Phylodynamic characteristics of the Russian population of rotavirus А (Reoviridae: Sedoreovirinae: Rotavirus) based on the VP6 gene

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Abstract

Introduction. Rotavirus A is one of the leading causes of acute gastroenteritis in children in the first years of life. Rotavirus infection is currently classified as a preventable infection. The most abundant rotavirion protein is VP6.

Material and methods. Phylogenetic analysis and calculation of phylodynamic characteristics were carried out for 262 nucleotide sequences of the VP6 gene of rotavirus species A, isolated in Russia, using the BEAST v.1.10.4 software package. The derivation and analysis of amino acid sequences was performed using the MEGAX program.

Results. This study provides phylodynamic characteristics of the rotaviruses in Russia based on the sequences coding VP6 protein. Bayesian analysis showed the circulation of rotaviruses of three sublineages of genotype I1 and three sublineages of genotype I2 in Russia. The level of accumulation of mutations was established, which turned out to be similar for genotypes I1 and I2 and amounted to 7.732E-4 and 1.008E-3 nucleotides/site/year, respectively. The effective population sizes based on nucleotide sequences of the VP6 I1 and I2 genotypes are relatively stable while after the 2000s there is a tendency of its decreasing. Comparative analysis of the amino acid sequences in the region of the intracellular neutralization sites A (231–260 aa) and B (265–292 aa) made it possible to reveal a mutation in position V252I in a proportion of Russian strains of genotype I1 some strains of genotypes I1 and I2 had mutation I281V. These substitutions were not associated with any sublineages to which the strains belong. The analysis of three T-cell epitopes revealed four amino acid differences (in aa positions 305, 315, 342, 348) that were associated with the first or second genogroup.

Conclusion. Based on the phylodynamic characteristics and amino acid composition of antigenic determinants, it was concluded that the VP6 protein is highly stable and could potentially be a good model for development of a rotavirus vaccine.

About the authors

O. V. Morozova

FSBI «Academician I.N. Blokhina Nizhny Novgorod Scientific Research Institute of Epidemiology and Microbiology» of the Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Author for correspondence.
Email: olga.morozova.bsc@gmail.com
ORCID iD: 0000-0002-8058-8187

researcher of Laboratory of Molecular Epidemiology of Viral Infections

Nizhny Novgorod, 603950

Russian Federation

T. F. Sashina

FSBI «Academician I.N. Blokhina Nizhny Novgorod Scientific Research Institute of Epidemiology and Microbiology» of the Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: tatyana.sashina@gmail.com
ORCID iD: 0000-0003-3203-7863

senior Researcher, laboratory of molecular epidemiology of viral infections

Nizhny Novgorod, 603950

Russian Federation

N. A. Novikova

FSBI «Academician I.N. Blokhina Nizhny Novgorod Scientific Research Institute of Epidemiology and Microbiology» of the Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: tatyana.sashina@gmail.com
ORCID iD: 0000-0002-3710-6648

