FAN1-MLH1 interaction affects repair of DNA interstrand cross-links and slipped-CAG/CTG repeats.


Journal

Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440

Informations de publication

Date de publication:
07 2021
Historique:
received: 19 11 2020
accepted: 15 06 2021
entrez: 31 7 2021
pubmed: 1 8 2021
medline: 16 4 2022
Statut: epublish

Résumé

FAN1, a DNA structure-specific nuclease, interacts with MLH1, but the repair pathways in which this complex acts are unknown. FAN1 processes DNA interstrand crosslinks (ICLs) and FAN1 variants are modifiers of the neurodegenerative Huntington's disease (HD), presumably by regulating HD-causing CAG repeat expansions. Here, we identify specific amino acid residues in two adjacent FAN1 motifs that are critical for MLH1 binding. Disruption of the FAN1-MLH1 interaction confers cellular hypersensitivity to ICL damage and defective repair of CAG/CTG slip-outs, intermediates of repeat expansion mutations. FAN1-S126 phosphorylation, which hinders FAN1-MLH1 association, is cell cycle-regulated by cyclin-dependent kinase activity and attenuated upon ICL induction. Our data highlight the FAN1-MLH1 complex as a phosphorylation-regulated determinant of ICL response and repeat stability, opening novel paths to modify cancer and neurodegeneration.

Identifiants

pubmed: 34330701
pii: 7/31/eabf7906
doi: 10.1126/sciadv.abf7906
pmc: PMC8324060
pii:
doi:

Substances chimiques

Multifunctional Enzymes 0
DNA 9007-49-2
Endodeoxyribonucleases EC 3.1.-
Exodeoxyribonucleases EC 3.1.-

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : European Research Council
ID : 714326
Pays : International

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

Références

DNA Repair (Amst). 2014 Sep;21:55-64
pubmed: 25037770
Mol Cell. 2018 Nov 1;72(3):568-582.e6
pubmed: 30344097
Oncotarget. 2013 Dec;4(12):2261-70
pubmed: 24259277
BMC Med Genet. 2009 Feb 11;10:11
pubmed: 19210789
J Biol Chem. 2007 Feb 2;282(5):2976-86
pubmed: 17148452
Nat Struct Mol Biol. 2013 Apr;20(4):461-8
pubmed: 23435383
Cell. 2019 Aug 8;178(4):887-900.e14
pubmed: 31398342
Sci Rep. 2019 Jul 22;9(1):10572
pubmed: 31332257
Lancet Neurol. 2020 Nov;19(11):930-939
pubmed: 33098802
DNA Repair (Amst). 2018 Sep;69:1-5
pubmed: 29990673
Am J Hum Genet. 2020 Jul 2;107(1):96-110
pubmed: 32589923
Cell. 2015 Jul 30;162(3):516-26
pubmed: 26232222
Mol Cell Biol. 2001 Aug;21(15):5142-55
pubmed: 11438669
Cell. 2010 Jul 9;142(1):77-88
pubmed: 20603016
EMBO J. 2019 Aug 15;38(16):e101379
pubmed: 31267591
Hum Mol Genet. 2004 Aug 15;13(16):1815-25
pubmed: 15198993
Proc Natl Acad Sci U S A. 2010 Jul 13;107(28):12593-8
pubmed: 20571119
J Biol Chem. 2012 Dec 7;287(50):41844-50
pubmed: 23086927
PLoS Genet. 2013;9(12):e1003866
pubmed: 24367268
PLoS Genet. 2013 Oct;9(10):e1003930
pubmed: 24204323
Dis Model Mech. 2018 Jan 30;11(1):
pubmed: 29419417
Crit Rev Biochem Mol Biol. 2015 Mar-Apr;50(2):142-67
pubmed: 25608779
Hum Mol Genet. 2020 Nov 4;29(18):3044-3053
pubmed: 32876667
Crit Rev Biochem Mol Biol. 1999;34(3):141-80
pubmed: 10473346
J Biol Chem. 2020 Dec 18;295(51):17460-17475
pubmed: 33453991
Hum Mol Genet. 2019 Feb 15;28(4):650-661
pubmed: 30358836
J Biol Chem. 2002 Apr 19;277(16):13926-34
pubmed: 11832482
Clin Cancer Res. 2010 Nov 1;16(21):5107-13
pubmed: 20823149
Nature. 2020 Oct;586(7830):618-622
pubmed: 32814904
Mol Cell. 2010 Jul 9;39(1):36-47
pubmed: 20603073
Cell. 2010 Jul 9;142(1):65-76
pubmed: 20603015
DNA Repair (Amst). 2016 Feb;38:117-126
pubmed: 26774442
Nucleic Acids Res. 2002 Oct 15;30(20):4534-47
pubmed: 12384601
Nat Struct Mol Biol. 2018 Aug;25(8):650-659
pubmed: 30061603
Nat Genet. 2020 Feb;52(2):146-159
pubmed: 32060489
Cancer Res. 1994 Aug 15;54(16):4308-12
pubmed: 8044777
PLoS Genet. 2018 Oct 12;14(10):e1007719
pubmed: 30312299
Science. 2010 Aug 6;329(5992):693-6
pubmed: 20671156
Proc Natl Acad Sci U S A. 2020 Feb 18;117(7):3535-3542
pubmed: 32015124
PLoS One. 2014 Mar 19;9(3):e92444
pubmed: 24647355
Nat Struct Mol Biol. 2005 Aug;12(8):654-62
pubmed: 16025129
Nat Commun. 2014 Dec 11;5:5726
pubmed: 25500724
Nat Commun. 2016 Aug 26;7:12628
pubmed: 27561354
J Huntingtons Dis. 2021;10(1):95-122
pubmed: 33579867
Nucleic Acids Res. 2001 Apr 15;29(8):1695-702
pubmed: 11292842
Hum Mol Genet. 2011 Feb 1;20(3):580-8
pubmed: 21088112
Nat Commun. 2017 Oct 20;8(1):1073
pubmed: 29051491
Proc Natl Acad Sci U S A. 2013 Jul 23;110(30):12277-82
pubmed: 23840062
Mol Cell Biol. 2009 Feb;29(3):907-18
pubmed: 19015241

