Both E protein glycans adversely affect dengue virus infectivity but are beneficial for virion release

Journal of Virology

Volumn 84, Issue 10, 2010, Pages 5171-5180

  Lee, Eva ^a   Leang, Sook Kwan ^a   Davidson, Andrew ^b   Lobigs, Mario ^a  

^a Australian National University   (Australia)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; E PROTEIN; GLYCAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENGUE; DENGUE VIRUS; GLYCOSYLATION; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; SEROTYPE; VIRION; VIROGENESIS; VIRUS INFECTIVITY; VIRUS MORPHOGENESIS;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CRICETINAE; CULICIDAE; DENGUE VIRUS; MUTATION, MISSENSE; SUPPRESSION, GENETIC; VIRAL ENVELOPE PROTEINS; VIRULENCE; VIRULENCE FACTORS; VIRUS RELEASE;

DENGUE VIRUS; MAMMALIA;

EID: 77951429019     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01900-09     Document Type: Article

References (45)

1. Adams, S. C., A. K. Broom, L. M. Sammels, A. C. Hartnett, M. J. Howard, R. J. Coelen, J. S. Mackenzie, and R. A. Hall. 1995. Glycosylation and antigenic variation among Kunjin virus isolates. Virology 206:49-56.
2. Beasley, D. W., C. T. Davis, J. Estrada-Franco, R. Navarro-Lopez, A. Campomanes-Cortes, R. B. Tesh, S. C. Weaver, and A. D. Barrett. 2004. Genome sequence and attenuating mutations in West Nile virus isolate from Mexico. Emerg. Infect. Dis. 10:2221-2224.
3. 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.
4. Berthet, F. X., H. G. Zeller, M. T. Drouet, J. Rauzier, J. P. Digoutte, and V. Deubel. 1997. Extensive nucleotide changes and deletions within the envelope glycoprotein gene of Euro-African West Nile viruses. J. Gen. Virol. 78:2293-2297.
5. Bryant, J. E., A. E. Calvert, K. Mesesan, M. B. Crabtree, K. E. Volpe, S. Silengo, R. M. Kinney, C. Y. Huang, B. R. Miller, and J. T. Roehrig. 2007. Glycosylation of the dengue 2 virus E protein at N67 is critical for virus growth in vitro but not for growth in intrathoracically inoculated Aedes aegypti mosquitoes. Virology 366:415-423.
6. Clark, D. C., M. Lobigs, E. Lee, M. J. Howard, K. Clark, B. J. Blitvich, and R. A. Hall. 2007. In situ reactions of monoclonal antibodies with a viable mutant of Murray Valley encephalitis virus reveal an absence of dimeric NS1 protein. J. Gen. Virol. 88:1175-1183.
7. Dalgarno, L., D. W. Trent, J. H. Strauss, and C. M. Rice. 1986. Partial nucleotide sequence of the Murray Valley encephalitis virus genome. J. Mol. Biol. 187:309-323.
8. Goto, A., K. Yoshii, M. Obara, T. Ueki, T. Mizutani, H. Kariwa, and I. Takashima. 2005. Role of the N-linked glycans of the prM and E envelope proteins in tick-borne encephalitis virus particle secretion. Vaccine 23:3043-3052. (Pubitemid 40462444)
9. Gruenberg, A., W. S. Woo, A. Biedrzycka, and P. J. Wright. 1988. Partial nucleotide sequence and deduced amino acid sequence of the structural proteins of dengue virus type 2, New Guinea C and PUO-218 strains. J. Gen. Virol. 69:1391-1398.
10. Gualano, R. C., M. J. Pryor, M. R. Cauchi, P. J. Wright, and A. D. Davidson. 1998. Identification of a major determinant of mouse neurovirulence of dengue virus type 2 using stably cloned genomic-length cDNA. J. Gen. Virol. 79:437-446.
11. 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)
12. Hanna, S. L., T. C. Pierson, M. D. Sanchez, A. A. Ahmed, M. M. Murtadha, and R. W. Doms. 2005. N-linked glycosylation of West Nile virus envelope proteins influences particle assembly and infectivity. J. Virol. 79:13262-13274. (Pubitemid 41508141)
13. Hase, T., P. L. Summers, and W. H. Cohen. 1989. A comparative study of entry modes into C6/36 cells by Semliki Forest and Japanese encephalitis viruses. Arch. Virol. 108:101-114.
14. Hase, T., P. L. Summers, and K. H. Eckels. 1989. Flavivirus entry into cultured mosquito cells and human peripheral blood monocytes. Arch. Virol. 104:129-143.
15. Johnson, A. J., F. Guirakhoo, and J. T. Roehrig. 1994. The envelope glycoproteins of dengue 1 and dengue 2 viruses grown in mosquito cells differ in their utilization of potential glycosylation sites. Virology 203:241-249.
16. Kawano, H., V. Rostapshov, L. Rosen, and C. J. Lai. 1993. Genetic determinants of dengue type 4 virus neurovirulence for mice. J. Virol. 67:6567-6575. (Pubitemid 23309123)
17. Kim, J. M., S. I. Yun, B. H. Song, Y. S. Hahn, C. H. Lee, H. W. Oh, and Y. M. Lee. 2008. A single N-linked glycosylation site in the Japanese encephalitis virus prM protein is critical for cell type-specific prM protein biogenesis, virus particle release, and pathogenicity in mice. J. Virol. 82:7846-7862.
18. 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.
19. 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.
20. Lee, E., and M. Lobigs. 2008. E protein domain III determinants of yellow fever virus 17D vaccine strain enhance binding to glycosaminoglycans, impede virus spread, and attenuate virulence. J. Virol. 82:6024-6033. (Pubitemid 351822276)
