Comprehensive functional analysis of N-linked glycans on ebola virus GP1

mBio

Volumn 5, Issue 1, 2014, Pages

  Lennemann, Nicholas J ^a   Rhein, Bethany A ^a   Ndungo, Esther ^b   Chandran, Kartik ^b   Qiu, Xiangguo ^c   Maury, Wendy ^a  

^a UNIVERSITY OF IOWA   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c PUBLIC HEALTH AGENCY OF CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ANTISERUM; CELL RECEPTOR; GLYCAN; LECTIN; PROTEIN GP1; PROTEIN NPC1; PROTEINASE; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CELL TRANSFER; EBOLA VIRUS; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; VERO CELL; VIRION; VIRUS ENTRY; VIRUS NEUTRALIZATION;

ANIMALS; CERCOPITHECUS AETHIOPS; DNA MUTATIONAL ANALYSIS; EBOLAVIRUS; MACROPHAGES; MICE; MUTAGENESIS, SITE-DIRECTED; POLYSACCHARIDES; TRANSDUCTION, GENETIC; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84903364048     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00862-13     Document Type: Article

References (47)

1. Feldmann H, Geisbert TW. 2011. Ebola haemorrhagic fever. Lancet 377:849-862. http://dx.doi.org/10.1016/S0140-6736(10)60667-8.
2. Richman DD, Cleveland PH, McCormick JB, Johnson KM. 1983. Antigenic analysis of strains of Ebola virus: identification of two Ebola virus serotypes. J. Infect. Dis. 147:268-271. http://dx.doi.org/10.1093/infdis/ 147.2.268.
3. Feldmann H, Nichol ST, Klenk HD, Peters CJ, Sanchez A. 1994. Characterization of filoviruses based on differences in structure and antigenicity of the virion glycoprotein. Virology 199:469-473. http:// dx.doi.org/10.1006/viro.1994.1147.
4. Kuhn JH, Becker S, Ebihara H, Geisbert TW, Johnson KM, Kawaoka Y, Lipkin WI, Negredo AI, Netesov SV, Nichol ST, Palacios G, Peters CJ, Tenorio A, Volchkov VE, Jahrling PB. 2010. Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations. Arch. Virol. 155:2083-2103. http:// dx.doi.org/10.1007/s00705-010-0814-x.
5. Jeffers SA, Sanders DA, Sanchez A. 2002. Covalent modifications of the Ebola virus glycoprotein. J. Virol. 76:12463-12472. http://dx.doi.org/ 10.1128/JVI.76.24.12463-12472.2002.
6. Lee JE, Fusco ML, Hessell AJ, Oswald WB, Burton DR, Saphire EO. 2008. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454:177-182. http://dx.doi.org/10.1038/ nature07082.
7. Martinez O, Tantral L, Mulherkar N, Chandran K, Basler CF. 2011. Impact of Ebola mucin-like domain on antiglycoprotein antibody responses induced by Ebola virus-like particles. J. Infect. Dis. 204(Suppl 3):S825-S832. http://dx.doi.org/10.1093/infdis/jir295.
8. Dowling W, Thompson E, Badger C, Mellquist JL, Garrison AR, Smith JM, Paragas J, Hogan RJ, Schmaljohn C. 2007. Influences of glycosylation on antigenicity, immunogenicity, and protective efficacy of Ebola virus GP DNA vaccines. J. Virol. 81:1821-1837. http://dx.doi.org/ 10.1128/JVI.02098-06.
9. Wilson JA, Hevey M, Bakken R, Guest S, Bray M, Schmaljohn AL, Hart MK. 2000. Epitopes involved in antibody-mediated protection from Ebola virus. Science 287:1664-1666. http://dx.doi.org/10.1126/ science.287.5458.1664.
10. Vigerust DJ, Shepherd VL. 2007. Virus glycosylation: role in virulence and immune interactions. Trends Microbiol. 15:211-218. http:// dx.doi.org/10.1016/j.tim.2007.03.003.
11. 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. http://dx.doi.org/ 10.1006/viro.2001.0899.
12. Eichler R, Lenz O, Garten W, Strecker T. 2006. The role of single N-glycans in proteolytic processing and cell surface transport of the Lassa virus glycoprotein GP-C. Virol. J. 3:41. http://dx.doi.org/10.1186/1743-422X-3-41.
13. Biering SB, Huang A, Vu AT, Robinson LR, Bradel-Tretheway B, Choi E, Lee B, Aguilar HC. 2012. N-glycans on the Nipah virus attachment glycoprotein modulate fusion and viral entry as they protect against antibody neutralization. J. Virol. 86:11991-12002. http://dx.doi.org/10.1128/ JVI.01304-12.
14. Aguilar HC, Matreyek KA, Filone CM, Hashimi ST, Levroney EL, Negrete OA, Bertolotti-Ciarlet A, Choi DY, McHardy I, Fulcher JA, Su SV, Wolf MC, Kohatsu L, Baum LG, Lee B. 2006. N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J. Virol. 80:4878-4889. http://dx.doi.org/10.1128/ JVI.80.10.4878-4889.2006.
