The DNA replication checkpoint targets the kinetochore to reposition DNA structure-induced replication damage to the nuclear periphery

Summary: Hairpin-forming CAG/CTG repeats pose significant challenges to DNA replication. In S. cerevisiae, long CAG/CTG repeat tracts reposition from the interior of the nucleus to the nuclear pore complex (NPC) to maintain their integrity. We show that relocation of a (CAG/CTG)130 tract to the NPC...

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Main Authors: Tyler M. Maclay, Jenna M. Whalen, Matthew J. Johnson, Catherine H. Freudenreich
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S221112472500854X
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author Tyler M. Maclay
Jenna M. Whalen
Matthew J. Johnson
Catherine H. Freudenreich
author_facet Tyler M. Maclay
Jenna M. Whalen
Matthew J. Johnson
Catherine H. Freudenreich
author_sort Tyler M. Maclay
collection DOAJ
description Summary: Hairpin-forming CAG/CTG repeats pose significant challenges to DNA replication. In S. cerevisiae, long CAG/CTG repeat tracts reposition from the interior of the nucleus to the nuclear pore complex (NPC) to maintain their integrity. We show that relocation of a (CAG/CTG)130 tract to the NPC is dependent on phosphorylation of Mrc1 (hClaspin) of the fork protection complex and activation of the Mrc1/Rad53 replication checkpoint, implicating an uncoupled fork as the initial damage signal. Dun1-mediated phosphorylation of the kinetochore protein Cep3 is required for repositioning, a constraint that can be overcome by centromere inactivation, connecting detachment of the kinetochore from microtubule ends to NPC association. Activation of this pathway leads to the formation of DNA damage-induced microtubules, which associate with the repeat and are necessary for locus repositioning. These data implicate the replication checkpoint in facilitating the movement of DNA structure-associated damage to the nuclear periphery by centromere release and microtubule-directed motion.
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spelling doaj-art-06cdeec6b49841d8801b5a94d56a59e22025-08-20T03:58:11ZengElsevierCell Reports2211-12472025-08-0144811608310.1016/j.celrep.2025.116083The DNA replication checkpoint targets the kinetochore to reposition DNA structure-induced replication damage to the nuclear peripheryTyler M. Maclay0Jenna M. Whalen1Matthew J. Johnson2Catherine H. Freudenreich3Department of Biology, Tufts University, Medford, MA 02155, USADepartment of Biology, Tufts University, Medford, MA 02155, USADepartment of Biology, Tufts University, Medford, MA 02155, USADepartment of Biology, Tufts University, Medford, MA 02155, USA; Corresponding authorSummary: Hairpin-forming CAG/CTG repeats pose significant challenges to DNA replication. In S. cerevisiae, long CAG/CTG repeat tracts reposition from the interior of the nucleus to the nuclear pore complex (NPC) to maintain their integrity. We show that relocation of a (CAG/CTG)130 tract to the NPC is dependent on phosphorylation of Mrc1 (hClaspin) of the fork protection complex and activation of the Mrc1/Rad53 replication checkpoint, implicating an uncoupled fork as the initial damage signal. Dun1-mediated phosphorylation of the kinetochore protein Cep3 is required for repositioning, a constraint that can be overcome by centromere inactivation, connecting detachment of the kinetochore from microtubule ends to NPC association. Activation of this pathway leads to the formation of DNA damage-induced microtubules, which associate with the repeat and are necessary for locus repositioning. These data implicate the replication checkpoint in facilitating the movement of DNA structure-associated damage to the nuclear periphery by centromere release and microtubule-directed motion.http://www.sciencedirect.com/science/article/pii/S221112472500854XCP: Molecular biology
spellingShingle Tyler M. Maclay
Jenna M. Whalen
Matthew J. Johnson
Catherine H. Freudenreich
The DNA replication checkpoint targets the kinetochore to reposition DNA structure-induced replication damage to the nuclear periphery
Cell Reports
CP: Molecular biology
title The DNA replication checkpoint targets the kinetochore to reposition DNA structure-induced replication damage to the nuclear periphery
title_full The DNA replication checkpoint targets the kinetochore to reposition DNA structure-induced replication damage to the nuclear periphery
title_fullStr The DNA replication checkpoint targets the kinetochore to reposition DNA structure-induced replication damage to the nuclear periphery
title_full_unstemmed The DNA replication checkpoint targets the kinetochore to reposition DNA structure-induced replication damage to the nuclear periphery
title_short The DNA replication checkpoint targets the kinetochore to reposition DNA structure-induced replication damage to the nuclear periphery
title_sort dna replication checkpoint targets the kinetochore to reposition dna structure induced replication damage to the nuclear periphery
topic CP: Molecular biology
url http://www.sciencedirect.com/science/article/pii/S221112472500854X
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