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Organelle segregation during mitosis: lessons from asymmetrically dividing cells.

Ouellet J, Barral Y - J. Cell Biol. (2012)

Bottom Line: Analysis of organelle partitioning in asymmetrically dividing cells has provided insights into the mechanisms through which cells control organelle distribution.Interestingly, these studies have revealed that segregation mechanisms frequently link organelle distribution to organelle growth and formation.Furthermore, in many cases, cells use organelles, such as the endoplasmic reticulum and P granules, as vectors for the segregation of information.

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Affiliation: Institute of Biochemistry, Department of Biology, Eidgenössische Technische Hochschule Zürich, 8093 Zurich, Switzerland.

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P granule formation in the C. elegans one-cell embryo. Formation of this organelle is proposed to occur through a dissolution/aggregation mechanism. After fertilization, P granule components (both RNAs and proteins) are distributed uniformly throughout the cytoplasm. Upon specification of the anterior–posterior axis, the posterior polarity protein PAR-1 (blue) promotes their aggregation. As a consequence, P granules assemble specifically in the posterior of the embryo. Once aggregated, P granule components diffuse more slowly and therefore remain preferentially in the posterior compartment of the embryo. On the anterior of the embryo, MEX-5 (red) promotes the dissolution of P granules. Once the different components are in solution in the anterior, they diffuse more rapidly and can replenish the posterior pool. Cleavage results in the inheritance of P granules only in the posterior daughter cell (the P1 cell).
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fig1: P granule formation in the C. elegans one-cell embryo. Formation of this organelle is proposed to occur through a dissolution/aggregation mechanism. After fertilization, P granule components (both RNAs and proteins) are distributed uniformly throughout the cytoplasm. Upon specification of the anterior–posterior axis, the posterior polarity protein PAR-1 (blue) promotes their aggregation. As a consequence, P granules assemble specifically in the posterior of the embryo. Once aggregated, P granule components diffuse more slowly and therefore remain preferentially in the posterior compartment of the embryo. On the anterior of the embryo, MEX-5 (red) promotes the dissolution of P granules. Once the different components are in solution in the anterior, they diffuse more rapidly and can replenish the posterior pool. Cleavage results in the inheritance of P granules only in the posterior daughter cell (the P1 cell).

Mentions: Instead of heat and cold, the asymmetric distribution of the granules is driven by the presence of polarity factors promoting their dissociation or condensation at opposite ends of the one-cell oocyte (Fig. 1). Among these polarity factors, the kinase PAR-1 and the RNA-binding protein MEX-5 are prime candidates to act in the control of P granule condensation and dissociation, respectively (Guo and Kemphues, 1995; Schubert et al., 2000). During P granule partition, the procondensation factor PAR-1 localizes to the posterior cortex of the embryo, whereas the dissociation promoter MEX-5 localizes to the cytoplasm of the anterior half of the cell. The importance of these two proteins in granule dynamics is underlined by the observation that P granules disassemble throughout the cell in par-1 mutant embryos, whereas they assemble and accumulate throughout the cell when MEX-5 is depleted (Brangwynne et al., 2009). However, it is unclear at this point whether both PAR-1 and MEX-5 act directly on P granule components. Indeed, PAR-1 is also known to control MEX-5 distribution (Tenlen et al., 2008; Daniels et al., 2010). Therefore, PAR-1 may act by promoting the condensation of granule components through their direct phosphorylation at the posterior end of the oocyte and by mediating the confinement of MEX-5 and P-granule disassembly to the anterior end of the cell. Alternatively, it may control P granule partition solely through this last process. It may also regulate the function of pptr-1, a regulatory subunit of PP2A recently shown to be required for P granule formation (Gallo et al., 2010). Regardless, it is attractive to think that the simple mechanism of dissociation/condensation might very generally drive the partition of cytoplasmic material into specialized organelles such as Cajal bodies, P bodies, and stress granules and control their spatial distribution. Together, these studies indicate that at least one mechanism controlling the distribution and the symmetric or asymmetric segregation of an organelle is to spatially control the dynamics of its assembly and disassembly. However, alternative pathways appear to coexist and ensure that asymmetry is achieved with high fidelity. In the case of P granules, such an alternative pathway is provided after division by autophagy, which eliminates missegregated granules in the somatic cells (Zhang et al., 2009; Zhao et al., 2009). However, this mechanism assumes that division is already asymmetric enough to allow the emergence of a somatic lineage. Therefore, autophagy appears to enhance asymmetry rather than generate it in the first place.


