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The  Xist  lncRNA mediates X chromosome inactivation (XCI). Here we show that Spen, an  Xist -binding repressor protein essential for XCI , binds to ancient retroviral RNA, performing a surveillance role to recruit chromatin silencing machinery to these parasitic loci. Spen loss activates a subset of endogenous retroviral (ERV) elements in mouse embryonic stem cells, with gain of chromatin accessibility, active histone modifications, and  ERV  RNA transcription. Spen binds directly to  ERV  RNAs that show structural similarity to the A-repeat of  Xist , a region critical for  Xist -mediated gene silencing.  ERV  RNA and  Xist  A-repeat bind the RRM domains of Spen in a competitive manner. Insertion of an ERV into an A-repeat deficient Xist rescues binding of  Xist  RNA to Spen and results in strictly local gene silencing in  cis . These results suggest that  Xist  may coopt transposable element RNA-protein interactions to repurpose powerful antiviral chromatin silencing machinery for sex chromosome dosage compensation.

Spen links RNA-mediated endogenous retrovirus silencing and X chromosome inactivation