Dynamic protein expression in golden hamster oocytes and embryos reveals extensive post-translational regulation of PIWIL1 during the oocyte-to-embryo transition

Abstract The golden hamster, renowned for its representative PIWI-piRNA pathway profile among mammals, has emerged as a promising animal model for investigating female mammalian fertility. Prior research uncovered that the disruption of Piwil1 leads to complete infertility of female golden hamsters, with embryos derived from homozygous knockout (Piwil1−/−) females mated with wild-type males arresting at the two-cell stage. However, the underlying deep mechanisms remain unexplored. In the current study, we utilized highly sensitive single-cell mass spectrometry to generate proteome data of five developmental stages from oocytes to embryos in both wild-type (WT) and Piwil1-deficient golden hamsters, thus profiling the dynamic proteome landscape during oocyte-to-embryo transition (OET). Integrative analyses highlighted the temporal dynamics and complexity of hamster oocytes and embryos. Notably, we observed that classical maternal proteins in hamsters exhibit a more intricate pattern compared to mice, while PIWIL1 deficiency led to aberrant expression of proteins with diverse functions in oocytes and early embryos. Analysis of Multi-omics data indicated that PIWIL1 primarily regulates differentially expressed proteins at the post-translational level during OET. Specifically, the stability of TDRD1, essential for embryogenesis and gametogenesis, is modulated by PIWIL1, and could be its downstream target. Our study provides an extensive database that offers valuable insights into mammalian oocyte and early embryo development, and represents an invaluable resource for further mechanistic studies to deepen the understanding of developmental regulation.