1887

Journal of General Virology header logo

Volume 91, Issue 8

Evolutionary trajectory of the VP1 gene of human enterovirus 71 genogroup B and C viruses Free

Abstract

From 1963 to 1986, human enterovirus 71 (HEV71) infections in the Netherlands were successively caused by viruses of subgenogroups B0, B1 and B2. A genogroup shift occurred in 1987, after which viruses of subgenogroups C1 and C2 were detected exclusively. This is in line with HEV71 typing in Australia, Europe and the USA, but is distinct from that in the Asian Pacific region, where HEV71 subgenogroups B3–B5 and C4–C5 have caused large outbreaks since 1997. To understand these observations in HEV71 epidemiology, the VP1-encoding regions of 199 HEV71 strains isolated in the Netherlands between 1963 and 2008 were used to study the detailed evolutionary trajectory and population dynamics of HEV71. Genogroup B viruses showed an epochal evolution, whereas genogroup C viruses evolved independently, which is in line with the co-circulation of C1 and C2 viruses in the Netherlands since 1997. Considering that strains from the Netherlands are interspersed phylogenetically with GenBank reference strains, the evolution of B1–B2, C1–C2 viruses has a global nature. Phylodynamic analysis confirmed that increased reporting of HEV71 infections in 1986 and 2007 reflected true epidemics of B2 and C2 viruses, respectively. Sequence analysis of the complete capsid region of a subset of isolates revealed several (sub)genogroup-specific residues. Subgenogroup B2-specific rabbit antiserum showed cross-neutralization of B0, B1 and B2 viruses, but not of subgenogroup C1 or C2 viruses, probably explaining the global shift to genogroup C in 1987 following a B2 epidemic. Anti-C1 rabbit serum neutralized both genogroup B and C viruses. Global herd immunity against C1 and C2 viruses possibly explains why epidemics with subgenogroups B4 and C4 are restricted to the Asian Pacific region.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.019695-0
2010-08-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/8/1949.html?itemId=/content/journal/jgv/10.1099/vir.0.019695-0&mimeType=html&fmt=ahah

