Retention of paternal DNA methylome in the developing zebrafish germline.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
11 07 2019
Historique:
received: 19 11 2018
accepted: 31 05 2019
entrez: 13 7 2019
pubmed: 13 7 2019
medline: 28 10 2019
Statut: epublish

Résumé

Two waves of DNA methylation reprogramming occur during mammalian embryogenesis; during preimplantation development and during primordial germ cell (PGC) formation. However, it is currently unclear how evolutionarily conserved these processes are. Here we characterise the DNA methylomes of zebrafish PGCs at four developmental stages and identify retention of paternal epigenetic memory, in stark contrast to the findings in mammals. Gene expression profiling of zebrafish PGCs at the same developmental stages revealed that the embryonic germline is defined by a small number of markers that display strong developmental stage-specificity and that are independent of DNA methylation-mediated regulation. We identified promoters that are specifically targeted by DNA methylation in somatic and germline tissues during vertebrate embryogenesis and that are frequently misregulated in human cancers. Together, these detailed methylome and transcriptome maps of the zebrafish germline provide insight into vertebrate DNA methylation reprogramming and enhance our understanding of the relationships between germline fate acquisition and oncogenesis.

Identifiants

pubmed: 31296860
doi: 10.1038/s41467-019-10895-6
pii: 10.1038/s41467-019-10895-6
pmc: PMC6624265
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3054

