SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere Recombination

In budding yeast, inactivation of telomerase and ensuing telomere erosion cause relocalization of telomeres to nuclear pore complexes (NPCs). However, neither the mechanism of such relocalization nor its significance are understood. We report that proteins bound to eroded telomeres are recognized by...

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Main Authors: Dmitri Churikov, Ferose Charifi, Nadine Eckert-Boulet, Sonia Silva, Marie-Noelle Simon, Michael Lisby, Vincent Géli
Format: Article
Language:English
Published: Elsevier 2016-05-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124716304077
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author Dmitri Churikov
Ferose Charifi
Nadine Eckert-Boulet
Sonia Silva
Marie-Noelle Simon
Michael Lisby
Vincent Géli
author_facet Dmitri Churikov
Ferose Charifi
Nadine Eckert-Boulet
Sonia Silva
Marie-Noelle Simon
Michael Lisby
Vincent Géli
author_sort Dmitri Churikov
collection DOAJ
description In budding yeast, inactivation of telomerase and ensuing telomere erosion cause relocalization of telomeres to nuclear pore complexes (NPCs). However, neither the mechanism of such relocalization nor its significance are understood. We report that proteins bound to eroded telomeres are recognized by the SUMO (small ubiquitin-like modifier)-targeted ubiquitin ligase (STUbL) Slx5-Slx8 and become increasingly SUMOylated. Recruitment of Slx5-Slx8 to eroded telomeres facilitates telomere relocalization to NPCs and type II telomere recombination, a counterpart of mammalian alternative lengthening of telomeres (ALT). Moreover, artificial tethering of a telomere to a NPC promotes type II telomere recombination but cannot bypass the lack of Slx5-Slx8 in this process. Together, our results indicate that SUMOylation positively contributes to telomere relocalization to the NPC, where poly-SUMOylated proteins that accumulated over time have to be removed. We propose that STUbL-dependent relocalization of telomeres to NPCs constitutes a pathway in which excessively SUMOylated proteins are removed from “congested” intermediates to ensure unconventional recombination.
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spelling doaj.art-f157344913c345958bbf7bf2fd175f1c2022-12-22T03:04:58ZengElsevierCell Reports2211-12472016-05-011561242125310.1016/j.celrep.2016.04.008SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere RecombinationDmitri Churikov0Ferose Charifi1Nadine Eckert-Boulet2Sonia Silva3Marie-Noelle Simon4Michael Lisby5Vincent Géli6Marseille Cancer Research Center (CRCM), U1068 INSERM, UMR7258 CNRS, Aix Marseille University, Institut Paoli-Calmettes (Equipe labellisée Ligue), Marseille 13009, FranceMarseille Cancer Research Center (CRCM), U1068 INSERM, UMR7258 CNRS, Aix Marseille University, Institut Paoli-Calmettes (Equipe labellisée Ligue), Marseille 13009, FranceDepartment of Biology, University of Copenhagen, 2200 Copenhagen N, DenmarkDepartment of Biology, University of Copenhagen, 2200 Copenhagen N, DenmarkMarseille Cancer Research Center (CRCM), U1068 INSERM, UMR7258 CNRS, Aix Marseille University, Institut Paoli-Calmettes (Equipe labellisée Ligue), Marseille 13009, FranceDepartment of Biology, University of Copenhagen, 2200 Copenhagen N, DenmarkMarseille Cancer Research Center (CRCM), U1068 INSERM, UMR7258 CNRS, Aix Marseille University, Institut Paoli-Calmettes (Equipe labellisée Ligue), Marseille 13009, FranceIn budding yeast, inactivation of telomerase and ensuing telomere erosion cause relocalization of telomeres to nuclear pore complexes (NPCs). However, neither the mechanism of such relocalization nor its significance are understood. We report that proteins bound to eroded telomeres are recognized by the SUMO (small ubiquitin-like modifier)-targeted ubiquitin ligase (STUbL) Slx5-Slx8 and become increasingly SUMOylated. Recruitment of Slx5-Slx8 to eroded telomeres facilitates telomere relocalization to NPCs and type II telomere recombination, a counterpart of mammalian alternative lengthening of telomeres (ALT). Moreover, artificial tethering of a telomere to a NPC promotes type II telomere recombination but cannot bypass the lack of Slx5-Slx8 in this process. Together, our results indicate that SUMOylation positively contributes to telomere relocalization to the NPC, where poly-SUMOylated proteins that accumulated over time have to be removed. We propose that STUbL-dependent relocalization of telomeres to NPCs constitutes a pathway in which excessively SUMOylated proteins are removed from “congested” intermediates to ensure unconventional recombination.http://www.sciencedirect.com/science/article/pii/S2211124716304077
spellingShingle Dmitri Churikov
Ferose Charifi
Nadine Eckert-Boulet
Sonia Silva
Marie-Noelle Simon
Michael Lisby
Vincent Géli
SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere Recombination
Cell Reports
title SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere Recombination
title_full SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere Recombination
title_fullStr SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere Recombination
title_full_unstemmed SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere Recombination
title_short SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere Recombination
title_sort sumo dependent relocalization of eroded telomeres to nuclear pore complexes controls telomere recombination
url http://www.sciencedirect.com/science/article/pii/S2211124716304077
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