The transcription factor GLI1 cooperates with the chromatin remodeler SMARCA2 to regulate chromatin accessibility at distal DNA regulatory elements.

ATAC-seq GLI family zinc finger 1 (GLI1) SWI/SNF related actin dependent regulator of chromatin cancer cancer cells chromatin chromatin remodeling enhancer epigenetic regulation gene transcription matrix associated member 2 (SMARCA2) subfamily A transcription enhancer transcriptomics

Journal

The Journal of biological chemistry
ISSN: 1083-351X
Titre abrégé: J Biol Chem
Pays: United States
ID NLM: 2985121R

Informations de publication

Date de publication:
26 06 2020
Historique:
received: 01 03 2020
revised: 04 05 2020
pubmed: 8 5 2020
medline: 14 1 2021
entrez: 8 5 2020
Statut: ppublish

Résumé

The transcription factor GLI1 (GLI family zinc finger 1) plays a key role in the development and progression of multiple malignancies. To date, regulation of transcriptional activity at target gene promoters is the only molecular event known to underlie the oncogenic function of GLI1. Here, we provide evidence that GLI1 controls chromatin accessibility at distal regulatory regions by modulating the recruitment of SMARCA2 (SWI/SNF-related, matrix-associated, actin-dependent regulator of chromatin, subfamily A, member 2) to these elements. We demonstrate that SMARCA2 endogenously interacts with GLI1 and enhances its transcriptional activity. Mapping experiments indicated that the C-terminal transcriptional activation domain of GLI1 and SMARCA2's central domains, including its ATPase motif, are required for this interaction. Interestingly, similar to SMARCA2, GLI1 overexpression increased chromatin accessibility, as indicated by results of the micrococcal nuclease assay. Further, results of assays for transposase-accessible chromatin with sequencing (ATAC-seq) after GLI1 knockdown supported these findings, revealing that GLI1 regulates chromatin accessibility at several regions distal to gene promoters. Integrated RNA-seq and ATAC-seq data analyses identified a subset of differentially expressed genes located in

Identifiants

pubmed: 32376693
pii: S0021-9258(17)49368-9
doi: 10.1074/jbc.RA120.013268
pmc: PMC7324497
pii:
doi:

Substances chimiques

Chromatin 0
GLI1 protein, human 0
SMARCA2 protein, human 0
Transcription Factors 0
Zinc Finger Protein GLI1 0
DNA 9007-49-2

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

8725-8735

Subventions

Organisme : NCI NIH HHS
ID : R01 CA136526
Pays : United States

Informations de copyright

© 2020 Safgren et al.

Déclaration de conflit d'intérêts

Conflict of interest—The authors declare that they have no conflicts of interest with the contents of this article.

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Auteurs

Stephanie L Safgren (SL)

Schulze Center for Novel Therapeutics, Division of Oncology Research, Schulze Center for Novel Therapeutics, Rochester, Minnesota, USA.

Rachel L O Olson (RLO)

Schulze Center for Novel Therapeutics, Division of Oncology Research, Schulze Center for Novel Therapeutics, Rochester, Minnesota, USA.

Anne M Vrabel (AM)

Schulze Center for Novel Therapeutics, Division of Oncology Research, Schulze Center for Novel Therapeutics, Rochester, Minnesota, USA.

Luciana L Almada (LL)

Schulze Center for Novel Therapeutics, Division of Oncology Research, Schulze Center for Novel Therapeutics, Rochester, Minnesota, USA.

David L Marks (DL)

Schulze Center for Novel Therapeutics, Division of Oncology Research, Schulze Center for Novel Therapeutics, Rochester, Minnesota, USA.

Nelmary Hernandez-Alvarado (N)

Schulze Center for Novel Therapeutics, Division of Oncology Research, Schulze Center for Novel Therapeutics, Rochester, Minnesota, USA.

Alexandre Gaspar-Maia (A)

Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota, USA.

Martin E Fernandez-Zapico (ME)

Schulze Center for Novel Therapeutics, Division of Oncology Research, Schulze Center for Novel Therapeutics, Rochester, Minnesota, USA. Electronic address: fernandez-zapico.martin@mayo.edu.

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Classifications MeSH