Most neutralizing human monoclonal antibodies target novel epitopes requiring both Lassa virus glycoprotein subunits

Nature Communications

Volumn 7, Issue , 2016, Pages

  Robinson, James E ^a   Hastie, Kathryn M ^b   Cross, Robert W ^c   Yenni, Rachael E ^a   Elliott, Deborah H ^a   Rouelle, Julie A ^a   Kannadka, Chandrika B ^a   Smira, Ashley A ^a   Garry, Courtney E ^a,d   Bradley, Benjamin T ^a   Yu, Haini ^a   Shaffer, Jeffrey G ^e   Boisen, Matt L ^f   Hartnett, Jessica N ^a   Zandonatti, Michelle A ^b   Rowland, Megan M ^g   Heinrich, Megan L ^g   Martinez Sobrido, Luis ^h   Cheng, Benson ^h   De La Torre, Juan C ^b   Andersen, Kristian G ^b,i   Goba, Augustine ^j   Momoh, Mambu ^j,k   Fullah, Mohamed ^j,k   Gbakie, Michael ^j   Kanneh, Lansana ^j   Koroma, Veronica J ^j   Fonnie, Richard ^j   Jalloh, Simbirie C ^j   Kargbo, Brima ^l   Vandi, Mohamed A ^j,l   Gbetuwa, Momoh ^j,l   Ikponmwosa, Odia ^m   Asogun, Danny A ^m   Okokhere, Peter O ^m   Follarin, Onikepe A ^m,n   Schieffelin, John S ^a   Pitts, Kelly R ^f   Geisbert, Joan B ^c   Kulakoski, Peter C ^d   Wilson, Russell B ^d   Happi, Christian T ^m,n   Sabeti, Pardis C ^o,p,q   Gevao, Sahr M ^r   Khan, S Humarr ^j,l   Grant, Donald S ^j,l   Geisbert, Thomas W ^c   Saphire, Erica Ollmann ^b   Branco, Luis M ^g   Garry, Robert F ^a,g   more..

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d Autoimmune Technologies LLC   (United States)

^e TULANE UNIVERSITY   (United States)

^f Division of Medicine   (United States)

^g Zalgen Labs   (United States)

^h UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

ⁱ SCRIPPS TRANSLATIONAL SCIENCE INSTITUTE   (United States)

^j Kenema Government Hospital   (Sierra Leone)

^k Polytechnic College   (Sierra Leone)

^l MINISTRY OF HEALTH AND SANITATION   (Sierra Leone)

^m IRRUA SPECIALIST TEACHING HOSPITAL   (Nigeria)

ⁿ REDEEMER S UNIVERSITY   (Nigeria)

^o HARVARD UNIVERSITY   (United States)

^p BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^q HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^r UNIVERSITY OF SIERRA LEONE   (Sierra Leone)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HUMAN MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; VIRUS FUSION PROTEIN; VIRUS GLYCOPROTEIN; GLYCOPROTEIN GP1, LASSA VIRUS; GLYCOPROTEIN GP2, LASSA VIRUS; MONOCLONAL ANTIBODY; VIRUS ANTIBODY; VIRUS ANTIGEN; VIRUS ENVELOPE PROTEIN;

ANTIBODY; CELLS AND CELL COMPONENTS; DISEASE; HUMAN ACTIVITY; PROTEIN; VACCINE; VIRUS;

ARTICLE; BINDING AFFINITY; CELL LYSATE; COMPLEMENTARITY DETERMINING REGION; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; HEAVY CHAIN; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; LASSA FEVER; LASSA VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY CELL; NEW WORLD ARENAVIRUS; ONTOGENY; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN GLYCOSYLATION; PROTEIN SUBUNIT; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; SMEAR; SURVIVOR; WESTERN BLOTTING; ANTIBODY SPECIFICITY; ARENAVIRIDAE; CHEMISTRY; GENE DELETION; GENETICS; IMMUNOLOGY; MOLECULAR MODEL;

WEST AFRICA;

LASSA VIRUS;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; ANTIGENS, VIRAL; ARENAVIRUS; CROSS REACTIONS; EPITOPE MAPPING; EPITOPES; HUMANS; LASSA FEVER; LASSA VIRUS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; SEQUENCE DELETION; VIRAL ENVELOPE PROTEINS;

EID: 84968627164     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11544     Document Type: Article

References (50)

