RIF1 acts in DNA repair through phosphopeptide recognition of 53BP1.


Journal

Molecular cell
ISSN: 1097-4164
Titre abrégé: Mol Cell
Pays: United States
ID NLM: 9802571

Informations de publication

Date de publication:
07 04 2022
Historique:
received: 26 04 2021
revised: 09 12 2021
accepted: 27 01 2022
pubmed: 27 2 2022
medline: 13 4 2022
entrez: 26 2 2022
Statut: ppublish

Résumé

The chromatin-binding protein 53BP1 promotes DNA repair by orchestrating the recruitment of downstream effectors including PTIP, RIF1, and shieldin to DNA double-strand break sites. While we know how PTIP recognizes 53BP1, the molecular details of RIF1 recruitment to DNA-damage sites remains undefined. Here, we report that RIF1 is a phosphopeptide-binding protein that directly interacts with three phosphorylated 53BP1 epitopes. The RIF1-binding sites on 53BP1 share an essential LxL motif followed by two closely apposed phosphorylated residues. Simultaneous mutation of these sites on 53BP1 abrogates RIF1 accumulation into ionizing-radiation-induced foci, but surprisingly, only fully compromises 53BP1-dependent DNA repair when an alternative mode of shieldin recruitment to DNA-damage sites is also disabled. Intriguingly, this alternative mode of recruitment still depends on RIF1 but does not require its interaction with 53BP1. RIF1 therefore employs phosphopeptide recognition to promote DNA repair but also modifies shieldin action independently of 53BP1 binding.

Identifiants

pubmed: 35216668
pii: S1097-2765(22)00101-0
doi: 10.1016/j.molcel.2022.01.025
pmc: PMC8995355
mid: NIHMS1783404
pii:
doi:

Substances chimiques

BRCA1 Protein 0
Carrier Proteins 0
Phosphopeptides 0
Telomere-Binding Proteins 0
Tumor Suppressor p53-Binding Protein 1 0
DNA 9007-49-2

Types de publication

Journal Article Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1359-1371.e9

Subventions

Organisme : Intramural NIH HHS
ID : ZIA BC010283
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA BC010959
Pays : United States
Organisme : CIHR
ID : FDN143343
Pays : Canada

Informations de copyright

Copyright © 2022. Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of interests D.D. is a shareholder of and advisor to Repare Therapeutics.

