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Metaphase I Arrest in LT/Sv Mouse Oocytes Involves the Spindle Assembly Checkpoint¹

Department of Embryology,⁷ Institute of Zoology, Faculty of Biology, University of Warsaw, 02-096 Warsaw, Poland Department of Developmental Biology,⁸ Max Planck Institute of Immunobiology, 79-108 Freiburg, Germany Institute of Genetics & Development,⁹ Centre National de la Recherche Scientifique-Unité Mixte de Recherche 606, "Mitosis & Meiosis" Group, IFR 140 GFAS, University of Rennes 1, 35043 Rennes, France Department of Genetics & Evolution,¹⁰ Institute of Zoology, Jagiellonian University, 30-060 Krakow, Poland Department of Cytology,¹¹ Institute of Zoology, Faculty of Biology, University of Warsaw, 02-096 Warsaw, Poland

ABSTRACT

During meiotic maturation, the majority of oocytes from LT/Sv mice arrest at metaphase I. However, anaphase may be induced through parthenogenetic activation. If this happens within the ovary, it often results in the development of ovarian teratomas. Here, we show that the induction of first meiotic anaphase in LT/Sv oocytes results in incorrect chromosome segregation. In search of the molecular basis of this complex phenotype, we analyzed the localization/destruction of cohesins, as well as the function of the components of the spindle assembly checkpoint (SAC). Both localization and removal of meiotic cohesin REC8 from chromosomes are unperturbed. In contrast, there is prolonged localization of SAC proteins BUB1 and MAD2L1 (MAD2) at the metaphase I kinetochores in mutant oocytes compared with the wild-type. Interfering with BUB1 function through expression of a dominant-negative mutant protein resulted in the increase of the number of LT/Sv oocytes completing the first meiosis, which indicates SAC involvement in metaphase I arrest. These data show for the first time that there is a direct link between the SAC function and the heritable meiotic incompetence of a mammalian oocyte.

BUB1, gamete biology, gametogenesis, LT/Sv, MAD2L1, meiosis, metaphase I, mouse, oocyte, oocyte development, REC8, spindle assembly checkpoint

¹Supported by a grant from Association pour la Recherche sur le Cancer (4900) and Ligue Contre le Cancer (Comité d'Ille-et-Vilaine et de la Vandée) to J.Z.K. M.A.C. was a recipient of a fellowship from the L'Oreal for Women and Science Foundation.

Correspondence: ²Correspondance: Zbigniew Polanski, Department of Genetics & Evolution, Institute of Zoology, Jagiellonian University, Ingardena 6, 30–060 Cracow, Poland. FAX: 48 12 6343716; e-mail: pola{at}iz.uj.edu.pl

Correspondence: ³Maria A. Ciemerych, Department of Cytology, Institute of Zoology, Faculty of Biology, University of Warsaw, Ilji Miecznikowa 1, 02–096 Warsaw, Poland. FAX: 48 22 55 41 210; e-mail: ciemerych{at}biol.uw.edu.pl

⁴Current address: Laboratory of Cell Biology, International Institute of Molecular and Cell Biology, 02-109 Warsaw, Poland.

⁵Current address: ProQinase GmbH, 79-106 Freiburg, Germany.

⁶Current address: Hematology and Oncology Department, University of Freiburg Medical Center, 79-095 Freiburg, Germany.

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				Z. Maciejewska, Z. Polanski, K. Kisiel, J. Z Kubiak, and M. A Ciemerych Spindle assembly checkpoint-related failure perturbs early embryonic divisions and reduces reproductive performance of LT/Sv mice Reproduction, June 1, 2009; 137(6): 931 - 942. [Abstract] [Full Text] [PDF]