Changes in population dynamics during long-term evolution of sabin type 1 poliovirus in an immunodeficient patient

Journal of Virology

Volumn 82, Issue 18, 2008, Pages 9179-9190

  Odoom, John K ^a   Yunus, Zaira ^a   Dunn, Glynis ^a   Minor, Philip D ^a   Martín, Javier ^a  

^a NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN; ORAL POLIOMYELITIS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGENICITY; ARTICLE; CASE REPORT; CONTROLLED STUDY; EVOLUTION; GENETIC HETEROGENEITY; HUMAN; IMMUNOGLOBULIN DEFICIENCY; INOCULATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; POLIOMYELITIS VIRUS 1; POPULATION DYNAMICS; PRESCHOOL CHILD; PRIORITY JOURNAL; SEQUENCE ANALYSIS; TEMPERATURE SENSITIVITY; TRANSGENIC MOUSE; VACCINATION; VIROGENESIS; VIRUS EXCRETION; VIRUS ISOLATION; VIRUS MUTATION; VIRUS VIRULENCE;

AGAMMAGLOBULINEMIA; ANIMALS; ANTIGENS, VIRAL; BASE SEQUENCE; CELL LINE; CHILD, PRESCHOOL; EVOLUTION, MOLECULAR; FECES; HUMANS; IMMUNIZATION; MALE; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; POLIOVIRUS; POLIOVIRUS VACCINE, ORAL; POPULATION DYNAMICS; SEQUENCE ANALYSIS, DNA; TEMPERATURE; TIME FACTORS; VIRULENCE; VIRUS SHEDDING;

MUS MUSCULUS; POLIOVIRUS;

EID: 50949120997     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00468-08     Document Type: Article

References (69)

