Induction of epitope-specific neutralizing antibodies against West Nile virus

Journal of Virology

Volumn 81, Issue 21, 2007, Pages 11828-11839

  Oliphant, Theodore ^a   Nybakken, Grant E ^a   Austin, S Kyle ^a   Xu, Qing ^b   Bramson, Jonathan ^c   Loeb, Mark ^c   Throsby, Mark ^d   Fremont, Daved H ^a   Pierson, Theodore C ^b   Diamond, Michael S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c MCMASTER UNIVERSITY   (Canada)

^d CRUCELL HOLLAND BV   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CROSS REACTING ANTIBODY; ENVELOPE PROTEIN; EPITOPE; IMMUNOGLOBULIN ANTIBODY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M ANTIBODY; NEUTRALIZING ANTIBODY;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; GENE FUNCTION; GENETIC VARIABILITY; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; VIRUS PARTICLE; WEST NILE FLAVIVIRUS; WILD TYPE;

ANIMALS; ANTIBODIES; CLONING, MOLECULAR; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MICE; MICE, INBRED C57BL; PROTEIN FOLDING; SURFACE PLASMON RESONANCE; WEST NILE VIRUS; WEST NILE VIRUS VACCINES;

FLAVIVIRUS; MUS; WEST NILE VIRUS;

EID: 35449004580     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00643-07     Document Type: Article

References (61)

