1887

Abstract

The envelope fusion (F) protein of baculoviruses is a heavily -glycosylated protein that plays a significant role in the virus infection cycle. -Linked glycosylation of virus envelope glycoprotein is important for virus envelope glycoprotein folding and its function in general. There are six predicted -glycosylation sites in the F (HaF) protein of nucleopolyhedrovirus (HearNPV). The -glycosylation site located in the F subunit (N104) of HaF has been identified and functionally characterized previously (Long ., 2007). In this study, the other five potential -glycosylation sites located in the HaF subunit, namely, N293, N361, N526, N571 and N595, were analysed extensively to examine their -glycosylation and relative importance to the function of HaF. The results showed that four of these five potential glycosylation sites in the F subunit, N293, N361, N526 and N571, were -glycosylated in F proteins of mature HearNPV budded viruses (BVs) but that N595 was not. In general, the conserved site N526 was critical to the functioning of HaF, as absence of -glycosylation of N526 reduced the efficiency of HaF folding and trafficking, consequently decreased fusogenicity and modified the subcellular localization of HaF proteins, and thus impaired virus production and infectivity. The absence of -glycosylation at other individual sites was found to have different effects on the fusogenicity and subcelluar distribution of HaF proteins in HzAM1 cells. In summary, -glycosylation plays comprehensive roles in HaF function and virus infectivity, which is further discussed.

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2016-04-01
2019-10-14
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References

  1. Abe Y. , Takashita E. , Sugawara K. , Matsuzaki Y. , Muraki Y. , Hongo S. . ( 2004;). Effect of the addition of oligosaccharides on the biological activities and antigenicity of influenza A/H3N2 virus hemagglutinin. J Virol 78: 9605–9611 [CrossRef] [PubMed].
    [Google Scholar]
  2. Aguilar H. C. , Matreyek K. A. , Filone C. M. , Hashimi S. T. , Levroney E. L. , Negrete O. A. , Bertolotti-Ciarlet A. , Choi D. Y. , McHardy I. , other authors . ( 2006;). N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J Virol 80: 4878–4889 [CrossRef] [PubMed].
    [Google Scholar]
  3. Arnold K. , Bordoli L. , Kopp J. , Schwede T. . ( 2006;). The swiss-model workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195–201 [CrossRef] [PubMed].
    [Google Scholar]
  4. Blissard G. W. , Wenz J. R. . ( 1992;). Baculovirus gp64 envelope glycoprotein is sufficient to mediate pH-dependent membrane fusion. J Virol 66: 6829–6835 [PubMed].
    [Google Scholar]
  5. Bone R. C. , Balk R. , Slotman G. , Maunder R. , Silverman H. , Hyers T. M. , Kerstein M. D. . ( 1992;). Adult respiratory distress syndrome. Sequence and importance of development of multiple organ failure. The Prostaglandin E1 Study Group. Chest 101: 320–326 [CrossRef] [PubMed].
    [Google Scholar]
  6. Braakman I. , Hebert D. N. . ( 2001;). Analysis of disulfide bond formation. Curr Protoc Protein Sci 3: 1411–14115.
    [Google Scholar]
  7. Braakman I. , Hoover-Litty H. , Wagner K. R. , Helenius A. . ( 1991;). Folding of influenza hemagglutinin in the endoplasmic reticulum. J Cell Biol 114: 401–411 [CrossRef] [PubMed].
    [Google Scholar]
  8. Burda P. , Aebi M. . ( 1999;). The dolichol pathway of N-linked glycosylation. Biochim Biophys Acta 1426: 239–257 [CrossRef] [PubMed].
    [Google Scholar]
  9. Chen L. , Gorman J. J. , McKimm-Breschkin J. , Lawrence L. J. , Tulloch P. A. , Smith B. J. , Colman P. M. , Lawrence M. C. . ( 2001;). The structure of the fusion glycoprotein of Newcastle disease virus suggests a novel paradigm for the molecular mechanism of membrane fusion. Structure 9: 255–266 [CrossRef] [PubMed].
    [Google Scholar]
  10. Cui J. , Smith T. , Robbins P. W. , Samuelson J. . ( 2009;). Darwinian selection for sites of Asn-linked glycosylation in phylogenetically disparate eukaryotes and viruses. Proc Natl Acad Sci U S A 106: 13421–13426 [CrossRef] [PubMed].
