Recent advances in “universal” influenza virus antibodies: the rise of a hidden trimeric interface in hemagglutinin globular head
Yulu Wang, Dan Hu, Yanling Wu(), Tianlei Ying()
MOE/NHC/CAMS Key Laboratory of Medical Molecular Virology, School of Basic Medical Sciences, Shanghai Medical College, Fudan University, Shanghai 200032, China
Influenza causes seasonal outbreaks yearly and unpredictable pandemics with high morbidity and mortality rates. Despite significant efforts to address influenza, it remains a major threat to human public health. This issue is partially due to the lack of antiviral drugs with potent antiviral activity and broad reactivity against all influenza virus strains and the rapid emergence of drug-resistant variants. Moreover, designing a universal influenza vaccine that is sufficiently immunogenic to induce universal antibodies is difficult. Some novel epitopes hidden in the hemagglutinin (HA) trimeric interface have been discovered recently, and a number of antibodies targeting these epitopes have been found to be capable of neutralizing a broad range of influenza isolates. These findings may have important implications for the development of universal influenza vaccines and antiviral drugs. In this review, we focused on the antibodies targeting these newly discovered epitopes in the HA domain of the influenza virus to promote the development of universal anti-influenza antibodies or vaccines and extend the discovery to other viruses with similar conformational changes in envelope proteins.
IN Zhilinskaia, VV Tets, DB Golubev. Genome structure of influenza virus. Vopr Virusol 1978; (4): 387–394 (in Russian)
pmid: 373248
2
IA Rudneva, EI Sklyanskaya, OS Barulina, SS Yamnikova, VP Kovaleva, IV Tsvetkova, NV Kaverin. Phenotypic expression of HA-NA combinations in human-avian influenza A virus reassortants. Arch Virol 1996; 141(6): 1091–1099 https://doi.org/10.1007/BF01718612
pmid: 8712926
S Pleschka. Overview of influenza viruses. In: Swine Influenza. Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 370). Springer: 2013. 1–20
TA Saw, et al.. Isolation of avian influenza A (H5N1) viruses from humans — Hong Kong, May–December 1997 (Reprinted from MMWR, vol 46, pg 1204–1207, 1997). JAMA 1998; 279(4): 263–264
pmid: 9450697
9
RB Tang, HL Chen. An overview of the recent outbreaks of the avian-origin influenza A (H7N9) virus in the human. J Chin Med Assoc 2013; 76(5): 245–248 https://doi.org/10.1016/j.jcma.2013.04.003
pmid: 23651506
10
H Ding, L Xie, Z Sun, QJ Kao, RJ Huang, XH Yang, CP Huang, YY Wen, JC Pan, XY Pu, T Jin, XH Zhou, L Zheng, J Li, FJ Wang. Epidemiologic characterization of 30 confirmed cases of human infection with avian influenza A(H7N9) virus in Hangzhou, China. BMC Infect Dis 2014; 14(1): 175 https://doi.org/10.1186/1471-2334-14-175
pmid: 24678603
11
W Tan, M Li, ZX Xie. An overview of avian influenza A H10N8 subtype viruses. Pak Vet J 2016; 36(3): 251–257
12
Y Guo, J Li, X Cheng. Discovery of men infected by avian influenza A (H9N2) virus. Chin J Exp Clin Viro (Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi) 1999; 13(2): 105–108 (in Chinese)
pmid: 12569771
13
A Stegeman, A Bouma, AR Elbers, MC de Jong, G Nodelijk, F de Klerk, G Koch, M van Boven. Avian influenza A virus (H7N7) epidemic in the Netherlands in 2003: course of the epidemic and effectiveness of control measures. J Infect Dis 2004; 190(12): 2088–2095 https://doi.org/10.1086/425583
pmid: 15551206
