Ciona intestinalis notochord as a new model to investigate the cellular and molecular mechanisms of tubulogenesis

Denker, Elsa; Jiang, Di

doi:10.1016/j.semcdb.2012.03.004

Cited by 41 publications

(47 citation statements)

References 67 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The most common bridge cell arrangement involves cells that have one apical surface; however, occasionally bridge cells exhibit two apical surfaces. Bipolar cells have also been observed during tubulogenesis in the Ciona notochord (Denker and Jiang, 2012). Although the mechanism by which a cell acquires two apical membranes is unknown, it is possible that the cells between lumens are unable to receive proper polarizing cues from the basement membrane.…”

Section: Discussionmentioning

confidence: 99%

Single continuous lumen formation in the zebrafish gut is mediated by smoothened-dependent tissue remodeling

et al. 2014

View full text Add to dashboard Cite

The formation of a single lumen during tubulogenesis is crucial for the development and function of many organs. Although 3D cell culture models have identified molecular mechanisms controlling lumen formation in vitro, their function during vertebrate organogenesis is poorly understood. Using light sheet microscopy and genetic approaches we have investigated single lumen formation in the zebrafish gut. Here we show that during gut development multiple lumens open and enlarge to generate a distinct intermediate, which consists of two adjacent unfused lumens separated by basolateral contacts. We observed that these lumens arise independently from each other along the length of the gut and do not share a continuous apical surface. Resolution of this intermediate into a single, continuous lumen requires the remodeling of contacts between adjacent lumens and subsequent lumen fusion. We show that lumen resolution, but not lumen opening, is impaired in smoothened (smo) mutants, indicating that fluid-driven lumen enlargement and resolution are two distinct processes. Furthermore, we show that smo mutants exhibit perturbations in the Rab11 trafficking pathway and demonstrate that Rab11-mediated trafficking is necessary for single lumen formation. Thus, lumen resolution is a distinct genetically controlled process crucial for single, continuous lumen formation in the zebrafish gut.

show abstract

Section: Discussionmentioning

confidence: 99%

Single continuous lumen formation in the zebrafish gut is mediated by smoothened-dependent tissue remodeling

et al. 2014

View full text Add to dashboard Cite

show abstract

“…The notochord cells, by contrast, are arranged as a flattened 'stack of coins' at the early tailbud stage. Later, as the tailbud matures, the notochord cells undergo a dramatic cell shape change, becoming elongated and cylindrical, followed by vacuolation and tubulogenesis (Denker and Jiang, 2012). The motor ganglion controls the swimming behavior of the tadpole and consists of five pairs of neurons.…”

Section: Discussionmentioning

confidence: 99%

Islet is a key determinant of ascidian palp morphogenesis

et al. 2014

View full text Add to dashboard Cite

The anterior-most ectoderm of ascidian larvae contains the adhesive papillae, or palps, which play an important role in triggering the metamorphosis of swimming tadpoles. In Ciona intestinalis, the palps consist of three conical protrusions within a field of thickened epithelium that form late in embryogenesis, as tailbuds mature into larvae. The palp protrusions express the LIM-homeodomain transcription factor Islet. Protrusion occurs through differential cell elongation, probably mediated by Islet, as we find that ectopic expression of Islet is sufficient to promote cell lengthening. FGF signaling is required for both Islet expression and palp morphogenesis. Importantly, we show that Islet expression can rescue the palpdeficient phenotype that results from inhibition of FGF signaling. We conclude that Islet is a key regulatory factor governing morphogenesis of the palps. It is conceivable that Islet is also essential for the cellular morphogenesis of placode-derived sensory neurons in vertebrates.

show abstract

“…The lumens between neighboring cells are connected through cell movement and cell shape changes, remarkably similar to what takes place in notochord (Herwig et al, 2011). Other cell types, including the Drosophila fusion cells during trachea morphogenesis and endothelial cells in vertebrate trunk intersegmental vessels during vasculogenesis involving intracellular vacuoles, also go through an transitory bipolar state, even though the tubulogenesis does not involve cord hollowing, but requires membrane fusion at the ends of the cells to create continuous lumen (Denker and Jiang, 2012). We therefore propose bipolarity, in the sense of having an axial symmetry and two apical domains at opposing ends, as a general principle to solve geometrical constraints during tubulogenesis involving a single file of cells.…”

Section: Bipolarity As a General Principle To Solve Geometrical Constmentioning

confidence: 88%

“…7A,AЈ), and unlike what is seen in non-chordates. It is interesting to note that at the later stage, during lumen connection, notochord cells will adopt another type of bipolarity by developing two leading edges, which crawl in opposite directions on the extracellular matrix, causing a bidirectional stretching of the cells, the retraction of the diametrically opposite cell extremities and the remodeling of cell junctions on both sides (Denker and Jiang, 2012).…”

Section: Research Articlementioning

confidence: 99%

“…We recently developed a new model for in vivo studies of tubulogenesis, the notochord of Ciona intestinalis, which provides a simple system to explore this process. Ciona notochord is composed of 40 large and geometrically identical cells that no longer divide, so that tubulogenesis involves only the remodeling of cell shape and tissue configuration (Denker and Jiang, 2012;Dong et al, 2009;Jiang and Smith, 2007). During development, notochord cells are also initially aligned in a single file.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Tubulogenesis in a simple cell cord requires the formation of bi-apical cells through two discrete Par domains

2013

Self Cite

View full text Add to dashboard Cite

SUMMARYApico-basal polarization is a crucial step in the de novo formation of biological tubes. In Ciona notochord, tubulogenesis occurs in a single file of cells in the absence of cell proliferation. This configuration presents a unique challenge for the formation of a continuous lumen. Here, we show that this geometric configuration is associated with a novel polarization strategy: the generation of bipolar epithelial cells possessing two apical/luminal domains instead of one, as in the conventional epithelium. At the molecular level, cells establish two discrete Par3/Par6/aPKC patches, and form two sets of tight junctions, in opposite points of the cells. The key molecule controlling the formation of both domains is Par3. Changing the position of the cells within the organ fundamentally changes their polarity and the number of apical domains they develop. These results reveal a new mechanism for tubulogenesis from the simplest cell arrangement, which occurs in other developmental contexts, including vertebrate vascular anastomosis.

show abstract

Ciona intestinalis notochord as a new model to investigate the cellular and molecular mechanisms of tubulogenesis

Cited by 41 publications

References 67 publications

Single continuous lumen formation in the zebrafish gut is mediated by smoothened-dependent tissue remodeling

Single continuous lumen formation in the zebrafish gut is mediated by smoothened-dependent tissue remodeling

Islet is a key determinant of ascidian palp morphogenesis

Tubulogenesis in a simple cell cord requires the formation of bi-apical cells through two discrete Par domains

Contact Info

Product

Resources

About