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. 1988 Sep;7(9):2839–2847. doi: 10.1002/j.1460-2075.1988.tb03140.x

Engineering a poliovirus type 2 antigenic site on a type 1 capsid results in a chimaeric virus which is neurovirulent for mice.

A Martin 1, C Wychowski 1, T Couderc 1, R Crainic 1, J Hogle 1, M Girard 1
PMCID: PMC457076  PMID: 2460345

Abstract

Poliovirus type 2 (PV-2) Lansing strain produces a fatal paralytic disease in mice after intracerebral injection, whereas poliovirus type 1 (PV-1) Mahoney strain causes disease only in primates. Atomic models derived from the three-dimensional crystal structure of the PV-1 Mahoney strain have been used to locate three antigenic sites on the surface of the virion. We report here the construction of type 1-type 2 chimaeric polioviruses in which antigenic site 1 from the PV-1 Mahoney strain was substituted by that of the PV-2 Lansing strain by nucleotide cassette exchange in a cloned PV-1 cDNA molecule. These chimaeras proved to have mosaic capsids with composite type 1 and type 2 antigenicity, and induced a neutralizing response against both PV-1 and PV-2 when injected into rabbits. Moreover, a six-amino-acid change in PV-1 antigenic site 1 was shown to be responsible for a remarkable host-range mutation in so far as one of the two type 1-type 2 chimaera was highly neurovirulent for mice.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Blondel B., Crainic R., Fichot O., Dufraisse G., Candrea A., Diamond D., Girard M., Horaud F. Mutations conferring resistance to neutralization with monoclonal antibodies in type 1 poliovirus can be located outside or inside the antibody-binding site. J Virol. 1986 Jan;57(1):81–90. doi: 10.1128/jvi.57.1.81-90.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burke K. L., Dunn G., Ferguson M., Minor P. D., Almond J. W. Antigen chimaeras of poliovirus as potential new vaccines. Nature. 1988 Mar 3;332(6159):81–82. doi: 10.1038/332081a0. [DOI] [PubMed] [Google Scholar]
  3. Cathala G., Savouret J. F., Mendez B., West B. L., Karin M., Martial J. A., Baxter J. D. A method for isolation of intact, translationally active ribonucleic acid. DNA. 1983;2(4):329–335. doi: 10.1089/dna.1983.2.329. [DOI] [PubMed] [Google Scholar]
  4. Crainic R., Couillin P., Blondel B., Cabau N., Boué A., Horodniceanu F. Natural variation of poliovirus neutralization epitopes. Infect Immun. 1983 Sep;41(3):1217–1225. doi: 10.1128/iai.41.3.1217-1225.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Geliebter J., Zeff R. A., Melvold R. W., Nathenson S. G. Mitotic recombination in germ cells generated two major histocompatibility complex mutant genes shown to be identical by RNA sequence analysis: Kbm9 and Kbm6. Proc Natl Acad Sci U S A. 1986 May;83(10):3371–3375. doi: 10.1073/pnas.83.10.3371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hogle J. M., Chow M., Filman D. J. Three-dimensional structure of poliovirus at 2.9 A resolution. Science. 1985 Sep 27;229(4720):1358–1365. doi: 10.1126/science.2994218. [DOI] [PubMed] [Google Scholar]
  8. Horaud F., Crainic R., Van der Werf S., Blondel B., Wichowski C., Akacem O., Bruneau P., Couillin P., Siffert O., Girard M. Identification and characterization of a continuous neutralization epitope (C3) present on type 1 poliovirus. Prog Med Virol. 1987;34:129–155. [PubMed] [Google Scholar]
  9. Kean K. M., Wychowski C., Kopecka H., Girard M. Highly infectious plasmids carrying poliovirus cDNA are capable of replication in transfected simian cells. J Virol. 1986 Aug;59(2):490–493. doi: 10.1128/jvi.59.2.490-493.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kuhn R. J., Wimmer E., Semler B. L. Expression of the poliovirus genome from infectious cDNA is dependent upon arrangements of eukaryotic and prokaryotic sequences in recombinant plasmids. Virology. 1987 Apr;157(2):560–564. doi: 10.1016/0042-6822(87)90302-3. [DOI] [PubMed] [Google Scholar]
  11. La Monica N., Almond J. W., Racaniello V. R. A mouse model for poliovirus neurovirulence identifies mutations that attenuate the virus for humans. J Virol. 1987 Sep;61(9):2917–2920. doi: 10.1128/jvi.61.9.2917-2920.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. La Monica N., Kupsky W. J., Racaniello V. R. Reduced mouse neurovirulence of poliovirus type 2 Lansing antigenic variants selected with monoclonal antibodies. Virology. 1987 Dec;161(2):429–437. doi: 10.1016/0042-6822(87)90136-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. La Monica N., Meriam C., Racaniello V. R. Mapping of sequences required for mouse neurovirulence of poliovirus type 2 Lansing. J Virol. 1986 Feb;57(2):515–525. doi: 10.1128/jvi.57.2.515-525.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Luo M., Vriend G., Kamer G., Minor I., Arnold E., Rossmann M. G., Boege U., Scraba D. G., Duke G. M., Palmenberg A. C. The atomic structure of Mengo virus at 3.0 A resolution. Science. 1987 Jan 9;235(4785):182–191. doi: 10.1126/science.3026048. [DOI] [PubMed] [Google Scholar]
