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ZNF432 stimulates PARylation and inhibits DNA resection to balance PARPi sensitivity and resistance

Zinc finger (ZNF) motifs are some of the most frequently occurring domains in the human genome. It was only recently that ZNF proteins emerged as key regulators of genome integrity in mammalian cells. In this study, we report a new role for the Krüppel-type ZNF-containing protein ZNF432 as a novel p...

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Autores principales: O’Sullivan, Julia, Kothari, Charu, Caron, Marie-Christine, Gagné, Jean-Philippe, Jin, Zhigang, Nonfoux, Louis, Beneyton, Adèle, Coulombe, Yan, Thomas, Mélissa, Atalay, Nurgul, Meng, X Wei, Milano, Larissa, Jean, Dominique, Boisvert, François-Michel, Kaufmann, Scott H, Hendzel, Michael J, Masson, Jean-Yves, Poirier, Guy G
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10639050/
https://www.ncbi.nlm.nih.gov/pubmed/37823600
http://dx.doi.org/10.1093/nar/gkad791
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author O’Sullivan, Julia
Kothari, Charu
Caron, Marie-Christine
Gagné, Jean-Philippe
Jin, Zhigang
Nonfoux, Louis
Beneyton, Adèle
Coulombe, Yan
Thomas, Mélissa
Atalay, Nurgul
Meng, X Wei
Milano, Larissa
Jean, Dominique
Boisvert, François-Michel
Kaufmann, Scott H
Hendzel, Michael J
Masson, Jean-Yves
Poirier, Guy G
author_facet O’Sullivan, Julia
Kothari, Charu
Caron, Marie-Christine
Gagné, Jean-Philippe
Jin, Zhigang
Nonfoux, Louis
Beneyton, Adèle
Coulombe, Yan
Thomas, Mélissa
Atalay, Nurgul
Meng, X Wei
Milano, Larissa
Jean, Dominique
Boisvert, François-Michel
Kaufmann, Scott H
Hendzel, Michael J
Masson, Jean-Yves
Poirier, Guy G
author_sort O’Sullivan, Julia
collection PubMed
description Zinc finger (ZNF) motifs are some of the most frequently occurring domains in the human genome. It was only recently that ZNF proteins emerged as key regulators of genome integrity in mammalian cells. In this study, we report a new role for the Krüppel-type ZNF-containing protein ZNF432 as a novel poly(ADP-ribose) (PAR) reader that regulates the DNA damage response. We show that ZNF432 is recruited to DNA lesions via DNA- and PAR-dependent mechanisms. Remarkably, ZNF432 stimulates PARP-1 activity in vitro and in cellulo. Knockdown of ZNF432 inhibits phospho-DNA-PKcs and increases RAD51 foci formation following irradiation. Moreover, purified ZNF432 preferentially binds single-stranded DNA and impairs EXO1-mediated DNA resection. Consequently, the loss of ZNF432 in a cellular system leads to resistance to PARP inhibitors while its overexpression results in sensitivity. Taken together, our results support the emerging concept that ZNF-containing proteins can modulate PARylation, which can be embodied by the pivotal role of ZNF432 to finely balance the outcome of PARPi response by regulating homologous recombination.
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spelling pubmed-106390502023-11-15 ZNF432 stimulates PARylation and inhibits DNA resection to balance PARPi sensitivity and resistance O’Sullivan, Julia Kothari, Charu Caron, Marie-Christine Gagné, Jean-Philippe Jin, Zhigang Nonfoux, Louis Beneyton, Adèle Coulombe, Yan Thomas, Mélissa Atalay, Nurgul Meng, X Wei Milano, Larissa Jean, Dominique Boisvert, François-Michel Kaufmann, Scott H Hendzel, Michael J Masson, Jean-Yves Poirier, Guy G Nucleic Acids Res Genome Integrity, Repair and Replication Zinc finger (ZNF) motifs are some of the most frequently occurring domains in the human genome. It was only recently that ZNF proteins emerged as key regulators of genome integrity in mammalian cells. In this study, we report a new role for the Krüppel-type ZNF-containing protein ZNF432 as a novel poly(ADP-ribose) (PAR) reader that regulates the DNA damage response. We show that ZNF432 is recruited to DNA lesions via DNA- and PAR-dependent mechanisms. Remarkably, ZNF432 stimulates PARP-1 activity in vitro and in cellulo. Knockdown of ZNF432 inhibits phospho-DNA-PKcs and increases RAD51 foci formation following irradiation. Moreover, purified ZNF432 preferentially binds single-stranded DNA and impairs EXO1-mediated DNA resection. Consequently, the loss of ZNF432 in a cellular system leads to resistance to PARP inhibitors while its overexpression results in sensitivity. Taken together, our results support the emerging concept that ZNF-containing proteins can modulate PARylation, which can be embodied by the pivotal role of ZNF432 to finely balance the outcome of PARPi response by regulating homologous recombination. Oxford University Press 2023-10-12 /pmc/articles/PMC10639050/ /pubmed/37823600 http://dx.doi.org/10.1093/nar/gkad791 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Genome Integrity, Repair and Replication
O’Sullivan, Julia
Kothari, Charu
Caron, Marie-Christine
Gagné, Jean-Philippe
Jin, Zhigang
Nonfoux, Louis
Beneyton, Adèle
Coulombe, Yan
Thomas, Mélissa
Atalay, Nurgul
Meng, X Wei
Milano, Larissa
Jean, Dominique
Boisvert, François-Michel
Kaufmann, Scott H
Hendzel, Michael J
Masson, Jean-Yves
Poirier, Guy G
ZNF432 stimulates PARylation and inhibits DNA resection to balance PARPi sensitivity and resistance
title ZNF432 stimulates PARylation and inhibits DNA resection to balance PARPi sensitivity and resistance
title_full ZNF432 stimulates PARylation and inhibits DNA resection to balance PARPi sensitivity and resistance
title_fullStr ZNF432 stimulates PARylation and inhibits DNA resection to balance PARPi sensitivity and resistance
title_full_unstemmed ZNF432 stimulates PARylation and inhibits DNA resection to balance PARPi sensitivity and resistance
title_short ZNF432 stimulates PARylation and inhibits DNA resection to balance PARPi sensitivity and resistance
title_sort znf432 stimulates parylation and inhibits dna resection to balance parpi sensitivity and resistance
topic Genome Integrity, Repair and Replication
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10639050/
https://www.ncbi.nlm.nih.gov/pubmed/37823600
http://dx.doi.org/10.1093/nar/gkad791
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