Importance of neutralizing monoclonal antibodies targeting multiple antigenic sites on the Middle East respiratory syndrome coronavirus spike glycoprotein to avoid neutralization escape

Journal of Virology

Volumn 92, Issue 10, 2018, Pages

  Wang, Lingshu ^a   Shi, Wei ^a   Chappell, James D ^b   Joyce, M Gordon ^a,f   Zhang, Yi ^a   Kanekiyo, Masaru ^a   Becker, Michelle M ^b   Doremalen, Neeltje van ^c   Fischer, Robert ^c   Wang, Nianshuang ^d   Corbett, Kizzmekia S ^a   Choe, Misook ^a   Mason, Rosemarie D ^a   Van Galen, Joseph G ^a   Zhou, Tongqing ^a   Saunders, Kevin O ^a,g   Tatti, Kathleen M ^e   Haynes, Lia M ^e   Kwong, Peter D ^a   Modjarrad, Kayvon ^a   Kong, Wing Pui ^a   McLellan, Jason S ^d   Denison, Mark R ^b   Munster, Vincent J ^c   Mascola, John R ^a   Graham, Barney S ^a   more..

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d DARTMOUTH MEDICAL SCHOOL   (United States)

^e NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^f WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^g DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Escape mutation; MERS CoV; Monoclonal antibody; Protection; RBD; S1

Indexed keywords

CORONAVIRUS SPIKE GLYCOPROTEIN; DNA VACCINE; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRAL PROTEIN S1; VIRUS VACCINE; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY COMBINING SITE; ANTIBODY STRUCTURE; ANTIGEN BINDING; ARTICLE; BINDING SITE; CELL ASSAY; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; IMMUNIZATION; LUNG INFECTION; MIDDLE EAST RESPIRATORY SYNDROME; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR BINDING; RHESUS MONKEY; STRUCTURE ANALYSIS; VIRUS ESCAPE ASSAY; VIRUS NEUTRALIZATION; VIRUS REPLICATION; ANIMAL; CHEMISTRY; CORONAVIRUS INFECTION; IMMUNOLOGY; METABOLISM; VACCINATION; X RAY CRYSTALLOGRAPHY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CORONAVIRUS INFECTIONS; CRYSTALLOGRAPHY, X-RAY; HUMANS; MACACA MULATTA; MICE; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; SPIKE GLYCOPROTEIN, CORONAVIRUS; VACCINATION;

EID: 85046008693     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.002002-17     Document Type: Article

References (69)

1. Durai P, Batool M, Shah M, Choi S. 2015. Middle East respiratory syndrome coronavirus: transmission, virology and therapeutic targeting to aid in outbreak control. Exp Mol Med 47:e181. https://doi.org/10.1038/ emm.2015.76
2. Assiri A, McGeer A, Perl TM, Price CS, Al Rabeeah AA, Cummings DA, Alabdullatif ZN, Assad M, Almulhim A, Makhdoom H, Madani H, Alhakeem R, Al-Tawfiq JA, Cotten M, Watson SJ, Kellam P, Zumla AI, Memish ZA, Team KM-CI. 2013. Hospital outbreak of Middle East respiratory syndrome coronavirus. N Engl J Med 369:407-416. https://doi.org/10 .1056/NEJMoa1306742
3. Assiri A, Al-Tawfiq JA, Al-Rabeeah AA, Al-Rabiah FA, Al-Hajjar S, Al-Barrak A, Flemban H, Al-Nassir WN, Balkhy HH, Al-Hakeem RF, Makhdoom HQ, Zumla AI, Memish ZA. 2013. Epidemiological, demographic, and clinical characteristics of 47 cases of Middle East respiratory syndrome coronavirus disease from Saudi Arabia: a descriptive study. Lancet Infect Dis 13:752-761. https://doi.org/10.1016/S1473-3099(13)70204-4
