MEIOSIS-SPECIFIC CELL-CYCLE REGULATION IN MATURING XENOPUS OOCYTES

Meiotic cell cycles differ from mitotic cell cycles in that the former lack S-phase in the interphase between meiosis I and meiosis II, To obtain clues for mechanisms involved in the cell cycle regulation unique to meiosis, we have examined changes in chromosomal morphology and H1 kinase activity during a meiotic period from metaphase I (MI) to metaphase II (MII) in Xenopus oocytes, Using populations of oocytes that underwent germinal vesicle breakdown (GVBD) within a 10 minute interval, we found that the kinase activity declined gradually during the 60 minute period after GVBD and then increased steadily during the following 80 minute interval, showing remarkable differences from the rapid drop and biphasic increase of the kinase activity in intermitotic periods (Solomon et al, (1990) Cell 63, 1013-1024; Dasso and Newport (1990) Cell 61, 811-823), We also found that the exit from MI lagged, by more than 30 minutes, behind the time of lowest H1 kinase activity, whereas the two events took place concomitantly at the end of meiosis II and mitosis, Consequently, the H1 kinase activity was already increasing during the first meiotic division, When H1 kinase activation at MII was delayed by a transient inhibition of protein synthesis after GVBD, oocytes were able to support formation of interphase nuclei and DNA replication between the first meiotic division and the MII arrest, indicating that the cell cycle entered S-phase between meiosis I and meiosis II, These results strongly suggest that the machinery required for entering S-phase has been established in maturing oocytes by the end of meiosis I, The lack of S-phase in oocyte meiotic interphase, therefore, should be ascribed to cell cycle regulation that enables the transition from meiosis I to meiosis TI without S-phase, The asynchrony between the inactivation of H1 kinase activity and the completion of meiosis I may be involved in the regulation of this unique feature of the meiotic cell cycle.