1. Alexander, L. N., J. F. Seward, T. A. Santibanez, M. A. Pallansch, O. M. Kew, D. R. Prevots, P. M. Strebel, J. Cono, M. Wharton, W. A. Orenstein, and R. W. Sutter. 2004. Vaccine policy changes and epidemiology of poliomyelitis in the United States. JAMA 292:1696-1701.
2. Bellmunt, A., G. May, R. Zell, P. Pring-Akerblom, W. Verhagen, and A. Heim. 1999. Evolution of poliovirus type I during 5.5 years of prolonged enteral replication in an immunodeficient patient. Virology 265:178-184.
3. Belnap, D. M., B. M. McDermott, Jr., D. J. Filman, N. Cheng, B. L. Trus, H. J. Zuccola, V. R. Racaniello, J. M. Hogle, and A. C. Steven. 2000. Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc. Natl. Acad. Sci. USA 97:73-78.
4. Blomqvist, S., A. L. Bruu, M. Stenvik, and T. Hovi. 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.
5. Blomqvist, S., C. Savolainen, P. Laine, P. Hirttio, E. Lamminsalo, E. Penttila, S. Joks, M. Roivainen, and T. Hovi. 2004. Characterization of a highly evolved vaccine-derived poliovirus type 3 isolated from sewage in Estonia. J. Virol. 78:4876-4883.
6. Bouchard, M. J., D. H. Lam, and V. R. Racaniello. 1995. Determinants of attenuation and temperature sensitivity in the type 1 poliovirus Sabin vaccine. J. Virol. 69:4972-4978.
7. Cammack, N., A. Phillips, G. Dunn, V. Patel, and P. D. Minor. 1988. Intertypic genomic rearrangements of poliovirus strains in vaccinees. Virology 167:507-514.
8. Cherkasova, E. A., E. A. Korotkova, M. L. Yakovenko, O. E. Ivanova, T. P. Eremeeva, K. M. Chumakov, and V. I. Agol. 2002. Long-term circulation of vaccine-derived poliovirus that causes paralytic disease. J. Virol. 76:6791-6799.
9. Christodoulou, C., F. Colbere-Garapin, A. Macadam, L. F. Taffs, S. Marsden, P. Minor, and F. Horaud. 1990. Mapping of mutations associated with neurovirulence in monkeys infected with Sabin 1 poliovirus revertants selected at high temperature. J. Virol. 64:4922-4929.
10. Chumakov, K. M., L. B. Powers, K. E. Noonan, I. B. Roninson, and I. S. Levenbook. 1991. Correlation between amount of virus with altered nucleotide sequence and the monkey test for acceptability of oral poliovirus vaccine. Proc. Natl. Acad. Sci. USA 88:199-203.
11. Combiescu, M., S. Guillot, A. Persu, A. Baicus, D. Pitigoi, J. Balanant, G. Oprisan, R. Crainic, F. Delpeyroux, and A. Aubert-Combiescu. 2007. Circulation of a type 1 recombinant vaccine-derived poliovirus strain in a limited area in Romania. Arch. Virol. 152:727-738.
12. Contreras, G., K. Dimock, J. Furesz, C. Gardell, D. Hazlett, K. Karpinski, G. McCorkle, and L. Wu. 1992. Genetic characterization of Sabin types 1 and 3 poliovaccine virus following serial passage in the human intestinal tract. Biologicals 20:15-26.
13. Dunn, G. Personal communication.
14. Felsenstein, J. 2000. PHYLIP: phylogeny inference package, version 3.6a3. University of Washington, Seattle.
15. Filman, D. J., R. Syed, M. Chow, A. J. Macadam, P. D. Minor, and J. M. Hogle. 1989. Structural factors that control conformational transitions and serotype specificity in type 3 poliovirus. EMBO J. 8:1567-1579.
16. Fricks, C. E., and J. M. Hogle. 1990. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64:1934-1945.
17. Fricks, C. E., J. P. Icenogle, and J. M. Hogle. 1985. Trypsin sensitivity of the Sabin strain of type 1 poliovirus: cleavage sites in virions and related particles. J. Virol. 54:856-859.
18. Gavrilin, G. V., E. A. Cherkasova, G. Y. Lipskaya, O. M. Kew, and V. I. Agol. 2000. Evolution of circulating wild poliovirus and of vaccine-derived poliovirus in an immunodeficient patient: a unifying model. J. Virol. 74:7381-7390.
