Overexpression of cyclin A1 promotes meiotic resumption but induces premature chromosome separation in mouse oocyte

J Cell Physiol. 2020 Oct;235(10):7136-7145. doi: 10.1002/jcp.29612. Epub 2020 Feb 6.

Abstract

Mammalian cyclin A1 is prominently expressed in testis and essential for meiosis in the male mouse, however, it shows weak expression in ovary, especially during oocyte maturation. To understand why cyclin A1 behaves in this way in the oocyte, we investigated the effect of cyclin A1 overexpression on mouse oocyte meiotic maturation. Our results revealed that cyclin A1 overexpression triggered meiotic resumption even in the presence of germinal vesicle breakdown inhibitor, milrinone. Nevertheless, the cyclin A1-overexpressed oocytes failed to extrude the first polar body but were completely arrested at metaphase I. Consequently, cyclin A1 overexpression destroyed the spindle morphology and chromosome alignment by inducing premature separation of chromosomes and sister chromatids. Therefore, cyclin A1 overexpression will prevent oocyte maturation although it can promote meiotic resumption. All these results show that decreased expression of cyclin A1 in oocytes may have an evolutional significance to keep long-lasting prophase arrest and orderly chromosome separation during oocyte meiotic maturation.

Keywords: chromosome separation; cyclin A1; meiosis; oocyte.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chromosome Segregation / drug effects
  • Chromosome Segregation / genetics*
  • Chromosome Segregation / physiology*
  • Cyclin A1 / genetics*
  • Cyclin A1 / metabolism*
  • Female
  • Meiosis / drug effects
  • Meiosis / genetics*
  • Meiosis / physiology*
  • Mice
  • Mice, Inbred ICR
  • Milrinone / pharmacology
  • Oocytes / cytology
  • Oocytes / drug effects
  • Oocytes / metabolism*
  • Oogenesis / drug effects
  • Oogenesis / genetics
  • Oogenesis / physiology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Separase / metabolism
  • Up-Regulation

Substances

  • Ccna1 protein, mouse
  • Cyclin A1
  • RNA, Messenger
  • Separase
  • Milrinone