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The resurrection of pseudogenes during evolution produced lncRNAs with new biological function. Here we show that pseudogene-evolution created an  Oct4  pseudogene lncRNA that is able to direct epigenetic silencing of the parental  Oct4  gene via a 2-step, lncRNA dependent mechanism. The murine  Oct4  pseudogene 4 ( mOct4P4 ) lncRNA recruits the RNA binding protein FUS to allow the binding of the SUV39H1 HMTase to a defined  mOct4P4  lncRNA sequence element. The  mOct4P4 -FUS-SUV39H1 silencing complex holds target site specificity for the parental  Oct4  promoter and interference with individual components results in loss of  Oct4  silencing. SUV39H1 and FUS do not bind parental  Oct4  mRNA, confirming the acquisition of a new biological function by the  mOct4P4  lncRNA. Importantly, all features of  mOct4P4  function are recapitulated by the human  hOCT4P3  pseudogene lncRNA, indicating evolutionary conservation. Our data highlight the biological relevance of rapidly evolving lncRNAs that infiltrate into central epigenetic regulatory circuits in vertebrate cells.

FUS-dependent loading of SUV39H1 to OCT4 pseudogene-lncRNA programs a silencing complex with OCT4 promoter specificity