A Potent Germline-like Human Monoclonal Antibody Targets a pH-Sensitive Epitope on H7N9 Influenza Hemagglutinin

Cell Host and Microbe

Volumn 22, Issue 4, 2017, Pages 471-483.e5

  Yu, Fei ^a,c   Song, He ^b   Wu, Yanling ^a   Chang, So Young ^d   Wang, Lili ^a   Li, Wei ^b   Hong, Binbin ^a   Xia, Shuai ^a   Wang, Chunyu ^a   Khurana, Surender ^e   Feng, Yang ^b   Wang, Yanping ^b   Sun, Zhiwu ^a   He, Biao ^a   Hou, Dongni ^a   Manischewitz, Jody ^e   King, Lisa R ^e   Song, Yuanlin ^a   Min, Ji Young ^d   Golding, Hana ^e   Ji, Xinhua ^b   Lu, Lu ^a   Jiang, Shibo ^a   Dimitrov, Dimiter S ^b   Ying, Tianlei ^a   more..

^a FUDAN UNIVERSITY   (China)

^b NATIONAL CANCER INSTITUTE   (United States)

^c AGRICULTURAL UNIVERSITY OF HEBEI   (China)

^d Institute Pasteur Korea   (South Korea)

^e CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

ADCC; germline; H7N9 influenza; hemagglutinin; monoclonal antibody

Indexed keywords

EPITOPE; HUMAN MONOCLONAL ANTIBODY; INFLUENZA VIRUS HEMAGGLUTININ; MONOCLONAL ANTIBODY M826; UNCLASSIFIED DRUG; HEMAGGLUTININ, AVIAN INFLUENZA A VIRUS; INFLUENZA VACCINE; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG POTENCY; DRUG TARGETING; IMMUNOGENICITY; INFLUENZA A VIRUS (H7N9); MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; CONFORMATION; DOG; FEMALE; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; INFLUENZA; MDCK CELL LINE; METABOLISM; ORTHOMYXOVIRUS INFECTION; VIROLOGY;

ANIMALS; ANTIBODIES, MONOCLONAL; DOGS; EPITOPES; FEMALE; HEK293 CELLS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; HYDROGEN-ION CONCENTRATION; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICE, INBRED BALB C; MOLECULAR CONFORMATION; ORTHOMYXOVIRIDAE INFECTIONS;

EID: 85030702561     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.08.011     Document Type: Article

References (67)

