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WIREs Dev Biol
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Cytoplasmic protein motility and polarized sorting during asymmetric cell division

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Abstract Cell polarity is inherent to the process of asymmetric cell division, which relies on the asymmetric distribution of multiple polarity proteins and cell‐fate determinants in the cell cortex. The establishment and maintenance of cell polarity require the orchestration of numerous cellular processes. These include cytoplasmic movements, cytoskeleton dynamics, and different signaling events. Equally relevant is the plasma membrane composition, such as the lipid environment that endows particular membrane subdomains with specific characteristics. Sorting receptors and sorting determinants, including posttranslational modifications, also contribute to cell polarization. Together, all these mechanisms would be expected to have great relevance in the context of asymmetric cell division, an essential process in both physiological and pathological conditions. WIREs Dev Biol 2013, 2:797–808. doi: 10.1002/wdev.116 This article is categorized under: Establishment of Spatial and Temporal Patterns > Cytoplasmic Localization

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Mira localization during asymmetric cell division is Myosin II‐ and Myosin VI‐dependent. At interphase, Mira forms an apical crescent in contact with inactive Myosin II. Later, at prophase, phosphorylation of Lgl activates Myosin II and Mira is excluded from the cortex and diffuses into the cytoplasm. At metaphase, Mira forms a basal crescent in contact with Myosin VI.

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Asymmetric endocytosis during asymmetric sensory organ precursors (SOP)/pI division. (a) Numb and α‐Adaptin promote the endocytosis of the Notch regulator Sanpodo (Spdo) in pIIb. (b) Neur induces Delta (Dl) endocytosis and Rab11 drives the recycling of Dl in pIIb. (c) SMAD anchor for receptor activation (SARA) endosomes localize Notch and Dl to pIIa cells after division.

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Vesicle trafficking during endocytosis and exocytosis. (1) Clathrin‐dependent endocytosis. Clathrin‐coated vesicles and clathrin‐adaptor proteins move along actin filaments using myosin motors. (2) After losing the clathrin coat, vesicles associate to Rab GTPases linked to kinesin motors to move along microtubules. (3) Rab5 GTPases associate with early endocytic vesicles to transport them using bidirectional kinesin motors. From here, there are two different pathways, the first of which (4a) involves the formation of early endosomes and subsequently late endosomes. Rab7 associates with the late endocytic vesicles to transport them using unidirectional dynein motors until the formation of late endosomes that will finally fuse with a lysosome. In the second pathway (4b) recycling endosomes are formed, which associate with Rab11 to transport them to the plasma membrane where Sec15 tethers the vesicle to the membrane. These vesicles will fuse with the plasma membrane and their components will be recycled.

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Polarized exocytosis during asymmetric sensory organ precursors (SOP)/pI division. (a) Drosophila melanogaster SOPs divide asymmetrically to give rise to two daughter cells, pIIa and pIIb, which in turn divide asymmetrically to generate the four different cells that will form the sensory organ: a neuron, a sheath, a shaft, and a socket. (b) The exocyst protein Sec15 tethers the Notch ligand Delta (Dl) to a particular sub‐membrane domain in the pIIb cell, while in the pIIa cell Sec15 helps the Notch regulator Sanpodo (Spdo) to reach the membrane.

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Polarized exocytosis: the exocyst and the soluble N‐ethylmaleimide‐sensitive factor attachment protein receptors (SNARE) complex. (1) The exocyst complex tethers secretory vesicles to the plasma membrane through Sec4, where tSNARE proteins associated to the plasma membrane interact with vSNARE proteins present on the vesicles. (2) During the docking process, secretory vesicles are found in tight contact with the plasma membrane. (3) The vesicles finally fuse with the plasma membrane.

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The actomyosin cytoskeleton induces an asymmetric distribution of cell‐fate determinants or polarity proteins in Caenorhabditis elegans. (a) RHO‐1 GTPase induces a cortical flow that promotes the displacement of P granules (green) and the actomyosin cytoskeleton to the posterior and to the anterior pole of the embryo, respectively. As a result, PAR proteins localize asymmetrically, with PAR‐1 and PAR‐2 proteins accumulating in the posterior part of the embryo, whereas PAR‐3, PAR‐6, and PKC‐3 form a complex in the anterior domain (1). The CDC‐42 GTPase maintains the asymmetric distribution of the PAR protein at later stages (2). (b) In Saccharomyces cerevisiae, the complex of cdc42p with PAK effectors drives the assembly of actin filaments in the growing bud. ASH1 mRNA (red) is transcribed in the nucleus (1) and it is then packed into RNP complexes that contain myosin‐binding proteins (green), which in turn bind to the myosin Myo4p motor (orange). Myo4p transports the RNPs along actin filaments toward the growing bud (2). At the membrane of the bud tip, the RNPs dissociate liberating ASH1 mRNAs at the cell membrane. These transcripts will later be translated into Ash1p protein, which will repress the mating‐type switching in this cell (3).

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Model systems in which to analyze asymmetric cell division. (a) Drosophila melanogaster central nervous system (CNS) neural stem cells (NBs). Apical proteins form a crescent (purple) at the apical pole of the NB, whereas cell‐fate determinants form a basal crescent (yellow) during metaphase (DNA is shown in red). After division, cell‐fate determinants segregate to the basal‐most daughter cell, the ganglion mother cell (gmc). (b) D. melanogaster peripheral nervous system (PNS) progenitor cells [sensory organ precursors (SOP)s/pIs]. Anterior (purple) and posterior (yellow) proteins segregate asymmetrically during metaphase and end up in the pIIa or pIIb daughter cells after division, respectively. (c) Caenorhabditis elegans one‐cell stage embryo. Anterior polarity proteins (purple), and posterior polarity proteins (yellow) accumulate asymmetrically at metaphase (DNA is shown in red). After division both types of proteins segregate differentially into the anterior (ac) or posterior (pc) daughter cells. (d) Saccharomyces cerevisiae budding yeast. Mother cell (mc) proteins (purple) and daughter cell (dc) determinants in the bud (yellow) localize asymmetrically at metaphase (DNA appears in red). After division, cell determinants segregate to the bud daughter cell.

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