19. Georgescu, M. M., J. Balanant, A. Macadam, D. Otelea, M. Combiescu, A. A. Combiescu, R. Crainic, and F. Delpeyroux. 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.
20. Guillot, S., V. Caro, N. Cuervo, E. Korotkova, M. Combiescu, A. Persu, A. Aubert-Combiescu, F. Delpeyroux, and R. Crainic. 2000. Natural genetic exchanges between vaccine and wild poliovirus strains in humans. J. Virol. 74:8434-8443.
21. Halsey, N. A., J. Pinto, F. Espinosa-Rosales, M. A. Faure-Fontenla, E. da Silva, A. J. Khan, A. D. Webster, P. Minor, G. Dunn, E. Asturias, H. Hussain, M. A. Pallansch, O. M. Kew, J. Winkelstein, and R. Sutter. 2004. Search for poliovirus carriers among people with primary immune deficiency diseases in the United States, Mexico, Brazil, and the United Kingdom. Bull. W. H. O. 82:3-8.
22. He, Y., V. D. Bowman, S. Mueller, C. M. Bator, J. Bella, X. Peng, T. S. Baker, E. Wimmer, R. J. Kuhn, and M. G. Rossmann. 2000. Interaction of the poliovirus receptor with poliovirus. Proc. Natl. Acad. Sci. USA 97:79-84.
23. Hogle, J. M., M. Chow, and D. J. Filman. 1985. Three-dimensional structure of poliovirus at 2.9 Å resolution. Science 229:1358-1365.
24. Kawamura, N., M. Kohara, S. Abe, T. Komatsu, K. Tago, M. Arita, and A. Nomoto. 1989. Determinants in the 5′ noncoding region of poliovirus Sabin 1 RNA that influence the attenuation phenotype. J. Virol. 63:1302-1309.
25. Kew, O. 1999. Genomic sequencing and epidemiologic tracking of polioviruses. Part III: reading the phylogenetic tree. Polio Lab Network Q. Update 5:1-2.
26. Kew, O., V. Morris-Glasgow, M. Landaverde, C. Burns, J. Shaw, Z. Garib, J. Andre, E. Blackman, C. J. Freeman, J. Jorba, R. Sutter, G. Tambini, L. Venczel, C. Pedreira, F. Laender, H. Shimizu, T. Yoneyama, T. Miyamura, H. van Der Avoort, M. S. Oberste, D. Kilpatrick, S. Cochi, M. Pallansch, and C. de Quadros. 2002. Outbreak of poliomyelitis in Hispaniola associated with circulating type 1 vaccine-derived poliovirus. Science 14:14.
27. Kew, O. M., M. N. Mulders, G. V. Lipskaya, E. E. da Silva, and M. A. Pallansch. 1995. Molecular epidemiology of polioviruses. Semin. Virol. 6:401-414.
28. Kew, O. M., R. W. Sutter, E. M. de Gourville, W. R. Dowdle, and M. A. Pallansch. 2005. Vaccine-derived polioviruses and the endgame strategy for global polio eradication. Annu. Rev. Microbiol. 59:587-635.
29. Kew, O. M., R. W. Sutter, B. K. Nottay, M. J. McDonough, D. R. Prevots, L. Quick, and M. A. Pallansch. 1998. Prolonged replication of a type 1 vaccine-derived poliovirus in an immunodeficient patient. J. Clin. Microbiol. 36:2893-2899.
30. Kew, O. M., P. F. Wright, V. I. Agol, F. Delpeyroux, H. Shimizu, N. Nathanson, and M. A. Pallansch. 2004. Circulating vaccine-derived polioviruses: current state of knowledge. Bull. W. H. O. 82:16-23.
31. Kohara, M., T. Omata, A. Kameda, B. L. Semler, H. Itoh, E. Wimmer, and A. Nomoto. 1985. In vitro phenotypic markers of a poliovirus recombinant constructed from infectious cDNA clones of the neurovirulent Mahoney strain and the attenuated Sabin 1 strain. J. Virol. 53:786-792.
32. Koike, S., C. Taya, J. Aoki, Y. Matsuda, I. Ise, H. Takeda, T. Matsuzaki, H. Amanuma, H. Yonekawa, and A. Nomoto. 1994. Characterization of three different transgenic mouse lines that carry human poliovirus receptor gene - influence of the transgene expression on pathogenesis. Arch. Virol. 139:351- 363.
33. Korotkova, E. A., R. Park, E. A. Cherkasova, G. Y. Lipskaya, K. M. Chumakov, E. V. Feldman, O. M. Kew, and V. I. Agol. 2003. Retrospective analysis of a local cessation of vaccination against poliomyelitis: a possible scenario for the future. J. Virol. 77:12460-12465.
