Vaccination induces broadly neutralizing antibody precursors to HIV gp41.
Journal
Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354
Informations de publication
Date de publication:
30 May 2024
30 May 2024
Historique:
received:
24
02
2024
accepted:
04
04
2024
medline:
31
5
2024
pubmed:
31
5
2024
entrez:
30
5
2024
Statut:
aheadofprint
Résumé
A key barrier to the development of vaccines that induce broadly neutralizing antibodies (bnAbs) against human immunodeficiency virus (HIV) and other viruses of high antigenic diversity is the design of priming immunogens that induce rare bnAb-precursor B cells. The high neutralization breadth of the HIV bnAb 10E8 makes elicitation of 10E8-class bnAbs desirable; however, the recessed epitope within gp41 makes envelope trimers poor priming immunogens and requires that 10E8-class bnAbs possess a long heavy chain complementarity determining region 3 (HCDR3) with a specific binding motif. We developed germline-targeting epitope scaffolds with affinity for 10E8-class precursors and engineered nanoparticles for multivalent display. Scaffolds exhibited epitope structural mimicry and bound bnAb-precursor human naive B cells in ex vivo screens, protein nanoparticles induced bnAb-precursor responses in stringent mouse models and rhesus macaques, and mRNA-encoded nanoparticles triggered similar responses in mice. Thus, germline-targeting epitope scaffold nanoparticles can elicit rare bnAb-precursor B cells with predefined binding specificities and HCDR3 features.
Identifiants
pubmed: 38816615
doi: 10.1038/s41590-024-01833-w
pii: 10.1038/s41590-024-01833-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI147826
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI144462
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI144462
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI144462
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI144462
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI144462
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI147826
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI144462
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI147826
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
ID : AI144462
Organisme : Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation)
ID : NV-007522
Organisme : Bill & Melinda Gates Foundation
ID : INV-008813
Pays : United States
Organisme : Bill & Melinda Gates Foundation
ID : INV-007522
Pays : United States
Organisme : Bill & Melinda Gates Foundation
ID : INV-008813
Pays : United States
Organisme : Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation)
ID : NV-007522
Organisme : Bill & Melinda Gates Foundation
ID : INV-008813
Pays : United States
Organisme : Bill & Melinda Gates Foundation
ID : INV-002916
Pays : United States
Organisme : Bill & Melinda Gates Foundation
ID : INV-007522
Pays : United States
Organisme : Bill & Melinda Gates Foundation
ID : INV-008813
Pays : United States
Organisme : Bill & Melinda Gates Foundation
ID : INV-007522
Pays : United States
Organisme : Bill & Melinda Gates Foundation
ID : INV-008813
Pays : United States
Organisme : Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation)
ID : INV046626
Informations de copyright
© 2024. The Author(s).
Références
Sok, D. & Burton, D. R. Recent progress in broadly neutralizing antibodies to HIV. Nat. Immunol. 19, 1179–1188 (2018).
pubmed: 30333615
pmcid: 6440471
doi: 10.1038/s41590-018-0235-7
Yechezkel, I., Law, M. & Tzarum, N. From structural studies to HCV vaccine design. Viruses 13, 833 (2021).
pubmed: 34064532
pmcid: 8147963
doi: 10.3390/v13050833
Guthmiller, J. J. et al. Broadly neutralizing antibodies target a haemagglutinin anchor epitope. Nature 602, 314–320 (2022).
pubmed: 34942633
doi: 10.1038/s41586-021-04356-8
Dacon, C. et al. Rare, convergent antibodies targeting the stem helix broadly neutralize diverse betacoronaviruses. Cell Host Microbe 31, 97–111.e12 (2023).
pubmed: 36347257
pmcid: 9639329
doi: 10.1016/j.chom.2022.10.010
Jardine, J. et al. Rational HIV immunogen design to target specific germline B cell receptors. Science 340, 711–716 (2013).
pubmed: 23539181
pmcid: 3689846
doi: 10.1126/science.1234150
McGuire, A. T. et al. Engineering HIV envelope protein to activate germline B cell receptors of broadly neutralizing anti-CD4 binding site antibodies. J. Exp. Med. 210, 655–663 (2013).