F Yu, H Song, Y Wu, SY Chang, L Wang, W Li, B Hong, S Xia, C Wang, S Khurana, Y Feng, Y Wang, Z Sun, B He, D Hou, J Manischewitz, LR King, Y Song, JY Min, H Golding, X Ji, L Lu, S Jiang, DS Dimitrov, T Ying. A potent germline-like human monoclonal antibody targets a pH-sensitive epitope on H7N9 influenza hemagglutinin. Cell Host Microbe 2017; 22(4): 471–483.e5 https://doi.org/10.1016/j.chom.2017.08.011
pmid: 28966056
A Watanabe, KR McCarthy, M Kuraoka, AG Schmidt, Y Adachi, T Onodera, K Tonouchi, TM Caradonna, G Bajic, S Song, CE McGee, GD Sempowski, F Feng, P Urick, TB Kepler, Y Takahashi, SC Harrison, G Kelsoe. Antibodies to a conserved influenza head interface epitope protect by an IgG subtype-dependent mechanism. Cell 2019; 177(5): 1124–1135.e16 https://doi.org/10.1016/j.cell.2019.03.048
18
HL Turner, J Pallesen, S Lang, S Bangaru, S Urata, S Li, CA Cottrell, CA Bowman, JE Crowe Jr, IA Wilson, AB Ward. Potent anti-influenza H7 human monoclonal antibody induces separation of hemagglutinin receptor-binding head domains. PLoS Biol 2019; 17(2): e3000139 https://doi.org/10.1371/journal.pbio.3000139
pmid: 30716060
19
RM Pielak, JR Schnell, JJ Chou. Mechanism of drug inhibition and drug resistance of influenza A M2 channel. Proc Natl Acad Sci USA 2009; 106(18): 7379–7384 https://doi.org/10.1073/pnas.0902548106
pmid: 19383794
20
IV Chizhmakov, FM Geraghty, DC Ogden, A Hayhurst, M Antoniou, AJ Hay. Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J Physiol 1996; 494(2): 329–336 https://doi.org/10.1113/jphysiol.1996.sp021495
pmid: 8841994
21
X Saelens. The role of matrix protein 2 ectodomain in the development of universal influenza vaccines. J Infect Dis 2019; 219(Supplement_1): S68–S74 https://doi.org/10.1093/infdis/jiz003
pmid: 30715367
22
X Zhang, M Liu, C Liu, J Du, W Shi, E Sun, H Li, J Li, Y Zhang. Vaccination with different M2e epitope densities confers partial protection against H5N1 influenza A virus challenge in chickens. Intervirology 2011; 54(5): 290–299 https://doi.org/10.1159/000319440
pmid: 21228535
23
D Corti, E Cameroni, B Guarino, NL Kallewaard, Q Zhu, A Lanzavecchia. Tackling influenza with broadly neutralizing antibodies. Curr Opin Virol 2017; 24: 60–69 https://doi.org/10.1016/j.coviro.2017.03.002
pmid: 28527859
24
LV Jones, RW Compans, AR Davis, TJ Bos, DP Nayak. Surface expression of influenza virus neuraminidase, an amino-terminally anchored viral membrane glycoprotein, in polarized epithelial cells. Mol Cell Biol 1985; 5(9): 2181–2189 https://doi.org/10.1128/MCB.5.9.2181
pmid: 3016520
25
SE Ohmit, JG Petrie, RT Cross, E Johnson, AS Monto. Influenza hemagglutination-inhibition antibody titer as a correlate of vaccine-induced protection. J Infect Dis 2011; 204(12): 1879–1885 https://doi.org/10.1093/infdis/jir661
pmid: 21998477
26
E Benjamin, W Wang, JM McAuliffe, FJ Palmer-Hill, NL Kallewaard, Z Chen, JA Suzich, WS Blair, H Jin, Q Zhu. A broadly neutralizing human monoclonal antibody directed against a novel conserved epitope on the influenza virus H3 hemagglutinin globular head. J Virol 2014; 88(12): 6743–6750 https://doi.org/10.1128/JVI.03562-13
pmid: 24696468
27
A Cho, J Wrammert. Implications of broadly neutralizing antibodies in the development of a universal influenza vaccine. Curr Opin Virol 2016; 17: 110–115 https://doi.org/10.1016/j.coviro.2016.03.002
pmid: 27031684
28
NC Wu, G Grande, HL Turner, AB Ward, J Xie, RA Lerner, IA Wilson. In vitro evolution of an influenza broadly neutralizing antibody is modulated by hemagglutinin receptor specificity. Nat Commun 2017; 8(1): 15371 https://doi.org/10.1038/ncomms15371
pmid: 28504265
