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

Volumn 366, Issue 2, 2007, Pages 415-423

  Bryant, Juliet E ^a   Calvert, Amanda E ^a   Mesesan, Kyeen ^a   Crabtree, Mary B ^a   Volpe, Katharine E ^a   Silengo, Shawn ^a   Kinney, Richard M ^a   Huang, Claire Y H ^a   Miller, Barry R ^a   Roehrig, John T ^a  

^a NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

Dengue virus; E glycosylation; Flavivirus; Mosquitoes

Indexed keywords

AMINO ACID DERIVATIVE; N67 AMINO ACID; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

AEDES AEGYPTI; ANIMAL CELL; ARTICLE; DENGUE VIRUS; DENGUE VIRUS 2; IN VITRO STUDY; INOCULATION; INSECT CELL CULTURE; MAMMAL CELL; MOSQUITO; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; VIROGENESIS; VIRUS MUTANT; VIRUS REPLICATION; VIRUS SURVIVAL;

AEDES; AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; DENGUE VIRUS; GLYCOSYLATION; HUMANS; MUTAGENESIS, SITE-DIRECTED; VIRAL ENVELOPE PROTEINS;

AEDES AEGYPTI; DENGUE VIRUS; DENGUE VIRUS TYPE 2; FLAVIVIRUS; HEXAPODA; MAMMALIA;

EID: 34548605884     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.05.007     Document Type: Article

References (47)

