1887

Abstract

The transient upsurge of G2P[4] group A rotavirus (RVA) after Rotarix vaccine introduction in several countries has been a matter of concern. To gain insight into the diversity and evolution of G2P[4] strains in South Africa pre- and post-RVA vaccination introduction, whole-genome sequencing was performed for RVA positive faecal specimens collected between 2003 and 2017 and samples previously sequenced were obtained from GenBank (=103; 56 pre- and 47 post-vaccine). Pre-vaccine G2 sequences predominantly clustered within sub-lineage IVa-1. In contrast, post-vaccine G2 sequences clustered mainly within sub-lineage IVa-3, whereby a radical amino acid (AA) substitution, S15F, was observed between the two sub-lineages. Pre-vaccine P[4] sequences predominantly segregated within sub-lineage IVa while post-vaccine sequences clustered mostly within sub-lineage IVb, with a radical AA substitution R162G. Both S15F and R162G occurred outside recognised antigenic sites. The AA residue at position 15 is found within the signal sequence domain of Viral Protein 7 (VP7) involved in translocation of VP7 into endoplasmic reticulum during infection process. The 162 AA residue lies within the hemagglutination domain of Viral Protein 4 (VP4) engaged in interaction with sialic acid-containing structure during attachment to the target cell. Free energy change analysis on VP7 indicated accumulation of stable point mutations in both antigenic and non-antigenic regions. The segregation of South African G2P[4] strains into pre- and post-vaccination sub-lineages is likely due to erstwhile hypothesized stepwise lineage/sub-lineage evolution of G2P[4] strains rather than RVA vaccine introduction. Our findings reinforce the need for continuous whole-genome RVA surveillance and investigation of contribution of AA substitutions in understanding the dynamic G2P[4] epidemiology.

Funding
This study was supported by the:
  • National Research Foundation (Award (NRF-120814))
    • Principle Award Recipient: MartinM Nyaga
  • Poliomyelitis Research Foundation (Award (PRF-19/16))
    • Principle Award Recipient: MartinM Nyaga
  • South African Medical Research Council (Award Self-Initiated Research grant (SIR),)
    • Principle Award Recipient: MartinM Nyaga
  • Bill and Melinda Gates Foundation (Award BMGF-OPP1180423_2017)
    • Principle Award Recipient: MartinM Nyaga
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000809
2022-04-21
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/4/mgen000809.html?itemId=/content/journal/mgen/10.1099/mgen.0.000809&mimeType=html&fmt=ahah

References

  1. Troeger C, Khalil IA, Rao PC, Cao S, Blacker BF et al. Rotavirus vaccination and the global burden of rotavirus diarrhea among children younger than 5 years. JAMA Pediatr 2018; 172:958–965 [View Article] [PubMed]
    [Google Scholar]
  2. Estes MK, Greenberg HB. Rotaviruses. In Knipe DM, Howley PM. eds Fields Virology, 6th ed. Philadelphia (PA): Wolters Kluwer Heath/Lippincott Williams and Wilkins; 2013 pp 1347–1401
    [Google Scholar]
  3. Estes MK, Kapikian AZ et al. Rotaviruses. In Knipe D, Griffin D, Lamb R, Martin M, Roizman B. eds Fields Virology Philadelphia (PA): Wolters Kluwer Health/Lippincott Williams and Wilkins; 2007 pp 1917–1975
    [Google Scholar]
  4. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Bányai K et al. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 2011; 156:1397–1413 [View Article] [PubMed]
    [Google Scholar]
  5. Virus Classification Rega.kuleuven.be; 2021 https://rega.kuleuven.be/cev/viralmetagenomics/virus-classification accessed 13 December 2021
  6. Dóró R, László B, Martella V, Leshem E, Gentsch J et al. Review of global rotavirus strain prevalence data from six years post vaccine licensure surveillance: is there evidence of strain selection from vaccine pressure. Infect Genet Evol 2014; 28:446–461 [View Article] [PubMed]
    [Google Scholar]
  7. Matthijnssens J, Van Ranst M. Genotype constellation and evolution of group A rotaviruses infecting humans. Curr Opin Virol 2012; 2:426–433 [View Article] [PubMed]
