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Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis

Nature Cell Biology volume 11, pages 839–844 (2009)Cite this article

Abstract

Although centrosomes serve to organize microtubules in most cell types, oocyte spindles form and mediate meiotic chromosome segregation in their absence. Here, we used high-resolution imaging of both bipolar and experimentally generated monopolar spindles in Caenorhabditis elegans to reveal a surprising organization of microtubules and chromosomes within acentrosomal structures. We found that homologous chromosome pairs (bivalents) are surrounded by microtubule bundles running along their sides, whereas microtubule density is extremely low at chromosome ends despite a high concentration of kinetochore proteins at those regions. Furthermore, we found that the chromokinesin KLP-19 (kinesin-like protein 19) is targeted to a ring around the centre of each bivalent and provides a polar ejection force that is required for congression. Together, these observations create a new picture of chromosome–microtubule association in acentrosomal spindles and reveal a mechanism by which metaphase alignment can be achieved using this organization. Specifically, we propose that ensheathment by lateral microtubule bundles places spatial constraints on the chromosomes, thereby promoting biorientation, and that localized motors mediate movement along these bundles, thereby promoting alignment.

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Figure 1: KLP-18 and MESP-1 are required for the bipolarity of acentrosomal oocyte meiotic spindles.
Figure 2: Chromosomes are ensheathed by lateral microtubule bundles in acentrosomal spindles.
Figure 3: Localization of the chromokinesin KLP-19 to a ring at the mid-bivalent is regulated by the chromosome passenger complex.
Figure 4: KLP-19 provides a polar ejection force to position meiotic chromosomes.
Figure 5: Model of chromosome organization and congression on acentrosomal spindles.

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Acknowledgements

We thank members of the Villeneuve laboratory for support and discussions, R. Heald, V. Indjeian and M. Schvarzstein for comments on the manuscript, J. Monen, P. Maddox and members of the Desai and Oegema laboratories for technical advice, J. Dumont and A. Desai for sharing data before publication, and J. Audhya, B. Bowerman, A. Desai, B. Meyer, J. Powers and J. Schumacher for reagents. Additionally, some strains used in this work were provided by the Caenorhabditis Genetics Center, which is funded by the NIH National Center for Research Resources (NCRR). This work was supported by an NIH grant (RO1 GM53804) to A.M.V.; S.M.W. was a Damon Runyon Fellow supported by the Damon Runyon Cancer Research Foundation (DRG-#1827-04) and is currently a Special Fellow of the Leukemia and Lymphoma Society.

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Authors and Affiliations

  1. Department of Developmental Biology, 279 Campus Drive, Stanford, 94305, CA, USA

    Sarah M. Wignall & Anne M. Villeneuve

  2. Department of Genetics, Stanford University School of Medicine, 279 Campus Drive, Stanford, 94305, CA, USA

    Sarah M. Wignall & Anne M. Villeneuve

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All experimental data and figures were generated by S.M.W., who also had primary responsibility for experimental design, data analysis and manuscript writing. A.M.V. contributed to experimental design, data analysis and manuscript writing.

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Correspondence to Sarah M. Wignall or Anne M. Villeneuve.

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Wignall, S., Villeneuve, A. Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat Cell Biol 11, 839–844 (2009). https://doi.org/10.1038/ncb1891

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