34. Li, J., L. B. Zhang, T. Yoneyama, H. Yoshida, H. Shimizu, K. Yoshii, M. Hara, T. Nomura, H. Yoshikura, T. Miyamura, and A. Hagiwara. 1996. Genetic basis of the neurovirulence of type 1 polioviruses isolated from vaccine-associated paralytic patients. Arch. Virol. 141:1047-1054.
35. Liang, X., Y. Zhang, W. Xu, N. Wen, S. Zuo, L. A. Lee, and J. Yu. 2006. An outbreak of poliomyelitis caused by type 1 vaccine-derived poliovirus in China. J. Infect. Dis. 194:545-551.
36. Liu, H. M., D. P. Zheng, L. B. Zhang, M. S. Oberste, O. M. Kew, and M. A. Pallansch. 2003. Serial recombination during circulation of type 1 wild-vaccine recombinant polioviruses in China. J. Virol. 77:10994-11005.
37. Liu, H. M., D. P. Zheng, L. B. Zhang, M. S. Oberste, M. A. Pallansch, and O. M. Kew. 2000. Molecular evolution of a type 1 wild-vaccine poliovirus recombinant during widespread circulation in China. J. Virol. 74:11153-11161.
38. Macadam, A. J., G. Ferguson, T. Fleming, D. M. Stone, J. W. Almond, and P. D. Minor. 1994. Role for poliovirus protease 2A in cap independent translation. EMBO J. 13:924-927.
39. Macadam, A. J., D. M. Stone, J. W. Almond, and P. D. Minor. 1994. The 5′ noncoding region and virulence of poliovirus vaccine strains. Trends Microbiol. 2:449-454.
40. MacCallum, F. O. 1971. Hypogammaglobulinaemia in the United Kingdom. VII. The role of humoral antibodies in protection against and recovery from bacterial and virus infections in hypogammaglobulinaemia. Spec. Rep. Ser. Med. Res. Counc. 310:72-85.
41. MacLennan, C., G. Dunn, A. P. Huissoon, D. S. Kumararatne, J. Martin, P. O'Leary, R. A. Thompson, H. Osman, P. Wood, P. Minor, D. J. Wood, and D. Pillay. 2004. Failure to clear persistent vaccine-derived neurovirulent poliovirus infection in an immunodeficient man. Lancet 363:1509-1513.
42. Magrath, D. I., L. R. Boulger, and E. G. Hartley. 1966. Strains of poliovirus from individuals fed Sabin vaccine studied by in vitro markers and the monkey neurovirulence test, p. 334-345. In Proceedings of the 10th Symposium of the European Association against Poliomyelitis Les Establishments Pharmaceutiques - Tarchomin - Polfa, Brussels, Belgium.
43. Martin, J. 2006. Vaccine-derived poliovirus from long term excretors and the end game of polio eradication. Biologicals 34:117-122.
44. Martin, J., G. Dunn, R. Hull, V. Patel, and P. D. Minor. 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.
45. Martin, J., K. Odoom, G. Tuite, G. Dunn, N. Hopewell, G. Cooper, C. Fitzharris, K. Butler, W. W. Hall, and P. D. Minor. 2004. Long-term excretion of vaccine-derived poliovirus by a healthy child. J. Virol. 78:13839-13847.
46. Martin, J., E. Samoilovich, G. Dunn, A. Lackenby, E. Feldman, A. Heath, E. Svirchevskaya, G. Cooper, M. Yermalovich, and P. D. Minor. 2002. Isolation of an intertypic poliovirus capsid recombinant from a child with vaccine-associated paralytic poliomyelitis. J. Virol. 76:10921-10928.
47. McGoldrick, A., A. J. Macadam, G. Dunn, A. Rowe, J. Burlison, P. D. Minor, J. Meredith, D. J. Evans, and J. W. Almond. 1995. Role of mutations G-480 and C-6203 in the attenuation phenotype of Sabin type 1 poliovirus. J. Virol. 69:7601-7605.
48. Minor, P. D. 1990. Antigenic structure of picornaviruses. Curr. Top. Microbiol. Immunol. 161:121-154.
49. Minor, P. D. 1980. Comparative biochemical studies of type 3 poliovirus. J. Virol. 34:73-84.
50. Minor, P. D. 1992. The molecular biology of poliovaccines. J. Gen. Virol. 73:3065-3077.
51. Minor, P. D., G. Dunn, M. E. Ramsay, and D. Brown. 2005. Effect of different immunisation schedules on the excretion and reversion of oral poliovaccine strains. J. Med. Virol. 75:153-160.
