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The chromosomal basis of meiotic acentrosomal spindle assembly and function in oocytes

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Abstract

Several aspects of meiosis are impacted by the absence of centrosomes in oocytes. Here, we review four aspects of meiosis I that are significantly affected by the absence of centrosomes in oocyte spindles. One, microtubules tend to assemble around the chromosomes. Two, the organization of these microtubules into a bipolar spindle is directed by the chromosomes. Three, chromosome bi-orientation and attachment to microtubules from the correct pole require modification of the mechanisms used in mitotic cells. Four, chromosome movement to the poles at anaphase cannot rely on polar anchoring of spindle microtubules by centrosomes. Overall, the chromosomes are more active participants during acentrosomal spindle assembly in oocytes, compared to mitotic and male meiotic divisions where centrosomes are present. The chromosomes are endowed with information that can direct the meiotic divisions and dictate their own behavior in oocytes. Processes beyond those known from mitosis appear to be required for their bi-orientation at meiosis I. As mitosis occurs without centrosomes in many systems other than oocytes, including all plants, the concepts discussed here may not be limited to oocytes. The study of meiosis in oocytes has revealed mechanisms that are operating in mitosis and will probably continue to do so.

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Acknowledgements

We thank the members of the McKim and Schindler labs for discussions and comments on the manuscript and Christian Lehner and two anonymous reviewers for suggestions leading to significant improvements in the manuscript. We apologize to the many authors whose papers we were not able to cite.

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Authors and Affiliations

  1. Waksman Institute, 190 Frelinghuysen Rd, Piscataway, NJ, 08854, USA

    Sarah J. Radford & Kim S. McKim

  2. Department of Genetics, Rutgers University, Piscataway, NJ, 08854, USA

    Alexandra L. Nguyen, Karen Schindler & Kim S. McKim

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  1. Sarah J. Radford
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  2. Alexandra L. Nguyen
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  3. Karen Schindler
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  4. Kim S. McKim
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Correspondence to Kim S. McKim.

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Writing of this review was supported by National Institutes of Health grants GM101955 to KMcK and GM112801 to KS. The authors declare that they have no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Radford, S.J., Nguyen, A.L., Schindler, K. et al. The chromosomal basis of meiotic acentrosomal spindle assembly and function in oocytes. Chromosoma 126, 351–364 (2017). https://doi.org/10.1007/s00412-016-0618-1

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