Production of functional oocytes requires maternally expressed PIWI genes and piRNAs in golden hamsters

Abstract

Many animals have a conserved adaptive genome defense system known as the Piwi-interacting RNA (piRNA) pathway which is essential for germ cell development and function. Disruption of individual mouse Piwi genes results in male but not female sterility, leading to the assumption that PIWI genes play little or no role in mammalian oocytes. Here, we report generation of PIWI-defective golden hamsters, which reveals defects in the production of functional oocytes. The mechanisms involved vary among the hamster PIWI genes; lack of PIWIL1 has a major impact on gene expression, including hamster-specific young transposon de-silencing, whereas PIWIL3 deficiency has little impact on gene expression in oocytes, although DNA methylation was found to be reduced to some extent in PIWIL3-defecient oocytes. Our findings serve as the foundation for developing useful models to study the piRNA pathway in mammalian oocytes, including humans, which is not possible with mice.