pubmed: 23530120
pmcid: 3620356
doi: 10.1084/jem.20122824
Steichen, J. M. et al. A generalized HIV vaccine design strategy for priming of broadly neutralizing antibody responses. Science 366, eaax4380 (2019).
pubmed: 31672916
pmcid: 7092357
doi: 10.1126/science.aax4380
Escolano, A. et al. Sequential immunization elicits broadly neutralizing anti-HIV-1 antibodies in Ig knockin mice. Cell 166, 1445–1458 (2016).
pubmed: 27610569
pmcid: 5019122
doi: 10.1016/j.cell.2016.07.030
Steichen, J. M. et al. HIV vaccine design to target germline precursors of glycan-dependent broadly neutralizing antibodies. Immunity 45, 483–496 (2016).
pubmed: 27617678
pmcid: 5040827
doi: 10.1016/j.immuni.2016.08.016
Chen, X. et al. Vaccination induces maturation in a mouse model of diverse unmutated VRC01-class precursors to HIV-neutralizing antibodies with >50% breadth. Immunity 54, 324–339 (2021).
pubmed: 33453152
pmcid: 8020832
doi: 10.1016/j.immuni.2020.12.014
Leggat, D. J. et al. Vaccination induces HIV broadly neutralizing antibody precursors in humans. Science 378, eadd6502 (2022).
pubmed: 36454825
pmcid: 11103259
doi: 10.1126/science.add6502
Huang, J. et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491, 406–412 (2012).
pubmed: 23151583
pmcid: 4854285
doi: 10.1038/nature11544
Pinto, D. et al. Structural basis for broad HIV-1 neutralization by the MPER-specific human broadly neutralizing antibody LN01. Cell Host Microbe 26, 623–637 (2019).
pubmed: 31653484
pmcid: 6854463
doi: 10.1016/j.chom.2019.09.016
Williams, L. D. et al. Potent and broad HIV-neutralizing antibodies in memory B cells and plasma. Sci. Immunol. 2, eaal2200 (2017).
pubmed: 28783671
pmcid: 5905719
doi: 10.1126/sciimmunol.aal2200
Pegu, A. et al. Neutralizing antibodies to HIV-1 envelope protect more effectively in vivo than those to the CD4 receptor. Sci. Transl. Med. 6, 243ra88 (2014).
pubmed: 24990883
pmcid: 4562469
doi: 10.1126/scitranslmed.3008992
Rantalainen, K. et al. HIV-1 envelope and MPER antibody structures in lipid assemblies. Cell Rep. 31, 107583 (2020).
pubmed: 32348769
pmcid: 7196886
doi: 10.1016/j.celrep.2020.107583
Klein, F. et al. Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell 153, 126–138 (2013).
pubmed: 23540694
pmcid: 3792590
doi: 10.1016/j.cell.2013.03.018
Soto, C. et al. Developmental pathway of the MPER-directed HIV-1-neutralizing antibody 10E8. PLoS ONE 11, e0157409 (2016).
pubmed: 27299673
pmcid: 4907498
doi: 10.1371/journal.pone.0157409
Zhang, L. et al. An MPER antibody neutralizes HIV-1 using germline features shared among donors. Nat. Commun. 10, 5389 (2019).
pubmed: 31772165
pmcid: 6879610
doi: 10.1038/s41467-019-12973-1
Haynes, B. F. et al. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308, 1906–1908 (2005).
pubmed: 15860590
doi: 10.1126/science.1111781
Verkoczy, L. et al. Autoreactivity in an HIV-1 broadly reactive neutralizing antibody variable region heavy chain induces immunologic tolerance. Proc. Natl Acad. Sci. USA 107, 181–186 (2010).
pubmed: 20018688
doi: 10.1073/pnas.0912914107
Verkoczy, L. et al. Rescue of HIV-1 broad neutralizing antibody-expressing B cells in 2F5 V
pubmed: 21908739
doi: 10.4049/jimmunol.1101633
Chen, Y. et al. Common tolerance mechanisms, but distinct cross-reactivities associated with gp41 and lipids, limit production of HIV-1 broad neutralizing antibodies 2F5 and 4E10. J. Immunol. 191, 1260–1275 (2013).
pubmed: 23825311
doi: 10.4049/jimmunol.1300770
Doyle-Cooper, C. et al. Immune tolerance negatively regulates B cells in knock-in mice expressing broadly neutralizing HIV antibody 4E10. J. Immunol. 191, 3186–3191 (2013).
pubmed: 23940276
doi: 10.4049/jimmunol.1301285
Rujas, E. et al. Structural basis for broad neutralization of HIV-1 through the molecular recognition of 10E8 helical epitope at the membrane interface. Sci. Rep. 6, 38177 (2016).
pubmed: 27905530
pmcid: 5131266
doi: 10.1038/srep38177
Irimia, A. et al. Lipid interactions and angle of approach to the HIV-1 viral membrane of broadly neutralizing antibody 10E8: insights for vaccine and therapeutic design. PLoS Pathog. 13, e1006212 (2017).
pubmed: 28225819
pmcid: 5338832
doi: 10.1371/journal.ppat.1006212
Briney, B., Inderbitzin, A., Joyce, C. & Burton, D. R. Commonality despite exceptional diversity in the baseline human antibody repertoire. Nature 566, 393–397 (2019).
pubmed: 30664748
pmcid: 6411386
doi: 10.1038/s41586-019-0879-y
DeKosky, B. J. et al. In-depth determination and analysis of the human paired heavy- and light-chain antibody repertoire. Nat. Med. 21, 86–91 (2015).
pubmed: 25501908
doi: 10.1038/nm.3743
DeKosky, B. J. et al. Large-scale sequence and structural comparisons of human naive and antigen-experienced antibody repertoires. Proc. Natl Acad. Sci. USA 113, E2636–E2645 (2016).
pubmed: 27114511
pmcid: 4868480
doi: 10.1073/pnas.1525510113
Sanders, R. W. et al. A next-generation cleaved, soluble HIV-1 Env trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies. PLoS Pathog. 9, e1003618 (2013).
pubmed: 24068931
pmcid: 3777863
doi: 10.1371/journal.ppat.1003618
Correia, B. E. et al. Computational design of epitope-scaffolds allows induction of antibodies specific for a poorly immunogenic HIV vaccine epitope. Structure 18, 1116–1126 (2010).
pubmed: 20826338
doi: 10.1016/j.str.2010.06.010
Correia, B. E., Holmes, M. A., Huang, P. S., Strong, R. K. & Schief, W. R. High-resolution structure prediction of a circular permutation loop. Protein Sci. 20, 1929–1934 (2011).
pubmed: 21898647
pmcid: 3267956
doi: 10.1002/pro.725
Abbott, R. K. et al. Precursor frequency and affinity determine B cell competitive fitness in germinal centers, tested with germline-targeting HIV vaccine immunogens. Immunity 48, 133–146 (2018).
pubmed: 29287996
doi: 10.1016/j.immuni.2017.11.023
Jardine, J. G. et al. HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogen. Science 351, 1458–1463 (2016).
pubmed: 27013733
pmcid: 4872700
doi: 10.1126/science.aad9195
Tokatlian, T. et al. Innate immune recognition of glycans targets HIV nanoparticle immunogens to germinal centers. Science 363, 649–654 (2018).
Duan, H. et al. Glycan masking focuses immune responses to the HIV-1 CD4-binding site and enhances elicitation of VRC01-class precursor antibodies. Immunity 49, 301–311 (2018).
pubmed: 30076101
pmcid: 6896779
doi: 10.1016/j.immuni.2018.07.005
Havenar-Daughton, C. et al. The human naive B cell repertoire contains distinct subclasses for a germline-targeting HIV-1 vaccine immunogen. Sci. Transl. Med. 10, eaat0381 (2018).
pubmed: 29973404
pmcid: 6145074
doi: 10.1126/scitranslmed.aat0381
Huang, D. et al. B cells expressing authentic naive human VRC01-class BCRs can be recruited to germinal centers and affinity mature in multiple independent mouse models. Proc. Natl Acad. Sci. USA 117, 22920–22931 (2020).
