Protonation of individual histidine residues is not required for the pH-dependent entry of west nile virus: Evaluation of the "histidine switch" hypothesis

Journal of Virology

Volumn 83, Issue 23, 2009, Pages 12631-12635

  Nelson, Steevenson ^a   Poddar, Subhajit ^a   Lin, Tsai Yu ^a   Pierson, Theodore C ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; HISTIDINE; VIRUS ENVELOPE PROTEIN; VIRUS FUSION PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FLAVIVIRUS; LIFE CYCLE; NONHUMAN; PH; PRIORITY JOURNAL; PROTON TRANSPORT; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS MUTANT; VIRUS PARTICLE; WEST NILE FLAVIVIRUS;

AMINO ACID SUBSTITUTION; CELL LINE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, TERTIARY; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION; WEST NILE VIRUS;

FLAVIVIRUS; WEST NILE VIRUS;

EID: 70450162409     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01072-09     Document Type: Article

References (35)

1. Ansarah-Sobrinho, C., S. Nelson, C. A. Jost, S. S. Whitehead, and T. C. Pierson. 2008. Temperature-dependent production of pseudoinfectious dengue reporter virus particles by complementation. Virology 381:67-74.
2. 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. (Pubitemid 38425440)
3. Briese, T., and K. A. Bernard. 2005. West Nile virus - an old virus learning new tricks? J. Neurovirol. 11:469-475. (Pubitemid 43064686)
4. Carneiro, F. A., F. Stauffer, C. S. Lima, M. A. Juliano, L. Juliano, and A. T. Da Poian. 2003. Membrane fusion induced by vesicular stomatitis virus depends on histidine protonation. J. Biol. Chem. 278:13789-13794.
5. Chanel-Vos, C., and M. Kielian. 2004. A conserved histidine in the ij loop of the Semliki Forest virus E1 protein plays an important role in membrane fusion. J. Virol. 78:13543-13552. (Pubitemid 39612754)
6. Corver, J., A. Ortiz, S. L. Allison, J. Schalich, F. X. Heinz, and J. Wilschut. 2000. Membrane fusion activity of tick-borne encephalitis virus and recombinant subviral particles in a liposomal model system. Virology 269:37-46. (Pubitemid 30183167)
7. Davis, C. W., H. Y. Nguyen, S. L. Hanna, M. D. Sanchez, R. W. Doms, and T. C. Pierson. 2006. West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J. Virol. 80:1290-1301.
8. Ferlenghi, I., M. Clarke, T. Ruttan, S. L. Allison, J. Schalich, F. X. Heinz, S. C. Harrison, F. A. Rey, and S. D. Fuller. 2001. Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol. Cell 7:593-602. (Pubitemid 32706351)
9. Fritz, R., K. Stiasny, and F. X. Heinz. 2008. Identification of specific histidines as pH sensors in flavivirus membrane fusion. J. Cell Biol. 183:353-361.
10. Gollins, S. W., and J. S. Porterfield. 1985. Flavivirus infection enhancement in macrophages: an electron microscopic study of viral cellular entry. J. Gen. Virol. 66(Pt. 9):1969-1982.
11. Gollins, S. W., and J. S. Porterfield. 1984. Flavivirus infection enhancement in macrophages: radioactive and biological studies on the effect of antibody on viral fate. J. Gen. Virol. 65(Pt. 8):1261-1272.
12. Gollins, S. W., and J. S. Porterfield. 1986. pH-dependent fusion between the flavivirus West Nile and liposomal model membranes. J. Gen. Virol. 67:157-166.
13. Guirakhoo, F., A. R. Hunt, J. G. Lewis, and J. T. Roehrig. 1993. Selection and partial characterization of dengue 2 virus mutants that induce fusion at elevated pH. Virology 194:219-223. (Pubitemid 23211755)
14. Harrison, S. C. 2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15:690-698.
