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© The Rockefeller University Press, 0021-9525/1999//1395 $5.00
The Journal of Cell Biology, Volume 145, Number 7, , 1999 1395-1406

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Chromosomal Influence on Meiotic Spindle Assembly: Abnormal Meiosis I in Female Mlh1 Mutant Mice



Linda M. Woods*, Craig A. Hodges*, Esther Baart{ddagger}, Sean M. Baker§, Michael Liskay||, and Patricia A. Hunt*

* Department of Genetics and Center for Human Genetics, Case Western Reserve University and University Hospitals of Cleveland, Cleveland, Ohio 44106; {ddagger} Department of Animal Breeding, Wageningen Agricultural University, Wageningen 6709 PG, The Netherlands; § Division of Nutritional Sciences and Toxicology, University of California, Berkeley, Berkeley, California 94720; and || Department of Molecular and Medical Genetics, Oregon Health Sciences University, Portland, Oregon 97201

In mouse oocytes, the first meiotic spindle is formed through the action of multiple microtubule organizing centers rather than a pair of centrosomes. Although the chromosomes are thought to play a major role in organizing the meiotic spindle, it remains unclear how a stable bipolar spindle is established. We have studied the formation of the first meiotic spindle in murine oocytes from mice homozygous for a targeted disruption of the DNA mismatch repair gene, Mlh1. In the absence of the MLH1 protein meiotic recombination is dramatically reduced and, as a result, the vast majority of chromosomes are present as unpaired univalents at the first meiotic division. The orientation of these univalent chromosomes at prometaphase suggests that they are unable to establish stable bipolar spindle attachments, presumably due to the inability to differentiate functional kinetochore domains on individual sister chromatids. In the presence of this aberrant chromosome behavior a stable first meiotic spindle is not formed, the spindle poles continue to elongate, and the vast majority of cells never initiate anaphase. These results suggest that, in female meiotic systems in which spindle formation is based on the action of multiple microtubule organizing centers, the chromosomes not only promote microtubule polymerization and organization but their attachment to opposite spindle poles acts to stabilize the forming spindle poles.

Key Words: cell cycle • meiosis • mismatch repair • oocyte • spindle formation

Abbreviations used in this paper: MI, first meiotic division; MII, second meiotic division.


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