Locus-resolution analysis of L1 regulation and retrotransposition potential in mouse embryonic development.


Journal

Genome research
ISSN: 1549-5469
Titre abrégé: Genome Res
Pays: United States
ID NLM: 9518021

Informations de publication

Date de publication:
09 2023
Historique:
received: 25 04 2023
accepted: 21 08 2023
medline: 2 11 2023
pubmed: 6 10 2023
entrez: 5 10 2023
Statut: ppublish

Résumé

Mice harbor ∼2800 intact copies of the retrotransposon Long Interspersed Element 1 (L1). The in vivo retrotransposition capacity of an L1 copy is defined by both its sequence integrity and epigenetic status, including DNA methylation of the monomeric units constituting young mouse L1 promoters. Locus-specific L1 methylation dynamics during development may therefore elucidate and explain spatiotemporal niches of endogenous retrotransposition but remain unresolved. Here, we interrogate the retrotransposition efficiency and epigenetic fate of source (donor) L1s, identified as mobile in vivo. We show that promoter monomer loss consistently attenuates the relative retrotransposition potential of their offspring (daughter) L1 insertions. We also observe that most donor/daughter L1 pairs are efficiently methylated upon differentiation in vivo and in vitro. We use Oxford Nanopore Technologies (ONT) long-read sequencing to resolve L1 methylation genome-wide and at individual L1 loci, revealing a distinctive "smile" pattern in methylation levels across the L1 promoter region. Using Pacific Biosciences (PacBio) SMRT sequencing of L1 5' RACE products, we then examine DNA methylation dynamics at the mouse L1 promoter in parallel with transcription start site (TSS) distribution at locus-specific resolution. Together, our results offer a novel perspective on the interplay between epigenetic repression, L1 evolution, and genome stability.

Identifiants

pubmed: 37798118
pii: gr.278003.123
doi: 10.1101/gr.278003.123
pmc: PMC10620060
doi:

Substances chimiques

Retroelements 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1465-1481

Informations de copyright

© 2023 Gerdes et al.; Published by Cold Spring Harbor Laboratory Press.

