N-glycans on nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry

Journal of Virology

Volumn 80, Issue 10, 2006, Pages 4878-4889

  Aguilar, Hector C ^a   Matreyek, Kenneth A ^a   Filone, Claire Marie ^b   Hashimi, Sara T ^a   Levroney, Ernest L ^a   Negrete, Oscar A ^a   Bertolotti Ciarlet, Andrea ^b   Choi, Daniel Y ^a   McHardy, Ian ^a   Fulcher, Jennifer A ^a   Su, Stephen V ^a   Wolf, Mike C ^a   Kohatsu, Luciana ^a   Baum, Linda G ^a   Lee, Benhur ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN DERIVATIVE; PROTEIN NIV F; PROTEIN NIV G; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUSION; FUSOGENICITY; HUMAN; HUMAN CELL; MEMBRANE FUSION; NIPAH VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAMYXOVIRUS; PRIORITY JOURNAL; SYNCYTIUM; VIRUS ADSORPTION; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS MUTANT; VIRUS NEUTRALIZATION;

ANIMALS; CELL LINE; DOGS; GLYCOSYLATION; HELA CELLS; HENIPAVIRUS INFECTIONS; HUMANS; MEMBRANE FUSION; NEUTRALIZATION TESTS; NIPAH VIRUS; POLYSACCHARIDES; VIRAL ENVELOPE PROTEINS; VIRAL FUSION PROTEINS;

ANIMALIA; NIPAH VIRUS; PARAMYXOVIRIDAE;

EID: 33646447520     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.10.4878-4889.2006     Document Type: Article

References (49)

