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Myosin and the PAR proteins polarize microfilament-dependent forces that shape and position mitotic spindles in Caenorhabditis elegans.

Severson AF, Bowerman B - J. Cell Biol. (2003)

Bottom Line: Unlike MFs, dynein, and dynactin, myosin II is not required for the production of these forces.Instead, myosin influences embryonic polarity by limiting PAR-3 to the anterior cortex.This in turn produces asymmetry in the forces applied to MTs at each pole and allows PAR-2 to accumulate in the posterior cortex of a one-cell zygote and maintain asymmetry.

View Article: PubMed Central - PubMed

Affiliation: Institute of Molecular Biology, University of Oregon, Eugene, OR 97403-1229, USA.

ABSTRACT
In Caenorhabditis elegans, the partitioning proteins (PARs), microfilaments (MFs), dynein, dynactin, and a nonmuscle myosin II all localize to the cortex of early embryonic cells. Both the PARs and the actomyosin cytoskeleton are required to polarize the anterior-posterior (a-p) body axis in one-cell zygotes, but it remains unknown how MFs influence embryonic polarity. Here we show that MFs are required for the cortical localization of PAR-2 and PAR-3. Furthermore, we show that PAR polarity regulates MF-dependent cortical forces applied to astral microtubules (MTs). These forces, which appear to be mediated by dynein and dynactin, produce changes in the shape and orientation of mitotic spindles. Unlike MFs, dynein, and dynactin, myosin II is not required for the production of these forces. Instead, myosin influences embryonic polarity by limiting PAR-3 to the anterior cortex. This in turn produces asymmetry in the forces applied to MTs at each pole and allows PAR-2 to accumulate in the posterior cortex of a one-cell zygote and maintain asymmetry.

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Models of the polarization of the C. elegans zygote. (a) F-actin recruits myosin II, PAR-2, and PAR-3 to the cortex. In addition, MFs or MF-associated proteins act on the mitotic spindle, flattening the posterior centrosome. Myosin II and PAR-2 restrict PAR-3 to the anterior cortex where PAR-3 inhibits centrosome flattening. (b) A model of cortical forces that act in the early embryo. MFs recruit dynein and the dynactin complex to the cortex. Dynein pulls on astral MTs nucleated by the centrosomes. PAR-3 (red) inhibits dynein localization or function, resulting in a lower activity in the anterior hemisphere than in the posterior (blue triangle). Consequently, less force is applied to the anterior centrosome than the posterior centrosome (arrows), and the spindle becomes posteriorly displaced. The high lateral forces in the posterior hemisphere stretch the posterior centrosome, flattening it into a disc shape. For an alternative model see Tsou et al. (2002).
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fig5: Models of the polarization of the C. elegans zygote. (a) F-actin recruits myosin II, PAR-2, and PAR-3 to the cortex. In addition, MFs or MF-associated proteins act on the mitotic spindle, flattening the posterior centrosome. Myosin II and PAR-2 restrict PAR-3 to the anterior cortex where PAR-3 inhibits centrosome flattening. (b) A model of cortical forces that act in the early embryo. MFs recruit dynein and the dynactin complex to the cortex. Dynein pulls on astral MTs nucleated by the centrosomes. PAR-3 (red) inhibits dynein localization or function, resulting in a lower activity in the anterior hemisphere than in the posterior (blue triangle). Consequently, less force is applied to the anterior centrosome than the posterior centrosome (arrows), and the spindle becomes posteriorly displaced. The high lateral forces in the posterior hemisphere stretch the posterior centrosome, flattening it into a disc shape. For an alternative model see Tsou et al. (2002).

Mentions: Our data suggest that the nonmuscle myosin II subunits NMY-2 and MLC-4 mediate only a subset of F-actin–dependent processes during polarization of the a-p axis in a C. elegans zygote. F-actin is required for at least four polarity functions in the one-cell stage embryo: the cortical localizations of PAR-2, PAR-3, and NMY-2, and centrosome flattening (Fig. 5 a). In contrast, NMY-2 and MLC-4 are dispensable for cortical PAR localization and for centrosome flattening. Myosin II instead restricts PAR-3 to the anterior cortex, which permits expansion of the PAR-2 domain. As ectopic PAR-3 accumulates in the posterior of par-2 single mutants, myosin is not sufficient to restrict PAR-3. Thus, both PAR-2 and myosin II are required to limit PAR-3 to the anterior cortex.


