N-linked glycans on dengue viruses grown in mammalian and insect cells

Journal of General Virology

Volumn 90, Issue 9, 2009, Pages 2097-2106

  Hacker, Kari ^a   White, Laura ^a   de Silva, Aravinda M ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EDETIC ACID; ENVELOPE PROTEIN; GLYCAN; INTERCELLULAR ADHESION MOLECULE 3; LECTIN; MANNOSE; PAUCIMANNOSE; PROTEIN DENV; UNCLASSIFIED DRUG; VIRUS PROTEIN; CD209 ANTIGEN; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; DC-SPECIFIC ICAM-3 GRABBING NONINTEGRIN; POLYSACCHARIDE; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; CELL TYPE; CONTROLLED STUDY; DEGLYCOSYLATION; DENDRITIC CELL; DENGUE; DENGUE VIRUS; HUMAN; HUMAN CELL; INSECT CELL; MAMMAL CELL; MONOCYTE; MOSQUITO; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; AEDES; ANIMAL; CELL CULTURE; CELL LINE; GENETICS; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS SHEDDING;

DENGUE VIRUS; DENGUE VIRUS GROUP; HEXAPODA; MAMMALIA;

AEDES; ANIMALS; CELL ADHESION MOLECULES; CELL LINE; CELLS, CULTURED; DENDRITIC CELLS; DENGUE VIRUS; HUMANS; LECTINS, C-TYPE; MONOCYTES; POLYSACCHARIDES; RECEPTORS, CELL SURFACE; VIRAL ENVELOPE PROTEINS; VIRUS SHEDDING;

EID: 70349332794     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.012120-0     Document Type: Article

References (58)

