1887

Abstract

Cross-neutralization between rabies virus (RABV) and two European bat lyssaviruses (EBLV-1 and -2) was analysed using lentiviral pseudotypes as antigen vectors. Glycoprotein (G-protein) cDNA from RABV challenge virus standard-11 (CVS-11) and EBLV-1 and -2 were cloned and co-expressed with human immunodeficiency virus (HIV) or murine leukemia virus (MLV) and packageable green fluorescent protein (GFP) or luciferase reporter genes in human cells. The harvested lentiviral (HIV) vector infected over 40 % of baby hamster kidney (BHK) target cells, providing high-titre pseudotype stocks. Tests on blinded antibody-positive (=15) and -negative (=45) sera, predetermined by the fluorescent antibody virus neutralization (FAVN) test approved by the World Health Organization (WHO) and Office International des Epizooties (OIE), revealed that the CVS-11 pseudotype assay had 100 % concordance with FAVN and strongly correlated with neutralization titres ( =0.89). Cross-neutralization tests using sera from RABV-vaccinated humans and animals on pseudotypes with CVS-11, EBLV-1 and EBLV-2 envelopes showed that the relative neutralization titres correlated broadly with the degree of G-protein diversity. Pseudotypes have three major advantages over live-virus neutralization tests: (i) they can be handled in low-biohazard-level laboratories; (ii) the use of reporter genes such as GFP or -galactosidase will allow the assay to be undertaken at low cost in laboratories worldwide; (iii) each assay requires <10 μl serum. This robust microassay will improve our understanding of the protective humoral immunity that current rabies vaccines confer against emerging lyssaviruses, and will be applicable to surveillance studies, thus helping to control the spread of rabies.

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2008-09-01
2024-03-29
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References