professor. Head of the laboratory of molecular epidemiology of viral infections

Nizhny Novgorod, 603950

Russian Federation

References

  1. Tate J.E., Burton A.H., Boschi-Pinto C., Steele A.D., Duque J., Parashar U.D. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 2012; 12(2): 136–41. https://doi.org/10.1016/S1473-3099(11)70253-5.
  2. Баранов А.А., Намазова-Баранова Л.С., Таточенко В.К., Вишнёва Е.А., Федосеенко М.В., Селимзянова Л.Р. и др. Ротавирусная инфекция у детей – нерешённая проблема. Обзор рекомендаций по вакцинопрофилактике. Педиатрическая фармакология. 2017; 14(4): 248–57. https://doi.org/10.15690/pf.v14i4.1756.
  3. Mirzayeva R., Cortese M.M., Mosina L., Biellik R., Lobanov A., Chernyshova L., et al. Rotavirus burden among children in the newly independent states of the former union of soviet socialist republics: literature review and first-year results from the rotavirus surveillance network. J. Infect. Dis. 2009; 200 (Suppl. 2): S203–14. https://doi.org/10.1086/605041.
  4. Ward R.L., Bernstein D.I. Rotarix: A rotavirus vaccine for the world. Clin. Infect. Dis. 2009; 48(2): 222–8. https://doi.org/10.1086/595702.
  5. Ciarlet M., Schödel F. Development of a rotavirus vaccine: Clinical safety, immunogenicity, and efficacy of the pentavalent rotavirus vaccine, RotaTeq. Vaccine. 2009; 27(Suppl. 6): G72–81. https://doi.org/10.1016/j.vaccine.2009.09.107.
  6. Glass R.I., Bhan M.K., Ray P., Bahl R., Parashar U.D., Greenberg H., et al. Development of candidate rotavirus vaccines derived from neonatal strains in India. J. Infect. Dis. 2005; 192(Suppl. 1): S30–5. https://doi.org/10.1086/431498.
  7. Naik S.P., Zade J.K., Sabale R.N., Pisal S.S., Menon R., Bankar S.G., et al. Stability of heat stable, live attenuated Rotavirus vaccine (ROTASIIL®). Vaccine. 2017; 35(22): 2962–9. https://doi.org/10.1016/j.vaccine.2017.04.025.
  8. Greenberg H.B., Flores J., Kalica A.R., Wyatt R.G., Jones R. Gene coding assignments for growth restriction, neutralization and subgroup specificities of the W and DS-1 strains of human rotavirus. J. Gen. Virol. 1983; 64 (Pt. 2): 313–20. https://doi.org/10.1099/0022-1317-64-2-313.
  9. Iturriza Gómara M., Wong C., Blome S., Desselberger U., Gray J. Molecular characterization of VP6 genes of human rotavirus isolates: correlation of genogroups with subgroups and evidence of independent segregation. J. Virol. 2002; 76(13): 6596–601. https://doi.org/10.1128/jvi.76.13.6596-6601.2002.
  10. Estes M.K., Greenberg H.B. Rotaviruses. In: Knipe D.M., Howley P.M., eds. Fields Virology. Philadelphia: Williams & Wilkins; 2013:1347–401.
  11. Nagashima S., Kobayashi N., Ishino M., Alam M.M., Ahmed M.U., Paul S.K., et al. Whole genomic characterization of a human rotavirus strain B219 belonging to a novel group of the genus Rotavirus. J. Med. Virol. 2008; 80(11): 2023–33. https://doi.org/10.1002/jmv.21286.
  12. López S., Espinosa R., Greenberg H.B., Arias C.F. Mapping the subgroup epitopes of rotavirus protein VP6. Virology. 1994; 204(1):153–62. https://doi.org/10.1006/viro.1994.1519.
  13. Tang B., Gilbert J.M., Matsui S.M., Greenberg H.B. Comparison of the rotavirus gene 6 from different species by sequence analysis and localization of subgroup-specific epitopes using site-directed mutagenesis. Virology. 1997; 237(1): 89–96. https://doi.org/10.1006/viro.1997.8762.
  14. Aiyegbo M.S., Sapparapu G., Spiller B.W., Eli I.M., Williams D.R., Kim R., et al. Human rotavirus VP6-specific antibodies mediate intracellular neutralization by binding to a quaternary structure in the transcriptional pore. PLoS One. 2013; 9(8): 1–15. https://doi.org/10.1371/journal.pone.0061101.
  15. Suchard M.A., Lemey P., Baele G., Ayres D.L., Drummond A.J., Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 2018; 4(1): vey016. https://doi.org/10.1093/ve/vey016.
  16. Husemann M., Zachos F.E., Paxton R.J., Habel J.C. Effective population size in ecology and evolution. Heredity. 2016; 117(4): 191–2. https://doi.org/10.1038/hdy.2016.75.
  17. Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018; 35(6): 1547–9. https://doi.org/10.1093/molbev/msy096.
  18. Rambaut A., Lam T.T., Max Carvalho L., Pybus O.G. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2016; 2(1): vew007. https://doi.org/10.1093/ve/vew007.
  19. Ayres D.L., Cummings M.P., Baele G., Darling A.E., Lewis P.O., Swofford D.L., et al. BEAGLE 3: improved performance, scaling and usability for a high-performance computing library for statistical phylogenetics. Syst. Biol. 2019; 68(6): 1052–61. https://doi.org/10.1093/sysbio/syz020.
  20. Hill V., Baele G. Bayesian estimation of past population dynamics in BEAST 1.10 using the Skygrid coalescent model. Mol. Biol. Evol. 2019; 36(11): 2620–8. https://doi.org/10.1093/molbev/msz172.
