Combinatorial peptide-based epitope mapping from Ebola virus DNA vaccines and infections reveals residue-level determinants of antibody binding

References

• Kuhn JH. Filoviruses. A compendium of 40 years of epidemiological, clinical, and laboratory studies. Arch Virol Suppl 2008;20:13-360. PMID:18637412
   PubMedGoogle Scholar
• World Health Organization. 2016 Ebola virus disease Fact Sheet. Retrieved from http://www.who.int/mediacentre/factsheets/fs103/en/.
   Google Scholar
• Olinger GG, Jr, Pettitt J, Kim D, Working C, Bohorov O, Bratcher B, Hiatt E, Hume SD, Johnson AK, Morton J, et al. Delayed treatment of Ebola virus infection with plant-derived monoclonal antibodies provides protection in rhesus macaques. Proc Natl Acad Sci U S A. 2012;109(44):18030-5. doi:10.1073/pnas.1213709109. PMID:23071322
   PubMed Web of Science ®Google Scholar
• Qiu X, Audet J, Wong G, Pillet S, Bello A, Cabral T, Strong JE, Plummer F, Corbett CR, Alimonti JB, et al. Successful treatment of ebola virus-infected cynomolgus macaques with monoclonal antibodies. Sci Transl Med. 2012;4(138):3003876. doi:10.1126/scitranslmed.3003876
   Web of Science ®Google Scholar
• Qiu X, Wong G, Audet J, Bello A, Fernando L, Alimonti JB, Fausther-Bovendo H, Wei H, Aviles J, Hiatt E, et al. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature. 2014;514(7520):47-53. PMID:25171469
   PubMed Web of Science ®Google Scholar
• Lee JE, Fusco ML, Hessell AJ, Oswald WB, Burton DR, Saphire EO. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature. 2008;454(7201):177-82. doi:10.1038/nature07082. PMID:18615077
   PubMed Web of Science ®Google Scholar
• Murin CD, Fusco ML, Bornholdt ZA, Qiu X, Olinger GG, Zeitlin L, Kobinger GP, Ward AB, Saphire EO. Structures of protective antibodies reveal sites of vulnerability on Ebola virus. Proc Natl Acad Sci U S A. 2014;111(48):17182-7. doi:10.1073/pnas.1414164111. PMID:25404321
   PubMed Web of Science ®Google Scholar
• Pallesen J, Murin CD, de Val N, Cottrell CA, Hastie KM, Turner HL, Fusco ML, Flyak AI, Zeitlin L, Crowe JE, Jr, et al. Structures of Ebola virus GP and sGP in complex with therapeutic antibodies. Nat Microbiol. 2016;1(9):16128. doi:10.1038/nmicrobiol.2016.128
   PubMed Web of Science ®Google Scholar
• Tran EE, Nelson EA, Bonagiri P, Simmons JA, Shoemaker CJ, Schmaljohn CS, Kobinger GP, Zeitlin L, Subramaniam S, White JM. Mapping of ebolavirus neutralization by monoclonal antibodies in the ZMapp cocktail using cryo-electron tomography and studies of cellular entry. J Virol. 2016;90(17):7618-27. doi:10.1128/JVI.00406-16. PMID:27279622
   PubMed Web of Science ®Google Scholar
• Bornholdt ZA, Turner HL, Murin CD, Li W, Sok D, Souders CA, Piper AE, Goff A, Shamblin JD, Wollen SE, et al.. Isolation of potent neutralizing antibodies from a survivor of the 2014 Ebola virus outbreak. Science. 2016;351(6277):1078-83. doi:10.1126/science.aad5788. PMID:26912366
   PubMed Web of Science ®Google Scholar
• Misasi J, Gilman MS, Kanekiyo M, Gui M, Cagigi A, Mulangu S, Corti D, Ledgerwood JE, Lanzavecchia A, Cunningham J, et al.. Structural and molecular basis for Ebola virus neutralization by protective human antibodies. Science. 2016;351(6279):1343-6. doi:10.1126/science.aad6117. PMID:26917592
   PubMed Web of Science ®Google Scholar
• Zhang Q, Gui M, Niu X, He S, Wang R, Feng Y, Kroeker A, Zuo Y, Wang H, Wang Y, et al.. Potent neutralizing monoclonal antibodies against Ebola virus infection. Sci Rep. 2016;6:25856. doi:10.1038/srep25856. PMID:27181584
   PubMed Web of Science ®Google Scholar
• Cerino A, Bremer CM, Glebe D, Mondelli MU. A human monoclonal antibody against Hepatitis B surface antigen with potent neutralizing activity. PLoS One 2015;10:4. doi:10.1371/journal.pone.0125704
   Web of Science ®Google Scholar
• Read AJ, Casey JL, Coley AM, Foley M, Gauci CG, Jackson DC, Lightowlers MW. Isolation of antibodies specific to a single conformation-dependant antigenic determinant on the EG95 hydatid vaccine. Vaccine. 2009;27(7):1024-31. doi:10.1016/j.vaccine.2008.11.096. PMID:19095030
   PubMed Web of Science ®Google Scholar
• Kuwata T, Takaki K, Yoshimura K, Enomoto I, Wu F, Ourmanov I, Hirsch VM, Yokoyama M, Sato H, Matsushita S. Conformational epitope consisting of the V3 and V4 loops as a target for potent and broad neutralization of simian immunodeficiency viruses. J Virol. 2013;87(10):5424-36. doi:10.1128/JVI.00201-13. PMID:23468483