W Hu, A Chen, Y Miao, S Xia, Z Ling, K Xu, T Wang, Y Xu, J Cui, H Wu, G Hu, L Tian, L Wang, Y Shu, X Ma, B Xu, J Zhang, X Lin, C Bian, B Sun. Fully human broadly neutralizing monoclonal antibodies against influenza A viruses generated from the memory B cells of a 2009 pandemic H1N1 influenza vaccine recipient. Virology 2013; 435(2): 320–328 https://doi.org/10.1016/j.virol.2012.09.034
pmid: 23084424
31
JJ Skehel, MD Waterfield. Studies on the primary structure of the influenza virus hemagglutinin. Proc Natl Acad Sci USA 1975; 72(1): 93–97 https://doi.org/10.1073/pnas.72.1.93
pmid: 1054518
32
CJ Russell, M Hu, FA Okda. Influenza hemagglutinin protein stability, activation, and pandemic risk. Trends Microbiol 2018; 26(10): 841–853 https://doi.org/10.1016/j.tim.2018.03.005
pmid: 29681430
NK Garcia, M Guttman, JL Ebner, KK Lee. Dynamic changes during acid-induced activation of influenza hemagglutinin. Structure 2015; 23(4): 665–676 https://doi.org/10.1016/j.str.2015.02.006
pmid: 25773144
36
Y Gaudin, RW Ruigrok, J Brunner. Low-pH induced conformational changes in viral fusion proteins: implications for the fusion mechanism. J Gen Virol 1995; 76(Pt 7): 1541–1556 https://doi.org/10.1099/0022-1317-76-7-1541
pmid: 9049361
37
Y Zhang, C Xu, H Zhang, GD Liu, C Xue, Y Cao. Targeting hemagglutinin: approaches for broad protection against the influenza A virus. Viruses 2019; 11(5): E405 https://doi.org/10.3390/v11050405
pmid: 31052339
38
PS Lee, IA Wilson. Structural characterization of viral epitopes recognized by broadly cross-reactive antibodies. In: Oldstone M, Compans R. Influenza Pathogenesis and Control—Volume II. Current Topics in Microbiology and Immunology, vol 386. Springer, Cham: 2014. 323–341
39
X Sun, Y Shi, X Lu, J He, F Gao, J Yan, J Qi, GF Gao. Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep 2013; 3(3): 769–778 https://doi.org/10.1016/j.celrep.2013.01.025
pmid: 23434510
40
X Zhu, W Yu, R McBride, Y Li, LM Chen, RO Donis, S Tong, JC Paulson, IA Wilson. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc Natl Acad Sci USA 2013; 110(4): 1458–1463 https://doi.org/10.1073/pnas.1218509110
pmid: 23297216
41
S Tong, X Zhu, Y Li, M Shi, J Zhang, M Bourgeois, H Yang, X Chen, S Recuenco, J Gomez, LM Chen, A Johnson, Y Tao, C Dreyfus, W Yu, R McBride, PJ Carney, AT Gilbert, J Chang, Z Guo, CT Davis, JC Paulson, J Stevens, CE Rupprecht, EC Holmes, IA Wilson, RO Donis. New world bats harbor diverse influenza A viruses. PLoS Pathog 2013; 9(10): e1003657 https://doi.org/10.1371/journal.ppat.1003657
pmid: 24130481
42
JC Krause, T Tsibane, TM Tumpey, CJ Huffman, R Albrecht, DL Blum, I Ramos, A Fernandez-Sesma, KM Edwards, A García-Sastre, CF Basler, JE Crowe Jr. Human monoclonal antibodies to pandemic 1957 H2N2 and pandemic 1968 H3N2 influenza viruses. J Virol 2012; 86(11): 6334–6340 https://doi.org/10.1128/JVI.07158-11
pmid: 22457520
43
PS Lee, N Ohshima, RL Stanfield, W Yu, Y Iba, Y Okuno, Y Kurosawa, IA Wilson. Receptor mimicry by antibody F045-092 facilitates universal binding to the H3 subtype of influenza virus. Nat Commun 2014; 5(1): 3614 https://doi.org/10.1038/ncomms4614
pmid: 24717798
44
B Brandenburg, W Koudstaal, J Goudsmit, V Klaren, C Tang, MV Bujny, HJ Korse, T Kwaks, JJ Otterstrom, J Juraszek, AM van Oijen, R Vogels, RH Friesen. Mechanisms of hemagglutinin targeted influenza virus neutralization. PLoS One 2013; 8(12): e80034 https://doi.org/10.1371/journal.pone.0080034
pmid: 24348996
45
