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Volume 85, Issue 2

Evolution of wild-type 1 poliovirus in two healthy siblings excreting the virus over a period of 6 months Free

Abstract

Wild-type 1 poliovirus (wtPV1) strains were isolated from two young healthy brothers shortly after arrival in Finland from Somalia in 1993. Twelve (sibling A) and 18 (sibling B) specimens collected over a period of more than 6 months yielded wtPV1. Partial sequences obtained from the one and two earliest isolates from sibling A and B, respectively, were nearly identical, differing from each other by only one or two nucleotides. Subsequently, the virus evolved separately in both siblings so that maximal differences between strains derived from a given subject peaked at 2·2 % for sibling A, at 1·5 % for sibling B and at 2·5 % between the two siblings in the VP1-coding part of the genome. All substitutions in the 150 nt VP1–2A junction region were synonymous, whereas as many as eight of the 31 variable positions in the remaining VP1-coding region encoded amino acid replacements in at least one strain. Probable structural locations of the variable amino acid positions were mapped to the published PV1/Mahoney structural model. Most of the substitutions occurred around the fivefold axis in motifs that are known to be or suspected to be targets of neutralizing antibodies. We suggest that the striking genetic divergence observed between the strains was based on a combination of bottleneck transmission events and antigenic drift during the prolonged period of poliovirus replication.

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2004-02-01
2024-04-28
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References

