N-linked glycosylation of dengue virus NS1 protein modulates secretion, cell-surface expression, hexamer stability, and interactions with human complement

Virology

Volumn 413, Issue 2, 2011, Pages 253-264

  Somnuke, Pawit ^a,b   Hauhart, Richard E ^a   Atkinson, John P ^a   Diamond, Michael S ^a   Avirutnan, Panisadee ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Complement; Dengue virus; Flavivirus; N linked glycosylation; Non structural protein nS1

Indexed keywords

COMPLEMENT; GLYCAN; NONSTRUCTURAL PROTEIN 1;

ARTICLE; CELL STRAIN BHK; CELL SURFACE; CONTROLLED STUDY; DENGUE VIRUS; GLYCOSYLATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY;

COMPLEMENT SYSTEM PROTEINS; DENGUE VIRUS; GENE EXPRESSION REGULATION, VIRAL; GLYCOSYLATION; HUMANS; MUTATION; POLYSACCHARIDES; SINDBIS VIRUS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS SHEDDING;

DENGUE VIRUS; FLAVIVIRUS;

EID: 79954633991     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.02.022     Document Type: Article

References (54)

1. Alcon S., Talarmin A., Debruyne M., Falconar A., Deubel V., Flamand M. Enzyme-linked immunosorbent assay specific to dengue virus type 1 nonstructural protein NS1 reveals circulation of the antigen in the blood during the acute phase of disease in patients experiencing primary or secondary infections. J. Clin. Microbiol. 2002, 40(2):376-381.
2. Alcon-LePoder S., Drouet M.T., Roux P., Frenkiel M.P., Arborio M., Durand-Schneider A.M., Maurice M., Le Blanc I., Gruenberg J., Flamand M. The secreted form of dengue virus nonstructural protein NS1 is endocytosed by hepatocytes and accumulates in late endosomes: implications for viral infectivity. J. Virol. 2005, 79(17):11403-11411.
3. Avirutnan P., Punyadee N., Noisakran S., Komoltri C., Thiemmeca S., Auethavornanan K., Jairungsri A., Kanlaya R., Tangthawornchaikul N., Puttikhunt C., Pattanakitsakul S.N., Yenchitsomanus P.T., Mongkolsapaya J., Kasinrerk W., Sittisombut N., Husmann M., Blettner M., Vasanawathana S., Bhakdi S., Malasit P. Vascular leakage in severe dengue virus infections: a potential role for the nonstructural viral protein NS1 and complement. J. Infect. Dis. 2006, 193(8):1078-1088.
4. Avirutnan P., Zhang L., Punyadee N., Manuyakorn A., Puttikhunt C., Kasinrerk W., Malasit P., Atkinson J.P., Diamond M.S. Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E. PLoS Pathog. 2007, 3(11):e183.
5. Avirutnan P., Fuchs A., Hauhart R.E., Somnuke P., Youn S., Diamond M.S., Atkinson J.P. Antagonism of the complement component C4 by flavivirus nonstructural protein NS1. J. Exp. Med. 2010, 207(4):793-806.
6. Baeuerle P.A., Huttner W.B. Chlorate-a potent inhibitor of protein sulfation in intact cells. Biochem. Biophys. Res. Commun. 1986, 141(2):870-877.
7. Chambers T.J., Hahn C.S., Galler R., Rice C.M. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 1990, 44:649-688.
8. Chang H.H., Shyu H.F., Wang Y.M., Sun D.S., Shyu R.H., Tang S.S., Huang Y.S. Facilitation of cell adhesion by immobilized dengue viral nonstructural protein 1 (NS1): arginine-glycine-aspartic acid structural mimicry within the dengue viral NS1 antigen. J. Infect. Dis. 2002, 186(6):743-751.
9. Chung K.M., Liszewski M.K., Nybakken G., Davis A.E., Townsend R.R., Fremont D.H., Atkinson J.P., Diamond M.S. West Nile virus nonstructural protein NS1 inhibits complement activation by binding the regulatory protein factor H. Proc. Natl Acad. Sci. USA 2006, 103(50):19111-19116.
10. Chung K.M., Nybakken G.E., Thompson B.S., Engle M.J., Marri A., Fremont D.H., Diamond M.S. Antibodies against West Nile Virus nonstructural protein NS1 prevent lethal infection through Fc gamma receptor-dependent and -independent mechanisms. J. Virol. 2006, 80(3):1340-1351.
11. Clyde K., Kyle J.L., Harris E. Recent advances in deciphering viral and host determinants of dengue virus replication and pathogenesis. J. Virol. 2006, 80(23):11418-11431.
12. Crabtree M.B., Kinney R.M., Miller B.R. Deglycosylation of the NS1 protein of dengue 2 virus, strain 16681: construction and characterization of mutant viruses. Arch. Virol. 2005, 150(4):771-786.
