Single B cell transcriptomics identifies multiple isotypes of broadly neutralizing antibodies against flaviviruses.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
10 2023
Historique:
received: 17 05 2023
accepted: 28 09 2023
revised: 19 10 2023
medline: 23 10 2023
pubmed: 9 10 2023
entrez: 9 10 2023
Statut: epublish

Résumé

Sequential dengue virus (DENV) infections often generate neutralizing antibodies against all four DENV serotypes and sometimes, Zika virus. Characterizing cross-flavivirus broadly neutralizing antibody (bnAb) responses can inform countermeasures that avoid enhancement of infection associated with non-neutralizing antibodies. Here, we used single cell transcriptomics to mine the bnAb repertoire following repeated DENV infections. We identified several new bnAbs with comparable or superior breadth and potency to known bnAbs, and with distinct recognition determinants. Unlike all known flavivirus bnAbs, which are IgG1, one newly identified cross-flavivirus bnAb (F25.S02) was derived from IgA1. Both IgG1 and IgA1 versions of F25.S02 and known bnAbs displayed neutralizing activity, but only IgG1 enhanced infection in monocytes expressing IgG and IgA Fc receptors. Moreover, IgG-mediated enhancement of infection was inhibited by IgA1 versions of bnAbs. We demonstrate a role for IgA in flavivirus infection and immunity with implications for vaccine and therapeutic strategies.

Identifiants

pubmed: 37812640
doi: 10.1371/journal.ppat.1011722
pii: PPATHOGENS-D-23-00811
pmc: PMC10586629
doi:

Substances chimiques

Broadly Neutralizing Antibodies 0
Antibodies, Neutralizing 0
Immunoglobulin G 0
Immunoglobulin A 0
Antibodies, Viral 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011722

Subventions

Organisme : NCI NIH HHS
ID : P30 CA015704
Pays : United States
Organisme : NIH HHS
ID : S10 OD028685
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM129325
Pays : United States
Organisme : NIAID NIH HHS
ID : T32 AI083203
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI146028
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI057229
Pays : United States

Commentaires et corrections

Type : UpdateOf

Informations de copyright

Copyright: © 2023 Lubow et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

I have read the journal’s policy and the authors of this manuscript have the following competing interests: LG, JL, FAM, DKR, LML are inventors on a patent application filed by Fred Hutchinson Cancer Center relating to newly discovered antibodies described in this paper. SK, ED, BJD are employees of Integral Molecular, Inc.; BJD is also a shareholder of the company.

