N-glycans on the Nipah virus attachment glycoprotein modulate fusion and viral entry as they protect against antibody neutralization

Journal of Virology

Volumn 86, Issue 22, 2012, Pages 11991-12002

  Biering, Scott B ^a,b   Huang, Andrew ^b   Vu, Andy T ^b   Robinson, L R ^b   Bradel Tretheway, Birgit ^a   Cho, Eric ^b   Lee, Benhur ^a,b   Aguilar, Hector C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN B2; GLYCAN DERIVATIVE; NEUTRALIZING ANTIBODY; VIRUS GLYCOPROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; MEMBRANE FUSION; MUTATIONAL ANALYSIS; NIPAH VIRUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; VIRION; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS NEUTRALIZATION; VIRUS RESISTANCE; VIRUS VIRULENCE; WILD TYPE;

ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETINAE; EPHRIN-B2; EPHRIN-B3; GLYCOPROTEINS; GLYCOSYLATION; HEK293 CELLS; HUMANS; MEMBRANE FUSION; MOLECULAR CONFORMATION; MUTATION; NIPAH VIRUS; PHENOTYPE; POLYSACCHARIDES; PROTEIN BINDING; VIRAL FUSION PROTEINS; VIRUS ATTACHMENT;

NIPAH VIRUS; PARAMYXOVIRIDAE;

EID: 84869132593     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01304-12     Document Type: Article

References (50)