1. Agrawal, A.S., Ying, T., Tao, X., Garron, T., Algaissi, A., Wang, Y., Wang, L., Peng, B.H., Jiang, S., Dimitrov, D.S., et al. Passive transfer of A germline-like neutralizing human monoclonal antibody protects transgenic mice against lethal Middle East respiratory syndrome coronavirus infection. Sci. Rep., 6, 2016, 31629.
2. Banerjee, I., Yamauchi, Y., Helenius, A., Horvath, P., High-content analysis of sequential events during the early phase of influenza A virus infection. PLoS One, 8, 2013, e68450.
3. Bernasconi-Elias, P., Hu, T., Jenkins, D., Firestone, B., Gans, S., Kurth, E., Capodieci, P., Deplazes-Lauber, J., Petropoulos, K., Thiel, P., et al. Characterization of activating mutations of NOTCH3 in T-cell acute lymphoblastic leukemia and anti-leukemic activity of NOTCH3 inhibitory antibodies. Oncogene 35 (2016), 6077–6086.
4. Bonsignori, M., Zhou, T.Q., Sheng, Z.Z., Chen, L., Gao, F., Joyce, M.G., Ozorowski, G., Chuang, G.Y., Schramm, C.A., Wiehe, K., et al. Maturation pathway from germline to broad HIV-1 neutralizer of a CD4-mimic antibody. Cell 165 (2016), 449–463.
5. Bossart, K.N., Geisbert, T.W., Feldmann, H., Zhu, Z., Feldmann, F., Geisbert, J.B., Yan, L., Feng, Y.R., Brining, D., Scott, D., et al. A neutralizing human monoclonal antibody protects African green monkeys from Hendra virus challenge. Sci. Transl. Med., 3, 2011, 105ra103.
6. Caton, A.J., Brownlee, G.G., Yewdell, J.W., Gerhard, W., The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 31 (1982), 417–427.
7. Chai, N., Swem, L.R., Park, S., Nakamura, G., Chiang, N., Estevez, A., Fong, R., Kamen, L., Kho, E., Reichelt, M., et al. A broadly protective therapeutic antibody against influenza B virus with two mechanisms of action. Nat. Commun., 8, 2017, 14234.
8. Chen, Z., Wang, J.M., Bao, L.L., Guo, L., Zhang, W.J., Xue, Y., Zhou, H.L., Xiao, Y., Wang, J.W., Wu, F., et al. Human monoclonal antibodies targeting the haemagglutinin glycoprotein can neutralize H7N9 influenza virus. Nat. Commun., 6, 2015, 6714.
9. Cox, F., Kwaks, T., Brandenburg, B., Koldijk, M.H., Klaren, V., Smal, B., Korse, H.J., Geelen, E., Tettero, L., Zuijdgeest, D., et al. HA antibody-mediated FcgammaRIIIa activity is both dependent on FcR engagement and interactions between HA and sialic acids. Front. Immunol., 7, 2016, 399.
10. DiLillo, D.J., Tan, G.S., Palese, P., Ravetch, J.V., Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgammaR interactions for protection against influenza virus in vivo. Nat. Med. 20 (2014), 143–151.
11. DiLillo, D.J., Palese, P., Wilson, P.C., Ravetch, J.V., Broadly neutralizing anti-influenza antibodies require Fc receptor engagement for in vivo protection. J. Clin. Invest. 126 (2016), 605–610.
12. Dimitrov, D.S., Therapeutic antibodies, vaccines and antibodyomes. MAbs 2 (2010), 347–356.
13. Dreyfus, C., Laursen, N.S., Kwaks, T., Zuijdgeest, D., Khayat, R., Ekiert, D.C., Lee, J.H., Metlagel, Z., Bujny, M.V., Jongeneelen, M., et al. Highly conserved protective epitopes on influenza B viruses. Science 337 (2012), 1343–1348.
14. Du, L.Y., Jin, L., Zhao, G.Y., Sun, S.H., Li, J.F., Yu, H., Li, Y., Zheng, B.J., Liddington, R.C., Zhou, Y.S., et al. Identification and structural characterization of a broadly neutralizing antibody targeting a novel conserved epitope on the influenza virus H5N1 hemagglutinin. J. Virol. 87 (2013), 2215–2225.
