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Background  In mammals, X chromosome genes are present in one copy in males and two in females. To balance the dosage of X-linked gene expression between the sexes, one of the X chromosomes in females is silenced. X inactivation is initiated by upregulation of the lncRNA (long non-coding RNA)  Xist  and recruitment of specific chromatin modifiers. The inactivated X chromosome becomes heterochromatic and visits a specific nuclear compartment adjacent to the nucleolus.    Results  Here, we show a novel role for the lncRNA  Firre  in anchoring the inactive mouse X chromosome and preserving one of its main epigenetic features, H3K27me3. Similar to  Dxz4 ,  Firre  is X-linked and expressed from a macrosatellite repeat locus associated with a cluster of CTCF and cohesin binding sites, and is preferentially located adjacent to the nucleolus. CTCF binding present initially in both male and female mouse embryonic stem cells is lost from the active X during development. Knockdown of  Firre  disrupts perinucleolar targeting and H3K27me3 levels in mouse fibroblasts, demonstrating a role in maintenance of an important epigenetic feature of the inactive X chromosome. No X-linked gene reactivation is seen after  Firre  knockdown; however, a compensatory increase in the expression of chromatin modifier genes implicated in X silencing is observed. Further experiments in female embryonic stem cells suggest that  Firre  does not play a role in X inactivation onset.    Conclusions  The X-linked lncRNA  Firre  helps to position the inactive X chromosome near the nucleolus and to preserve one of its main epigenetic features.    Electronic supplementary material  The online version of this article (doi:10.1186/s13059-015-0618-0) contains supplementary material, which is available to authorized users.

The lncRNA Firre anchors the inactive X chromosome to the nucleolus by binding CTCF and maintains H3K27me3 methylation