1. Adams S.C., Broom A.K., Sammels L.M., Hartnett A.C., Howard M.J., Coelen R.J., Mackenzie J.S., and Hall R.A. Glycosylation and antigenic variation among Kunjin virus isolates. Virology 206 1 (1995) 49-56
2. Allison S.L., Schalich J., Stiasny K., Mandl C.W., Kunz C., and Heinz F.X. Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH. J. Virol. 69 2 (1995) 695-700
3. 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., and Barrett A.D. Envelope protein glycosylation status influences mouse neuroinvasion phenotype of genetic lineage 1 West Nile virus strains. J. Virol. 79 13 (2005) 8339-8347
4. Butrapet S., Kinney R.M., and Huang C.Y. Determining genetic stabilities of chimeric dengue vaccine candidates based on dengue 2 PDK-53 virus by sequencing and quantitative TaqMAMA. J. Virol. Methods 131 1 (2006) 1-9
5. Crill W.D., and Chang G.J. Localization and characterization of flavivirus envelope glycoprotein cross-reactive epitopes. J. Virol. 78 24 (2004) 13975-13986
6. Crill W.D., and Roehrig J.T. 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 16 (2001) 7769-7773
7. Deubel V., Kinney R.M., and Trent D.W. Nucleotide sequence and deduced amino acid sequence of the structural proteins of dengue type 2 virus, Jamaica genotype. Virology 155 2 (1986) 365-377
8. Gollins S.W., and Porterfield J.S. Flavivirus infection enhancement in macrophages: and electron microscopic study on the effects of antibody on viral fate. J. Gen. Virol. 65 9 (1985) 1261-1271
9. Gubler D.J. Application of serotype-specific monoclonal antibodies for the identification of dengue viruses. In: Yunker C. (Ed). Arboviruses in Arthropod Cells In Vitro (1987), CRC Press, Boca Raton, FL 3-14
10. Guirakhoo F., Heinz F.X., and Kunz C. Epitope model of tick-borne encephalitis virus envelope glycoprotein E: analysis of structural properties, role of carbohydrate side chain, and conformational changes occurring at acidic pH. Virology 169 1 (1989) 90-99
11. Guirakhoo F., Hunt A.R., Lewis J.G., and Roehrig J.T. Selection and partial characterization of dengue 2 virus mutants that induce fusion at elevated pH. Virology 194 1 (1993) 219-223
12. Hanna S.L., Pierson T.C., Sanchez M.D., Ahmed A.A., Murtadha M.M., and Doms R.W. N-linked glycosylation of West Nile virus envelope proteins influences particle assembly and infectivity. J. Virol. 79 21 (2005) 13262-13274
13. Hase T., Summers P.L., and Eckels K.H. Flavivirus entry into cultured mosquito and human peripheral blood monocytes. Arch. Virol. 104 (1989) 129-143
14. Henchal E.A., McCown J.M., Burke D.S., Seguin M.C., and Brandt W.E. Epitopic analysis of antigenic determinants on the surface of dengue-2 virions using monoclonal antibodies. Am. J. Trop. Med. Hyg. 34 1 (1985) 162-169
15. Ishak H., Takegami T., Kamimura K., and Funada H. Comparative sequences of two type 1 dengue virus strains possessing different growth characteristics in vitro. Microbiol. Immunol. 45 4 (2001) 327-331
16. Johnson A.J., Guirakhoo F., and Roehrig J.T. The envelope glycoproteins of dengue 1 and dengue 2 viruses grown in mosquito cells differ in their utilization of potential glycosylation sites. Virology 203 2 (1994) 241-249
17. Kawano H., Rostapshov V., Rosen L., and Lai C.J. Genetic determinants of dengue type 4 virus neurovirulence for mice. J. Virol. 67 11 (1993) 6567-6575
18. Kinney R.M., Butrapet S., Chang G.J., Tsuchiya K.R., Roehrig J.T., Bhamarapravati N., and Gubler D.J. Construction of infectious cDNA clones for dengue 2 virus: strain 16681 and its attenuated vaccine derivative, strain PDK-53. Virology 230 2 (1997) 300-308
19. Kuhn R.J., Zhang W., Rossmann M.G., Pletnev S.V., Corver J., Lenches E., Jones C.T., Mukhopadhyay S., Chipman P.R., Strauss E.G., Baker T.S., and Strauss J.H. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108 5 (2002) 717-725
20. Laemmli U.K. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227 5259 (1970) 680-685
21. Lanciotti R.S., Calisher C.H., Gubler D.J., Chang G.J., and Vorndam A.V. Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J. Clin. Microbiol. 30 3 (1992) 545-551
22. Lee E., Weir R.C., and Dalgarno L. Changes in the dengue virus major envelope protein on passaging and their localization on the three-dimensional structure of the protein. Virology 232 2 (1997) 281-290
23. Mason P.W. Maturation of Japanese encephalitis virus glycoproteins produced by infected mammalian and mosquito cells. Virology 169 2 (1989) 354-364
24. Mason P.W., McAda P.C., Mason T.L., and Fournier M.J. Sequence of the dengue-1 virus genome in the region encoding the three structural proteins and the major nonstructural protein NS1. Virology 161 1 (1987) 262-267
25. Miller B.R., Mitchell C.J., and Ballinger M.E. Replication, tissue tropisms and transmission of yellow fever virus in Aedes albopictus. Trans. R. Soc. Trop. Med. Hyg. 83 2 (1989) 252-255
26. Modis Y., Ogata S., Clements D., and Harrison S.C. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 100 12 (2003) 6986-6991
27. Modis Y., Ogata S., Clements D., and Harrison S.C. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J. Virol. 79 2 (2005) 1223-1231
28. Mukhopadhyay S., Kuhn R.J., and Rossmann M.G. A structural perspective of the flavivirus life cycle. Nat. Rev., Microbiol. 3 1 (2005) 13-22
29. Navarro-Sanchez E., Altmeyer R., Amara A., Schwartz O., Fieschi F., Virelizier J.L., Arenzana-Seisdedos F., and Despres P. 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 7 (2003) 723-728
30. Osatomi K., Fuke I., Tsuru D., Shiba T., Sakaki Y., and Sumiyoshi H. Nucleotide sequence of dengue type 3 virus genomic RNA encoding viral structural proteins. Virus Genes 2 1 (1988) 99-108
31. Pletnev A.G., Bray M., and Lai C.J. Chimeric tick-borne encephalitis and dengue type 4 viruses: effects of mutations on neurovirulence in mice. J. Virol. 67 8 (1993) 4956-4963
32. 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., and Rossmann M.G. Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 124 3 (2006) 485-493
33. Rey F.A., Heinz F.X., Mandl C., Kunz C., and Harrison S.C. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375 6529 (1995) 291-298
34. Roehrig J.T., Bolin R.A., and Kelly R.G. Monoclonal antibody mapping of the envelope glycoprotein of the dengue 2 virus, Jamaica. Virology 246 2 (1998) 317-328
35. Scherret J.H., Mackenzie J.S., Khromykh A.A., and Hall R.A. Biological significance of glycosylation of the envelope protein of Kunjin virus. Ann. N. Y. Acad. Sci. 951 (2001) 361-363
36. Shirato K., Miyoshi H., Goto A., Ako Y., Ueki T., Kariwa H., and Takashima I. Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus. J. Gen. Virol. 85 Pt 12 (2004) 3637-3645
37. Stiasny K., Allison S.L., Marchler-Bauer A., Kunz C., and Heinz F.X. Structural requirements for low-pH-induced rearrangements in the envelope glycoprotein of tick-borne encephalitis virus. J. Virol. 70 11 (1996) 8142-8147
38. Tassaneetrithep B., Burgess T.H., Granelli-Piperno A., Trumpfheller C., Finke J., Sun W., Eller M.A., Pattanapanyasat K., Sarasombath S., Birx D.L., Steinman R.M., Schlesinger S., and Marovich M.A. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197 7 (2003) 823-829
39. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76 9 (1979) 4350-4354
40. Vorndam V., Mathews J.H., Barrett A.D., Roehrig J.T., and Trent D.W. Molecular and biological characterization of a non-glycosylated isolate of St. Louis encephalitis virus. J. Gen. Virol. 74 Pt 12 (1993) 2653-2660
41. Wengler G., Castle E., Leidner U., Nowak T., and Wengler G. Sequence analysis of the membrane protein V3 of the flavivirus West Nile virus and of its gene. Virology 147 2 (1985) 264-274
42. WHO, 2007. http://www.who.int/csr/disease/dengue/impact/en/.
43. Winkler G., Heinz F.X., and Kunz C. Studies on the glycosylation of flavivirus E proteins and the role of carbohydrate in antigenic structure. Virology 159 2 (1987) 237-243
44. Wright P.J. Envelope protein of the flavivirus Kunjin is apparently not glycosylated. J. Gen. Virol. 59 Pt 1 (1982) 29-38
45. Wu S.J., Grouard-Vogel G., Sun W., Mascola J.R., Brachtel E., Putvatana R., Louder M.K., Filgueira L., Marovich M.A., Wong H.K., Blauvelt A., Murphy G.S., Robb M.L., Innes B.L., Birx D.L., Hayes C.G., and Frankel S.S. Human skin Langerhans cells are targets of dengue virus infection. Nat. Med. 6 7 (2000) 816-820
46. Zhang Y., Corver J., Chipman P.R., Zhang W., Pletnev S.V., Sedlak D., Baker T.S., Strauss J.H., Kuhn R.J., and Rossmann M.G. Structures of immature flavivirus particles. EMBO J. 22 11 (2003) 2604-2613
47. Zhao B., Mackow E., Buckler-White A., Markoff L., Chanock R.M., Lai C.J., and Makino Y. Cloning full-length dengue type 4 viral DNA sequences: analysis of genes coding for structural proteins. Virology 155 1 (1986) 77-88