13. Despres P., Girard M., Bouloy M. Characterization of yellow fever virus proteins E and NS1 expressed in Vero and Spodoptera frugiperda cells. J. Gen. Virol. 1991, 72(Pt 6):1331-1342.
14. Doms R.W., Lamb R.A., Rose J.K., Helenius A. Folding and assembly of viral membrane proteins. Virology 1993, 193(2):545-562.
15. Falgout B., Markoff L. Evidence that flavivirus NS1-NS2A cleavage is mediated by a membrane-bound host protease in the endoplasmic reticulum. J. Virol. 1995, 69(11):7232-7243.
16. Flamand M., Megret F., Mathieu M., Lepault J., Rey F.A., Deubel V. Dengue virus type 1 nonstructural glycoprotein NS1 is secreted from mammalian cells as a soluble hexamer in a glycosylation-dependent fashion. J. Virol. 1999, 73(7):6104-6110.
17. Fuchs A., Lin T.Y., Beasley D.W., Stover C.M., Schwaeble W.J., Pierson T.C., Diamond M.S. Direct complement restriction of flavivirus infection requires glycan recognition by mannose-binding lectin. Cell Host Microbe 2010, 8(2):186-195.
18. Gubler D.J. Dengue and dengue hemorrhagic fever. Clin. Microbiol. Rev. 1998, 11(3):480-496.
19. Halstead S.B. Pathogenesis of dengue: challenges to molecular biology. Science 1988, 239(4839):476-481.
20. Halstead S.B. Dengue. Lancet 2007, 370(9599):1644-1652.
21. Hershkovitz O., Jarahian M., Zilka A., Bar-Ilan A., Landau G., Jivov S., Tekoah Y., Glicklis R., Gallagher J.T., Hoffmann S.C., Zer H., Mandelboim O., Watzl C., Momburg F., Porgador A. Altered glycosylation of recombinant NKp30 hampers binding to heparan sulfate: a lesson for the use of recombinant immunoreceptors as an immunological tool. Glycobiology 2008, 18(1):28-41.
22. Ito K., Ishimaru T., Kimura F., Matsudomi N. Importance of N-glycosylation positioning for secretion and folding of ovalbumin. Biochem. Biophys. Res. Commun. 2007, 361(3):725-731.
23. Ito K., Seri A., Kimura F., Matsudomi N. Site-specific glycosylation at Asn-292 in ovalbumin is essential to efficient secretion in yeast. J. Biochem. 2007, 141(2):193-199.
24. Jacobs M.G., Robinson P.J., Bletchly C., Mackenzie J.M., Young P.R. Dengue virus nonstructural protein 1 is expressed in a glycosyl-phosphatidylinositol-linked form that is capable of signal transduction. FASEB J. 2000, 14(11):1603-1610.
25. Kayser V., Chennamsetty N., Voynov V., Forrer K., Helk B., Trout B.L. Glycosylation influences on the aggregation propensity of therapeutic monoclonal antibodies. Biotechnol. J. 2011, 6:38-44.
26. Khromykh A.A., Sedlak P.L., Guyatt K.J., Hall R.A., Westaway E.G. Efficient trans-complementation of the flavivirus kunjin NS5 protein but not of the NS1 protein requires its coexpression with other components of the viral replicase. J. Virol. 1999, 73(12):10272-10280.
27. Kurosu T., Chaichana P., Yamate M., Anantapreecha S., Ikuta K. Secreted complement regulatory protein clusterin interacts with dengue virus nonstructural protein 1. Biochem. Biophys. Res. Commun. 2007, 362(4):1051-1056.
28. Libraty D.H., Young P.R., Pickering D., Endy T.P., Kalayanarooj S., Green S., Vaughn D.W., Nisalak A., Ennis F.A., Rothman A.L. High circulating levels of the dengue virus nonstructural protein NS1 early in dengue illness correlate with the development of dengue hemorrhagic fever. J. Infect. Dis. 2002, 186(8):1165-1168.
29. Lin C.F., Lei H.Y., Shiau A.L., Liu C.C., Liu H.S., Yeh T.M., Chen S.H., Lin Y.S. Antibodies from dengue patient sera cross-react with endothelial cells and induce damage. J. Med. Virol. 2003, 69(1):82-90.
30. Lindenbach B.D., Rice C.M. trans-Complementation of yellow fever virus NS1 reveals a role in early RNA replication. J. Virol. 1997, 71(12):9608-9617.
31. Mackenzie J.M., Jones M.K., Young P.R. Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. Virology 1996, 220(1):232-240.
32. Maley F., Trimble R.B., Tarentino A.L., Plummer T.H. Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal. Biochem. 1989, 180(2):195-204.
33. Malvoisin E., Wild F. The role of N-glycosylation in cell fusion induced by a vaccinia recombinant virus expressing both measles virus glycoproteins. Virology 1994, 200(1):11-20.