15. Dunand, C.J.H., Leon, P.E., Huang, M., Choi, A., Chromikova, V., Ho, I.Y., Tan, G.S., Cruz, J., Hirsh, A., Zheng, N.Y., et al. Both neutralizing and non-neutralizing human H7N9 influenza vaccine-induced monoclonal antibodies confer protection. Cell Host Microbe 19 (2016), 800–813.
16. Echols, N., Grosse-Kunstleve, R.W., Afonine, P.V., Bunkoczi, G., Chen, V.B., Headd, J.J., McCoy, A.J., Moriarty, N.W., Read, R.J., Richardson, D.C., et al. Graphical tools for macromolecular crystallography in PHENIX. J. Appl. Crystallogr. 45 (2012), 581–586.
17. Feng, Y., Wang, Y., Zhu, Z., Li, W., Sussman, R.T., Randall, M., Bosse, K.R., Maris, J.M., Dimitrov, D.S., Differential killing of CD56-expressing cells by drug-conjugated human antibodies targeting membrane-distal and membrane-proximal non-overlapping epitopes. MAbs 8 (2016), 799–810.
18. Fibriansah, G., Tan, J.L., Smith, S.A., de Alwis, R., Ng, T.S., Kostyuchenko, V.A., Jadi, R.S., Kukkaro, P., de Silva, A.M., Crowe, J.E., et al. A highly potent human antibody neutralizes dengue virus serotype 3 by binding across three surface proteins. Nat. Commun., 6, 2015, 6341.
19. Gao, R., Cao, B., Hu, Y., Feng, Z., Wang, D., Hu, W., Chen, J., Jie, Z., Qiu, H., Xu, K., et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N. Engl. J. Med. 368 (2013), 1888–1897.
20. Geisbert, T.W., Mire, C.E., Geisbert, J.B., Chan, Y.P., Agans, K.N., Feldmann, F., Fenton, K.A., Zhu, Z., Dimitrov, D.S., Scott, D.P., et al. Therapeutic treatment of Nipah virus infection in nonhuman primates with a neutralizing human monoclonal antibody. Sci. Transl. Med., 6, 2014, 242ra82.
21. Gerhard, W., Yewdell, J., Frankel, M.E., Webster, R., Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature 290 (1981), 713–717.
22. Henry Dunand, C.J., Leon, P.E., Kaur, K., Tan, G.S., Zheng, N.Y., Andrews, S., Huang, M., Qu, X., Huang, Y., Salgado-Ferrer, M., et al. Preexisting human antibodies neutralize recently emerged H7N9 influenza strains. J. Clin. Invest. 125 (2015), 1255–1268.
23. Hobson, D., Curry, R.L., Beare, A.S., Ward-Gardner, A., The role of serum haemagglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. J. Hyg. (Lond) 70 (1972), 767–777.
24. Hoot, S., McGuire, A.T., Cohen, K.W., Strong, R.K., Hangartner, L., Klein, F., Diskin, R., Scheid, J.F., Sather, D.N., Burton, D.R., et al. Recombinant HIV envelope proteins fail to engage germline versions of anti-CD4bs bNAbs. PLoS Pathog., 9, 2013, e1003106.
25. Hou, D.N., Ying, T.L., Wang, L.L., Chen, C.C., Lu, S.H., Wang, Q., Seeley, E., Xu, J.Q., Xi, X.H., Li, T., et al. Immune repertoire diversity correlated with mortality in avian influenza A (H7N9) virus infected patients. Sci. Rep., 6, 2016, 33843.
26. Houser, K.V., Gretebeck, L., Ying, T.L., Wang, Y.P., Vogel, L., Lamirande, E.W., Bock, K.W., Moore, I.N., Dimitrov, D.S., Subbarao, K., Prophylaxis with a Middle East respiratory syndrome coronavirus (MERS-CoV)-specific human monoclonal antibody protects rabbits from MERS-CoV infection. J. Infect. Dis. 213 (2016), 1557–1561.
27. Huang, C.C., Venturi, M., Majeed, S., Moore, M.J., Phogat, S., Zhang, M.Y., Dimitrov, D.S., Hendrickson, W.A., Robinson, J., Sodroski, J., et al. Structural basis of tyrosine sulfation and VH-gene usage in antibodies that recognize the HIV type 1 coreceptor-binding site on gp120. Proc. Natl. Acad. Sci. USA 101 (2004), 2706–2711.