References

  1. Bible J. M., Iturriza-Gomara M., Megson B., Brown D., Pantelidis P., Earl P., Bendig J., Tong C. Y. 2008; Molecular epidemiology of human enterovirus 71 in the United Kingdom from 1998 to 2006. J Clin Microbiol 46:3192–3200
     [Google Scholar]
  2. Brown B. A., Oberste M. S., Alexander J. P. Jr, Kennett M. L., Pallansch M. A. 1999; Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol 73:9969–9975
     [Google Scholar]
  3. Cardosa M. J., Perera D., Brown B. A., Cheon D., Chan H. M., Chan K. P., Cho H., McMinn P. 2003; Molecular epidemiology of human enterovirus 71 strains and recent outbreaks in the Asia-Pacific region: comparative analysis of the VP1 and VP4 genes. Emerg Infect Dis 9:461–468
     [Google Scholar]
  4. Cello J., Samuelson A., Stalhandske P., Svennerholm B., Jeansson S., Forsgren M. 1993; Identification of group-common linear epitopes in structural and nonstructural proteins of enteroviruses by using synthetic peptides. J Clin Microbiol 31:911–916
     [Google Scholar]
  5. Chu P. Y., Lin K. H., Hwang K. P., Chou L. C., Wang C. F., Shih S. R., Wang J. R., Shimada Y., Ishiko H. 2001; Molecular epidemiology of enterovirus 71 in Taiwan. Arch Virol 146:589–600
     [Google Scholar]
  6. Drummond A. J., Rambaut A. 2007; beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
     [Google Scholar]
  7. Drummond A. J., Rambaut A., Shapiro B., Pybus O. G. 2005; Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192
     [Google Scholar]
  8. Drummond A. J., Ho S. Y., Phillips M. J., Rambaut A. 2006; Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88
     [Google Scholar]
  9. Foo D. G. W., Alonso S., Phoon M. C., Ramachandran N. P., Kwong Chow V. T., Poh C. L. 2007; Identification of neutralizing linear epitopes from the VP1 capsid protein of enterovirus 71 using synthetic peptides. Virus Res 125:61–68
     [Google Scholar]
  10. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
     [Google Scholar]
  11. Huang S. W., Hsu Y. W., Smith D. J., Kiang D., Tsai H. P., Lin K. H., Wang S. M., Liu C. C., Su I. J., Wang J. R. 2009; Reemergence of enterovirus 71 in 2008 in Taiwan: dynamics of genetic and antigenic evolution from 1998 to 2008. J Clin Microbiol 47:3653–3662
     [Google Scholar]
  12. Kärber G. 1931; Beitrag zur kollektiven behandlung pharmakologischer reihenversuce. Arch Exp Pathol Pharmakol 162:480–483 (in German
    [Google Scholar]
  13. Kozakovsky Pond S. L., Frost S. D. W., Muse S. V. 2005; HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679
     [Google Scholar]
  14. Kung S. H., Wang S. F., Huang C. W., Hsu C. C., Liu H. F., Yang J. Y. 2007; Genetic and antigenic analyses of enterovirus 71 isolates in Taiwan during 1998–2005. Clin Microbiol Infect 13:782–787
     [Google Scholar]
  15. Li L., He Y., Yang H., Zhu J., Xu X., Dong J., Zhu Y., Jin Q. 2005; Genetic characteristics of human enterovirus 71 and coxsackievirus A16 circulating from 1999 to 2004 in Shenzhen, People's Republic of China. J Clin Microbiol 43:3835–3839
     [Google Scholar]
  16. Lin Y. W., Chang K. C., Kao C. M., Chang S. P., Tung Y. Y., Chen S. H. 2009; Lymphocyte and antibody responses reduce enterovirus 71 lethality in mice by decreasing tissue viral loads. J Virol 83:6477–6483
     [Google Scholar]
  17. McMinn P., Lindsay K., Perera D., Chan H. M., Chan K. P., Cardosa M. J. 2001; Phylogenetic analysis of enterovirus 71 strains isolated during linked epidemics in Malaysia, Singapore, and Western Australia. J Virol 75:7732–7738
     [Google Scholar]
  18. Mizuta K., Abiko C., Murata T., Matsuzaki Y., Itagaki T., Sanjoh K., Sakamoto M., Hongo S., Murayama S., Hayasaka K. 2005; Frequent importation of enterovirus 71 from surrounding countries into the local community of Yamagata, Japan, between 1998 and 2003. J Clin Microbiol 43:6171–6175
     [Google Scholar]
  19. Mizuta K., Aoki Y., Suto A., Ootani K., Katsushima N., Itagaki T., Ohmi A., Okamoto M., Nishimura H. other authors 2009; Cross-antigenicity among EV71 strains from different genogroups isolated in Yamagata, Japan, between 1990 and 2007. Vaccine 27:3153–3158
     [Google Scholar]
  20. Perez-Velez C. M., Anderson M. S., Robinson C. C., McFarland E. J., Nix W. A., Pallansch M. A., Oberste M. S., Glode M. P. 2007; Outbreak of neurologic enterovirus type 71 disease: a diagnostic challenge. Clin Infect Dis 45:950–957
     [Google Scholar]
  21. Rambaut A., Pybus O. G., Nelson M. I., Viboud C., Taubenberger J. K., Holmes E. C. 2008; The genomic and epidemiological dynamics of human influenza A virus. Nature 453:615–619
     [Google Scholar]
  22. Samuelson A., Forsgren M., Johansson B., Wahren B., Sallberg M. 1994; Molecular basis for serological cross-reactivity between enteroviruses. Clin Diagn Lab Immunol 1:336–341
     [Google Scholar]
  23. Sanders S. A., Herrero L. J., McPhie K., Chow S. S., Craig M. E., Dwyer D. E., Rawlinson W., McMinn P. C. 2006; Molecular epidemiology of enterovirus 71 over two decades in an Australian urban community. Arch Virol 151:1003–1013
     [Google Scholar]
  24. Sivasamugham L. A., Cardosa M. J., Tan W. S., Yusoff K. 2006; Recombinant Newcastle disease virus capsids displaying enterovirus 71 VP1 fragment induce a strong immune response in rabbits. J Med Virol 78:1096–1104
     [Google Scholar]
  25. Tu P. V., Thao N. T., Perera D., Huu T. K., Tien N. T., Thuong T. C., How O. M., Cardosa M. J., McMinn P. C. 2007; Epidemiologic and virologic investigation of hand, foot, and mouth disease, Southern Vietnam, 2005. Emerg Infect Dis 13:1733–1741
     [Google Scholar]
  26. van der Sanden S., Koopmans M., Uslu G., van der Avoort H. 2009; Epidemiology of enterovirus 71 in the Netherlands; 1963 to 2008 J Clin Microbiol 47:2826–2833
     [Google Scholar]
  27. von Zeipel G. 1979; Neutralisation of aggregated strains of enterovirus 71 and echovirus type 4 in RD and Vero or GMK-AH1 cells. Acta Pathol Microbiol Scand B 87B:71–73
     [Google Scholar]
  28. Wang S. M., Liu C. C. 2009; Enterovirus 71: epidemiology, pathogenesis and management. Expert Rev Anti Infect Ther 7:735–742
     [Google Scholar]
  29. Wu S. C., Liu C. C., Lian W. C. 2004; Optimization of microcarrier cell culture process for the inactivated enterovirus type 71 vaccine development. Vaccine 22:3858–3864
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.019695-0
Loading
Evolutionary trajectory of the VP1 gene of human enterovirus 71 genogroup B and C viruses
J. Gen. Virol. 91, 1949 (2010); https://doi.org/10.1099/vir.0.019695-0
/content/journal/jgv/10.1099/vir.0.019695-0
/content/journal/jgv/10.1099/vir.0.019695-0
Loading

Data & Media loading...

Supplements

Supplementary material 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