4. Breban R, Riou J, Fontanet A. 2013. Interhuman transmissibility of Middle East respiratory syndrome coronavirus: estimation of pandemic risk. Lancet 382:694-699. https://doi.org/10.1016/S0140-6736(13)61492-0
5. Cauchemez S, Fraser C, Van Kerkhove MD, Donnelly CA, Riley S, Rambaut A, Enouf V, van der Werf S, Ferguson NM. 2014. Middle East respiratory syndrome coronavirus: quantification of the extent of the epidemic surveillance biases, and transmissibility. Lancet Infect Dis 14:50-56. https://doi.org/10.1016/S1473-3099(13)70304-9
6. Memish ZA, Cotten M, Meyer B, Watson SJ, Alsahafi AJ, Al Rabeeah AA, Corman VM, Sieberg A, Makhdoom HQ, Assiri A, Al Masri M, Aldabbagh S, Bosch BJ, Beer M, Muller MA, Kellam P, Drosten C. 2014. Human infection with MERS coronavirus after exposure to infected camels, Saudi Arabia, 2013. Emerg Infect Dis 20:1012-1015. https://doi.org/10.3201/ eid2006.140402
7. Graham BS, Ambrosino DM. 2015. History of passive antibody administration for prevention and treatment of infectious diseases. Curr Opin HIV AIDS 10:129-134. https://doi.org/10.1097/COH.0000000000000154
8. Cavanagh D. 1983. Coronavirus IBV: structural characterization of the spike protein. J Gen Virol 64(Part 12):2577-2583
9. Buchholz UJ, Bukreyev A, Yang L, Lamirande EW, Murphy BR, Subbarao K, Collins PL. 2004. Contributions of the structural proteins of severe acute respiratory syndrome coronavirus to protective immunity. Proc Natl Acad Sci U S A 101:9804-9809. https://doi.org/10.1073/pnas .0403492101
10. Lu G, Hu Y, Wang Q, Qi J, Gao F, Li Y, Zhang Y, Zhang W, Yuan Y, Bao J, Zhang B, Shi Y, Yan J, Gao GF. 2013. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 500:227-231. https://doi.org/10.1038/nature12328
11. Wang N, Shi X, Jiang L, Zhang S, Wang D, Tong P, Guo D, Fu L, Cui Y, Liu X, Arledge KC, Chen YH, Zhang L, Wang X. 2013. Structure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4. Cell Res 23:986-993. https://doi.org/10.1038/cr.2013.92
12. Mou H, Raj VS, van Kuppeveld FJ, Rottier PJ, Haagmans BL, Bosch BJ. 2013. The receptor binding domain of the new Middle East respiratory syndrome coronavirus maps to a 231-residue region in the spike protein that efficiently elicits neutralizing antibodies. J Virol 87:9379-9383. https://doi.org/10.1128/JVI.01277-13
13. Pascal KE, Coleman CM, Mujica AO, Kamat V, Badithe A, Fairhurst J, Hunt C, Strein J, Berrebi A, Sisk JM, Matthews KL, Babb R, Chen G, Lai KM, Huang TT, Olson W, Yancopoulos GD, Stahl N, Frieman MB, Kyratsous CA. 2015. Pre-and postexposure efficacy of fully human antibodies against Spike protein in a novel humanized mouse model of MERS-CoV infection. Proc Natl Acad Sci U S A 112:8738-8743. https://doi.org/10.1073/ pnas.1510830112
14. Corti D, Zhao J, Pedotti M, Simonelli L, Agnihothram S, Fett C, Fernandez-Rodriguez B, Foglierini M, Agatic G, Vanzetta F, Gopal R, Langrish CJ, Barrett NA, Sallusto F, Baric RS, Varani L, Zambon M, Perlman S, Lanzavecchia A. 2015. Prophylactic and postexposure efficacy of a potent human monoclonal antibody against MERS coronavirus. Proc Natl Acad Sci U S A 112:10473-10478. https://doi.org/10.1073/pnas .1510199112