Organelle segregation during mitosis: lessons from asymmetrically dividing cells.

Ouellet J, Barral Y - J. Cell Biol. (2012)

P granule formation in the C. elegans one-cell embryo. Formation of this organelle is proposed to occur through a dissolution/aggregation mechanism. After fertilization, P granule components (both RNAs and proteins) are distributed uniformly throughout the cytoplasm. Upon specification of the anterior–posterior axis, the posterior polarity protein PAR-1 (blue) promotes their aggregation. As a consequence, P granules assemble specifically in the posterior of the embryo. Once aggregated, P granule components diffuse more slowly and therefore remain preferentially in the posterior compartment of the embryo. On the anterior of the embryo, MEX-5 (red) promotes the dissolution of P granules. Once the different components are in solution in the anterior, they diffuse more rapidly and can replenish the posterior pool. Cleavage results in the inheritance of P granules only in the posterior daughter cell (the P1 cell).
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC3275374&req=5

fig1: P granule formation in the C. elegans one-cell embryo. Formation of this organelle is proposed to occur through a dissolution/aggregation mechanism. After fertilization, P granule components (both RNAs and proteins) are distributed uniformly throughout the cytoplasm. Upon specification of the anterior–posterior axis, the posterior polarity protein PAR-1 (blue) promotes their aggregation. As a consequence, P granules assemble specifically in the posterior of the embryo. Once aggregated, P granule components diffuse more slowly and therefore remain preferentially in the posterior compartment of the embryo. On the anterior of the embryo, MEX-5 (red) promotes the dissolution of P granules. Once the different components are in solution in the anterior, they diffuse more rapidly and can replenish the posterior pool. Cleavage results in the inheritance of P granules only in the posterior daughter cell (the P1 cell).
Mentions: Instead of heat and cold, the asymmetric distribution of the granules is driven by the presence of polarity factors promoting their dissociation or condensation at opposite ends of the one-cell oocyte (Fig. 1). Among these polarity factors, the kinase PAR-1 and the RNA-binding protein MEX-5 are prime candidates to act in the control of P granule condensation and dissociation, respectively (Guo and Kemphues, 1995; Schubert et al., 2000). During P granule partition, the procondensation factor PAR-1 localizes to the posterior cortex of the embryo, whereas the dissociation promoter MEX-5 localizes to the cytoplasm of the anterior half of the cell. The importance of these two proteins in granule dynamics is underlined by the observation that P granules disassemble throughout the cell in par-1 mutant embryos, whereas they assemble and accumulate throughout the cell when MEX-5 is depleted (Brangwynne et al., 2009). However, it is unclear at this point whether both PAR-1 and MEX-5 act directly on P granule components. Indeed, PAR-1 is also known to control MEX-5 distribution (Tenlen et al., 2008; Daniels et al., 2010). Therefore, PAR-1 may act by promoting the condensation of granule components through their direct phosphorylation at the posterior end of the oocyte and by mediating the confinement of MEX-5 and P-granule disassembly to the anterior end of the cell. Alternatively, it may control P granule partition solely through this last process. It may also regulate the function of pptr-1, a regulatory subunit of PP2A recently shown to be required for P granule formation (Gallo et al., 2010). Regardless, it is attractive to think that the simple mechanism of dissociation/condensation might very generally drive the partition of cytoplasmic material into specialized organelles such as Cajal bodies, P bodies, and stress granules and control their spatial distribution. Together, these studies indicate that at least one mechanism controlling the distribution and the symmetric or asymmetric segregation of an organelle is to spatially control the dynamics of its assembly and disassembly. However, alternative pathways appear to coexist and ensure that asymmetry is achieved with high fidelity. In the case of P granules, such an alternative pathway is provided after division by autophagy, which eliminates missegregated granules in the somatic cells (Zhang et al., 2009; Zhao et al., 2009). However, this mechanism assumes that division is already asymmetric enough to allow the emergence of a somatic lineage. Therefore, autophagy appears to enhance asymmetry rather than generate it in the first place.

Bottom Line: Analysis of organelle partitioning in asymmetrically dividing cells has provided insights into the mechanisms through which cells control organelle distribution.Interestingly, these studies have revealed that segregation mechanisms frequently link organelle distribution to organelle growth and formation.Furthermore, in many cases, cells use organelles, such as the endoplasmic reticulum and P granules, as vectors for the segregation of information.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Biochemistry, Department of Biology, Eidgenössische Technische Hochschule Zürich, 8093 Zurich, Switzerland.

Show MeSH
Related in: MedlinePlus