Genome-wide profiling of p53-regulated enhancer RNAs uncovers a subset of enhancers controlled by a lncRNA

Léveillé, Nicolas; Melo, Carlos A.; Rooijers, Koos; Díaz-Lagares, Angel; Melo, Sonia A.; Korkmaz, Gozde; Lopes, Rui; Moqadam, Farhad Akbari; Maia, Ana R.; Wijchers, Patrick J.; Geeven, Geert; den Boer, Monique L.; Kalluri, Raghu; de Laat, Wouter; Esteller, Manel; Agami, Reuven

doi:10.1038/ncomms7520

Cited by 183Cancer-related molecular mechanisms researchGenomics and Chromatin DynamicsCancer-related Molecular Pathways

Genome-wide profiling of p53-regulated enhancer RNAs uncovers a subset of enhancers controlled by a lncRNA

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Léveillé, Nicolas, Melo, Carlos A., Rooijers, Koos, Díaz-Lagares, Angel, Melo, Sonia A., Korkmaz, Gozde, Lopes, Rui, Moqadam, Farhad Akbari +8 more·2015·Nature Communications

DOI 10.1038/ncomms7520PMC PMC4389233

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Abstract

p53 binds enhancers to regulate key target genes. Here, we globally mapped p53-regulated enhancers by looking at enhancer RNA (eRNA) production. Intriguingly, while many p53-induced enhancers contained p53-binding sites, most did not. As long non-coding RNAs (lncRNAs) are prominent regulators of chromatin dynamics, we hypothesized that p53-induced lncRNAs contribute to the activation of enhancers by p53. Among p53-induced lncRNAs, we identified LED and demonstrate that its suppression attenuates p53 function. Chromatin-binding and eRNA expression analyses show that LED associates with and activates strong enhancers. One prominent target of LED was located at an enhancer region within CDKN1A gene, a potent p53-responsive cell cycle inhibitor. LED knockdown reduces CDKN1A enhancer induction and activity, and cell cycle arrest following p53 activation. Finally, promoter-associated hypermethylation analysis shows silencing of LED in human tumours. Thus, our study identifies a new layer of complexity in the p53 pathway and suggests its dysregulation in cancer.

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Long-distance transactivation is mediated by the binding of p53 to enhancers.
“long-distance transactivation is reportedly mediated by the binding of p53 to enhancers.30, 65, 66”
From Census and evaluation of p53 target genes (2017) · cites this paper as [66]

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Authors: Léveillé, N., Melo, C. A., Rooijers, K., Díaz-Lagares, A., Melo, S. A., Korkmaz, G., Lopes, R., Moqadam, F. A., Maia, A. R., Wijchers, P. J., Geeven, G., den Boer, M. L., Kalluri, R., de Laat, W., Esteller, M., & Agami, R.
Affiliations: The Netherlands Cancer Institute (NL)
Erasmus MC (NL)
University Medical Center Utrecht (NL)
The University of Texas MD Anderson Cancer Center (US)
Institució Catalana de Recerca i Estudis Avançats (ES)
Corresponding author: Agami, Reuven
ORCID: Léveillé, Nicolas
Melo, Carlos A.
Rooijers, Koos
Lopes, Rui
Maia, Ana R.
Geeven, Geert
Kalluri, Raghu
Esteller, Manel
Agami, Reuven
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2015-03-27
Volume: 6
Issue: 1
Pages: 6520-6520
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/ncomms7520
PMC: PMC4389233
OpenAlex: W2024265215
Cited by: 183
References: 43
Citations by year: 2026: 5 · 2025: 7 · 2024: 3 · 2023: 8 · 2022: 25 · 2021: 16 · 2020: 20 · 2019: 15 · 2018: 29 · 2017: 17 · 2016: 26 · 2015: 11
FWCI: 9.15
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Nature Communications (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (publishedVersion, cc-by)
Pure Amsterdam UMC (publishedVersion, cc-by)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion, other-oa)
KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, other-oa)
RECERCAT (Consorci de Serveis Universitaris de Catalunya) (publishedVersion, other-oa)
Estudo Geral (Universidad de Coimbra) (submittedVersion, cc-by)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
RePEc: Research Papers in Economics (submittedVersion)
Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
RePub (Erasmus University Rotterdam) (submittedVersion)
Funders: Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Ministerio de Economía y Competitividad
Instituto de Salud Carlos III (CD12/00738)
FP7 Ideas: European Research Council (268626)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Keywords: p53, enhancer RNA, long non-coding RNA, enhancer activation, p21, cell cycle arrest, promoter hypermethylation, cancer, chromatin regulation
MeSH terms: Adenocarcinoma, Breast Neoplasms, Enhancer Elements, Genetic, Female, Humans, Promoter Regions, Genetic, Gene Expression Regulation, Neoplastic, Tumor Suppressor Protein p53, In Situ Hybridization, Fluorescence, Sequence Analysis, RNA, DNA Methylation, Chromatin Immunoprecipitation, Cyclin-Dependent Kinase Inhibitor p21, Real-Time Polymerase Chain Reaction, MCF-7 Cells, RNA, Long Noncoding

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Genome-wide profiling of p53-regulated enhancer RNAs uncovers a subset of enhancers controlled by a lncRNA

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