D., Venkatasubramaniam S. et al. 2013; Diversity of circulating rotavirus strains in children hospitalized with diarrhea in India, 2005-2009. Vaccine 31:2879–2883 [View Article][PubMed]
     [Google Scholar]
  31. Lahon A., Walimbe A. M., Chitambar S. D. 2012; Full genome analysis of group b rotaviruses from western India: genetic relatedness and evolution. J Gen Virol 93:2252–2266 [View Article][PubMed]
     [Google Scholar]
  32. Lemey P., Rambaut A., Drummond A. J., Suchard M. A. 2009; Bayesian phylogeography finds its roots. PLoS Comput Biol 5:e1000520 [View Article][PubMed]
     [Google Scholar]
  33. Lewis J., Roy S., Esona M. D., Mijatovic-Rustempasic S., Hardy C., Wang Y., Cortese M., Bowen M. D. 2014; Full genome sequence of a reassortant human G9P[4] rotavirus strain. Genome Announc 2:e0128414 [View Article][PubMed]
     [Google Scholar]
  34. 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 [View Article][PubMed]
     [Google Scholar]
  35. Matthijnssens J., Ciarlet M., Heiman E., Arijs I., Delbeke T., McDonald S. M., Palombo E. A., Iturriza-Gómara M., Maes P. et al. 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]
  36. Matthijnssens J., Ciarlet M., McDonald S. M., Attoui H., Bányai K., Brister J. R., Buesa J., Esona M. D., Estes M. K. et al. 2011; Uniformity of rotavirus strain nomenclature proposed by the rotavirus classification working group (RCWG). Arch Virol 156:1397–1413 [View Article][PubMed]
     [Google Scholar]
  37. Matthijnssens J., Van Ranst M. 2012; Genotype constellation and evolution of group A rotaviruses infecting humans. Curr Opin Virol 2:426–433 [View Article][PubMed]
     [Google Scholar]
  38. Matthijnssens J., Theuns S. 2015; Minutes of the 7th rotavirus classification working group (Rcwg meeting). https://rega.kuleuven.be/cev/viralmetagenomics/virus-classification/minutes-of-the-7th-rcwg-meeting
  39. Mattion N. M., Cohen J., Aponte C., Estes M. K. 1992; Characterization of an oligomerization domain and RNA-binding properties on rotavirus nonstructural protein NS34. Virology 190:68–83 [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. Mullick S., Mandal P., Nayak M. K., Ghosh S., De P., Rajendran K., Bhattacharya M. K., Mitra U., Ramamurthy T. et al. 2014; Hospital based surveillance and genetic characterization of rotavirus strains in children (<5 years) with acute gastroenteritis in Kolkata, India, revealed resurgence of G9 and G2 genotypes during 2011-2013. Vaccine 32:A20–A28 [View Article][PubMed]
     [Google Scholar]
  42. Nagashima S., Kobayashi N., Ishino M., Alam M. M., Ahmed M. U., Paul S. K., Ganesh B., Chawla-Sarkar M., Krishnan T. et al. 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]
  43. O'Reilly E. K., Kao C. C. 1998; Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure. Virology 252:287–303 [View Article][PubMed]
     [Google Scholar]
  44. 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]
  45. Okada J., Urasawa T., Kobayashi N., Taniguchi K., Hasegawa A., Mise K., Urasawa S. 2000; New P serotype of group A human rotavirus closely related to that of a porcine rotavirus. J Med Virol 60:63–69 [View Article][PubMed]
     [Google Scholar]
  46. Phan T. G., Okitsu S., Maneekarn N., Ushijima H. 2007; Genetic heterogeneity, evolution and recombination in emerging G9 rotaviruses. Infect Genet Evol 7:656–663 [View Article]
     [Google Scholar]
  47. Piron M., Vende P., Cohen J., Poncet D. 1998; Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J 17:5811–5821 [View Article][PubMed]
     [Google Scholar]
  48. Piron M., Delaunay T., Grosclaude J., Poncet D. 1999; Identification of the RNA-binding, dimerization, and eIF4GI-binding domains of rotavirus nonstructural protein NSP3. J Virol 73:5411–5421[PubMed]
     [Google Scholar]
  49. Poncet D., Aponte C., Cohen J. 1993; Rotavirus protein NSP3 (NS34) is bound to the 3′ end consensus sequence of viral mRNAs in infected cells. J Virol 67:3159–3165[PubMed]
     [Google Scholar]
  50. Quaye O., McDonald S., Esona M. D., Lyde F. C., Mijatovic-Rustempasic S., Roy S., Banegas D. J., Quiñonez Y. M., Chinchilla B. L. et al. 2013; Rotavirus G9P[4] in 3 countries in Latin America, 2009-2010. Emerg Infect Dis 19:1332–1333 [View Article][PubMed]
     [Google Scholar]
  51. Rahman M., Matthijnssens J., Yang X., Delbeke T., Arijs I., Taniguchi K., Iturriza-Gómara M., Iftekharuddin N., Azim T. et al. 2007; Evolutionary history and global spread of the emerging g12 human rotaviruses. J Virol 81:2382–2390 [View Article][PubMed]