   PubMed Web of Science ®Google Scholar
• Varshney AK, Wang X, Cook E, Dutta K, Scharff MD, Goger MJ, Fries BC. Generation, characterization, and epitope mapping of neutralizing and protective monoclonal antibodies against staphylococcal enterotoxin B-induced lethal shock. J Biol Chem. 2011;286(11):9737-47. doi:10.1074/jbc.M110.212407. PMID:21233204
   PubMed Web of Science ®Google Scholar
• Hou VC, Moe GR, Raad Z, Wuorimaa T, Granoff DM. Conformational epitopes recognized by protective anti-neisserial surface protein A antibodies. Infect Immun. 2003;71(12):6844-9. doi:10.1128/IAI.71.12.6844-6849.2003. PMID:14638771
   PubMed Web of Science ®Google Scholar
• Wild MA, Xin H, Maruyama T, Nolan MJ, Calveley PM, Malone JD, Wallace MR, Bowdish KS. Human antibodies from immunized donors are protective against anthrax toxin in vivo. Nat Biotechnol. 2003;21(11):1305-6. doi:10.1038/nbt891. PMID:14555959
   PubMed Web of Science ®Google Scholar
• Woollard DJ, Gauci CG, Heath DD, Lightowlers MW. Protection against hydatid disease induced with the EG95 vaccine is associated with conformational epitopes. Vaccine. 2000;19(4-5):498-507. doi:10.1016/S0264-410X(00)00192-4. PMID:11027814
   PubMed Web of Science ®Google Scholar
• Timmerman P, Beld J, Puijk WC, Meloen RH. Rapid and quantitative cyclization of multiple peptide loops onto synthetic scaffolds for structural mimicry of protein surfaces. Chembiochem. 2005;6(5):821-4. doi:10.1002/cbic.200400374. PMID:15812852
   PubMed Web of Science ®Google Scholar
• Mitchell DAJ, Dupuy LC, Sanchez-Lockhart M, Palacios G, Back JW, Shimanovskaya K, Chaudhury S, Ripoll DR, Anders Wallqvist A, Schmaljohn CS. Epitope mapping of Ebola virus dominant and subdominant glycoprotein epitopes facilitates construction of an epitope-based DNA vaccine able to focus the antibody response in mice. Hum Vaccin Immunother 2017 Jul 12:0. [Epub ahead of print]; doi:10.1080/21645515.2017.1347740.
   Google Scholar
• Wilson JA, Hevey M, Bakken R, Guest S, Bray M, Schmaljohn AL, Hart MK. Epitopes involved in antibody-mediated protection from Ebola virus. Science. 2000;287(5458):1664-6. doi:10.1126/science.287.5458.1664. PMID:10698744
   PubMed Web of Science ®Google Scholar
• Dowling W, Thompson E, Badger C, Mellquist JL, Garrison AR, Smith JM, Paragas J, Hogan RJ, Schmaljohn C. Influences of glycosylation on antigenicity, immunogenicity, and protective efficacy of ebola virus GP DNA vaccines. J Virol. 2007;81(4):1821-37. doi:10.1128/JVI.02098-06. PMID:17151111
   PubMed Web of Science ®Google Scholar
• Shedlock DJ, Bailey MA, Popernack PM, Cunningham JM, Burton DR, Sullivan NJ. Antibody-mediated neutralization of Ebola virus can occur by two distinct mechanisms. Virology. 2010;401(2):228-35. doi:10.1016/j.virol.2010.02.029. PMID:20304456
   PubMed Web of Science ®Google Scholar
• Davidson E, Bryan C, Fong RH, Barnes T, Pfaff JM, Mabila M, Rucker JB, Doranz BJ. Mechanism of binding to ebola virus Glycoprotein by the ZMapp, ZMAb, and MB-003 cocktail antibodies. J Virol. 2015;89(21):10982-92. doi:10.1128/JVI.01490-15. PMID:26311869
   PubMed Web of Science ®Google Scholar
• Kugelman JR, Kugelman-Tonos J, Ladner JT, Pettit J, Keeton CM, Nagle ER, Garcia KY, Froude JW, Kuehne AI, Kuhn JH, et al.. Emergence of ebola virus escape variants in infected nonhuman primates treated with the MB-003 antibody cocktail. Cell Rep. 2015;12(12):2111-20. doi:10.1016/j.celrep.2015.08.038. PMID:26365189
   PubMed Web of Science ®Google Scholar
• Lawson CL, Baker ML, Best C, Bi C, Dougherty M, Feng P, van Ginkel G, Devkota B, Lagerstedt I, Ludtke SJ, et al.. EMDataBank.org: unified data resource for CryoEM. Nucleic Acids Res. 2011;39(Database issue):D456-64
   PubMedGoogle Scholar
• O'Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, Rajput B, Robbertse B, Smith-White B, Ako-Adjei D, et al.. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 2016;44(D1):D733-45. doi:10.1093/nar/gkv1189
   PubMedGoogle Scholar
• Ponomarenko J, Vaughan K, Sette A, Maurer-Stroh S. Conservancy of mAb Epitopes in Ebolavirus Glycoproteins of Previous and 2014 Outbreaks. PLoS Curr. 2014;6. pii: ecurrents.outbreaks.f1a7028a13ce1c5f0bdbb4b0cc0b919b. doi:10.1371/currents.outbreaks.f1a7028a13ce1c5f0bdbb4b0cc0b919b
   PubMedGoogle Scholar
• Larsen RJ, Marx ML. An Introduction to mathematical statistics and Its applications. 3rd ed. Upper Saddle River, NJ: Prentice Hall. 2002:p. 282. ISBN 0-13-922303-7.
