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A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis

Nature Cell Biology volume 12, pages 894–901 (2010)Cite this article

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Abstract

Although assembly of acentrosomal meiotic spindles has been extensively studied1, little is known about the segregation of chromosomes on these spindles. Here, we show in Caenorhabditis elegans oocytes that the kinetochore protein, KNL-1, directs assembly of meiotic kinetochores that orient chromosomes. However, in contrast to mitosis, chromosome separation during meiotic anaphase is kinetochore-independent. Before anaphase, meiotic kinetochores and spindle poles disassemble along with the microtubules on the poleward side of chromosomes. During anaphase, microtubules then form between the separating chromosomes. Functional analysis implicated a set of proteins that localize to a ring-shaped domain between kinetochores during pre-anaphase spindle assembly and anaphase separation. These proteins are localized by the chromosomal passenger complex, which regulates the loss of meiotic chromosome cohesion2,3,4. Thus, meiotic segregation in C. elegans is a two-stage process, where kinetochores orient chromosomes, but are then dispensable for their separation. We suggest that separation is controlled by a meiosis-specific chromosomal domain to coordinate cohesin removal and chromosome segregation.

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Figure 1: Cup-shaped meiotic kinetochores are assembled by a KNL-1-dependent mechanism and are required for accurate meiotic chromosome segregation.
Figure 2: KNL-1 is required to orient chromosomes on the acentrosomal meiotic spindle before anaphase onset.
Figure 3: Anaphase chromosome separation on acentrosomal meiotic spindles occurs by a kinetochore-independent mechanism.
Figure 4: Proteins that localize to a ring-shaped domain between the kinetochores form linker structures during anaphase.
Figure 5: Ring domain proteins contribute to both pre-anaphase spindle assembly and anaphase separation.

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Acknowledgements

We are grateful to J. Canman and R. Green for critical reading of the manuscript. This work was supported by an EMBO long-term postdoctoral fellowship to J.D., grants from Human Frontiers Science Program (RGY0084) and the NIH (GM074215) to A.D., and funding from the Ludwig Institute for Cancer Research to A.D. and K.O.

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  1. Department of Cellular & Molecular Medicine, Ludwig Institute for Cancer Research, University of California, San Diego, CA 92093-0653, La Jolla, USA

    Julien Dumont, Karen Oegema & Arshad Desai

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Contributions

All experimental data were generated by J.D., who also had primary responsibility for experimental design and data analysis. A.D. and K.O. contributed to experimental design and data analysis. J.D., A.D. and K.O. wrote the manuscript.

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Correspondence to Arshad Desai.

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The authors declare no competing financial interests.

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Dumont, J., Oegema, K. & Desai, A. A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat Cell Biol 12, 894–901 (2010). https://doi.org/10.1038/ncb2093

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