Wnt/β-catenin signaling pathway safeguards epigenetic stability and homeostasis of mouse embryonic stem cells.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
30 01 2019
Historique:
received: 11 06 2018
accepted: 03 12 2018
entrez: 1 2 2019
pubmed: 1 2 2019
medline: 25 7 2020
Statut: epublish

Résumé

Mouse embryonic stem cells (mESCs) are pluripotent and can differentiate into cells belonging to the three germ layers of the embryo. However, mESC pluripotency and genome stability can be compromised in prolonged in vitro culture conditions. Several factors control mESC pluripotency, including Wnt/β-catenin signaling pathway, which is essential for mESC differentiation and proliferation. Here we show that the activity of the Wnt/β-catenin signaling pathway safeguards normal DNA methylation of mESCs. The activity of the pathway is progressively silenced during passages in culture and this results into a loss of the DNA methylation at many imprinting control regions (ICRs), loss of recruitment of chromatin repressors, and activation of retrotransposons, resulting into impaired mESC differentiation. Accordingly, sustained Wnt/β-catenin signaling maintains normal ICR methylation and mESC homeostasis and is a key regulator of genome stability.

Identifiants

pubmed: 30700782
doi: 10.1038/s41598-018-37442-5
pii: 10.1038/s41598-018-37442-5
pmc: PMC6353868
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