1. Allison, S. L., J. Schalich, K. Stiasny, C. W. Mandl, and F. X. Heinz. 2001. Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. J. Virol. 75:4268-4275.
2. Baumgarth, N., O. C. Herman, G. C. Jager, L. Brown, and L. A. Herzenberg. 1999. Innate and acquired humoral immunities to influenza virus are mediated by distinct arms of the immune system. Proc. Natl. Acad. Sci. USA 96:2250-2255.
3. Baumgarth, N., O. C. Herman, G. C. Jager, L. E. Brown, L. A. Herzenberg, and J. Chen. 2000. B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J. Exp. Med. 192:271-280.
4. Beasley, D. W., and A. D. Barrett. 2002. Identification of neutralizing epitopes within structural domain III of the West Nile virus envelope protein. J. Virol. 76:13097-13100.
5. Beasley, D. W., M. C. Whiteman, S. Zhang, C. Y. Huang, B. S. Schneider, D. R. Smith, G. D. Gromowski, S. Higgs, R. M. Kinney, and A. D. Barrett. 2005. Envelope protein glycosylation status influences mouse neuroinvasion phenotype of genetic lineage 1 West Nile virus strains. J. Virol. 79:8339-8347.
6. Ben-Nathan, D., S. Lustig, G. Tam, S. Robinzon, S. Segal, and B. Rager-Zisman. 2003. Prophylactic and therapeutic efficacy of human intravenous immunoglobulin in treating West Nile virus infection in mice. J. Infect. Dis. 188:5-12.
7. Berek, C., A. Berger, and M. Apel. 1991. Maturation of the immune response in germinal centers. Cell 67:1121-1129.
8. Bhardwaj, S., M. Holbrook, R. E. Shope, A. D. Barrett, and S. J. Watowich. 2001. Biophysical characterization and vector-specific antagonist activity of domain III of the tick-borne flavivirus envelope protein. J. Virol. 75:4002-4007.
9. Bressanelli, S., K. Stiasny, S. L. Allison, E. A. Stura, S. Duquerroy, J. Lescar, F. X. Heinz, and F. A. Rey. 2004. Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J. 23:728-738.
10. Chambers, T. J., M. Halevy, A. Nestorowicz, C. M. Rice, and S. Lustig. 1998. West Nile virus envelope proteins: nucleotide sequence analysis of strains differing in mouse neuroinvasiveness. J. Gen. Virol. 79(Pt. 10):2375-2380.
11. Chu, J. H., C. C. Chiang, and M. L. Ng. 2007. Immunization of flavivirus West Nile recombinant envelope domain III protein induced specific immune response and protection against West Nile virus infection. J. Immunol. 178:2699-2705.
12. Chu, J. J., R. Rajamanonmani, J. Li, R. Bhuvanakantham, J. Lescar, and M. L. Ng. 2005. Inhibition of West Nile virus entry by using a recombinant domain III from the envelope glycoprotein. J. Gen. Virol. 86:405-412.
13. Crill, W. D., and G. J. Chang. 2004. Localization and characterization of flavivirus envelope glycoprotein cross-reactive epitopes. J. Virol. 78:13975-13986.
14. Crill, W. D., and J. T. Roehrig. 2001. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J. Virol. 75:7769-7773.
15. Czar, M. J., E. N. Kersh, L. A. Mijares, G. Lanier, J. Lewis, G. Yap, A. Chen, A. Sher, C. S. Duckett, R. Ahmed, and P. L. Schwartzberg. 2001. Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lymphoproliferative disease gene SH2D1A/DSHP/SAP. Proc. Natl. Acad. Sci. USA 98:7449-7454.
16. Diamond, M. S., B. Shrestha, A. Marri, D. Mahan, and M. Engle. 2003. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J. Virol. 77:2578-2586.
17. Diamond, M. S., E. M. Sitati, L. D. Friend, S. Higgs, B. Shrestha, and M. Engle. 2003. A critical role for induced IgM in the protection against West Nile virus infection. J. Exp. Med. 198:1853-1862.
18. Engle, M. J., and M. S. Diamond. 2003. Antibody prophylaxis and therapy against West Nile virus infection in wild-type and immunodeficient mice. J. Virol. 77:12941-12949.
19. Goncalvez, A. P., R. H. Purcell, and C. J. Lai. 2004. Epitope determinants of a chimpanzee Fab antibody that efficiently cross-neutralizes dengue type 1 and type 2 viruses map to inside and in close proximity to fusion loop of the dengue type 2 virus envelope glycoprotein. J. Virol. 78:12919-12928.
20. Gould, L. H., J. Sui, H. Foellmer, T. Oliphant, T. Wang, M. Ledizet, A. Murakami, K. Noonan, C. Lambeth, K. Kar, J. F. Anderson, A. M. de Silva, M. S. Diamond, R. A. Koski, W. A. Marasco, and E. Fikrig. 2005. Protective and therapeutic capacity of human single-chain Fv-Fc fusion proteins against West Nile virus. J. Virol. 79:14606-14613.
21. Hoover, D. M., and J. Lubkowski. 2002. DNAWorks: an automated method for designing oligonucleotides for PCR-based gene synthesis. Nucleic Acids Res. 30:e43.
