Apoptotic cell fragments locally activate tingible body macrophages in the germinal center.
B cells
apoptosis
autoimmunity
germinal center
tingible body macrophages
Journal
Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066
Informations de publication
Date de publication:
16 03 2023
16 03 2023
Historique:
received:
23
09
2022
revised:
04
01
2023
accepted:
31
01
2023
pubmed:
4
3
2023
medline:
22
3
2023
entrez:
3
3
2023
Statut:
ppublish
Résumé
Germinal centers (GCs) that form within lymphoid follicles during antibody responses are sites of massive cell death. Tingible body macrophages (TBMs) are tasked with apoptotic cell clearance to prevent secondary necrosis and autoimmune activation by intracellular self antigens. We show by multiple redundant and complementary methods that TBMs derive from a lymph node-resident, CD169-lineage, CSF1R-blockade-resistant precursor that is prepositioned in the follicle. Non-migratory TBMs use cytoplasmic processes to chase and capture migrating dead cell fragments using a "lazy" search strategy. Follicular macrophages activated by the presence of nearby apoptotic cells can mature into TBMs in the absence of GCs. Single-cell transcriptomics identified a TBM cell cluster in immunized lymph nodes which upregulated genes involved in apoptotic cell clearance. Thus, apoptotic B cells in early GCs trigger activation and maturation of follicular macrophages into classical TBMs to clear apoptotic debris and prevent antibody-mediated autoimmune diseases.
Identifiants
pubmed: 36868219
pii: S0092-8674(23)00106-X
doi: 10.1016/j.cell.2023.02.004
pmc: PMC7614509
mid: EMS174789
pii:
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1144-1161.e18Subventions
Organisme : Wellcome Trust
ID : 220219
Pays : United Kingdom
Organisme : Medical Research Council
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 220219/Z/20/Z
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Informations de copyright
Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests The authors declare no competing interests.
Références
Nat Rev Immunol. 2020 Apr;20(4):254-267
pubmed: 31822793
Nat Med. 2016 Jan;22(1):64-71
pubmed: 26692332
Immunity. 2015 Apr 21;42(4):704-18
pubmed: 25840682
Anat Rec. 1991 Apr;229(4):511-20
pubmed: 2048755
Proc Natl Acad Sci U S A. 2008 Aug 5;105(31):10871-6
pubmed: 18663225
Immunol Cell Biol. 2010 May-Jun;88(4):438-44
pubmed: 20066001
Nature. 2007 Mar 1;446(7131):83-7
pubmed: 17268470
J Autoimmun. 2007 Mar-May;28(2-3):114-21
pubmed: 17368845
Science. 2004 May 21;304(5674):1147-50
pubmed: 15155946
Cell. 2021 Mar 4;184(5):1330-1347.e13
pubmed: 33636130
Lupus. 2008 May;17(5):371-5
pubmed: 18490410
Cell Rep. 2017 Mar 7;18(10):2427-2440
pubmed: 28273457
J Leukoc Biol. 2012 Sep;92(3):489-97
pubmed: 22715140
Annu Rev Pathol. 2020 Jan 24;15:123-147
pubmed: 31530089
Nature. 2001 May 10;411(6834):207-11
pubmed: 11346799
Nat Immunol. 2013 Oct;14(10):986-95
pubmed: 24048120
Immunol Cell Biol. 1998 Feb;76(1):34-40
pubmed: 9553774
Immunity. 2007 May;26(5):655-67
pubmed: 17509908
J Exp Med. 1983 Nov 1;158(5):1522-36
pubmed: 6355361
J Biol Chem. 2011 Sep 23;286(38):33335-44
pubmed: 21828049
Proc Natl Acad Sci U S A. 2004 Mar 23;101(12):4164-9
pubmed: 15016911
Nat Neurosci. 2010 Jan;13(1):133-40
pubmed: 20023653
Immunity. 2013 Jan 24;38(1):79-91
pubmed: 23273845
Immunity. 2015 Sep 15;43(3):502-14
pubmed: 26341401
