A trans-complementing recombination trap demonstrates a low propensity of flaviviruses for intermolecular recombination

Journal of Virology

Volumn 84, Issue 1, 2010, Pages 599-611

  Taucher, Christian ^a   Berger, Angelika ^a   Mandl, Christian W ^a,b  

^a UNIVERSITY OF VIENNA   (Austria)

^b NOVARTIS VACCINES AND DIAGNOSTICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA;

ANTIGENICITY; ARTICLE; FLAVIVIRUS; GENETIC RECOMBINATION; JAPANESE ENCEPHALITIS VIRUS; NONHUMAN; PRIORITY JOURNAL; REPLICON; RNA REPLICATION; RNA VIRUS; TICK BORNE ENCEPHALITIS FLAVIVIRUS; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS REPLICATION; WEST NILE FLAVIVIRUS;

FLAVIVIRUS; FLAVIVIRUS INFECTIONS; GENETIC COMPLEMENTATION TEST; GENOME, VIRAL; METHODS; RECOMBINATION, GENETIC; VACCINES, ATTENUATED;

FLAVIVIRUS; JAPANESE ENCEPHALITIS VIRUS; RNA VIRUSES; TICK-BORNE ENCEPHALITIS VIRUS; WEST NILE VIRUS;

EID: 72849121447     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01063-09     Document Type: Article

References (59)

