Piwi Proteins and piRNAs in Mammalian Oocytes and Early Embryos

Germ cells of most animals critically depend on piRNAs and Piwi proteins. Surprisingly, piRNAs in mouse oocytes are relatively rare and dispensable. We present compelling evidence for strong Piwi and piRNA expression in oocytes of other mammals. Human fetal oocytes express PIWIL2 and transposon-enriched piRNAs. Oocytes in adult human ovary express PIWIL1 and PIWIL2, whereas those in bovine ovary only express PIWIL1. In human, macaque, and bovine ovaries, we find piRNAs that resemble testis-borne pachytene piRNAs. Isolated bovine follicular oocytes were shown to contain abundant, relatively short piRNAs that preferentially target transposable elements. Using label-free quantitative proteome analysis, we show that these maturing oocytes strongly and specifically express the PIWIL3 protein, alongside other, known piRNA-pathway components. A piRNA pool is still present in early bovine embryos, revealing a potential impact of piRNAs on mammalian embryogenesis. Our results reveal that there are highly dynamic piRNA pathways in mammalian oocytes and early embryos. [Display omitted] •PIWIL1, PIWIL2, and PIWIL3 are dynamically expressed during mammalian oogenesis•Human, bovine, and macaque ovaries express piRNAs that resemble piRNAs from testis•Maturing oocytes express PIWIL3 and non-methylated, transposon-targeting piRNAs•Predominant adenylation of piRNAs is observed in maturing oocytes and early embryos Piwi proteins and piRNAs are essential for animal germ cells, yet their presence in mammalian oocytes has remained enigmatic. Using bovine, macaque, and human material, Roovers et al. demonstrate dynamic expression of these molecules during oogenesis. Notably, PIWIL3 is found specifically in oocytes, together with a non-methylated, adenylated piRNA population.