The shroom family proteins play broad roles in the morphogenesis of thickened epithelial sheets

Lee, Chanjae; Le, Minh Phuong; Wallingford, John B.

doi:10.1002/dvdy.21942

Cited by 52 publications

(57 citation statements)

References 27 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…In contrast to apical constriction, the mechanisms of lateral elongation are poorly understood. Shroom family members again are known to drive not only apical constriction but also lateral elongation (Lee et al, 2009;. The latter is thought to be caused by Shroom-driven accumulation of ␥-tubulin, a microtubule nucleating protein, at the apical surface of cells, although the precise mechanism of the accumulation has not been clarified.…”

Section: Discussionmentioning

confidence: 99%

Epithelial cell shape is regulated by Lulu proteins via myosin-II

Nakajima

Tanoue

2010

Journal of Cell Science

View full text Add to dashboard Cite

SummaryCell-shape change in epithelial structures is fundamental to animal morphogenesis. Recent studies identified myosin-II as the major generator of driving forces for cell-shape changes during morphogenesis. Lulu (Epb41l5) is a major regulator of morphogenesis, although the downstream molecular and cellular mechanisms remain obscure in mammals. In Drosophila and zebrafish, Lulu proteins were reported to negatively regulate Crumbs, an apical domain regulator, thus regulating morphogenesis. In this study, we show that mammalian Lulu activates myosin-II, thus regulating epithelial cell shape. In our experiments, Lulu expression in epithelial cells resulted in apical constriction and lateral elongation in the cells, accompanied by upregulation of myosin-II. The inhibition of myosin-II activity almost completely blocked this Lulu-driven cell-shape change. We further found that Rock participates in the myosin-II activation. Additionally, RNAi-mediated depletion of Lulu in epithelial cells resulted in disorganization of myosin-II and a concomitant loss of proper lateral domain organization in the cells. From these results, we propose that Lulu regulates epithelial cell shape by controlling myosin-II activity.

show abstract

Section: Discussionmentioning

confidence: 99%

Epithelial cell shape is regulated by Lulu proteins via myosin-II

Nakajima

Tanoue

2010

Journal of Cell Science

View full text Add to dashboard Cite

show abstract

“…The actin-binding protein Shroom3 has been shown to drive AC of epithelial cells in different biological systems by activating nonmuscle myosin Haigo et al, 2003;Hildebrand, 2005;Hildebrand and Soriano, 1999;Lee et al, 2009;Nishimura and Takeichi, 2008;Plageman et al, 2011;Plageman et al, 2010). We therefore decided to determine whether Shroom3 plays a role in the assembly of apically constricted rosettes in the zebrafish pLLP.…”

Section: Shroom3 Is Expressed In the Rosette-forming Region Of The Plmentioning

confidence: 99%

“…In vertebrates, the actin-binding protein Shroom3 has been reported to be involved in the regulation of apical constriction Haigo et al, 2003;Hildebrand, 2005;Hildebrand and Soriano, 1999;Nishimura and Takeichi, 2008;Plageman et al, 2011;Plageman et al, 2010). Shroom3 belongs to the Shroom family of proteins, which are characterized by conserved domains including a PDZ domain at their N-terminus, and two Apx/Shrm-specific domains, ASD1 and ASD2, separated by a poly-proline domain (Dietz et al, 2006;Hagens et al, 2006;Haigo et al, 2003;Hildebrand, 2005;Hildebrand and Soriano, 1999;Lee et al, 2009). The ASD1 domain mediates direct binding to actin but is not essential to the apical constriction activity of Shroom3.…”

