Dynamic positioning of the fission yeast cell division plane - PubMed (original) (raw)

Dynamic positioning of the fission yeast cell division plane

Rafael R Daga et al. Proc Natl Acad Sci U S A. 2005.

Abstract

A key question in cytokinesis is how the cell division plane is positioned. Whereas microtubules of the mitotic apparatus specify the division site in animal cells, we show here that the nucleus plays this role in the fission yeast Schizosaccharomyces pombe. By centrifuging cells to move the nucleus, we find that the nucleus (or a nuclear-associated structure) actively influences the position of contractile ring assembly during early mitosis. Displacement of the nucleus during this induction period can lead to formation of multiple rings. The nucleus signals its position in a microtubule-independent manner by emitting the protein mid1p. Furthermore, movement of ring fragments together minimizes formation of multiple division sites. These dynamic mechanisms of ring positioning provide a robust coordination of nuclear and cell division.

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Figures

Fig. 1.

Fig. 1.

The position of the predivisional nucleus determines the position of ring assembly. Fission yeast cells expressing rlc1-GFP nup107-GFP GFP-atb2 (a and b) (RD48) (markers for the contractile ring, nuclear envelope, and MTs, respectively) and cells expressing rlc1-GFP GFP-atb2 cells (RD104) (c) were centrifuged to displace the nucleus from the middle of the cell, and then imaged by time-lapse 3D confocal microscopy (see Materials and Methods for details). Maximal projections of Z series of representative frames are shown. Shown are cells centrifuged during interphase (a and b), a cell with a displaced nucleus and ring (b), and a cell centrifuged in mid-mitosis (c). (Scale bars, 3 μm.)

Fig. 2.

Fig. 2.

Effect of nuclear displacement on contractile ring assembly. (a) Asynchronous wild-type cells were centrifuged and assayed for positions of the spindle, nucleus, and rlc1-GFP by using time-lapse microscopy. Percentages of cells forming contractile rings or ring fragments (as visualized by rlc1-GFP) at the specified positions are listed. (b) cdc25-22 cells were synchronized in mitosis by temperature shifts, centrifuged at specified cell-cycle points, and then imaged. (c) cdc25-22 cells were synchronized and centrifuged twice (see Materials and Methods).

Fig. 3.

Fig. 3.

Induction of extra contractile rings and ring fragments by the nucleus. cdc25-22 rlc1-GFP GFP-atb2 cells (RD129) were synchronized in mitosis by temperature shift to 36°C for 4 h, released to 25°C, and then centrifuged to displace the nucleus. Representative images of maximum _Z_-series projections and kymographs of the indicated boxed regions are shown. (a) Example of a cell centrifuged during anaphase that did not form a second ring or ring fragment. (b) Example of a cell centrifuged in early mitosis that assembled a second ring at the position of the displaced nucleus (arrows). Both rings were stable and functional, because they contracted and directed septum assembly (arrow heads). (c) Example of two rings that move toward each other. (d) Example of a stable strand of rlc1-GFP that extended from the region of displaced nucleus to the central ring. (e) Example of an rlc1-GFP fragment that moved from the nucleus to the ring at the old site, fusing with it (arrow at 18 min). (f) Example of cell after a double-centrifugation procedure (see Materials and Methods) that assembled two stable rings near each cell tip. (g) In cells with two rings, the percentages of cells in which rings do not move toward each other were compared with the initial distances between the rings (n ≥ 5 each point; data from both single- and double-centrifugation protocols). (Scale bars, 5 μm; kymographs, ×1.5.)

Fig. 4.

Fig. 4.

The nucleus positions mid1p at the cortex. (a_–_c) Time-lapse images (Left) of cells expressing mid1-GFP. Kymographs (Center and Right) depict mid1-GFP behavior in boxed regions located at the cortex (c) and the nuclear envelope (n). (a) Interphase mid1-GFP cells (FC958) without centrifugation. (b and c) Two representative examples of interphase mid1-GFP cells in which the nucleus is recentering, after centrifugation. An arrow indicates large nuclear envelope deformation associated with nuclear movement. Asterisks mark representative mid1-GFP cortical dots that move with the nucleus. (Scale bars, 3 μm; kymographs, ×1.5.)

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