  15. Martin A., Wychowski C., Benichou D., Crainic R., Girard M. Construction of a chimaeric type 1/type 2 poliovirus by genetic recombination. Ann Inst Pasteur Virol. 1988 Jan-Mar;139(1):79–88. doi: 10.1016/s0769-2617(88)80008-x. [DOI] [PubMed] [Google Scholar]
  16. Minor P. D., Ferguson M., Evans D. M., Almond J. W., Icenogle J. P. Antigenic structure of polioviruses of serotypes 1, 2 and 3. J Gen Virol. 1986 Jul;67(Pt 7):1283–1291. doi: 10.1099/0022-1317-67-7-1283. [DOI] [PubMed] [Google Scholar]
  17. Murray M. G., Kuhn R. J., Arita M., Kawamura N., Nomoto A., Wimmer E. Poliovirus type 1/type 3 antigenic hybrid virus constructed in vitro elicits type 1 and type 3 neutralizing antibodies in rabbits and monkeys. Proc Natl Acad Sci U S A. 1988 May;85(9):3203–3207. doi: 10.1073/pnas.85.9.3203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nomoto A., Omata T., Toyoda H., Kuge S., Horie H., Kataoka Y., Genba Y., Nakano Y., Imura N. Complete nucleotide sequence of the attenuated poliovirus Sabin 1 strain genome. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5793–5797. doi: 10.1073/pnas.79.19.5793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Racaniello V. R., Baltimore D. Cloned poliovirus complementary DNA is infectious in mammalian cells. Science. 1981 Nov 20;214(4523):916–919. doi: 10.1126/science.6272391. [DOI] [PubMed] [Google Scholar]
  20. Racaniello V. R., Baltimore D. Molecular cloning of poliovirus cDNA and determination of the complete nucleotide sequence of the viral genome. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4887–4891. doi: 10.1073/pnas.78.8.4887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rossmann M. G., Arnold E., Erickson J. W., Frankenberger E. A., Griffith J. P., Hecht H. J., Johnson J. E., Kamer G., Luo M., Mosser A. G. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature. 1985 Sep 12;317(6033):145–153. doi: 10.1038/317145a0. [DOI] [PubMed] [Google Scholar]
  22. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Semler B. L., Dorner A. J., Wimmer E. Production of infectious poliovirus from cloned cDNA is dramatically increased by SV40 transcription and replication signals. Nucleic Acids Res. 1984 Jun 25;12(12):5123–5141. doi: 10.1093/nar/12.12.5123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sompayrac L. M., Danna K. J. Efficient infection of monkey cells with DNA of simian virus 40. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7575–7578. doi: 10.1073/pnas.78.12.7575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Stanway G., Hughes P. J., Mountford R. C., Reeve P., Minor P. D., Schild G. C., Almond J. W. Comparison of the complete nucleotide sequences of the genomes of the neurovirulent poliovirus P3/Leon/37 and its attenuated Sabin vaccine derivative P3/Leon 12a1b. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1539–1543. doi: 10.1073/pnas.81.5.1539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Toyoda H., Kohara M., Kataoka Y., Suganuma T., Omata T., Imura N., Nomoto A. Complete nucleotide sequences of all three poliovirus serotype genomes. Implication for genetic relationship, gene function and antigenic determinants. J Mol Biol. 1984 Apr 25;174(4):561–585. doi: 10.1016/0022-2836(84)90084-6. [DOI] [PubMed] [Google Scholar]
  27. Uytdehaag F. G., Osterhaus A. D. Induction of neutralizing antibody in mice against poliovirus type II with monoclonal anti-idiotypic antibody. J Immunol. 1985 Feb;134(2):1225–1229. [PubMed] [Google Scholar]
  28. Wieslander L. A simple method to recover intact high molecular weight RNA and DNA after electrophoretic separation in low gelling temperature agarose gels. Anal Biochem. 1979 Oct 1;98(2):305–309. doi: 10.1016/0003-2697(79)90145-3. [DOI] [PubMed] [Google Scholar]
  29. Wychowski C., van der Werf S., Siffert O., Crainic R., Bruneau P., Girard M. A poliovirus type 1 neutralization epitope is located within amino acid residues 93 to 104 of viral capsid polypeptide VP1. EMBO J. 1983;2(11):2019–2024. doi: 10.1002/j.1460-2075.1983.tb01694.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. van der Werf S., Bregegere F., Kopecka H., Kitamura N., Rothberg P. G., Kourilsky P., Wimmer E., Girard M. Molecular cloning of the genome of poliovirus type 1. Proc Natl Acad Sci U S A. 1981 Oct;78(10):5983–5987. doi: 10.1073/pnas.78.10.5983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. van der Werf S., Wychowski C., Bruneau P., Blondel B., Crainic R., Horodniceanu F., Girard M. Localization of a poliovirus type 1 neutralization epitope in viral capsid polypeptide VP1. Proc Natl Acad Sci U S A. 1983 Aug;80(16):5080–5084. doi: 10.1073/pnas.80.16.5080. [DOI] [PMC free article] [PubMed] [Google Scholar]

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