Single-cell analysis reveals dynamics of human B cell differentiation and identifies novel B and antibody-secreting cell intermediates.

B cell antibody-secreting cell cell biology differentiation human immunology inflammation single-cell RNA sequencing

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
02 03 2023
Historique:
received: 20 09 2022
accepted: 24 02 2023
pubmed: 3 3 2023
medline: 15 3 2023
entrez: 2 3 2023
Statut: epublish

Résumé

Differentiation of B cells into antibody-secreting cells (ASCs) is a key process to generate protective humoral immunity. A detailed understanding of the cues controlling ASC differentiation is important to devise strategies to modulate antibody formation. Here, we dissected differentiation trajectories of human naive B cells into ASCs using single-cell RNA sequencing. By comparing transcriptomes of B cells at different stages of differentiation from an in vitro model with ex vivo B cells and ASCs, we uncovered a novel pre-ASC population present ex vivo in lymphoid tissues. For the first time, a germinal-center-like population is identified in vitro from human naive B cells and possibly progresses into a memory B cell population through an alternative route of differentiation, thus recapitulating in vivo human GC reactions. Our work allows further detailed characterization of human B cell differentiation into ASCs or memory B cells in both healthy and diseased conditions.

Identifiants

pubmed: 36861964
doi: 10.7554/eLife.83578
pii: 83578
pmc: PMC10005767
doi:
pii:

Banques de données

GEO
['GSE214265', 'GSE12366', 'GSE137275']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023, Verstegen, Pollastro et al.

Déclaration de conflit d'intérêts

NV, SP, PU, CM, GE, TJ, MS, KB, KH, TR, JS, At, MB, Sv No competing interests declared

