Disruption of Zar1 leads to arrested oogenesis by regulating polyadenylation via Cpeb1 in tilapia (Oreochromis niloticus)

Int J Biol Macromol. 2024 Mar;260(Pt 2):129632. doi: 10.1016/j.ijbiomac.2024.129632. Epub 2024 Jan 20.

Abstract

Oogenesis is a complex process regulated by precise coordination of multiple factors, including maternal genes. Zygote arrest 1 (zar1) has been identified as an ovary-specific maternal gene that is vital for oocyte-to-embryo transition and oogenesis in mouse and zebrafish. However, its function in other species remains to be elucidated. In the present study, zar1 was identified with conserved C-terminal zinc finger domains in Nile tilapia. zar1 was highly expressed in the ovary and specifically expressed in phase I and II oocytes. Disruption of zar1 led to the failed transition from oogonia to phase I oocytes, with somatic cell apoptosis. Down-regulation and failed polyadenylation of figla, gdf9, bmp15 and wee2 mRNAs were observed in the ovaries of zar1-/- fish. Cpeb1, a gene essential for polyadenylation that interacts with Zar1, was down-regulated in zar1-/- fish. Moreover, decreased levels of serum estrogen and increased levels of androgen were observed in zar1-/- fish. Taken together, zar1 seems to be essential for tilapia oogenesis by regulating polyadenylation and estrogen synthesis. Our study shows that Zar1 has different molecular functions during gonadal development by the similar signaling pathway in different species.

Keywords: Oogenesis; Polyadenylation; Zar1.

MeSH terms

  • Animals
  • Cichlids* / genetics
  • Cichlids* / metabolism
  • Egg Proteins / metabolism
  • Estrogens
  • Female
  • Mice
  • Oogenesis / genetics
  • Polyadenylation
  • Tilapia* / genetics
  • Tilapia* / metabolism
  • Transcription Factors / genetics
  • Zebrafish / metabolism
  • mRNA Cleavage and Polyadenylation Factors / genetics

Substances

  • Egg Proteins
  • Estrogens
  • Zar1 protein, mouse
  • Cpeb1 protein, mouse
  • Transcription Factors
  • mRNA Cleavage and Polyadenylation Factors