Nuclear microRNA 9 mediates G-quadruplex formation and 3D genome organization during TGF-β-induced transcription

Julio Cordero (), Guruprasadh Swaminathan, Diana G. Rogel-Ayala, Karla Rubio, Adel Elsherbiny, Samina Mahmood, Witold Szymanski, Johannes Graumann, Thomas Braun, Stefan Günther, Gergana Dobreva and Guillermo Barreto ()
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Julio Cordero: Heidelberg University
Guruprasadh Swaminathan: UMR 7365
Diana G. Rogel-Ayala: Max-Planck-Institute for Heart and Lung Research
Karla Rubio: Max-Planck-Institute for Heart and Lung Research
Adel Elsherbiny: Heidelberg University
Samina Mahmood: Max-Planck-Institute for Heart and Lung Research
Witold Szymanski: Philipps-University Marburg
Johannes Graumann: Philipps-University Marburg
Thomas Braun: Max-Planck-Institute for Heart and Lung Research
Stefan Günther: Max-Planck-Institute for Heart and Lung Research
Gergana Dobreva: Heidelberg University
Guillermo Barreto: Max-Planck-Institute for Heart and Lung Research

Nature Communications, 2024, vol. 15, issue 1, 1-21

Abstract: Abstract The dynamics of three-dimensional (3D) genome organization are essential to transcriptional regulation. While enhancers regulate spatiotemporal gene expression, chromatin looping is a means for enhancer-promoter interactions yielding cell-type-specific gene expression. Further, non-canonical DNA secondary structures, such as G-quadruplexes (G4s), are related to increased gene expression. However, the role of G4s in promoter-distal regulatory elements, such as super-enhancers (SE), and in chromatin looping has remained elusive. Here we show that mature microRNA 9 (miR-9) is enriched at promoters and SE of genes that are inducible by transforming growth factor beta 1 (TGFB1) signaling. Moreover, we find that miR-9 is required for formation of G4s, promoter-super-enhancer looping and broad domains of the euchromatin histone mark H3K4me3 at TGFB1-responsive genes. Our study places miR-9 in the same functional context with G4s and promoter-enhancer interactions during 3D genome organization and transcriptional activation induced by TGFB1 signaling, a critical signaling pathway in cancer and fibrosis.

Date: 2024
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DOI: 10.1038/s41467-024-54740-x

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