Dual functions of TET1 in germ layer lineage bifurcation distinguished by genomic context and dependence on 5-methylcytosine oxidation.
Journal
Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011
Informations de publication
Date de publication:
23 06 2023
23 06 2023
Historique:
accepted:
22
03
2023
revised:
12
03
2023
received:
07
10
2022
medline:
26
6
2023
pubmed:
7
4
2023
entrez:
6
4
2023
Statut:
ppublish
Résumé
Gastrulation begins when the epiblast forms the primitive streak or becomes definitive ectoderm. During this lineage bifurcation, the DNA dioxygenase TET1 has bipartite functions in transcriptional activation and repression, but the mechanisms remain unclear. By converting mouse embryonic stem cells (ESCs) into neuroprogenitors, we defined how Tet1-/- cells switch from neuroectoderm fate to form mesoderm and endoderm. We identified the Wnt repressor Tcf7l1 as a TET1 target that suppresses Wnt/β-catenin and Nodal signalling. ESCs expressing catalytic dead TET1 retain neural potential but activate Nodal and subsequently Wnt/β-catenin pathways to generate also mesoderm and endoderm. At CpG-poor distal enhancers, TET1 maintains accessible chromatin at neuroectodermal loci independently of DNA demethylation. At CpG-rich promoters, DNA demethylation by TET1 affects the expression of bivalent genes. In ESCs, a non-catalytic TET1 cooperation with Polycomb represses primitive streak genes; post-lineage priming, the interaction becomes antagonistic at neuronal genes, when TET1's catalytic activity is further involved by repressing Wnt signalling. The convergence of repressive DNA and histone methylation does not inhibit neural induction in Tet1-deficient cells, but some DNA hypermethylated loci persist at genes with brain-specific functions. Our results reveal versatile switching of non-catalytic and catalytic TET1 activities based on genomic context, lineage and developmental stage.
Identifiants
pubmed: 37021585
pii: 7109501
doi: 10.1093/nar/gkad231
pmc: PMC10287924
doi:
Substances chimiques
5-Methylcytosine
6R795CQT4H
beta Catenin
0
DNA-Binding Proteins
0
TET1 protein, mouse
0
Proto-Oncogene Proteins
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
5469-5498Subventions
Organisme : NIEHS NIH HHS
ID : P30 ES030285
Pays : United States
Informations de copyright
© The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research.
Références
Mol Cell Biol. 2015 Nov 23;36(3):452-61
pubmed: 26598602
Genes Dev. 2011 Apr 1;25(7):679-84
pubmed: 21460036
Cell. 2006 Apr 21;125(2):315-26
pubmed: 16630819
Cell Stem Cell. 2014 Jun 5;14(6):838-53
pubmed: 24905168
Nature. 2011 May 19;473(7347):343-8
pubmed: 21490601
Nat Immunol. 2019 Feb;20(2):163-172
pubmed: 30643263
Nat Genet. 2020 Aug;52(8):819-827
pubmed: 32514123
Cell Stem Cell. 2021 Mar 4;28(3):453-471.e8
pubmed: 33271069
Science. 2005 Feb 11;307(5711):929-32
pubmed: 15705853
Mol Cell. 2011 May 20;42(4):451-64
pubmed: 21514197
Development. 2013 Apr;140(8):1665-75
pubmed: 23487311
Genome Biol. 2013 Aug 29;14(8):R91
pubmed: 23987249
Elife. 2017 Jan 16;6:
pubmed: 28079019
Proc Natl Acad Sci U S A. 2006 Nov 7;103(45):16806-11
pubmed: 17077151
Nature. 2011 May 19;473(7347):394-7
pubmed: 21552279
Nature. 2011 May 19;473(7347):389-93
pubmed: 21451524
Nat Rev Mol Cell Biol. 2009 Feb;10(2):91-103
pubmed: 19129791
Mol Cell. 2016 Dec 15;64(6):1062-1073
pubmed: 27916660
Science. 2011 Sep 2;333(6047):1303-7
pubmed: 21817016
Epigenetics Chromatin. 2019 Jul 12;12(1):42
pubmed: 31300027
PLoS Biol. 2014 Aug 26;12(8):e1001937
pubmed: 25157815
Mol Cell. 2020 Mar 19;77(6):1350-1364.e6
pubmed: 31999955
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nat Genet. 2009 Feb;41(2):178-186
