Identification of residues in West Nile virus premembrane protein that influence viral particle secretion and virulence

Journal of General Virology

Volumn 93, Issue PART 9, 2012, Pages 1965-1975

  Setoh, Y X ^a   Prow, N A ^a   Hobson Peters, J ^a   Lobigs, M ^a   Young, P R ^a   Khromykh, A A ^a   Hall, R A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; ISOLEUCINE; LEUCINE; PRE MEMBRANE PROTEIN; SERINE; UNCLASSIFIED DRUG; VALINE; VIRUS PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN STRUCTURE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GOLGI COMPLEX; MOLECULAR CLONING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; VERO CELL; VIRUS PARTICLE; VIRUS RECOMBINANT; VIRUS STRAIN; VIRUS VIRULENCE; WEST NILE FLAVIVIRUS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; FEMALE; MICE; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; VIRAL ENVELOPE PROTEINS; VIRULENCE; VIRUS RELEASE; VIRUS REPLICATION; WEST NILE FEVER; WEST NILE VIRUS;

EID: 84865130553     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.044453-0     Document Type: Article

References (38)

1. Adams, S. C., Broom, A. K., Sammels, L. M., Hartnett, A. C., Howard, M. J., Coelen, R. J., Mackenzie, J. S. & Hall, R. A. (1995). Glycosylation and antigenic variation among Kunjin virus isolates. Virology 206, 49-56.
2. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. (2006). The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201.
3. Audsley, M., Edmonds, J., Liu, W., Mokhonov, V., Mokhonova, E., Melian, E. B., Prow, N., Hall, R. A. & Khromykh, A. A. (2011). Virulence determinants between New York 99 and Kunjin strains of West Nile virus. Virology 414, 63-73.
4. Beasley, D. W., Whiteman, M. C., Zhang, S., Huang, C. Y., Schneider, B. S., Smith, D. R., Gromowski, G. D., Higgs, S., Kinney, R. M. & Barrett, A. D. (2005). Envelope protein glycosylation status influences mouse neuroinvasion phenotype of genetic lineage 1 West Nile virus strains. J Virol 79, 8339-8347.
5. Bosshart, H., Humphrey, J., Deignan, E., Davidson, J., Drazba, J., Yuan, L., Oorschot, V., Peters, P. J. & Bonifacino, J. S. (1994). The cytoplasmic domain mediates localization of furin to the trans-Golgi network en route to the endosomal/lysosomal system. J Cell Biol 126, 1157-1172.
6. Brault, A. C., Huang, C. Y., Langevin, S. A., Kinney, R. M., Bowen, R. A., Ramey, W. N., Panella, N. A., Holmes, E. C., Powers, A. M. & Miller, B. R. (2007). A single positively selected West Nile viral mutation confers increased virogenesis in American crows. Nat Genet 39, 1162-1166.
7. Chang, G. J., Davis, B. S., Hunt, A. R., Holmes, D. A. & Kuno, G. (2001). Flavivirus DNA vaccines: current status and potential. Ann N Y Acad Sci 951, 272-285.
8. Ellgaard, L. & Helenius, A. (2003). Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4, 181-191.
9. Goto, A., Yoshii, K., Obara, M., Ueki, T., Mizutani, T., Kariwa, H. & Takashima, I. (2005). Role of the N-linked glycans of the prM and Eenvelope proteins in tick-borne encephalitis virus particle secretion. Vaccine 23, 3043-3052.
10. Hall, R. A., Broom, A. K., Smith, D. W. & Mackenzie, J. S. (2002). The ecology and epidemiology of Kunjin virus. Curr Top Microbiol Immunol 267, 253-269.
11. Hanna, S. L., Pierson, T. C., Sanchez, M. D., Ahmed, A. A., Murtadha, M. M. & Doms, R. W. (2005). N-linked glycosylation of West Nile virus envelope proteins influences particle assembly and infectivity. J Virol 79, 13262-13274.
12. Hunt, A. R., Hall, R. A., Kerst, A. J., Nasci, R. S., Savage, H. M., Panella, N. A., Gottfried, K. L., Burkhalter, K. L. & Roehrig, J. T. (2002). Detection of West Nile virus antigen in mosquitoes and avian tissues by a monoclonal antibody-based capture enzyme immunoassay. J Clin Microbiol 40, 2023-2030.
13. Keelapang, P., Sriburi, R., Supasa, S., Panyadee, N., Songjaeng, A., Jairungsri, A., Puttikhunt, C., Kasinrerk, W., Malasit, P. & Sittisombut, N. (2004). Alterations of pr-M cleavage and virus export in pr-M junction chimeric dengue viruses. J Virol 78, 2367-2381.
14. Khromykh, A. A., Kenney, M. T. & Westaway, E. G. (1998). Trans- Complementation of flavivirus RNA polymerase gene NS5 by using Kunjin virus replicon-expressing BHK cells. J Virol 72, 7270-7279.
15. Kim, J. H., Johannes, L., Goud, B., Antony, C., Lingwood, C. A., Daneman, R. & Grinstein, S. (1998). Noninvasive measurement of the pH of the endoplasmic reticulum at rest and during calcium release. Proc Natl Acad Sci U S A 95, 2997-3002.
16. Konishi, E. & Mason, P. W. (1993). Proper maturation of the Japanese encephalitis virus envelope glycoprotein requires cosynthesis with the premembrane protein. J Virol 67, 1672-1675.