Références

J Cell Biochem. 2003 Mar 1;88(4):660-72
pubmed: 12577300
Cell. 2013 May 9;153(4):759-72
pubmed: 23663776
Nat Genet. 2016 Apr;48(4):417-26
pubmed: 26928226
Mob DNA. 2015 Jun 02;6:11
pubmed: 26045719
Nature. 2012 Mar 28;484(7394):339-44
pubmed: 22456710
Mar Biotechnol (NY). 2019 Apr;21(2):217-228
pubmed: 30671659
Nat Rev Genet. 2003 Sep;4(9):690-700
pubmed: 12951570
Cell. 2007 Dec 28;131(7):1273-86
pubmed: 18155131
Curr Protoc Bioinformatics. 2004 May;Chapter 4:Unit 4.10
pubmed: 18428725
Science. 2015 Jan 23;347(6220):1260419
pubmed: 25613900
Cell. 2002 Nov 27;111(5):647-59
pubmed: 12464177
Nat Commun. 2013;4:2531
pubmed: 24100690
Cancer Res. 2017 Nov 1;77(21):5712-5716
pubmed: 29061671
Epigenetics. 2012 Apr;7(4):383-9
pubmed: 22419071
Nature. 2011 Sep 04;477(7366):606-10
pubmed: 21892189
J Cell Biol. 2000 May 15;149(4):875-88
pubmed: 10811828
Nat Rev Cancer. 2005 Aug;5(8):615-25
pubmed: 16034368
Cell. 2015 Jun 4;161(6):1437-52
pubmed: 26046443
Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5
pubmed: 27079975
Genome Biol. 2009;10(3):R25
pubmed: 19261174
Nucleic Acids Res. 2002 Jan 1;30(1):207-10
pubmed: 11752295
Annu Rev Cell Dev Biol. 2014;30:581-613
pubmed: 25150012
Nat Genet. 2014 Feb;46(2):194-9
pubmed: 24390283
Science. 2008 Mar 7;319(5868):1398-401
pubmed: 18239089
Genome Res. 2012 Oct;22(10):2043-53
pubmed: 22593555
Reproduction. 2015 Dec;150(6):485-96
pubmed: 26399853
Nature. 2010 Feb 25;463(7284):1101-5
pubmed: 20098412
Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3740-5
pubmed: 11891299
Genome Res. 2011 Aug;21(8):1313-27
pubmed: 21636662
Science. 2017 May 5;356(6337):
pubmed: 28473536
RNA. 2013 Jun;19(6):803-10
pubmed: 23611983
Nature. 1986 May 15-21;321(6067):209-13
pubmed: 2423876
Biochim Biophys Acta. 2001 Oct 31;1521(1-3):39-44
pubmed: 11690634
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W193-200
pubmed: 17478515
Cell. 2009 May 1;137(3):571-84
pubmed: 19410550
Nat Genet. 1999 Oct;23(2):139-40
pubmed: 10508504
Science. 2001 Nov 23;294(5547):1679-84
pubmed: 11721045
Nature. 2013 Oct 24;502(7472):472-9
pubmed: 24153300
Curr Biol. 2003 Aug 19;13(16):1429-34
pubmed: 12932328
BMC Dev Biol. 2008 May 28;8:58
pubmed: 18507824
Cell. 2008 May 2;133(3):523-36
pubmed: 18423832
J Cell Sci. 2005 Sep 1;118(Pt 17):4027-38
pubmed: 16129886
Nat Commun. 2019 Jul 16;10(1):3053
pubmed: 31311924
Dev Biol. 2013 Feb 15;374(2):308-18
pubmed: 23228893
Nat Commun. 2016 Apr 18;7:11288
pubmed: 27088892
Mol Oncol. 2011 Apr;5(2):164-82
pubmed: 21376678
Nat Chem Biol. 2018 Sep;14(9):844-852
pubmed: 29988067
Curr Biol. 2000 Apr 20;10(8):475-8
pubmed: 10801417
Epigenetics Chromatin. 2017 Dec 8;10(1):59
pubmed: 29216900
Curr Opin Cell Biol. 2015 Oct;36:80-5
pubmed: 26232877
Int Rev Cytol. 1975;43:229-80
pubmed: 770367
Curr Biol. 2015 Apr 20;25(8):1096-103
pubmed: 25843033
Dev Cell. 2017 Dec 18;43(6):704-715.e5
pubmed: 29257950
Genome Res. 2012 Apr;22(4):633-41
pubmed: 22357612
Genome Biol. 2012 Feb 09;13(2):R8
pubmed: 22322129
Chembiochem. 2011 Jan 24;12(2):206-22
pubmed: 21243710
Nature. 2013 Jun 13;498(7453):241-5
pubmed: 23739326
Cell. 2015 Jun 4;161(6):1453-67
pubmed: 26046444
Cell. 2013 Feb 28;152(5):1146-59
pubmed: 23434322
Elife. 2013 Feb 26;2:e00348
pubmed: 23467541
Bioinformatics. 2016 Nov 15;32(22):3507-3509
pubmed: 27466624
Biochem Biophys Res Commun. 2005 May 13;330(3):950-7
pubmed: 15809088
Mol Cell. 2012 Dec 28;48(6):849-62
pubmed: 23219530
Cell Stem Cell. 2014 Jun 5;14(6):710-9
pubmed: 24905162
Nat Commun. 2011;2:248
pubmed: 21427719
BMC Bioinformatics. 2011 Aug 04;12:323
pubmed: 21816040
Nat Commun. 2011;2:241
pubmed: 21407207
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Nature. 2011 Feb 10;470(7333):279-83
pubmed: 21160473
Nature. 2008 Mar 13;452(7184):215-9
pubmed: 18278030
Genes Dev. 1998 Jul 15;12(14):2108-13
pubmed: 9679055
Cell. 2013 Jan 17;152(1-2):82-96
pubmed: 23313552
Mech Dev. 1999 Mar;81(1-2):223-6