1. Baric, R. S., K. Fu, M. C. Schaad, and S. A. Stohlman. 1990. Establishing a genetic recombination map for murine coronavirus strain A59 complementation groups. Virology 177:646-656.
2. Becher, P., M. Orlich, M. Konig, and H. J. Thiel. 1999. Nonhomologous RNA recombination in bovine viral diarrhea virus: molecular characterization of a variety of subgenomic RNAs isolated during an outbreak of fatal mucosal disease. J. Virol. 73:5646-5653. (Pubitemid 29274849)
3. Becher, P., M. Orlich, and H. J. Thiel. 2000. Mutations in the 5′ nontranslated region of bovine viral diarrhea virus result in altered growth characteristics. J. Virol. 74:7884-7894. (Pubitemid 30641632)
4. Becher, P., M. Orlich, and H. J. Thiel. 1998. Ribosomal S27a coding sequences upstream of ubiquitin coding sequences in the genome of a pestivirus. J. Virol. 72:8697-8704. (Pubitemid 28471810)
5. Becher, P., H. J. Thiel, M. Collins, J. Brownlie, and M. Orlich. 2002. Cellular sequences in pestivirus genomes encoding gamma-aminobutyric acid (A) receptor-associated protein and Golgi-associated ATPase enhancer of 16 kilodaltons. J. Virol. 76:13069-13076. (Pubitemid 35386992)
6. 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. (Pubitemid 19037142)
7. Cascone, P. J., C. D. Carpenter, X. H. Li, and A. E. Simon. 1990. Recombination between satellite RNAs of turnip crinkle virus. EMBO J. 9:1709-1715. (Pubitemid 20170001)
8. Elshuber, S., and C. W. Mandl. 2005. Resuscitating mutations in a furin cleavage-deficient mutant of the flavivirus tick-borne encephalitis virus. J. Virol. 79:11813-11823. (Pubitemid 41279299)
9. Gallei, A., T. Rumenapf, H. J. Thiel, and P. Becher. 2005. Characterization of helper virus-independent cytopathogenic classical swine fever virus generated by an in vivo RNA recombination system. J. Virol. 79:2440-2448. (Pubitemid 40204599)
10. Gehrke, R., M. Ecker, S. W. Aberle, S. L. Allison, F. X. Heinz, and C. W. Mandl. 2003. Incorporation of tick-borne encephalitis virus replicons into virus-like particles by a packaging cell line. J. Virol. 77:8924-8933. (Pubitemid 36936102)
11. Gehrke, R., F. X. Heinz, N. L. Davis, and C. W. Mandl. 2005. Heterologous gene expression by infectious and replicon vectors derived from tick-borne encephalitis virus and direct comparison of this flavivirus system with an alphavirus replicon. J. Gen. Virol. 86:1045-1053.
12. Guirakhoo, F., F. X. Heinz, and C. Kunz. 1989. Epitope model of tick-borne encephalitis virus envelope glycoprotein E: analysis of structural properties, role of carbohydrate side chain, and conformational changes occurring at acidic pH. Virology 169:90-99. (Pubitemid 19080151)
13. Guirakhoo, F., K. Pugachev, Z. Zhang, G. Myers, I. Levenbook, K. Draper, J. Lang, S. Ocran, F. Mitchell, M. Parsons, N. Brown, S. Brandler, C. Fournier, B. Barrere, F. Rizvi, A. Travassos, R. Nichols, D. Trent, and T. Monath. 2004. Safety and efficacy of chimeric yellow fever-dengue virus tetravalent vaccine formulations in nonhuman primates. J. Virol. 78:4761-4775. (Pubitemid 38501097)
14. Hahn, C. S., S. Lustig, E. G. Strauss, and J. H. Strauss. 1988. Western equine encephalitis virus is a recombinant virus. Proc. Natl. Acad. Sci. U. S. A. 85:5997-6001.
15. Harvey, T. J., W. J. Liu, X. J. Wang, R. Linedale, M. Jacobs, A. Davidson, T. T. Le, I. Anraku, A. Suhrbier, P. Y. Shi, and A. A. Khromykh. 2004. Tetracycline-inducible packaging cell line for production of flavivirus replicon particles. J. Virol. 78:531-538.
16. Heinz, F. X., W. Tuma, F. Guirakhoo, and C. Kunz. 1986. A model study of the use of monoclonal antibodies in capture enzyme immunoassays for antigen quantification exploiting the epitope map of tick-borne encephalitis virus. J. Biol. Stand. 14:133-141.
17. Higgs, S., D. L. Vanlandingham, K. A. Klingler, K. L. McElroy, C. E. McGee, L. Harrington, J. Lang, T. P. Monath, and F. Guirakhoo. 2006. Growth characteristics of ChimeriVax-Den vaccine viruses in Aedes aegypti and Aedes albopictus from Thailand. Am. J. Trop. Med. Hyg. 75:986-993.
18. Holland, J., K. Spindler, F. Horodyski, E. Grabau, S. Nichol, and S. Vande- Pol. 1982. Rapid evolution of RNA genomes. Science 215:1577-1585.