1. Monath, T. P., Newhouse, V. F., Kemp, G. E., Setzer, H. W., & Cacciapuoti, A. Lassa virus isolation from Mastomys natalensis rodents during an epidemic in Sierra Leone. Science 185, 263-265 (1974).
2. Richmond, J. K., & Baglole, D. J. Lassa fever: epidemiology, clinical features, and social consequences. BMJ 327, 1271-1275 (2003).
3. Andersen, K. G., et al. Clinical sequencing uncovers origins and evolution of Lassa virus. Cell 162, 738-750 (2015).
4. Ehichioya, D. U., et al. Current molecular epidemiology of Lassa virus in Nigeria. J. Clin. Microbiol. 49, 1157-1161 (2011).
5. Shaffer, J. G., et al. Lassa fever in post-conflict Sierra Leone. PLoS Negl. Trop. Dis. 8, e2748 (2014).
6. Cohen, J. Unfilled vials. Science 351, 16-19 (2016).
7. Hashiguchi, T., et al. Structural basis for Marburg virus neutralization by a cross-reactive human antibody. Cell 160, 904-912 (2015).
8. Lee, J. E., et al. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454, 177-182 (2008).
9. Xu, R., et al. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328, 357-360 (2010).
10. Correia, B. E., et al. Proof of principle for epitope-focused vaccine design. Nature 507, 201-206 (2014).
11. Zhu, Z., et al. Human monoclonal antibodies as candidate therapeutics against emerging viruses and HIV-1. Virol. Sin. 28, 71-80 (2013).
12. York, J., & Nunberg, J. H. A novel zinc-binding domain is essential for formation of the functional Junin virus envelope glycoprotein complex. J. Virol. 81, 13385-13391 (2007).
13. Messina, E. L., York, J., & Nunberg, J. H. Dissection of the role of the stable signal peptide of the arenavirus envelope glycoprotein in membrane fusion. J. Virol. 86, 6138-6145 (2012).
14. Hastie, K. M., et al. Crystal structure of the prefusion surface glycoprotein of the prototypic arenavirus LCMV. Nat. Struct. Mol. Biol, doi:10.1038/nsmb.3210 (2016).
15. Igonet, S., et al. X-ray structure of the arenavirus glycoprotein GP2 in its postfusion hairpin conformation. Proc. Natl Acad. Sci. USA 108, 19967-19972 (2011).
16. Cohen-Dvashi, H., Cohen, N., Israeli, H., & Diskin, R. Molecular mechanism for LAMP1 recognition by Lassa virus. J. Virol. 89, 7584-7592 (2015).
17. Sommerstein, R., et al. Arenavirus glycan shield promotes neutralizing antibody evasion and protracted infection. PLoS Pathog. 11, e1005276 (2015).
18. Blattner, C., et al. Structural delineation of a quaternary, cleavage-dependent epitope at the gp41-gp120 interface on intact HIV-1 Env trimers. Immunity 40, 669-680 (2014).
19. Bruns, M., Cihak, J., Muller, G., & Lehmann-Grube, F. Lymphocytic choriomeningitis virus. VI. Isolation of a glycoprotein mediating neutralization. Virology 130, 247-251 (1983).
20. Weber, E. L., & Buchmeier, M. J. Fine mapping of a peptide sequence containing an antigenic site conserved among arenaviruses. Virology 164, 30-38 (1988).
21. Eschli, B., et al. Early antibodies specific for the neutralizing epitope on the receptor binding subunit of the lymphocytic choriomeningitis virus glycoprotein fail to neutralize the virus. J. Virol. 81, 11650-11657 (2007).
22. Ruo, S. L., et al. Antigenic relatedness between arenaviruses defined at the epitope level by monoclonal antibodies. J. Gen. Virol. 72, 549-555 (1991).
23. Buchmeier, M. J., Southern, P. J., Parekh, B. S., Wooddell, M. K., & Oldstone, M. B. Site-specific antibodies define a cleavage site conserved among arenavirus GP-C glycoproteins. J. Virol. 61, 982-985 (1987).
24. Parekh, B. S., & Buchmeier, M. J. Proteins of lymphocytic choriomeningitis virus: antigenic topography of the viral glycoproteins. Virology 153, 168-178 (1986).
25. Seiler, P., et al. In vivo selection of neutralization-resistant virus variants but no evidence of B cell tolerance in lymphocytic choriomeningitis virus carrier mice expressing a transgenic virus-neutralizing antibody. J. Immunol. 162, 4536-4541 (1999).
