E3 ligase RFWD3 is a novel modulator of stalled fork stability in BRCA2-deficient cells.


Journal

The Journal of cell biology
ISSN: 1540-8140
Titre abrégé: J Cell Biol
Pays: United States
ID NLM: 0375356

Informations de publication

Date de publication:
01 06 2020
Historique:
received: 23 08 2019
revised: 15 01 2020
accepted: 03 03 2020
entrez: 12 5 2020
pubmed: 12 5 2020
medline: 20 3 2021
Statut: ppublish

Résumé

BRCA1/2 help maintain genomic integrity by stabilizing stalled forks. Here, we identify the E3 ligase RFWD3 as an essential modulator of stalled fork stability in BRCA2-deficient cells and show that codepletion of RFWD3 rescues fork degradation, collapse, and cell sensitivity upon replication stress. Stalled forks in BRCA2-deficient cells accumulate phosphorylated and ubiquitinated replication protein A (ubq-pRPA), the latter of which is mediated by RFWD3. Generation of this intermediate requires SMARCAL1, suggesting that it depends on stalled fork reversal. We show that in BRCA2-deficient cells, rescuing fork degradation might not be sufficient to ensure fork repair. Depleting MRE11 in BRCA2-deficient cells does block fork degradation, but it does not prevent fork collapse and cell sensitivity in the presence of replication stress. No such ubq-pRPA intermediate is formed in BRCA1-deficient cells, and our results suggest that BRCA1 may function upstream of BRCA2 in the stalled fork repair pathway. Collectively, our data uncover a novel mechanism by which RFWD3 destabilizes forks in BRCA2-deficient cells.

Identifiants

pubmed: 32391871
pii: 151752
doi: 10.1083/jcb.201908192
pmc: PMC7265328
pii:
doi:

Substances chimiques

BRCA1 Protein 0
BRCA1 protein, human 0
BRCA2 Protein 0
BRCA2 protein, human 0
MRE11 protein, human 0
RNA, Small Interfering 0
Replication Protein A 0
RFWD3 protein, human EC 2.3.2.27
Ubiquitin-Protein Ligases EC 2.3.2.27
Rad51 Recombinase EC 2.7.7.-
SMARCAL1 protein, human EC 2.7.7.-
MRE11 Homologue Protein EC 3.1.-
DNA Helicases EC 3.6.4.-
Hydroxyurea X6Q56QN5QC

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2020 Duan et al.