52. Minor, P. D., A. John, M. Ferguson, and J. P. Icenogle. 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.
53. Mosser, A. G., J. Y. Sgro, and R. R. Rueckert. 1994. Distribution of drug resistance mutations in type 3 poliovirus identifies three regions involved in uncoating functions. J. Virol. 68:8193-8201.
54. Mulders, M. N., J. H. Reimerink, M. Stenvik, I. Alaeddinoglu, H. G. van der Avoort, T. Hovi, and M. P. Koopmans. 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.
55. Omata, T., M. Kohara, S. Kuge, T. Komatsu, S. Abe, B. L. Semler, A. Kameda, H. Itoh, M. Arita, E. Wimmer, et al. 1986. Genetic analysis of the attenuation phenotype of poliovirus type 1. J. Virol. 58:348-358.
56. Page, R. D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
57. Perriere, G., and M. Gouy. 1996. WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364-369.
58. Pertinacova, J., E. Bohmova, and Z. Sobotova. 2004. Isalation of highly divergent vaccine strains of polioviruses in Slovakia. Epidemiol. Mikrobiol. Imunol. 53:22-24.
59. Roussel, D., M. Rakoto-Andrianarivelo, R. Razafindratsimandresy, B. Randriamanalina, S. Guillot, J. Balanant, P. Mauclere, and F. Delpeyroux. 2003. Recombinant vaccine-derived poliovirus in Madagascar. Einerg. Infect. Dis. 9:885-887.
60. Shimizu, H., B. Thorley, F. J. Paladin, K. A. Brussen, V. Stambos, L. Yuen, A. Utama, Y. Tano, M. Arita, H. Yoshida, T. Yoneyama, A. Benegas, S. Roesel, M. Pallansch, O. Kew, and T. Miyamura. 2004. Circulation of type 1 vaccine-derived poliovirus in the Philippines in 2001. J. Virol. 78:13512-13521.
61. Shulman, L. M., Y. Manor, R. Handsher, F. Delpeyroux, M. J. McDonough, T. Halmut, I. Silberstein, J. Alfandari, J. Quay, T. Fisher, J. Robinov, O. M. Kew, R. Crainic, and E. Mendelson. 2000. Molecular and antigenic characterization of a highly evolved derivative of the type 2 oral poliovaccine strain isolated from sewage in Israel. J. Clin. Microbiol. 38:3729-3734.
62. Skinner, M. A., V. R. Racaniello, G. Dunn, J. Cooper, P. D. Minor, and J. W. Almond. 1989. New model for the secondary structure of the 5′ non-coding RNA of poliovirus is supported by biochemical and genetic data that also show that RNA secondary structure is important in neurovirulence. J. Mol. Biol. 207:379-392.
63. Sutter, R. W., and R. Prevots. 1994. Vaccine-associated paralytic poliomyelitis among immunodeficient persons. Infect. Med. 11:426-438.
64. Tardy-Panit, M., B. Blondel, A. Martin, F. Tekaia, F. Horaud, and F. Delpeyroux. 1993. A mutation in the RNA polymerase of poliovirus type 1 contributes to attenuation in mice. J. Virol. 67:4630-4638.
65. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
66. World Health Organization. 2007. Global update on vaccine derived polioviruses, January 2006-August 2007. Wkly. Epidemiol. Rec. 39:337-343.
67. World Health Organization. 2006. Vaccine derived polioviruses - update. W.E.R. 39:398-403.
68. Yang, C. F., H. Y. Chen, J. Jorba, H. C. Sun, S. J. Yang, H. C. Lee, Y. C. Huang, T. Y. Lin, P. J. Chen, H. Shimizu, Y. Nishimura, A. Utama, M. Pallansch, T. Miyamura, O. Kew, and J. Y. Yang. 2005. Intratypic recombination among lineages of type 1 vaccine-derived poliovirus t merging during chronic infection of an immunodeficient patient. J. Virol. 79:12623-12634.
69. Yang, C. F., T. Naguib, S. J. Yang, E. Nasr, J. Jorba, N. Ahmed, R. Campagnoli, H. van der Avoort, H. Shimizu, T. Yoneyama, T. Miyamura, M. Pallansch, and O. Kew. 2003. Circulation of endemic type 2 vaccine-derived poliovirus in Egypt from 1983 to 1993. J. Virol. 77:8366-83'7.