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Rewiring of the promoter-enhancer interactome and regulatory landscape in glioblastoma orchestrates gene expression underlying neurogliomal synaptic communication
Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Umeå University, Faculty of Medicine, Wallenberg Centre for Molecular Medicine at Umeå University (WCMM).
Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Umeå University, Faculty of Medicine, Wallenberg Centre for Molecular Medicine at Umeå University (WCMM).
Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Umeå University, Faculty of Medicine, Wallenberg Centre for Molecular Medicine at Umeå University (WCMM).
Umeå University, Faculty of Medicine, Umeå Centre for Molecular Medicine (UCMM). Umeå University, Faculty of Medicine, Wallenberg Centre for Molecular Medicine at Umeå University (WCMM).
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2023 (English)In: Nature Communications, E-ISSN 2041-1723, Vol. 14, no 1, article id 6446Article in journal (Refereed) Published
Abstract [en]

Chromatin organization controls transcription by modulating 3D-interactions between enhancers and promoters in the nucleus. Alterations in epigenetic states and 3D-chromatin organization result in gene expression changes contributing to cancer. Here, we map the promoter-enhancer interactome and regulatory landscape of glioblastoma, the most aggressive primary brain tumour. Our data reveals profound rewiring of promoter-enhancer interactions, chromatin accessibility and redistribution of histone marks in glioblastoma. This leads to loss of long-range regulatory interactions and overall activation of promoters, which orchestrate changes in the expression of genes associated to glutamatergic synapses, axon guidance, axonogenesis and chromatin remodelling. SMAD3 and PITX1 emerge as major transcription factors controlling genes related to synapse organization and axon guidance. Inhibition of SMAD3 and neuronal activity stimulation cooperate to promote proliferation of glioblastoma cells in co-culture with glutamatergic neurons, and in mice bearing patient-derived xenografts. Our findings provide mechanistic insight into the regulatory networks that mediate neurogliomal synaptic communication.

Place, publisher, year, edition, pages
Springer Nature, 2023. Vol. 14, no 1, article id 6446
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Biochemistry and Molecular Biology
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URN: urn:nbn:se:umu:diva-216189DOI: 10.1038/s41467-023-41919-xPubMedID: 37833281Scopus ID: 2-s2.0-85174178290OAI: oai:DiVA.org:umu-216189DiVA, id: diva2:1810780
Available from: 2023-11-09 Created: 2023-11-09 Last updated: 2023-11-09Bibliographically approved

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Chakraborty, ChaitaliNissen, ItzelVincent, Craig A.Hägglund, Anna-CarinHörnblad, AndreasRemeseiro, Silvia

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Chakraborty, ChaitaliNissen, ItzelVincent, Craig A.Hägglund, Anna-CarinHörnblad, AndreasRemeseiro, Silvia
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Umeå Centre for Molecular Medicine (UCMM)Wallenberg Centre for Molecular Medicine at Umeå University (WCMM)
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