Myosin and the PAR proteins polarize microfilament-dependent forces that shape and position mitotic spindles in Caenorhabditis elegans.

Severson AF, Bowerman B - J. Cell Biol. (2003)

Models of the polarization of the C. elegans zygote. (a) F-actin recruits myosin II, PAR-2, and PAR-3 to the cortex. In addition, MFs or MF-associated proteins act on the mitotic spindle, flattening the posterior centrosome. Myosin II and PAR-2 restrict PAR-3 to the anterior cortex where PAR-3 inhibits centrosome flattening. (b) A model of cortical forces that act in the early embryo. MFs recruit dynein and the dynactin complex to the cortex. Dynein pulls on astral MTs nucleated by the centrosomes. PAR-3 (red) inhibits dynein localization or function, resulting in a lower activity in the anterior hemisphere than in the posterior (blue triangle). Consequently, less force is applied to the anterior centrosome than the posterior centrosome (arrows), and the spindle becomes posteriorly displaced. The high lateral forces in the posterior hemisphere stretch the posterior centrosome, flattening it into a disc shape. For an alternative model see Tsou et al. (2002).
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Related In: Results  -  Collection

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fig5: Models of the polarization of the C. elegans zygote. (a) F-actin recruits myosin II, PAR-2, and PAR-3 to the cortex. In addition, MFs or MF-associated proteins act on the mitotic spindle, flattening the posterior centrosome. Myosin II and PAR-2 restrict PAR-3 to the anterior cortex where PAR-3 inhibits centrosome flattening. (b) A model of cortical forces that act in the early embryo. MFs recruit dynein and the dynactin complex to the cortex. Dynein pulls on astral MTs nucleated by the centrosomes. PAR-3 (red) inhibits dynein localization or function, resulting in a lower activity in the anterior hemisphere than in the posterior (blue triangle). Consequently, less force is applied to the anterior centrosome than the posterior centrosome (arrows), and the spindle becomes posteriorly displaced. The high lateral forces in the posterior hemisphere stretch the posterior centrosome, flattening it into a disc shape. For an alternative model see Tsou et al. (2002).
Mentions: Our data suggest that the nonmuscle myosin II subunits NMY-2 and MLC-4 mediate only a subset of F-actin–dependent processes during polarization of the a-p axis in a C. elegans zygote. F-actin is required for at least four polarity functions in the one-cell stage embryo: the cortical localizations of PAR-2, PAR-3, and NMY-2, and centrosome flattening (Fig. 5 a). In contrast, NMY-2 and MLC-4 are dispensable for cortical PAR localization and for centrosome flattening. Myosin II instead restricts PAR-3 to the anterior cortex, which permits expansion of the PAR-2 domain. As ectopic PAR-3 accumulates in the posterior of par-2 single mutants, myosin is not sufficient to restrict PAR-3. Thus, both PAR-2 and myosin II are required to limit PAR-3 to the anterior cortex.

Bottom Line: Unlike MFs, dynein, and dynactin, myosin II is not required for the production of these forces.Instead, myosin influences embryonic polarity by limiting PAR-3 to the anterior cortex.This in turn produces asymmetry in the forces applied to MTs at each pole and allows PAR-2 to accumulate in the posterior cortex of a one-cell zygote and maintain asymmetry.

View Article: PubMed Central - PubMed

Affiliation: Institute of Molecular Biology, University of Oregon, Eugene, OR 97403-1229, USA.

ABSTRACT
In Caenorhabditis elegans, the partitioning proteins (PARs), microfilaments (MFs), dynein, dynactin, and a nonmuscle myosin II all localize to the cortex of early embryonic cells. Both the PARs and the actomyosin cytoskeleton are required to polarize the anterior-posterior (a-p) body axis in one-cell zygotes, but it remains unknown how MFs influence embryonic polarity. Here we show that MFs are required for the cortical localization of PAR-2 and PAR-3. Furthermore, we show that PAR polarity regulates MF-dependent cortical forces applied to astral microtubules (MTs). These forces, which appear to be mediated by dynein and dynactin, produce changes in the shape and orientation of mitotic spindles. Unlike MFs, dynein, and dynactin, myosin II is not required for the production of these forces. Instead, myosin influences embryonic polarity by limiting PAR-3 to the anterior cortex. This in turn produces asymmetry in the forces applied to MTs at each pole and allows PAR-2 to accumulate in the posterior cortex of a one-cell zygote and maintain asymmetry.

Show MeSH
Related in: MedlinePlus