  1. Badrane H., Bahloul C., Perrin P., Tordo N. 2001; Evidence of two Lyssavirus phylogroups with distinct pathogenicity and immunogenicity. J Virol 75:3268–3276 [CrossRef]
    [Google Scholar]
  2. Bartosch B., Bukh J., Meunier J. C., Granier C., Engle R. E., Blackwelder W. C., Emerson S. U., Cosset F. L., Purcell R. H. 2003; In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc Natl Acad Sci U S A 100:14199–14204 [CrossRef]
    [Google Scholar]
  3. Bresson J. L., Perronne C., Launay O., Gerdil C., Saville M., Wood J., Hoschler K., Zambon M. C. 2006; Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet 367:1657–1664 [CrossRef]
    [Google Scholar]
  4. Brookes S. M., Parsons G., Johnson N., McElhinney L. M., Fooks A. R. 2005; Rabies human diploid cell vaccine elicits cross-neutralising and cross-protecting immune responses against European and Australian bat lyssaviruses. Vaccine 23:4101–4109 [CrossRef]
    [Google Scholar]
  5. Clapham P., Nagy K., Weiss R. A. 1984; Pseudotypes of human T-cell leukemia virus types 1 and 2: neutralization by patients' sera. Proc Natl Acad Sci U S A 81:2886–2889 [CrossRef]
    [Google Scholar]
  6. Cliquet F., Aubert M., Sagne L. 1998; Development of a fluorescent antibody virus neutralisation test (FAVN test) for the quantitation of rabies-neutralising antibody. J Immunol Methods 212:79–87 [CrossRef]
    [Google Scholar]
  7. Cliquet F., McElhinney L. M., Servat A., Boucher J. M., Lowings J. P., Goddard T., Mansfield K. L., Fooks A. R. 2004; Development of a qualitative indirect ELISA for the measurement of rabies virus-specific antibodies from vaccinated dogs and cats. J Virol Methods 117:1–8 [CrossRef]
    [Google Scholar]
  8. Condit R. C. 2001; Principles of Virology. In Fields Virology . , 4th edn. vol 1 pp 19–51Edited by Knipe D. M., Howley. Philadelphia: Lippincott Williams & Wilkins;
  9. Cox J. H., Dietzschold B., Schneider L. G. 1977; Rabies virus glycoprotein. II. Biological and serological characterization. Infect Immun 16:754–759
    [Google Scholar]
  10. Cox R. J., Mykkeltvedt E., Robertson J., Haaheim L. R. 2002; Non-lethal viral challenge of influenza haemagglutinin and nucleoprotein DNA vaccinated mice results in reduced viral replication. Scand J Immunol 55:14–23 [CrossRef]
    [Google Scholar]
  11. Dalgleish A. G., Beverley P. C., Clapham P. R., Crawford D. H., Greaves M. F., Weiss R. A. 1984; The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312:763–767 [CrossRef]
    [Google Scholar]
  12. Demaison C., Parsley K., Brouns G., Scherr M., Battmer K., Kinnon C., Grez M., Thrasher A. J. 2002; High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther 13:803–813 [CrossRef]
    [Google Scholar]
  13. Desmaris N., Bosch A., Salaun C., Petit C., Prevost M. C., Tordo N., Perrin P., Schwartz O., de Rocquigny H. other authors 2001; Production and neurotropism of lentivirus vectors pseudotyped with lyssavirus envelope glycoproteins. Mol Ther 4:149–156 [CrossRef]
    [Google Scholar]
  14. Dietzschold B., Lafon M., Wang H., Otvos L. Jr, Celis E., Wunner W. H., Koprowski H. 1987; Localization and immunological characterization of antigenic domains of the rabies virus internal N and NS proteins. Virus Res 8:103–125 [CrossRef]
    [Google Scholar]
  15. DuBridge R. B., Tang P., Hsia H. C., Leong P. M., Miller J. H., Calos M. P. 1987; Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol Cell Biol 7:379–387
    [Google Scholar]
  16. Fooks A. 2004; The challenge of new and emerging lyssaviruses. Expert Rev Vaccines 3:333–336 [CrossRef]
    [Google Scholar]
  17. Fooks A. R. 2005; Rabies remains a ‘neglected disease’. Euro Surveill 10:211–212
    [Google Scholar]
  18. Fooks A. R., Brookes S. M., Johnson N., McElhinney L. M., Hutson A. M. 2003; European bat lyssaviruses: an emerging zoonosis. Epidemiol Infect 131:1029–1039 [CrossRef]
    [Google Scholar]
  19. Hanlon C. A., Kuzmin I. V., Blanton J. D., Weldon W. C., Manangan J. S., Rupprecht C. E. 2005; Efficacy of rabies biologics against new lyssaviruses from Eurasia. Virus Res 111:44–54 [CrossRef]
    [Google Scholar]
  20. Khawplod P., Inoue K., Shoji Y., Wilde H., Ubol S., Nishizono A., Kurane I., Morimoto K. 2005; A novel rapid fluorescent focus inhibition test for rabies virus using a recombinant rabies virus visualizing a green fluorescent protein. J Virol Methods 125:35–40 [CrossRef]
    [Google Scholar]
  21. Mallewa M., Fooks A. R., Banda D., Chikungwa P., Mankhambo L., Molyneux E., Molyneux M. E., Solomon T. 2007; Rabies encephalitis in malaria-endemic area, Malawi, Africa. Emerg Infect Dis 13:136–139 [CrossRef]
    [Google Scholar]
  22. Mazarakis N. D., Azzouz M., Rohll J. B., Ellard F. M., Wilkes F. J., Olsen A. L., Carter E. E., Barber R. D., Baban D. F. other authors 2001; Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum Mol Genet 10:2109–2121 [CrossRef]
    [Google Scholar]
  23. Mentis G. Z., Gravell M., Hamilton R., Shneider N. A., O'Donovan M. J., Schubert M. 2006; Transduction of motor neurons and muscle fibers by intramuscular injection of HIV-1-based vectors pseudotyped with select rabies virus glycoproteins. J Neurosci Methods 157:208–217 [CrossRef]
    [Google Scholar]
  24. Naldini L., Blomer U., Gallay P., Ory D., Mulligan R., Gage F. H., Verma I. M., Trono D. 1996; In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263–267 [CrossRef]
    [Google Scholar]
  25. Op De Beeck A., Voisset C., Bartosch B., Ciczora Y., Cocquerel L., Keck Z., Foung S., Cosset F. L., Dubuisson J. 2004; Characterization of functional hepatitis C virus envelope glycoproteins. J Virol 78:2994–3002 [CrossRef]
    [Google Scholar]
  26. Soda Y., Shimizu N., Jinno A., Liu H. Y., Kanbe K., Kitamura T., Hoshino H. 1999; Establishment of a new system for determination of coreceptor usages of HIV based on the human glioma NP-2 cell line. Biochem Biophys Res Commun 258:313–321 [CrossRef]
    [Google Scholar]
  27. Stoker M., Macpherson I. 1964; Syrian hamster fibroblast cell line BHK21 and its derivatives. Nature 203:1355–1357 [CrossRef]
    [Google Scholar]
  28. Stratton M. R., Darling J., Pilkington G. J., Lantos P. L., Reeves B. R., Cooper C. S. 1989; Characterization of the human cell line TE671. Carcinogenesis 10:899–905 [CrossRef]
    [Google Scholar]
  29. Takeuchi Y., Porter C. D., Strahan K. M., Preece A. F., Gustafsson K., Cosset F. L., Weiss R. A., Collins M. K. 1996; Sensitization of cells and retroviruses to human serum by (alpha 1–3) galactosyltransferase. Nature 379:85–88 [CrossRef]
    [Google Scholar]
  30. Temperton N. J., Chan P. K., Simmons G., Zambon M. C., Tedder R. S., Takeuchi Y., Weiss R. A. 2005; Longitudinally profiling neutralizing antibody response to SARS coronavirus with pseudotypes. Emerg Infect Dis 11:411–416 [CrossRef]
    [Google Scholar]
  31. Temperton N. J., Hoschler K., Major D., Nicolson C., Manvell R., Hien V. M., Ha D. Q., Jong M. D., Zambon M. other authors 2007; A sensitive retroviral pseudotype assay for influenza H5N1-neutralizing antibodies. Influenza Resp Viruses 1:105–112 [CrossRef]
    [Google Scholar]
  32. Towers G. J. 2007; The control of viral infection by tripartite motif proteins and cyclophilin A. Retrovirology 4:40 [CrossRef]
    [Google Scholar]
  33. Towers G., Bock M., Martin S., Takeuchi Y., Stoye J. P., Danos O. 2000; A conserved mechanism of retrovirus restriction in mammals. Proc Natl Acad Sci U S A 97:12295–12299 [CrossRef]
    [Google Scholar]
  34. WHO 2006; Rabies . Fact Sheet No: 99 Geneva: World Helath Organisation;
    [Google Scholar]
  35. Wool-Lewis R. J., Bates P. 1998; Characterization of Ebola virus entry by using pseudotyped viruses: identification of receptor-deficient cell lines. J Virol 72:3155–3160
    [Google Scholar]
  36. Zufferey R., Nagy D., Mandel R. J., Naldini L., Trono D. 1997; Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 15:871–875 [CrossRef]
    [Google Scholar]
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