22. Iglesias, M. C., M. P. Frenkiel, K. Mollier, P. Souque, P. Despres, and P. Charneau. 2006. A single immunization with a minute dose of a lentiviral vector-based vaccine is highly effective at eliciting protective humoral immunity against West Nile virus. J. Gene Med. 8:265-274.
23. Jacob, J., G. Kelsoe, K. Rajewsky, and U. Weiss. 1991. Intraclonal generation of antibody mutants in germinal centres. Nature 354:389-392.
24. Johnson, A. J., and J. T. Roehrig. 1999. New mouse model for dengue virus vaccine testing. J. Virol. 73:783-786.
25. Kaufman, B. M., P. L. Summers, D. R. Dubois, and K. H. Eckels. 1987. Monoclonal antibodies against dengue 2 virus E-glycoprotein protect mice against lethal dengue infection. Am. J. Trop. Med. Hyg. 36:427-434.
26. Kim, I. J., C. E. Burkum, T. Cookenham, P. L. Schwartzberg, D. L. Woodland, and M. A. Blackman. 2007. Perturbation of B cell activation in SLAM-associated protein-deficient mice is associated with changes in gammaherpesvirus latency reservoirs. J. Immunol. 178:1692-1701.
27. Kuhn, R. J., W. Zhang, M. G. Rossmann, S. V. Pletnev, J. Corver, E. Lenches, C. T. Jones, S. Mukhopadhyay, P. R. Chipman, E. G. Strauss, T. S. Baker, and J. H. Strauss. 2002. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108:717-725.
28. Lanciotti, R. S., J. T. Roehrig, V. Deubel, J. Smith, M. Parker, K. Steele, B. Crise, K. E. Volpe, M. B. Crabtree, J. H. Scherret, R. A. Hall, J. S. MacKenzie, C. B. Cropp, B. Panigrahy, E. Ostlund, B. Schmitt, M. Malkinson, C. Banet, J. Weissman, N. Komar, H. M. Savage, W. Stone, T. McNamara, and D. J. Gubler. 1999. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286:2333-2337.
29. Ledizet, M., K. Kar, H. G. Foellmer, T. Wang, S. L. Bushmich, J. F. Anderson, E. Fikrig, and R. A. Koski. 2005. A recombinant envelope protein vaccine against West Nile virus. Vaccine 23:3915-3924.
30. Lieberman, M. M., D. E. Clements, S. Ogata, G. Wang, G. Corpuz, T. Wong, T. Martyak, L. Gilson, B. A. Coller, J. Leung, D. M. Watts, R. B. Tesh, M. Siirin, A. Travassos da Rosa, T. Humphreys, and C. Weeks-Levy. 2006. Preparation and immunogenic properties of a recombinant West Nile subunit vaccine. Vaccine.
31. Mason, P. W., A. V. Shustov, and I. Frolov. 2006. Production and characterization of vaccines based on flaviviruses defective in replication. Virology 351:432-443.
32. Mehlhop, E., and M. S. Diamond. 2006. Protective immune responses against West Nile virus are primed by distinct complement activation pathways. J. Exp. Med. 203:1371-1381.
33. Mehlhop, E., K. Whitby, T. Oliphant, A. Marri, M. Engle, and M. S. Diamond. 2005. Complement activation is required for induction of a protective antibody response against West Nile virus infection. J. Virol. 79:7466-7477.
34. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2003. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. USA 100:6986-6991.
35. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313-319.
36. Monath, T. P., J. Liu, N. Kanesa-Thasan, G. A. Myers, R. Nichols, A. Deary, K. McCarthy, C. Johnson, T. Ermak, S. Shin, J. Arroyo, F. Guirakhoo, J. S. Kennedy, F. A. Ennis, S. Green, and P. Bedford. 2006. A live, attenuated recombinant West Nile virus vaccine. Proc. Natl. Acad. Sci. USA 103:6694-6699.
37. Morrey, J. D., V. Siddharthan, A. L. Olsen, G. Y. Roper, H. Wang, T. J. Baldwin, S. Koenig, S. Johnson, J. L. Nordstrom, and M. S. Diamond. 2006. Humanized monoclonal antibody against West Nile virus envelope protein administered after neuronal infection protects against lethal encephalitis in hamsters. J. Infect. Dis. 194:1300-1308.
38. Mukhopadhyay, S., B. S. Kim, P. R. Chipman, M. G. Rossmann, and R. J. Kuhn. 2003. Structure of West Nile virus. Science 302:248.
39. Nash, D., F. Mostashari, A. Fine, J. Miller, D. O'Leary, K. Murray, A. Huang, A. Rosenberg, A. Greenberg, M. Sherman, S. Wong, and M. Layton. 2001. The outbreak of West Nile virus infection in the New York City area in 1999. N. Engl. J. Med. 344:1807-1814.
40. Ng, T., D. Hathaway, N. Jennings, D. Champ, Y. W. Chiang, and H. J. Chu. 2003. Equine vaccine for West Nile virus. Dev. Biol. 114:221-227.
41. Nybakken, G. E., C. A. Nelson, B. R. Chen, M. S. Diamond, and D. H. Fremont. 2006. Crystal structure of the West Nile virus envelope glycoprotein. J. Virol. 80:11467-11474.
42. Nybakken, G. E., T. Oliphant, S. Johnson, S. Burke, M. S. Diamond, and D. H. Fremont. 2005. Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature 437:764-769.