Références

JCI Insight. 2017 Apr 20;2(8):
pubmed: 28422757
Methods Mol Biol. 2019;1904:109-145
pubmed: 30539468
Elife. 2019 Dec 10;8:
pubmed: 31820734
Cell Rep. 2020 Oct 6;33(1):108226
pubmed: 33027653
Immunity. 2012 Sep 21;37(3):412-25
pubmed: 22999947
Vaccine. 2019 Aug 14;37(35):4848-4849
pubmed: 30424888
Sci Rep. 2021 Jun 21;11(1):12987
pubmed: 34155267
mBio. 2015 Nov 03;6(6):e01559-15
pubmed: 26530385
PLoS Pathog. 2017 Feb 16;13(2):e1006178
pubmed: 28207910
Virology. 2008 Jul 5;376(2):429-35
pubmed: 18452966
Virology. 2006 Mar 1;346(1):53-65
pubmed: 16325883
PLoS Negl Trop Dis. 2013 Sep 19;7(9):e2451
pubmed: 24069496
Cell. 2019 Dec 12;179(7):1636-1646.e15
pubmed: 31787378
PLoS Pathog. 2008 May 09;4(5):e1000060
pubmed: 18464894
Nature. 2016 Aug 4;536(7614):48-53
pubmed: 27338953
Science. 2013 Oct 25;342(6157):415
pubmed: 24159024
Cell. 2020 Jul 9;182(1):73-84.e16
pubmed: 32425270
EMBO J. 2009 Oct 21;28(20):3269-76
pubmed: 19713934
Science. 2018 Dec 14;362(6420):1306-1309
pubmed: 30545888
PLoS Negl Trop Dis. 2011 Jun;5(6):e1188
pubmed: 21713020
J Immunol. 2012 Dec 15;189(12):5877-85
pubmed: 23152560
Nat Biomed Eng. 2020 Nov;4(11):1030-1043
pubmed: 32747832
J Infect Dis. 2016 Oct 1;214(7):986-93
pubmed: 26984144
Parasit Vectors. 2017 Aug 31;10(1):406
pubmed: 28859676
Annu Rev Immunol. 2003;21:177-204
pubmed: 12524384
J Virol. 2012 Mar;86(6):2911-8
pubmed: 22238318
Cell Host Microbe. 2007 Apr 19;1(2):135-45
pubmed: 18005691
Sci Transl Med. 2022 Oct 26;14(668):eabo5019
pubmed: 36288280
Viruses. 2011 Sep;3(9):1562-608
pubmed: 21994796
Am J Trop Med Hyg. 2014 Dec;91(6):1203-17
pubmed: 25311700
Front Immunol. 2019 Mar 22;10:553
pubmed: 30984170
J Exp Med. 1990 Mar 1;171(3):597-613
pubmed: 2137852
N Engl J Med. 2015 Jan 8;372(2):113-23
pubmed: 25365753
Immunol Lett. 2004 Mar 29;92(1-2):23-31
pubmed: 15081523
J Immunol. 1990 Apr 15;144(8):3183-6
pubmed: 2139079
Nature. 2020 Aug;584(7821):353-363
pubmed: 32659783
Nature. 2015 Apr 2;520(7545):109-13
pubmed: 25581790
J Virol. 2013 Dec;87(23):12562-75
pubmed: 24027331
PLoS Comput Biol. 2022 Nov 28;18(11):e1010723
pubmed: 36441808
J Infect Dis. 2007 Jun 15;195(12):1808-17
pubmed: 17492597
J Virol. 2015 Apr;89(7):3610-8
pubmed: 25589655
J Exp Med. 2022 Sep 5;219(9):
pubmed: 35938988
Am J Epidemiol. 2000 Nov 1;152(9):793-9; discussion 804
pubmed: 11085389
Lancet. 2015 Jan 31;385(9966):453-65
pubmed: 25230594
PLoS Comput Biol. 2020 Nov 11;16(11):e1008391
pubmed: 33175831
Sci Immunol. 2017 Aug 18;2(14):
pubmed: 28821561
Int J Mol Sci. 2021 Nov 26;22(23):
pubmed: 34884580
Nat Immunol. 2015 Feb;16(2):170-177
pubmed: 25501631
Infect Genet Evol. 2003 May;3(1):19-28
pubmed: 12797969
Blood. 1999 Jun 15;93(12):4387-94
pubmed: 10361137
J Virol. 2009 Jul;83(13):6494-507
pubmed: 19386704
J Virol. 2006 Dec;80(24):12149-59
pubmed: 17035317
Curr Opin Virol. 2020 Aug;43:50-58
pubmed: 32950933
Proc Natl Acad Sci U S A. 2022 May 3;119(18):e2113766119
pubmed: 35486691
EBioMedicine. 2019 Mar;41:465-478
pubmed: 30857944
Cell. 2017 May 04;169(4):597-609.e11
pubmed: 28475892
J Immunol. 2013 Jan 1;190(1):80-7
pubmed: 23203929
Cell Host Microbe. 2021 Nov 10;29(11):1634-1648.e5
pubmed: 34610295
Sci Transl Med. 2021 Jan 20;13(577):
pubmed: 33288661
Immunology. 2018 Jan;153(1):31-41
pubmed: 28898398
Nat Methods. 2017 Nov;14(11):1083-1086
pubmed: 28991892
Nat Microbiol. 2019 Jan;4(1):71-77
pubmed: 30455471
iScience. 2021 Apr 29;24(5):102482
pubmed: 34113823
Nat Microbiol. 2019 May;4(5):854-863
pubmed: 30833735
J Virol. 2016 May 27;90(12):5574-85
pubmed: 27030262
Cell. 2021 Dec 9;184(25):6052-6066.e18
pubmed: 34852239
Immunity. 2005 Jan;22(1):31-42
pubmed: 15664157
Nat Med. 2020 Feb;26(2):228-235
pubmed: 32015557
Virol J. 2008 Jan 09;5:1
pubmed: 18182120
Cell Rep. 2018 Oct 30;25(5):1214-1224
pubmed: 30380413
EBioMedicine. 2020 Apr;54:102733
pubmed: 32315970
J Infect Dis. 2004 Apr 15;189(8):1411-8
pubmed: 15073678
Proc Natl Acad Sci U S A. 2019 Jan 2;116(1):227-232