pubmed: 19151715
Mol Cell. 2013 Feb 21;49(4):645-56
pubmed: 23352454
JCI Insight. 2018 Dec 6;3(23):
pubmed: 30518695
Nat Genet. 2014 Jan;46(1):17-23
pubmed: 24270360
Genes Dev. 2011 May 15;25(10):1010-22
pubmed: 21576262
Cell. 2011 Aug 19;146(4):519-32
pubmed: 21820164
Nat Genet. 2017 Jul;49(7):1061-1072
pubmed: 28504700
Nat Commun. 2019 Aug 29;10(1):3892
pubmed: 31467272
Nature. 2019 Feb;566(7745):490-495
pubmed: 30787436
Development. 2004 Jan;131(2):263-74
pubmed: 14668413
Nat Struct Mol Biol. 2020 Aug;27(8):696-705
pubmed: 32572255
Development. 2007 Mar;134(6):1023-34
pubmed: 17287255
Nucleic Acids Res. 2022 Apr 8;50(6):3169-3189
pubmed: 35150568
Cell. 2021 Jun 24;184(13):3573-3587.e29
pubmed: 34062119
Nature. 2022 Sep;609(7925):136-143
pubmed: 35709828
Nature. 2020 Jul;583(7818):760-767
pubmed: 32728245
Nat Genet. 2020 Jan;52(1):95-105
pubmed: 31844322
Nat Struct Mol Biol. 2020 Aug;27(8):706-716
pubmed: 32572256
Nat Rev Mol Cell Biol. 2021 Dec;22(12):815-833
pubmed: 34400841
Cell. 2010 Oct 29;143(3):470-84
pubmed: 21029866
Nature. 2021 Dec;600(7888):285-289
pubmed: 34789876
Science. 2022 Mar 4;375(6584):1053-1058
pubmed: 35143257
Nature. 2020 Jun;582(7812):410-415
pubmed: 32528178
Nat Genet. 2018 Jan;50(1):83-95
pubmed: 29203910
Nature. 2016 Oct 27;538(7626):528-532
pubmed: 27760115
Biostatistics. 2017 Apr 1;18(2):275-294
pubmed: 27756721
Science. 2009 May 15;324(5929):930-5
pubmed: 19372391
Proc Natl Acad Sci U S A. 2022 Feb 8;119(6):
pubmed: 35110400
Cell Stem Cell. 2013 Aug 1;13(2):237-45
pubmed: 23770080
Dev Cell. 2014 Apr 14;29(1):102-11
pubmed: 24735881
Science. 2012 May 18;336(6083):934-7
pubmed: 22539555
Cell Stem Cell. 2008 Nov 6;3(5):493-507
pubmed: 18983965
Nat Methods. 2013 Dec;10(12):1213-8
pubmed: 24097267
Cell Stem Cell. 2014 Jan 2;14(1):107-20
pubmed: 24139757
Development. 2018 Feb 23;145(4):
pubmed: 29361574
Nucleic Acids Res. 2018 Jan 4;46(D1):D380-D386
pubmed: 29087512
Genome Med. 2011 Jun 07;3(6):36
pubmed: 21658297
Science. 2018 Sep 28;361(6409):1336-1340
pubmed: 30262495
PLoS One. 2013 Dec 06;8(12):e81148
pubmed: 24324667
Cell. 2013 May 23;153(5):1134-48
pubmed: 23664764
Cell Rep. 2020 Feb 18;30(7):2150-2169.e9
pubmed: 32075734
J Biol Chem. 2013 Jul 19;288(29):20776-20784
pubmed: 23729667
Development. 2017 Feb 1;144(3):365-373
pubmed: 28143843
Elife. 2018 Oct 16;7:
pubmed: 30325306
Science. 2000 Jun 9;288(5472):1796-802
pubmed: 10846156
Nucleic Acids Res. 2022 Aug 26;50(15):8491-8511
pubmed: 35904814
Genome Biol. 2018 Feb 8;19(1):18
pubmed: 29422066
Nature. 2019 Dec;576(7787):487-491
pubmed: 31827285
Nat Commun. 2020 Sep 22;11(1):4782
pubmed: 32963223
J Biol Chem. 2014 Dec 19;289(51):35397-408
pubmed: 25331951
Brief Bioinform. 2021 Jan 18;22(1):416-427
pubmed: 31925417
Nat Biotechnol. 2003 Feb;21(2):183-6
pubmed: 12524553
Elife. 2019 Jun 24;8:
pubmed: 31232687
Nature. 2011 Dec 14;480(7378):490-5
pubmed: 22170606
PLoS One. 2011 Feb 02;6(2):e16627
pubmed: 21311766
Cell. 2021 May 27;184(11):2825-2842.e22
pubmed: 33932341
Nat Methods. 2017 Oct;14(10):959-962
pubmed: 28846090
Cell Stem Cell. 2011 Feb 4;8(2):200-13
pubmed: 21295276
Neuron. 2013 Sep 18;79(6):1109-1122
pubmed: 24050401
Nat Methods. 2017 Apr;14(4):417-419
pubmed: 28263959
Cell Stem Cell. 2017 May 4;20(5):689-705.e9
pubmed: 28285903
J Exp Clin Cancer Res. 2019 Aug 9;38(1):348
pubmed: 31399111
Methods Mol Biol. 2021;2328:171-182
pubmed: 34251625
Science. 2011 Sep 2;333(6047):1300-3
pubmed: 21778364
Science. 2021 Apr 9;372(6538):
pubmed: 33833093
Nat Commun. 2017 Jun 26;8(1):36
pubmed: 28652613
Genes Dev. 2020 Apr 1;34(7-8):598-618
pubmed: 32115407
Neuron. 2001 Apr;30(1):65-78
pubmed: 11343645
Genome Biol. 2018 Jul 12;19(1):88
pubmed: 30001199