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. 2007 Dec 31;179(7):1347-54.
doi: 10.1083/jcb.200706005. Epub 2007 Dec 24.

Local cortical pulling-force repression switches centrosomal centration and posterior displacement in C. elegans

Akatsuki Kimura  1 , Shuichi Onami
Affiliations

Local cortical pulling-force repression switches centrosomal centration and posterior displacement in C. elegans

Akatsuki Kimura et al. J Cell Biol. .

Abstract

Centrosome positioning is actively regulated by forces acting on microtubules radiating from the centrosomes. Two mechanisms, center-directed and polarized cortical pulling, are major contributors to the successive centering and posteriorly displacing migrations of the centrosomes in single-cell-stage Caenorhabditis elegans. In this study, we analyze the spatial distribution of the forces acting on the centrosomes to examine the mechanism that switches centrosomal migration from centering to displacing. We clarify the spatial distribution of the forces using image processing to measure the micrometer-scale movements of the centrosomes. The changes in distribution show that polarized cortical pulling functions during centering migration. The polarized cortical pulling force directed posteriorly is repressed predominantly in the lateral regions during centering migration and is derepressed during posteriorly displacing migration. Computer simulations show that this local repression of cortical pulling force is sufficient for switching between centering and displacing migration. Local regulation of cortical pulling might be a mechanism conserved for the precise temporal regulation of centrosomal dynamic positioning.

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Figures

Figure 1.
Figure 1.
Cortex-directed micromovements during the centering phase. (A) Schematic outline of centrosomal movements in a single-cell–stage C. elegans embryo. Centrosomes (red stars), nuclei (blue circles), and mitotic spindles (MTs, green; chromosomes, blue) are shown. (B) Distance-time graph of the pronucleus–centrosome complex in wild-type (WT) and RNAi-treated embryos. EL, egg length. (C) Mean speed of the pronucleus–centrosome complex during 20–80% of the overall migration (n = 5 for each strain). (D) Trajectory of migration over 40 s during the establishment stage. The position of the center of the nuclear–centrosome complex was quantified every 4 s and plotted. The bottom panels show magnified trajectories. The bold lines at the right of each bottom panel indicate the right-hand margins of the cells. (E) Distribution of micromovements at 4-s intervals. Endpoints of the vectors were plotted. X and y axes are as indicated in D. (F and G) Mean angle (F; in cosine) and velocity (G) of micromovements (n = 5 each). θ is the angle between the direction of a micromovement and the center. Error bars represent SD. Bars, 10 μm.
Figure 2.
Figure 2.
Comparison of micromovements during the centering and displacing phase. (A) Image processing to detect centrosomes and chromosomes (bottom) in images of GFP-tubulin and -histone embryos (top). Time is shown in minutes and seconds. (B) Micromovements were classified according to their angles to the AP axis (θ). (C) Posterior indexes (see Results and discussion) for each angle class. n = 13 for WT and n = 15 for Gα(RNAi). (D) Lateral components of the micromovements (V × sinθ). (E) Micromovements of the anterior centrosome (V × F A) and the posterior centrosome (V × F P) toward the polar regions (0–15°). Error bars represent SD. Bar, 10 μm.
Figure 3.
Figure 3.
Model of centering and displacing migration of centrosomes in C. elegans embryo. (A) Roles of three mechanisms in centering migration as examined by computer simulation (top). The bottom images are from real embryos expected to reflect the conditions in the top panels. The asterisks indicate centrosomes. The center-directed mechanism alone brings the centrosomes to the cell center (left), but addition of polarized cortical pulling mechanisms does not (middle). Further addition of a local repression mechanism brings the centrosomes to the center (right). Interestingly, we observed timely nuclear rotation when we included local repression in the model (right), which is consistent with the proposal made by Tsou et al. (2002). (B) Schematic outline and computer simulation of the proposed model. In the schematic outline (top), embryos (yellow ovals), centrosomes (blue stars), center-directed forces (green arrows), cortical pulling forces (red bars), and repression of cortical pulling forces (dashed red box) are indicated. The width of the red bar indicates the strength of the cortical pulling forces along the AP axis. During the displacing phase (right), the cortical pulling force is polarized and stronger toward the posterior half of the embryo. During the centering phase (left), the polarized cortical pulling mechanism is already active but is repressed in the posterior region and prominently in the posterolateral region. In computer simulation panels (bottom), each panel shows a snapshot of the simulation result (left) and movements in the real WT embryo (right). Asterisks indicate chromosomes. Time is shown in minutes and seconds. Bars, 10 μm.
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