A cytokinesis furrow is positioned by two consecutive signals

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Abstract

The position of the cytokinesis furrow in a cell determines the relative sizes of its two daughter cells as well as the distribution of their contents. In animal cells, the position of the cytokinesis furrow is specified by the position of the mitotic spindle1. The cytokinesis furrow bisects the spindle midway between the microtubule asters, at the site of the microtubule-based midzone, producing two daughter cells. Experiments in some cell types have suggested that the midzone positions the furrow2,3, but experiments in other cells have suggested that the asters position the furrow4,5. One possibility is that different organisms and cell types use different mechanisms to position the cytokinesis furrow. An alternative possibility is that both asters and the midzone contribute to furrow positioning6,7. Recent work in C. elegans has suggested that centrosome separation and the midzone are implicated in cytokinesis8. Here we examine the relative contributions of different parts of the mitotic spindle to positioning of the cytokinesis furrow in the C. elegans zygote. By spatially separating the spindle midzone from one of the asters using an ultraviolet laser, we show that the cytokinesis furrow is first positioned by a signal determined by microtubule asters, and then by a second signal that is derived from the spindle midzone. Thus, the position of the cytokinesis furrow is specified by two consecutive furrowing activities.

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Figure 1: Asymmetric spindle severing spatially separates the spindle midzone and the region midway between the asters, leading to the generation of two furrows.
Figure 2: Microtubule asters position the first cytokinesis furrow.
Figure 3: Genetic control of redundant cleavage plane positioning.

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Acknowledgements

We thank the Caenorhabditis Genetics Center, the UK HGMP Resource Centre, Cenix Bioscience, T. Stiernagle, J. Ahringer, M. Glotzer, M. Srayko, C. Cowan, L. Pelletier, P. E. Mains, A. Schwager and A. Pozniakovskiy for reagents; C. Cowan, S. Grill, S. Schoenegg, J. Stamford and M. Srayko for advice and help on the experimental setup; and C. Cowan, J. Howard and K. Verbrugghe for comments on the manuscript. H.B. was supported by a predoctoral fellowship from the Boehringer Ingelheim Foundation.

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Correspondence to Henrik Bringmann.

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Supplementary information

Supplementary Video S1

This movie shows a C. elegans zygote at metaphase-to-anaphase transition. (MOV 17386 kb)

Supplementary Video S2

This movie shows asymmetric spindle severing: the anterior centrosome (left) is chopped off. (MOV 17064 kb)

Supplementary Video S3

This movie shows cytokinesis in an unsevered control C. elegans zygote. (MOV 30172 kb)

Supplementary Video S4

This movie shows cytokinesis after anterior ASS: Note the formation of two distinct furrows after ASS. (MOV 74611 kb)

Supplementary Video S5

This movie shows cytokinesis after posterior ASS: Note the furrow correction observed after ASS. (MOV 39186 kb)

Supplementary Video S6

This movie shows asymmetric spindle severing with subsequent disintegration of the chopped-off aster. (MOV 28777 kb)

Supplementary Video S7

This movie shows cytokinesis after ASS with disintegration of the chopped-off aster. (MOV 46692 kb)

Supplementary Video S8

This movie shows cytokinesis in a zen-4(RNAi) depleted one-cell embryo. (MOV 24644 kb)

Supplementary Video S9

This movie shows cytokinesis after ASS in a zen-4(RNAi) depleted embryo (MOV 20788 kb)

Supplementary Video S10

This movie shows cytokinesis in a klp-7(RNAi) depleted zygote. (MOV 28475 kb)

Supplementary Video S11

This movie shows cytokinesis after posterior ASS in a klp-7(RNAi) depleted zygote. (MOV 30971 kb)

Supplementary Video S12

This movie shows cytokinesis in a mel-11(it26) mutant zygote. (MOV 33120 kb)

Supplementary Video S13

This movie shows cytokinesis after posterior ASS in a mel-11(it26) mutant zygote. (MOV 34526 kb)

Supplementary Video S14

This movie shows cytokinesis in an NMY2::GFP strain observed by spinning disk microscopy. (MOV 22223 kb)

Supplementary Video S15

This movie shows cytokinesis after posterior ASS plus aster ablation in an NMY2::GFP strain observed by spinning disk microscopy. (MOV 43962 kb)

Supplementary Table S1

Genes with known or potential involvement in the first cytokinesis of the C. elegans zygote, and their roles in redundant cleavage plane specification as analysed by asymmetric spindle severing (ASS): Shown are gene names, loci, knockout method and phenotypes after ASS. (XLS 20 kb)

Supplementary Legends

Full text descriptions to accompany the above Supplementary Videos and Supplementary Table. (DOC 116 kb)

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Bringmann, H., Hyman, A. A cytokinesis furrow is positioned by two consecutive signals. Nature 436, 731–734 (2005) doi:10.1038/nature03823

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