Références

Science. 2003 Oct 24;302(5645):639-42
pubmed: 14576433
Mol Cell. 2016 Aug 18;63(4):686-695
pubmed: 27453045
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
Nat Commun. 2017 Dec 4;8(1):1921
pubmed: 29203878
Cell. 2018 May 3;173(4):972-988.e23
pubmed: 29656893
Curr Protoc Immunol. 2001 May;Chapter 10:Unit 10.17C
pubmed: 18432682
Nature. 2021 Aug;596(7873):583-589
pubmed: 34265844
Dev Cell. 2015 Aug 24;34(4):466-74
pubmed: 26256213
PLoS Biol. 2018 Jul 3;16(7):e2005970
pubmed: 29969450
Nat Struct Mol Biol. 2017 Jul;24(7):588-595
pubmed: 28604726
Gene Anal Tech. 1988 Mar-Apr;5(2):22-31
pubmed: 3192155
Nat Commun. 2018 Sep 25;9(1):3925
pubmed: 30254264
Protein Sci. 2014 Jun;23(6):747-59
pubmed: 24639379
J Cell Biol. 2004 Dec 6;167(5):819-30
pubmed: 15583028
Nat Immunol. 2004 May;5(5):481-7
pubmed: 15077110
Mol Cell. 2011 May 6;42(3):319-29
pubmed: 21549309
Cell. 2010 Jun 11;141(6):970-81
pubmed: 20550933
Methods Mol Biol. 2015;1261:91-114
pubmed: 25502195
Nucleic Acids Res. 2007;35(16):5312-22
pubmed: 17690115
DNA Repair (Amst). 2007 Oct 1;6(10):1536-44
pubmed: 17553757
Mol Cell. 2016 Oct 6;64(1):51-64
pubmed: 27546791
Nature. 2013 Jul 4;499(7456):50-4
pubmed: 23760478
EMBO J. 2018 Sep 14;37(18):
pubmed: 30154076
Microb Cell. 2018 May 17;5(7):327-343
pubmed: 29992129
Mol Cell. 2013 Mar 7;49(5):872-83
pubmed: 23333306
Cell Rep. 2014 Sep 11;8(5):1583-94
pubmed: 25159151
Cell. 2006 Dec 29;127(7):1361-73
pubmed: 17190600
Science. 2013 Feb 8;339(6120):711-5
pubmed: 23306439
Nucleic Acids Res. 2012 Jan;40(Database issue):D261-70
pubmed: 22135298
Nature. 2018 Aug;560(7716):122-127
pubmed: 30046110
Nature. 2018 Aug;560(7716):112-116
pubmed: 30022158
EMBO J. 2010 Sep 15;29(18):3140-55
pubmed: 20711169
Cell Rep. 2018 Sep 25;24(13):3513-3527.e7
pubmed: 30257212
Genes Dev. 2014 Feb 15;28(4):372-83
pubmed: 24532715
Hum Gene Ther. 1996 Aug 1;7(12):1405-13
pubmed: 8844199
Cell. 2013 Jun 6;153(6):1266-80
pubmed: 23727112
Trends Biochem Sci. 2010 Aug;35(8):450-8
pubmed: 20399103
Nat Commun. 2020 Apr 24;11(1):1972
pubmed: 32332881
Nat Protoc. 2018 Dec;13(12):2964-2990
pubmed: 30446747
Nat Cell Biol. 2018 Aug;20(8):954-965
pubmed: 30022119
Nat Commun. 2017 May 19;8:15473
pubmed: 28524877
Mol Cell. 2013 Mar 7;49(5):858-71
pubmed: 23333305
J Cell Biol. 2001 Apr 30;153(3):613-20
pubmed: 11331310
Nature. 2008 Nov 27;456(7221):524-8
pubmed: 18931659
Mol Cell Biol. 2001 Mar;21(5):1719-29
pubmed: 11238909
Nat Rev Mol Cell Biol. 2014 Jan;15(1):7-18
pubmed: 24326623
Nature. 2018 Aug;560(7716):117-121
pubmed: 30022168
Science. 2013 Feb 8;339(6120):700-4
pubmed: 23306437
EMBO Rep. 2019 May;20(5):
pubmed: 30948458
Science. 2003 Oct 24;302(5645):636-9
pubmed: 14576432
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834
J Cell Biol. 2009 Nov 2;187(3):385-98
pubmed: 19948482
Mol Cell. 2020 Jan 2;77(1):26-38.e7
pubmed: 31653568
Nature. 2015 Dec 17;528(7582):422-6
pubmed: 26649820
Cell Rep. 2019 Aug 6;28(6):1389-1399.e6
pubmed: 31390554
Genes Dev. 2020 Jan 1;34(1-2):7-23
pubmed: 31896689
Nature. 2019 Oct;574(7779):571-574
pubmed: 31645724
EMBO Rep. 2017 Mar;18(3):403-419
pubmed: 28077461
Cell. 2010 Apr 16;141(2):243-54
pubmed: 20362325

Auteurs

Dheva Setiaputra (D)

Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto, ON M5G 1X5, Canada. Electronic address: setiaputra@lunenfeld.ca.

Cristina Escribano-Díaz (C)

Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto, ON M5G 1X5, Canada.

Julia K Reinert (JK)

Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland; University of Basel, Petersplatz 1, 4003 Basel, Switzerland.

Pooja Sadana (P)

Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland.

Dali Zong (D)

Laboratory of Genome Integrity, National Cancer Institute, 37 Convent Drive, National Institutes of Health, Bethesda, MD 20892, USA.

Elsa Callen (E)

Laboratory of Genome Integrity, National Cancer Institute, 37 Convent Drive, National Institutes of Health, Bethesda, MD 20892, USA.

Chérine Sifri (C)

Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto, ON M5G 1X5, Canada; Department of Biochemistry, University of Toronto, 1 King's College Circle, Toronto, ON M5S 1A8, Canada.

Jan Seebacher (J)

Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland.

André Nussenzweig (A)

Laboratory of Genome Integrity, National Cancer Institute, 37 Convent Drive, National Institutes of Health, Bethesda, MD 20892, USA.

Nicolas H Thomä (NH)

Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland; University of Basel, Petersplatz 1, 4003 Basel, Switzerland.

Daniel Durocher (D)

Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto, ON M5G 1X5, Canada; Department of Molecular Genetics, University of Toronto, 1 King's College Circle, Toronto, ON M5S 1A8, Canada. Electronic address: durocher@lunenfeld.ca.

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Classifications MeSH