1887

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Volume 91, Issue 2

Characterization of a rare natural intertypic type 2/type 3 penta-recombinant vaccine-derived poliovirus isolated from a child with acute flaccid paralysis Free

Abstract

A type 2 vaccine-derived poliovirus (VDPV) (strain CHN1025), with a 1.1 % (10/903) difference from Sabin strain in the coding region, was isolated from a child with poliomyelitis caused by a poliovirus variant infection. The patient was from Shandong Province of China and developed acute flaccid paralysis in 1997. The child was infected with a rare and complicated penta-recombinant poliovirus with the uncommon genomic recombinant organization S2/S3/S1/S3/S1/S3. At least five successive rounds of recombination occurred in the capsid coding region and in the , (twice) and non-capsid coding regions, respectively, during virus evolution. Strain CHN1025 had most of the characteristics of the type 2 vaccine strain; it had Sabin-specific epitopes, suggesting that the virus was antigenically indistinguishable from the Sabin 2 reference strain. Typical mutations in the 5′-untranslated region and VP1 associated with reversion to neurovirulence for Sabin 2 poliovirus were found, and the virus showed moderate neurovirulence in transgenic mice. A few nucleotide substitutions were located in the donor sequences, and two donor sequences contained no nucleotide substitutions, suggesting that these sequences were relatively new. The appearance of these mutations within approximately 192 days of at least five successive rounds of recombination events derived from a single ancestral infection illustrates the rapid emergence of new recombinants among VDPVs. This is the first report on the isolation of a type 2/type 3 poliovirus capsid recombinant with one of the five crossover sites located in the coding region.

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2010-02-01
2024-04-19
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References