J Biol Chem. 1998 Sep 4;273(36):23376-80
pubmed: 9722572
Immunity. 2017 Aug 15;47(2):349-362.e5
pubmed: 28801233
Annu Rev Immunol. 2022 Apr 26;40:413-442
pubmed: 35113731
Sci Immunol. 2022 Mar 11;7(69):eabm0775
pubmed: 35275753
Blood. 2003 Feb 1;101(3):1155-63
pubmed: 12393599
Immunity. 2020 Jun 16;52(6):957-970
pubmed: 32553181
Cell Syst. 2018 Dec 26;7(6):656-666.e4
pubmed: 30528274
Nat Methods. 2017 Sep;14(9):865-868
pubmed: 28759029
PLoS Biol. 2020 Oct 8;18(10):e3000859
pubmed: 33031383
Immunobiology. 1998 Aug;199(2):265-85
pubmed: 9777411
Nat Immunol. 2009 Jul;10(7):786-93
pubmed: 19503106
Dev Immunol. 1998;6(3-4):285-94
pubmed: 9814602
Cell Tissue Res. 1998 May;292(2):311-23
pubmed: 9560474
Trends Immunol. 2019 Jan;40(1):35-48
pubmed: 30502023
J Exp Med. 2008 Jun 9;205(6):1293-302
pubmed: 18490487
Nat Rev Immunol. 2014 Jun;14(6):361-76
pubmed: 24854588
Trends Cell Biol. 2015 Nov;25(11):639-650
pubmed: 26437594
Immunol Rev. 2020 Jul;296(1):62-86
pubmed: 32472583
Immunity. 2019 Jun 18;50(6):1453-1466.e4
pubmed: 31053503
Clin Immunol. 2009 Oct;133(1):138-44
pubmed: 19631584
Nat Immunol. 2007 Sep;8(9):992-1000
pubmed: 17660822
J Leukoc Biol. 2007 Jul;82(1):111-23
pubmed: 17438263
J Invest Dermatol. 2006 Apr;126(4):787-96
pubmed: 16439974
BMC Biotechnol. 2002 Jun 11;2:11
pubmed: 12079497
Science. 2007 Jan 26;315(5811):528-31
pubmed: 17185562
Sci Rep. 2014 Aug 12;4:6030
pubmed: 25112380
Front Immunol. 2018 Jul 04;9:1553
pubmed: 30022984
Nat Commun. 2019 Jul 19;10(1):3215
pubmed: 31324781
EMBO J. 2015 Apr 1;34(7):925-39
pubmed: 25630702
Science. 2015 Feb 6;347(6222):667-72
pubmed: 25657250
Nat Commun. 2018 Aug 22;9(1):3372
pubmed: 30135429
Immunol Res. 2011 Dec;51(2-3):125-33
pubmed: 22038528
Anat Rec. 1988 Dec;222(4):380-90
pubmed: 2465705
Apoptosis. 2008 Apr;13(4):463-82
pubmed: 18322800
Immunity. 2018 Sep 18;49(3):477-489.e7
pubmed: 30231983
Nat Methods. 2005 Jun;2(6):419-26
pubmed: 15908920
J Am Soc Nephrol. 2015 Apr;26(4):896-906
pubmed: 25266072
Annu Rev Immunol. 2018 Apr 26;36:489-517
pubmed: 29400998
Genome Biol. 2021 Jan 27;22(1):50
pubmed: 33504367
Curr Biol. 2012 May 8;22(9):830-6
pubmed: 22503503
J Cell Biol. 1963 Dec;19:641-6
pubmed: 14086143
Blood. 2014 Oct 9;124(15):e33-44
pubmed: 25030063
Cell Rep. 2021 Nov 23;37(8):110058
pubmed: 34818538
Methods Cell Biol. 2013;113:311-23
pubmed: 23317908
J R Soc Interface. 2016 Sep;13(122):
pubmed: 27628175
BMC Dev Biol. 2009 Sep 09;9:49
pubmed: 19740427
J Exp Med. 2003 Apr 7;197(7):845-60
pubmed: 12668643
J Immunol. 2010 Nov 15;185(10):5859-68
pubmed: 20952679
Science. 2017 Oct 13;358(6360):
pubmed: 28935768
J Immunol. 2020 Dec 1;205(11):3154-3166
pubmed: 33139489
Immunity. 2017 Aug 15;47(2):374-388.e6
pubmed: 28813662
Annu Rev Immunol. 2018 Apr 26;36:339-357
pubmed: 29356584
Mol Cell Biol. 2000 Jun;20(11):4106-14
pubmed: 10805752
Trends Immunol. 2019 Feb;40(2):98-112
pubmed: 30579704
Annu Rev Immunol. 2021 Apr 26;39:313-344
pubmed: 33902313
Arthritis Rheum. 2002 Jan;46(1):191-201
pubmed: 11817590
PLoS One. 2012;7(6):e38258
pubmed: 22675532
PLoS Comput Biol. 2016 Sep 02;12(9):e1005082
pubmed: 27589606
Science. 2005 May 27;308(5726):1314-8
pubmed: 15831717
J Cell Sci. 1993 Apr;104 ( Pt 4):1021-9
pubmed: 8314887
Apoptosis. 2017 Oct;22(10):1189-1204
pubmed: 28861714
Blood. 2010 Nov 11;116(19):3955-63
pubmed: 20682855
Nat Rev Immunol. 2016 Mar;16(3):193-201
pubmed: 26852928