Mouse oocytes at different stages of maturation were fused together an
d the ensuing cell cycle events were analyzed with the objective of id
entifying checkpoints in meiosis. Fusion of maturing oocytes just unde
rgoing germinal vesicle breakdown (GVBD) induces PCC (premature chromo
some condensation) but no spindle formation in immature (GV) partner o
ocytes. On the other hand, fusion of metaphase I (MI) oocytes containi
ng spindles to GV oocytes induces both PCC and spindle formation in th
e immature partner. Thus, while molecules required for condensation ar
e present throughout metaphase, those involved in spindle formation ar
e absent in early M-phase. Oocytes cultured for 6 h-early metaphase I
(i.e., similar to 2 h before the onset of anaphase I) - and then fused
to anaphase - telophase I (A-TI) fusion partners block meiotic progre
ssion in the more advanced oocytes and induce chromatin dispersal on t
he spindle. By contrast, oocytes cultured for 8 h (late MI) before fus
ion to A-TI partners are driven into anaphase by signals from the more
advanced oocytes and thereafter advance in synchrony to telophase I.
When early (10 h) or late (12 h) metaphase II oocytes were fused to A-
TI partners the signals generated from early MII oocytes block the ana
phase to telophase I transition and induce a dispersal of A-TI chromos
omes along the spindle, On the other hand, late MII oocytes respond to
A-TI signals by exiting from the MII block and undergoing the A-TII t
ransition. Moreover, the oocytes in late MI are not arrested in this s
tage and progress without any delay through ATI to MII when fused to m
etaphase II partners. The signals from the less-developed partner forc
e the MII oocyte through A-TII to MIII. In total, these studies demons
trate that the metaphase period is divided into at least three distinc
t phases and that a checkpoint in late metaphase controls the progress
of meiosis in mammalian oocytes. (C) 1995 Academic Press, Inc.