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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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PAR proteins and mitotic spindle polarity in the C. elegans zygote. (a and b) In wild-type embryos, PAR-3 accumulates at the anterior cortex, whereas PAR-2 is localized to the posterior. (c) The posterior centrosome flattens in telophase. (d–f) In par-2(lw32) mutant embryos, PAR-3 spreads around much of the posterior cortex, PAR-2 is undetectable at the cortex, and both mitotic spindle poles remain symmetrical and rounded. (g–i) In par-3(it71) mutant embryos, PAR-2 encircles the embryo and both centrosomes flatten. In this and all subsequent figures, embryos are oriented with their anterior pole to the left.
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fig1: PAR proteins and mitotic spindle polarity in the C. elegans zygote. (a and b) In wild-type embryos, PAR-3 accumulates at the anterior cortex, whereas PAR-2 is localized to the posterior. (c) The posterior centrosome flattens in telophase. (d–f) In par-2(lw32) mutant embryos, PAR-3 spreads around much of the posterior cortex, PAR-2 is undetectable at the cortex, and both mitotic spindle poles remain symmetrical and rounded. (g–i) In par-3(it71) mutant embryos, PAR-2 encircles the embryo and both centrosomes flatten. In this and all subsequent figures, embryos are oriented with their anterior pole to the left.

Mentions: First identified in the nematode Caenorhabditis elegans (Kemphues et al., 1988), the conserved partitioning proteins (PARs)* are required for cell polarity in many animal cell types (for review see Doe and Bowerman, 2001; Wodarz, 2002). In the one-cell stage C. elegans embryo, the PDZ domain protein PAR-3 and the Ring finger protein PAR-2 concentrate in complementary anterior and posterior cortical domains, respectively. Both are required to specify the anterior-posterior (a-p) body axis and to orient and position mitotic spindles relative to the a-p axis (Kemphues et al., 1988; Cheng et al., 1995; Etemad-Moghadam et al., 1995; Boyd et al., 1996) (Fig. 1 , a and b).


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)

PAR proteins and mitotic spindle polarity in the C. elegans zygote. (a and b) In wild-type embryos, PAR-3 accumulates at the anterior cortex, whereas PAR-2 is localized to the posterior. (c) The posterior centrosome flattens in telophase. (d–f) In par-2(lw32) mutant embryos, PAR-3 spreads around much of the posterior cortex, PAR-2 is undetectable at the cortex, and both mitotic spindle poles remain symmetrical and rounded. (g–i) In par-3(it71) mutant embryos, PAR-2 encircles the embryo and both centrosomes flatten. In this and all subsequent figures, embryos are oriented with their anterior pole to the left.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2172887&req=5

fig1: PAR proteins and mitotic spindle polarity in the C. elegans zygote. (a and b) In wild-type embryos, PAR-3 accumulates at the anterior cortex, whereas PAR-2 is localized to the posterior. (c) The posterior centrosome flattens in telophase. (d–f) In par-2(lw32) mutant embryos, PAR-3 spreads around much of the posterior cortex, PAR-2 is undetectable at the cortex, and both mitotic spindle poles remain symmetrical and rounded. (g–i) In par-3(it71) mutant embryos, PAR-2 encircles the embryo and both centrosomes flatten. In this and all subsequent figures, embryos are oriented with their anterior pole to the left.
Mentions: First identified in the nematode Caenorhabditis elegans (Kemphues et al., 1988), the conserved partitioning proteins (PARs)* are required for cell polarity in many animal cell types (for review see Doe and Bowerman, 2001; Wodarz, 2002). In the one-cell stage C. elegans embryo, the PDZ domain protein PAR-3 and the Ring finger protein PAR-2 concentrate in complementary anterior and posterior cortical domains, respectively. Both are required to specify the anterior-posterior (a-p) body axis and to orient and position mitotic spindles relative to the a-p axis (Kemphues et al., 1988; Cheng et al., 1995; Etemad-Moghadam et al., 1995; Boyd et al., 1996) (Fig. 1 , a and b).

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