Histone methyltransferase DOT1L controls state-specific identity during B cell differentiation.


Journal

EMBO reports
ISSN: 1469-3178
Titre abrégé: EMBO Rep
Pays: England
ID NLM: 100963049

Informations de publication

Date de publication:
03 02 2021
Historique:
received: 26 06 2020
revised: 01 12 2020
accepted: 08 12 2020
pubmed: 8 1 2021
medline: 1 6 2021
entrez: 7 1 2021
Statut: ppublish

Résumé

Differentiation of naïve peripheral B cells into terminally differentiated plasma cells is characterized by epigenetic alterations, yet the epigenetic mechanisms that control B-cell fate remain unclear. Here, we identified a role for the histone H3K79 methyltransferase DOT1L in controlling B-cell differentiation. Mouse B cells lacking Dot1L failed to establish germinal centers (GC) and normal humoral immune responses in vivo. In vitro, activated B cells in which Dot1L was deleted showed aberrant differentiation and prematurely acquired plasma cell characteristics. Similar results were obtained when DOT1L was chemically inhibited in mature B cells in vitro. Mechanistically, combined epigenomics and transcriptomics analysis revealed that DOT1L promotes expression of a pro-proliferative, pro-GC program. In addition, DOT1L indirectly supports the repression of an anti-proliferative plasma cell differentiation program by maintaining the repression of Polycomb Repressor Complex 2 (PRC2) targets. Our findings show that DOT1L is a key modulator of the core transcriptional and epigenetic landscape in B cells, establishing an epigenetic barrier that warrants B-cell naivety and GC B-cell differentiation.

Identifiants

pubmed: 33410591
doi: 10.15252/embr.202051184
pmc: PMC7857439
doi:

Substances chimiques

Histones 0
Dot1l protein, mouse EC 2.1.1.-
Methyltransferases EC 2.1.1.-
Histone-Lysine N-Methyltransferase EC 2.1.1.43

Banques de données

GEO
['GSE138909', 'GSE138906']

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e51184

Informations de copyright

© 2021 The Authors. Published under the terms of the CC BY NC ND 4.0 license.