DD Raymond, G Bajic, J Ferdman, P Suphaphiphat, EC Settembre, MA Moody, AG Schmidt, SC Harrison. Conserved epitope on influenza-virus hemagglutinin head defined by a vaccine-induced antibody. Proc Natl Acad Sci USA 2018; 115(1): 168–173 https://doi.org/10.1073/pnas.1715471115
pmid: 29255041
46
M Russier, G Yang, JE Rehg, SS Wong, HH Mostafa, TP Fabrizio, S Barman, S Krauss, RG Webster, RJ Webby, CJ Russell. Molecular requirements for a pandemic influenza virus: an acid-stable hemagglutinin protein. Proc Natl Acad Sci USA 2016; 113(6): 1636–1641 https://doi.org/10.1073/pnas.1524384113
pmid: 26811446
47
R Yoshida, M Igarashi, H Ozaki, N Kishida, D Tomabechi, H Kida, K Ito, A Takada. Cross-protective potential of a novel monoclonal antibody directed against antigenic site B of the hemagglutinin of influenza A viruses. PLoS Pathog 2009; 5(3): e1000350 https://doi.org/10.1371/journal.ppat.1000350
pmid: 19300497
48
JRR Whittle, R Zhang, S Khurana, LR King, J Manischewitz, H Golding, PR Dormitzer, BF Haynes, EB Walter, MA Moody, TB Kepler, HX Liao, SC Harrison. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc Natl Acad Sci USA 2011; 108(34): 14216–14221 https://doi.org/10.1073/pnas.1111497108
pmid: 21825125
49
DC Ekiert, AK Kashyap, J Steel, A Rubrum, G Bhabha, R Khayat, JH Lee, MA Dillon, RE O’Neil, AM Faynboym, M Horowitz, L Horowitz, AB Ward, P Palese, R Webby, RA Lerner, RR Bhatt, IA Wilson. Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 2012; 489(7417): 526–532 https://doi.org/10.1038/nature11414
pmid: 22982990
50
N Ohshima, Y Iba, R Kubota-Koketsu, Y Asano, Y Okuno, Y Kurosawa. Naturally occurring antibodies in humans can neutralize a variety of influenza virus strains, including H3, H1, H2, and H5. J Virol 2011; 85(21): 11048–11057 https://doi.org/10.1128/JVI.05397-11
pmid: 21865387
51
K Matsuda, J Huang, T Zhou, Z Sheng, BH Kang, E Ishida, T Griesman, S Stuccio, L Bolkhovitinov, TJ Wohlbold, V Chromikova, A Cagigi, K Leung, S Andrews, CSF Cheung, AA Pullano, J Plyler, C Soto, B Zhang, Y Yang, MG Joyce, Y Tsybovsky, A Wheatley, SR Narpala, Y Guo, S Darko, RT Bailer, A Poole, CJ Liang, J Smith, J Alexander, M Gurwith, SA Migueles, RA Koup, H Golding, S Khurana, AB McDermott, L Shapiro, F Krammer, PD Kwong, M Connors. Prolonged evolution of the memory B cell response induced by a replicating adenovirus-influenza H5 vaccine. Sci Immunol 2019; 4(34): eaau2710 https://doi.org/10.1126/sciimmunol.aau2710
pmid: 31004012
52
C Dreyfus, NS Laursen, T Kwaks, D Zuijdgeest, R Khayat, DC Ekiert, JH Lee, Z Metlagel, MV Bujny, M Jongeneelen, R van der Vlugt, M Lamrani, HJ Korse, E Geelen, Ö Sahin, M Sieuwerts, JP Brakenhoff, R Vogels, OT Li, LL Poon, M Peiris, W Koudstaal, AB Ward, IA Wilson, J Goudsmit, RH Friesen. Highly conserved protective epitopes on influenza B viruses. Science 2012; 337(6100): 1343–1348 https://doi.org/10.1126/science.1222908
pmid: 22878502
53
C Shen, J Chen, R Li, M Zhang, G Wang, S Stegalkina, L Zhang, J Chen, J Cao, X Bi, SF Anderson, T Alefantis, M Zhang, X Cai, K Yang, Q Zheng, M Fang, H Yu, W Luo, Z Zheng, Q Yuan, J, Zhang J Wai-Kuo Shih, H Kleanthous, H Chen, Y Chen, N Xia. A multimechanistic antibody targeting the receptor binding site potently cross-protects against influenza B viruses. Sci Transl Med 2017; 9(412): eaam5752 https://doi.org/10.1126/scitranslmed.aam5752
54
C Dreyfus, DC Ekiert, IA Wilson. Structure of a classical broadly neutralizing stem antibody in complex with a pandemic H2 influenza virus hemagglutinin. J Virol 2013; 87(12): 7149–7154 https://doi.org/10.1128/JVI.02975-12
pmid: 23552413
55