pubmed: 32873644
pmcid: 7502816
doi: 10.1073/pnas.2004489117
Wang, X. et al. Multiplexed CRISPR/CAS9-mediated engineering of pre-clinical mouse models bearing native human B cell receptors. EMBO J. 40, e105926 (2021).
pubmed: 33258500
doi: 10.15252/embj.2020105926
Lefranc, M. P. IMGT, the international ImMunoGeneTics database. Nucleic Acids Res. 29, 207–209 (2001).
pubmed: 11125093
pmcid: 29797
doi: 10.1093/nar/29.1.207
Vazquez Bernat, N. et al. Rhesus and cynomolgus macaque immunoglobulin heavy-chain genotyping yields comprehensive databases of germline VDJ alleles. Immunity 54, 355–366 (2021).
pubmed: 33484642
doi: 10.1016/j.immuni.2020.12.018
Cirelli, K. M. et al. Slow delivery immunization enhances HIV neutralizing antibody and germinal center responses via modulation of immunodominance. Cell 177, 1153–1171 (2019).
pubmed: 31080066
pmcid: 6619430
doi: 10.1016/j.cell.2019.04.012
Silva, M. et al. A particulate saponin/TLR agonist vaccine adjuvant alters lymph flow and modulates adaptive immunity. Sci. Immunol. 6, eabf1152 (2021).
pubmed: 34860581
pmcid: 8763571
doi: 10.1126/sciimmunol.abf1152
Ofek, G. et al. Elicitation of structure-specific antibodies by epitope scaffolds. Proc. Natl Acad. Sci. USA 107, 17880–17887 (2010).
pubmed: 20876137
pmcid: 2964213
doi: 10.1073/pnas.1004728107
Correia, B. E. et al. Proof of principle for epitope-focused vaccine design. Nature 507, 201–206 (2014).
pubmed: 24499818
pmcid: 4260937
doi: 10.1038/nature12966
Krebs, S. J. et al. Longitudinal analysis reveals early development of three MPER-directed neutralizing antibody lineages from an HIV-1-infected individual. Immunity 50, 677–691 (2019).
pubmed: 30876875
pmcid: 6555550
doi: 10.1016/j.immuni.2019.02.008
Sesterhenn, F. et al. De novo protein design enables the precise induction of RSV-neutralizing antibodies. Science 368, eaay5051 (2020).
pubmed: 32409444
pmcid: 7391827
doi: 10.1126/science.aay5051
Schoeder, C. T. et al. Epitope-focused immunogen design based on the ebolavirus glycoprotein HR2-MPER region. PLoS Pathog. 18, e1010518 (2022).
pubmed: 35584193
pmcid: 9170092
doi: 10.1371/journal.ppat.1010518
Olsen, T. H., Boyles, F. & Deane, C. M. Observed antibody space: a diverse database of cleaned, annotated, and translated unpaired and paired antibody sequences. Protein Sci. 31, 141–146 (2022).
pubmed: 34655133
doi: 10.1002/pro.4205
Lee, J. H. et al. Long-primed germinal centres with enduring affinity maturation and clonal migration. Nature 609, 998–1004 (2022).
pubmed: 36131022
pmcid: 9491273
doi: 10.1038/s41586-022-05216-9
Willis, J. R. et al. Human immunoglobulin repertoire analysis guides design of vaccine priming immunogens targeting HIV V2-apex broadly neutralizing antibody precursors. Immunity 55, 2149–2167 (2022).
pubmed: 36179689
pmcid: 9671094
doi: 10.1016/j.immuni.2022.09.001
Leaver-Fay, A. et al. ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol. 487, 545–574 (2011).
pubmed: 21187238
pmcid: 4083816
doi: 10.1016/B978-0-12-381270-4.00019-6
Leman, J. K. et al. Macromolecular modeling and design in Rosetta: recent methods and frameworks. Nat. Methods 17, 665–680 (2020).
pubmed: 32483333
doi: 10.1038/s41592-020-0848-2
Chao, G. et al. Isolating and engineering human antibodies using yeast surface display. Nat. Protoc. 1, 755–768 (2006).