1. Bryant, J. E., Calvert, A. E., Mesesan, K., Crabtree, M. B., Volpe, K. E., Silengo, S., Kinney, R. M., Huang, C. Y., Miller, B. R. & Roehrig, J. T. (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.
2. Cambi, A. & Figdor, C. G. (2003). Dual function of C-type lectin-like receptors in the immune system. Curr Opin Cell Biol 15, 539-546.
3. Cambi, A., Gijzen, K., de Vries, J.M., Torensma, R., Joosten, B., Adema, G. J., Netea, M. G., Kullberg, B. J., Romani, L. & Figdor, C. G. (2003). The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur J Immunol 33, 532-538.
4. Chambers, T. J., McCourt, D. W. & Rice, C. M. (1990a). Production of yellow fever virus proteins in infected cells: identification of discrete polyprotein species and analysis of cleavage kinetics using region-specific polyclonal antisera. Virology 177, 159-174.
5. Chambers, T. J., Hahn, C. S., Galler, R. & Rice, C. M. (1990b). Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 44, 649-688.
6. Chen, Y. C. & Wang, S. Y. (2002). Activation of terminally differentiated human monocytes/macrophages by dengue virus: productive infection, hierarchical production of innate cytokines and chemokines, and the synergistic effect of lipopolysaccharide. J Virol 76, 9877-9887.
7. Crowley, J. F., Goldstein, I. J., Arnarp, J. & Lonngren, J. (1984). Carbohydrate binding studies on the lectin from Datura stramonium seeds. Arch Biochem Biophys 231, 524-533.
8. Davis, N. L., Caley, I. J., Brown, K. W., Betts, M. R., Irlbeck, D. M., McGrath, K. M., Connell, M. J., Montefiori, D. C., Frelinger, J. A. & other authors (2000). Vaccination of macaques against pathogenic simian immunodeficiency virus with Venezuelan equine encephalitis virus replicon particles. J Virol 74, 371-378.
9. Davis, C. W., Mattei, L. M., Nguyen, H. Y., Ansarah-Sobrinho, C., Doms, R. W. & Pierson, T. C. (2006a). The location of asparagine-linked glycans on West Nile virions controls their interactions with CD209 (dendritic cell-specific ICAM-3 grabbing nonintegrin). J Biol Chem 281, 37183-37194.
10. Davis, C. W., Nguyen, H. Y., Hanna, S. L., Sanchez, M. D., Doms, R. W. & Pierson, T. C. (2006b). West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J Virol 80, 1290-1301.
11. Despres, P., Frenkiel, M. P. & Deubel, V. (1993). Differences between cell membrane fusion activities of two dengue type-1 isolates reflect modifications of viral structure. Virology 196, 209-219.
12. Engering, A., Geijtenbeek, T. B., van Vliet, S. J., Wijers, M., van Liempt, E., Demaurex, N., Lanzavecchia, A., Fransen, J., Figdor, C. G. & other authors (2002). The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol 168, 2118-2126.
13. Feinberg, H., Mitchell, D. A., Drickamer, K. & Weis, W. I. (2001). Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294, 2163-2166.
14. Ferlenghi, I., Clarke, M., Ruttan, T., Allison, S. L., Schalich, J., Heinz, F. X., Harrison, S. C., Rey, F. A. & Fuller, S. D. (2001). Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol Cell 7, 593-602.
15. Gramberg, T., Hofmann, H., Moller, P., Lalor, P. F., Marzi, A., Geier, M., Krumbiegel, M., Winkler, T., Kirchhoff, F. & other authors (2005). LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus. Virology 340, 224-236.
16. Gubler, D. J. (2002). Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 10, 100-103.
17. Gubler, D. J. & Clark, G. G. (1995). Dengue/dengue hemorrhagic fever: the emergence of a global health problem. Emerg Infect Dis 1, 55-57.
18. 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.
19. Heinz, F. X. & Allison, S. L. (2003). Flavivirus structure and membrane fusion. Adv Virus Res 59, 63-97.
20. Ho, L. J., Wang, J. J., Shaio, M. F., Kao, C. L., Chang, D. M., Han, S. W. & Lai, J. H. (2001). Infection of human dendritic cells by dengue virus causes cell maturation and cytokine production. J Immunol 166, 1499-1506.
21. Houng, H. S., Chen, R. C.-M., Vaughn, D. W. & Kanesa-thasan, N. (2001). Development of a fluorogenic RT-PCR system for quantitative identification of dengue virus serotypes 1-4 using conserved and serotype-specific 3′ noncoding sequences. J Virol Methods 95, 19-32.
22. Hsieh, P. & Robbins, P. W. (1984). Regulation of asparagine-linked oligosaccharide processing. oligosaccharide processing in Aedes albopictus mosquito cells. J Biol Chem 259, 2375-2382.
23. Hubbard, S. C. (1988). Regulation of glycosylation. the influence of protein structure on N-linked oligosaccharide processing. J Biol Chem 263, 19303-19317.
24. Hubbard, S. C. & Ivatt, R. J. (1981). Synthesis and processing of asparagine-linked oligosaccharides. Annu Rev Biochem 50, 555-583.
25. Jarvis, D. L. (2003). Developing baculovirus-insect cell expression systems for humanized recombinant glycoprotein production. Virology 310, 1-7.
26. Johnson, A. J., Guirakhoo, F. & Roehrig, J. T. (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.
27. Klimstra, W. B., Nangle, E. M., Smith, M. S., Yurochko, A. D. & Ryman, K. D. (2003). DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses. J Virol 77, 12022-12032.
28. Kraus, A. A., Messer, W., Haymore, L. B. & de Silva, A. M. (2007). Comparison of plaque- and flow cytometry-based methods for measuring dengue virus neutralization. J Clin Microbiol 45, 3777-3780.
29. Kuhn, R. J., Zhang, W., Rossmann, M. G., Pletnev, S. V., Corver, J., Lenches, E., Jones, C. T., Mukhopadhyay, S., Chipman, P. R. & other authors (2002). Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108, 717-725.
30. Lambeth, C. R., White, L. J., Johnston, R. E. & de Silva, A. M. (2005). Flow cytometry-based assay for titrating dengue virus. J Clin Microbiol 43, 3267-3272.