15. Li Y, Wan Y, Liu P, Zhao J, Lu G, Qi J, Wang Q, Lu X, Wu Y, Liu W, Zhang B, Yuen KY, Perlman S, Gao GF, Yan J. 2015. A humanized neutralizing antibody against MERS-CoV targeting the receptor-binding domain of the spike protein. Cell Res 25:1237-1249. https://doi.org/10.1038/cr.2015 .113
16. Jiang L, Wang N, Zuo T, Shi X, Poon KM, Wu Y, Gao F, Li D, Wang R, Guo J, Fu L, Yuen KY, Zheng BJ, Wang X, Zhang L. 2014. Potent neutralization of MERS-CoV by human neutralizing monoclonal antibodies to the viral spike glycoprotein. Sci Transl Med 6:234ra259. https://doi.org/10.1126/ scitranslmed.3008140
17. Tang XC, Agnihothram SS, Jiao Y, Stanhope J, Graham RL, Peterson EC, Avnir Y, Tallarico AS, Sheehan J, Zhu Q, Baric RS, Marasco WA. 2014. Identification of human neutralizing antibodies against MERS-CoV and their role in virus adaptive evolution. Proc Natl Acad Sci U S A 111: E2018-E2026. https://doi.org/10.1073/pnas.1402074111
18. Ying T, Du L, Ju TW, Prabakaran P, Lau CC, Lu L, Liu Q, Wang L, Feng Y, Wang Y, Zheng BJ, Yuen KY, Jiang S, Dimitrov DS. 2014. Exceptionally potent neutralization of Middle East respiratory syndrome coronavirus by human monoclonal antibodies. J Virol 88:7796-7805. https://doi.org/ 10.1128/JVI.00912-14
19. Du L, Zhao G, Yang Y, Qiu H, Wang L, Kou Z, Tao X, Yu H, Sun S, Tseng CT, Jiang S, Li F, Zhou Y. 2014. A conformation-dependent neutralizing monoclonal antibody specifically targeting receptor-binding domain in Middle East respiratory syndrome coronavirus spike protein. J Virol 88:7045-7053. https://doi.org/10.1128/JVI.00433-14
20. Wang L, Shi W, Joyce MG, Modjarrad K, Zhang Y, Leung K, Lees CR, Zhou T, Yassine HM, Kanekiyo M, Yang ZY, Chen X, Becker MM, Freeman M, Vogel L, Johnson JC, Olinger G, Todd JP, Bagci U, Solomon J, Mollura DJ, Hensley L, Jahrling P, Denison MR, Rao SS, Subbarao K, Kwong PD, Mascola JR, Kong WP, Graham BS. 2015. Evaluation of candidate vaccine approaches for MERS-CoV. Nat Commun 6:7712. https://doi.org/10 .1038/ncomms8712
21. Chen Y, Lu S, Jia H, Deng Y, Zhou J, Huang B, Yu Y, Lan J, Wang W, Lou Y, Qin K, Tan W. 2017. A novel neutralizing monoclonal antibody targeting the N-terminal domain of the MERS-CoV spike protein. Emerg Microbes Infect 6:e60. https://doi.org/10.1038/emi.2017.50
22. Yu X, Zhang S, Jiang L, Cui Y, Li D, Wang D, Wang N, Fu L, Shi X, Li Z, Zhang L, Wang X. 2015. Structural basis for the neutralization of MERSCoV by a human monoclonal antibody MERS-27. Sci Rep 5:13133. https://doi.org/10.1038/srep13133
23. Ying T, Prabakaran P, Du L, Shi W, Feng Y, Wang Y, Wang L, Li W, Jiang S, Dimitrov DS, Zhou T. 2015. Junctional and allele-specific residues are critical for MERS-CoV neutralization by an exceptionally potent germline-like antibody. Nat Commun 6:8223. https://doi.org/10.1038/ ncomms9223
24. Chen Z, Bao L, Chen C, Zou T, Xue Y, Li F, Lv Q, Gu S, Gao X, Cui S, Wang J, Qin C, Jin Q. 2017. Human neutralizing monoclonal antibody efficiently inhibits MERS-CoV replication in common marmoset. J Infect Dis 215: 1807-1815. https://doi.org/10.1093/infdis/jix209