    [Google Scholar]
  8. Doan YH, Nakagomi T, Cunliffe NA, Pandey BD, Sherchand JB et al. The occurrence of amino acid substitutions D96N and S242N in VP7 of emergent G2P [4] rotaviruses in Nepal in 2004-2005: a global and evolutionary perspective. Arch Virol 2011; 156:1960–1978 [View Article] [PubMed]
    [Google Scholar]
  9. Vizzi E, Piñeros OA, Oropeza MD, Naranjo L, Suárez JA et al. Human rotavirus strains circulating in Venezuela after vaccine introduction: predominance of G29 [P4] and reemergence of G1P [8]. Virol J 2017; 14:1–4 [View Article] [PubMed]
    [Google Scholar]
  10. Khandoker N, Thongprachum A, Takanashi S, Okitsu S, Nishimura S et al. Molecular epidemiology of rotavirus gastroenteritis in Japan during 2014-2015: Characterization of re-emerging G2P[4] after rotavirus vaccine introduction. J Med Virol 2018; 90:1040–1046 [View Article] [PubMed]
    [Google Scholar]
  11. Thanh HD, Tran VT, Lim I, Kim W. Emergence of Human G2P[4] Rotaviruses in the Post-vaccination Era in South Korea: Footprints of Multiple Interspecies Re-assortment Events. Sci Rep 2018; 8:1–10 [View Article] [PubMed]
    [Google Scholar]
  12. Braeckman T, Van Herck K, Meyer N, Pirçon J-Y, Soriano-Gabarró M et al. Effectiveness of rotavirus vaccination in prevention of hospital admissions for rotavirus gastroenteritis among young children in Belgium: case-control study. BMJ 2012; 345:e4752 [View Article] [PubMed]
    [Google Scholar]
  13. Bar-Zeev N, Jere KC, Bennett A, Pollock L, Tate JE et al. Population impact and effectiveness of monovalent rotavirus vaccination in urban Malawian children 3 years after vaccine introduction: ecological and case-control analyses. Clin Infect Dis 2016; 62 Suppl 2:S213–9 [View Article] [PubMed]
    [Google Scholar]
  14. Parashar UD, Gibson CJ, Bresee JS, Glass RI. Rotavirus and severe childhood diarrhea. Emerg Infect Dis 2006; 12:304–306 [View Article] [PubMed]
    [Google Scholar]
  15. World Health Organization Meeting of the immunization Strategic Advisory Group of Experts, April 2009—conclusions and recommendations. WER 2009; 84:220–236 [View Article]
    [Google Scholar]
  16. Msimang VMY, Page N, Groome MJ, Moyes J, Cortese MM et al. Impact of rotavirus vaccine on childhood diarrheal hospitalization after introduction into the South African public immunization program. Pediatr Infect Dis J 2013; 32:1359–1364 [View Article] [PubMed]
    [Google Scholar]
  17. Steele AD, Groome MJ. Measuring Rotavirus Vaccine Impact in Sub-Saharan Africa. Clin Infect Dis 2020; 70:2314–2316 [View Article] [PubMed]
    [Google Scholar]
  18. Leshem E, Lopman B, Glass R, Gentsch J, Bányai K et al. Distribution of rotavirus strains and strain-specific effectiveness of the rotavirus vaccine after its introduction: a systematic review and meta-analysis. Lancet Infect Dis 2014; 14:847–856 [View Article] [PubMed]
    [Google Scholar]
  19. Bibera GL, Chen J, Pereira P, Benninghoff B. Dynamics of G2P[4] strain evolution and rotavirus vaccination: A review of evidence for Rotarix. Vaccine 2020; 38:5591–5600 [View Article] [PubMed]
    [Google Scholar]
  20. Gurgel RQ, Cuevas LE, Vieira SCF, Barros VCF, Fontes PB et al. Predominance of rotavirus P[4]G2 in a vaccinated population, Brazil. Emerg Infect Dis 2007; 13:1571–1573 [View Article] [PubMed]
    [Google Scholar]
  21. Donato C. Molecular epidemiology of rotavirus in the era of vaccination. Microbiol Aust 2012; 33:64 [View Article]
    [Google Scholar]
  22. Al-Ayed MSZ, Asaad AM, Qureshi MA, Hawan AA. Epidemiology of group A rotavirus infection after the introduction of monovalent vaccine in the National Immunization Program of Saudi Arabia. J Med Virol 2017; 89:429–434 [View Article] [PubMed]
    [Google Scholar]
  23. Zeller M, Heylen E, Tamim S, McAllen JK, Kirkness EF et al. Comparative analysis of the Rotarix vaccine strain and G1P[8] rotaviruses detected before and after vaccine introduction in Belgium. PeerJ 2017; 5:e2733 [View Article] [PubMed]
