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Abstract

Virologic surveillance is a critical component of measles management. One of the criteria for verification of elimination of endemic measles is genetic analysis of wild-type viruses to demonstrate lack of an indigenous genotype. Measles is yet to be eliminated in China, and genotype H1 has been detected continuously since virologic surveillance was initiated in 1993. Virologic surveillance has been very active in China, providing a unique opportunity to conduct a detailed study of the evolution of a single, endemic genotype over a timespan of nearly two decades. Phylogenetic analysis performed on the 450 nt coding sequence for the C-terminal 150 amino acids of the nucleoprotein (N-450), fusion (F) gene and haemagglutinin (H) gene confirmed the continued circulation of genotype H1 viruses for 19 years. No evidence of selective pressure for the H protein was found. The substitution rates ranged from 0.75×10 substitutions site year for H to 1.65×10 substitutions site year for N-450. The time of most recent common ancestor (TMRCA) for genotype H1 was estimated as approximately 1985 (95 % highest probability density, 1979–1989). Finally, the overall diversity of measles sequences from China decreased from 2005 to 2012, coincident with a substantial decrease in measles cases. The results suggest that detailed evolutionary analyses should facilitate the documentation of eventual measles elimination in China. Moreover, the molecular approaches used in this study can be applied in other countries approaching measles elimination.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2014-09-01
2024-04-20
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References

  1. Anonymous. 2013; Global Vaccine Action Plan: decade of vaccines collaboration. Vaccine 31:Suppl 2B5–B31 [View Article][PubMed]
    [Google Scholar]
  2. Domingo E., Holland J. J. 1997; RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178 [View Article][PubMed]
    [Google Scholar]
  3. 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 [View Article][PubMed]
    [Google Scholar]
  4. Drummond A. J., Suchard M. A., Xie D., Rambaut A. 2012; Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973 [View Article][PubMed]
    [Google Scholar]
  5. Duffy S., Shackelton L. A., Holmes E. C. 2008; Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276 [View Article][PubMed]
    [Google Scholar]
  6. Edgar R. C. 2004; MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  7. Efron B., Tibshirani R. J. 1994 An Introduction to the Bootstrap Boca Raton: CRC Press;
    [Google Scholar]
  8. Griffin D. E. B., Bellini W. J. 1996; Measles viruses. In Fields Virology, 3rd edn. pp. 1267–1296 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott-Raven;
    [Google Scholar]
  9. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [View Article][PubMed]
    [Google Scholar]
  10. Hahné S., van Houdt R., Koedijk F., van Ballegooijen M., Cremer J., Bruisten S., Coutinho R., Boot H. 2013; Selective hepatitis B virus vaccination has reduced hepatitis B virus transmission in the Netherlands. PLoS ONE 8:e67866 [View Article][PubMed]
    [Google Scholar]
  11. Ji Y., Zhang Y., Xu S., Zhu Z., Zuo S., Jiang X., Lu P., Wang C., Liang Y. other authors 2009; Measles resurgence associated with continued circulation of genotype H1 viruses in China, 2005. Virol J 6:135 [View Article][PubMed]
    [Google Scholar]
  12. Ji Y., Xu S., Zhang Y., Zhu Z., Mao N., Jiang X., Ma C., Lu P., Wang C. other authors 2010; Genetic characterization of wild-type measles viruses isolated in China, 2006-2007. Virol J 7:105 [View Article][PubMed]
    [Google Scholar]
  13. Kobune F., Sakata H., Sugiura A. 1990; Marmoset lymphoblastoid cells as a sensitive host for isolation of measles virus. J Virol 64:700–705[PubMed]
    [Google Scholar]
  14. Mahar J. E., Bok K., Green K. Y., Kirkwood C. D. 2013; The importance of intergenic recombination in norovirus GII.3 evolution. J Virol 87:3687–3698 [View Article][PubMed]
    [Google Scholar]
  15. Mizuta K., Saitoh M., Kobayashi M., Tsukagoshi H., Aoki Y., Ikeda T., Abiko C., Katsushima N., Itagaki T. other authors 2011; Detailed genetic analysis of hemagglutinin-neuraminidase glycoprotein gene in human parainfluenza virus type 1 isolates from patients with acute respiratory infection between 2002 and 2009 in Yamagata prefecture, Japan. Virol J 8:533 [View Article][PubMed]