Références

Genome Res. 2001 Oct;11(10):1677-85
pubmed: 11591644
Elife. 2018 Jan 08;7:
pubmed: 29309036
J Mol Biol. 1987 Aug 20;196(4):757-67
pubmed: 3681977
Elife. 2017 Aug 14;6:
pubmed: 28806172
J Biol Chem. 2004 Jun 25;279(26):27753-63
pubmed: 15056671
Nature. 2012 Mar 28;484(7394):339-44
pubmed: 22456710
BMC Genomics. 2015 Jul 10;16:473
pubmed: 26159513
Nat Commun. 2022 Dec 3;13(1):7470
pubmed: 36463236
Nature. 2004 May 20;429(6989):314-8
pubmed: 15152256
PLoS Genet. 2010 Oct 07;6(10):
pubmed: 20949108
Oncotarget. 2014 Feb 15;5(3):853-9
pubmed: 24553397
Cell. 1996 Nov 29;87(5):917-27
pubmed: 8945518
Nucleic Acids Res. 2004 Jul 22;32(13):3846-55
pubmed: 15272086
Elife. 2016 Mar 26;5:
pubmed: 27016617
Mol Cell. 2015 Dec 3;60(5):728-741
pubmed: 26585388
Nat Rev Genet. 2019 Jul;20(7):417-431
pubmed: 30867571
Nature. 2018 Jan 11;553(7687):228-232
pubmed: 29211708
Nature. 2023 May;617(7961):540-547
pubmed: 37165195
Anal Biochem. 2000 Sep 10;284(2):435-8
pubmed: 10964437
Mol Cell. 2019 Aug 8;75(3):590-604.e12
pubmed: 31230816
PLoS One. 2011;6(8):e23848
pubmed: 21886830
Nature. 2020 Aug;584(7822):635-639
pubmed: 32674113
Cell. 1993 Feb 26;72(4):595-605
pubmed: 7679954
Nature. 2010 Feb 25;463(7284):1101-5
pubmed: 20098412
Genome Res. 2017 Nov;27(11):1916-1929
pubmed: 28855259
Genome Res. 2008 Jun;18(6):869-80
pubmed: 18381897
Nat Rev Mol Cell Biol. 2019 Oct;20(10):590-607
pubmed: 31399642
Mol Cell. 2020 Dec 3;80(5):915-928.e5
pubmed: 33186547
Nat Rev Genet. 2021 Nov;22(11):691-711
pubmed: 34354263
Nucleic Acids Res. 2017 Jan 4;45(D1):D68-D73
pubmed: 27924012
BMC Bioinformatics. 2005 Feb 15;6:31
pubmed: 15713233
Cell. 2010 Jun 25;141(7):1159-70
pubmed: 20602998
Genes Dev. 2014 Jul 15;28(14):1544-9
pubmed: 25030694
Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17608-13
pubmed: 17101974
Cell. 1996 Nov 29;87(5):905-16
pubmed: 8945517
Genome Biol. 2016 Nov 18;17(1):234
pubmed: 27863519
Genome Res. 2000 Apr;10(4):411-5
pubmed: 10779482
Mamm Genome. 1992;2(1):41-50
pubmed: 1311970
Nat Genet. 1994 Jun;7(2):143-8
pubmed: 7920631
Mol Biol Evol. 2000 Apr;17(4):616-28
pubmed: 10742052
Neuromuscul Disord. 2003 Mar;13(3):216-22
pubmed: 12609503
Mob DNA. 2013 Jan 03;4(1):3
pubmed: 23286374
J Mol Biol. 1998 Jul 24;280(4):611-22
pubmed: 9677292
Genome Res. 2001 Dec;11(12):2059-65
pubmed: 11731496
Genome Res. 2005 Jun;15(6):780-9
pubmed: 15930490
Genome Res. 2017 Aug;27(8):1395-1405
pubmed: 28483779
J Mol Biol. 1994 Aug 19;241(3):390-7
pubmed: 8064855
Mech Dev. 2002 Sep;117(1-2):15-23
pubmed: 12204247
Nature. 2004 Sep 2;431(7004):96-9
pubmed: 15318244
J Biol Chem. 1992 Oct 5;267(28):19765-8
pubmed: 1328181
Nucleic Acids Res. 1987 Nov 11;15(21):8593-606
pubmed: 3684566
Genomics. 1987 Oct;1(2):113-25
pubmed: 3692483
EMBO J. 1998 Jan 15;17(2):590-7
pubmed: 9430649
Mol Biol Evol. 1994 Sep;11(5):778-89
pubmed: 7968491
Science. 1991 Dec 20;254(5039):1805-8
pubmed: 1662412
Nat Commun. 2020 Nov 11;11(1):5712
pubmed: 33177501
Nucleic Acids Res. 1983 Dec 20;11(24):8847-59
pubmed: 6324106
Genomics. 2009 Feb;93(2):152-8
pubmed: 18950698
Proc Natl Acad Sci U S A. 2009 Jan 20;106(3):731-6
pubmed: 19139409
Genes Dev. 2014 Jul 1;28(13):1397-409
pubmed: 24939876
Nat Genet. 2006 Jun;38(6):626-35
pubmed: 16645617
Bioinformatics. 2022 May 26;38(11):3109-3112
pubmed: 35482479
Mol Cell. 2012 Dec 28;48(6):849-62
pubmed: 23219530
Hum Mol Genet. 2000 Mar 1;9(4):653-7
pubmed: 10699189
EMBO J. 1984 Aug;3(8):1753-9
pubmed: 6090124
Semin Cell Dev Biol. 2020 Jan;97:93-105
pubmed: 31551132
Stem Cell Res. 2013 Nov;11(3):1045-59
pubmed: 23954693
Methods Mol Biol. 2016;1400:139-56
pubmed: 26895052
EMBO J. 2007 Jul 25;26(14):3346-59
pubmed: 17599069
Bioinformatics. 2011 Mar 1;27(5):718-9
pubmed: 21208982
Nat Rev Genet. 2020 Dec;21(12):721-736
pubmed: 32576954
Mob DNA. 2021 Feb 21;12(1):6
pubmed: 33612119
Nature. 1988 Dec 15;336(6200):684-7
pubmed: 3143916
Genome Res. 2018 May;28(5):639-653
pubmed: 29643204
J Mol Evol. 2001 Jan;52(1):51-62
pubmed: 11139294
Mol Cell Biol. 2019 Mar 19;39(7):
pubmed: 30692270
Nat Struct Mol Biol. 2020 Feb;27(2):179-191
pubmed: 32042152
Genome Res. 2004 Jun;14(6):1188-90
pubmed: 15173120
Proc Natl Acad Sci U S A. 2006 May 23;103(21):8036-41
pubmed: 16698926
Cold Spring Harb Protoc. 2016 Dec 1;2016(12):
pubmed: 27934689
Nat Commun. 2020 Jul 27;11(1):3739
pubmed: 32719317
Cell. 2018 Nov 15;175(5):1259-1271.e13
pubmed: 30454646
Nat Genet. 1998 Nov;20(3):288-90
pubmed: 9806550
EMBO J. 1996 Feb 1;15(3):630-9
pubmed: 8599946
Cell. 2013 Nov 21;155(5):1034-48
pubmed: 24267889
Mob DNA. 2016 Aug 11;7:16
pubmed: 27525044
PLoS Biol. 2008 Oct 21;6(10):e253
pubmed: 18942890
Genome Res. 2002 Apr;12(4):656-64
pubmed: 11932250
Nat Struct Mol Biol. 2013 Mar;20(3):282-9
pubmed: 23463313
Genome Biol. 2012 Jun 15;13(6):R45
pubmed: 22703977
Mol Cell Biol. 2001 Jan;21(2):467-75
pubmed: 11134335
Nat Genet. 1994 Jun;7(2):136-41
pubmed: 7920630
Cell. 2019 May 2;177(4):837-851.e28
pubmed: 30955886
Cell Rep. 2018 Jun 26;23(13):3730-3740
pubmed: 29949758
Science. 1999 Mar 5;283(5407):1530-4
pubmed: 10066175
Nature. 1988 Dec 15;336(6200):688-90
pubmed: 3143917
Dev Biol. 2005 Feb 15;278(2):440-58
pubmed: 15680362
Nature. 2001 Feb 15;409(6822):860-921
pubmed: 11237011
Gene. 1997 Apr 21;189(2):227-34
pubmed: 9168132
Mob DNA. 2017 May 10;8:8
pubmed: 28491150
Mob DNA. 2019 Apr 13;10:15
pubmed: 31011371
Nat Methods. 2017 Apr;14(4):407-410
pubmed: 28218898
Mob DNA. 2022 Apr 20;13(1):13
pubmed: 35443687
Mol Cell Biol. 1988 Apr;8(4):1385-97
pubmed: 2454389
Development. 2012 Jan;139(1):15-31
pubmed: 22147951
PLoS One. 2010 Jun 29;5(6):e11353
pubmed: 20613872
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Mol Biol Evol. 1993 May;10(3):552-70
pubmed: 8336543
Nature. 2014 Dec 11;516(7530):242-5
pubmed: 25274305
Nucleic Acids Res. 2017 Mar 17;45(5):e31
pubmed: 27899577
Bioinformatics. 2018 Sep 15;34(18):3094-3100
pubmed: 29750242
Science. 2014 Aug 01;345(6196):1251343
pubmed: 25082706
Nucleic Acids Res. 1988 Oct 11;16(19):9215-31
pubmed: 2845369
Mol Cell Biol. 2003 Aug;23(16):5594-605
pubmed: 12897133
Science. 1991 Dec 20;254(5039):1808-10
pubmed: 1722352
Nature. 2008 May 22;453(7194):539-43
pubmed: 18404146
Elife. 2018 Mar 22;7:
pubmed: 29565245
Genome Res. 2016 Jun;26(6):745-55
pubmed: 27197217
Nat Genet. 1998 Jul;19(3):219-20
pubmed: 9662389
Cell. 2002 Aug 9;110(3):327-38
pubmed: 12176320
Genome Res. 2022 Jul;32(7):1298-1314
pubmed: 35728967
Genomics. 1999 Mar 15;56(3):317-23
pubmed: 10087199
Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W170-5
pubmed: 18487274
Genes Dev. 2008 Apr 1;22(7):908-17
pubmed: 18381894
Genome Res. 2017 Mar;27(3):335-348
pubmed: 27965292
Mob DNA. 2019 Apr 08;10:14
pubmed: 31007728
Cell Genom. 2023 Apr 05;3(5):100291
pubmed: 37228752
Nature. 2002 Dec 5;420(6915):520-62
pubmed: 12466850