    [Google Scholar]
  24. Mhango C, Mandolo JJ, Chinyama E, Wachepa R, Kanjerwa O et al. Rotavirus Genotypes in Hospitalized Children with Acute Gastroenteritis Before and After Rotavirus Vaccine Introduction in. J Infect Dis 2020jiaa616 [View Article] [PubMed]
    [Google Scholar]
  25. Simwaka JC, Mpabalwani EM, Seheri M, Peenze I, Monze M et al. Diversity of rotavirus strains circulating in children under five years of age who presented with acute gastroenteritis before and after rotavirus vaccine introduction. Vaccine 2018; 36:7243–7247 [View Article] [PubMed]
    [Google Scholar]
  26. Wandera EA, Mohammad S, Bundi M, Komoto S, Nyangao J et al. Impact of rotavirus vaccination on rotavirus and all-cause gastroenteritis in peri-urban Kenyan children. Vaccine 2017; 35:5217–5223 [View Article] [PubMed]
    [Google Scholar]
  27. Mokomane M, Esona MD, Bowen MD, Tate JE, Steenhoff AP et al. Diversity of Rotavirus Strains Circulating in Botswana before and after introduction of the Monovalent Rotavirus Vaccine. Vaccine 2019; 37:6324–6328 [View Article] [PubMed]
    [Google Scholar]
  28. Page NA, Steele AD. Antigenic and genetic characterization of serotype G2 human rotavirus strains from South Africa from 1984 to 1998. J Med Virol 2004; 72:320–327 [View Article] [PubMed]
    [Google Scholar]
  29. Linhares AC, Justino MCA. Rotavirus vaccination in Brazil: effectiveness and health impact seven years post-introduction. Expert Rev Vaccines 2014; 13:43–57 [View Article] [PubMed]
    [Google Scholar]
  30. Patton JT. Rotavirus diversity and evolution in the post-vaccine world. Discov Med 2012; 13:68
    [Google Scholar]
  31. Pitzer VE, Patel MM, Lopman BA, Viboud C, Parashar UD et al. Modeling rotavirus strain dynamics in developed countries to understand the potential impact of vaccination on genotype distributions. Proc Natl Acad Sci U S A 2011; 108:19353–19358 [View Article] [PubMed]
    [Google Scholar]
  32. Dennis AF, McDonald SM, Payne DC, Mijatovic-Rustempasic S, Esona MD et al. Molecular epidemiology of contemporary G2P[4] human rotaviruses cocirculating in a single U.S. community: footprints of a globally transitioning genotype. J Virol 2014; 88:3789–3801 [View Article] [PubMed]
    [Google Scholar]
  33. Page NA, Seheri LM, Groome MJ, Moyes J, Walaza S et al. Temporal association of rotavirus vaccination and genotype circulation in South Africa: Observations from 2002 to 2014. Vaccine 2018; 36:7231–7237 [View Article] [PubMed]
    [Google Scholar]
  34. Doan YH, Nakagomi T, Agbemabiese CA, Nakagomi O. Changes in the distribution of lineage constellations of G2P[4] Rotavirus A strains detected in Japan over 32 years (1980-2011). Infect Genet Evol 2015; 34:423–433 [View Article] [PubMed]
    [Google Scholar]
  35. Seheri M, Nemarude L, Peenze I, Netshifhefhe L, Nyaga MM et al. Update of rotavirus strains circulating in Africa from 2007 through 2011. Pediatr Infect Dis J 2014; 33 Suppl 1:S76–84 [View Article] [PubMed]
    [Google Scholar]
  36. Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M et al. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 1992; 30:1365–1373 [View Article] [PubMed]
    [Google Scholar]
  37. Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF et al. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 1990; 28:276–282 [View Article] [PubMed]
    [Google Scholar]
  38. Maringa WM, Mwangi PN, Simwaka J, Mpabalwani EM, Mwenda JM et al. Molecular characterisation of a rare reassortant porcine-like G5P[6] rotavirus strain detected in an unvaccinated child in Kasama, Zambia. Pathogens 2020; 9:E663 [View Article] [PubMed]
    [Google Scholar]
  39. Potgieter AC, Page NA, Liebenberg J, Wright IM, Landt O et al. Improved strategies for sequence-independent amplification and sequencing of viral double-stranded RNA genomes. J Gen Virol 2009; 90:1423–1432 [View Article] [PubMed]
    [Google Scholar]
  40. Mwangi PN, Mogotsi MT, Seheri ML, Mphahlele MJ, Peenze I et al. Whole Genome In-Silico Analysis of South African G1P[8] Rotavirus Strains Before and After Vaccine Introduction Over A Period of 14 Years. Vaccines (Basel) 2020; 8:609 [View Article] [PubMed]