43. Ochsenbein, A. F., T. Fehr, C. Lutz, M. Suter, F. Brombacher, H. Hengartner, and R. M. Zinkernagel. 1999. Control of early viral and bacterial distribution and disease by natural antibodies. Science 286:2156-2159.
44. Oliphant, T., M. Engle, G. E. Nybakken, C. Doane, S. Johnson, L. Huang, S. Gorlatov, E. Mehlhop, A. Marri, K. M. Chung, G. D. Ebel, L. D. Kramer, D. H. Fremont, and M. S. Diamond. 2005. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat. Med. 11:522-530.
45. Oliphant, T., G. E. Nybakken, M. Engle, Q. Xu, C. A. Nelson, S. Sukupolvi-Petty, A. Marri, B. E. Lachmi, U. Olshevsky, D. H. Fremont, T. C. Pierson, and M. S. Diamond. 2006. Antibody recognition and neutralization determinants on domains I and II of West Nile virus envelope protein. J. Virol. 80:12149-12159.
46. Pierson, T. C., M. D. Sanchez, B. A. Puffer, A. A. Ahmed, B. J. Geiss, L. E. Valentine, L. A. Altamura, M. S. Diamond, and R. W. Doms. 2006. A rapid and quantitative assay for measuring antibody-mediated neutralization of West Nile virus infection. Virology 346:53-65.
47. Pierson, T. C., Q. Xu, S. Nelson, T. Oliphant, G. E. Nybakken, D. H. Fremont, and M. S. Diamond. 2007. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1:135-145.
48. Pletnev, A. G., M. S. Claire, R. Elkins, J. Speicher, B. R. Murphy, and R. M. Chanock. 2003. Molecularly engineered live-attenuated chimeric West Nile/dengue virus vaccines protect rhesus monkeys from West Nile virus. Virology 314:190-195.
49. Sanchez, M. D., T. C. Pierson, M. M. Degrace, L. M. Mattei, S. L. Hanna, F. Del Piero, and R. W. Doms. 2007. The neutralizing antibody response against West Nile virus in naturally infected horses. Virology 359:336-348.
50. Sanchez, M. D., T. C. Pierson, D. McAllister, S. L. Hanna, B. A. Puffer, L. E. Valentine, M. M. Murtadha, J. A. Hoxie, and R. W. Doms. 2005. Characterization of neutralizing antibodies to West Nile virus. Virology 336:70-82.
51. Stiasny, K., S. Kiermayr, H. Holzmann, and F. X. Heinz. 2006. Cryptic properties of a cluster of dominant flavivirus cross-reactive antigenic sites. J. Virol. 80:9557-9568.
52. Throsby, M., C. Geuijen, J. Goudsmit, A. Q. Bakker, J. Korimbocus, R. A. Kramer, M. Clijsters-van der Horst, M. de Jong, M. Jongeneelen, S. Thijsse, R. Smit, T. J. Visser, N. Bijl, W. E. Marissen, M. Loeb, D. J. Kelvin, W. Preiser, J. ter Meulen, and J. de Kruif. 2006. Isolation and characterization of human monoclonal antibodies from individuals infected with West Nile Virus. J. Virol. 80:6982-6992.
53. Turbica, I., F. Simon, J. M. Besnier, B. LeJeune, P. Choutet, A. Goudeau, and F. Barin. 1997. Temporal development and prognostic value of antibody response to the major neutralizing epitopes of gp120 during HIV-1 infection. J. Med. Virol. 52:309-315.
54. Wang, T., J. F. Anderson, L. A. Magnarelli, S. J. Wong, R. A. Koski, and E. Fikrig. 2001. Immunization of mice against West Nile virus with recombinant envelope protein. J. Immunol. 167:5273-5277.
55. Wang, T., T. Town, L. Alexopoulou, J. F. Anderson, E. Fikrig, and R. A. Flavell. 2004. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med. 10:1366-1373.
56. + T cells mediate recovery and immunopathology in West Nile virus encephalitis. J. Virol. 77:13323-13334.
57. Wolf, R. F., J. F. Papin, R. Hines-Boykin, M. Chavez-Suarez, G. L. White, M. Sakalian, and D. P. Dittmer. 2006. Baboon model for West Nile virus infection and vaccine evaluation. Virology 355:44-51.
58. Wu, C., K. B. Nguyen, G. C. Pien, N. Wang, C. Gullo, D. Howie, M. R. Sosa, M. J. Edwards, P. Borrow, A. R. Satoskar, A. H. Sharpe, C. A. Biron, and C. Terhorst. 2001. SAP controls T-cell responses to virus and terminal differentiation of TH2 cells. Nat. Immunol. 2:410-414.
59. Zhang, S., L. Li, S. E. Woodson, C. Y. Huang, R. M. Kinney, A. D. Barrett, and D. W. Beasley. 2006. A mutation in the envelope protein fusion loop attenuates mouse neuroinvasiveness of the NY99 strain of West Nile virus. Virology 353:35-40.
60. Zhang, Y., W. Zhang, S. Ogata, D. Clements, J. H. Strauss, T. S. Baker, R. J. Kuhn, and M. G. Rossmann. 2004. Conformational changes of the flavivirus E glycoprotein. Structure 12:1607-1618.
61. Zwart, G., L. van der Hoek, M. Valk, M. T. Cornelissen, E. Baan, J. Dekker, M. Koot, C. L. Kuiken, and J. Goudsmit. 1994. Antibody responses to HIV-1 envelope and gag epitopes in HIV-1 seroconverters with rapid versus slow disease progression. Virology 201:285-293.