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Tousled-like kinases stabilize replication forks and show synthetic lethality with checkpoint and PARP inhibitors

Lee, Sung Bau ; Segura-Bayona, Sandra ; Villamor-Payà, Marina ; Saredi, Giulia LU ; Todd, Matthew A.M. ; Attolini, Camille Stephan Otto ; Chang, Ting Yu ; Stracker, Travis H. and Groth, Anja (2018) In Science Advances 4(8).
Abstract

DNA sequence and epigenetic information embedded in chromatin must be faithfully duplicated and transmitted to daughter cells during cell division. However, how chromatin assembly and DNA replication are integrated remains unclear. We examined the contribution of the Tousled-like kinases 1 and 2 (TLK1/TLK2) to chromatin assembly and maintenance of replication fork integrity. We show that TLK activity is required for DNA replication and replication-coupled nucleosome assembly and that lack of TLK activity leads to replication fork stalling and the accumulation of single-stranded DNA, a phenotype distinct from ASF1 depletion. Consistent with these results, sustained TLK depletion gives rise to replication-dependent DNA damage and... (More)

DNA sequence and epigenetic information embedded in chromatin must be faithfully duplicated and transmitted to daughter cells during cell division. However, how chromatin assembly and DNA replication are integrated remains unclear. We examined the contribution of the Tousled-like kinases 1 and 2 (TLK1/TLK2) to chromatin assembly and maintenance of replication fork integrity. We show that TLK activity is required for DNA replication and replication-coupled nucleosome assembly and that lack of TLK activity leads to replication fork stalling and the accumulation of single-stranded DNA, a phenotype distinct from ASF1 depletion. Consistent with these results, sustained TLK depletion gives rise to replication-dependent DNA damage and p53-dependent cell cycle arrest in G1. We find that deficient replication-coupled de novo nucleosome assembly renders replication forks unstable and highly dependent on the ATR and CHK1 checkpoint kinases, as well as poly(adenosine 5′-diphosphate–ribose) polymerase (PARP) activity, to avoid collapse. Human cancer data revealed frequent up-regulation of TLK genes and an association with poor patient outcome in multiple types of cancer, and depletion of TLK activity leads to increased replication stress and DNA damage in a panel of cancer cells. Our results reveal a critical role for TLKs in chromatin replication and suppression of replication stress and identify a synergistic lethal relationship with checkpoint signaling and PARP that could be exploited in treatment of a broad range of cancers.

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author
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publishing date
type
Contribution to journal
publication status
published
in
Science Advances
volume
4
issue
8
article number
eaat4985
publisher
American Association for the Advancement of Science (AAAS)
external identifiers
  • scopus:85051404535
  • pmid:30101194
ISSN
2375-2548
DOI
10.1126/sciadv.aat4985
language
English
LU publication?
no
additional info
Publisher Copyright: Copyright © 2018 The Authors.
id
ced2ae3a-f2f7-4f7c-aaf0-cc6555412a1f
date added to LUP
2025-11-03 11:16:41
date last changed
2025-11-17 12:22:29
@article{ced2ae3a-f2f7-4f7c-aaf0-cc6555412a1f,
  abstract     = {{<p>DNA sequence and epigenetic information embedded in chromatin must be faithfully duplicated and transmitted to daughter cells during cell division. However, how chromatin assembly and DNA replication are integrated remains unclear. We examined the contribution of the Tousled-like kinases 1 and 2 (TLK1/TLK2) to chromatin assembly and maintenance of replication fork integrity. We show that TLK activity is required for DNA replication and replication-coupled nucleosome assembly and that lack of TLK activity leads to replication fork stalling and the accumulation of single-stranded DNA, a phenotype distinct from ASF1 depletion. Consistent with these results, sustained TLK depletion gives rise to replication-dependent DNA damage and p53-dependent cell cycle arrest in G<sub>1</sub>. We find that deficient replication-coupled de novo nucleosome assembly renders replication forks unstable and highly dependent on the ATR and CHK1 checkpoint kinases, as well as poly(adenosine 5′-diphosphate–ribose) polymerase (PARP) activity, to avoid collapse. Human cancer data revealed frequent up-regulation of TLK genes and an association with poor patient outcome in multiple types of cancer, and depletion of TLK activity leads to increased replication stress and DNA damage in a panel of cancer cells. Our results reveal a critical role for TLKs in chromatin replication and suppression of replication stress and identify a synergistic lethal relationship with checkpoint signaling and PARP that could be exploited in treatment of a broad range of cancers.</p>}},
  author       = {{Lee, Sung Bau and Segura-Bayona, Sandra and Villamor-Payà, Marina and Saredi, Giulia and Todd, Matthew A.M. and Attolini, Camille Stephan Otto and Chang, Ting Yu and Stracker, Travis H. and Groth, Anja}},
  issn         = {{2375-2548}},
  language     = {{eng}},
  month        = {{08}},
  number       = {{8}},
  publisher    = {{American Association for the Advancement of Science (AAAS)}},
  series       = {{Science Advances}},
  title        = {{Tousled-like kinases stabilize replication forks and show synthetic lethality with checkpoint and PARP inhibitors}},
  url          = {{http://dx.doi.org/10.1126/sciadv.aat4985}},
  doi          = {{10.1126/sciadv.aat4985}},
  volume       = {{4}},
  year         = {{2018}},
}