    [Google Scholar]
  41. Andrews SF. A quality control tool for high throughput sequence data; 2010
  42. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article] [PubMed]
    [Google Scholar]
  43. Pickett BE, Sadat EL, Zhang Y, Noronha JM, Squires RB et al. ViPR: an open bioinformatics database and analysis resource for virology research. Nucleic Acids Res 2012; 40:D593–8 [View Article] [PubMed]
    [Google Scholar]
  44. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  45. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  46. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article]
    [Google Scholar]
  47. GitHub Tamuri/treesub [Internet]; 2021 https://github.com/tamuri/treesub
  48. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007; 24:1586–1591 [View Article] [PubMed]
    [Google Scholar]
  49. Kalica AR, Greenberg HB, Espejo RT, Flores J, Wyatt RG et al. Distinctive ribonucleic acid patterns of human rotavirus subgroups 1 and 2. Infect Immun 1981; 33:958–961 [View Article] [PubMed]
    [Google Scholar]
  50. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 2018; 46:W296–W303 [View Article] [PubMed]
    [Google Scholar]
  51. Aoki ST, Settembre EC, Trask SD, Greenberg HB, Harrison SC et al. Structure of rotavirus outer-layer protein VP7 bound with a neutralizing Fab. Science 2009; 324:1444–1447 [View Article] [PubMed]
    [Google Scholar]
  52. DeLano WL. Pymol: An open-source molecular graphics tool. CCP4 Newsletter on protein crystallography 2002; 40:82–92
    [Google Scholar]
  53. Blanchard H, Yu X, Coulson BS, von Itzstein M. Insight into host cell carbohydrate-recognition by human and porcine rotavirus from crystal structures of the virion spike associated carbohydrate-binding domain (VP8. J Mol Biol 2007; 367:1215–1226 [View Article] [PubMed]
    [Google Scholar]
  54. Van Durme J, Delgado J, Stricher F, Serrano L, Schymkowitz J et al. A graphical interface for the FoldX forcefield. Bioinformatics 2011; 27:1711–1712 [View Article] [PubMed]
    [Google Scholar]
  55. Krieger E, Vriend G. YASARA View—molecular graphics for all devices—from smartphones to workstations. Bioinformatics 2014; 30:2981–2982 [View Article] [PubMed]
    [Google Scholar]
  56. Weaver S, Shank SD, Spielman SJ, Li M, Muse SV et al. Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol Biol Evol 2018; 35:773–777 [View Article] [PubMed]
    [Google Scholar]
  57. Kosakovsky Pond SL, Frost SDW. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 2005; 22:1208–1222 [View Article] [PubMed]
    [Google Scholar]
  58. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K et al. Detecting individual sites subject to episodic diversifying selection. PLoS Genet 2012; 8:e1002764 [View Article] [PubMed]
    [Google Scholar]
  59. Murrell B, Moola S, Mabona A, Weighill T, Sheward D et al. FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 2013; 30:1196–1205 [View Article]
    [Google Scholar]
  60. Burke RM, Tate JE, Kirkwood CD, Steele AD, Parashar UD. Current and new rotavirus vaccines. Curr Opin Infect Dis 2019; 32:435–444 [View Article] [PubMed]
    [Google Scholar]
  61. Franco MA, Tin C, Greenberg HB. CD8+ T cells can mediate almost complete short-term and partial long-term immunity to rotavirus in mice. J Virol 1997; 71:4165–4170 [View Article] [PubMed]
    [Google Scholar]
  62. Betts MJ, Russell RB. Amino acid properties and consequences of substitutions. Bioinformatics for geneticists 2003; 317:289
    [Google Scholar]
  63. Dormitzer PR, Sun Z-YJ, Wagner G, Harrison SC. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 2002; 21:885–897 [View Article] [PubMed]
    [Google Scholar]
  64. Agbemabiese CA, Nakagomi T, Damanka SA, Dennis FE, Lartey BL et al. Sub-genotype phylogeny of the non-G, non-P genes of genotype 2 Rotavirus A strains. PLoS One 2019; 14:e0217422 [View Article] [PubMed]
    [Google Scholar]