25. Johnson RF, Bagci U, Keith L, Tang X, Mollura DJ, Zeitlin L, Qin J, Huzella L, Bartos CJ, Bohorova N, Bohorov O, Goodman C, Kim do H, Paulty MH, Velasco J, Whaley KJ, Johnson JC, Pettitt J, Ork BL, Solomon J, Oberlander N, Zhu Q, Sun J, Holbrook MR, Olinger GG, Baric RS, Hensley LE, Jahrling PB, Marasco WA. 2016. 3B11-N, a monoclonal antibody against MERSCoV, reduces lung pathology in rhesus monkeys following intratracheal inoculation of MERS-CoV Jordan-n3/2012. Virology 490:49-58. https:// doi.org/10.1016/j.virol.2016.01.004
26. Houser KV, Gretebeck L, Ying T, Wang Y, Vogel L, Lamirande EW, Bock KW, Moore IN, Dimitrov DS, Subbarao K. 2016. Prophylaxis with a Middle East respiratory syndrome coronavirus (MERS-CoV)-specific human monoclonal antibody protects rabbits from MERS-CoV infection. J Infect Dis 213:1557-1561. https://doi.org/10.1093/infdis/jiw080
27. Sui J, Deming M, Rockx B, Liddington RC, Zhu QK, Baric RS, Marasco WA. 2014. Effects of human anti-spike protein receptor binding domain antibodies on severe acute respiratory syndrome coronavirus neutralization escape and fitness. J Virol 88:13769-13780. https://doi.org/10 .1128/JVI.02232-14
28. Coughlin MM, Prabhakar BS. 2012. Neutralizing human monoclonal antibodies to severe acute respiratory syndrome coronavirus: target, mechanism of action, and therapeutic potential. Rev Med Virol 22:2-17. https://doi.org/10.1002/rmv.706
29. Elshabrawy HA, Coughlin MM, Baker SC, Prabhakar BS. 2012. Human monoclonal antibodies against highly conserved HR1 and HR2 domains of the SARS-CoV spike protein are more broadly neutralizing. PLoS One 7:e50366. https://doi.org/10.1371/journal.pone.0050366
30. Kong R, Louder MK, Wagh K, Bailer RT, deCamp A, Greene K, Gao H, Taft JD, Gazumyan A, Liu C, Nussenzweig MC, Korber B, Montefiori DC, Mascola JR. 2015. Improving neutralization potency and breadth by combining broadly reactive HIV-1 antibodies targeting major neutralization epitopes. J Virol 89:2659-2671. https://doi.org/10 .1128/JVI.03136-14
31. Klein F, Halper-Stromberg A, Horwitz JA, Gruell H, Scheid JF, Bournazos S, Mouquet H, Spatz LA, Diskin R, Abadir A, Zang T, Dorner M, Billerbeck E, Labitt RN, Gaebler C, Marcovecchio PM, Incesu RB, Eisenreich TR, Bieniasz PD, Seaman MS, Bjorkman PJ, Ravetch JV, Ploss A, Nussenzweig MC. 2012. HIV therapy by a combination of broadly neutralizing antibodies in humanized mice. Nature 492:118-122. https://doi.org/10 .1038/nature11604
32. Shingai M, Nishimura Y, Klein F, Mouquet H, Donau OK, Plishka R, Buckler-White A, Seaman M, Piatak M, Jr, Lifson JD, Dimitrov DS, Nussenzweig MC, Martin MA. 2013. Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia. Nature 503:277-280. https://doi.org/10.1038/nature12746
33. Sundling C, Phad G, Douagi I, Navis M, Karlsson Hedestam GB. 2012. Isolation of antibody V(D)J sequences from single cell sorted rhesus macaque B cells. J Immunol Methods 386:85-93. https://doi.org/10 .1016/j.jim.2012.09.003
34. Mason RD, Welles HC, Adams C, Chakrabarti BK, Gorman J, Zhou T, Nguyen R, O'Dell S, Lusvarghi S, Bewley CA, Li H, Shaw GM, Sheng Z, Shapiro L, Wyatt R, Kwong PD, Mascola JR, Roederer M. 2016. Targeted isolation of antibodies directed against major sites of SIV Env vulnerability. PLoS Pathog 12:e1005537. https://doi.org/10.1371/journal.ppat .1005537