    [Google Scholar]
  11. Danielsson R. , Bååth M. , Kölbeck K. G. , Klominek J. , Svensson L. . ( 2003;). Accumulation of Tc-99m depreotide (NeoSpect) in axillary sweat glands. Clin Nucl Med 28: 789–790 [CrossRef] [PubMed].
    [Google Scholar]
  12. Deng F. , Wang R. , Fang M. , Jiang Y. , Xu X. , Wang H. , Chen X. , Arif B. M. , Guo L. , other authors . ( 2007;). Proteomics analysis of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus identified two new occlusion-derived virus-associated proteins, HA44 and HA100. J Virol 81: 9377–9385 [CrossRef] [PubMed].
    [Google Scholar]
  13. Gagneux P. , Varki A. . ( 1999;). Evolutionary considerations in relating oligosaccharide diversity to biological function. Glycobiology 9: 747–755 [CrossRef] [PubMed].
    [Google Scholar]
  14. Garry C. E. , Garry R. F. . ( 2008;). Proteomics computational analyses suggest that baculovirus GP64 superfamily proteins are class III penetrenes. Virol J 5: 28 [CrossRef] [PubMed].
    [Google Scholar]
  15. Helenius A. . ( 1994;). How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum. Mol Biol Cell 5: 253–265 [CrossRef] [PubMed].
    [Google Scholar]
  16. Hewson R. , Gmyl A. , Gmyl L. , Smirnova S. E. , Karganova G. , Jamil B. , Hasan R. , Chamberlain J. , Clegg C. . ( 2004;). Evidence of segment reassortment in Crimean-Congo haemorrhagic fever virus. J Gen Virol 85: 3059–3070 [CrossRef] [PubMed].
    [Google Scholar]
  17. Ho S. N. , Hunt H. D. , Horton R. M. , Pullen J. K. , Pease L. R. . ( 1989;). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51–59 [CrossRef] [PubMed].
    [Google Scholar]
  18. Hou D. , Zhang L. , Deng F. , Fang W. , Wang R. , Liu X. , Guo L. , Rayner S. , Chen X. , other authors . ( 2013;). Comparative proteomics reveal fundamental structural and functional differences between the two progeny phenotypes of a baculovirus. J Virol 87: 829–839 [CrossRef] [PubMed].
    [Google Scholar]
  19. IJkel W. F. , Westenberg M. , Goldbach R. W. , Blissard G. W. , Vlak J. M. , Zuidema D. . ( 2000;). A novel baculovirus envelope fusion protein with a proprotein convertase cleavage site. Virology 275: 30–41 [CrossRef] [PubMed].
    [Google Scholar]
  20. Jones J. , Krag S. S. , Betenbaugh M. J. . ( 2005;). Controlling N-linked glycan site occupancy. Biochim Biophys Acta 1726: 121–137 [CrossRef] [PubMed].
    [Google Scholar]
  21. Kadlec J. , Loureiro S. , Abrescia N. G. , Stuart D. I. , Jones I. M. . ( 2008;). The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat Struct Mol Biol 15: 1024–1030 [CrossRef] [PubMed].
    [Google Scholar]
  22. Kiefer F. , Arnold K. , Künzli M. , Bordoli L. , Schwede T. . ( 2009;). The swiss-model repository and associated resources. Nucleic Acids Res 37: (Database issue), D387–D392 [CrossRef] [PubMed].
    [Google Scholar]
  23. Land A. , Zonneveld D. , Braakman I. . ( 2003;). Folding of HIV-1 envelope glycoprotein involves extensive isomerization of disulfide bonds and conformation-dependent leader peptide cleavage. FASEB J 17: 1058–1067.[CrossRef]
    [Google Scholar]
  24. Lázaro M. E. , Cantoni G. E. , Calanni L. M. , Resa A. J. , Herrero E. R. , Iacono M. A. , Enria D. A. , González Cappa S. M. . ( 2007;). Clusters of hantavirus infection, southern Argentina. Emerg Infect Dis 13: 104–110 [CrossRef] [PubMed].
    [Google Scholar]
  25. Long G. , Westenberg M. , Wang H. , Vlak J. M. , Hu Z. . ( 2006;). Function, oligomerization and N-linked glycosylation of the Helicoverpa armigera single nucleopolyhedrovirus envelope fusion protein. J Gen Virol 87: 839–846 [CrossRef] [PubMed].