Références

Nat Commun. 2019 Jun 26;10(1):2803
pubmed: 31243293
Biomolecules. 2018 Feb 27;8(1):
pubmed: 29495487
Blood. 2013 Aug 8;122(6):1017-25
pubmed: 23801631
EMBO J. 2019 Jul 15;38(14):e101564
pubmed: 31304633
Haematologica. 2019 Jan;104(1):155-165
pubmed: 30171029
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Nat Immunol. 2006 Jul;7(7):773-82
pubmed: 16767092
Cancer Res. 2017 May 1;77(9):2522-2533
pubmed: 28209620
Mol Cell. 2013 Sep 12;51(5):647-61
pubmed: 24034696
Cell. 2007 Feb 23;128(4):707-19
pubmed: 17320508
Bioinformatics. 2010 Sep 1;26(17):2176-82
pubmed: 20610611
Nat Immunol. 2003 Feb;4(2):124-31
pubmed: 12496962
Cancer Cell. 2013 May 13;23(5):677-92
pubmed: 23680150
Nat Immunol. 2015 Jun;16(6):663-73
pubmed: 25894659
Clin Epigenetics. 2019 Jan 7;11(1):4
pubmed: 30616689
Cold Spring Harb Perspect Biol. 2014 Jun 02;6(6):
pubmed: 24890513
Nat Genet. 2008 Jul;40(7):897-903
pubmed: 18552846
Blood. 2010 Nov 25;116(22):4483-91
pubmed: 20798234
Cancer Cell. 2011 Jul 12;20(1):66-78
pubmed: 21741597
Blood. 2018 Jun 14;131(24):2661-2669
pubmed: 29724899
Cancer Cell. 2011 Jul 12;20(1):53-65
pubmed: 21741596
Nucleic Acids Res. 2012 May;40(10):4288-97
pubmed: 22287627
Clin Epigenetics. 2019 Dec 30;11(1):199
pubmed: 31888761
Leukemia. 2014 Nov;28(11):2131-8
pubmed: 24854991
Nat Commun. 2016 Aug 10;7:12284
pubmed: 27506838
Nat Chem Biol. 2021 Jan;17(1):47-56
pubmed: 32807969
EMBO Rep. 2011 Sep 01;12(9):956-62
pubmed: 21760613
Clin Rev Allergy Immunol. 2016 Jun;50(3):301-11
pubmed: 26066671
Mol Cell. 2013 Jun 27;50(6):894-907
pubmed: 23806335
Mol Cancer Res. 2011 Apr;9(4):418-29
pubmed: 21383005
Proc Natl Acad Sci U S A. 2020 Aug 25;117(34):20706-20716
pubmed: 32764145
Front Immunol. 2019 Mar 12;10:438
pubmed: 30915081
Semin Cancer Biol. 2018 Aug;51:139-148
pubmed: 28851627
Nature. 1996 Jun 27;381(6585):751-8
pubmed: 8657279
EMBO Rep. 2021 Feb 3;22(2):e51184
pubmed: 33410591
Nat Rev Immunol. 2006 Aug;6(8):573-83
pubmed: 16868548
Mol Cell. 2019 Jan 3;73(1):61-72.e3
pubmed: 30472189
Trends Immunol. 2004 Jan;25(1):17-24
pubmed: 14698280
Nat Struct Mol Biol. 2010 Dec;17(12):1495-9
pubmed: 21057525
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
Cancer Cell. 2016 Aug 8;30(2):197-213
pubmed: 27505670
Nat Med. 2015 Oct;21(10):1190-8
pubmed: 26366712
Nature. 2004 Jun 3;429(6991):566-71
pubmed: 15152264
Nat Commun. 2020 Aug 19;11(1):4153
pubmed: 32814769
Blood. 2017 May 18;129(20):2749-2759
pubmed: 28381397
Cell. 2002 Jun 14;109(6):745-56
pubmed: 12086673
Epigenetics. 2009 Oct 1;4(7):462-8
pubmed: 19875937
Annu Rev Immunol. 2012;30:429-57
pubmed: 22224772
Nat Immunol. 2012 Nov;13(11):1092-100
pubmed: 23001146
Chromosoma. 2016 Sep;125(4):593-605
pubmed: 26728620
Nat Commun. 2018 Apr 27;9(1):1698
pubmed: 29703886
PLoS Genet. 2008 Sep 12;4(9):e1000190
pubmed: 18787701
Annu Rev Biochem. 2007;76:1-22
pubmed: 17328676
Nat Struct Mol Biol. 2008 Jun;15(6):550-7
pubmed: 18511943
Genes Dev. 2011 Jul 1;25(13):1345-58
pubmed: 21724828
Annu Rev Immunol. 2008;26:133-69
pubmed: 18370921
Nat Cell Biol. 2006 Sep;8(9):1017-24
pubmed: 16921363
J Biol Chem. 2006 Jun 30;281(26):18059-68
pubmed: 16636056
Nat Commun. 2020 Oct 15;11(1):5200
pubmed: 33060580
EMBO J. 2010 Dec 1;29(23):4048-61
pubmed: 20953163
Am J Physiol Cell Physiol. 2006 Mar;290(3):C936-46
pubmed: 16236820
Nature. 2020 Sep;585(7824):277-282
pubmed: 32879489
Blood. 2008 Sep 1;112(5):1570-80
pubmed: 18725575
Nat Med. 2015 Apr;21(4):335-43
pubmed: 25822366
Nat Rev Immunol. 2012 Jun 25;12(7):517-31
pubmed: 22728528
Nature. 2004 Nov 18;432(7015):406-11
pubmed: 15525939
Oncotarget. 2020 Mar 17;11(11):956-968
pubmed: 32215184
Infect Immun. 1982 Feb;35(2):507-14
pubmed: 6460001
Mol Cell Biol. 2008 Apr;28(8):2825-39
pubmed: 18285465
Nat Commun. 2017 Oct 12;8(1):877
pubmed: 29026085
PLoS Biol. 2011 Jun;9(6):e1001075
pubmed: 21666805
Sci Rep. 2013;3:1911
pubmed: 23714854
Annu Rev Immunol. 1994;12:117-39
pubmed: 8011279
Genes Dev. 2004 Jun 1;18(11):1263-71
pubmed: 15175259
Exp Cell Res. 2016 Jun 10;344(2):167-75
pubmed: 26404731
J Immunol. 2018 Feb 1;200(3):1039-1052
pubmed: 29288200
J Exp Med. 2004 Oct 18;200(8):967-77
pubmed: 15492122
Science. 2016 Nov 4;354(6312):623-626
pubmed: 27708052
Nat Immunol. 2016 Mar;17(3):323-30
pubmed: 26779600
J Clin Invest. 2013 Dec;123(12):5009-22
pubmed: 24200695
Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13789-94
pubmed: 16940357
Immunity. 2005 Jun;22(6):656-7
pubmed: 15963779
Cell Res. 2015 Feb;25(2):181-92
pubmed: 25572281
Cell Regul. 1989 Nov;1(1):27-35
pubmed: 2519615
EMBO Rep. 2014 Oct;15(10):1077-84
pubmed: 25141862
Curr Opin Genet Dev. 2016 Feb;36:68-72
pubmed: 27151433

Auteurs

Muhammad Assad Aslam (MA)

Division of Tumor Biology and Immunology, Netherlands Cancer Institute, Amsterdam, The Netherlands.
Institute of Molecular Biology and Biotechnology, Bahauddin Zakariya University, Multan, Pakistan.

Mir Farshid Alemdehy (MF)

Division of Tumor Biology and Immunology, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Eliza Mari Kwesi-Maliepaard (EM)

Division of Gene Regulation, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Fitriari Izzatunnisa Muhaimin (FI)

Division of Tumor Biology and Immunology, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Marieta Caganova (M)

Max-Delbrück-Center for Molecular Medicine, Berlin, Germany.

Iris N Pardieck (IN)

Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, The Netherlands.

Teun van den Brand (T)

Division of Gene Regulation, Netherlands Cancer Institute, Amsterdam, The Netherlands.
Division of Gene Regulation, Oncode Institute, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Tibor van Welsem (T)

Division of Gene Regulation, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Iris de Rink (I)

Genome Core Facility, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Ji-Ying Song (JY)

Division of Experimental Animal Pathology, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Elzo de Wit (E)

Division of Gene Regulation, Netherlands Cancer Institute, Amsterdam, The Netherlands.
Division of Gene Regulation, Oncode Institute, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Ramon Arens (R)

Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, The Netherlands.

Heinz Jacobs (H)

Division of Tumor Biology and Immunology, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Fred van Leeuwen (F)

Division of Gene Regulation, Netherlands Cancer Institute, Amsterdam, The Netherlands.
Department of Medical Biology, Amsterdam UMC, Location AMC, University of Amsterdam, Amsterdam, The Netherlands.

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