  1. Alexander J. P. Jr, Gary H. E. Jr, Pallansch M. A. 1997; Duration of poliovirus excretion and its implications for acute flaccid paralysis surveillance: a review of the literature. J Infect Dis 175 (Suppl. 1):176–182
     [Google Scholar]
  2. Bellmunt A., May G., Zell R., Pring-Akerblom P., Verhagen W., Heim A. 1999; Evolution of poliovirus type I during 5·5 years of prolonged enteral replication in an immunodeficient patient. Virology 265:178–184
     [Google Scholar]
  3. Birmingham M. E., Linkins R. W., Hull B. P., Hull H. F. 1997; Poliomyelitis surveillance: the compass for eradication. J Infect Dis 175 (Suppl. 1):146–150
     [Google Scholar]
  4. De L., Nottay B., Yang C. F., Holloway B. P., Pallansch M., Kew O. 1995; Identification of vaccine-related polioviruses by hybridization with specific RNA probes. J Clin Microbiol 33:562–571
     [Google Scholar]
  5. Diamond D. C., Jameson B. A., Bonin J. 10 other authors 1985; Antigenic variation and resistance to neutralization in poliovirus type 1. Science 229:1090–1093
     [Google Scholar]
  6. Domingo E., Holland J. J. 1997; RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178
     [Google Scholar]
  7. Fares M. A., Moya A., Escarmís C., Baranowski E., Domingo E., Barrio E. 2001; Evidence for positive selection in the capsid protein-coding region of the foot-and-mouth-disease virus (FMDV) subjected to experimental passage regimens. Mol Biol Evol 18:10–21
     [Google Scholar]
  8. Felsenstein J. 1993 phylip (Phylogeny Inference Package) version 3.5c Department of Genetics, University of Washington; Seattle, WA, USA:
     [Google Scholar]
  9. Furione M., Guillot S., Otelea D., Balanant J., Candrea A., Crainic R. 1993; Polioviruses with natural recombinant genomes isolated from vaccine-associated paralytic poliomyelitis. Virology 196:199–208
     [Google Scholar]
  10. Gavrilin G. V., Cherkasova E. A., Lipskaya G. Y., Kew O. M., Agol V. I. 2000; Evolution of circulating wild poliovirus and of vaccine-derived poliovirus in an immunodeficient patient: a unifying model. J Virol 74:7381–7390
     [Google Scholar]
  11. Goldman N., Thorne J. L., Jones D. T. 1998; Assessing the impact of secondary structure and solvent accessibility on protein evolution. Genetics 149:444–458
     [Google Scholar]
  12. Hogle J. M., Chow M., Filman D. J. 1985; Three-dimensional structure of poliovirus at 2·9 Å resolution. Science 229:1358–1365
     [Google Scholar]
  13. Hovi T., Stenvik M. 1994; Selective isolation of poliovirus in recombinant murine cell line expressing the human poliovirus receptor gene. J Clin Microbiol 32:1366–1368
     [Google Scholar]
  14. Hovi T., Vaisanen V., Ukkonen P., von Bonsdorff C. H. 1982; Solid-phase enzyme immunoassay for rotavirus antigen: faecal protease activity as a reason for false-negative results. J Virol Methods 5:45–53
     [Google Scholar]
  15. Hovi T., Huovilainen A., Murdin A., Wimmer E. 1995; Isolation of escape mutants of a hybrid poliovirus with the aid of insert-specific polyclonal antibodies. J Gen Virol 76:1861–1865
     [Google Scholar]
  16. Hovi T., Stenvik M., Partanen H., Kangas A. 2001; Poliovirus surveillance by examining sewage specimens. Quantitative recovery of virus after introduction into sewerage at remote upstream location. Epidemiol Infect 127:101–106
     [Google Scholar]
  17. Huovilainen A., Hovi T., Kinnunen L., Takkinen K., Ferguson M., Minor P. 1987; Evolution of poliovirus during an outbreak: sequential type 3 poliovirus isolates from several persons show shifts of neutralization determinants. J Gen Virol 68:1373–1378
     [Google Scholar]
  18. Huovilainen A., Kinnunen L., Ferguson M., Hovi T. 1988; Antigenic variation among 173 strains of type 3 poliovirus isolated in Finland during the 1984 to 1985 outbreak. J Gen Virol 69:1941–1948
     [Google Scholar]
  19. Kew O. M., Nottay B. K. 1984; Molecular epidemiology of polioviruses. Rev Infect Dis 6 (Suppl. 2):499–504
     [Google Scholar]
  20. Kew O. M., Sutter R. W., Nottay B. K., McDonough M. J., Prevots D. R., Quick L., Pallansch M. A. 1998; Prolonged replication of a type 1 vaccine-derived poliovirus in an immunodeficient patient. J Clin Microbiol 36:2893–2899
     [Google Scholar]
  21. Kew O. M., Morris-Glasgow V., Landaverde M. 21 other authors 2002; Outbreak of poliomyelitis in Hispaniola associated with circulating type 1 vaccine-derived poliovirus. Science 296:356–359
     [Google Scholar]
  22. Kilpatrick D. R., Nottay B., Yang C. F., Yang S. J., Mulders M. N., Holloway B. P., Pallansch M. A., M Kew O. 1996; Group-specific identification of polioviruses by PCR using primers containing mixed-base or deoxyinosine residue at positions of codon degeneracy. J Clin Microbiol 34:2990–2996
     [Google Scholar]
  23. Kinnunen L., Huovilainen A., Poyry T., Hovi T. 1990; Rapid molecular evolution of wild type 3 poliovirus during infection in individual hosts. J Gen Virol 71:317–324
     [Google Scholar]
  24. Kinnunen L., Poyry T., Hovi T. 1991; Generation of virus genetic lineages during an outbreak of poliomyelitis. J Gen Virol 72:2483–2489
     [Google Scholar]
  25. Kinnunen L., Poyry T., Hovi T. 1992; Genetic diversity and rapid evolution of poliovirus in human hosts. Curr Top Microbiol Immunol 176:49–61
     [Google Scholar]
  26. Lipskaya G. Y., Muzychenko A. R., Kutitova O. K., Maslova S. V., Equestre M., Drozdov S. G., Bercoff R. P., Agol V. I. 1991; Frequent isolation of intertypic poliovirus recombinants with serotype 2 specificity from vaccine-associated polio cases. J Med Virol 35:290–296
     [Google Scholar]
  27. Liu H. M., Zheng D. P., Zhang L. B., Oberste M. S., Pallansch M. A., Kew O. M. 2000; Molecular evolution of a type 1 wild-vaccine poliovirus recombinant during widespread circulation in China. J Virol 74:11153–11161
     [Google Scholar]
  28. Martín J., Dunn G., Hull R., Patel V., Minor P. D. 2000; Evolution of the Sabin strain of type 3 poliovirus in an immunodeficient patient during the entire 637-day period of virus excretion. J Virol 74:3001–3010
     [Google Scholar]
  29. Minor P. D., Evans D. M. A., Ferguson M., Schild G. C., Westrop G., Almond J. W. 1985; Principal and subsidiary antigenic sites of VP1 involved in the neutralization of poliovirus type 3. J Gen Virol 65:1159–1165
     [Google Scholar]
  30. Minor P. D., John A., Ferguson M., Icenogle J. P. 1986; Antigenic and molecular evolution of the vaccine strain of type 3 poliovirus during the period of excretion by a primary vaccinee. J Gen Virol 67:693–706
     [Google Scholar]
  31. MMWR 2001; Acute flaccid paralysis associated with circulating vaccine-derived poliovirus – Philippines, 2001. Morb Mortal Wkly Rep 50:874–875
     [Google Scholar]
  32. Mulders M. N., Lipskaya G. Y., van der Avoort H. G., Koopmans M. P., Kew O. M., van Loon A. M. 1995; Molecular epidemiology of wild poliovirus type 1 in Europe, the Middle East, and the Indian subcontinent. J Infect Dis 171:1399–1405
     [Google Scholar]
  33. Mulders M. N., Reimerink J. H., Stenvik M., Alaeddinoglu I., van der Avoort H. G., Hovi T., Koopmans M. P. 1999; A Sabin vaccine-derived field isolate of poliovirus type 1 displaying aberrant phenotypic and genetic features, including a deletion in antigenic site 1. J Gen Virol 80:907–916
     [Google Scholar]
  34. Mulders M. N., Salminen M., Kalkkinen N., Hovi T. 2000; Molecular epidemiology of coxsackievirus B4 and disclosure of the correct VP1/2A(pro) cleavage site: evidence for high genomic diversity and long-term endemicity of distinct genotypes. J Gen Virol 81:803–812
     [Google Scholar]
  35. Piirainen L., Stenvik M., Roivainen M., Eskola J., Beuvery E. C., Hovi T. 1999; Randomised, controlled trial with the trypsin-modified inactivated poliovirus vaccine: assessment of intestinal immunity with live challenge virus. Vaccine 17:1084–1090
     [Google Scholar]
  36. Pipkin P. A., Wood D. J., Racaniello V. R., Minor P. D. 1993; Characterisation of L cells expressing the human poliovirus receptor for the specific detection of polioviruses in vitro. J Virol Methods 41:333–340
     [Google Scholar]
  37. Poyry T., Stenvik M., Hovi T. 1988; Viruses in sewage waters during and after a poliomyelitis outbreak and subsequent nationwide oral poliovirus vaccination campaign in Finland. Appl Environ Microbiol 54:371–374
     [Google Scholar]
  38. Rico-Hesse R., Pallansch M. A., Nottay B. K., Kew O. M. 1987; Geographic distribution of wild poliovirus type 1 genotypes. Virology 160:311–322
     [Google Scholar]
  39. Roivainen M., Narvanen A., Korkolainen M., Huhtala M. L., Hovi T. 1991; Antigenic regions of poliovirus type 3/Sabin capsid proteins recognized by human sera in the peptide scanning technique. Virology 180:99–107
     [Google Scholar]
  40. Savilahti E., Klemola T., Carlsson B., Mellander L., Stenvik M., Hovi T. 1988; Inadequacy of mucosal IgM antibodies in selective IgA deficiency: excretion of attenuated polio viruses is prolonged. J Clin Immunol 8:89–94
     [Google Scholar]
  41. Valtanen S., Roivainen M., Piirainen L., Stenvik M., Hovi T. 2000; Poliovirus-specific intestinal antibody responses coincide with decline of poliovirus excretion. J Infect Dis 182:1–5
     [Google Scholar]
  42. van der Avoort H. G., Hull B. P., Hovi T., Pallansch M. A., Kew O. M., Crainic R., Wood D. J., Mulders M. N., van Loon A. M. 1995; Comparative study of five methods for intratypic differentiation of polioviruses. J Clin Microbiol 33:2562–2566
     [Google Scholar]
  43. WHO 2000; Outbreak news. Wkly Epidemiol Rec 75:397–399
     [Google Scholar]
  44. WHO 2002; Paralytic poliomyelitis in Madagascar. Wkly Epidemiol Rec 77:241–242
     [Google Scholar]
  45. Yoneyama T., Hagiwara A., Hara M., Shimojo H. 1982; Alteration in oligonucleotide fingerprint patterns of the viral genome in poliovirus type 2 isolated from paralytic patients. Infect Immun 37:46–53
     [Google Scholar]
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Evolution of wild-type 1 poliovirus in two healthy siblings excreting the virus over a period of 6 months
J. Gen. Virol. 85, 369 (2004); https://doi.org/10.1099/vir.0.19518-0
/content/journal/jgv/10.1099/vir.0.19518-0
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