TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALT

Abstract In some types of cancer, telomere length is maintained by the alternative lengthening of telomeres (ALT) mechanism. In many ALT cancers, the α‐thalassemia/mental retardation syndrome X‐linked (ATRX) gene is mutated leading to the conclusion that the ATRX complex represses ALT. Here, we repo...

Full description

Saved in:
Bibliographic Details
Main Authors: Alexandre de Nonneville, Sébastien Salas, François Bertucci, Alexander P Sobinoff, José Adélaïde, Arnaud Guille, Pascal Finetti, Jane R Noble, Dimitri Churikov, Max Chaffanet, Elise Lavit, Hilda A Pickett, Corinne Bouvier, Daniel Birnbaum, Roger R Reddel, Vincent Géli
Format: Article
Language:English
Published: Springer Nature 2022-08-01
Series:EMBO Molecular Medicine
Subjects:
Online Access:https://doi.org/10.15252/emmm.202215859
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849234700491554816
author Alexandre de Nonneville
Sébastien Salas
François Bertucci
Alexander P Sobinoff
José Adélaïde
Arnaud Guille
Pascal Finetti
Jane R Noble
Dimitri Churikov
Max Chaffanet
Elise Lavit
Hilda A Pickett
Corinne Bouvier
Daniel Birnbaum
Roger R Reddel
Vincent Géli
author_facet Alexandre de Nonneville
Sébastien Salas
François Bertucci
Alexander P Sobinoff
José Adélaïde
Arnaud Guille
Pascal Finetti
Jane R Noble
Dimitri Churikov
Max Chaffanet
Elise Lavit
Hilda A Pickett
Corinne Bouvier
Daniel Birnbaum
Roger R Reddel
Vincent Géli
author_sort Alexandre de Nonneville
collection DOAJ
description Abstract In some types of cancer, telomere length is maintained by the alternative lengthening of telomeres (ALT) mechanism. In many ALT cancers, the α‐thalassemia/mental retardation syndrome X‐linked (ATRX) gene is mutated leading to the conclusion that the ATRX complex represses ALT. Here, we report that most high‐grade pediatric osteosarcomas maintain their telomeres by ALT, and that the majority of these ALT tumors are ATRX wild‐type (wt) and instead carry an amplified 17p11.2 chromosomal region containing TOP3A. We found that TOP3A was overexpressed in the ALT‐positive ATRX‐wt tumors consistent with its amplification. We demonstrated the functional significance of these results by showing that TOP3A overexpression in ALT cancer cells countered ATRX‐mediated ALT inhibition and that TOP3A knockdown disrupted the ALT phenotype in ATRX‐wt cells. Moreover, we report that TOP3A is required for proper BLM localization and promotes ALT DNA synthesis in ALT cell lines. Collectively, our results identify TOP3A as a major ALT player and potential therapeutic target.
format Article
id doaj-art-948680b27447452fa822018d83b4b8e5
institution Kabale University
issn 1757-4676
1757-4684
language English
publishDate 2022-08-01
publisher Springer Nature
record_format Article
series EMBO Molecular Medicine
spelling doaj-art-948680b27447452fa822018d83b4b8e52025-08-20T04:03:02ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842022-08-01141012210.15252/emmm.202215859TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALTAlexandre de Nonneville0Sébastien Salas1François Bertucci2Alexander P Sobinoff3José Adélaïde4Arnaud Guille5Pascal Finetti6Jane R Noble7Dimitri Churikov8Max Chaffanet9Elise Lavit10Hilda A Pickett11Corinne Bouvier12Daniel Birnbaum13Roger R Reddel14Vincent Géli15Marseille Cancer Research Centre (CRCM), Inserm U1068, CNRS UMR7258, Institut Paoli‐Calmettes, Team « Telomere and Chromatin ». Equipe labellisée Ligue Nationale Contre Le Cancer, Aix‐Marseille UnivDepartment of Medical Oncology, Assistance Publique Hôpitaux de Marseille ‐ Timone HospitalPredictive Oncology Laboratory, Marseille Cancer Research Centre (CRCM), Inserm U1068, CNRS UMR7258, Institut Paoli‐Calmettes, Aix‐Marseille UniversityTelomere Length Regulation Unit, Faculty of Medicine and Health, Children's Medical Research Institute, University of SydneyPredictive Oncology Laboratory, Marseille Cancer Research Centre (CRCM), Inserm U1068, CNRS UMR7258, Institut Paoli‐Calmettes, Aix‐Marseille UniversityPredictive Oncology Laboratory, Marseille Cancer Research Centre (CRCM), Inserm U1068, CNRS UMR7258, Institut Paoli‐Calmettes, Aix‐Marseille UniversityPredictive Oncology Laboratory, Marseille Cancer Research Centre (CRCM), Inserm U1068, CNRS UMR7258, Institut Paoli‐Calmettes, Aix‐Marseille UniversityCancer Research Unit, Faculty of Medicine and Health, Children's Medical Research Institute, University of SydneyMarseille Cancer Research Centre (CRCM), Inserm U1068, CNRS