    [Google Scholar]
  26. Long G. , Pan X. , Vlak J. M. . ( 2007;). Absence of N-linked glycans from the F2 subunit of the major baculovirus envelope fusion protein F enhances fusogenicity. J Gen Virol 88: 441–449 [CrossRef] [PubMed].
    [Google Scholar]
  27. Ohuchi M. , Ohuchi R. , Feldmann A. , Klenk H. D. . ( 1997a;). Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J Virol 71: 8377–8384 [PubMed].
    [Google Scholar]
  28. Ohuchi R. , Ohuchi M. , Garten W. , Klenk H. D. . ( 1997b;). Oligosaccharides in the stem region maintain the influenza virus hemagglutinin in the metastable form required for fusion activity. J Virol 71: 3719–3725 [PubMed].
    [Google Scholar]
  29. Pearson M. N. , Groten C. , Rohrmann G. F. . ( 2000;). Identification of the Lymantria dispar nucleopolyhedrovirus envelope fusion protein provides evidence for a phylogenetic division of the Baculoviridae . J Virol 74: 6126–6131 [CrossRef] [PubMed].
    [Google Scholar]
  30. Peitsch M. C. . ( 1995;). Protein modeling by e-mail. Biotechnology (N Y) 13: 658–660 [CrossRef].
    [Google Scholar]
  31. Roy A. , Kucukural A. , Zhang Y. . ( 2010;). i-tasser: A unified platform for automated protein structure and function prediction. Nat Protoc 5: 725–738 [CrossRef] [PubMed].
    [Google Scholar]
  32. Scalia S. , Sharma P. , Rodriguez J. , Roche F. , Luchette F. , Chambers R. , Flint L. M. , Steinberg S. . ( 1992;). Decreased mesenteric blood flow in experimental multiple organ failure. J Surg Res 52: 1–5 [CrossRef] [PubMed].
    [Google Scholar]
  33. Tan Y. , Jiang L. , Wang M. , Yin F. , Deng F. , Liu M. , Hu Z. , Wang H. . ( 2008;). Mutagenesis and nuclear magnetic resonance analyses of the fusion peptide of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus F protein. J Virol 82: 8138–8148 [CrossRef] [PubMed].
    [Google Scholar]
  34. Tong S. , Yi F. , Martin A. , Yao Q. , Li M. , Compans R. W. . ( 2001;). Three membrane-proximal amino acids in the human parainfluenza type 2 (HPIV 2) F protein are critical for fusogenic activity. Virology 280: 52–61 [CrossRef] [PubMed].
    [Google Scholar]
  35. Varki A. . ( 2006;). Nothing in glycobiology makes sense, except in the light of evolution. Cell 126: 841–845 [CrossRef] [PubMed].
    [Google Scholar]
  36. von Messling V. , Cattaneo R. . ( 2003;). N-linked glycans with similar location in the fusion protein head modulate paramyxovirus fusion. J Virol 77: 10202–10212 [CrossRef] [PubMed].
    [Google Scholar]
  37. Wang M. , Tan Y. , Yin F. , Deng F. , Vlak J. M. , Hu Z. , Wang H. . ( 2008;). The F protein of Helicoverpa armigera single nucleopolyhedrovirus can be substituted functionally with its homologue from Spodoptera exigua multiple nucleopolyhedrovirus. J Gen Virol 89: 791–798 [CrossRef] [PubMed].
    [Google Scholar]
  38. Wang M. , Yin F. , Shen S. , Tan Y. , Deng F. , Vlak J. M. , Hu Z. , Wang H. . ( 2010;). Partial functional rescue of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus infectivity by replacement of F protein with GP64 from Autographa californica multicapsid nucleopolyhedrovirus. J Virol 84: 11505–11514 [CrossRef] [PubMed].
    [Google Scholar]
  39. Westenberg M. , Veenman F. , Roode E. C. , Goldbach R. W. , Vlak J. M. , Zuidema D. . ( 2004;). Functional analysis of the putative fusion domain of the baculovirus envelope fusion protein F. J Virol 78: 6946–6954 [CrossRef] [PubMed].
    [Google Scholar]
  40. Zhang M. , Gaschen B. , Blay W. , Foley B. , Haigwood N. , Kuiken C. , Korber B. . ( 2004;). Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14: 1229–1246 [CrossRef] [PubMed].
    [Google Scholar]
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