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The First Mitosis of the Mouse Embryo Is Prolonged by Transitional Metaphase Arrest¹

Department of Embryology,⁴ Institute of Zoology, Warsaw University, 02–096 Warsaw, Poland Department of Developmental Biology,⁵ Max-Planck-Institute of Immunobiology, D-79108 Freiburg, Germany UMR 6061 CNRS,⁶ University of Rennes 1, IFR 140 GFAS, Faculty of Medicine, 35043 Rennes Cedex, France

ABSTRACT

The first mitosis of the mouse embryo is almost twice as long as the second. The mechanism of the prolongation of the first mitosis remains unknown, and it is not clear whether prometaphase or metaphase or both are prolonged. Prometaphase is characterized by dynamic chromosome movements and spindle assembly checkpoint activity, which prevents anaphase until establishment of stable kinetochore-microtubule connections. The end of prometaphase is correlated with checkpoint inactivation and disappearance of MAD2L1 (MAD2) and RSN (CLIP-170) proteins from kinetochores. Spindle assembly checkpoint operates during the early mouse mitoses, but it is not clear whether it influences their duration. Here, we determine the length of prometaphases and metaphases during the first two embryonic mitoses by time-lapse video recording of chromosomes and by immunolocalization of MAD2L1 and RSN proteins. We show that the duration of the two prometaphases does not differ and that MAD2L1 and RSN disappear from kinetochores very early during each mitosis. The first metaphase is significantly longer than the second one. Therefore, the prolongation of the first embryonic mitosis is due to a prolonged metaphase, and the spindle assembly checkpoint cannot be involved in this process. We show also that MAD2L1 staining disappears gradually from kinetochores of oocytes arrested at metaphase of the second meiotic division. This shows a striking similarity between the first embryonic mitosis and metaphase arrest in oocytes. We postulate that the first embryonic mitosis is prolonged by a transient metaphase arrest that is independent of the spindle assembly checkpoint and is similar to metaphase II arrest. The molecular mechanism of this transient arrest remains to be elucidated.

developmental biology, early development, embryo, meiosis

¹ Supported by ARC (grant 4298) to J.Z.K., Polish-French POLONIUM Program 2004 to M.A.C. and J.Z.K., and Deutsche Forschungsgemeinschaft Special Program (Schwerpunktprogramme) 1109 to Z.P.

² Correspondence: Maria A. Ciemerych, Department of Embryology, Institute of Zoology, Warsaw University, Miecznikowa 1, Room 214A, 02–132 Warsaw, Poland. FAX: 48 22 55 41 210; ciemerych{at}biol.uw.edu.pl

³ Current address: Department of Genetics and Evolution, Institute of Zoology, Jagiellonian University, Ingardena 6, 30–060 Krakow, Poland.