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After fertilization of the transcriptionally silent oocyte, expression from both parental chromosomes is launched through zygotic genome activation (ZGA), occurring in the mouse at the 2‐cell (2C) stage. Among the first elements to be transcribed are the  Dux  gene, the product of which induces a wide array of ZGA genes, and a subset of evolutionary recent LINE‐1 retrotransposons that regulate chromatin accessibility in the early embryo. The maternally inherited factors that activate  Dux  and LINE‐1 transcription have so far remained unknown. Mouse embryonic stem cells (mESCs) recapitulate some aspects of ZGA in culture, owing to their ability to cycle through a 2C‐like stage when  Dux , its target genes, and LINE‐1 integrants are expressed. Here, we identify the paralog proteins DPPA2 and DPPA4 as necessary for the activation of  Dux  and LINE‐1 expression in mESCs. Since their encoding RNAs are maternally transmitted to the zygote, it is likely that these factors are important upstream mediators of murine ZGA.

DPPA2 and DPPA4 are necessary to establish a 2C‐like state in mouse embryonic stem cells