    [Google Scholar]
  16. Ono N., Tatsuo H., Hidaka Y., Aoki T., Minagawa H., Yanagi Y. 2001; Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J Virol 75:4399–4401 [View Article][PubMed]
    [Google Scholar]
  17. Perry R. T., Gacic-Dobo M., Dabbagh A., Mulders M. N., Strebel P. M., Okwo-Bele J. M., Rota P. A., Goodson J. L. Centers for Disease Control and Prevention (CDC) 2014; Global control and regional elimination of measles, 2014. MMWR Morb Mortal Wkly Rep 63:103–107[PubMed]
    [Google Scholar]
  18. Pomeroy L. W., Bjørnstad O. N., Holmes E. C. 2008; The evolutionary and epidemiological dynamics of the paramyxoviridae. J Mol Evol 66:98–106 [View Article][PubMed]
    [Google Scholar]
  19. Pond S. L., Frost S. D. 2005; Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533 [View Article][PubMed]
    [Google Scholar]
  20. Posada D. 2008; jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256 [View Article][PubMed]
    [Google Scholar]
  21. Pretorius M. A., van Niekerk S., Tempia S., Moyes J., Cohen C., Madhi S. A., Venter M. SARI Surveillance Group 2013; Replacement and positive evolution of subtype A and B respiratory syncytial virus G-protein genotypes from 1997-2012 in South Africa. J Infect Dis 208:Suppl 3S227–S237 [View Article][PubMed]
    [Google Scholar]
  22. Rambaut A., Drummond A. 2010; FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh; Edinburgh, UK: http://tree.bio.ed.ac.uk/software/figtree/
    [Google Scholar]
  23. Rima B. K., Earle J. A., Baczko K., ter Meulen V., Liebert U. G., Carstens C., Carabaña J., Caballero M., Celma M. L., Fernandez-Muñoz R. 1997; Sequence divergence of measles virus haemagglutinin during natural evolution and adaptation to cell culture. J Gen Virol 78:97–106[PubMed]
    [Google Scholar]
  24. Rota P. A., Brown K., Mankertz A., Santibanez S., Shulga S., Muller C. P., Hübschen J. M., Siqueira M., Beirnes J. other authors 2011; Global distribution of measles genotypes and measles molecular epidemiology. J Infect Dis 204:Suppl 1S514–S523 [View Article][PubMed]
    [Google Scholar]
  25. Saitoh M., Takeda M., Gotoh K., Takeuchi F., Sekizuka T., Kuroda M., Mizuta K., Ryo A., Tanaka R. other authors 2012; Molecular evolution of hemagglutinin (H) gene in measles virus genotypes D3, D5, D9, and H1. PLoS ONE 7:e50660 [View Article][PubMed]
    [Google Scholar]
  26. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
    [Google Scholar]
  27. Stadler T., Kühnert D., Bonhoeffer S., Drummond A. J. 2013; Birth-death skyline plot reveals temporal changes of epidemic spread in HIV and hepatitis C virus (HCV). Proc Natl Acad Sci U S A 110:228–233 [View Article][PubMed]
    [Google Scholar]
  28. 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 [CrossRef]
    [Google Scholar]
  29. Wei C., Shi J., Liu B., Shi Y., Zheng J., Xu G., Ma J., Wang G., Li F. 2012; Molecular characterization of the measles virus genotypes in JiLin Province, China. PLoS ONE 7:e46011 [View Article][PubMed]
    [Google Scholar]
  30. WHO 2012a; The Measles & Rubella Initiative Welcomes World Health Assembly Commitment to Measles and Rubella Elimination Goals.
    [Google Scholar]
  31. WHO 2012b; Measles virus nomenclature update: 2012. Wkly Epidemiol Rec 87:73–81[PubMed]
    [Google Scholar]
  32. Woelk C. H., Pybus O. G., Jin L., Brown D. W., Holmes E. C. 2002; Increased positive selection pressure in persistent (SSPE) versus acute measles virus infections. J Gen Virol 83:1419–1430[PubMed]
    [Google Scholar]
  33. Xu W., Tamin A., Rota J. S., Zhang L., Bellini W. J., Rota P. A. 1998; New genetic group of measles virus isolated in the People’s Republic of China. Virus Res 54:147–156 [View Article][PubMed]
    [Google Scholar]
  34. Zhang Y., Zhu Z., Rota P. A., Jiang X., Hu J., Wang J., Tang W., Zhang Z., Li C. other authors 2007; Molecular epidemiology of measles viruses in China, 1995-2003. Virol J 4:14 [View Article][PubMed]
    [Google Scholar]
  35. Zhang Y., Ji Y., Jiang X., Xu S., Zhu Z., Zheng L., He J., Ling H., Wang Y. other authors 2008; Genetic characterization of measles viruses in China, 2004. Virol J 5:120 [View Article][PubMed]
    [Google Scholar]
  36. Zhang Y., Zhou J., Bellini W. J., Xu W., Rota P. A. 2009; Genetic characterization of Chinese measles vaccines by analysis of complete genomic sequences. J Med Virol 81:1477–1483 [View Article][PubMed]
    [Google Scholar]
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