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© The Rockefeller University Press, 0021-9525/1997//1611 $5.00
The Journal of Cell Biology, Volume 139, Number 7, , 1997 1611-1619

Article

Lack of Checkpoint Control at the Metaphase/Anaphase Transition: A Mechanism of Meiotic Nondisjunction in Mammalian Females



Renée LeMaire-Adkins, Kristi Radke, and Patricia A. Hunt

Department of Genetics and Center for Human Genetics, Case Western Reserve University School of Medicine and University Hospitals of Cleveland, Cleveland, Ohio 44106-4955

A checkpoint mechanism operates at the metaphase/anaphase transition to ensure that a bipolar spindle is formed and that all the chromosomes are aligned at the spindle equator before anaphase is initiated. Since mistakes in the segregation of chromosomes during meiosis have particularly disastrous consequences, it seems likely that the meiotic cell division would be characterized by a stringent metaphase/ anaphase checkpoint. To determine if the presence of an unaligned chromosome activates the checkpoint and delays anaphase onset during mammalian female meiosis, we investigated meiotic cell cycle progression in murine oocytes from XO females and control siblings. Despite the fact that the X chromosome failed to align at metaphase in a significant proportion of cells, we were unable to detect a delay in anaphase onset. Based on studies of cell cycle kinetics, the behavior and segregation of the X chromosome, and the aberrant behavior and segregation of autosomal chromosomes in oocytes from XO females, we conclude that mammalian female meiosis lacks chromosome-mediated checkpoint control. The lack of this control mechanism provides a biological explanation for the high incidence of meiotic nondisjunction in the human female. Furthermore, since available evidence suggests that a stringent checkpoint mechanism operates during male meiosis, the lack of a comparable checkpoint in females provides a reason for the difference in the error rate between oogenesis and spermatogenesis.

Abbreviations used in this paper: FISH, fluorescence in situ hybridization; NGS, normal goat serum.

The work was supported by grants R01 HD31866 from the National Institutes of Health and FY96-0621 from the March of Dimes to P.A. Hunt.

Address all correspondence to Patricia A. Hunt, Department of Genetics, School of Medicine, Case Western Reserve University, 10900 Euclid Ave., Cleveland, OH 44106-4955. Tel.: (216) 368-3458. Fax: (216) 368-3432. E-mail: pah13{at}po.cwru.edu


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