948

Références

Nat Genet. 1999 Aug;22(4):361-5
pubmed: 10431240
J Cell Biol. 2000 Feb 7;148(3):567-78
pubmed: 10662781
Free Radic Biol Med. 2000 Feb 1;28(3):463-99
pubmed: 10699758
Nat Genet. 2000 Apr;24(4):372-6
pubmed: 10742100
Nat Genet. 2001 Jan;27(1):31-9
pubmed: 11137995
Mol Cell. 2001 Apr;7(4):801-9
pubmed: 11336703
Hematol J. 2000;1(1):3-6
pubmed: 11920163
J Cell Physiol. 2002 Sep;192(3):245-58
pubmed: 12124770
Nat Genet. 2002 Dec;32(4):594-605
pubmed: 12426568
Nature. 2002 Dec 5;420(6915):520-62
pubmed: 12466850
Nat Biotechnol. 2003 Feb;21(2):183-6
pubmed: 12524553
FEBS Lett. 2003 Apr 10;540(1-3):3-6
pubmed: 12681474
Cell. 2003 May 30;113(5):643-55
pubmed: 12787505
Mol Cell Biol. 2003 Aug;23(16):5594-605
pubmed: 12897133
J Med Genet. 2003 Nov;40(11):797-801
pubmed: 14627666
Nature. 2004 Sep 2;431(7004):96-9
pubmed: 15318244
Mol Cell Biol. 2004 Oct;24(20):8862-71
pubmed: 15456861
Nat Genet. 2005 Oct;37(10):1099-103
pubmed: 16142235
Cell. 2005 Sep 23;122(6):947-56
pubmed: 16153702
Nucleic Acids Res. 2005 Oct 13;33(18):5868-77
pubmed: 16224102
Cancer Cell. 2005 Oct;8(4):275-85
pubmed: 16226703
Nat Genet. 2005 Nov;37(11):1274-9
pubmed: 16244654
Biochem Biophys Res Commun. 2006 Apr 28;343(1):159-66
pubmed: 16530170
Nat Cell Biol. 2006 May;8(5):532-8
pubmed: 16570078
Cytogenet Genome Res. 2006;113(1-4):279-91
pubmed: 16575191
Cell. 2006 Apr 21;125(2):315-26
pubmed: 16630819
Biochem Biophys Res Commun. 2006 Jun 30;345(2):789-95
pubmed: 16707109
Genes Cells. 2006 Jul;11(7):805-14
pubmed: 16824199
Mol Cell Biol. 2006 Oct;26(20):7479-91
pubmed: 16894029
Development. 2007 Feb;134(4):635-46
pubmed: 17215298
Biochem Biophys Res Commun. 2007 May 11;356(3):648-54
pubmed: 17376403
Curr Opin Cell Biol. 2007 Jun;19(3):281-9
pubmed: 17467259
Nature. 2007 Jul 12;448(7150):196-9
pubmed: 17597760
J Biosci Bioeng. 2007 May;103(5):389-98
pubmed: 17609152
J Biol Chem. 2007 Sep 14;282(37):27298-305
pubmed: 17623658
Clin Cancer Res. 2007 Jul 15;13(14):4042-5
pubmed: 17634527
Science. 2007 Sep 21;317(5845):1760-4
pubmed: 17673620
Mol Cell Biol. 2007 Dec;27(23):8243-58
pubmed: 17893328
FEBS Lett. 2007 Nov 13;581(27):5247-54
pubmed: 17950287
Development. 2008 Jan;135(2):367-75
pubmed: 18077588
Nature. 2007 Dec 20;450(7173):1230-4
pubmed: 18097409
J Biol Chem. 2008 Apr 4;283(14):9224-30
pubmed: 18250171
Development. 2008 Mar;135(5):909-18
pubmed: 18263842
Cell. 2008 Feb 22;132(4):567-82
pubmed: 18295576
Nature. 2008 May 22;453(7194):519-23
pubmed: 18497825
Cancer Res. 2008 Jun 1;68(11):4229-38
pubmed: 18519682
Nature. 2008 Oct 9;455(7214):818-21
pubmed: 18772891
Cell Mol Life Sci. 2008 Nov;65(21):3383-98
pubmed: 18818872
Cell Mol Life Sci. 2008 Nov;65(21):3329-47
pubmed: 18818875
Cell Stem Cell. 2008 Oct 9;3(4):391-401
pubmed: 18940731
Cell Stem Cell. 2008 Nov 6;3(5):508-18
pubmed: 18983966
Cell Stem Cell. 2009 Jun 5;4(6):487-92
pubmed: 19497275
Nature. 2010 Jan 14;463(7278):237-40
pubmed: 20075919
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
PLoS One. 2010 Feb 23;5(2):e9370
pubmed: 20186325
J Biol Chem. 2010 Jul 2;285(27):21082-91
pubmed: 20404320
Mol Cell. 2010 May 28;38(4):576-89
pubmed: 20513432
Circ Res. 2010 Jun 25;106(12):1798-806
pubmed: 20576942
Virology. 2011 Mar 15;411(2):273-87
pubmed: 21251689
BMC Bioinformatics. 2011 Jan 26;12:35
pubmed: 21269502
Cell Stem Cell. 2011 Feb 4;8(2):214-27
pubmed: 21295277
Cell Res. 2011 Mar;21(3):381-95
pubmed: 21321607
Bioinformatics. 2011 Jun 1;27(11):1571-2
pubmed: 21493656
Neural Dev. 2011 May 10;6:23
pubmed: 21569278
J Cell Sci. 2011 Jun 15;124(Pt 12):1992-2000
pubmed: 21610099
Mol Biol Rep. 2012 Feb;39(2):789-95
pubmed: 21611753
EMBO Rep. 2011 Jul 01;12(7):720-6
pubmed: 21617704
Cell Stem Cell. 2011 Jun 3;8(6):676-87
pubmed: 21624812
Cell. 2011 Jun 10;145(6):875-89
pubmed: 21663792
Nat Cell Biol. 2011 Jun 19;13(7):753-61
pubmed: 21685890
Nat Cell Biol. 2011 Aug 14;13(9):1070-5
pubmed: 21841791
PLoS Genet. 2011 Sep;7(9):e1002301
pubmed: 21980304
Mol Cell. 2011 Nov 4;44(3):341-2
pubmed: 22055179
Mol Cell. 2011 Nov 4;44(3):361-72
pubmed: 22055183
Science. 2012 Feb 10;335(6069):709-12
pubmed: 22323818
Molecules. 2012 May 25;17(6):6196-236
pubmed: 22634835
Nucleic Acids Res. 2012 Oct;40(18):8993-9007
pubmed: 22844087
Nature. 2012 Sep 6;489(7414):57-74
pubmed: 22955616
Nat Commun. 2012;3:1070
pubmed: 22990866
Genome Biol. 2012 Oct 03;13(10):R87
pubmed: 23034086
Genome Res. 2013 Mar;23(3):452-61
pubmed: 23233547
Development. 2013 Mar;140(6):1171-83
pubmed: 23444350
Stem Cells. 2013 Dec;31(12):2667-79
pubmed: 23505158
Mol Cell Proteomics. 2013 Jul;12(7):1980-94
pubmed: 23592333
Nat Rev Mol Cell Biol. 2013 Jun;14(6):357-68
pubmed: 23673969
PLoS One. 2013 May 14;8(5):e63265
pubmed: 23691006
Oncogene. 2014 May 22;33(21):2737-47
pubmed: 23752181
Wiley Interdiscip Rev Dev Biol. 2012 Nov-Dec;1(6):789-802
pubmed: 23799624
J Clin Invest. 2013 Aug;123(8):3409-19
pubmed: 23867625
Nature. 2013 Nov 21;503(7476):392-6
pubmed: 24141946
Cancer Sci. 2014 Apr;105(4):418-24
pubmed: 24447505
Cold Spring Harb Perspect Biol. 2014 Feb 01;6(2):null
pubmed: 24492710
Nat Commun. 2014 Mar 03;5:3388
pubmed: 24584437
Genes (Basel). 2011 Feb 25;2(1):229-59
pubmed: 24710147
Stem Cell Reports. 2014 May 08;2(5):707-20
pubmed: 24936456
Stem Cells Dev. 2015 Mar 1;24(5):653-62
pubmed: 25254421
Nature. 2014 Dec 4;516(7529):56-61
pubmed: 25471879
PLoS One. 2015 Feb 25;10(2):e0118307
pubmed: 25714340
Methods Mol Biol. 2016;1341:209-16
pubmed: 25720370
Mol Cancer Res. 2015 Jun;13(6):969-81
pubmed: 25753001
Dev Cell. 2015 Jun 22;33(6):660-74
pubmed: 26004508
Mol Cell Neurosci. 2015 Sep;68:131-42
pubmed: 26164566
Nucleic Acids Res. 2016 Feb 18;44(3):1118-32
pubmed: 26481358
Oncol Rep. 2016 Mar;35(3):1425-32
pubmed: 26707142
Cell Rep. 2016 Feb 2;14(4):956-965
pubmed: 26804902
Ann Transl Med. 2016 Feb;4(4):78
pubmed: 27004225
Cell Rep. 2016 Apr 5;15(1):77-85
pubmed: 27052169
Mol Med Rep. 2016 Jun;13(6):5207-15
pubmed: 27108540
Sci Rep. 2016 Aug 17;6:31665
pubmed: 27530555
Stem Cells. 2017 Feb;35(2):445-457
pubmed: 27570105
Sci Rep. 2016 Nov 09;6:36863
pubmed: 27827439
Proc Natl Acad Sci U S A. 2016 Dec 20;113(51):E8267-E8276
pubmed: 27930333
Cell Mol Life Sci. 2017 Jun;74(11):2055-2065
pubmed: 28160052
Proc Natl Acad Sci U S A. 1978 Nov;75(11):5565-9
pubmed: 281705
PLoS Genet. 2017 Mar 27;13(3):e1006682
pubmed: 28346462
Bioinformatics. 2017 Sep 15;33(18):2938-2940
pubmed: 28645171
Nature. 2017 Aug 10;548(7666):219-223
pubmed: 28746311
NPJ Syst Biol Appl. 2017 Aug 3;3:19
pubmed: 28794899
Sci Rep. 2017 Aug 29;7(1):9705
pubmed: 28852087
Br J Haematol. 2018 Nov;183(3):445-456
pubmed: 30106181
Nature. 1988 Dec 15;336(6200):684-7
pubmed: 3143916
Nature. 1988 Dec 15;336(6200):688-90
pubmed: 3143917
Curr Top Microbiol Immunol. 1978;81:51-3
pubmed: 688761
Proc Natl Acad Sci U S A. 1981 Dec;78(12):7634-8
pubmed: 6950406
Nature. 1981 Jul 9;292(5819):154-6
pubmed: 7242681
Genes Dev. 1994 Jan;8(2):174-89
pubmed: 8299937
Development. 1995 Nov;121(11):3529-37
pubmed: 8582267
Development. 1996 Oct;122(10):3195-205
pubmed: 8898232
Nucleic Acids Res. 1997 Jun 15;25(12):2532-4
pubmed: 9171110
Trends Genet. 1997 Aug;13(8):335-40
pubmed: 9260521