Références

Nat Commun. 2017 Oct 16;8(1):859
pubmed: 29038466
Carcinogenesis. 2010 Jun;31(6):961-7
pubmed: 20400477
Mol Cell. 2001 Feb;7(2):263-72
pubmed: 11239455
Science. 2003 Jun 6;300(5625):1542-8
pubmed: 12791985
Nat Rev Cancer. 2015 May;15(5):276-89
pubmed: 25907220
Nat Rev Mol Cell Biol. 2010 Mar;11(3):208-19
pubmed: 20177396
Nat Commun. 2017 Oct 16;8(1):860
pubmed: 29038425
Nat Protoc. 2012 Mar 01;7(3):594-605
pubmed: 22383038
Sci Signal. 2013 Apr 02;6(269):pl1
pubmed: 23550210
J Clin Oncol. 2013 May 10;31(14):1748-57
pubmed: 23569316
Nucleic Acids Res. 2017 Sep 6;45(15):8859-8872
pubmed: 28666352
Breast Cancer Res. 2016 Nov 11;18(1):112
pubmed: 27836010
Proc Natl Acad Sci U S A. 2013 Aug 13;110(33):13558-63
pubmed: 23901102
Hum Mol Genet. 2001 Apr;10(7):705-13
pubmed: 11257103
Mol Cell. 2017 Jun 1;66(5):622-634.e8
pubmed: 28575658
Mol Cell. 2016 Dec 15;64(6):1127-1134
pubmed: 27984746
Nature. 2016 Jul 20;535(7612):382-7
pubmed: 27443740
EMBO Rep. 2018 Sep;19(9):
pubmed: 30108055
Mol Cell. 2018 Nov 1;72(3):568-582.e6
pubmed: 30344097
J Biol Chem. 2011 Jun 24;286(25):22308-13
pubmed: 21504906
Proc Natl Acad Sci U S A. 2018 Dec 26;115(52):13282-13287
pubmed: 30530694
Nat Chem Biol. 2008 Feb;4(2):119-25
pubmed: 18176557
Cell Rep. 2018 Jul 17;24(3):538-545
pubmed: 30021152
Cell Cycle. 2012 Apr 1;11(7):1432-44
pubmed: 22421153
Nat Commun. 2014 Nov 17;5:5496
pubmed: 25400221
Mol Cell. 2014 Oct 2;56(1):174-85
pubmed: 25219499
JAMA. 2017 Jun 20;317(23):2402-2416
pubmed: 28632866
J Biol Chem. 2011 Jun 24;286(25):22314-22
pubmed: 21558276
Mol Cell Biol. 2004 Mar;24(5):1930-43
pubmed: 14966274
Nat Struct Mol Biol. 2010 Nov;17(11):1305-11
pubmed: 20935632
Science. 2002 Jul 26;297(5581):599-602
pubmed: 12142537
Cell Stress. 2017 Dec;1(3):115-133
pubmed: 29355244
Genes Dev. 2005 May 1;19(9):1040-52
pubmed: 15833913
J Cell Biol. 2014 Aug 18;206(4):493-507
pubmed: 25113031
FEBS Lett. 2017 Apr;591(8):1083-1100
pubmed: 28079255
Mol Cell. 2017 Sep 7;67(5):867-881.e7
pubmed: 28757209
Oncogene. 2003 Feb 27;22(8):1115-23
pubmed: 12606939
Carcinogenesis. 2001 Nov;22(11):1789-96
pubmed: 11698340
Cancer Discov. 2012 May;2(5):401-4
pubmed: 22588877
Mol Oncol. 2013 Jun;7(3):567-79
pubmed: 23415752
Cancer Cell. 2012 Jul 10;22(1):106-16
pubmed: 22789542
Proc Natl Acad Sci U S A. 2004 Aug 31;101(35):12783-8
pubmed: 15328417
J Clin Invest. 2017 Aug 1;127(8):3013-3027
pubmed: 28691929
Cancer Cell. 2007 Feb;11(2):103-5
pubmed: 17292821
Nat Rev Mol Cell Biol. 2015 Apr;16(4):207-20
pubmed: 25714681
Genes Dev. 2011 Jun 15;25(12):1320-7
pubmed: 21685366
Mol Cell. 2011 Oct 21;44(2):235-51
pubmed: 21963239
Cancer Cell. 2018 Aug 13;34(2):197-210.e5
pubmed: 30017478
Nature. 2017 Nov 30;551(7682):590-595
pubmed: 29168504
Mol Cell. 2010 Oct 22;40(2):179-204
pubmed: 20965415
Cell. 2011 May 13;145(4):529-42
pubmed: 21565612
Nat Struct Mol Biol. 2006 Aug;13(8):729-33
pubmed: 16845393
Nucleic Acids Res. 2015 Nov 16;43(20):9835-55
pubmed: 26354865
Cancer Discov. 2015 Feb;5(2):135-42
pubmed: 25472942
Nat Rev Cancer. 2011 Dec 23;12(1):68-78
pubmed: 22193408
Nat Rev Cancer. 2016 Feb;16(2):110-20
pubmed: 26775620
Annu Rev Pathol. 2015;10:425-48
pubmed: 25621662
J Cell Biol. 2015 Mar 2;208(5):563-79
pubmed: 25733714
Nature. 2010 Oct 7;467(7316):678-83
pubmed: 20729832
Cancer Res. 2012 Jun 1;72(11):2814-21
pubmed: 22447567
Cancer Epidemiol Biomarkers Prev. 2013 May;22(5):803-11
pubmed: 23456555
Mol Cell. 2002 Jul;10(1):2-4
pubmed: 12150898
Nat Rev Cancer. 2004 Sep;4(9):665-76
pubmed: 15343273
Mol Cell. 2017 Jun 1;66(5):610-621.e4
pubmed: 28575657
Breast Cancer Res. 2008;10(4):108
pubmed: 18710587
Nat Cell Biol. 2014 Jan;16(1):2-9
pubmed: 24366029
Cell Res. 2015 Jan;25(1):9-23
pubmed: 25403473
Mol Cell. 2017 Dec 7;68(5):830-833
pubmed: 29220651
Mol Cell. 2015 Oct 15;60(2):280-93
pubmed: 26474068
Nature. 2014 Jun 26;510(7506):556-9
pubmed: 24776801
Mol Cell. 2012 Apr 27;46(2):125-35
pubmed: 22445484
Genes Dev. 2005 May 1;19(9):1007-12
pubmed: 15879550
Mol Cell. 2017 Oct 19;68(2):414-430.e8
pubmed: 29053959

Auteurs

Haohui Duan (H)

Center for Personalized Cancer Therapy, University of Massachusetts, Boston, MA.
Department of Biology, University of Massachusetts, Boston, MA.

Sarah Mansour (S)

Department of Biology, University of Massachusetts, Boston, MA.

Rachel Reed (R)

Dana-Farber Cancer Institute, Boston, MA.

Margaret K Gillis (MK)

Department of Biology, University of Massachusetts, Boston, MA.

Benjamin Parent (B)

Dana-Farber Cancer Institute, Boston, MA.

Ben Liu (B)

Dana-Farber Cancer Institute, Boston, MA.

Zsofia Sztupinszki (Z)

Danish Cancer Society Research Center, Copenhagen, Denmark.

Nicolai Birkbak (N)

Department of Molecular Medicine, Aarhus University, Aarhus, Denmark.
Bioinformatics Research Centre, Aarhus University, Aarhus, Denmark.

Zoltan Szallasi (Z)

Danish Cancer Society Research Center, Copenhagen, Denmark.
Boston Children's Hospital, Computational Health Informatics Program, Boston, MA.

Andrew E H Elia (AEH)

Massachusetts General Hospital, Department of Radiation Oncology, Center for Cancer Research, Boston, MA.

Judy E Garber (JE)

Dana-Farber Cancer Institute, Boston, MA.

Shailja Pathania (S)

Center for Personalized Cancer Therapy, University of Massachusetts, Boston, MA.
Department of Biology, University of Massachusetts, Boston, MA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH