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The ubiquitin-dependent ATPase p97 removes cytotoxic trapped PARP1 from chromatin

Abstract:
Poly (ADP-ribose) polymerase (PARP) inhibitors elicit antitumour activity in homologous recombination-defective cancers by trapping PARP1 in a chromatin-bound state. How cells process trapped PARP1 remains unclear. Using wild-type and a trapping-deficient PARP1 mutant combined with rapid immunoprecipitation mass spectrometry of endogenous proteins and Apex2 proximity labelling, we delineated mass spectrometry-based interactomes of trapped and non-trapped PARP1. These analyses identified an interaction between trapped PARP1 and the ubiquitin-regulated p97 ATPase/segregase. We found that following trapping, PARP1 is SUMOylated by PIAS4 and subsequently ubiquitylated by the SUMO-targeted E3 ubiquitin ligase RNF4, events that promote recruitment of p97 and removal of trapped PARP1 from chromatin. Small-molecule p97-complex inhibitors, including a metabolite of the clinically used drug disulfiram (CuET), prolonged PARP1 trapping and enhanced PARP inhibitor-induced cytotoxicity in homologous recombination-defective tumour cells and patient-derived tumour organoids. Together, these results suggest that p97 ATPase plays a key role in the processing of trapped PARP1 and the response of tumour cells to PARP inhibitors.
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1038/s41556-021-00807-6

Authors


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Role:
Author
ORCID:
0000-0003-4298-7272
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Role:
Author
ORCID:
0000-0002-6249-2704
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Role:
Author
ORCID:
0000-0002-9307-3262
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Role:
Author
ORCID:
0000-0002-0030-7761


Publisher:
Springer Nature
Journal:
Nature Cell Biology More from this journal
Volume:
24
Issue:
1
Pages:
62-73
Publication date:
2022-01-10
Acceptance date:
2021-11-03
DOI:
EISSN:
1476-4679
ISSN:
1465-7392
Pmid:
35013556


Language:
English
Keywords:
Pubs id:
1231620
Local pid:
pubs:1231620
Deposit date:
2022-04-23

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