pubmed: 17406305
doi: 10.1038/nprot.2006.94
Zhou, J., Panaitiu, A. E. & Grigoryan, G. A general-purpose protein design framework based on mining sequence-structure relationships in known protein structures. Proc. Natl Acad. Sci. USA 117, 1059–1068 (2020).
pubmed: 31892539
doi: 10.1073/pnas.1908723117
Alexander, J. et al. Development of high potency universal DR-restricted helper epitopes by modification of high affinity DR-blocking peptides. Immunity 1, 751–761 (1994).
pubmed: 7895164
doi: 10.1016/S1074-7613(94)80017-0
Cohen, K. W. et al. A first-in-human germline-targeting HIV nanoparticle vaccine induced broad and publicly targeted helper T cell responses. Sci. Transl. Med. 15, eadf3309 (2023).
pubmed: 37224227
pmcid: 11036875
doi: 10.1126/scitranslmed.adf3309
Allen, J. D. et al. Site-specific steric control of SARS-CoV-2 spike glycosylation. Biochemistry 60, 2153–2169 (2021).
pubmed: 34213308
doi: 10.1021/acs.biochem.1c00279
Baboo, S. et al. DeGlyPHER: an ultrasensitive method for the analysis of viral spike N-glycoforms. Anal. Chem. 93, 13651–13657 (2021).
pubmed: 34597027
pmcid: 8848675
doi: 10.1021/acs.analchem.1c03059
Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1997).
pubmed: 27754618
doi: 10.1016/S0076-6879(97)76066-X
McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
pubmed: 19461840
pmcid: 2483472
doi: 10.1107/S0021889807021206
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
pubmed: 20383002
pmcid: 2852313
doi: 10.1107/S0907444910007493
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
pubmed: 20124702
pmcid: 2815670
doi: 10.1107/S0907444909052925
Williams, C. J. et al. MolProbity: more and better reference data for improved all-atom structure validation. Protein Sci. 27, 293–315 (2018).
pubmed: 29067766
doi: 10.1002/pro.3330
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
pubmed: 28165473
doi: 10.1038/nmeth.4169
Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).
pubmed: 32881101
doi: 10.1002/pro.3943
Casanal, A., Lohkamp, B. & Emsley, P. Current developments in Coot for macromolecular model building of electron cryo-microscopy and crystallographic data. Protein Sci. 29, 1069–1078 (2020).
pubmed: 31730249
pmcid: 7096722
doi: 10.1002/pro.3791
Afonine, P. V. et al. Real-space refinement in PHENIX for cryo-EM and crystallography. Acta Crystallogr. D 74, 531–544 (2018).
doi: 10.1107/S2059798318006551
Tiller, T. et al. Efficient generation of monoclonal antibodies from single human B cells by single cell RT–PCR and expression vector cloning. J. Immunol. Methods 329, 112–124 (2008).
pubmed: 17996249
doi: 10.1016/j.jim.2007.09.017
Lee, J. H. et al. Vaccine genetics of IGHV1-2 VRC01-class broadly neutralizing antibody precursor naive human B cells. NPJ Vaccines 6, 113 (2021).
pubmed: 34489473
pmcid: 8421370
doi: 10.1038/s41541-021-00376-7
Gupta, N. T. et al. Change-O: a toolkit for analyzing large-scale B cell immunoglobulin repertoire sequencing data. Bioinformatics 31, 3356–3358 (2015).
pubmed: 26069265
pmcid: 4793929
doi: 10.1093/bioinformatics/btv359
Lin, Y. C. et al. One-step CRISPR/Cas9 method for the rapid generation of human antibody heavy chain knock-in mice. EMBO J. 37, e99243 (2018).
pubmed: 30087111
pmcid: 6138433
doi: 10.15252/embj.201899243
von Boehmer, L. et al. Sequencing and cloning of antigen-specific antibodies from mouse memory B cells. Nat. Protoc. 11, 1908–1923 (2016).
doi: 10.1038/nprot.2016.102
Brochet, X., Lefranc, M.-P. & Giudicelli, V. 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 (2008).