UMR7258, Institut Paoli‐Calmettes, Team « Telomere and Chromatin ». Equipe labellisée Ligue Nationale Contre Le Cancer, Aix‐Marseille UnivPredictive Oncology Laboratory, Marseille Cancer Research Centre (CRCM), Inserm U1068, CNRS UMR7258, Institut Paoli‐Calmettes, Aix‐Marseille UniversityDepartment of Medical Oncology, Assistance Publique Hôpitaux de Marseille ‐ Timone HospitalTelomere Length Regulation Unit, Faculty of Medicine and Health, Children's Medical Research Institute, University of SydneyDepartment of Pathology, Assistance Publique Hôpitaux de Marseille ‐ Timone HospitalPredictive Oncology Laboratory, Marseille Cancer Research Centre (CRCM), Inserm U1068, CNRS UMR7258, Institut Paoli‐Calmettes, Aix‐Marseille UniversityCancer Research Unit, Faculty of Medicine and Health, Children's Medical Research Institute, University of SydneyMarseille Cancer Research Centre (CRCM), Inserm U1068, CNRS UMR7258, Institut Paoli‐Calmettes, Team « Telomere and Chromatin ». Equipe labellisée Ligue Nationale Contre Le Cancer, Aix‐Marseille UnivAbstract In some types of cancer, telomere length is maintained by the alternative lengthening of telomeres (ALT) mechanism. In many ALT cancers, the α‐thalassemia/mental retardation syndrome X‐linked (ATRX) gene is mutated leading to the conclusion that the ATRX complex represses ALT. Here, we report that most high‐grade pediatric osteosarcomas maintain their telomeres by ALT, and that the majority of these ALT tumors are ATRX wild‐type (wt) and instead carry an amplified 17p11.2 chromosomal region containing TOP3A. We found that TOP3A was overexpressed in the ALT‐positive ATRX‐wt tumors consistent with its amplification. We demonstrated the functional significance of these results by showing that TOP3A overexpression in ALT cancer cells countered ATRX‐mediated ALT inhibition and that TOP3A knockdown disrupted the ALT phenotype in ATRX‐wt cells. Moreover, we report that TOP3A is required for proper BLM localization and promotes ALT DNA synthesis in ALT cell lines. Collectively, our results identify TOP3A as a major ALT player and potential therapeutic target.https://doi.org/10.15252/emmm.202215859alternative lengthening of telomeresATRXosteosarcomastelomeresTOP3A
spellingShingle Alexandre de Nonneville
Sébastien Salas
François Bertucci
Alexander P Sobinoff
José Adélaïde
Arnaud Guille
Pascal Finetti
Jane R Noble
Dimitri Churikov
Max Chaffanet
Elise Lavit
Hilda A Pickett
Corinne Bouvier
Daniel Birnbaum
Roger R Reddel
Vincent Géli
TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALT
EMBO Molecular Medicine
alternative lengthening of telomeres
ATRX
osteosarcomas
telomeres
TOP3A
title TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALT
title_full TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALT
title_fullStr TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALT
title_full_unstemmed TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALT
title_short TOP3A amplification and ATRX inactivation are mutually exclusive events in pediatric osteosarcomas using ALT
title_sort top3a amplification and atrx inactivation are mutually exclusive events in pediatric osteosarcomas using alt
topic alternative lengthening of telomeres
ATRX
osteosarcomas
telomeres
TOP3A
url https://doi.org/10.15252/emmm.202215859
work_keys_str_mv AT alexandredenonneville top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT sebastiensalas top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT francoisbertucci top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT alexanderpsobinoff top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT joseadelaide top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT arnaudguille top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT pascalfinetti top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT janernoble top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT dimitrichurikov top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT maxchaffanet top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT eliselavit top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT hildaapickett top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT corinnebouvier top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT danielbirnbaum top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT rogerrreddel top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt
AT vincentgeli top3aamplificationandatrxinactivationaremutuallyexclusiveeventsinpediatricosteosarcomasusingalt