Trans- and cis-acting effects of Firre on epigenetic features of the inactive X chromosome

He Fang, Giancarlo Bonora, Jordan P. Lewandowski, Jitendra Thakur, Galina N. Filippova, Steven Henikoff, Jay Shendure, Zhijun Duan, John L. Rinn, Xinxian Deng (), William S. Noble () and Christine M. Disteche ()
Additional contact information
He Fang: University of Washington
Giancarlo Bonora: University of Washington
Jordan P. Lewandowski: Harvard University
Jitendra Thakur: Fred Hutchinson Cancer Research Center
Galina N. Filippova: University of Washington
Steven Henikoff: Fred Hutchinson Cancer Research Center
Jay Shendure: University of Washington
Zhijun Duan: University of Washington
John L. Rinn: University of Colorado at Boulder
Xinxian Deng: University of Washington
William S. Noble: University of Washington
Christine M. Disteche: University of Washington

Nature Communications, 2020, vol. 11, issue 1, 1-17

Abstract: Abstract Firre encodes a lncRNA involved in nuclear organization. Here, we show that Firre RNA expressed from the active X chromosome maintains histone H3K27me3 enrichment on the inactive X chromosome (Xi) in somatic cells. This trans-acting effect involves SUZ12, reflecting interactions between Firre RNA and components of the Polycomb repressive complexes. Without Firre RNA, H3K27me3 decreases on the Xi and the Xi-perinucleolar location is disrupted, possibly due to decreased CTCF binding on the Xi. We also observe widespread gene dysregulation, but not on the Xi. These effects are measurably rescued by ectopic expression of mouse or human Firre/FIRRE transgenes, supporting conserved trans-acting roles. We also find that the compact 3D structure of the Xi partly depends on the Firre locus and its RNA. In common lymphoid progenitors and T-cells Firre exerts a cis-acting effect on maintenance of H3K27me3 in a 26 Mb region around the locus, demonstrating cell type-specific trans- and cis-acting roles of this lncRNA.

Date: 2020
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DOI: 10.1038/s41467-020-19879-3

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