  21. Rambaut A., Drummond A.J., Xie D., Baele G., Suchard M.A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 2018; 67(5): 901–4. https://doi.org/10.1093/sysbio/syy03.
  22. Svensson L., Sheshberadaran H., Vene S., Norrby E., Grandien M., Wadell G. Serum antibody responses to individual viral polypeptides in human rotavirus infections. J. Gen. Virol. 1987; 68(Pt. 3): 643–51. https://doi.org/10.1099/0022-1317-68-3-643.
  23. Svensson L., Sheshberadaran H., Vesikari T., Norrby E., Wadell G. Immune response to rotavirus polypeptides after vaccination with heterologous rotavirus vaccines (RIT 4237, RRV‑1). J. Gen. Virol. 1987; 68(Pt. 7): 1993–9. https://doi.org/10.1099/0022-1317-68-7-1993.
  24. Ishida S., Feng N., Tang B., Gilbert J.M., Greenberg H.B. Quantification of systemic and local immune responses to individual rotavirus proteins during rotavirus infection in mice. J. Clin. Microbiol. 1996; 34(7): 1694–700. https://doi.org/10.1128/JCM.34.7.1694-1700.1996.
  25. Colomina J., Gil M.T., Codoñer P., Buesa J. Viral proteins VP2, VP6, and NSP2 are strongly precipitated by serum and fecal antibodies from children with rotavirus symptomatic infection. J. Med. Virol. 1998; 56(1): 58–65. https://doi.org/10.1002/(sici)1096-9071(199809)56:1<58::aid-jmv10>3.0.co;2-s.
  26. Estes M.K., Cohen J. Rotavirus gene structure and function. Microbiol. Rev. 1989; 53(4): 410–49.
  27. Afchangi A., Jalilvand S., Mohajel N., Marashi S.M., Shoja Z. Rotavirus VP6 as a potential vaccine candidate. Rev. Med. Virol. 2019; 29(2): e2027. https://doi.org/10.1002/rmv.2027.
  28. Духовлинов И.В., Богомолова Е.Г., Фёдорова Е.А., Симбирцев А.С. Исследование протективной активности кандидатной вакцины против ротавирусной инфекции на основе рекомбинантного белка FliCVP6VP8. Медицинская иммунология. 2016; 18(5): 417–24. https://doi.org/10.15789/1563-0625-2016-5-417-424.
  29. Choi A.H., McNeal M.M., Basu M., Flint J.A., Stone S.C., Clements J.D., et al. Intranasal or oral immunization of inbred and outbred mice with murine or human rotavirus VP6 proteins protects against viral shedding after challenge with murine rotaviruses. Vaccine. 2002; 20(27-28): 3310–21. https://doi.org/10.1016/s0264-410x(02)00315-8.
  30. McNeal M.M., Basu M., Bean J.A., Clements J.D., Lycke N.Y., Ramne A., et al. Intrarectal immunization of mice with VP6 and either LT(R192G) or CTA1-DD as adjuvant protects against fecal rotavirus shedding after EDIM challenge. Vaccine. 2007; 25(33):6224–31. https://doi.org/10.1016/j.vaccine.2007.05.065.
  31. Gill M.S., Lemey P., Faria N.R., Rambaut A., Shapiro B., Suchard M.A. Improving Bayesian population dynamics inference: a coalescent- based model for multiple loci. Mol. Biol. Evol. 2013; 30(3):713–24. https://doi.org/10.1093/molbev/mss265.
  32. Faria N.R., Suchard M.A., Abecasis A., Sousa J.D., Ndembi N., Camacho R.J., et al. Phylodynamics of the HIV-1 CRF02_AG clade in Cameroon. Infect. Genet. Evol. 2012; 12(2): 453–60. https://doi.org/10.1016/j.meegid.2011.04.028.
  33. Rambaut A., Pybus O.G., Nelson M.I., Viboud C., Taubenberger J.K., Holmes E.C. The genomic and epidemiological dynamics of human influenza A virus. Nature. 2008; 453(7195): 615–9. https://doi.org/10.1038/nature06945
  34. Новикова Н.А., Епифанова Н.В., Фёдорова О.Ф. Цикличность эпидемического процесса ротавирусного гастроэнтерита и ее причины. В кн.: Материалы научной конференции «Новые технологии в профилактике, диагностике, эпиднадзоре и лечении инфекционных заболеваний». Н. Новгород; 2004: 74–7.
  35. Zeller M., Patton J.T., Heylen E., De Coster S., Ciarlet M., Van Ranst M., et al. Genetic analyses reveal differences in the VP7 and VP4 antigenic epitopes between human rotaviruses circulating in Belgium and rotaviruses in Rotarix and RotaTeq. J. Clin. Microbiol. 2012; 50(3): 966–76. https://doi.org/10.1128/JCM.05590-11.
  36. Morozova O.V., Sashina T.A., Fomina S.G., Novikova N.A. Comparative characteristics of the VP7 and VP4 antigenic epitopes of the rotaviruses circulating in Russia (Nizhniy Novgorod) and the Rotarix and RotaTeq vaccines. Arch. Virol. 2015; 160(7): 1693–703. https://doi.org/10.1007/s00705-015-2439-6.
  37. Motamedi-Rad M., Farahmand M., Arashkia A., Jalilvand S., Shoja Z. VP7 and VP4 genotypes of rotaviruses cocirculating in Iran, 2015 to 2017: Comparison with cogent sequences of Rotarix and RotaTeq vaccine strains before their use for universal mass vaccination. J. Med. Virol. 2020; 92(8): 1110–23. https://doi.org/10.1002/jmv.25642

Copyright (c) 2021 Morozova O.V., Sashina T.F., Novikova N.A.

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