19. Holmes, E. C., and S. S. Twiddy. 2003. The origin, emergence and evolutionary genetics of dengue virus. Infect. Genet. Evol. 3:19-28.
20. Holmes, E. C., M. Worobey, and A. Rambaut. 1999. Phylogenetic evidence for recombination in dengue virus. Mol. Biol. Evol. 16:405-409.
21. Hu, W. S., and H. M. Temin. 1990. Retroviral recombination and reverse transcription. Science 250:1227-1233.
22. Huang, C. Y., S. Butrapet, K. R. Tsuchiya, N. Bhamarapravati, D. J. Gubler, and R. M. Kinney. 2003. Dengue 2 PDK-53 virus as a chimeric carrier for tetravalent dengue vaccine development. J. Virol. 77:11436-11447.
23. Jenkins, G. M., A. Rambaut, O. G. Pybus, and E. C. Holmes. 2002. Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J. Mol. Evol. 54:156-165.
24. Khromykh, A. A., A. N. Varnavski, and E. G. Westaway. 1998. Encapsidation of the flavivirus kunjin replicon RNA by using a complementation system providing Kunjin virus structural proteins in trans. J. Virol. 72:5967-5977.
25. Kofler, R. M., J. H. Aberle, S. W. Aberle, S. L. Allison, F. X. Heinz, and C. W. Mandl. 2004. Mimicking live flavivirus immunization with a noninfectious RNA vaccine. Proc. Natl. Acad. Sci. U. S. A. 101:1951-1956.
26. Kofler, R. M., F. X. Heinz, and C. W. Mandl. 2002. Capsid protein C of tick-borne encephalitis virus tolerates large internal deletions and is a favorable target for attenuation of virulence. J. Virol. 76:3534-3543.
27. Kofler, R. M., F. X. Heinz, and C. W. Mandl. 2004. A novel principle of attenuation for the development of new generation live flavivirus vaccines. Arch. Virol. Suppl. 18:191-200.
28. Kofler, R. M., V. M. Hoenninger, C. Thurner, and C. W. Mandl. 2006. Functional analysis of the tick-borne encephalitis virus cyclization elements indicates major differences between mosquito-borne and tick-borne flaviviruses. J. Virol. 80:4099-4113.
29. Kofler, R. M., A. Leitner, G. O'Riordain, F. X. Heinz, and C. W. Mandl. 2003. Spontaneous mutations restore the viability of tick-borne encephalitis virus mutants with large deletions in protein C. J. Virol. 77:443-451.
30. Kopek, B. G., G. Perkins, D. J. Miller, M. H. Ellisman, and P. Ahlquist. 2007. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 5:e220.
31. Lai, M. M. 1992. RNA recombination in animal and plant viruses. Microbiol. Rev. 56:61-79.
32. Lazzarini, R. A., J. D. Keene, and M. Schubert. 1981. The origins of defective interfering particles of the negative-strand RNA viruses. Cell 26:145-154.
33. Liao, C. L., and M. M. Lai. 1992. RNA recombination in a coronavirus: recombination between viral genomic RNA and transfected RNA fragments. J. Virol. 66:6117-6124.
34. Mandl, C. W., M. Ecker, H. Holzmann, C. Kunz, and F. X. Heinz. 1997. Infectious cDNA clones of tick-borne encephalitis virus European subtype prototypic strain Neudoerfl and high virulence strain Hypr. J. Gen. Virol. 78(pt. 5):1049-1057.
35. Meyers, G., N. Tautz, E. J. Dubovi, and H. J. Thiel. 1991. Viral cytopathogenicity correlated with integration of ubiquitin-coding sequences. Virology 180:602-616.
36. Meyers, G., and H. J. Thiel. 1996. Molecular characterization of pestiviruses. Adv. Virus Res. 47:53-118.
37. 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(pt. 4):693-706.
38. Monath, T. P., F. Guirakhoo, R. Nichols, S. Yoksan, R. Schrader, C. Murphy, P. Blum, S. Woodward, K. McCarthy, D. Mathis, C. Johnson, and P. Bedford. 2003. Chimeric live, attenuated vaccine against Japanese encephalitis (ChimeriVax-JE): phase 2 clinical trials for safety and immunogenicity, effect of vaccine dose and schedule, and memory response to challenge with inactivated Japanese encephalitis antigen. J. Infect. Dis. 188:1213-1230.
39. Monath, T. P., N. Kanesa-Thasan, F. Guirakhoo, K. Pugachev, J. Almond, J. Lang, M. J. Quentin-Millet, A. D. Barrett, M. A. Brinton, M. S. Cetron, R. S. Barwick, T. J. Chambers, S. B. Halstead, J. T. Roehrig, R. M. Kinney, R. Rico-Hesse, and J. H. Strauss. 2005. Recombination and flavivirus vaccines: a commentary. Vaccine 23:2956-2958.