21. Lee, E., and M. Lobigs. 2000. Substitutions at the putative receptor-binding site of an encephalitic flavivirus alter virulence and host cell tropism and reveal a role for glycosaminoglycans in entry. J. Virol. 74:8867-8875.
22. Lee, E., M. Pavy, N. Young, C. Freeman, and M. Lobigs. 2006. Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses. Antiviral Res. 69:31-38. (Pubitemid 41790479)
23. Lee, E., R. C. Weir, and L. Dalgarno. 1997. Changes in the dengue virus major envelope protein on passaging and their localization on the three-dimensional structure of the protein. Virology 232:281-290. (Pubitemid 27293571)
24. Lee, E., P. J. Wright, A. Davidson, and M. Lobigs. 2006. Virulence attenuation of Dengue virus due to augmented glycosaminoglycan-binding affinity and restriction in extraneural dissemination. J. Gen. Virol. 87:2791-2801.
25. Lewis, J. A., G. J. Chang, R. S. Lanciotti, R. M. Kinney, L. W. Mayer, and D. W. Trent. 1993. Phylogenetic relationships of dengue-2 viruses. Virology 197:216-224.
26. Li, J., R. Bhuvanakantham, J. Howe, and M. L. Ng. 2006. The glycosylation site in the envelope protein of West Nile virus (Sarafend) plays an important role in replication and maturation processes. J. Gen. Virol. 87:613-622.
27. Licon Luna, R. M., E. Lee, A. Müllbacher, R. V. Blanden, R. Langman, and M. Lobigs. 2002. Lack of both Fas ligand and perforin protects from flavivirus-mediated encephalitis in mice. J. Virol. 76:3202-3211.
28. Lim, H. Y., and M. L. Ng. 1999. A different mode of entry by dengue-2 neutralisation escape mutant virus. Arch. Virol. 144:989-995.
29. Liu, W. J., H. B. Chen, and A. A. Khromykh. 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.
30. Lobigs, M., I. D. Marshall, R. C. Weir, and L. Dalgarno. 1988. Murray Valley encephalitis virus field strains from Australia and Papua New Guinea: studies on the sequence of the major envelope protein gene and virulence for mice. Virology 165:245-255.
31. Marsh, M., and R. Bron. 1997. SFV infection in CHO cells: cell-type specific restrictions to productive virus entry at the cell surface. J. Cell Sci. 110:95-103. (Pubitemid 27057948)
32. May, F. J., M. Lobigs, E. Lee, D. J. Gendle, J. S. Mackenzie, A. K. Broom, J. V. Conlan, and R. A. Hall. 2006. Biological, antigenic and phylogenetic characterization of the flavivirus Alfuy. J. Gen. Virol. 87:329-337.
33. 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. U. S. A. 100:6986-6991.
34. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2005. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J. Virol. 79:1223-1231. (Pubitemid 40053904)
35. Mondotte, J. A., P. Y. Lozach, A. Amara, and A. V. Gamarnik. 2007. Essential role of dengue virus envelope protein N glycosylation at asparagine-67 during viral propagation. J. Virol. 81:7136-7148.
36. Pokidysheva, E., Y. Zhang, A. J. Battisti, C. M. Bator-Kelly, P. R. Chipman, C. Xiao, G. G. Gregorio, W. A. Hendrickson, R. J. Kuhn, and M. G. Rossmann. 2006. Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 124:485-493. (Pubitemid 43199435)
37. Post, P. R., C. N. Santos, R. Carvalho, A. C. Cruz, C. M. Rice, and R. Galler. 1992. Heterogeneity in envelope protein sequence and N-linked glycosylation among yellow fever virus vaccine strains. Virology 188:160-167.
38. Rey, F. A., F. X. Heinz, C. Mandl, C. Kunz, and S. C. Harrison. 1995. The envelope glycoprotein from tick-borne encephalitis virus at 2Å resolution. Nature 375:291-298.
39. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a labotatory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Scherret, J. H., J. S. Mackenzie, A. A. Khromykh, and R. A. Hall. 2001. Biological significance of glycosylation of the envelope protein of Kunjin virus. Ann. N. Y. Acad. Sci. 951:361-363.
41. Scherret, J. H., M. Poidinger, J. S. Mackenzie, A. K. Broom, V. Deubel, W. I. Lipkin, T. Briese, E. A. Gould, and R. A. Hall. 2001. The relationships between West Nile and Kunjin viruses. Emerg. Infect. Dis. 7:697-705.
42. Shirato, K., H. Miyoshi, A. Goto, Y. Ako, T. Ueki, H. Kariwa, and I. Takashima. 2004. Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus. J. Gen. Virol. 85:3637-3645.
43. Stocks, C. E., and M. Lobigs. 1998. Signal peptidase cleavage at the flavivirus C-prM junction: dependence on the viral NS2B-3 protease for efficient processing requires determinants in C, the signal peptide, and prM. J. Virol. 72:2141-2149.
44. Vorndam, V., J. H. Mathews, A. D. Barrett, J. T. Roehrig, and D. W. Trent. 1993. Molecular and biological characterization of a non-glycosylated isolate of St Louis encephalitis virus. J. Gen. Virol. 74:2653-2660.
45. Wu, S. J., G. Grouard-Vogel, W. Sun, J. R. Mascola, E. Brachtel, R. Putvatana, M. K. Louder, L. Filgueira, M. A. Marovich, H. K. Wong, A. Blauvelt, G. S. Murphy, M. L. Robb, B. L. Innes, D. L. Birx, C. G. Hayes, and S. S. Frankel. 2000. Human skin Langerhans cells are targets of dengue virus infection. Nat. Med. 6:816-820.