Identification of regulators of poly-ADP-ribose polymerase inhibitor response through complementary CRISPR knockout and activation screens.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
30 11 2020
Historique:
received: 18 12 2019
accepted: 30 10 2020
entrez: 1 12 2020
pubmed: 2 12 2020
medline: 22 12 2020
Statut: epublish

Résumé

Inhibitors of poly-ADP-ribose polymerase 1 (PARPi) are highly effective in killing cells deficient in homologous recombination (HR); thus, PARPi have been clinically utilized to successfully treat BRCA2-mutant tumors. However, positive response to PARPi is not universal, even among patients with HR-deficiency. Here, we present the results of genome-wide CRISPR knockout and activation screens which reveal genetic determinants of PARPi response in wildtype or BRCA2-knockout cells. Strikingly, we report that depletion of the ubiquitin ligase HUWE1, or the histone acetyltransferase KAT5, top hits from our screens, robustly reverses the PARPi sensitivity caused by BRCA2-deficiency. We identify distinct mechanisms of resistance, in which HUWE1 loss increases RAD51 levels to partially restore HR, whereas KAT5 depletion rewires double strand break repair by promoting 53BP1 binding to double-strand breaks. Our work provides a comprehensive set of putative biomarkers that advance understanding of PARPi response, and identifies novel pathways of PARPi resistance in BRCA2-deficient cells.

Identifiants

pubmed: 33257658
doi: 10.1038/s41467-020-19961-w
pii: 10.1038/s41467-020-19961-w
pmc: PMC7704667
doi:

Substances chimiques

BRCA2 Protein 0
BRCA2 protein, human 0
Biomarkers 0
MAD2L2 protein, human 0
Mad2 Proteins 0
Poly(ADP-ribose) Polymerase Inhibitors 0
TP53BP1 protein, human 0
Tumor Suppressor Proteins 0
Tumor Suppressor p53-Binding Protein 1 0
KAT5 protein, human EC 2.3.1.48
Lysine Acetyltransferase 5 EC 2.3.1.48
HUWE1 protein, human EC 2.3.2.26
Ubiquitin-Protein Ligases EC 2.3.2.27
Poly(ADP-ribose) Polymerases EC 2.4.2.30
RAD51 protein, human EC 2.7.7.-
Rad51 Recombinase EC 2.7.7.-

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

6118

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM134681
Pays : United States
Organisme : NIEHS NIH HHS
ID : R01 ES026184
Pays : United States
Organisme : NCI NIH HHS
ID : F31 CA243301
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA222349
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM129066
Pays : United States

