Letter | Published:

Polar actomyosin contractility destabilizes the position of the cytokinetic furrow

Nature volume 476, pages 462466 (25 August 2011) | Download Citation

Abstract

Cytokinesis, the physical separation of daughter cells at the end of mitosis, requires precise regulation of the mechanical properties of the cell periphery1,2. Although studies of cytokinetic mechanics mostly focus on the equatorial constriction ring3, a contractile actomyosin cortex is also present at the poles of dividing cells2,4. Whether polar forces influence cytokinetic cell shape and furrow positioning remains an open question. Here we demonstrate that the polar cortex makes cytokinesis inherently unstable. We show that limited asymmetric polar contractions occur during cytokinesis, and that perturbing the polar cortex leads to cell shape oscillations, resulting in furrow displacement and aneuploidy. A theoretical model based on a competition between cortex turnover and contraction dynamics accurately accounts for the oscillations. We further propose that membrane blebs, which commonly form at the poles of dividing cells5 and whose role in cytokinesis has long been enigmatic, stabilize cell shape by acting as valves releasing cortical contractility. Our findings reveal an inherent instability in the shape of the dividing cell and unveil a novel, spindle-independent mechanism ensuring the stability of cleavage furrow positioning.

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Change history

  • Corrected online 25 August 2011

    Fig. 3e axis label was corrected.

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Acknowledgements

We thank J. S. Bois, A. G. Clark, S. W. Grill, C. P. Heisenberg, J. Howard, A. A. Hyman, J. F. Joanny, D. K. Lubensky, A. Oates, M. Piel, I. M. Tolic-Norrelykke, W. Zachariae and M. Zerial for discussions and comments on the manuscript, and J. Roensch and the Max Planck Institute of Molecular Cell Biology and Genetics Light Microscopy Facility for technical assistance. This work was supported by the Polish Ministry of Science and Higher Education and by the Max Planck Society.

Author information

Author notes

    • Jean-Yves Tinevez

    Present address: Pasteur Institute, 75724 Paris, France.

    • Jakub Sedzinski
    •  & Maté Biro

    These authors contributed equally to this work.

Affiliations

  1. Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany

    • Jakub Sedzinski
    • , Maté Biro
    • , Annelie Oswald
    • , Jean-Yves Tinevez
    •  & Ewa Paluch
  2. International Institute of Molecular and Cell Biology, 02109 Warsaw, Poland

    • Jakub Sedzinski
    • , Maté Biro
    • , Jean-Yves Tinevez
    •  & Ewa Paluch
  3. Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany

    • Guillaume Salbreux

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Contributions

J.S., M.B., G.S. and E.P. designed the research and wrote the paper; J.S. performed the experiments except the local drug delivery; M.B. developed the image analysis tools; J.S., M.B. and G.S. analysed the data; A.O. and J.-Y.T. designed and performed the local drug-delivery experiments; G.S. developed the theoretical model.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Ewa Paluch.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Texts 1-5 for the theoretical model, a Supplementary Discussion, additional references, Supplementary Figures 1-14 with legends, Supplementary Table 1 and legends for Supplementary Movies 1-11.

Videos

  1. 1.

    Supplementary Movie 1

    This movie shows bleb formation during cytokinesis (see Supplementary Information file for full legend).

  2. 2.

    Supplementary Movie 2

    In this movie we see cytoplasmic flows in control dividing cell (see Supplementary Information file for full legend).

  3. 3.

    Supplementary Movie 3

    This movie shows that large amplitude cell shape oscillations lead to cytokinesis failure (see Supplementary Information file for full legend).

  4. 4.

    Supplementary Movie 4

    This movie shows large amplitude cell shape oscillations upon spindle depolymerisation (see Supplementary Information file for full legend).

  5. 5.

    Supplementary Movie 5

    This movie shows the adhesion of a cell to the substrate during division (see Supplementary Information file for full legend).

  6. 6.

    Supplementary Movie 6

    This movie shows that local actin depolymerisation leads to assymetric contractility and cell shape oscillations (see Supplementary Information file for full legend).

  7. 7.

    Supplementary Movie 7

    This movie shows that the Laser ablation of the polar cortex leads to cell shape oscillations and cytokinesis failure.

  8. 8.

    Supplementary Movie 8

    This movie shows that anillin depletion leads to cell shape oscillations and cytokinesis failure (see Supplementary Information file for full legend).

  9. 9.

    Supplementary Movie 9

    In this movie we see that the laser ablation of the equatorial cortex in L929 fibroblast leads to periodic cortical disassembly-assembly cycles and cell shape oscillations (see Supplementary Information file for full legend).

  10. 10.

    Supplementary Movie 10

    In this movie we see that the bleb induction in the contracting pole during cell shape oscillations causes premature reversal of the direction of the cytoplasmic flow (see Supplementary Information file for full legend).

  11. 11.

    Supplementary Movie 11

    This movie shows shape oscillations induced by global stabilisation of the acto-myosin cortex by lectin crosslinking (see Supplementary Information file for full legend).

About this article

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DOI

https://doi.org/10.1038/nature10286

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