Satoh SK et al. (2013), The tension at the top of the animal pole decre...

ECB-ART-43130

PLoS One 2013 Jan 01;811:e79389. doi: 10.1371/journal.pone.0079389.

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The tension at the top of the animal pole decreases during meiotic cell division.

Satoh SK , Tsuchi A , Satoh R , Miyoshi H , Hamaguchi MS , Hamaguchi Y .

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Meiotic maturation is essential for the reproduction procedure of many animals. During this process an oocyte produces a large egg cell and tiny polar bodies by highly asymmetric division. In this study, to fully understand the sophisticated spatiotemporal regulation of accurate oocyte meiotic division, we focused on the global and local changes in the tension at the surface of the starfish (Asterina pectinifera) oocyte in relation to the surface actin remodeling. Before the onset of the bulge formation, the tension at the animal pole globally decreased, and started to increase after the onset of the bulge formation. Locally, at the onset of the bulge formation, tension at the top of the animal pole began to decrease, whereas that at the base of the bulge remarkably increased. As the bulge grew, the tension at the base of the bulge additionally increased. Such a change in the tension at the surface was similar to the changing pattern of actin distribution. Therefore, meiotic cell division was initiated by the bulging of the cortex, which had been weakened by actin reduction, and was followed by contraction at the base of the bulge, which had been reinforced by actin accumulation. The force generation system is assumed to allow the meiotic apparatus to move just under the membrane in the small polar body. Furthermore, a detailed comparison of the tension at the surface and the cortical actin distribution indicated another sophisticated feature, namely that the contraction at the base of the bulge was more vigorous than was presumed based on the actin distribution. These features of the force generation system will ensure the precise chromosome segregation necessary to produce a normal ovum with high accuracy in the meiotic maturation.

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Genes referenced: LOC105444658 LOC115919910 LOC115925415 LOC590297 pole

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	Figure 1. Procedure of rough estimation of the tension at the surface of whole oocytes.(A) Image of an oocyte at low resolution. Tension at the surface in the longitudinal direction (the direction joining pole to pole), T1, that in the latitudinal direction (the direction at right angles to the former), T2, and principal radii of curvature, R1 and R2 are indicated. Scale bar, 50 µm. (C) Binary image of the oocyte in (A) processed by NIH-Image, and the outline curve of the oocyte expressed in polar coordinates. (D) The radius of the oocyte and the tensions at the surface. The spline function accurately fits the radius of the original outline curve except for the animal pole.
	Figure 2. Procedure of fine estimation of tension at the surface of the animal hemisphere.(A) Image of the animal hemisphere of an oocyte at high resolution. Scale bar, 50 µm. (B) The outline curve in the animal hemisphere expressed in polar coordinates. (C) Tensions at the surface in the animal hemisphere and the radius of the oocyte versus the distance along the cord, vertical to the animal vegetal axis. The spline function accurately fits the radius of the original outline curve.
	Figure 3. Shape change of a starfish oocyte during meiotic cell division.The top side is the animal pole. Numbers shown are the time after the onset of the bulge formation. Scale bar, 50 µm.
	Figure 4. Global changes in the tension at the surface of the oocytes.The tension at the surface is calculated by the rough estimation based on the images shown in Fig.3. Abscissa: time after the onset of bulge formation. Ordinate: Tension, (T1+T2)/2, averaged over 20 degrees at the animal pole (solid line with filled triangle), that at the vegetal pole (broken line with open triangle), thdat at the equator (dotted line with open circle).
	Figure 5. Time-course of relative tension around the animal pole.Relative tension, Tr, at the surface, calculated by the fine estimation at a vertical distance of 20 µm below the animal pole and the bulge is represented with a pseudocolor on the 3D oocyte surface. The numbers shown below are the elapsed time (min) after the onset of the bulge formation. A color scale from 0 to 4.0 is shown at the bottom right of the figure. Scale bar, 50 µm.
	Figure 6. Characteristics of spatiotemporal changes in the tension at the surface around the animal pole.Time-course of the relative tension, Tr, at the top of the animal pole (solid line with triangle), the maximum of Tr at the base of the bulge (dotted line with filled circle), and the diameter of the maximum Tr ring at the base of the bulge (broken line with open circle). Abscissa: time after the onset of bulge formation. Left ordinate: relative tension, Tr. Right ordinate: distance of two peaks at the base of the bulge.
	Figure 7. Time-course of actin distribution around the animal pole.Actin distribution (A) before and (B) at the onset of, and (C, D, E) after the bulge formation. Actin fluorescence distribution that had been analyzed previously [10] is shown in pseudocolor on the 3D cell surface whose image is restricted to the surface near the animal pole, at the height of 20 µm except for the bulge. For comparison with the data of the relative tension at the surface in Fig. 5, the fluorescence distribution is normalized by the ratio of actin fluorescent intensity around the animal pole to that at the surface at a vertical distance of 20 µm below the animal pole. A color scale indicating the normalized actin fluorescence from 0 to 2.5 is shown at the bottom right of the figure. Scal bar, 50 µm.
	Figure 8. Force generation mechanism to ensure precise chromosome segregation for normal meiotic cell division.The magnitude of the tension is indicated by varying the thickness of the blue line. The meiotic apparatus is shown by the green line. Chromosomes are shown by the filled blue circles. (A) Before bulging started, the global tension around the animal pole is smaller than that in the vegetal pole. The meiotic apparatus exists just under the cell membrane at the animal pole. (B) After the onset of the bulge formation, the global tension around the animal pole starts to increase. Locally, the surface at the top of the animal pole weakens to form a bulge of the polar body; in contrast, the tension at the base of the bulge increases. The dividing furrow is formed in the equatorial plane of the meiotic apparatus. (C) As the bulge grows, the tension additionally increases at the base of the bulge. The meiotic apparatus moves into the bulge and is kept under the membrane. The position of the dividing furrow is in the equatorial plane of the mitotic apparatus.

References [+] :

Azoury, Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization. 2011, Pubmed