15. Cook JD, Lee JE. 2013. The secret life of viral entry glycoproteins: moonlighting in immune evasion. PLoS Pathog. 9:e1003258.
16. Moller-Tank S, Kondratowicz AS, Davey RA, Rennert PD, Maury W. 2013. Role of the phosphatidylserine receptor TIM-1 in enveloped virus entry. J. Virol. 87:8327-8341.
17. Hood CL, Abraham J, Boyington JC, Leung K, Kwong PD, Nabel GJ. 2010. Biochemical and structural characterization of cathepsin L-processed Ebola virus glycoprotein: implications for viral entry and immunogenicity. J. Virol. 84:2972-2982. http://dx.doi.org/10.1128/ JVI.02151-09.
18. Dube D, Brecher MB, Delos SE, Rose SC, Park EW, Schornberg KL, Kuhn JH, White JM. 2009. The primed ebolavirus glycoprotein (19-kilodalton GP1,2): sequence and residues critical for host cell binding. J. Virol. 83:2883-2891. http://dx.doi.org/10.1128/JVI.01956-08.
19. Chandran K, Sullivan NJ, Felbor U, Whelan SP, Cunningham JM. 2005. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308:1643-1645. http://dx.doi.org/10.1126/ science.1110656.
20. Schornberg K, Matsuyama S, Kabsch K, Delos S, Bouton A, White J. 2006. Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. J. Virol. 80:4174-4178. http://dx.doi.org/10.1128/ JVI.80.8.4174-4178.2006.
21. Wong AC, Sandesara RG, Mulherkar N, Whelan SP, Chandran K. 2010. A forward genetic strategy reveals destabilizing mutations in the Ebolavirus glycoprotein that alter its protease dependence during cell entry. J. Virol. 84:163-175. http://dx.doi.org/10.1128/JVI.01832-09.
22. Varki A. 1993. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3:97-130. http://dx.doi.org/10.1093/glycob/3.2.97.
23. Miller EH, Obernosterer G, Raaben M, Herbert AS, Deffieu MS, Krishnan A, Ndungo E, Sandesara RG, Carette JE, Kuehne AI, Ruthel G, Pfeffer SR, Dye JM, Whelan SP, Brummelkamp TR, Chandran K. 2012. Ebola virus entry requires the host-programmed recognition of an intracellular receptor. EMBO J. 31:1947-1960. http://dx.doi.org/10.1038/ emboj.2012.53.
24. Côté M, Misasi J, Ren T, Bruchez A, Lee K, Filone CM, Hensley L, Li Q, Ory D, Chandran K, Cunningham J. 2011. Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature 477: 344-348. http://dx.doi.org/10.1038/nature10380.
25. Powlesland AS, Fisch T, Taylor ME, Smith DF, Tissot B, Dell A, Pöhlmann S, Drickamer K. 2008. A novel mechanism for LSECtin binding to Ebola virus surface glycoprotein through truncated glycans. J. Biol. Chem. 283:593-602.
26. Guo Y, Feinberg H, Conroy E, Mitchell DA, Alvarez R, Blixt O, Taylor ME, Weis WI, Drickamer K. 2004. Structural basis for distinct ligandbinding and targeting properties of the receptors DC-SIGN and DCSIGNR. Nat. Struct. Mol. Biol. 11:591-598. http://dx.doi.org/10.1038/ nsmb784.
27. Khoo US, Chan KY, Chan VS, Lin CL. 2008. DC-SIGN and L-SIGN: the SIGNs for infection. J. Mol. Med. 86:861-874. http://dx.doi.org/10.1007/ s00109-008-0350-2.
28. Feinberg H, Mitchell DA, Drickamer K, Weis WI. 2001. Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294:2163-2166. http://dx.doi.org/10.1126/science.1066371.
29. Meier M, Bider MD, Malashkevich VN, Spiess M, Burkhard P. 2000. Crystal structure of the carbohydrate recognition domain of the H1 subunit of the asialoglycoprotein receptor. J. Mol. Biol. 300:857-865. http:// dx.doi.org/10.1006/jmbi.2000.3853.
30. Jemielity S, Wang JJ, Chan YK, Ahmed AA, Li W, Monahan S, Bu X, Farzan M, Freeman GJ, Umetsu DT, Dekruyff RH, Choe H. 2013. TIM-family proteins promote infection of multiple enveloped viruses through virion-associated phosphatidylserine. PLoS Pathog. 9:e1003232. http://dx.doi.org/10.1371/journal.ppat.1003232.
31. Ryabchikova EI, Kolesnikova LV, Luchko SV. 1999. An analysis of features of pathogenesis in two animal models of Ebola virus infection. J. Infect. Dis. 179(Suppl 1):S199-S202. http://dx.doi.org/10.1086/514293.
