Hominoid-Specific Transposable Elements and KZFPs Facilitate Human Embryonic Genome Activation and Control Transcription in Naive Human ESCs.
Animals
Biological Evolution
Chromatin
/ genetics
DNA Transposable Elements
/ genetics
Embryonic Stem Cells
/ physiology
Evolution, Molecular
Gene Expression Regulation
Gene Regulatory Networks
Genetic Speciation
Hominidae
Humans
Kruppel-Like Transcription Factors
/ genetics
Phylogeny
Sequence Alignment
Species Specificity
HERVH
HERVK
KRAB-zinc finger proteins
Krüppel-like factors
SVA
Transposable elements
cis-regulatory elements
embryonic genome activation
human genome evolution
morula
Journal
Cell stem cell
ISSN: 1875-9777
Titre abrégé: Cell Stem Cell
Pays: United States
ID NLM: 101311472
Informations de publication
Date de publication:
02 05 2019
02 05 2019
Historique:
received:
09
11
2018
revised:
04
02
2019
accepted:
12
03
2019
pubmed:
23
4
2019
medline:
17
7
2020
entrez:
23
4
2019
Statut:
ppublish
Résumé
Expansion of transposable elements (TEs) coincides with evolutionary shifts in gene expression. TEs frequently harbor binding sites for transcriptional regulators, thus enabling coordinated genome-wide activation of species- and context-specific gene expression programs, but such regulation must be balanced against their genotoxic potential. Here, we show that Krüppel-associated box (KRAB)-containing zinc finger proteins (KZFPs) control the timely and pleiotropic activation of TE-derived transcriptional cis regulators during early embryogenesis. Evolutionarily recent SVA, HERVK, and HERVH TE subgroups contribute significantly to chromatin opening during human embryonic genome activation and are KLF-stimulated enhancers in naive human embryonic stem cells (hESCs). KZFPs of corresponding evolutionary ages are simultaneously induced and repress the transcriptional activity of these TEs. Finally, the same KZFP-controlled TE-based enhancers later serve as developmental and tissue-specific enhancers. Thus, by controlling the transcriptional impact of TEs during embryogenesis, KZFPs facilitate their genome-wide incorporation into transcriptional networks, thereby contributing to human genome regulation.
Identifiants
pubmed: 31006620
pii: S1934-5909(19)30111-0
doi: 10.1016/j.stem.2019.03.012
pmc: PMC6509360
pii:
doi:
Substances chimiques
Chromatin
0
DNA Transposable Elements
0
Kruppel-Like Transcription Factors
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
724-735.e5Subventions
Organisme : European Research Council
ID : 268721
Pays : International
Organisme : European Research Council
ID : 694658
Pays : International
Organisme : NINDS NIH HHS
ID : R01 NS088538
Pays : United States
Organisme : NICHD NIH HHS
ID : R37 HD045022
Pays : United States
Informations de copyright
Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.
Références
Cell Stem Cell. 2015 Feb 5;16(2):135-41
pubmed: 25658370
Cell Stem Cell. 2016 Oct 6;19(4):502-515
pubmed: 27424783
Genes Dev. 2014 Jul 1;28(13):1397-409
pubmed: 24939876
Trends Genet. 2017 Nov;33(11):871-881
pubmed: 28935117
Nature. 2015 Jun 11;522(7555):221-5
pubmed: 25896322
Nature. 2009 Apr 30;458(7242):1201-4
pubmed: 19270682
Nat Struct Mol Biol. 2014 Apr;21(4):423-5
pubmed: 24681886
Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
Nat Struct Mol Biol. 2013 Sep;20(9):1131-9
pubmed: 23934149
Development. 2017 Aug 1;144(15):2748-2763
pubmed: 28765214
Genome Biol. 2016 Jul 05;17(1):148
pubmed: 27380939
Nature. 2014 Jul 31;511(7511):611-5
pubmed: 25079558
Cell Rep. 2014 Oct 23;9(2):767-79
pubmed: 25373911
Elife. 2018 Aug 02;7:
pubmed: 30070637
Genome Res. 2006 May;16(5):669-77
pubmed: 16606702
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
pubmed: 12136088
Mol Syst Biol. 2014 Nov 17;10:760
pubmed: 25403753
Genome Res. 2014 Aug;24(8):1251-9
pubmed: 24879558
BMC Bioinformatics. 2017 May 31;18(1):287
pubmed: 28569135
Nature. 2012 Jul 5;487(7405):57-63
pubmed: 22722858
Cell. 2018 Mar 22;173(1):248-259.e15
pubmed: 29526463
Brookhaven Symp Biol. 1956 Feb;(8):58-74
pubmed: 13293421
Curr Protoc Bioinformatics. 2012 Dec;Chapter 1:Unit1.4
pubmed: 23255150
Mol Biol Evol. 2016 Jun;33(6):1635-8
pubmed: 26921390
Cell Rep. 2013 Sep 26;4(6):1108-15
pubmed: 24035396
Genome Biol Evol. 2014 Mar;6(3):510-25
pubmed: 24534434
Nat Rev Genet. 2009 Oct;10(10):691-703
pubmed: 19763152
Cell Stem Cell. 2014 Oct 2;15(4):488-497
pubmed: 25280221
Nat Methods. 2015 Dec;12(12):1143-9
pubmed: 26501517
Nature. 2014 Jul 31;511(7511):606-10
pubmed: 25079557
Nature. 2011 Oct 19;478(7369):343-8
pubmed: 22012392
Development. 2018 May 30;145(10):
pubmed: 29739838
Nat Genet. 2017 Jun;49(6):941-945
pubmed: 28459456
Cell. 2015 Jun 4;161(6):1453-67
pubmed: 26046444
Nature. 2010 Apr 8;464(7290):927-31
pubmed: 20164836
Genome Res. 2017 Oct;27(10):1623-1633
pubmed: 28855262
Cell. 2014 Sep 11;158(6):1254-1269
pubmed: 25215486
Cell Stem Cell. 2016 Feb 4;18(2):262-75
pubmed: 26686465
Q Rev Biol. 1971 Jun;46(2):111-38
pubmed: 5160087
Genes Dev. 2015 Mar 1;29(5):538-54
pubmed: 25737282
Proc Natl Acad Sci U S A. 2014 Aug 26;111(34):12426-31
pubmed: 25097266
Genome Biol. 2004;5(10):R80
pubmed: 15461798
Genome Res. 2017 Apr;27(4):567-579
pubmed: 28223401
Nat Methods. 2013 Dec;10(12):1213-8
pubmed: 24097267
Development. 2017 Aug 1;144(15):2719-2729
pubmed: 28765213
Nat Rev Genet. 2017 Feb;18(2):71-86
pubmed: 27867194
Genome Biol. 2008;9(9):R137
pubmed: 18798982
Genome Biol. 2014 Feb 03;15(2):R29
pubmed: 24485249
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Nat Cell Biol. 2018 May;20(5):553-564
pubmed: 29695788
Genome Res. 2014 Aug;24(8):1260-70
pubmed: 24879559
Mol Cell. 2010 May 28;38(4):576-89
pubmed: 20513432
J Biol Chem. 2016 Feb 26;291(9):4386-98
pubmed: 26719341
Proc Natl Acad Sci U S A. 2013 Nov 26;110(48):19472-7
pubmed: 24218577
Cell Stem Cell. 2014 Oct 2;15(4):471-487
pubmed: 25090446
Nature. 2010 Jan 14;463(7278):237-40
pubmed: 20075919
Nat Biotechnol. 2011 Jan;29(1):24-6
pubmed: 21221095
Nat Methods. 2015 Apr;12(4):357-60
pubmed: 25751142
Genome Biol. 2013 Apr 25;14(4):R36
pubmed: 23618408
Sci Rep. 2017 Mar 27;7:45311
pubmed: 28345668
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Cell Stem Cell. 2017 Jun 1;20(6):874-890.e7
pubmed: 28343983
Nature. 2014 Dec 11;516(7530):242-5
pubmed: 25274305
Nature. 2017 Mar 23;543(7646):550-554
pubmed: 28273063
Genome Biol Evol. 2015 Jan 09;7(2):567-80
pubmed: 25577199
Methods Mol Biol. 2014;1150:141-52
pubmed: 24743995
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278