28. Huang, J., Ofek, G., Laub, L., Louder, M.K., Doria-Rose, N.A., Longo, N.S., Imamichi, H., Bailer, R.T., Chakrabarti, B., Sharma, S.K., et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491 (2012), 406–412.
29. Huang, J., Kang, B.H., Pancera, M., Lee, J.H., Tong, T., Feng, Y., Georgiev, I.S., Chuang, G.-Y., Druz, A., Doria-Rose, N.A., et al. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-120 interface. Nature 515 (2014), 138–142.
30. Jardine, J., Julien, J.P., Menis, S., Ota, T., Kalyuzhniy, O., McGuire, A., Sok, D., Huang, P.S., MacPherson, S., Jones, M., et al. Rational HIV immunogen design to target specific germline B cell receptors. Science 340 (2013), 711–716.
31. Jardine, J.G., Kulp, D.W., Havenar-Daughton, C., Sarkar, A., Briney, B., Sok, D., Sesterhenn, F., Ereno-Orbea, J., Kalyuzhniy, O., Deresa, I., et al. HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogen. Science 351 (2016), 1458–1463.
32. Jegaskanda, S., Reading, P.C., Kent, S.J., Influenza-specific antibody-dependent cellular cytotoxicity: toward a universal influenza vaccine. J. Immunol. 193 (2014), 469–475.
33. Kallewaard, N.L., Corti, D., Collins, P.J., Neu, U., McAuliffe, J.M., Benjamin, E., Wachter-Rosati, L., Palmer-Hill, F.J., Yuan, A.Q., Walker, P.A., et al. Structure and function analysis of an antibody recognizing all influenza A subtypes. Cell 166 (2016), 596–608.
34. Keller, M.A., Stiehm, E.R., Passive immunity in prevention and treatment of infectious diseases. Clin. Microbiol. Rev. 13 (2000), 602–614.
35. Khurana, S., Chung, K.Y., Coyle, E.M., Meijer, A., Golding, H., Antigenic fingerprinting of antibody response in humans following exposure to highly pathogenic H7N7 avian influenza virus: evidence for anti-PA-X antibodies. J. Virol. 90 (2016), 9383–9393.
36. Kiso, M., Mitamura, K., Sakai-Tagawa, Y., Shiraishi, K., Kawakami, C., Kimura, K., Hayden, F.G., Sugaya, N., Kawaoka, Y., Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364 (2004), 759–765.
37. Lin, Q., Lin, Z., Chiu, A.P., He, D., Seasonality of influenza A(H7N9) virus in china-fitting simple epidemic models to human cases. PLoS One, 11, 2016, e0151333.
38. Lingwood, D., McTamney, P.M., Yassine, H.M., Whittle, J.R.R., Guo, X.T., Boyington, J.C., Wei, C.J., Nabel, G.J., Structural and genetic basis for development of broadly neutralizing influenza antibodies. Nature 489 (2012), 566–570.
39. Pappas, L., Foglierini, M., Piccoli, L., Kallewaard, N.L., Turrini, F., Silacci, C., Fernandez-Rodriguez, B., Agatic, G., Giacchetto-Sasselli, I., Pellicciotta, G., et al. Rapid development of broadly influenza neutralizing antibodies through redundant mutations. Nature 516 (2014), 418–422.
40. Prabakaran, P., Zhu, Z., Chen, W., Gong, R., Feng, Y., Streaker, E., Dimitrov, D.S., Origin, diversity, and maturation of human antiviral antibodies analyzed by high-throughput sequencing. Front. Microbiol., 3, 2012, 277.
41. Puligujja, P., Balkundi, S.S., Kendrick, L.M., Baldridge, H.M., Hilaire, J.R., Bade, A.N., Dash, P.K., Zhang, G., Poluektova, L.Y., Gorantla, S., et al. Pharmacodynamics of long-acting folic acid-receptor targeted ritonavir-boosted atazanavir nanoformulations. Biomaterials 41 (2015), 141–150.
42. Sakai, T., Ohuchi, M., Imai, M., Mizuno, T., Kawasaki, K., Kuroda, K., Yamashina, S., Dual wavelength imaging allows analysis of membrane fusion of influenza virus inside cells. J. Virol. 80 (2006), 2013–2018.