35. Lingwood D, McTamney PM, Yassine HM, Whittle JR, Guo X, Boyington JC, Wei CJ, Nabel GJ. 2012. Structural and genetic basis for development of broadly neutralizing influenza antibodies. Nature 489:566-570. https://doi.org/10.1038/nature11371
36. Prabakaran P, Zhu Z, Chen W, Gong R, Feng Y, Streaker E, Dimitrov DS. 2012. Origin, diversity, and maturation of human antiviral antibodies analyzed by high-throughput sequencing. Front Microbiol 3:277. https:// doi.org/10.3389/fmicb.2012.00277
37. Huang CC, Venturi M, Majeed S, Moore MJ, Phogat S, Zhang MY, Dimitrov DS, Hendrickson WA, Robinson J, Sodroski J, Wyatt R, Choe H, Farzan M, Kwong PD. 2004. Structural basis of tyrosine sulfation and VH-gene usage in antibodies that recognize the HIV type 1 coreceptorbinding site on gp120. Proc Natl Acad Sci U S A 101:2706-2711. https:// doi.org/10.1073/pnas.0308527100
38. Pallesen J, Wang N, Corbett KS, Wrapp D, Kirchdoerfer RN, Turner HL, Cottrell CA, Becker MM, Wang L, Shi W, Kong WP, Andres EL, Kettenbach AN, Denison MR, Chappell JD, Graham BS, Ward AB, McLellan JS. 2017. Immunogenicity and structures of a rationally designed prefusion MERSCoV spike antigen. Proc Natl Acad Sci U S A 114:E7348-E7357. https:// doi.org/10.1073/pnas.1707304114
39. van Doremalen N, Falzarano D, Ying T, de Wit E, Bushmaker T, Feldmann F, Okumura A, Wang Y, Scott DP, Hanley PW, Feldmann H, Dimitrov DS, Munster VJ. 2017. Efficacy of antibody-based therapies against Middle East respiratory syndrome coronavirus (MERS-CoV) in common marmosets. Antiviral Res 143:30-37. https://doi.org/10.1016/j.antiviral.2017.03.025
40. Luke T, Wu H, Zhao J, Channappanavar R, Coleman CM, Jiao JA, Matsushita H, Liu Y, Postnikova EN, Ork BL, Glenn G, Flyer D, Defang G, Raviprakash K, Kochel T, Wang J, Nie W, Smith G, Hensley LE, Olinger GG, Kuhn JH, Holbrook MR, Johnson RF, Perlman S, Sullivan E, Frieman MB. 2016. Human polyclonal immunoglobulin G from transchromosomic bovines inhibits MERS-CoV in vivo. Sci Transl Med 8:326ra321. https:// doi.org/10.1126/scitranslmed.aaf1061
41. Zhao J, Perera RA, Kayali G, Meyerholz D, Perlman S, Peiris M. 2015. Passive immunotherapy with dromedary immune serum in an experimental animal model for Middle East respiratory syndrome coronavirus infection. J Virol 89:6117-6120. https://doi.org/10.1128/JVI.00446-15
42. Qiu X, Wong G, Audet J, Bello A, Fernando L, Alimonti JB, Fausther-Bovendo H, Wei H, Aviles J, Hiatt E, Johnson A, Morton J, Swope K, Bohorov O, Bohorova N, Goodman C, Kim D, Pauly MH, Velasco J, Pettitt J, Olinger GG, Whaley K, Xu B, Strong JE, Zeitlin L, Kobinger GP. 2014. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 514:47-53. https://doi.org/10.1038/nature13777
43. Xu L, Pegu A, Rao E, Doria-Rose N, Beninga J, McKee K, Lord DM, Wei RR, Deng G, Louder M, Schmidt SD, Mankoff Z, Wu L, Asokan M, Beil C, Lange C, Leuschner WD, Kruip J, Sendak R, Do Kwon Y, Zhou T, Chen X, Bailer RT, Wang K, Choe M, Tartaglia LJ, Barouch DH, O'Dell S, Todd JP, Burton DR, Roederer M, Connors M, Koup RA, Kwong PD, Yang ZY, Mascola JR, Nabel GJ. 2017. Trispecific broadly neutralizing HIV antibodies mediate potent SHIV protection in macaques. Science 358:85-90. https://doi.org/ 10.1126/science.aan8630