DC Ekiert, G Bhabha, MA Elsliger, RH Friesen, M Jongeneelen, M Throsby, J Goudsmit, IA Wilson. Antibody recognition of a highly conserved influenza virus epitope. Science 2009; 324(5924): 246–251 https://doi.org/10.1126/science.1171491
pmid: 19251591
56
S Yamayoshi, R Uraki, M Ito, M Kiso, S Nakatsu, A Yasuhara, K Oishi, T Sasaki, K Ikuta, Y Kawaoka. A broadly reactive human anti-hemagglutinin stem monoclonal antibody that inhibits influenza A virus particle release. EBioMedicine 2017; 17: 182–191 https://doi.org/10.1016/j.ebiom.2017.03.007
pmid: 28286060
57
NL Kallewaard, D Corti, PJ Collins, U Neu, JM McAuliffe, E Benjamin, L Wachter-Rosati, FJ Palmer-Hill, AQ Yuan, PA Walker, MK Vorlaender, S Bianchi, B Guarino, A De Marco, F Vanzetta, G Agatic, M Foglierini, D Pinna, B Fernandez-Rodriguez, A Fruehwirth, C Silacci, RW Ogrodowicz, SR Martin, F Sallusto, JA Suzich, A Lanzavecchia, Q Zhu, SJ Gamblin, JJ Skehel. Structure and function analysis of an antibody recognizing all influenza A subtypes. Cell 2016; 166(3): 596–608 https://doi.org/10.1016/j.cell.2016.05.073
pmid: 27453466
58
J Sui, WC Hwang, S Perez, G Wei, D Aird, LM Chen, E Santelli, B Stec, G Cadwell, M Ali, H Wan, A Murakami, A Yammanuru, T Han, NJ Cox, LA Bankston, RO Donis, RC Liddington, WA Marasco. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 2009; 16(3): 265–273 https://doi.org/10.1038/nsmb.1566
pmid: 19234466
59
JE Ledgerwood, CJ Wei, Z Hu, IJ Gordon, ME Enama, CS Hendel, PM McTamney, MB Pearce, HM Yassine, JC Boyington, R Bailer, TM Tumpey, RA Koup, JR Mascola, GJ Nabel, BS Graham; VRC 306 Study Team. DNA priming and influenza vaccine immunogenicity: two phase 1 open label randomised clinical trials. Lancet Infect Dis 2011; 11(12): 916–924 https://doi.org/10.1016/S1473-3099(11)70240-7
pmid: 21975270
60
AK Wheatley, JR Whittle, D Lingwood, M Kanekiyo, HM Yassine, SS Ma, SR Narpala, MS Prabhakaran, RA Matus-Nicodemos, RT Bailer, GJ Nabel, BS Graham, JE Ledgerwood, RA Koup, AB McDermott. H5N1 vaccine-elicited memory B cells are genetically constrained by the IGHV locus in the recognition of a neutralizing epitope in the hemagglutinin stem. J Immunol 2015; 195(2): 602–610 https://doi.org/10.4049/jimmunol.1402835
pmid: 26078272
61
JRR Whittle, AK Wheatley, L Wu, D Lingwood, M Kanekiyo, SS Ma, SR Narpala, HM Yassine, GM Frank, JW Yewdell, JE Ledgerwood, CJ Wei, AB McDermott, BS Graham, RA Koup, GJ Nabel. Flow cytometry reveals that H5N1 vaccination elicits cross-reactive stem-directed antibodies from multiple Ig heavy-chain lineages. J Virol 2014; 88(8): 4047–4057 https://doi.org/10.1128/JVI.03422-13
pmid: 24501410
62
J Sui, WC Hwang, S Perez, G Wei, D Aird, LM Chen, E Santelli, B Stec, G Cadwell, M Ali, H Wan, A Murakami, A Yammanuru, T Han, NJ Cox, LA Bankston, RO Donis, RC Liddington, WA Marasco. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 2009; 16(3): 265–273 https://doi.org/10.1038/nsmb.1566
pmid: 19234466
63
C Dreyfus, NS Laursen, T Kwaks, D Zuijdgeest, R Khayat, DC Ekiert, JH Lee, Z Metlagel, MV Bujny, M Jongeneelen, R van der Vlugt, M Lamrani, HJ Korse, E Geelen, Ö Sahin, M Sieuwerts, JP Brakenhoff, R Vogels, OT Li, LL Poon, M Peiris, W Koudstaal, AB Ward, IA Wilson, J Goudsmit, RH Friesen. Highly conserved protective epitopes on influenza B viruses. Science 2012; 337(6100): 1343–1348 https://doi.org/10.1126/science.1222908
pmid: 22878502
64
DC Ekiert, RH Friesen, G Bhabha, T Kwaks, M Jongeneelen, W Yu, C Ophorst, F Cox, HJ Korse, B Brandenburg, R Vogels, JP Brakenhoff, R Kompier, MH Koldijk, LA Cornelissen, LL Poon, M Peiris, W Koudstaal, IA Wilson, J Goudsmit. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 2011; 333(6044): 843–850 https://doi.org/10.1126/science.1204839