32. Takada A, Fujioka K, Tsuiji M, Morikawa A, Higashi N, Ebihara H, Kobasa D, Feldmann H, Irimura T, Kawaoka Y. 2004. Human macrophage C-type lectin specific for galactose and N-acetylgalactosamine promotes filovirus entry. J. Virol. 78:2943-2947. http://dx.doi.org/10.1128/ JVI.78.6.2943-2947.2004.
33. Alvarez CP, Lasala F, Carrillo J, Muñiz O, Corbí AL, Delgado R. 2002. C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J. Virol. 76:6841-6844. http://dx.doi.org/10.1128/ JVI.76.13.6841-6844.2002.
34. Taylor PR, Brown GD, Herre J, Williams DL, Willment JA, Gordon S. 2004. The role of SIGNR1 and the beta-glucan receptor (dectin-1) in the nonopsonic recognition of yeast by specific macrophages. J. Immunol. 172:1157-1162.
35. Onami TM, Lin MY, Page DM, Reynolds SA, Katayama CD, Marth JD, Irimura T, Varki A, Varki N, Hedrick SM. 2002. Generation of mice deficient for macrophage galactose-and N-acetylgalactosamine-specific lectin: limited role in lymphoid and erythroid homeostasis and evidence for multiple lectins. Mol. Cell. Biol. 22:5173-5181. http://dx.doi.org/ 10.1128/MCB.22.14.5173-5181.2002.
36. Rubinstein S, Familletti PC, Pestka S. 1981. Convenient assay for interferons. J. Virol. 37:755-758.
37. Volchkov VE, Blinov VM, Netesov SV. 1992. The envelope glycoprotein of Ebola virus contains an immunosuppressive-like domain similar to oncogenic retroviruses. FEBS Lett. 305:181-184. http://dx.doi.org/ 10.1016/0014-5793(92)80662-Z.
38. Gramberg T, Hofmann H, Möller P, Lalor PF, Marzi A, Geier M, Krumbiegel M, Winkler T, Kirchhoff F, Adams DH, Becker S, Münch J, Pöhlmann S. 2005. LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus. Virology 340:224-236. http:// dx.doi.org/10.1016/j.virol.2005.06.026.
39. Becker S, Spiess M, Klenk HD. 1995. The asialoglycoprotein receptor is a potential liver-specific receptor for Marburg virus. J. Gen. Virol. 76(Pt 2):393-399. http://dx.doi.org/10.1099/0022-1317-76-2-393.
40. Ritchie G, Harvey DJ, Stroeher U, Feldmann F, Feldmann H, Wahl-Jensen V, Royle L, Dwek RA, Rudd PM. 2010. Identification of N-glycans from Ebola virus glycoproteins by matrix-assisted laser desorption/ionisation time-of-flight and negative ion electrospray tandem mass spectrometry. Rapid Commun. Mass Spectrom. 24:571-585. http://dx.doi.org/10.1002/rcm.4410.
41. Croset A, Delafosse L, Gaudry JP, Arod C, Glez L, Losberger C, Begue D, Krstanovic A, Robert F, Vilbois F, Chevalet L, Antonsson B. 2012. Differences in the glycosylation of recombinant proteins expressed in HEK and CHO cells. J. Biotechnol. 161:336-348. http://dx.doi.org/ 10.1016/j.jbiotec.2012.06.038.
42. Zampieri CA, Fortin JF, Nolan GP, Nabel GJ. 2007. The ERK mitogenactivated protein kinase pathway contributes to Ebola virus glycoproteininduced cytotoxicity. J. Virol. 81:1230-1240. http://dx.doi.org/10.1128/ JVI.01586-06.
43. Bhattacharyya S, Hope TJ. 2011. Full-length Ebola glycoprotein accumulates in the endoplasmic reticulum. Virol. J. 8:11. http://dx.doi.org/ 10.1186/1743-422X-8-11.
44. Krueger RL, Albritton LM. 2013. Characteristics of the cellular receptor influence the intracellular fate and efficiency of virus infection. J. Virol. 87:5916-5925. http://dx.doi.org/10.1128/JVI.00398-13.
45. Carette JE, Raaben M, Wong AC, Herbert AS, Obernosterer G, Mulherkar N, Kuehne AI, Kranzusch PJ, Griffin AM, Ruthel G, Dal Cin P, Dye JM, Whelan SP, Chandran K, Brummelkamp TR. 2011. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477: 340-343. http://dx.doi.org/10.1038/nature10348.
46. Misasi J, Chandran K, Yang JY, Considine B, Filone CM, Côté M, Sullivan N, Fabozzi G, Hensley L, Cunningham J. 2012. Filoviruses require endosomal cysteine proteases for entry but exhibit distinct protease preferences. J. Virol. 86:3284-3292. http://dx.doi.org/10.1128/ JVI.06346-11.
47. Wang YV, Wade M, Wong E, Li YC, Rodewald LW, Wahl GM. 2007. Quantitative analyses reveal the importance of regulated Hdmx degradation for p53 activation. Proc. Natl. Acad. Sci. U. S. A. 104:12365-12370. http://dx.doi.org/10.1073/pnas.0701497104.