43. Schmidt, A.G., Do, K.T., McCarthy, K.R., Kepler, T.B., Liao, H.X., Moody, M.A., Haynes, B.F., Harrison, S.C., Immunogenic stimulus for germline precursors of antibodies that engage the influenza hemagglutinin receptor-binding site. Cell Rep. 13 (2015), 2842–2850.
44. Steichen, J.M., Kulp, D.W., Tokatlian, T., Escolano, A., Dosenovic, P., Stanfield, R.L., McCoy, L.E., Ozorowski, G., Hu, X.Z., Kalyuzhniy, O., et al. HIV vaccine design to target germline precursors of glycan-dependent broadly neutralizing antibodies. Immunity 45 (2016), 483–496.
45. Sun, Z.W., Zhu, Y., Wang, Q., Ye, L., Dai, Y.Y., Su, S., Yu, F., Ying, T.L., Yang, C.L., Jiang, S.B., et al. An immunogen containing four tandem 10E8 epitope repeats with exposed key residues induces antibodies that neutralize HIV-1 and activates an ADCC reporter gene. Emerg. Microbes Infect., 5, 2016, e65.
46. Tan, G.S., Leon, P.E., Albrecht, R.A., Margine, I., Hirsh, A., Bahl, J., Krammer, F., Broadly-reactive neutralizing and non-neutralizing antibodies directed against the H7 influenza virus hemagglutinin reveal divergent mechanisms of protection. PLoS Pathog., 12, 2016, e1005578.
47. Tang, X.C., Agnihothram, S.S., Jiao, Y., Stanhope, J., Graham, R.L., Peterson, E.C., Avnir, Y., Tallarico, A.S., Sheehan, J., Zhu, Q., et al. Identification of human neutralizing antibodies against MERS-CoV and their role in virus adaptive evolution. Proc. Natl. Acad. Sci. USA 111 (2014), E2018–E2026.
48. Tharakaraman, K., Jayaraman, A., Raman, R., Viswanathan, K., Stebbins, N.W., Johnson, D., Shriver, Z., Sasisekharan, V., Sasisekharan, R., Glycan receptor binding of the influenza A virus H7N9 hemagglutinin. Cell 153 (2013), 1486–1493.
49. Tharakaraman, K., Subramanian, V., Viswanathan, K., Sloan, S., Yen, H.L., Barnard, D.L., Leung, Y.H.C., Szretter, K.J., Koch, T.J., Delaney, J.C., et al. A broadly neutralizing human monoclonal antibody is effective against H7N9. Proc. Natl. Acad. Sci. USA 112 (2015), 10890–10895.
50. Thornburg, N.J., Zhang, H., Bangaru, S., Sapparapu, G., Kose, N., Lampley, R.M., Bombardi, R.G., Yu, Y.C., Graham, S., Branchizio, A., et al. H7N9 influenza virus neutralizing antibodies that possess few somatic mutations. J. Clin. Invest. 126 (2016), 1482–1494.
51. van Doremalen, N., Falzarano, D., Ying, T., de Wit, E., Bushmaker, T., Feldmann, F., Okumura, A., Wang, Y., Scott, D.P., Hanley, P.W., et al. Efficacy of antibody-based therapies against Middle East respiratory syndrome coronavirus (MERS-CoV) in common marmosets. Antiviral Res 143 (2017), 30–37.
52. Wang, J., Chen, Z., Bao, L., Zhang, W., Xue, Y., Pang, X., Zhang, X., Qin, C., Jin, Q., Characterization of two human monoclonal antibodies neutralizing influenza A H7N9 viruses. J. Virol. 89 (2015), 9115–9118.
53. Wang, Q., Bi, W.W., Zhu, X.J., Li, H.Y., Qi, Q.Q., Yu, F., Lu, L., Jiang, S.B., Nonneutralizing antibodies induced by the HIV-1 gp41 NHR domain gain neutralizing activity in the presence of the HIV fusion inhibitor enfuvirtide: a potential therapeutic vaccine strategy. J. Virol. 89 (2015), 6960–6964.
54. Xiong, X., Martin, S.R., Haire, L.F., Wharton, S.A., Daniels, R.S., Bennett, M.S., McCauley, J.W., Collins, P.J., Walker, P.A., Skehel, J.J., et al. Receptor binding by an H7N9 influenza virus from humans. Nature 499 (2013), 496–499.