1. Abrahamyan, L. G., S. R. Mkrtchyan, J. Binley, M. Lu, G. B. Melikyan, and F. S. Cohen. 2005. The cytoplasmic tail slows the folding of human immunodeficiency virus type 1 Env from a late prebundle configuration into the six-helix bundle. J. Virol. 79:106-115.
2. Aguilar, H. C., W. F. Anderson, and P. M. Cannon. 2003. Cytoplasmic tail of Moloney murine leukemia virus envelope protein influences the conformation of the extracellular domain: implications for mechanism of action of the R peptide. J. Virol. 77:1281-1291.
3. Bagai, S., and R. A. Lamb. 1995. Individual roles of N-linked oligosaccharide chains in intracellular transport of the paramyxovirus SV5 fusion protein. Virology 209:250-256.
4. Bonaparte, M. I., A. S. Dimitrov, K. N. Bossart, G. Crameri, B. A. Mungall, K. A. Bishop, V. Choudhry, D. S. Dimitrov, L. F. Wang, B. T. Eaton, and C. C. Broder. 2005. Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc. Natl. Acad. Sci. USA 102:10652-10657.
5. Bossart, K. N., B. A. Mungall, G. Crameri, L. F. Wang, B. T. Eaton, and C. C. Broder. 2005. Inhibition of Henipavirus fusion and infection by heptad-derived peptides of the Nipah virus fusion glycoprotein. Virol. J. 2:57. [Online.]
6. Bossart, K. N., L. F. Wang, B. T. Eaton, and C. C. Broder. 2001. Functional expression and membrane fusion tropism of the envelope glycoproteins of Hendra virus. Virology 290:121-135.
7. Carter, J. R., C. T. Pager, S. D. Fowler, and R. E. Dutch. 2005. Role of N-linked glycosylation of the Hendra virus fusion protein. J. Virol. 79:7922-7925.
8. Cheng-Mayer, C., A. Brown, J. Harouse, P. A. Luciw, and A. J. Mayer. 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.
9. Derdeyn, C. A., J. M. Decker, J. N. Sfakianos, X. Wu, W. A. O'Brien, L. Ratner, J. C. Kappes, G. M. Shaw, and E. Hunter. 2000. Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J. Virol. 74:8358-8367.
10. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
11. Gallo, S. A., C. M. Finnegan, M. Viard, Y. Raviv, A. Dimitrov, S. S. Rawat, A. Puri, S. Durell, and R. Blumenthal. 2003. The HIV Env-mediated fusion reaction. Biochim. Biophys. Acta 1614:36-50.
12. Gallo, S. A., A. Puri, and R. Blumenthal. 2001. HIV-1 gp41 six-helix bundle formation occurs rapidly after the engagement of gp120 by CXCR4 in the HIV-1 Env-mediated fusion process. Biochemistry 40:12231-12236.
13. Hu, A., T. Cathomen, R. Cattaneo, and E. Norrby. 1995. Influence of N-linked oligosaccharide chains on the processing, cell surface expression and function of the measles virus fusion protein. J. Gen. Virol. 76:705-710.
14. Lam, S. K. 2003. Nipah virus-a potential agent of bioterrorism? Antivir. Res. 57:113-119.
15. Lamb, R. A. 1993. Paramyxovirus fusion: a hypothesis for changes. Virology 197:1-11.
16. Lee, J., J. S. Park, J. Y. Moon, K. Y. Kim, and H. M. Moon. 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.
17. Levroney, E. L., H. C. Aguilar, J. A. Fulcher, L. Kohatsu, K. E. Pace, M. Pang, K. B. Gurney, L. G. Baum, and B. Lee. 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.
18. Lineberger, J. E., R. Danzeisen, D. J. Hazuda, A. J. Simon, and M. D. Miller. 2002. Altering expression levels of human immunodeficiency virus type 1 gp120-gp41 affects efficiency but not kinetics of cell-cell fusion. J. Virol. 76:3522-3533.
19. McGinnes, L., T. Sergel, J. Reitter, and T. Morrison. 2001. Carbohydrate modifications of the NDV fusion protein heptad repeat domains influence maturation and fusion activity. Virology 283:332-342.
20. McGinnes, L. W., K. Gravel, and T. G. Morrison. 2002. Newcastle disease virus HN protein alters the conformation of the F protein at cell surfaces. J. Virol. 76:12622-12633.
21. Moll, M., A. Kaufmann, and A. Maisner. 2004. Influence of N-glycans on processing and biological activity of the Nipah virus fusion protein. J. Virol. 78:7274-7278.
22. Moore, J. P., J. A. McKeating, R. A. Weiss, and Q. J. Sattentau. 1990. Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science 250:1139-1142.
23. Morrison, T. G. 2003. Structure and function of a paramyxovirus fusion protein. Biochim. Biophys. Acta 1614:73-84.
24. Navarro-Sanchez, E., R. Altmeyer, A. Amara, O. Schwartz, F. Fieschi, J. L. Virelizier, F. Arenzana-Seisdedos, and P. Despres. 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.
25. Negrete, O. A., E. L. Levroney, H. C. Aguilar, A. Bertolotti-Ciarlet, R. Nazarian, S. Tajyar, and B. Lee. 2005. EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 436:401-405.
26. Olofsson, S., and J. E. Hansen. 1998. Host cell glycosylation of viral glycoproteins-a battlefield for host defence and viral resistance. Scand. J. Infect. Dis. 30:435-440.