44. Wang J, Bardelli M, Espinosa DA, Pedotti M, Ng TS, Bianchi S, Simonelli L, Lim EXY, Foglierini M, Zatta F, Jaconi S, Beltramello M, Cameroni E, Fibriansah G, Shi J, Barca T, Pagani I, Rubio A, Broccoli V, Vicenzi E, Graham V, Pullan S, Dowall S, Hewson R, Jurt S, Zerbe O, Stettler K, Lanzavecchia A, Sallusto F, Cavalli A, Harris E, Lok SM, Varani L, Corti D. 2017. A human bi-specific antibody against Zika virus with high therapeutic potential. Cell 171:229-241.e215. https://doi.org/10.1016/j.cell .2017.09.002
45. Yuan Y, Cao D, Zhang Y, Ma J, Qi J, Wang Q, Lu G, Wu Y, Yan J, Shi Y, Zhang X, Gao GF. 2017. Cryo-EM structures of MERS-CoV and SARS-CoV spike glycoproteins reveal the dynamic receptor binding domains. Nat Commun 8:15092. https://doi.org/10.1038/ncomms15092
46. Gui M, Song W, Zhou H, Xu J, Chen S, Xiang Y, Wang X. 2017. Cryoelectron microscopy structures of the SARS-CoV spike glycoprotein reveal a prerequisite conformational state for receptor binding. Cell Res 27:119-129. https://doi.org/10.1038/cr.2016.152
47. Gilman MS, Moin SM, Mas V, Chen M, Patel NK, Kramer K, Zhu Q, Kabeche SC, Kumar A, Palomo C, Beaumont T, Baxa U, Ulbrandt ND, Melero JA, Graham BS, McLellan JS. 2015. Characterization of a prefusion-specific antibody that recognizes a quaternary, cleavage-dependent epitope on the RSV fusion glycoprotein. PLoS Pathog 11:e1005035. https://doi.org/ 10.1371/journal.ppat.1005035
48. Kirchdoerfer RN, Cottrell CA, Wang N, Pallesen J, Yassine HM, Turner HL, Corbett KS, Graham BS, McLellan JS, Ward AB. 2016. Pre-fusion structure of a human coronavirus spike protein. Nature 531:118-121. https://doi .org/10.1038/nature17200
49. Barouch DH, Yang ZY, Kong WP, Korioth-Schmitz B, Sumida SM, Truitt DM, Kishko MG, Arthur JC, Miura A, Mascola JR, Letvin NL, Nabel GJ. 2005. A human T-cell leukemia virus type 1 regulatory element enhances the immunogenicity of human immunodeficiency virus type 1 DNA vaccines in mice and nonhuman primates. J Virol 79:8828-8834. https:// doi.org/10.1128/JVI.79.14.8828-8834.2005
50. Catanzaro AT, Roederer M, Koup RA, Bailer RT, Enama ME, Nason MC, Martin JE, Rucker S, Andrews CA, Gomez PL, Mascola JR, Nabel GJ, Graham BS. 2007. Phase I clinical evaluation of a six-plasmid multiclade HIV-1 DNA candidate vaccine. Vaccine 25:4085-4092. https://doi.org/10 .1016/j.vaccine.2007.02.050
51. Naldini L, Blomer U, Gage FH, Trono D, Verma IM. 1996. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci U S A 93:11382-11388
52. Yang ZY, Werner HC, Kong WP, Leung K, Traggiai E, Lanzavecchia A, Nabel GJ. 2005. Evasion of antibody neutralization in emerging severe acute respiratory syndrome coronaviruses. Proc Natl Acad Sci U S A 102:797-801. https://doi.org/10.1073/pnas.0409065102