Auteurs

Patricia Gerdes (P)

Mater Research Institute - University of Queensland, TRI Building, Woolloongabba, Queensland 4102, Australia.

Dorothy Chan (D)

Mater Research Institute - University of Queensland, TRI Building, Woolloongabba, Queensland 4102, Australia.

Mischa Lundberg (M)

Mater Research Institute - University of Queensland, TRI Building, Woolloongabba, Queensland 4102, Australia.
The University of Queensland Diamantina Institute, The University of Queensland, Woolloongabba, Queensland 4102, Australia.
Translational Bioinformatics, Commonwealth Scientific and Industrial Research Organisation, Sydney, New South Wales 2113, Australia.

Francisco J Sanchez-Luque (FJ)

Mater Research Institute - University of Queensland, TRI Building, Woolloongabba, Queensland 4102, Australia.
GENYO. Centre for Genomics and Oncological Research (Pfizer-University of Granada-Andalusian Regional Government), PTS Granada, 18016, Spain.
MRC Human Genetics Unit, Institute of Genetics and Cancer (IGC), University of Edinburgh, Western General Hospital, Edinburgh EH4 2XU, United Kingdom.

Gabriela O Bodea (GO)

Mater Research Institute - University of Queensland, TRI Building, Woolloongabba, Queensland 4102, Australia.
Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4072, Australia.

Adam D Ewing (AD)

Mater Research Institute - University of Queensland, TRI Building, Woolloongabba, Queensland 4102, Australia.

Geoffrey J Faulkner (GJ)

Mater Research Institute - University of Queensland, TRI Building, Woolloongabba, Queensland 4102, Australia; faulknergj@gmail.com sandra.richardson@mater.uq.edu.au.
Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4072, Australia.

Sandra R Richardson (SR)

Mater Research Institute - University of Queensland, TRI Building, Woolloongabba, Queensland 4102, Australia; faulknergj@gmail.com sandra.richardson@mater.uq.edu.au.

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