pubmed: 30518559
J Virol. 2008 Jul;82(13):6631-43
pubmed: 18448542
J Immunol. 1985 Dec;135(6):3878-81
pubmed: 3840825
Acta Crystallogr D Biol Crystallogr. 2013 Mar;69(Pt 3):388-97
pubmed: 23519414
Front Immunol. 2019 Jul 24;10:1694
pubmed: 31396218
Elife. 2017 Sep 05;6:
pubmed: 28871961
Cell. 2022 Dec 8;185(25):4826-4840.e17
pubmed: 36402135
Cell Host Microbe. 2020 Aug 12;28(2):335-349.e6
pubmed: 32504577
Nat Microbiol. 2020 Jun;5(6):796-812
pubmed: 32367055
Cell Host Microbe. 2010 Sep 16;8(3):271-83
pubmed: 20833378
Nature. 2018 May;557(7707):719-723
pubmed: 29795354
mBio. 2013 Nov 19;4(6):e00873-13
pubmed: 24255124
PLoS Negl Trop Dis. 2012;6(3):e1568
pubmed: 22448292
Science. 2017 Nov 17;358(6365):929-932
pubmed: 29097492
J Infect Dis. 2017 Feb 1;215(3):351-358
pubmed: 27932620
Cell Host Microbe. 2020 Jun 10;27(6):963-975.e5
pubmed: 32315598
Mucosal Immunol. 2011 Nov;4(6):590-7
pubmed: 21937984
NPJ Vaccines. 2017 Jan 23;2:2
pubmed: 29263863
Cell Rep. 2020 May 12;31(6):107642
pubmed: 32402275
Cell Rep. 2020 Apr 28;31(4):107584
pubmed: 32348755
J Infect Dis. 2013 Jun 15;207(12):1898-908
pubmed: 23526830
Front Microbiol. 2013 Oct 11;4:305
pubmed: 24130557
J Virol. 2021 Nov 9;95(23):e0095621
pubmed: 34549976
Am J Trop Med Hyg. 2009 Mar;80(3):416-24
pubmed: 19270292
Am J Epidemiol. 1984 Nov;120(5):653-69
pubmed: 6496446
J Exp Med. 2000 Jun 19;191(12):2171-82
pubmed: 10859341
Nat Rev Immunol. 2020 Oct;20(10):633-643
pubmed: 32782358
Virology. 2008 Nov 10;381(1):67-74
pubmed: 18801552
J Virol. 2014 Oct;88(20):11726-37
pubmed: 25078693
Nat Commun. 2023 Feb 13;14(1):798
pubmed: 36781872
Southeast Asian J Trop Med Public Health. 2014 Jan;45(1):53-61
pubmed: 24964654
Rev Inst Med Trop Sao Paulo. 2011 Nov-Dec;53(6):321-3
pubmed: 22183455
Immunology. 2014 Sep;143(1):13-20
pubmed: 24854488
Nat Med. 2017 May;23(5):548-550
pubmed: 28263312
PLoS Pathog. 2023 Aug 28;19(8):e1011616
pubmed: 37639455
MAbs. 2019 Aug/Sep;11(6):1122-1138
pubmed: 31122132
Am J Trop Med Hyg. 1985 Jan;34(1):170-3
pubmed: 3970307
Microbiol Spectr. 2014 Dec;2(6):
pubmed: 26104444
Cell. 2016 Aug 11;166(4):1016-1027
pubmed: 27475895
J Virol. 2006 Feb;80(3):1290-301
pubmed: 16415006
J Immunol. 2001 Jan 1;166(1):346-52
pubmed: 11123311
Cell Rep. 2019 Jan 29;26(5):1104-1111.e4
pubmed: 30699342
Trends Mol Med. 2022 Nov;28(11):979-988
pubmed: 36117072
Am J Trop Med Hyg. 2007 Nov;77(5):910-3
pubmed: 17984352
Sci Transl Med. 2021 Jun 23;13(599):
pubmed: 34162751
Cell Rep. 2016 Aug 9;16(6):1485-1491
pubmed: 27481466
Nat Microbiol. 2019 Sep;4(9):1508-1515
pubmed: 31182801
Vaccine. 2010 Jun 11;28(26):4229-34
pubmed: 20434551
N Engl J Med. 2015 Sep 24;373(13):1195-206
pubmed: 26214039
Cell Rep. 2020 Nov 24;33(8):108430
pubmed: 33238131
Epidemiol Infect. 2020 Jun 29;148:e119
pubmed: 32594967
PLoS Negl Trop Dis. 2016 Feb 05;10(2):e0004398
pubmed: 26848841
J Infect Dis. 2020 Jul 23;222(4):590-600
pubmed: 32193549
Virology. 1990 Feb;174(2):479-93
pubmed: 2129562
J Infect Dis. 2008 Aug 15;198(4):516-24
pubmed: 18598189
PLoS One. 2011;6(11):e27252
pubmed: 22096543
Proc Natl Acad Sci U S A. 2023 Aug 29;120(35):e2216521120
pubmed: 37603748
Science. 2015 Sep 18;349(6254):1338-43
pubmed: 26383952
Nature. 2011 Sep 22;477(7365):466-70
pubmed: 21849977
Elife. 2019 Aug 06;8:
pubmed: 31385805
J Med Virol. 2008 Jan;80(1):134-46
pubmed: 18041019
J Immunol. 1989 Apr 1;142(7):2244-9
pubmed: 2647847
Sci Transl Med. 2020 Jun 10;12(547):
pubmed: 32522807
Science. 2020 Aug 28;369(6507):1123-1128
pubmed: 32855339
Nat Commun. 2020 May 1;11(1):2130
pubmed: 32358588
J Leukoc Biol. 1995 Aug;58(2):256-62
pubmed: 7643018
Science. 2017 Jan 27;355(6323):395-398
pubmed: 28126818
Virology. 2018 Feb;515:191-202
pubmed: 29304471
Microbiol Mol Biol Rev. 2016 Oct 26;80(4):989-1010
pubmed: 27784796
Proc Natl Acad Sci U S A. 2018 Sep 4;115(36):E8378-E8387
pubmed: 30127007
Proc Natl Acad Sci U S A. 2018 Dec 26;115(52):E12363-E12369
pubmed: 30530648

