Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation.

The DNA-damage checkpoint kinase Chk1 is essential in higher eukaryotes due to its role in maintaining genome stability in proliferating cells. CHK1 gene deletion is embryonically lethal, and Chk1 inhibition in replicating cells causes cell-cycle defects that eventually lead to perturbed replication...

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Main Authors: Josep V Forment, Melanie Blasius, Ilaria Guerini, Stephen P Jackson
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0023517&type=printable
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author Josep V Forment
Melanie Blasius
Ilaria Guerini
Stephen P Jackson
author_facet Josep V Forment
Melanie Blasius
Ilaria Guerini
Stephen P Jackson
author_sort Josep V Forment
collection DOAJ
description The DNA-damage checkpoint kinase Chk1 is essential in higher eukaryotes due to its role in maintaining genome stability in proliferating cells. CHK1 gene deletion is embryonically lethal, and Chk1 inhibition in replicating cells causes cell-cycle defects that eventually lead to perturbed replication and replication-fork collapse, thus generating endogenous DNA damage. What is the cause of replication-fork collapse when Chk1 is inactivated, however, remains poorly understood. Here, we show that generation of DNA double-strand breaks at replication forks when Chk1 activity is compromised relies on the DNA endonuclease complex Mus81/Eme1. Importantly, we show that Mus81/Eme1-dependent DNA damage--rather than a global increase in replication-fork stalling--is the cause of incomplete replication in Chk1-deficient cells. Consequently, Mus81/Eme1 depletion alleviates the S-phase progression defects associated with Chk1 deficiency, thereby increasing cell survival. Chk1-mediated protection of replication forks from Mus81/Eme1 even under otherwise unchallenged conditions is therefore vital to prevent uncontrolled fork collapse and ensure proper S-phase progression in human cells.
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spelling doaj-art-4d31517ce9114da7bfb8a6972a4653762025-08-20T03:10:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-0168e2351710.1371/journal.pone.0023517Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation.Josep V FormentMelanie BlasiusIlaria GueriniStephen P JacksonThe DNA-damage checkpoint kinase Chk1 is essential in higher eukaryotes due to its role in maintaining genome stability in proliferating cells. CHK1 gene deletion is embryonically lethal, and Chk1 inhibition in replicating cells causes cell-cycle defects that eventually lead to perturbed replication and replication-fork collapse, thus generating endogenous DNA damage. What is the cause of replication-fork collapse when Chk1 is inactivated, however, remains poorly understood. Here, we show that generation of DNA double-strand breaks at replication forks when Chk1 activity is compromised relies on the DNA endonuclease complex Mus81/Eme1. Importantly, we show that Mus81/Eme1-dependent DNA damage--rather than a global increase in replication-fork stalling--is the cause of incomplete replication in Chk1-deficient cells. Consequently, Mus81/Eme1 depletion alleviates the S-phase progression defects associated with Chk1 deficiency, thereby increasing cell survival. Chk1-mediated protection of replication forks from Mus81/Eme1 even under otherwise unchallenged conditions is therefore vital to prevent uncontrolled fork collapse and ensure proper S-phase progression in human cells.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0023517&type=printable
spellingShingle Josep V Forment
Melanie Blasius
Ilaria Guerini
Stephen P Jackson
Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation.
PLoS ONE
title Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation.
title_full Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation.
title_fullStr Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation.
title_full_unstemmed Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation.
title_short Structure-specific DNA endonuclease Mus81/Eme1 generates DNA damage caused by Chk1 inactivation.
title_sort structure specific dna endonuclease mus81 eme1 generates dna damage caused by chk1 inactivation
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0023517&type=printable
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AT ilariaguerini structurespecificdnaendonucleasemus81eme1generatesdnadamagecausedbychk1inactivation
AT stephenpjackson structurespecificdnaendonucleasemus81eme1generatesdnadamagecausedbychk1inactivation