pmid: 21737702
65
D Corti, J Voss, SJ Gamblin, G Codoni, A Macagno, D Jarrossay, SG Vachieri, D Pinna, A Minola, F Vanzetta, C Silacci, BM Fernandez-Rodriguez, G Agatic, S Bianchi, I Giacchetto-Sasselli, L Calder, F Sallusto, P Collins, LF Haire, N Temperton, JP Langedijk, JJ Skehel, A Lanzavecchia. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 2011; 333(6044): 850–856 https://doi.org/10.1126/science.1205669
pmid: 21798894
66
DJ DiLillo, GS Tan, P Palese, JV Ravetch. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgR interactions for protection against influenza virus in vivo. Nat Med 2014; 20(2): 143–151 https://doi.org/10.1038/nm.3443
pmid: 24412922
67
F Krammer, P Palese. Advances in the development of influenza virus vaccines. Nat Rev Drug Discov 2015; 14(3): 167–182 https://doi.org/10.1038/nrd4529
pmid: 25722244
68
PS Lee, IA Wilson. Structural characterization of viral epitopes recognized by broadly cross-reactive antibodies. Curr Top Microbiol Immunol 2015; 386: 323–341 https://doi.org/10.1007/82_2014_413
pmid: 25037260
69
JH Seok, J Kim, DB Lee, KJ Cho, JH Lee, G Bae, MS Chung, KH Kim. Conformational modulation of influenza virus hemagglutinin: characterization and in vivo efficacy of monomeric form. Sci Rep 2017; 7(1): 7540 https://doi.org/10.1038/s41598-017-08021-x
pmid: 28790432
70
D Angeletti, I Kosik, JJS Santos, WT Yewdell, CM Boudreau, VVA Mallajosyula, MC Mankowski, M Chambers, M Prabhakaran, HD Hickman, AB McDermott, G Alter, J Chaudhuri, JW Yewdell. Outflanking immunodominance to target subdominant broadly neutralizing epitopes. Proc Natl Acad Sci USA 2019; 116(27): 13474–13479 https://doi.org/10.1073/pnas.1816300116
pmid: 31213541
71
F Krammer, P Palese. Advances in the development of influenza virus vaccines. Nat Rev Drug Discov 2015; 14(3): 167–182 https://doi.org/10.1038/nrd4529
pmid: 25722244
72
DD Raymond, G Bajic, J Ferdman, P Suphaphiphat, EC Settembre, MA Moody, AG Schmidt, SC Harrison. Conserved epitope on influenza-virus hemagglutinin head defined by a vaccine-induced antibody. Proc Natl Acad Sci USA 2018; 115(1): 168–173 https://doi.org/10.1073/pnas.1715471115
pmid: 29255041
73
BE Correia, JT Bates, RJ Loomis, G Baneyx, C Carrico, JG Jardine, P Rupert, C Correnti, O Kalyuzhniy, V Vittal, MJ Connell, E Stevens, A Schroeter, M Chen, S Macpherson, AM Serra, Y Adachi, MA Holmes, Y Li, RE Klevit, BS Graham, RT Wyatt, D Baker, RK Strong, JE Jr1 Crowe, PR Johnson, WR Schief. Proof of principle for epitope-focused vaccine design. Nature 2014; 507(7491): 201–206 https://doi.org/10.1038/nature12966
74
BF Haynes, G Kelsoe, SC Harrison, TB Kepler. B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nat Biotechnol 2012; 30(5): 423–433 https://doi.org/10.1038/nbt.2197
pmid: 22565972
G Bajic, MJ Maron, Y Adachi, T Onodera, KR McCarthy, CE McGee, GD Sempowski, Y Takahashi, G Kelsoe, M Kuraoka, AG Schmidt. Influenza antigen engineering focuses immune responses to a subdominant but broadly protective viral epitope. Cell Host Microbe 2019; 25(6): 827–835.e6 https://doi.org/DOI: 10.1016/j.chom.2019.04.003
pmid: 31104946
77
M Lavie, X Hanoulle, J Dubuisson. Glycan shielding and modulation of hepatitis C virus neutralizing antibodies. Front Immunol 2018; 9: 910 https://doi.org/10.3389/fimmu.2018.00910
pmid: 29755477
78