53. Wu X, Zhou T, Zhu J, Zhang B, Georgiev I, Wang C, Chen X, Longo NS, Louder M, McKee K, O'Dell S, Perfetto S, Schmidt SD, Shi W, Wu L, Yang Y, Yang ZY, Yang Z, Zhang Z, Bonsignori M, Crump JA, Kapiga SH, Sam NE, Haynes BF, Simek M, Burton DR, Koff WC, Doria-Rose NA, Connors M, NISC Comparative Sequencing Program, Mullikin JC, Nabel GJ, Roederer M, Shapiro L, Kwong PD, Mascola JR. 2011. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333:1593-1602. https://doi.org/10.1126/science.1207532
54. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, Longo NS, McKee K, O'Dell S, Louder MK, Wycuff DL, Feng Y, Nason M, Doria-Rose N, Connors M, Kwong PD, Roederer M, Wyatt RT, Nabel GJ, Mascola JR. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861. https://doi.org/10.1126/science.1187659
55. Brochet X, Lefranc MP, Giudicelli V. 2008. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res 36:W503-W508. https://doi .org/10.1093/nar/gkn316
56. Giudicelli V, Brochet X, Lefranc MP. 2011. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb Protoc 2011:695-715. https://doi.org/ 10.1101/pdb.prot5633
57. Kong R, Li H, Georgiev I, Changela A, Bibollet-Ruche F, Decker JM, Rowland-Jones SL, Jaye A, Guan Y, Lewis GK, Langedijk JP, Hahn BH, Kwong PD, Robinson JE, Shaw GM. 2012. Epitope mapping of broadly neutralizing HIV-2 human monoclonal antibodies. J Virol 86: 12115-12128. https://doi.org/10.1128/JVI.01632-12
58. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326. https://doi .org/10.1016/S0076-6879(97)76066-X
59. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG. 2011. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 67(Part 4):271-281. https://doi.org/10.1107/S0907444910048675
60. Evans PR, Murshudov GN. 2013. How good are my data and what is the resolution? Acta Crystallogr D Biol Crystallogr 69(Part 7):1204-1214
61. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40(Part 4):658-674. https://doi.org/10.1107/S0021889807021206
62. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66(Part 1):12-21
63. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Part 12):2126-2132. https://doi.org/10.1107/S0907444904019158
64. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC. 2002. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58(Part 11):1948-1954. https://doi.org/10.1107/S0907444902016657
65. Scobey T, Yount BL, Sims AC, Donaldson EF, Agnihothram SS, Menachery VD, Graham RL, Swanstrom J, Bove PF, Kim JD, Grego S, Randell SH, Baric RS. 2013. Reverse genetics with a full-length infectious cDNA of the Middle East respiratory syndrome coronavirus. Proc Natl Acad Sci U S A 110:16157-16162. https://doi.org/10.1073/pnas.1311542110
66. Office of Laboratory Animal Welfare. 2015. Public Health Service policy on humane care and use of laboratory animals. NIH, Bethesda, MD
67. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC
68. Agrawal AS, Garron T, Tao X, Peng BH, Wakamiya M, Chan TS, Couch RB, Tseng CT. 2015. Generation of a transgenic mouse model of Middle East respiratory syndrome coronavirus infection and disease. J Virol 89: 3659-3670. https://doi.org/10.1128/JVI.03427-14
69. van Doremalen N, Munster VJ. 2015. Animal models of Middle East respiratory syndrome coronavirus infection. Antiviral Res 122:28-38. https://doi.org/10.1016/j.antiviral.2015.07.005