1. Aguilar HC, Aspericueta V, Robinson LR, Aanensen KE, Lee B. 2010. A quantitative and kinetic fusion protein-triggering assay can discern distinct steps in the Nipah virus membrane fusion cascade. J. Virol. 84:8033-8041.
2. Aguilar HC, et al. 2009. A novel receptor-induced activation site in the Nipah virus attachment glycoprotein (G) involved in triggering the fusion glycoprotein (F). J. Biol. Chem. 284:1628-1635.
3. Aguilar HC, Iorio RM. 2012. Henipavirus membrane fusion and viral entry. Curr. Top. Microbiol. Immunol. 359:79-94.
4. Aguilar HC, Lee B. 2011. Emerging paramyxoviruses: molecular mechanisms and antiviral strategies. Expert Rev. Mol. Med. 13:e6.
5. Aguilar HC, et al. 2007. Polybasic KKR motif in the cytoplasmic tail of Nipah virus fusion protein modulates membrane fusion by inside-out signaling. J. Virol. 81:4520-4532.
6. Aguilar HC, et al. 2006. N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J.Virol. 80:4878-4889.
7. Bowden TA, et al. 2008. Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat. Struct. Mol. Biol.15:567-572.
8. Bowden TA, et al. 2008. Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: a template for antiviral and vaccine design. J. Virol. 82:11628-11636.8a. Bowden TA, Crispin M, Harvey DJ, Jones EY, Stuart DI. 2010. Dimeric architecture of the Hendra virus attachment glycoprotein: evidence for a conserved mode of assembly. J. Virol. 84:6208-6217.
9. Bowden TA, Crispin M, Harvey DJ, Jones EY, Stuart DI. 2010. Dimeric architecture of the Hendra virus attachment glycoprotein: evidence for a conserved mode of assembly. J. Virol. 84:6208-6217.
10. Carter JR, Pager CT, Fowler SD, Dutch RE. 2005. Role of N-linked glycosylation of the Hendra virus fusion protein. J. Virol. 79:7922-7925.
11. Cheng-Mayer C, Brown A, Harouse J, Luciw PA, Mayer AJ. 1999.Selection for neutralization resistance of the simian/human immunodeficiency virus SHIVSF33A variant in vivo by virtue of sequence changes in the extracellular envelope glycoprotein that modify N-linked glycosylation.J. Virol. 73:5294-5300.
12. Chua KB, et al. 2000. Nipah virus: a recently emergent deadly paramyxovirus. Science 288:1432-1435.
13. Colgrave ML, et al. 2012. Site occupancy and glycan compositional analysis of two soluble recombinant forms of the attachment glycoprotein of Hendra virus. Glycobiology 22:572-584.
14. Davis D, Stephens DM, Willers C, Lachmann PJ. 1990. Glycosylation governs the binding of antipeptide antibodies to regions of hypervariable amino acid sequence within recombinant gp120 of human immunodeficiency virus type 1. J. Gen. Virol. 71(Pt 12):2889-2898.
15. Garner OB, et al. 2010. Endothelial galectin-1 binds to specific glycans on Nipah virus fusion protein and inhibits maturation, mobility, and function to block syncytia formation. PLoS Pathog. 6:e1000993. doi:10.1371/journal.ppat.1000993.
16. Herfst S, et al. 2008. Low-pH-induced membrane fusion mediated by human metapneumovirus F protein is a rare, strain-dependent phenomenon.J. Virol. 82:8891-8895.
17. Iorio RM, Glickman RL, Sheehan JP. 1992. Inhibition of fusion by neutralizing monoclonal antibodies to the haemagglutininneuraminidase glycoprotein of Newcastle disease virus. J. Gen. Virol.73(Pt 5):1167-1176.
18. Iorio RM, Mahon PJ. 2008. Paramyxoviruses: different receptors-different mechanisms of fusion. Trends Microbiol. 16:135-137.
19. Iorio RM, Melanson VR, Mahon PJ. 2009. Glycoprotein interactions in paramyxovirus fusion. Future Virol. 4:335-351.
20. Johnson JB, Aguilar HC, Lee B, Parks GD. 2011. Interactions of human complement with virus particles containing the Nipah virus glycoproteins.J. Virol. 85:5940-5948.
21. Kahn JS, Schnell MJ, Buonocore L, Rose JK. 1999. Recombinant vesicular stomatitis virus expressing respiratory syncytial virus (RSV)glycoproteins: RSV fusion protein can mediate infection and cell fusion. Virology 254:81-91.
22. Lam SK. 2003. Nipah virus-a potential agent of bioterrorism? Antivir. Res.57:113-119.
23. Lamb RA, Paterson RG, Jardetzky TS. 2006. Paramyxovirus membrane fusion: lessons from the F andHNatomic structures. Virology 344:30-37.
24. Lee J, Park JS, Moon JY, Kim KY, Moon HM. 2003. The influence of glycosylation on secretion, stability, and immunogenicity of recombinant HBV pre-S antigen synthesized in Saccharomyces cerevisiae. Biochem. Biophys.Res. Commun. 303:427-432.
25. Levroney EL, et al. 2005. Novel innate immune functions for galectin-1:galectin-1 inhibits cell fusion by Nipah virus envelope glycoproteins and augments dendritic cell secretion of proinflammatory cytokines. J. Immunol.175:413-420.
26. Luby SP, et al. 2009. Recurrent zoonotic transmission of Nipah virus into humans, Bangladesh, 2001-2007. Emerg. Infect. Dis. 15:1229-1235.
27. Luby SP, et al. 2006. Foodborne transmission of Nipah virus, Bangladesh.Emerg. Infect. Dis. 12:1888-1894.
28. Maar D, et al. 2012. Cysteines in the stalk of the nipah virus G glycoprotein are located in a distinct subdomain critical for fusion activation. J.Virol. 86:6632-6642.
29. McGinnes L, Sergel T, Reitter J, Morrison T. 2001. Carbohydrate modifications of the NDV fusion protein heptad repeat domains influence maturation and fusion activity. Virology 283:332-342.
30. McGinnes LW, Morrison TG. 1995. The role of individual oligosaccharide chains in the activities of the HN glycoprotein of Newcastle disease virus. Virology 212:398-410.
31. McKinnell JA, Saag MS. 2009. Novel drug classes: entry inhibitors [enfuvirtide, chemokine (C-C motif) receptor 5 antagonists]. Curr. Opin. HIV AIDS 4:513-517.
32. Moll M, Kaufmann A, Maisner A. 2004. Influence of N-glycans on processing and biological activity of the Nipah virus fusion protein. J.Virol. 78:7274-7278.
33. Murineddu G, Murruzzu C, Pinna GA. 2010. An overview on different classes of viral entry and respiratory syncytial virus (RSV) fusion inhibitors.Curr. Med. Chem. 17:1067-1091.
34. Navarro-Sanchez E, et al. 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.
35. Negrete OA, et al. 2005. EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 436:401-405.
36. Negrete OA, et al. 2006. Two key residues in ephrinB3 are critical for its use as an alternative receptor for Nipah virus. PLoS Pathog. 2:e7. doi:10.1371/journal.ppat.0020007.
37. Olofsson S, Hansen JE. 1998. Host cell glycosylation of viral glycoproteins:a battlefield for host defence and viral resistance. Scand. J. Infect.Dis. 30:435-440.
38. Pikora CA. 2004. Glycosylation of the ENV spike of primate immunodeficiency viruses and antibody neutralization. Curr. HIV Res. 2:243-254.
39. Reitter JN, Means RE, Desrosiers RC. 1998. A role for carbohydrates in immune evasion in AIDS. Nat. Med. 4:679-684.
40. Salinovich O, et al. 1986. Rapid emergence of novel antigenic and genetic variants of equine infectious anemia virus during persistent infection. J.Virol. 57:71-80.
41. Sawatsky B, von Messling V. 2010. Canine distemper viruses expressing a hemagglutinin without N-glycans lose virulence but retain immunosuppression.J. Virol. 84:2753-2761.
42. Schowalter RM, Smith SE, Dutch RE. 2006. Characterization of human metapneumovirus F protein-promoted membrane fusion: critical roles for proteolytic processing and low pH. J. Virol. 80:10931-10941.
43. Skehel JJ, et al. 1984. A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody.Proc. Natl. Acad. Sci. U. S. A. 81:1779-1783.
44. Tan CT, Wong KT. 2003. Nipah encephalitis outbreak in Malaysia. Ann.Acad. Med. Singapore 32:112-117.
45. 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.
46. Wei X, et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
47. Whitman SD, Smith EC, Dutch RE. 2009. Differential rates of protein folding and cellular trafficking for the Hendra virus F and G proteins:implications for F-G complex formation. J. Virol. 83:8998-9001.
48. Wong KT, et al. 2002. Nipah virus infection: pathology and pathogenesis of an emerging paramyxoviral zoonosis. Am. J. Pathol. 161:2153-2167.
49. Xu K, et al. 2008. Host cell recognition by the henipaviruses: crystal structures of the Nipah G attachment glycoprotein and its complex with ephrin-B3. Proc. Natl. Acad. Sci. U. S. A. 105:9953-9958
50. Xu Y, et al. 2004. Crystallization and preliminary crystallographic analysis of the fusion core from two new zoonotic paramyxoviruses, Nipah virus and Hendra virus. Acta Crystallogr. D Biol. Crystallogr. 60:1161-1164.