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Laminin is required to orient epithelial polarity in the C. elegans pharynx.

ABSTRACT: The development of many animal organs involves a mesenchymal to epithelial transition, in which cells develop and coordinate polarity through largely unknown mechanisms. The C. elegans pharynx, which is an epithelial tube in which cells polarize around a central lumen, provides a simple system with which to understand the coordination of epithelial polarity. We show that cell fate regulators cause pharyngeal precursor cells to group into a bilaterally symmetric, rectangular array of cells called the double plate. The double plate cells polarize with apical localization of the PAR-3 protein complex, then undergo apical constriction to form a cylindrical cyst. We show that laminin, but not other basement membrane components, orients the polarity of the double plate cells. Our results provide in vivo evidence that laminin has an early role in cell polarity that can be distinguished from its later role in basement membrane integrity.

SUBMITTER: Rasmussen JP

PROVIDER: S-EPMC3347693 | biostudies-literature | 2012 Jun

REPOSITORIES: biostudies-literature

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Laminin is required to orient epithelial polarity in the C. elegans pharynx.

Rasmussen Jeffrey P JP Reddy Sowmya Somashekar SS Priess James R JR

Development (Cambridge, England) 20120425 11

The development of many animal organs involves a mesenchymal to epithelial transition, in which cells develop and coordinate polarity through largely unknown mechanisms. The C. elegans pharynx, which is an epithelial tube in which cells polarize around a central lumen, provides a simple system with which to understand the coordination of epithelial polarity. We show that cell fate regulators cause pharyngeal precursor cells to group into a bilaterally symmetric, rectangular array of cells called ...[more]

PMID: 22535412

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Project description:During development, cell polarization is often coordinated to harmonize tissue patterning and morphogenesis. However, how extrinsic signals synchronize cell polarization is not understood. In Caenorhabditis elegans, most mitotic cells are polarized along the anterior-posterior axis and divide asymmetrically. Although this process is regulated by a Wnt-signaling pathway, Wnts functioning in cell polarity have been demonstrated in only a few cells. We analyzed how Wnts control cell polarity, using compound Wnt mutants, including animals with mutations in all five Wnt genes. We found that somatic gonadal precursor cells (SGPs) are properly polarized and oriented in quintuple Wnt mutants, suggesting Wnts are dispensable for the SGPs' polarity, which instead requires signals from the germ cells. Thus, signals from the germ cells organize the C. elegans somatic gonad. In contrast, in compound but not single Wnt mutants, most of the six seam cells, V1-V6 (which are epithelial stem cells), retain their polarization, but their polar orientation becomes random, indicating that it is redundantly regulated by multiple Wnt genes. In contrast, in animals in which the functions of three Wnt receptors (LIN-17, MOM-5, and CAM-1) are disrupted--the stem cells are not polarized and divide symmetrically--suggesting that the Wnt receptors are essential for generating polarity and that they function even in the absence of Wnts. All the seam cells except V5 were polarized properly by a single Wnt gene expressed at the cell's anterior or posterior. The ectopic expression of posteriorly expressed Wnts in an anterior region and vice versa rescued polarity defects in compound Wnt mutants, raising two possibilities: one, Wnts permissively control the orientation of polarity; or two, Wnt functions are instructive, but which orientation they specify is determined by the cells that express them. Our results provide a paradigm for understanding how cell polarity is coordinated by extrinsic signals.

Dataset Information

Laminin is required to orient epithelial polarity in the C. elegans pharynx.

Publications

Laminin is required to orient epithelial polarity in the C. elegans pharynx.

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