Y Watanabe, J Raghwani, JD Allen, GE Seabright, S Li, F Moser, JT Huiskonen, T Strecker, TA Bowden, M Crispin. Structure of the Lassa virus glycan shield provides a model for immunological resistance. Proc Natl Acad Sci USA 2018; 115(28): 7320–7325 https://doi.org/10.1073/pnas.1803990115
pmid: 29941589
79
PL Hervé, V Lorin, G Jouvion, B Da Costa, N Escriou. Addition of N-glycosylation sites on the globular head of the H5 hemagglutinin induces the escape of highly pathogenic avian influenza A H5N1 viruses from vaccine-induced immunity. Virology 2015; 486: 134–145 https://doi.org/10.1016/j.virol.2015.08.033
pmid: 26433051
80
WC Liu, JT Jan, YJ Huang, TH Chen, SC Wu. Unmasking stem-specific neutralizing epitopes by abolishing N-linked glycosylation sites of influenza virus hemagglutinin proteins for vaccine design. J Virol 2016; 90(19): 8496–8508 https://doi.org/10.1128/JVI.00880-16
pmid: 27440889
81
NW Florek, JT Weinfurter, S Jegaskanda, JN Brewoo, TD Powell, GR Young, SC Das, M Hatta, KW Broman, O Hungnes, SG Dudman, Y Kawaoka, SJ Kent, DT Stinchcomb, JE Osorio, TC Friedrich. Modified vaccinia virus Ankara encoding influenza virus hemagglutinin induces heterosubtypic immunity in macaques. J Virol 2014; 88(22): 13418–13428 https://doi.org/10.1128/JVI.01219-14
pmid: 25210172
82
A Kamlangdee, B Kingstad-Bakke, TK Anderson, TL Goldberg, JE Osorio. Broad protection against avian influenza virus by using a modified vaccinia Ankara virus expressing a mosaic hemagglutinin gene. J Virol 2014; 88(22): 13300–13309 https://doi.org/10.1128/JVI.01532-14
pmid: 25210173
83
JW Yewdell, A Taylor, A Yellen, A Caton, W Gerhard, T Bächi. Mutations in or near the fusion peptide of the influenza virus hemagglutinin affect an antigenic site in the globular region. J Virol 1993; 67(2): 933–942 https://doi.org/10.1128/JVI.67.2.933-942.1993
pmid: 7678310
84
JW Yewdell, A Yellen, T Bächi. Monoclonal antibodies localize events in the folding, assembly, and intracellular transport of the influenza virus hemagglutinin glycoprotein. Cell 1988; 52(6): 843–852 https://doi.org/10.1016/0092-8674(88)90426-6
pmid: 2450677
85
JW Yewdell, W Gerhard, T Bachi. Monoclonal anti-hemagglutinin antibodies detect irreversible antigenic alterations that coincide with the acid activation of influenza virus A/PR/834-mediated hemolysis. J Virol 1983; 48(1): 239–248 https://doi.org/10.1128/JVI.48.1.239-248.1983
pmid: 6193286
86
J Lee, DR Boutz, V Chromikova, MG Joyce, C Vollmers, K Leung, AP Horton, BJ DeKosky, CH Lee, JJ Lavinder, EM Murrin, C Chrysostomou, KH Hoi, Y Tsybovsky, PV Thomas, A Druz, B Zhang, Y Zhang, L Wang, WP Kong, D Park, LI Popova, CL Dekker, MM Davis, CE Carter, TM Ross, AD Ellington, PC Wilson, EM Marcotte, JR Mascola, GC Ippolito, F Krammer, SR Quake, PD Kwong, G Georgiou. Molecular-level analysis of the serum antibody repertoire in young adults before and after seasonal influenza vaccination. Nat Med 2016; 22(12): 1456–1464 https://doi.org/10.1038/nm.4224
pmid: 27820605
87
S Bangaru, S Lang, M Schotsaert, HA Vanderven, X Zhu, N Kose, R Bombardi, JA Finn, SJ Kent, P Gilchuk, I Gilchuk, HL Turner, A García-Sastre, S Li, AB Ward, IA Wilson, JE Crowe Jr. A site of vulnerability on the influenza virus hemagglutinin head domain trimer interface. Cell 2019; 177(5): 1136–1152.e18 https://doi.org/10.1016/j.cell.2019.04.011
pmid: 31100268
88
DK Das, R Govindan, I Nikić-Spiegel, F Krammer, EA Lemke, JB Munro. Direct visualization of the conformational dynamics of single influenza hemagglutinin trimers. Cell 2018; 174(4): 926–937.e12 https://doi.org/10.1016/j.cell.2018.05.050
pmid: 29961575
89