  65. Maiorov VN, Crippen GM. Significance of root-mean-square deviation in comparing three-dimensional structures of globular proteins. J Mol Biol 1994; 235:625–634 [View Article] [PubMed]
    [Google Scholar]
  66. Piron M, Delaunay T, Grosclaude J, Poncet D. Identification of the RNA-binding, dimerization, and eIF4GI-binding domains of rotavirus nonstructural protein NSP3. J Virol 1999; 73:5411–5421 [View Article] [PubMed]
    [Google Scholar]
  67. Charpilienne A, Lepault J, Rey F, Cohen J. Identification of rotavirus VP6 residues located at the interface with VP2 that are essential for capsid assembly and transcriptase activity. J Virol 2002; 76:7822–7831 [View Article] [PubMed]
    [Google Scholar]
  68. Dormitzer PR, Sun Z-YJ, Wagner G, Harrison SC. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 2002; 21:885–897 [View Article] [PubMed]
    [Google Scholar]
  69. McDonald SM, Patton JT. Rotavirus VP2 core shell regions critical for viral polymerase activation. J Virol 2011; 85:3095–3105 [View Article] [PubMed]
    [Google Scholar]
  70. Viskovska M, Anish R, Hu L, Chow D-C, Hurwitz AM et al. Probing the sites of interactions of rotaviral proteins involved in replication. J Virol 2014; 88:12866–12881 [View Article] [PubMed]
    [Google Scholar]
  71. Donato CM, Zhang ZA, Donker NC, Kirkwood CD. Characterization of G2P[4] rotavirus strains associated with increased detection in Australian states using the RotaTeq® vaccine during the 2010-2011 surveillance period. Infect Genet Evol 2014; 28:398–412 [View Article] [PubMed]
    [Google Scholar]
  72. Nyaga MM, Stucker KM, Esona MD, Jere KC, Mwinyi B et al. Whole-genome analyses of DS-1-like human G2P[4] and G8P[4] rotavirus strains from Eastern, Western and Southern Africa. Virus Genes 2014; 49:196–207 [View Article] [PubMed]
    [Google Scholar]
  73. Agbemabiese CA, Nakagomi T, Doan YH, Do LP, Damanka S et al. Genomic constellation and evolution of Ghanaian G2P[4] rotavirus strains from a global perspective. Infect Genet Evol 2016; 45:122–131 [View Article] [PubMed]
    [Google Scholar]
  74. Stirzaker SC, Poncet D, Both GW. Sequences in rotavirus glycoprotein VP7 that mediate delayed translocation and retention of the protein in the endoplasmic reticulum. J Cell Biol 1990; 111:1343–1350 [View Article] [PubMed]
    [Google Scholar]
  75. Gómez MM, de Mendonça MCL, Volotão E de M, Tort LFL, da Silva MFM et al. Rotavirus A genotype P[4]G2: genetic diversity and reassortment events among strains circulating in Brazil between 2005 and 2009. J Med Virol 2011; 83:1093–1106 [View Article] [PubMed]
    [Google Scholar]
  76. Giammanco GM, Bonura F, Zeller M, Heylen E, Van Ranst M et al. Evolution of DS-1-like human G2P[4] rotaviruses assessed by complete genome analyses. J Gen Virol 2014; 95:91–109 [View Article] [PubMed]
    [Google Scholar]
  77. Fuentes-Pananá EM, López S, Gorziglia M, Arias CF. Mapping the hemagglutination domain of rotaviruses. J Virol 1995; 69:2629–2632 [View Article] [PubMed]
    [Google Scholar]
  78. Gualtero DF, Guzmán F, Acosta O, Guerrero CA. Amino acid domains 280–297 of VP6 and 531–554 of VP4 are implicated in heat shock cognate protein hsc70-mediated rotavirus infection. Arch Virol 2007; 152:2183–2196 [View Article] [PubMed]
    [Google Scholar]
  79. Ogden KM, Snyder MJ, Dennis AF, Patton JT. Predicted structure and domain organization of rotavirus capping enzyme and innate immune antagonist VP3. J Virol 2014; 88:9072–9085 [View Article] [PubMed]
    [Google Scholar]
  80. Seo NS, Zeng CQ, Hyser JM, Utama B, Crawford SE et al. Integrins α1β1 and α2β1 are receptors for the rotavirus enterotoxin. PNAS 2008; 105:8811–8818 [View Article]
    [Google Scholar]
  81. Akashi H. Gene expression and molecular evolution. Curr Opin Genet Dev 2001; 11:660–666 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000809
Loading
/content/journal/mgen/10.1099/mgen.0.000809
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Supplementary material 3

EXCEL

Supplementary material 4

EXCEL
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