   Google Scholar
• Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792-7. doi:10.1093/nar/gkh340. PMID:15034147
   PubMed Web of Science ®Google Scholar
• Lee MS, Bondugula R, Desai V, Zavaljevski N, Yeh IC, Wallqvist A, Reifman J. PSPP: a protein structure prediction pipeline for computing clusters. PLoS One. 2009;4:e6254. doi:10.1371/journal.pone.0006254. PMID:19606223
   PubMed Web of Science ®Google Scholar
• Warfield KL, Swenson DL, Olinger GG, Nichols DK, Pratt WD, Blouch R, Stein DA, Aman MJ, Iversen PL, Bavari S. Gene-specific countermeasures against Ebola virus based on antisense phosphorodiamidate morpholino oligomers. PLoS Pathog. 2006;2(1):e1. doi:10.1371/journal.ppat.0020001. PMID:16415982
   PubMed Web of Science ®Google Scholar
• Geisbert TW, Hensley LE, Jahrling PB, Larsen T, Geisbert JB, Paragas J, Young HA, Fredeking TM, Rote WE, Vlasuk GP. Treatment of Ebola virus infection with a recombinant inhibitor of factor VIIa/tissue factor: a study in rhesus monkeys. Lancet. 2003;362(9400):1953-8. doi:10.1016/S0140-6736(03)15012-X. PMID:14683653
   PubMed Web of Science ®Google Scholar
• Grant-Klein RJ, Van Deusen NM, Badger CV, Hannaman D, Dupuy LC, Schmaljohn CS. A multiagent filovirus DNA vaccine delivered by intramuscular electroporation completely protects mice from ebola and Marburg virus challenge. Hum Vaccin Immunother. 2012;8(11):1703-6. doi:10.4161/hv.21873. PMID:22922764
   PubMed Web of Science ®Google Scholar
• Pushko P, Bray M, Ludwig GV, Parker M, Schmaljohn A, Sanchez A, Jahrling PB, Smith JF. Recombinant RNA replicons derived from attenuated Venezuelan equine encephalitis virus protect guinea pigs and mice from Ebola hemorrhagic fever virus. Vaccine. 2000;19(1):142-53. doi:10.1016/S0264-410X(00)00113-4. PMID:10924796
   PubMed Web of Science ®Google Scholar
• Geisbert TW, Pushko P, Anderson K, Smith J, Davis KJ, Jahrling PB. Evaluation in nonhuman primates of vaccines against Ebola virus. Emerg Infect Dis. 2002;8(5):503-7. doi:10.3201/eid0805.010284. PMID:11996686
   PubMed Web of Science ®Google Scholar
• Lee JE, Kuehne A, Abelson DM, Fusco ML, Hart MK, Saphire EO. Complex of a protective antibody with its Ebola virus GP peptide epitope: unusual features of a V lambda x light chain. J Mol Biol. 2008;375(1):202-16. doi:10.1016/j.jmb.2007.10.017. PMID:18005986
   PubMed Web of Science ®Google Scholar
• Olal D, Kuehne AI, Bale S, Halfmann P, Hashiguchi T, Fusco ML, Lee JE, King LB, Kawaoka Y, Dye JM, Jr, et al.. Structure of an antibody in complex with its mucin domain linear epitope that is protective against Ebola virus. J Virol. 2012;86(5):2809-16. doi:10.1128/JVI.05549-11. PMID:22171276
   PubMed Web of Science ®Google Scholar
• Bale S, Dias JM, Fusco ML, Hashiguchi T, Wong AC, Liu T, Keuhne AI, Li S, Woods VL, Jr, Chandran K, et al.. Structural basis for differential neutralization of ebolaviruses. Viruses. 2012;4(4):447-70. doi:10.3390/v4040447. PMID:22590681
   PubMed Web of Science ®Google Scholar