Auteurs

Antonio Porro (A)

Institute of Molecular Cancer Research, University of Zurich, Zurich, Switzerland.

Mohiuddin Mohiuddin (M)

Program of Genetics and Genome Biology, The Hospital for Sick Children, Toronto, ON M5G 0A4, Canada.

Christina Zurfluh (C)

Institute of Molecular Cancer Research, University of Zurich, Zurich, Switzerland.

Vincent Spegg (V)

Department of Molecular Mechanisms of Disease, University of Zurich, Zurich, Switzerland.

Jingqi Dai (J)

Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France.

Florence Iehl (F)

Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France.

Virginie Ropars (V)

Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France.

Giulio Collotta (G)

Institute of Molecular Cancer Research, University of Zurich, Zurich, Switzerland.

Keri M Fishwick (KM)

Institute of Molecular Cancer Research, University of Zurich, Zurich, Switzerland.

Nour L Mozaffari (NL)

Institute of Molecular Cancer Research, University of Zurich, Zurich, Switzerland.

Raphaël Guérois (R)

Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France.

Josef Jiricny (J)

Institute of Molecular Cancer Research, University of Zurich, Zurich, Switzerland.

Matthias Altmeyer (M)

Department of Molecular Mechanisms of Disease, University of Zurich, Zurich, Switzerland.

Jean-Baptiste Charbonnier (JB)

Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198, Gif-sur-Yvette, France.

Christopher E Pearson (CE)

Program of Genetics and Genome Biology, The Hospital for Sick Children, Toronto, ON M5G 0A4, Canada. cepearson.sickkids@gmail.com sartori@imcr.uzh.ch.
Program of Molecular Genetics, University of Toronto, Toronto, ON M5S 1A8, Canada.

Alessandro A Sartori (AA)

Institute of Molecular Cancer Research, University of Zurich, Zurich, Switzerland. cepearson.sickkids@gmail.com sartori@imcr.uzh.ch.

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Classifications MeSH