     [Google Scholar]
  52. Ramachandran M., Gentsch J. R., Parashar U. D., Jin S., Woods P. A., Holmes J. L., Kirkwood C. D., Bishop R. F., Greenberg H. B. et al. 1998; Detection and characterization of novel rotavirus strains in the United States. J Clin Microbiol 36:3223–3229[PubMed]
     [Google Scholar]
  53. Ramachandran M., Kirkwood C. D., Unicomb L., Cunliffe N. A., Ward R. L., Bhan M. K., Clark H. F., Glass R. I., Gentsch J. R. 2000; Molecular characterization of serotype G9 rotavirus strains from a global collection. Virology 278:436–444 [View Article][PubMed]
     [Google Scholar]
  54. Rao C. D., Das M., Ilango P., Lalwani R., Rao B. S., Gowda K. 1995; Comparative nucleotide and amino acid sequence analysis of the sequence-specific RNA-binding rotavirus nonstructural protein NSP3. Virology 207:327–333 [View Article][PubMed]
     [Google Scholar]
  55. Saluja T., Sharma S. D., Gupta M., Kundu R., Kar S., Dutta A., Silveira M., Singh J. V., Kamath V. G. et al. 2014; A multicenter prospective hospital-based surveillance to estimate the burden of rotavirus gastroenteritis in children less than five years of age in India. Vaccine 32:A13–A19 [View Article][PubMed]
     [Google Scholar]
  56. Santos N., Volotão E. M., Soares C. C., Albuquerque M. C., da Silva F. M., Chizhikov V., Hoshino Y. 2002; VP7 gene polymorphism of serotype G9 rotavirus strains and its impact on G genotype determination by PCR. Virus Res 90:1–14 [View Article][PubMed]
     [Google Scholar]
  57. Sharma S., Paul V. K., Bhan M. K., Ray P. 2009; Genomic characterization of nontypeable rotaviruses and detection of a rare G8 strain in Delhi, India. J Clin Microbiol 47:3998–4005 [View Article][PubMed]
     [Google Scholar]
  58. 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]
  59. 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[PubMed]
     [Google Scholar]
  60. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
     [Google Scholar]
  61. Tang B., Gilbert J. M., Matsui S. M., Greenberg H. B. 1997; Comparison of the rotavirus gene 6 from different species by sequence analysis and localization of subgroup-specific epitopes using site-directed mutagenesis. Virology 237:89–96 [View Article][PubMed]
     [Google Scholar]
  62. Tatsumi M., Nagaoka Y., Tsugawa T., Yoto Y., Hori T., Tsutsumi H. 2014; Characterization of the NSP4 gene of group A human rotavirus G1P[8] strains circulating in Sapporo, Japan from 1987 to 2000. J Med Virol 86:354–359 [View Article][PubMed]
     [Google Scholar]
  63. Tiku V. R., Sharma S., Verma A., Kumar P., Raghavendhar S., Aneja S., Paul V. K., Bhan M. K., Ray P. 2014; Rotavirus diversity among diarrheal children in Delhi, India during 2007-2012. Vaccine 32:A62–A67 [View Article][PubMed]
     [Google Scholar]
  64. Wang Y. H., Pang B. B., Ghosh S., Zhou X., Shintani T., Urushibara N., Song Y. W., He M. Y., Liu M. Q. et al. 2014; Molecular epidemiology and genetic evolution of the whole genome of G3P[8] human rotavirus in Wuhan, China, from 2000 through 2013. PLoS One 9:e88850 [View Article][PubMed]
     [Google Scholar]
  65. Ward R. L., Nakagomi O., Knowlton D. R., McNeal M. M., Nakagomi T., Clemens J. D., Sack D. A., Schiff G. M. 1990; Evidence for natural reassortants of human rotaviruses belonging to different genogroups. J Virol 64:3219–3225[PubMed]
     [Google Scholar]
  66. Ward M. L., Mijatovic-Rustempasic S., Roy S., Rungsrisuriyachai K., Boom J. A., Sahni L. C., Baker C. J., Rench M. A., Wikswo M. E. et al. 2016; Molecular characterization of the first G24P[14] rotavirus strain detected in humans. Infect Genet Evol 43:338–342 [View Article][PubMed]
     [Google Scholar]
  67. Xu L., Tian Y., Tarlow O., Harbour D., McCrae M. A. 1994; Molecular biology of rotaviruses. IX. conservation and divergence in genome segment 5. J Gen Virol 75:3413–3421 [View Article][PubMed]
     [Google Scholar]
  68. Yamamoto S. P., Kaida A., Ono A., Kubo H., Iritani N. 2015; Detection and characterization of a human G9P[4] rotavirus strain in Japan. J Med Virol 87:1311–1318 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000650
Loading
Molecular characterization of emerging G9P[4] rotavirus strains possessing a rare E6 NSP4 or T1 NSP3 genotype on a genogroup-2 backbone using a refined classification framework
J. Gen. Virol. 97, 3139 (2016); https://doi.org/10.1099/jgv.0.000650
/content/journal/jgv/10.1099/jgv.0.000650
/content/journal/jgv/10.1099/jgv.0.000650
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