Activation-induced deaminase is critical for the establishment of DNA methylation patterns prior to the germinal center reaction.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
21 05 2021
Historique:
accepted: 19 04 2021
revised: 15 04 2021
received: 07 02 2020
pubmed: 6 5 2021
medline: 7 7 2021
entrez: 5 5 2021
Statut: ppublish

Résumé

Activation-induced deaminase (AID) initiates antibody diversification in germinal center B cells by deaminating cytosines, leading to somatic hypermutation and class-switch recombination. Loss-of-function mutations in AID lead to hyper-IgM syndrome type 2 (HIGM2), a rare human primary antibody deficiency. AID-mediated deamination has been proposed as leading to active demethylation of 5-methycytosines in the DNA, although evidence both supports and casts doubt on such a role. In this study, using whole-genome bisulfite sequencing of HIGM2 B cells, we investigated direct AID involvement in active DNA demethylation. HIGM2 naïve and memory B cells both display widespread DNA methylation alterations, of which ∼25% are attributable to active DNA demethylation. For genes that undergo active demethylation that is impaired in HIGM2 individuals, our analysis indicates that AID is not directly involved. We demonstrate that the widespread alterations in the DNA methylation and expression profiles of HIGM2 naïve B cells result from premature overstimulation of the B-cell receptor prior to the germinal center reaction. Our data support a role for AID in B cell central tolerance in preventing the expansion of autoreactive cell clones, affecting the correct establishment of DNA methylation patterns.

Identifiants

pubmed: 33950194
pii: 6266447
doi: 10.1093/nar/gkab322
pmc: PMC8136777
doi:

Substances chimiques

Receptors, Antigen, B-Cell 0
AICDA (activation-induced cytidine deaminase) EC 3.5.4.-
Cytidine Deaminase EC 3.5.4.5

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

5057-5073

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.

Références

Genome Biol. 2010 Jan 12;11(1):R3
pubmed: 20067622
Nat Rev Immunol. 2006 Oct;6(10):728-40
pubmed: 16998507
J Immunol. 2013 Nov 15;191(10):4926-39
pubmed: 24108696
J Biol Chem. 1999 Jun 25;274(26):18470-6
pubmed: 10373455
Science. 2002 Feb 15;295(5558):1301-6
pubmed: 11847344
PLoS One. 2013 Jul 29;8(7):e69815
pubmed: 23922811
Sci Immunol. 2019 Apr 26;4(34):
pubmed: 31028100
Immunity. 2015 Nov 17;43(5):884-95
pubmed: 26546282
Nat Immunol. 2013 Jul;14(7):749-55
pubmed: 23708250
Nat Struct Mol Biol. 2014 Jan;21(1):110-2
pubmed: 24336222
Nat Genet. 2015 Jul;47(7):746-56
pubmed: 26053498
Cancer Res. 2018 Feb 1;78(3):769-780
pubmed: 29229604
Bioinformatics. 2010 Mar 1;26(5):589-95
pubmed: 20080505
Nature. 2010 Feb 25;463(7284):1042-7
pubmed: 20027182
Mol Immunol. 2005 Mar;42(5):599-604
pubmed: 15607819
Cell. 2014 Dec 18;159(7):1538-48
pubmed: 25483776
Genome Res. 2014 Feb;24(2):177-84
pubmed: 24068705
Nat Immunol. 2011 Jun;12(6):536-43
pubmed: 21572431
Cell. 2011 Sep 30;147(1):107-19
pubmed: 21962511
Nature. 2010 Aug 26;466(7310):1129-33
pubmed: 20639862
Immunity. 2016 Nov 15;45(5):1148-1161
pubmed: 27851915
Adv Immunol. 2014;122:253-77
pubmed: 24507160
Cell Rep. 2015 Sep 29;12(12):2086-98
pubmed: 26365193
Cell. 2011 Sep 30;147(1):95-106
pubmed: 21962510
Cell. 2000 Sep 1;102(5):553-63
pubmed: 11007474
Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11554-9
pubmed: 21700883
Nature. 2010 Apr 15;464(7291):993-8
pubmed: 20393554
Hum Mutat. 2006 Dec;27(12):1185-91
pubmed: 16964591
Nature. 2009 Nov 19;462(7271):315-22
pubmed: 19829295
J Virol. 2004 Apr;78(8):4108-19
pubmed: 15047827
J Allergy Clin Immunol Pract. 2019 Jul - Aug;7(6):1763-1770
pubmed: 30776527
Science. 2009 May 15;324(5929):930-5
pubmed: 19372391
Bioinformatics. 2018 May 15;34(10):1781-1783
pubmed: 29329372
Cell. 2013 Apr 11;153(2):307-19
pubmed: 23582322
Nucleic Acids Res. 2016 Jan 8;44(1):75-94
pubmed: 26635396
Clin Immunol. 2004 Jan;110(1):22-9
pubmed: 14962793
Nat Protoc. 2013 Oct;8(10):2022-32
pubmed: 24071908
Nat Chem Biol. 2012 Sep;8(9):751-8
pubmed: 22772155
Annu Rev Immunol. 2002;20:165-96
pubmed: 11861601
Cell. 2014 Dec 18;159(7):1524-37
pubmed: 25483777
Nat Genet. 2016 Mar;48(3):253-64
pubmed: 26780610
Immunity. 2013 May 23;38(5):918-29
pubmed: 23684984
Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11560-5
pubmed: 21700885
Nat Biotechnol. 2010 May;28(5):495-501
pubmed: 20436461
Trends Biochem Sci. 2015 Mar;40(3):172-81
pubmed: 25661247
Nat Genet. 2018 Apr;50(4):591-602
pubmed: 29610480
J Biol Chem. 2004 Dec 10;279(50):52353-60
pubmed: 15448152
Nucleic Acids Res. 2013 May 1;41(10):5457-68
pubmed: 23585279
Blood. 2009 Jul 16;114(3):547-54
pubmed: 19478044
Nature. 2017 Mar 2;543(7643):72-77
pubmed: 28225755
Cell Host Microbe. 2017 May 10;21(5):580-591.e7
pubmed: 28494239
J Exp Med. 2018 Mar 5;215(3):761-771
pubmed: 29374026
Blood. 2007 Nov 15;110(10):3715-21
pubmed: 17682125
Cell. 2000 Sep 1;102(5):565-75
pubmed: 11007475
Nat Rev Genet. 2017 Sep;18(9):517-534
pubmed: 28555658
Science. 2004 Oct 22;306(5696):636-40
pubmed: 15499007
Nucleic Acids Res. 2012 Oct;40(18):9206-17
pubmed: 22798497
Blood. 2016 Feb 4;127(5):572-81
pubmed: 26660426
Immunity. 2018 Feb 20;48(2):313-326.e5
pubmed: 29396161
Biochim Biophys Acta. 1992 Nov 15;1171(1):11-8
pubmed: 1420357
Cell. 2008 Dec 26;135(7):1201-12
pubmed: 19109892

