Elevated enhancer-oncogene contacts and higher oncogene expression levels by recurrent CTCF inactivating mutations in acute T cell leukemia.


Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
25 04 2023
Historique:
received: 25 10 2022
revised: 18 03 2023
accepted: 23 03 2023
medline: 4 10 2023
pubmed: 16 4 2023
entrez: 15 4 2023
Statut: ppublish

Résumé

Monoallelic inactivation of CCCTC-binding factor (CTCF) in human cancer drives altered methylated genomic states, altered CTCF occupancy at promoter and enhancer regions, and deregulated global gene expression. In patients with T cell acute lymphoblastic leukemia (T-ALL), we find that acquired monoallelic CTCF-inactivating events drive subtle and local genomic effects in nearly half of t(5; 14) (q35; q32.2) rearranged patients, especially when CTCF-binding sites are preserved in between the BCL11B enhancer and the TLX3 oncogene. These solitary intervening sites insulate TLX3 from the enhancer by inducing competitive looping to multiple binding sites near the TLX3 promoter. Reduced CTCF levels or deletion of the intervening CTCF site abrogates enhancer insulation by weakening competitive looping while favoring TLX3 promoter to BCL11B enhancer looping, which elevates oncogene expression levels and leukemia burden.

Identifiants

pubmed: 37060567
pii: S2211-1247(23)00384-4
doi: 10.1016/j.celrep.2023.112373
pii:
doi:

Substances chimiques

BCL11B protein, human 0
CCCTC-Binding Factor 0
Chromatin 0
Repressor Proteins 0
Transcription Factors 0
Tumor Suppressor Proteins 0
CTCF protein, human 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

112373

Subventions

Organisme : NCI NIH HHS
ID : R35 CA197695
Pays : United States

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Willem K Smits (WK)

Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands.

Carlo Vermeulen (C)

Oncode Institute, Utrecht, the Netherlands; Hubrecht Institute-KNAW, Utrecht, the Netherlands; Center for Molecular Medicine, University Medical Center Utrecht, Utrecht, the Netherlands.

Rico Hagelaar (R)

Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands; Oncode Institute, Utrecht, the Netherlands.

Shunsuke Kimura (S)

Laboratory of Pathology, St. Jude's Children's Research Hospital, Memphis TN, USA.

Eric M Vroegindeweij (EM)

Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands.

Jessica G C A M Buijs-Gladdines (JGCAM)

Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands.

Ellen van de Geer (E)

Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands.

Marjon J A M Verstegen (MJAM)

Oncode Institute, Utrecht, the Netherlands; Hubrecht Institute-KNAW, Utrecht, the Netherlands.

Erik Splinter (E)

Cergentis BV, Utrecht, the Netherlands.

Simon V van Reijmersdal (SV)

Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands.

Arjan Buijs (A)

Department of Genetics, University Medical Center Utrecht, Utrecht, the Netherlands.

Niels Galjart (N)

Department of Cell Biology, Erasmus University Medical Center Rotterdam, Rotterdam, the Netherlands.

Winfried van Eyndhoven (W)

Diagnostics and Genomics Group, Agilent Technologies, Amstelveen, the Netherlands.

Max van Min (M)

Cergentis BV, Utrecht, the Netherlands.

Roland Kuiper (R)

Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands; Department of Genetics, University Medical Center Utrecht, Utrecht, the Netherlands.

Patrick Kemmeren (P)

Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands.

Charles G Mullighan (CG)

Laboratory of Pathology, St. Jude's Children's Research Hospital, Memphis TN, USA.

Wouter de Laat (W)

Oncode Institute, Utrecht, the Netherlands; Hubrecht Institute-KNAW, Utrecht, the Netherlands.

Jules P P Meijerink (JPP)

Princess Máxima Center for Pediatric Oncology, Utrecht, the Netherlands. Electronic address: jules.meijerink@acerta-pharma.com.

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Classifications MeSH