Auteurs

Ilda Theka (I)

Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003, Barcelona, Spain.

Francesco Sottile (F)

Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003, Barcelona, Spain.

Marco Cammisa (M)

Institute of Genetics and Biophysics 'A. Buzzati-Traverso', CNR, 80131, Naples, Italy.
Department of Environmental, Biological and Pharmaceutical Sciences and Technologies, Second University of Naples, 81100, Caserta, Italy.

Sarah Bonnin (S)

Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003, Barcelona, Spain.

Marta Sanchez-Delgado (M)

Imprinting and Cancer Group, Cancer Epigenetic and Biology Program, Institut d'Investigació Biomedica de Bellvitge, Hospital Duran i Reynals, Barcelona, Spain.

Umberto Di Vicino (U)

Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003, Barcelona, Spain.

Maria Victoria Neguembor (MV)

Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003, Barcelona, Spain.

Karthik Arumugam (K)

Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003, Barcelona, Spain.

Francesco Aulicino (F)

Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003, Barcelona, Spain.

David Monk (D)

Imprinting and Cancer Group, Cancer Epigenetic and Biology Program, Institut d'Investigació Biomedica de Bellvitge, Hospital Duran i Reynals, Barcelona, Spain.

Andrea Riccio (A)

Institute of Genetics and Biophysics 'A. Buzzati-Traverso', CNR, 80131, Naples, Italy.
Department of Environmental, Biological and Pharmaceutical Sciences and Technologies, Second University of Naples, 81100, Caserta, Italy.

Maria Pia Cosma (MP)

Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003, Barcelona, Spain. pia.cosma@crg.es.
Universitat Pompeu Fabra, (UPF), Dr. Aiguader 88, Barcelona, 08003, Spain. pia.cosma@crg.es.
Institució Catalana de Recerca i Estudis Avançat (ICREA), Pg. Lluís Companys 23, 08010, Barcelona, Spain. pia.cosma@crg.es.

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