Auteurs

Francesc Català-Moll (F)

Epigenetics and Immune Disease Group, Josep Carreras Research Institute (IJC), 08916 Badalona, Barcelona, Spain.
Chromatin and Disease Group, Cancer Epigenetics and Biology Programme (PEBC), Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Spain.

Anna G Ferreté-Bonastre (AG)

Epigenetics and Immune Disease Group, Josep Carreras Research Institute (IJC), 08916 Badalona, Barcelona, Spain.
Chromatin and Disease Group, Cancer Epigenetics and Biology Programme (PEBC), Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Spain.

Tianlu Li (T)

Epigenetics and Immune Disease Group, Josep Carreras Research Institute (IJC), 08916 Badalona, Barcelona, Spain.
Chromatin and Disease Group, Cancer Epigenetics and Biology Programme (PEBC), Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Spain.

Dieter Weichenhan (D)

Division of Cancer Epigenomics, German Cancer Research Center (DKFZ), Heidelberg 69120, Germany.

Pavlo Lutsik (P)

Division of Cancer Epigenomics, German Cancer Research Center (DKFZ), Heidelberg 69120, Germany.

Laura Ciudad (L)

Epigenetics and Immune Disease Group, Josep Carreras Research Institute (IJC), 08916 Badalona, Barcelona, Spain.
Chromatin and Disease Group, Cancer Epigenetics and Biology Programme (PEBC), Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Spain.

Ángel F Álvarez-Prado (ÁF)

B Cell Biology Laboratory, Centro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC), 28029 Madrid, Spain.

Javier Rodríguez-Ubreva (J)

Epigenetics and Immune Disease Group, Josep Carreras Research Institute (IJC), 08916 Badalona, Barcelona, Spain.
Chromatin and Disease Group, Cancer Epigenetics and Biology Programme (PEBC), Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Spain.

Christian Klemann (C)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency (CCI), Medical Center, Faculty of Medicine, University of Freiburg, 79110 Freiburg, Germany.