55. Xu, K., Rockx, B., Xie, Y., DeBuysscher, B.L., Fusco, D.L., Zhu, Z., Chan, Y.P., Xu, Y., Luu, T., Cer, R.Z., et al. Crystal structure of the Hendra virus attachment G glycoprotein bound to a potent cross-reactive neutralizing human monoclonal antibody. PLoS Pathog., 9, 2013, e1003684.
56. Yang, H., Carney, P.J., Chang, J.C., Villanueva, J.M., Stevens, J., Structural analysis of the hemagglutinin from the recent 2013 H7N9 influenza virus. J. Virol. 87 (2013), 12433–12446.
57. Ye, Z.W., Yuan, S., Poon, K.M., Wen, L., Yang, D., Sun, Z., Li, C., Hu, M., Shuai, H., Zhou, J., et al. Antibody-dependent cell-mediated cytotoxicity epitopes on the hemagglutinin head region of pandemic H1N1 influenza virus play detrimental roles in H1N1-infected mice. Front. Immunol., 8, 2017, 317.
58. Yen, H.L., McKimm-Breschkin, J.L., Choy, K.T., Wong, D.D.Y., Cheung, P.P.H., Zhou, J., Ng, I.H., Zhu, H., Webby, R.J., Guan, Y., et al. Resistance to neuraminidase inhibitors conferred by an R292K mutation in a human influenza virus H7N9 isolate can be masked by a mixed R/K viral population. MBio, 4, 2013, 10.1128/mBio.00396-13.
59. Ying, T., Du, L., Ju, T.W., Prabakaran, P., Lau, C.C., Lu, L., Liu, Q., Wang, L., Feng, Y., Wang, Y., et al. Exceptionally potent neutralization of Middle East respiratory syndrome coronavirus by human monoclonal antibodies. J. Virol. 88 (2014), 7796–7805.
60. Ying, T.L., Feng, Y., Wang, Y.P., Chen, W.Z., Dimitrov, D.S., Monomeric IgG1 Fc molecules displaying unique Fc receptor interactions that are exploitable to treat inflammation-mediated diseases. Mabs 6 (2014), 1201–1210.
61. Ying, T.L., Prabakaran, P., Du, L.Y., Shi, W., Feng, Y., Wang, Y.P., Wang, L.S., Li, W., Jiang, S.B., Dimitrov, D.S., et al. Junctional and allele-specific residues are critical for MERS-CoV neutralization by an exceptionally potent germline-like antibody. Nat. Commun., 6, 2015, 8223.
62. Zhou, T., Georgiev, I., Wu, X., Yang, Z.Y., Dai, K., Finzi, A., Kwon, Y.D., Scheid, J.F., Shi, W., Xu, L., et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329 (2010), 811–817.
63. Zhou, T., Zhu, J., Wu, X., Moquin, S., Zhang, B., Acharya, P., Georgiev, I.S., Altae-Tran, H.R., Chuang, G.Y., Joyce, M.G., et al. Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 39 (2013), 245–258.
64. Zhu, Z., Dimitrov, A.S., Bossart, K.N., Crameri, G., Bishop, K.A., Choudhry, V., Mungall, B.A., Feng, Y.R., Choudhary, A., Zhang, M.Y., et al. Potent neutralization of Hendra and Nipah viruses by human monoclonal antibodies. J. Virol. 80 (2006), 891–899.
65. Zhu, Z., Chakraborti, S., He, Y., Roberts, A., Sheahan, T., Xiao, X., Hensley, L.E., Prabakaran, P., Rockx, B., Sidorov, I.A., et al. Potent cross-reactive neutralization of SARS coronavirus isolates by human monoclonal antibodies. Proc. Natl. Acad. Sci. USA 104 (2007), 12123–12128.
66. Zhu, Z., Bossart, K.N., Bishop, K.A., Crameri, G., Dimitrov, A.S., McEachern, J.A., Feng, Y., Middleton, D., Wang, L.F., Broder, C.C., et al. Exceptionally potent cross-reactive neutralization of Nipah and Hendra viruses by a human monoclonal antibody. J. Infect. Dis. 197 (2008), 846–853.
67. Zuo, T., Sun, J., Wang, G., Jiang, L., Zuo, Y., Li, D., Shi, X., Liu, X., Fan, S., Ren, H., et al. Comprehensive analysis of antibody recognition in convalescent humans from highly pathogenic avian influenza H5N1 infection. Nat. Commun., 6, 2015, 8855.