27. Pikora, C. A. 2004. Glycosylation of the ENV spike of primate immunodeficiency viruses and antibody neutralization. Curr. HIV Res. 2:243-254.
28. Plemper, R. K., A. L. Hammond, D. Gerlier, A. K. Fielding, and R. Cattaneo. 2002. Strength of envelope protein interaction modulates cytopathicity of measles virus. J. Virol. 76:5051-5061.
29. Rasmussen, T. B., A. Uttenthal, J. Fernandez, and T. Storgaard. 2005. Quantitative multiplex assay for simultaneous detection and identification of Indiana and New Jersey serotypes of vesicular stomatitis virus. J. Clin. Microbiol. 43:356-362.
30. Reeves, J. D., S. A. Gallo, N. Ahmad, J. L. Miamidian, P. E. Harvey, M. Sharron, S. Pohlmann, J. N. Sfakianos, C. A. Derdeyn, R. Blumenthal, E. Hunter, and R. W. Doms. 2002. Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics. Proc. Natl. Acad. Sci. USA 99:16249-16254.
31. Reeves, J. D., J. L. Miamidian, M. J. Biscone, F. H. Lee, N. Ahmad, T. C. Pierson, and R. W. Doms. 2004. Impact of mutations in the coreceptor binding site on human immunodeficiency virus type 1 fusion, infection, and entry inhibitor sensitivity. J. Virol. 78:5476-5485.
32. Reitter, J. N., R. E. Means, and R. C. Desrosiers. 1998. A role for carbohydrates in immune evasion in AIDS. Nat. Med. 4:679-684.
33. Salinovich, O., S. L. Payne, R. C. Montelaro, K. A. Hussain, C. J. Issel, and K. L. Schnorr. 1986. Rapid emergence of novel antigenic and genetic variants of equine infectious anemia virus during persistent infection. J. Virol. 57:71-80.
34. Schoonman, M. J., R. M. Knegtel, and P. D. Grootenhuis. 1998. Practical evaluation of comparative modelling and threading methods. Comput. Chem. 22:369-375.
35. Segawa, H., T. Yamashita, M. Kawakita, and H. Taira. 2000. Functional analysis of the individual oligosaccharide chains of Sendai virus fusion protein. J. Biochem. (Tokyo) 128:65-72.
36. Si, Z., N. Madani, J. M. Cox, J. J. Chruma, J. C. Klein, A. Schon, N. Phan, L. Wang, A. C. Biorn, S. Cocklin, I. Chaiken, E. Freire, A. B. Smith III, and J. G. Sodroski. 2004. Small-molecule inhibitors of HIV-1 entry block receptor-induced conformational changes in the viral envelope glycoproteins. Proc. Natl. Acad. Sci. USA 101:5036-5041.
37. Skehel, J. J., D. J. Stevens, R. S. Daniels, A. R. Douglas, M. Knossow, I. A. Wilson, and D. C. Wiley. 1984. A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody. Proc. Natl. Acad. Sci. USA 81:1779-1783.
38. Takimoto, T., G. L. Taylor, H. C. Connaris, S. J. Crennell, and A. Portner. 2002. Role of the hemagglutinin-neuraminidase protein in the mechanism of paramyxovirus-cell membrane fusion. J. Virol. 76:13028-13033.
39. Tan, C. T., and K. T. Wong. 2003. Nipah encephalitis outbreak in Malaysia. Ann. Acad. Med. Singapore 32:112-117.
40. von Messling, V., and R. Cattaneo. 2003. N-linked glycans with similar location in the fusion protein head modulate paramyxovirus fusion. J. Virol. 77:10202-10212.
41. Wang, L.-F., M. Yu, E. Hansson, L. I. Pritchard, B. Shiell, W. P. Michalski, and B. T. Eaton. 2000. The exceptionally large genome of Hendra virus: support for creation of a new genus within the family Paramyxoviridae. J. Virol. 74:9972-9979.
42. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
43. Wild, C. T., D. C. Shugars, T. K. Greenwell, C. B. McDanal, and T. J. Matthews. 1994. Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc. Natl. Acad. Sci. USA 91:9770-9774.
44. Wildlife Trust. 28 April 2004, posting date. Nipah virus breaks out in Bangladesh: mortality rates of 60% to 74%. Human to-human transmission may be implicated. Wildlife Trust, New York, N.Y. [Online.] www.ewire.com /display.cfm/Wire_ID/2117.
45. Wong, K. T., W. J. Shieh, S. Kumar, K. Norain, W. Abdullah, J. Guarner, C. S. Goldsmith, K. B. Chua, S. K. Lam, C. T. Tan, K. J. Goh, H. T. Chong, R. Jusoh, P. E. Rollin, T. G. Ksiazek, and S. R. Zaki. 2002. Nipah virus infection: pathology and pathogenesis of an emerging paramyxoviral zoonosis. Am. J. Pathol. 161:2153-2167.
46. World Health Organization. 2004. Nipah virus outbreak(s) in Bangladesh, January-April 2004. Wkly. Epidemiol. Rec 79:168-171.
47. Yao, Q., and R. W. Compans. 1996. Peptides corresponding to the heptad repeat sequence of human parainfluenza virus fusion protein are potent inhibitors of virus infection. Virology 223:103-112.
48. Yin, H. S., R. G. Paterson, X. Wen, R. A. Lamb, and T. S. Jardetzky. 2005. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. USA 102:9288-9293.
49. Zaitsev, V., M. von Itzstein, D. Groves, M. Kiefel, T. Takimoto, A. Portner, and G. Taylor. 2004. Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase: implications for fusion. J. Virol. 78:3733-3741.