26. York, J., et al. An antibody directed against the fusion peptide of Junin virus envelope glycoprotein GPC inhibits pH-induced membrane fusion. J. Virol. 84, 6119-6129 (2010).
27. Mahmutovic, S., et al. Molecular basis for antibody-mediated neutralization of new world hemorrhagic fever Mammarenaviruses. Cell Host Microbe 18, 705-713 (2015).
28. McCormick, J. B., et al. Lassa fever. Effective therapy with ribavirin. N. Engl. J. Med. 314, 20-26 (1986).
29. Enria, D. A., Briggiler, A. M., Fernandez, N. J., Levis, S. C., & Maiztegui, J. I. Importance of dose of neutralising antibodies in treatment of Argentine haemorrhagic fever with immune plasma. Lancet 2, 255-256 (1984).
30. Jahrling, P. B., & Peters, C. J. Passive antibody therapy of Lassa fever in cynomolgus monkeys: importance of neutralizing antibody and Lassa virus strain. Infect. Immun. 44, 528-533 (1984).
31. Wei, X., et al. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46, 1896-1905 (2002).
32. Luo, X. M., et al. Engineering human hematopoietic stem/progenitor cells to produce a broadly neutralizing anti-HIV antibody after in vitro maturation to human B lymphocytes. Blood 113, 1422-1431 (2009).
33. Costin, J. M., et al. Mechanistic study of broadly neutralizing human monoclonal antibodies against dengue virus that target the fusion loop. J. Virol. 87, 52-66 (2013).
34. Kong, R., et al. Epitope mapping of broadly neutralizing HIV-2 human monoclonal antibodies. J. Virol. 86, 12115-12128 (2012).
35. Liao, H. X., et al. High-Throughput isolation of immunoglobulin genes from single human B cells and expression as monoclonal antibodies. J. Virol. Methods 158, 171-179 (2009).
36. Smith, K., et al. Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat. Protoc. 4, 372-384 (2009).
37. Guan, Y., et al. Discordant memory B cell and circulating anti-Env antibody responses in HIV-1 infection. Proc. Natl Acad. Sci. USA 106, 3952-3957 (2009).
38. Lee, K. J., Perez, M., Pinschewer, D. D., & de la Torre, J. C. Identification of the lymphocytic choriomeningitis virus (LCMV) proteins required to rescue LCMV RNA analogs into LCMV-like particles. J. Virol. 76, 6393-6397 (2002).
39. Illick, M. M., et al. Uncoupling GP1 and GP2 expression in the Lassa virus glycoprotein complex: implications for GP1 ectodomain shedding. Virol J. 5, 161 (2008).
40. Benoit, R. M., Wilhelm, R. N., Scherer-Becker, D., & Ostermeier, C. An improved method for fast, robust, and seamless integration of DNA fragments into multiple plasmids. Protein Expr. Purif. 45, 66-71 (2006).
41. Rodrigo, W. W., de la Torre, J. C., & Martinez-Sobrido, L. Use of single-cycle infectious lymphocytic choriomeningitis virus to study hemorrhagic fever arenaviruses. J. Virol. 85, 1684-1695 (2011).
42. Bontjer, I., et al. Comparative immunogenicity of Evolved V1V2-deleted HIV-1 envelope glycoprotein trimers. PLoS ONE 8, e67484 (2013).
43. Wyatt, R., et al. Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding. J. Virol. 69, 5723-5733 (1995).
44. Liu, H., & Naismith, J. H. An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol. 8, 91 (2008).
45. Wei, X., et al. Antibody neutralization and escape by HIV-1. Nature 422, 307-312 (2003).
46. Robinson, J. E., et al. Quaternary epitope specificities of anti-HIV-1 neutralizing antibodies generated in rhesus macaques infected by the simian/human immunodeficiency virus SHIVSF162P4. J. Virol. 84, 3443-3453 (2010).
47. Jahrling, P. B., Smith, S., Hesse, R. A., & Rhoderick, J. B. Pathogenesis of Lassa virus infection in guinea pigs. Infect. Immun. 37, 771-778 (1982).
48. Biasini, M., et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42, W252-W258 (2014).
49. Emsley, P., & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
50. Alamyar, E., Duroux, P., Lefranc, M. P., & Giudicelli, V. IMGT((R)) tools for the nucleotide analysis of immunoglobulin (IG) and T cell receptor (TR) V-(D)-J repertoires, polymorphisms, and IG mutations: IMGT/V-QUEST and IMGT/HighV-QUEST for NGS. Methods Mol. Biol. 882, 569-604 (2012).