31. Leonard, C. K., Spellman, M. W., Riddle, L., Harris, R. J., Thomas, J. N. & Gregory, T. J. (1990). Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J Biol Chem 265, 10373-10382.
32. 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.
33. Lozach, P. Y., Burleigh, L., Staropoli, I., Navarro-Sanchez, E., Harriague, J., Virelizier, J. L., Rey, F. A., Despres, P., Arenzana-Seisdedos, F. & Amara, A. (2005). Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN)-mediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals. J Biol Chem 280, 23698-23708.
34. Maley, F., Trimble, R. B., Tarentino, A. L. & Plummer, T. H., Jr (1989). Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal Biochem 180, 195-204.
35. Marchal, I., Jarvis, D. L., Cacan, R. & Verbert, A. (2001). Glycoproteins from insect cells: sialylated or not? Biol Chem 382, 151-159.
36. Marovich, M., Grouard-Vogel, G., Louder, M., Eller, M., Sun, W., Wu, S. J., Putvatana, R., Murphy, G., Tassaneetrithep, B. & other authors (2001). Human dendritic cells as targets of dengue virus infection. J Investig Dermatol Symp Proc 6, 219-224.
37. Miller, J. L., deWet, B. J., Martinez-Pomares, L., Radcliffe, C. M., Dwek, R. A., Rudd, P. M. & Gordon, S. (2008). The mannose receptor mediates dengue virus infection of macrophages. PLoS Pathog 4, e17.
38. Mitchell, D. A., Fadden, A. J. & Drickamer, K. (2001). A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR. Subunit organization and binding to multivalent ligands. J Biol Chem 276, 28939-28945.
39. Modis, Y., Ogata, S., Clements, D. & Harrison, S. C. (2003). A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc Natl Acad Sci U S A 100, 6986-6991.
40. Modis, Y., Ogata, S., Clements, D. & Harrison, S. C. (2005). Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J Virol 79, 1223-1231.
41. Mondotte, J. A., Lozach, P. Y., Amara, A. & Gamarnik, A. V. (2007). Essential role of dengue virus envelope protein N glycosylation at asparagine-67 during viral propagation. J Virol 81, 7136-7148.
42. Moran, T. P., Collier, M., McKinnon, K. P., Davis, N. L., Johnston, R. E. & Serody, J. S. (2005). A novel viral system for generating antigen-specific T cells. J Immunol 175, 3431-3438.
43. Navarro-Sanchez, E., Altmeyer, R., Amara, A., Schwartz, O., Fieschi, F., Virelizier, J. L., Arenzana-Seisdedos, F. & Despres, P. (2003). Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep 4, 723-728.
44. Palmer, D. R., Sun, P., Celluzzi, C., Bisbing, J., Pang, S., Sun, W., Marovich, M. A. & Burgess, T. (2005). Differential effects of dengue virus on infected and bystander dendritic cells. J Virol 79, 2432-2439.
45. Pfeffer, S. R. & Rothman, J. E. (1987). Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annu Rev Biochem 56, 829-852.
46. Pokidysheva, E., Zhang, Y., Battisti, A. J., Bator-Kelly, C. M., Chipman, P. R., Xiao, C., Gregorio, G. G., Hendrickson, W. A., Kuhn, R. J. & Rossmann, M. G. (2006). Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 124, 485-493.
47. Shabman, R. S., Morrison, T. E., Moore, C., White, L., Suthar, M. S., Hueston, L., Rulli, N., Lidbury, B., Ting, J. P. & other authors (2007). Differential induction of type I interferon responses in myeloid dendritic cells by mosquito and mammalian-cell-derived alpha-viruses. J Virol 81, 237-247.
48. Shabman, R. S., Rogers, K. M. & Heise, M. T. (2008). Ross River virus envelope glycans contribute to type I interferon production in myeloid dendritic cells. J Virol 82, 12374-12383.
49. Shibuya, N., Goldstein, I. J., Van Damme, E. J. & Peumans, W. J. (1988). Binding properties of a mannose-specific lectin from the snowdrop (Galanthus nivalis) bulb. J Biol Chem 263, 728-734.
50. Silva, M. C., Guerrero-Plata, A., Gilfoy, F. D., Garofalo, R. P. & Mason, P. W. (2007). Differential activation of human monocyte-derived and plasmacytoid dendritic cells by West Nile virus generated in different host cells. J Virol 81, 13640-13648.
51. Smith, G. W. & Wright, P. J. (1985). Synthesis of proteins and glycoproteins in dengue type 2 virus-infected Vero and Aedes albopictus cells. J Gen Virol 66, 559-571.
52. Sun, P., Fernandez, S., Marovich, M. A., Palmer, D. R., Celluzzi, C. M., Boonnak, K., Liang, Z., Subramanian, H., Porter, K. R. & other authors (2009). Functional characterization of ex vivo blood myeloid and plasmacytoid dendritic cells after infection with dengue virus. Virology 383, 207-215.
53. Tassaneetrithep, B., Burgess, T. H., Granelli-Piperno, A., Trumpfheller, C., Finke, J., Sun, W., Eller, M. A., Pattanapanyasat, K., Sarasombath, S. & other authors (2003). DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197, 823-829.
54. Vigerust, D. J. & Shepherd, V. L. (2007). Virus glycosylation: role in virulence and immune interactions. Trends Microbiol 15, 211-218.
55. White, L. J., Parsons, M. M., Whitmore, A. C., Williams, B. M., de Silva, A. & Johnston, R. E. (2007). An immunogenic and protective alphavirus replicon particle-based dengue vaccine overcomes maternal antibody interference in weanling mice. J Virol 81, 10329-10339.
56. Whitehead, S. S., Blaney, J. E., Durbin, A. P. & Murphy, B. R. (2007). Prospects for a dengue virus vaccine. Nat Rev Microbiol 5 , 518-528.
57. WHO (2009). Dengue and dengue hemorrhagic fever. Fact sheet no. 117. http://www.who.int/mediacentre/factsheets/fs117/en/
58. Wu, S. J., Grouard-Vogel, G., Sun, W., Mascola, J. R., Brachtel, E., Putvatana, R., Louder, M. K., Filgueira, L., Marovich, M. A. & other authors (2000). Human skin Langerhans cells are targets of dengue virus infection. Nat Med 6, 816-820.