17. Lanciotti, R. S., Ebel, G. D., Deubel, V., Kerst, A. J., Murri, S., Meyer, R., Bowen, M., McKinney, N., Morrill, W. E. & other authors (2002). Complete genome sequences and phylogenetic analysis of West Nile virus strains isolated from the United States, Europe, and the Middle East. Virology 298, 96-105.
18. Li, L., Lok, S. M., Yu, I. M., Zhang, Y., Kuhn, R. J., Chen, J. & Rossmann, M. G. (2008). The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319, 1830-1834.
19. Lin, Y. J. & Wu, S. C. (2005). Histidine at residue 99 and the transmembrane region of the precursor membrane prM protein are important for the prM-E heterodimeric complex formation of Japanese encephalitis virus. J Virol 79, 8535-8544.
20. Lin, Y.-J., Peng, J.-G. & Wu, S.-C. (2010). Characterization of the GXXXG motif in the first transmembrane segment of Japanese encephalitis virus precursor membrane (prM) protein. J Biomed Sci 17, 39.
21. Liu, W. J., Chen, H. B. & Khromykh, A. A. (2003). Molecular and functional analyses of Kunjin virus infectious cDNA clones demonstrate the essential roles for NS2A in virus assembly and for a nonconservative residue in NS3 in RNA replication. J Virol 77, 7804-7813.
22. Lorenz, I. C., Allison, S. L., Heinz, F. X. & Helenius, A. (2002). Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. J Virol 76, 5480-5491.
23. Molloy, S. S., Bresnahan, P. A., Leppla, S. H., Klimpel, K. R. & Thomas, G. (1992). Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J Biol Chem 267, 16396-16402.
24. Molloy, S. S., Anderson, E. D., Jean, F. & Thomas, G. (1999). Bicycling the furin pathway: from TGN localization to pathogen activation and embryogenesis. Trends Cell Biol 9, 28-35.
25. Mukherjee, S., Lin, T. Y., Dowd, K. A., Manhart, C. J. & Pierson, T. C. (2011). The infectivity of prM-containing partially mature West Nile virus does not require the activity of cellular furin-like proteases. J Virol 85, 12067-12072.
26. Prow, N. A., May, F. J., Westlake, D. J., Hurrelbrink, R. J., Biron, R. M., Leung, J. Y., McMinn, P. C., Clark, D. C., Mackenzie, J. S. & other authors (2011). Determinants of attenuation in the envelope protein of the flavivirus Alfuy. J Gen Virol 92, 2286-2296.
27. Pryor, M. J., Azzola, L., Wright, P. J. & Davidson, A. D. (2004). Histidine 39 in the dengue virus type 2 M protein has an important role in virus assembly. J Gen Virol 85, 3627-3636.
28. Reed, L. J. & Muench, H. (1938). A simple method for estimating fifty per cent end points. Am J Hygiene 27, 493-497.
29. Scherret, J. H., Mackenzie, J. S., Khromykh, A. A. & Hall, R. A. (2001a). Biological significance of glycosylation of the envelope protein of Kunjin virus. Ann N Y Acad Sci 951, 361-363.
30. Scherret, J. H., Poidinger, M., Mackenzie, J. S., Broom, A. K., Deubel, V., Lipkin, W. I., Briese, T., Gould, E. A. & Hall, R. A. (2001b). The relationships between West Nile and Kunjin viruses. Emerg Infect Dis 7, 697-705.
31. Setoh, Y. X., Hobson-Peters, J., Prow, N. A., Young, P. R. & Hall, R. A. (2011). Expression of recombinantWest Nile virus prMprotein fused to an affinity tag for use as a diagnostic antigen. J Virol Methods 175, 20-27.
32. Sousa, M. & Parodi, A. J. (1995). The molecular basis for the recognition of misfolded glycoproteins by the UDP-Glc:glycoprotein glucosyltransferase. EMBO J 14, 4196-4203.
33. Stadler, K., Allison, S. L., Schalich, J. & Heinz, F. X. (1997). Proteolytic activation of tick-borne encephalitis virus by furin. J Virol 71, 8475-8481.
34. Tan, T. T., Bhuvanakantham, R., Li, J., Howe, J. & Ng, M. L. (2009). Tyrosine 78 of premembrane protein is essential for assembly of West Nile virus. J Gen Virol 90, 1081-1092.
35. Vey, M., Schäfer, W., Berghöfer, S., Klenk, H. D. & Garten, W. (1994). Maturation of the trans-Golgi network protease furin: compartmentalization of propeptide removal, substrate cleavage, and COOHterminal truncation. J Cell Biol 127, 1829-1842.
36. Voorhees, P., Deignan, E., van Donselaar, E., Humphrey, J., Marks, M. S., Peters, P. J. & Bonifacino, J. S. (1995). An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J 14, 4961-4975.
37. Yoshii, K., Konno, A., Goto, A., Nio, J., Obara, M., Ueki, T., Hayasaka, D., Mizutani, T., Kariwa, H. & Takashima, I. (2004). Single point mutation in tick-borne encephalitis virus prM protein induces a reduction of virus particle secretion. J Gen Virol 85, 3049-3058.
38. Yoshii, K., Igarashi, M., Ichii, O., Yokozawa, K., Ito, K., Kariwa, H. & Takashima, I. (2012). A conserved region in the prM protein is a critical determinant in the assembly of flavivirus particles. J Gen Virol 93, 27-38.