Section: Introductionmentioning

confidence: 99%

Shroom3 is required downstream of FGF signalling to mediate proneuromast assembly in zebrafish

et al. 2012

View full text Add to dashboard Cite

SUMMARYDuring development, morphogenetic processes require a precise coordination of cell differentiation, cell shape changes and, often, cell migration. Yet, how pattern information is used to orchestrate these different processes is still unclear. During lateral line (LL) morphogenesis, a group of cells simultaneously migrate and assemble radially organized cell clusters, termed rosettes, that prefigure LL sensory organs. This process is controlled by Fibroblast growth factor (FGF) signalling, which induces cell fate changes, cell migration and cell shape changes. However, the exact molecular mechanisms induced by FGF activation that mediate these changes on a cellular level are not known. Here, we focus on the mechanisms by which FGFs control apical constriction and rosette assembly. We show that apical constriction in the LL primordium requires the activity of non-muscle myosin. We demonstrate further that shroom3, a well-known regulator of non-muscle myosin activity, is expressed in the LL primordium and that its expression requires FGF signalling. Using gain-and loss-of-function experiments, we demonstrate that Shroom3 is the main organizer of cell shape changes during rosette assembly, probably by coordinating Rho kinase recruitment and non-muscle myosin activation. In order to quantify morphogenesis in the LL primordium in an unbiased manner, we developed a unique trainable 'rosette detector'. We thus propose a model in which Shroom3 drives rosette assembly in the LL downstream of FGF in a Rho kinase-and non-muscle myosindependent manner. In conclusion, we uncovered the first mechanistic link between patterning and morphogenesis during LL sensory organ formation.

show abstract

“…Shroom3 is essential for cell shape changes during gut morphogenesis Shroom family proteins are known to be necessary and sufficient to drive cell shape changes in epithelial sheets, including apical constriction and apicobasal cell elongation (Haigo et al, 2003;Lee et al, 2009;Lee et al, 2007). However, the role of Shroom3 in controlling cell shape changes in non-neural tissues has not been explored in detail.…”

Section: Shroom3 Is Essential For Morphogenesis In the Developing Vermentioning

confidence: 99%

“…However, apical constriction and cell elongation are observed in several morphogenetically active epithelial tissues. Indeed, Shroom3 is expressed in several thickened epithelial sheets (Lee et al, 2009), but its function in these tissues has not been tested experimentally. Of particular interest is the gut, where complex changes in the thickness of cell sheets are important for morphogenesis (Chalmers and Slack, 1998;Davis et al, 2008;Muller et al, 2003;Reed et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Direct activation of Shroom3 transcription by Pitx proteins drives epithelial morphogenesis in the developing gut

et al. 2010

Self Cite

View full text Add to dashboard Cite

SUMMARYIndividual cell shape changes are essential for epithelial morphogenesis. A transcriptional network for epithelial cell shape change is emerging in Drosophila, but this area remains largely unexplored in vertebrates. The distinction is important as so far, key downstream effectors of cell shape change in Drosophila appear not to be conserved. Rather, Shroom3 has emerged as a central effector of epithelial morphogenesis in vertebrates, driving both actin-and microtubule-based cell shape changes. To date, the morphogenetic role of Shroom3 has been explored only in the neural epithelium, so the broad expression of this gene raises two important questions: what are the requirements for Shroom3 in non-neural tissues and what factors control Shroom3 transcription? Here, we show in Xenopus that Shroom3 is essential for cell shape changes and morphogenesis in the developing vertebrate gut and that Shroom3 transcription in the gut requires the Pitx1 transcription factor. Moreover, we show that Pitx proteins directly activate Shroom3 transcription, and we identify Pitx-responsive regulatory elements in the genomic DNA upstream of Shroom3. Finally, we show that ectopic expression of Pitx proteins is sufficient to induce Shroom3-dependent cytoskeletal reorganization and epithelial cell shape change. These data demonstrate new breadth to the requirements for Shroom3 in morphogenesis, and they also provide a cell-biological basis for the role of Pitx transcription factors in morphogenesis. More generally, these results provide a foundation for deciphering the transcriptional network that underlies epithelial cell shape change in developing vertebrates.

show abstract

The shroom family proteins play broad roles in the morphogenesis of thickened epithelial sheets

Cited by 52 publications

References 27 publications

Epithelial cell shape is regulated by Lulu proteins via myosin-II

Epithelial cell shape is regulated by Lulu proteins via myosin-II

Shroom3 is required downstream of FGF signalling to mediate proneuromast assembly in zebrafish

Direct activation of Shroom3 transcription by Pitx proteins drives epithelial morphogenesis in the developing gut

Contact Info

Product

Resources

About