15. Kadlec, J., S. Loureiro, N. G. Abrescia, D. I. Stuart, and I. M. Jones. 2008. The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat. Struct. Mol. Biol. 15:1024-1030.
16. Kampmann, T., D. S. Mueller, A. E. Mark, P. R. Young, and B. Kobe. 2006. The role of histidine residues in low-pH-mediated viral membrane fusion. Structure 14:1481-1487. (Pubitemid 44486813)
17. Kanai, R., K. Kar, K. Anthony, L. H. Gould, M. Ledizet, E. Fikrig, W. A. Marasco, R. A. Koski, and Y. Modis. 2006. Crystal structure of West Nile virus envelope glycoprotein reveals viral surface epitopes. J. Virol. 80:11000-11008. (Pubitemid 44706541)
18. Krishnan, M. N., B. Sukumaran, U. Pal, H. Agaisse, J. L. Murray, T. W. Hodge, and E. Fikrig. 2007. Rab 5 is required for the cellular entry of dengue and West Nile viruses. J. Virol. 81:4881-4885.
19. 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.
20. Lindenbach, B. D., H. J. Thiel, and C. M. Rice. 2007. Flaviviridae: the viruses and their replication, p. 1101-1152. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 5th ed., vol.1. Lippincott-Williams & Wilkins, Philadelphia, PA.
21. Mueller, D. S., T. Kampmann, R. Yennamalli, P. R. Young, B. Kobe, and A. E. Mark. 2008. Histidine protonation and the activation of viral fusion proteins. Biochem. Soc. Trans. 36:43-45.
22. Mukhopadhyay, S., R. J. Kuhn, and M. G. Rossmann. 2005. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3:13-22.
23. Nelson, S., C. A. Jost, Q. Xu, J. Ess, J. E. Martin, T. Oliphant, S. S. Whitehead, A. P. Durbin, B. S. Graham, M. S. Diamond, and T. C. Pierson. 2008. Maturation of West Nile virus modulates sensitivity to antibody-mediated neutralization. PLoS Pathog. 4:e1000060.
24. 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.
25. 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.
26. 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. (Pubitemid 46554914)
27. Qin, Z. L., Y. Zheng, and M. Kielian. 2009. Role of conserved histidine residues in the low-pH dependence of the Semliki Forest virus fusion protein. J. Virol. 83:4670-4677.
28. Randolph, V. B., and V. Stollar. 1990. Low pH-induced cell fusion in flavivirus- infected Aedes albopictus cell cultures. J. Gen. Virol. 71(Pt. 8):1845-1850.
29. Stiasny, K., and F. X. Heinz. 2006. Flavivirus membrane fusion. J. Gen. Virol. 87:2755-2766.
30. Stiasny, K., C. Koessl, and F. X. Heinz. 2003. Involvement of lipids in different steps of the flavivirus fusion mechanism. J. Virol. 77:7856-7862. (Pubitemid 36792782)
31. Thoennes, S., Z. N. Li, B. J. Lee, W. A. Langley, J. J. Skehel, R. J. Russell, and D. A. Steinhauer. 2008. Analysis of residues near the fusion peptide in the influenza hemagglutinin structure for roles in triggering membrane fusion. Virology 370:403-414. (Pubitemid 350199676)
32. Thurlkill, R. L., G. R. Grimsley, J. M. Scholtz, and C. N. Pace. 2006. pK values of the ionizable groups of proteins. Protein Sci. 15:1214-1218.
33. van der Schaar, H. M., M. J. Rust, C. Chen, H. van der Ende-Metselaar, J. Wilschut, X. Zhuang, and J. M. Smit. 2008. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 4:e1000244.
34. van der Schaar, H. M., M. J. Rust, B. L. Waarts, H. van der Ende-Metselaar, R. J. Kuhn, J. Wilschut, X. Zhuang, and J. M. Smit. 2007. Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J. Virol. 81:12019-12028.
35. Vogt, M. R., B. Moesker, J. Goudsmit, M. Jongeneelen, S. K. Austin, T. Oliphant, S. Nelson, T. C. Pierson, J. Wilschut, M. Throsby, and M. S. Diamond. 2009. Human monoclonal antibodies against West Nile virus induced by natural infection neutralize at a postattachment step. J. Virol. 83:6494-6507.