Carsten Speckmann (C)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency (CCI), Medical Center, Faculty of Medicine, University of Freiburg, 79110 Freiburg, Germany.
Faculty of Medicine, Center for Pediatrics and Adolescent Medicine, Medical Center, University of Freiburg, Germany.

Amaya Vilas-Zornoza (A)

Center for Applied Medical Research (CIMA), University of Navarra, 31008 Pamplona, Spain.

Hassan Abolhassani (H)

Division of Clinical Immunology, Department of Laboratory Medicine, Karolinska Institutet, Karolinska University Hospital Huddinge, SE 14186 Stockholm , Sweden.

Mónica Martínez-Gallo (M)

Immunology Division, Hospital Universitari Vall d'Hebron and Diagnostic Immunology Research Group, Vall d'Hebron Research Institute (VHIR), Barcelona, Spain.

Romina Dieli-Crimi (R)

Immunology Division, Hospital Universitari Vall d'Hebron and Diagnostic Immunology Research Group, Vall d'Hebron Research Institute (VHIR), Barcelona, Spain.

Jacques G Rivière (JG)

Pediatric Infectious Diseases & Immunodeficiencies Unit, Hospital Universitari Vall d'Hebron, Vall d'Hebron Research Institute (VHIR), Autonomous University of Barcelona, Barcelona, Spain.
Infection in Immunocompromised Pediatric Patients Research Group, Vall d'Hebron Institut de Recerca (VHIR), Hospital Universitari Vall d'Hebron, 08035 Barcelona, Spain.
Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiencies, Barcelona, Spain.

Andrea Martín-Nalda (A)

Pediatric Infectious Diseases & Immunodeficiencies Unit, Hospital Universitari Vall d'Hebron, Vall d'Hebron Research Institute (VHIR), Autonomous University of Barcelona, Barcelona, Spain.
Infection in Immunocompromised Pediatric Patients Research Group, Vall d'Hebron Institut de Recerca (VHIR), Hospital Universitari Vall d'Hebron, 08035 Barcelona, Spain.
Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiencies, Barcelona, Spain.

Roger Colobran (R)

Immunology Division, Hospital Universitari Vall d'Hebron and Diagnostic Immunology Research Group, Vall d'Hebron Research Institute (VHIR), Barcelona, Spain.
Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiencies, Barcelona, Spain.
Department of Cell Biology, Physiology and Immunology, Universitat Autònoma de Barcelona (UAB), Bellaterra, Catalonia, Spain.

Pere Soler-Palacín (P)

Pediatric Infectious Diseases & Immunodeficiencies Unit, Hospital Universitari Vall d'Hebron, Vall d'Hebron Research Institute (VHIR), Autonomous University of Barcelona, Barcelona, Spain.
Infection in Immunocompromised Pediatric Patients Research Group, Vall d'Hebron Institut de Recerca (VHIR), Hospital Universitari Vall d'Hebron, 08035 Barcelona, Spain.
Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiencies, Barcelona, Spain.

Sven Kracker (S)

Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163, Université de Paris, Paris, France.

Lennart Hammarström (L)

Division of Clinical Immunology, Department of Laboratory Medicine, Karolinska Institutet, Karolinska University Hospital Huddinge, SE 14186 Stockholm , Sweden.

Felipe Prosper (F)

Center for Applied Medical Research (CIMA), University of Navarra, 31008 Pamplona, Spain.

Anne Durandy (A)

Laboratory of Human Lymphohematopoiesis, Imagine Institute, INSERM UMR 1163, Université de Paris, Paris, France.

Bodo Grimbacher (B)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency (CCI), Medical Center, Faculty of Medicine, University of Freiburg, 79110 Freiburg, Germany.
German Center for Infection Research (DZIF), Satellite Center Freiburg, Germany.
Centre for Integrative Biological Signalling Studies (CIBSS), Albert-Ludwigs University, Freiburg, Germany.
RESIST, Cluster of Excellence 2155 to Hanover Medical School, Satellite Center Freiburg, Germany.
Institute of Immunity & Transplantation, Royal Free Hospital, University College London, UK.

Christoph Plass (C)

Division of Cancer Epigenomics, German Cancer Research Center (DKFZ), Heidelberg 69120, Germany.

Esteban Ballestar (E)

Epigenetics and Immune Disease Group, Josep Carreras Research Institute (IJC), 08916 Badalona, Barcelona, Spain.
Chromatin and Disease Group, Cancer Epigenetics and Biology Programme (PEBC), Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Spain.

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