NK Garcia, KK Lee. Dynamic viral glycoprotein machines: approaches for probing transient states that drive membrane fusion. Viruses 2016; 8(1): E15 https://doi.org/10.3390/v8010015
90
C Puchades, B Kűkrer, O Diefenbach, E Sneekes-Vriese, J Juraszek, W Koudstaal, A Apetri. Epitope mapping of diverse influenza hemagglutinin drug candidates using HDX-MS. Sci Rep 2019; 9(1): 4735 https://doi.org/10.1038/s41598-019-41179-0
pmid: 30894620
91
CS Copeland, RW Doms, EM Bolzau, RG Webster, A Helenius. Assembly of influenza hemagglutinin trimers and its role in intracellular transport. J Cell Biol 1986; 103(4): 1179–1191 https://doi.org/10.1083/jcb.103.4.1179
pmid: 2429970
92
MJ Gething, K McCammon, J Sambrook. Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell 1986; 46(6): 939–950 https://doi.org/10.1016/0092-8674(86)90076-0
pmid: 3757030
93
J Chen, KH Lee, DA Steinhauer, DJ Stevens, JJ Skehel, DC Wiley. Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 1998; 95(3): 409–417 https://doi.org/10.1016/S0092-8674(00)81771-7
pmid: 9814710
K Suzuki, I Grigorova, TG Phan, LM Kelly, JG Cyster. Visualizing B cell capture of cognate antigen from follicular dendritic cells. J Exp Med 2009; 206(7): 1485–1493 https://doi.org/10.1084/jem.20090209
pmid: 19506051
96
BA Heesters, P Chatterjee, YA Kim, SF Gonzalez, MP Kuligowski, T Kirchhausen, MC Carroll. Endocytosis and recycling of immune complexes by follicular dendritic cells enhances B cell antigen binding and activation. Immunity 2013; 38(6): 1164–1175 https://doi.org/10.1016/j.immuni.2013.02.023
pmid: 23770227
97
A Pincetic, S Bournazos, DJ DiLillo, J Maamary, TT Wang, R Dahan, BM Fiebiger, JV Ravetch. Type I and type II Fc receptors regulate innate and adaptive immunity. Nat Immunol 2014; 15(8): 707–716 https://doi.org/10.1038/ni.2939
pmid: 25045879
98
AB Bohn, L Nederby, T Harbo, A Skovbo, T Vorup-Jensen, J Krog, J Jakobsen, ME Hokland. The effect of IgG levels on the number of natural killer cells and their Fc receptors in chronic inflammatory demyelinating polyradiculoneuropathy. Eur J Neurol 2011; 18(6): 919–924 https://doi.org/10.1111/j.1468-1331.2010.03333.x
pmid: 21219545
99
F Nimmerjahn. Fc-receptors and innate immune effector cells involved in IgG activity. Immunology 2011; 135: 19
FA Rey, K Stiasny, MC Vaney, M Dellarole, FX Heinz. The bright and the dark side of human antibody responses to flaviviruses: lessons for vaccine design. EMBO Rep 2018; 19(2): 206–224 https://doi.org/10.15252/embr.201745302
pmid: 29282215
102
Y Yuan, D Cao, Y Zhang, J Ma, J Qi, Q Wang, G Lu, Y Wu, J Yan, Y Shi, X Zhang, GF Gao. Cryo-EM structures of MERS-CoV and SARS-CoV spike glycoproteins reveal the dynamic receptor binding domains. Nat Commun 2017; 8(1): 15092 https://doi.org/10.1038/ncomms15092
pmid: 28393837
103
Y Wu, S Li, L Du, C Wang, P Zou, B Hong, M Yuan, X Ren, W Tai, Y Kong, C Zhou, L Lu, X Zhou, S Jiang, T Ying. Neutralization of Zika virus by germline-like human monoclonal antibodies targeting cryptic epitopes on envelope domain III. Emerg Microbes Infect 2017; 6(10): e89 https://doi.org/10.1038/emi.2017.79
pmid: 29018252
104
LH Miller, HC Ackerman, XZ Su, TE Wellems. Malaria biology and disease pathogenesis: insights for new treatments. Nat Med 2013; 19(2): 156–167 https://doi.org/10.1038/nm.3073
pmid: 23389616
105
K Mozdzanowska, J Feng, W Gerhard. Virus-neutralizing activity mediated by the Fab fragment of a hemagglutinin-specific antibody is sufficient for the resolution of influenza virus infection in SCID mice. J Virol 2003; 77(15): 8322–8328 https://doi.org/10.1128/JVI.77.15.8322-8328.2003
pmid: 12857901