pubmed: 18503082
pmcid: 2447746
doi: 10.1093/nar/gkn316
Giudicelli, V., Brochet, X. & Lefranc, M.-P. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb. Protoc. 2011, 695–715 (2011).
pubmed: 21632778
Tian, M. et al. Induction of HIV neutralizing antibody lineages in mice with diverse precursor repertoires. Cell 166, 1471–1484 (2016).
pubmed: 27610571
pmcid: 5103708
doi: 10.1016/j.cell.2016.07.029
Chen, J., Lansford, R., Stewart, V., Young, F. & Alt, F. W. RAG-2-deficient blastocyst complementation: an assay of gene function in lymphocyte development. Proc. Natl Acad. Sci. USA 90, 4528–4532 (1993).
pubmed: 8506294
pmcid: 46545
doi: 10.1073/pnas.90.10.4528
Hu, J. et al. Detecting DNA double-stranded breaks in mammalian genomes by linear amplification-mediated high-throughput genome-wide translocation sequencing. Nat. Protoc. 11, 853–871 (2016).
pubmed: 27031497
pmcid: 4895203
doi: 10.1038/nprot.2016.043
Lin, S. G. et al. Highly sensitive and unbiased approach for elucidating antibody repertoires. Proc. Natl Acad. Sci. USA 113, 7846–7851 (2016).
pubmed: 27354528
pmcid: 4948367
doi: 10.1073/pnas.1608649113
Corbett, K. S. et al. Evaluation of the mRNA-1273 vaccine against SARS-CoV-2 in nonhuman primates. N. Engl. J. Med. 383, 1544–1555 (2020).
pubmed: 32722908
doi: 10.1056/NEJMoa2024671
Baden, L. R. et al. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N. Engl. J. Med. 384, 403–416 (2021).
pubmed: 33378609
doi: 10.1056/NEJMoa2035389
Hurtado, J. et al. Efficient isolation of rare B cells using next-generation antigen barcoding. Front. Cell. Infect. Microbiol. 12, 962945 (2022).
pubmed: 36968243
doi: 10.3389/fcimb.2022.962945
Breden, F. et al. Reproducibility and reuse of adaptive immune receptor repertoire data. Front. Immunol. 8, 1418 (2017).
pubmed: 29163494
pmcid: 5671925
doi: 10.3389/fimmu.2017.01418
Rodriguez, O. L. et al. A novel framework for characterizing genomic haplotype diversity in the human immunoglobulin heavy chain locus. Front. Immunol. 11, 2136 (2020).
pubmed: 33072076
pmcid: 7539625
doi: 10.3389/fimmu.2020.02136
Gibson, W. S. et al. Characterization of the immunoglobulin lambda chain locus from diverse populations reveals extensive genetic variation chain locus from diverse populations reveals extensive genetic variation. Genes Immun. 24, 21–31 (2023).
pubmed: 36539592
doi: 10.1038/s41435-022-00188-2
Cottrell, C. A. et al. Mapping the immunogenic landscape of near-native HIV-1 envelope trimers in non-human primates. PLoS Pathog. 16, e1008753 (2020).
pubmed: 32866207
pmcid: 7485981
doi: 10.1371/journal.ppat.1008753
Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587 (2021).
pubmed: 34062119
pmcid: 8238499
doi: 10.1016/j.cell.2021.04.048
Sarzotti-Kelsoe, M. et al. Optimization and validation of the TZM-bl assay for standardized assessments of neutralizing antibodies against HIV-1. J. Immunol. Methods 409, 131–146 (2014).
pubmed: 24291345
doi: 10.1016/j.jim.2013.11.022
Zhao, F. et al. Mapping neutralizing antibody epitope specificities to an HIV Env trimer in immunized and in infected rhesus macaques. Cell Rep. 32, 108122 (2020).
pubmed: 32905766
pmcid: 7487785
doi: 10.1016/j.celrep.2020.108122
Schiffner, T. SchiefLab/Schiffner2024: v1.0.0. Zenodo https://doi.org/10.5281/zenodo.11003090 (2024).