Auteurs

Jay Lubow (J)

Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.

Lisa M Levoir (LM)

Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.

Duncan K Ralph (DK)

Computational Biology Program, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.

Laura Belmont (L)

Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.
Molecular and Cellular Biology Graduate Program, University of Washington, Seattle, Washington, United States of America.

Maya Contreras (M)

Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.

Catiana H Cartwright-Acar (CH)

Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.

Caroline Kikawa (C)

Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.
Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.
Medical Scientist Training Program, University of Washington, Seattle, Washington, United States of America.

Shruthi Kannan (S)

Integral Molecular, Inc., Philadelphia, Pennsylvania, United States of America.

Edgar Davidson (E)

Integral Molecular, Inc., Philadelphia, Pennsylvania, United States of America.

Veronica Duran (V)

Division of Infectious Diseases and Geographic Medicine, Department of Medicine, Stanford University School of Medicine, Stanford, California, United States of America.
Chan Zuckerberg Biohub, San Francisco, California, United States of America.

David E Rebellon-Sanchez (DE)

Clinical Research Center, Fundación Valle del Lili, Cali, Colombia.

Ana M Sanz (AM)

Clinical Research Center, Fundación Valle del Lili, Cali, Colombia.

Fernando Rosso (F)

Clinical Research Center, Fundación Valle del Lili, Cali, Colombia.
Department of Internal Medicine, Division of Infectious Diseases, Fundación Valle del Lili, Cali, Colombia.

Benjamin J Doranz (BJ)

Integral Molecular, Inc., Philadelphia, Pennsylvania, United States of America.

Shirit Einav (S)

Division of Infectious Diseases and Geographic Medicine, Department of Medicine, Stanford University School of Medicine, Stanford, California, United States of America.
Chan Zuckerberg Biohub, San Francisco, California, United States of America.
Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, California, United States of America.

Frederick A Matsen Iv (FA)

Computational Biology Program, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.
Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America.
Department of Statistics, University of Washington, Seattle, Washington, United States of America.
Howard Hughes Medical Institute, Seattle, Washington, United States of America.

Leslie Goo (L)

Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, Washington, United States of America.

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