pubmed: 10330505
Genome Biol. 2008;9(9):R137
pubmed: 18798982
Genome Res. 2017 Oct;27(10):1759-1768
pubmed: 28855263
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Dev Biol. 2017 Feb 1;422(1):33-46
pubmed: 27940159
Cell. 2014 May 8;157(4):979-991
pubmed: 24813617
Nat Rev Mol Cell Biol. 2018 Dec;19(12):774-790
pubmed: 30425324
Cell Stem Cell. 2014 Oct 2;15(4):416-430
pubmed: 25280218
Nucleic Acids Res. 2009 Jan;37(Database issue):D816-9
pubmed: 18838390
Nat Rev Mol Cell Biol. 2010 Jan;11(1):37-49
pubmed: 20027186
Nat Biotechnol. 2010 May;28(5):495-501
pubmed: 20436461
Cell Rep. 2015 Aug 18;12(7):1133-43
pubmed: 26257178
Nature. 2018 Mar 15;555(7696):392-396
pubmed: 29513657
Nat Genet. 2013 Oct;45(10):1113-20
pubmed: 24071849
Nucleic Acids Res. 2015 Dec 2;43(21):e141
pubmed: 26184873
J Mol Biol. 1987 Jul 20;196(2):261-82
pubmed: 3656447
Mamm Genome. 1999 Jan;10(1):1-5
pubmed: 9892724
Cell Stem Cell. 2014 Aug 7;15(2):239-53
pubmed: 24835570
Biol Reprod. 2000 Dec;63(6):1893-8
pubmed: 11090462
Nat Commun. 2018 Nov 26;9(1):4977
pubmed: 30478328
Nat Commun. 2015 Dec 18;6:10148
pubmed: 26679111
Hum Mol Genet. 2000 Oct;9(16):2395-402
pubmed: 11005794
Nat Rev Genet. 2013 Mar;14(3):204-20
pubmed: 23400093
Drug Des Devel Ther. 2015 Aug 28;9:4953-64
pubmed: 26356032
Immunol Lett. 2016 Sep;177:6-15
pubmed: 27363619
Dev Dyn. 2011 Mar;240(3):695-703
pubmed: 21337467
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Philos Trans R Soc Lond B Biol Sci. 2013 Jan 5;368(1609):20110336
pubmed: 23166397
Nat Cell Biol. 2016 Feb;18(2):225-233
pubmed: 26751286
J Cell Biol. 1999 Oct 4;147(1):25-32
pubmed: 10508852
Cell. 2013 May 9;153(4):773-84
pubmed: 23663777
Dev Cell. 2016 Sep 26;38(6):610-20
pubmed: 27676434
Curr Opin Cell Biol. 2015 Oct;36:103-12
pubmed: 26363959
Curr Opin Genet Dev. 2017 Oct;46:9-14
pubmed: 28651214
Cell Res. 2017 Feb;27(2):165-183
pubmed: 27824029
Cell. 2015 Jun 4;161(6):1425-36
pubmed: 26004067
Nature. 2013 Apr 25;496(7446):498-503
pubmed: 23594743
Development. 2013 Feb 1;140(3):562-72
pubmed: 23293288
Dev Biol. 2002 May 15;245(2):304-14
pubmed: 11977983
Nat Rev Genet. 2011 Sep 16;12(10):715-29
pubmed: 21921927
Nat Genet. 2010 Dec;42(12):1093-100
pubmed: 21057502
Cell. 2018 Feb 22;172(5):993-1006.e13
pubmed: 29456083
Genes Dev. 2002 Jan 1;16(1):6-21
pubmed: 11782440
Nucleic Acids Res. 2014 Apr;42(8):e69
pubmed: 24561809
Dev Biol. 2018 Apr 15;436(2):84-93
pubmed: 29477339
PLoS One. 2015 May 14;10(5):e0127007
pubmed: 25973848
Genome Biol. 2008;9(5):R79
pubmed: 18477403
Nature. 2015 Jan 15;517(7534):321-6
pubmed: 25592537
Curr Biol. 2006 Nov 7;16(21):2135-42
pubmed: 17084698
Database (Oxford). 2011 Jul 23;2011:bar030
pubmed: 21785142

Auteurs

Ksenia Skvortsova (K)

Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, NSW, 2010, Australia.

Katsiaryna Tarbashevich (K)

Institute of Cell Biology, Center for Molecular Biology of Inflammation, University of Münster, Münster, 48149, Germany.

Martin Stehling (M)

Flow Cytometry Unit, Max-Planck-Institute for Molecular Biomedicine, Roentgenstraße 20, 48149, Münster, Germany.

Ryan Lister (R)

ARC CoE Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, WA, 6009, Australia.
Molecular Medicine Division, Harry Perkins Institute of Medical Research, Perth, WA, 6009, Australia.

Manuel Irimia (M)

Centre for Genomic Regulation, The Barcelona Institute for Science and Technology, Barcelona, 08003, Spain.
Universitat Pompeu Fabra (UPF), Barcelona, 08002, Spain.
ICREA, Barcelona, 08010, Spain.

Erez Raz (E)

Institute of Cell Biology, Center for Molecular Biology of Inflammation, University of Münster, Münster, 48149, Germany.

Ozren Bogdanovic (O)

Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, NSW, 2010, Australia. o.bogdanovic@garvan.org.au.
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW, 2010, Australia. o.bogdanovic@garvan.org.au.

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