Références

Bioinformatics. 2010 Feb 15;26(4):493-500
pubmed: 20022975
Annu Rev Immunol. 2022 Apr 26;40:413-442
pubmed: 35113731
Nat Rev Immunol. 2020 Apr;20(4):229-238
pubmed: 31836872
J Exp Med. 2009 May 11;206(5):991-9
pubmed: 19380637
J Biol Chem. 2007 Mar 9;282(10):7591-605
pubmed: 17213195
Bioinformatics. 2017 Feb 1;33(3):425-427
pubmed: 28172415
Blood. 1990 Nov 1;76(9):1739-47
pubmed: 2224123
J Biol Chem. 2014 Mar 7;289(10):7011-7024
pubmed: 24469453
EMBO J. 2017 Dec 15;36(24):3619-3633
pubmed: 29030486
J Exp Med. 1998 Nov 2;188(9):1691-703
pubmed: 9802981
J Immunol. 2010 Jul 1;185(1):190-202
pubmed: 20525889
Immunity. 2015 Dec 15;43(6):1064-74
pubmed: 26620759
Blood. 2012 Sep 13;120(11):2240-8
pubmed: 22740445
Genome Med. 2018 Mar 20;10(1):20
pubmed: 29558968
Eur J Immunol. 2011 Feb;41(2):491-502
pubmed: 21268018
J Exp Med. 2020 Oct 5;217(10):
pubmed: 32603407
Nat Protoc. 2014 Jan;9(1):171-81
pubmed: 24385147
Cells. 2021 May 12;10(5):
pubmed: 34066151
Nat Methods. 2018 Aug;15(8):563-565
pubmed: 30065371
Front Immunol. 2021 Sep 20;12:734282
pubmed: 34616402
Genes Dev. 2018 Jan 15;32(2):112-126
pubmed: 29440259
Nat Biotechnol. 2020 Dec;38(12):1408-1414
pubmed: 32747759
Blood. 2008 Mar 1;111(5):2755-64
pubmed: 18180376
Blood. 2009 Apr 16;113(16):3706-15
pubmed: 19023113
Nat Rev Immunol. 2006 Oct;6(10):741-50
pubmed: 16977339
Nat Immunol. 2016 Mar;17(3):331-43
pubmed: 26779602
Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Annu Rev Immunol. 2008;26:741-66
pubmed: 18173374
Nat Biotechnol. 2019 May;37(5):547-554
pubmed: 30936559
Leuk Res. 1996 Jun;20(6):507-15
pubmed: 8709623
Cell. 2021 Jun 24;184(13):3573-3587.e29
pubmed: 34062119
Cell Rep. 2021 Feb 9;34(6):108684
pubmed: 33567273
Mol Syst Biol. 2021 Aug;17(8):e10282
pubmed: 34435732
J Immunol. 2018 Dec 15;201(12):3569-3579
pubmed: 30446568
Proc Natl Acad Sci U S A. 2019 May 7;116(19):9511-9520
pubmed: 31000603
Blood. 2019 Mar 7;133(10):1119-1129
pubmed: 30591526
Nat Immunol. 2012 Nov;13(11):1092-100
pubmed: 23001146
Immunity. 2021 Oct 12;54(10):2256-2272.e6
pubmed: 34555336
Immunity. 2021 Sep 14;54(9):2005-2023.e10
pubmed: 34525339
J Immunol. 2007 Dec 15;179(12):8180-90
pubmed: 18056361
Nat Commun. 2011 Sep 06;2:465
pubmed: 21897376
Immunity. 2015 Jul 21;43(1):132-45
pubmed: 26187412
F1000Res. 2015 Dec 30;4:1521
pubmed: 26925227
Nat Biotechnol. 2018 Jun;36(5):411-420
pubmed: 29608179
Nat Immunol. 2009 Apr;10(4):385-93
pubmed: 19252490
Cell Syst. 2015 Dec 23;1(6):417-425
pubmed: 26771021
Nat Commun. 2017 May 05;8:15081
pubmed: 28474673
Elife. 2019 Dec 09;8:
pubmed: 31815664
Nat Commun. 2018 May 1;9(1):1758
pubmed: 29717110
Front Immunol. 2020 Mar 03;11:216
pubmed: 32194545
Nat Immunol. 2013 Mar;14(3):298-305
pubmed: 23354484
Bioinformatics. 2018 Aug 15;34(16):2846-2847
pubmed: 29659703
Nat Immunol. 2018 Sep;19(9):1013-1024
pubmed: 30104629
Blood. 2003 Jul 15;102(2):592-600
pubmed: 12663452
EMBO J. 1997 Jun 2;16(11):2996-3006
pubmed: 9214617
J Immunol. 2021 Aug 15;207(4):1018-1032
pubmed: 34330755
Genome Biol. 2019 Mar 19;20(1):59
pubmed: 30890159
Nat Commun. 2017 Oct 12;8(1):877
pubmed: 29026085
J Immunol. 2009 Jun 15;182(12):7473-81
pubmed: 19494270
Elife. 2019 Jun 03;8:
pubmed: 31157616
Front Immunol. 2019 Oct 18;10:2458
pubmed: 31681331
J Immunol. 2003 Aug 15;171(4):1684-90
pubmed: 12902466
Adv Immunol. 2010;105:193-210
pubmed: 20510734
Elife. 2023 Mar 02;12:
pubmed: 36861964
Immunity. 2015 Dec 15;43(6):1075-86
pubmed: 26620760
J Exp Med. 2009 May 11;206(5):1001-7
pubmed: 19380638
Nature. 2021 Oct;598(7880):327-331
pubmed: 34588693
Immunity. 2016 Jan 19;44(1):116-130
pubmed: 26795247
Nat Immunol. 2020 Sep;21(9):1082-1093
pubmed: 32601467
Nat Immunol. 2012 Nov;13(11):1083-91
pubmed: 23001145
Cell Regul. 1989 Nov;1(1):27-35
pubmed: 2519615
Blood. 1987 Nov;70(5):1316-24
pubmed: 3117132

Auteurs

Niels J M Verstegen (NJM)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
Synthetic Systems Biology and Nuclear Organization, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, Netherlands.

Sabrina Pollastro (S)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.

Peter-Paul A Unger (PA)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.

Casper Marsman (C)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.

George Elias (G)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.

Tineke Jorritsma (T)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.

Marij Streutker (M)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.

Kevin Bassler (K)

Genomics and Immunoregulation, University of Bonn, Bonn, Germany.

Kristian Haendler (K)

Genomics and Immunoregulation, University of Bonn, Bonn, Germany.
Platform for Single Cell Genomics and Epigenomics, German Center for Neurodegenerative Diseases (DZNE), University of Bonn, Bonn, Germany.

Theo Rispens (T)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.

Joachim L Schultze (JL)

Genomics and Immunoregulation, University of Bonn, Bonn, Germany.
Platform for Single Cell Genomics and Epigenomics, German Center for Neurodegenerative Diseases (DZNE), University of Bonn, Bonn, Germany.

Anja Ten Brinke (A)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.

Marc Beyer (M)

Genomics and Immunoregulation, University of Bonn, Bonn, Germany.
Platform for Single Cell Genomics and Epigenomics, German Center for Neurodegenerative Diseases (DZNE), University of Bonn, Bonn, Germany.
Immunogenomics & Neurodegeneration, German Center for Neurodegenerative Diseases, Bonn, Germany.

S Marieke van Ham (SM)

Department of Immunopathology, Sanquin Research and Landsteiner Laboratory, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, Netherlands.

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