40. Monath, T. P., I. Levenbook, K. Soike, Z. X. Zhang, M. Ratterree, K. Draper, A. D. Barrett, R. Nichols, R. Weltzin, J. Arroyo, and F. Guirakhoo. 2000. Chimeric yellow fever virus 17D-Japanese encephalitis virus vaccine: dose-response effectiveness and extended safety testing in rhesus monkeys. J. Virol. 74:1742-1751.
41. Mukhopadhyay, S., R. J. Kuhn, and M. G. Rossmann. 2005. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3:13-22.
42. Nagy, P. D., and A. E. Simon. 1997. New insights into the mechanisms of RNA recombination. Virology 235:1-9. (Pubitemid 27380801)
43. Orlinger, K. K., V. M. Hoenninger, R. M. Kofler, and C. W. Mandl. 2006. Construction and mutagenesis of an artificial bicistronic tick-borne encephalitis virus genome reveals an essential function of the second transmembrane region of protein E in flavivirus assembly. J. Virol. 80:12197-12208.
44. Raju, R., S. V. Subramaniam, and M. Hajjou. 1995. Genesis of Sindbis virus by in vivo recombination of nonreplicative RNA precursors. J. Virol. 69: 7391-7401. (Pubitemid 3004387)
45. Sabchareon, A., J. Lang, P. Chanthavanich, S. Yoksan, R. Forrat, P. Attanath, C. Sirivichayakul, K. Pengsaa, C. Pojjaroen-Anant, L. Chambonneau, J. F. Saluzzo, and N. Bhamarapravati. 2004. Safety and immunogenicity of a three dose regimen of two tetravalent live-attenuated dengue vaccines in five- to twelve-year-old Thai children. Pediatr. Infect. Dis. J. 23:99-109.
46. Schlick, P., C. Taucher, B. Schittl, J. L. Tran, R. M. Kofler, W. Schueler, A. von Gabain, A. Meinke, and C. W. Mandl. 2009. Helices 2 and 3 of West Nile virus capsid protein are dispensable for assembly of infectious virions. J. Virol. 83:5581-5591.
47. Scholle, F., Y. A. Girard, Q. Zhao, S. Higgs, and P. W. Mason. 2004. trans-Packaged West Nile virus-like particles: infectious properties in vitro and in infected mosquito vectors. J. Virol. 78:11605-11614.
48. Schrauf, S., P. Schlick, T. Skern, and C. W. Mandl. 2008. Functional analysis of potential carboxy-terminal cleavage sites of tick-borne encephalitis virus capsid protein. J. Virol. 82:2218-2229. (Pubitemid 351293522)
49. Seligman, S. J., and E. A. Gould. 2004. Live flavivirus vaccines: reasons for caution. Lancet 363:2073-2075. (Pubitemid 38781111)
50. Shustov, A. V., P. W. Mason, and I. Frolov. 2007. Production of pseudoinfectious yellow fever virus with a two-component genome. J. Virol. 81:11737-11748.
51. Stuhlmann, H., and P. Berg. 1992. Homologous recombination of copackaged retrovirus RNAs during reverse transcription. J. Virol. 66:2378-2388.
52. Tolou, H. J., P. Couissinier-Paris, J. P. Durand, V. Mercier, J. J. de Pina, P. de Micco, F. Billoir, R. N. Charrel, and X. de Lamballerie. 2001. Evidence for recombination in natural populations of dengue virus type 1 based on the analysis of complete genome sequences. J. Gen. Virol. 82:1283-1290.
53. Twiddy, S. S., and E. C. Holmes. 2003. The extent of homologous recombination in members of the genus Flavivirus. J. Gen. Virol. 84:429-440.
54. Uzcategui, N. Y., D. Camacho, G. Comach, R. Cuello de Uzcategui, E. C. Holmes, and E. A. Gould. 2001. Molecular epidemiology of dengue type 2 virus in Venezuela: evidence for in situ virus evolution and recombination. J. Gen. Virol. 82:2945-2953.
55. Weiss, B. G., and S. Schlesinger. 1991. Recombination between Sindbis virus RNAs. J. Virol. 65:4017-4025.
56. Welsch, S., S. Miller, I. Romero-Brey, A. Merz, C. K. Bleck, P. Walther, S. D. Fuller, C. Antony, J. Krijnse-Locker, and R. Bartenschlager. 2009. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5:365-375.
57. Widman, D. G., T. Ishikawa, R. Fayzulin, N. Bourne, and P. W. Mason. 2008. Construction and characterization of a second-generation pseudoinfectious West Nile virus vaccine propagated using a new cultivation system. Vaccine 26:2762-2771.
58. Worobey, M., and E. C. Holmes. 1999. Evolutionary aspects of recombination in RNA viruses. J. Gen. Virol. 80(pt. 10):2535-2543.
59. Worobey, M., A. Rambaut, and E. C. Holmes. 1999. Widespread intra-serotype recombination in natural populations of dengue virus. Proc. Natl. Acad. Sci. U. S. A. 96:7352-7357.