34. Muylaert I.R., Chambers T.J., Galler R., Rice C.M. Mutagenesis of the N-linked glycosylation sites of the yellow fever virus NS1 protein: effects on virus replication and mouse neurovirulence. Virology 1996, 222(1):159-168.
35. Ng D.T., Hiebert S.W., Lamb R.A. Different roles of individual N-linked oligosaccharide chains in folding, assembly, and transport of the simian virus 5 hemagglutinin-neuraminidase. Mol. Cell. Biol. 1990, 10(5):1989-2001.
36. Noisakran S., Dechtawewat T., Avirutnan P., Kinoshita T., Siripanyaphinyo U., Puttikhunt C., Kasinrerk W., Malasit P., Sittisombut N. Association of dengue virus NS1 protein with lipid rafts. J. Gen. Virol. 2008, 89(Pt 10):2492-2500.
37. Pletnev A.G., Bray M., Lai C.J. Chimeric tick-borne encephalitis and dengue type 4 viruses: effects of mutations on neurovirulence in mice. J. Virol. 1993, 67(8):4956-4963.
38. Post P.R., Carvalho R., Galler R. Glycosylation and secretion of yellow fever virus nonstructural protein NS1. Virus Res. 1991, 18(2-3):291-302.
39. Pryor M.J., Wright P.J. Glycosylation mutants of dengue virus NS1 protein. J. Gen. Virol. 1994, 75(Pt 5):1183-1187.
40. Pryor M.J., Gualano R.C., Lin B., Davidson A.D., Wright P.J. Growth restriction of dengue virus type 2 by site-specific mutagenesis of virus-encoded glycoproteins. J. Gen. Virol. 1998, 79(Pt 11):2631-2639.
41. Puttikhunt C., Kasinrerk W., Srisa-ad S., Duangchinda T., Silakate W., Moonsom S., Sittisombut N., Malasit P. Production of anti-dengue NS1 monoclonal antibodies by DNA immunization. J. Virol. Meth. 2003, 109(1):55-61.
42. Rademacher T.W., Parekh R.B., Dwek R.A. Glycobiology. Annu. Rev. Biochem. 1988, 57:785-838.
43. Ryman K.D., Gardner C.L., Burke C.W., Meier K.C., Thompson J.M., Klimstra W.B. Heparan sulfate binding can contribute to the neurovirulence of neuroadapted and nonneuroadapted Sindbis viruses. J. Virol. 2007, 81(7):3563-3573.
44. Sun D.S., King C.C., Huang H.S., Shih Y.L., Lee C.C., Tsai W.J., Yu C.C., Chang H.H. Antiplatelet autoantibodies elicited by dengue virus non-structural protein 1 cause thrombocytopenia and mortality in mice. J. Thromb. Haemost. 2007, 5(11):2291-2299.
45. Tajima S., Takasaki T., Kurane I. Characterization of Asn130-to-Ala mutant of dengue type 1 virus NS1 protein. Virus Genes 2008, 36(2):323-329.
46. Tarentino A.L., Maley F. Purification and properties of an endo-beta-N-acetylglucosaminidase from Streptomyces griseus. J. Biol. Chem. 1974, 249(3):811-817.
47. Tarentino A.L., Gomez C.M., Plummer T.H. Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase F. Biochemistry 1985, 24(17):4665-4671.
48. Trombetta E.S., Helenius A. Lectins as chaperones in glycoprotein folding. Curr. Opin. Struct. Biol. 1998, 8(5):587-592.
49. Whiteman M.C., Li L., Wicker J.A., Kinney R.M., Huang C., Beasley D.W., Chung K.M., Diamond M.S., Solomon T., Barrett A.D. Development and characterization of non-glycosylated E and NS1 mutant viruses as a potential candidate vaccine for West Nile virus. Vaccine 2010, 28(4):1075-1083.
50. Winkler G., Randolph V.B., Cleaves G.R., Ryan T.E., Stollar V. Evidence that the mature form of the flavivirus nonstructural protein NS1 is a dimer. Virology 1988, 162(1):187-196.
51. Winkler G., Maxwell S.E., Ruemmler C., Stollar V. Newly synthesized dengue-2 virus nonstructural protein NS1 is a soluble protein but becomes partially hydrophobic and membrane-associated after dimerization. Virology 1989, 171(1):302-305.
52. Youn S., Cho H., Fremont D.H., Diamond M.S. A short N-terminal peptide motif on flavivirus nonstructural protein NS1 modulates cellular targeting and immune recognition. J. Virol. 2010, 84(18):9516-9532.
53. Young P.R., Hilditch P.A., Bletchly C., Halloran W. An antigen capture enzyme-linked immunosorbent assay reveals high levels of the dengue virus protein NS1 in the sera of infected patients. J. Clin. Microbiol. 2000, 38(3):1053-1057.
54. Zhou W., Tsai H.M. N-Glycans of ADAMTS13 modulate its secretion and von Willebrand factor cleaving activity. Blood 2009, 113(4):929-935.