Références

Elife. 2017 Nov 06;6:
pubmed: 29106372
Gynecol Oncol. 2017 Dec;147(3):695-704
pubmed: 29037806
Cell. 2018 May 3;173(4):972-988.e23
pubmed: 29656893
Drugs. 2019 Jul;79(11):1231-1239
pubmed: 31267481
Mol Cell Biol. 2015 Dec;35(24):4147-57
pubmed: 26438602
Mol Cell. 2017 Aug 3;67(3):374-386.e5
pubmed: 28735897
Trends Cell Biol. 2016 Jan;26(1):52-64
pubmed: 26437586
Lancet Oncol. 2017 Jan;18(1):75-87
pubmed: 27908594
Mol Cell Biol. 2007 Oct;27(20):7028-40
pubmed: 17709392
Nat Struct Mol Biol. 2010 Jun;17(6):688-95
pubmed: 20453858
Cell. 2005 Nov 4;123(3):409-21
pubmed: 16269333
Nat Cell Biol. 2017 Nov;19(11):1371-1378
pubmed: 29035360
Nature. 2018 Jul;559(7713):279-284
pubmed: 29950726
Nat Struct Mol Biol. 2016 Aug;23(8):714-21
pubmed: 27348077
Nature. 2015 May 28;521(7553):541-544
pubmed: 25799992
PLoS One. 2013 Apr 25;8(4):e61520
pubmed: 23634208
Methods Mol Biol. 2012;920:379-91
pubmed: 22941618
J Cell Biol. 2019 Apr 1;218(4):1096-1107
pubmed: 30670471
Br J Cancer. 2016 Aug 9;115(4):431-41
pubmed: 27415012
Nature. 2016 Jul 20;535(7612):382-7
pubmed: 27443740
Nat Struct Mol Biol. 2013 Mar;20(3):317-25
pubmed: 23377543
Open Biol. 2019 Sep 27;9(9):190156
pubmed: 31506018
Cytometry A. 2012 Oct;81(10):922-8
pubmed: 22893507
Cancer Res. 2012 Nov 1;72(21):5588-99
pubmed: 23118055
EMBO Rep. 2016 Jun;17(6):874-86
pubmed: 27146073
Nat Cell Biol. 2019 Apr;21(4):487-497
pubmed: 30804506
Mol Cell. 2016 May 5;62(3):409-421
pubmed: 27153538
Nat Biotechnol. 2016 Feb;34(2):184-191
pubmed: 26780180
Nat Protoc. 2015 Sep;10(9):1297-307
pubmed: 26226461
Nature. 2011 Jun 29;474(7353):609-15
pubmed: 21720365
Nucleic Acids Res. 2016 Jan 29;44(2):648-56
pubmed: 26446986
Nature. 2005 Apr 14;434(7035):917-21
pubmed: 15829967
Nature. 2018 Jul;559(7713):285-289
pubmed: 29973717
Nature. 2015 Feb 26;518(7540):495-501
pubmed: 25719666
Cancer Discov. 2013 Jan;3(1):68-81
pubmed: 23103855
Cold Spring Harb Protoc. 2016 Mar 01;2016(3):pdb.prot090811
pubmed: 26933250
Nucleic Acids Res. 2018 Sep 28;46(17):8898-8907
pubmed: 30032296
Nature. 2018 Nov;563(7732):522-526
pubmed: 30464262
Nature. 2005 Apr 14;434(7035):913-7
pubmed: 15829966
Nat Commun. 2018 Dec 21;9(1):5416
pubmed: 30575746
Genome Biol. 2014;15(12):554
pubmed: 25476604
N Engl J Med. 2012 Apr 12;366(15):1382-92
pubmed: 22452356
Nat Commun. 2018 May 10;9(1):1849
pubmed: 29748565
Cell. 2011 May 13;145(4):529-42
pubmed: 21565612
Genes Dev. 2012 Feb 1;26(3):235-40
pubmed: 22267412
Nature. 2018 Aug;560(7716):117-121
pubmed: 30022168
Genes Dev. 2015 Mar 1;29(5):489-94
pubmed: 25737278
Mol Cell Biol. 2018 Mar 29;38(8):
pubmed: 29378830
J Biol Chem. 2014 May 9;289(19):13627-37
pubmed: 24695737
Lancet Oncol. 2017 Sep;18(9):1274-1284
pubmed: 28754483
Commun Biol. 2019 Sep 9;2:335
pubmed: 31508509
Mol Cell Biol. 2010 Jul;30(14):3582-95
pubmed: 20479123
Mol Cell Biol. 2016 May 02;36(10):1595-607
pubmed: 26976643
Cancer Cell. 2008 Jul 8;14(1):10-21
pubmed: 18598940
Cell. 2010 Apr 16;141(2):243-54
pubmed: 20362325
Nat Commun. 2017 Jul 17;8:15981
pubmed: 28714471
Mol Cell. 2017 Oct 19;68(2):414-430.e8
pubmed: 29053959

Auteurs

Kristen E Clements (KE)

Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Emily M Schleicher (EM)

Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Tanay Thakar (T)

Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Anastasia Hale (A)

Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Ashna Dhoonmoon (A)

Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Nathanial J Tolman (NJ)

Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Anchal Sharma (A)

Rutgers Cancer Institute of New Jersey, Rutgers the State University of New Jersey, New Brunswick, NJ, 08901, USA.

Xinwen Liang (X)

Department of Pediatrics, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Yuka Imamura Kawasawa (Y)

Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.
Department of Pharmacology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.
Institute for Personalized Medicine, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Claudia M Nicolae (CM)

Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Hong-Gang Wang (HG)

Department of Pediatrics, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.
Department of Pharmacology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA.

Subhajyoti De (S)

Rutgers Cancer Institute of New Jersey, Rutgers the State University of New Jersey, New Brunswick, NJ, 08901, USA.

George-Lucian Moldovan (GL)

Department of Biochemistry and Molecular Biology, The Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA. glm29@psu.edu.

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Classifications MeSH