  1. Avellón, A., Cabrerizo, M., de Miguel, T., Pérez-Breña, P., Tenorio, A., Pérez, J. L., de Aragón, M. V. & Trallero, G.(2008). Paralysis case and contact spread of recombinant vaccine-derived poliovirus, Spain. Emerg Infect Dis 14, 1807–1809.[CrossRef] [Google Scholar]
  2. Balanant, J., Guillot, S., Candrea, A., Delpeyroux, F. & Crainic, R.(1991). The natural genomic variability of poliovirus analyzed by a restriction fragment length polymorphism assay. Virology 184, 645–654.[CrossRef] [Google Scholar]
  3. 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.[CrossRef] [Google Scholar]
  4. Blomqvist, S., Bruu, A. L., Stenvik, M. & Hovi, T.(2003). Characterization of a recombinant type 3/type 2 poliovirus isolated from a healthy vaccinee and containing a chimeric capsid protein VP1. J Gen Virol 84, 573–580.[CrossRef] [Google Scholar]
  5. Buttinelli, G., Donati, V., Fiore, S., Marturano, J., Plebani, A., Balestri, P., Soresina, A. R., Vivarelli, R., Delpeyroux, F. & other authors(2003). Nucleotide variation in Sabin type 2 poliovirus from an immunodeficient patient with poliomyelitis. J Gen Virol 84, 1215–1221.[CrossRef] [Google Scholar]
  6. Cammack, N., Phillips, A., Dunn, G., Patel, V. & Minor, P. D.(1988). Intertypic genomic rearrangements of poliovirus strains in vaccinees. Virology 167, 507–514.[CrossRef] [Google Scholar]
  7. Cuervo, N. S., Guillot, S., Romanenkova, N., Combiescu, M., Aubert-Combiescu, A., Seghier, M., Caro, V., Crainic, R. & Delpeyroux, F.(2001). Genomic features of intertypic recombinant Sabin poliovirus strains excreted by primary vaccinees. J Virol 75, 5740–5751.[CrossRef] [Google Scholar]
  8. Dedepsidis, E., Pliaka, V., Kyriakopoulou, Z., Brakoulias, C., Levidiotou-Stefanou, S., Pratti, A., Mamuris, Z. & Markoulatos, P.(2008). Complete genomic characterization of an intertypic Sabin 3/Sabin 2 capsid recombinant. FEMS Immunol Med Microbiol 52, 343–351.[CrossRef] [Google Scholar]
  9. Dowdle, W. R., De Gourville, E., Kew, O. M., Pallansch, M. A. & Wood, D. J.(2003). Polio eradication: the OPV paradox. Rev Med Virol 13, 277–291.[CrossRef] [Google Scholar]
  10. Fine, P. E. & Carneiro, I. A.(1999). Transmissibility and persistence of oral polio vaccine viruses: implications for the global poliomyelitis eradication initiative. Am J Epidemiol 150, 1001–1021.[CrossRef] [Google Scholar]
  11. Freistadt, M. S., Vaccaro, J. A. & Eberle, K. E.(2007). Biochemical characterization of the fidelity of poliovirus RNA-dependent RNA polymerase. Virol J 4, 44[CrossRef] [Google Scholar]
  12. 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.[CrossRef] [Google Scholar]
  13. Georgescu, M. M., Balanant, J., Macadam, A., Otelea, D., Combiescu, M., Combiescu, A. A., Crainic, R. & Delpeyroux, F.(1997). Evolution of the Sabin type 1 poliovirus in humans: characterization of strains isolated from patients with vaccine-associated paralytic poliomyelitis. J Virol 71, 7758–7768. [Google Scholar]
  14. Guillot, S., Caro, V., Cuervo, N., Korotkova, E., Combiescu, M., Persu, A., Aubert-Combiescu, A., Delpeyroux, F. & Crainic, R.(2000). Natural genetic exchanges between vaccine and wild poliovirus strains in humans. J Virol 74, 8434–8443.[CrossRef] [Google Scholar]
  15. Jorba, J., Campagnoli, R., De, L. & Kew, O.(2008). Calibration of multiple poliovirus molecular clocks covering an extended evolutionary range. J Virol 82, 4429–4440.[CrossRef] [Google Scholar]
  16. Karakasiliotis, I., Markoulatos, P. & Katsorchis, T.(2004). Site analysis of recombinant and mutant poliovirus isolates of Sabin origin from patients and from vaccinees. Mol Cell Probes 18, 103–109.[CrossRef] [Google Scholar]
  17. Kärber, G.(1931). Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Naunyn Schmiedebergs Arch Pharmacol 162, 480–483 (in German).[CrossRef] [Google Scholar]
  18. 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]
  19. Kew, O., Morris-Glasgow, V., Landaverde, M., Burns, C., Shaw, J., Garib, Z., André, J., Blackman, E., Freeman, C. J. & other authors(2002). Outbreak of poliomyelitis in Hispaniola associated with circulating type 1 vaccine-derived poliovirus. Science 296, 356–359.[CrossRef] [Google Scholar]
  20. Kew, O. M., Wright, P. F., Agol, V. I., Delpeyroux, F., Shimizu, H., Nathanson, N. & Pallansch, M. A.(2004). Circulating vaccine-derived polioviruses: current state of knowledge. Bull World Health Organ 82, 16–23. [Google Scholar]
  21. Kew, O. M., Sutter, R. W., de Gourville, E. M., Dowdle, W. R. & Pallansch, M. A.(2005). Vaccine-derived polioviruses and the endgame strategy for global polio eradication. Annu Rev Microbiol 59, 587–635.[CrossRef] [Google Scholar]
  22. Kohara, M., Abe, S., Komatsu, T., Tago, K., Arita, M. & Nomoto, A.(1988). A recombinant virus between the Sabin 1 and Sabin 3 vaccine strains of poliovirus as a possible candidate for a new type 3 poliovirus live vaccine strain. J Virol 62, 2828–2835. [Google Scholar]
  23. Lentz, K. N., Smith, A. D., Geisler, S. C., Cox, S., Buontempo, P., Skelton, A., DeMartino, J., Rozhon, E., Schwartz, J. & other authors(1997). Structure of poliovirus type 2 Lansing complexed with antiviral agent SCH48973: comparison of the structural and biological properties of three poliovirus serotypes. Structure 5, 961–978.[CrossRef] [Google Scholar]
  24. Liang, X., Zhang, Y., Xu, W., Wen, N., Zuo, S., Lee, L. A. & Yu, J.(2006). An outbreak of poliomyelitis caused by type 1 vaccine-derived poliovirus in China. J Infect Dis 194, 545–551.[CrossRef] [Google Scholar]
  25. Lole, K. S., Bollinger, R. C., Paranjape, R. S., Gadkari, D., Kulkarni, S. S., Novak, N. G., Ingersoll, R., Sheppard, H. W. & Ray, S. C.(1999). Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73, 152–160. [Google Scholar]
  26. Macadam, A. J., Pollard, S. R., Ferguson, G., Skuce, R., Wood, D., Almond, J. W. & Minor, P. D.(1993). Genetic basis of attenuation of the Sabin type 2 vaccine strain of poliovirus in primates. Virology 192, 18–26.[CrossRef] [Google Scholar]
  27. Martín, J., Samoilovich, E., Dunn, G., Lackenby, A., Feldman, E., Heath, A., Svirchevskaya, E., Cooper, G., Yermalovich, M. & Minor, P. D.(2002). Isolation of an intertypic poliovirus capsid recombinant from a child with vaccine-associated paralytic poliomyelitis. J Virol 76, 10921–10928.[CrossRef] [Google Scholar]
  28. Minor, P. D.(1990). Antigenic structure of picornaviruses. Curr Top Microbiol Immunol 161, 121–154. [Google Scholar]
  29. Minor, P. D. & Dunn, G.(1988). The effect of sequences in the 5′ non-coding region on the replication of polioviruses in the human gut. J Gen Virol 69, 1091–1096.[CrossRef] [Google Scholar]
  30. Minor, P. D., Macadam, A. J., Stone, D. M. & Almond, J. W.(1993). Genetic basis of attenuation of the Sabin oral poliovirus vaccines. Biologicals 21, 357–363.[CrossRef] [Google Scholar]
  31. Rakoto-Andrianarivelo, M., Guillot, S., Iber, J., Balanant, J., Blondel, B., Riquet, F., Martín, J., Kew, O., Randriamanalina, B. & other authors(2007). Co-circulation and evolution of polioviruses and species C enteroviruses in a district of Madagascar. PLoS Pathog 3, e191[CrossRef] [Google Scholar]
  32. Ren, R. B., Moss, E. G. & Racaniello, V. R.(1991). Identification of two determinants that attenuate vaccine-related type 2 poliovirus. J Virol 65, 1377–1382. [Google Scholar]
  33. Rousset, D., Rakoto-Andrianarivelo, M., Razafindratsimandresy, R., Randriamanalina, B., Guillot, S., Balanant, J., Mauclere, P. & Delpeyroux, F.(2003). Recombinant vaccine-derived poliovirus in Madagascar. Emerg Infect Dis 9, 885–887.[CrossRef] [Google Scholar]
  34. Shimizu, H., Thorley, B., Paladin, F. J., Brussen, K. A., Stambos, V., Yuen, L., Utama, A., Tano, Y., Arita, M. & other authors(2004). Circulation of type 1 vaccine-derived poliovirus in the Philippines in 2001. J Virol 78, 13512–13521.[CrossRef] [Google Scholar]
  35. Stanway, G., Brown, F., Christian, P., Hovi, T., Hyypiä, T., King, A. M. Q., Knowles, N. J., Lemon, S. M., Minor, P. D. & other authors(2005). Family Picornaviridae. In Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses, pp. 757–778. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. London: Elsevier.
  36. Tamura, K., Dudley, J., Nei, M. & Kumar, S.(2007).mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef] [Google Scholar]
  37. Toyoda, H., Kohara, M., Kataoka, Y., Suganuma, T., Omata, T., Imura, N. & Nomoto, A.(1984). Complete nucleotide sequences of all three poliovirus serotype genomes. Implication for genetic relationship, gene function and antigenic determinants. J Mol Biol 174, 561–585.[CrossRef] [Google Scholar]
  38. 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]
  39. WHO(2004a). Global Polio Eradication Initiative, strategic plan 2004–2008. Wkly Epidemiol Rec 79, 55–57. [Google Scholar]
  40. WHO(2004b).Polio Laboratory Manual, 4th edn. Document WHO/IVB/04.10. Geneva, Switzerland: World Health Organization. www.who.int/vaccines/en/poliolab/WHO-Polio-Manual-9.pdf.
  41. Wimmer, E., Hellen, C. U. & Cao, X.(1993). Genetics of poliovirus. Annu Rev Genet 27, 353–436.[CrossRef] [Google Scholar]
  42. Yang, C. F., Naguib, T., Yang, S. J., Nasr, E., Jorba, J., Ahmed, N., Campagnoli, R., van der Avoort, H., Shimizu, H. & other authors(2003). Circulation of endemic type 2 vaccine-derived poliovirus in Egypt from 1983 to 1993. J Virol 77, 8366–8377.[CrossRef] [Google Scholar]
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Characterization of a rare natural intertypic type 2/type 3 penta-recombinant vaccine-derived poliovirus isolated from a child with acute flaccid paralysis
J. Gen. Virol. 91, 421 (2010); https://doi.org/10.1099/vir.0.014258-0
/content/journal/jgv/10.1099/vir.0.014258-0
/content/journal/jgv/10.1099/vir.0.014258-0
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