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

Denker, Elsa; Bočina, Ivana; Jiang, Di

doi:10.1242/dev.092387

Cited by 36 publications

(49 citation statements)

References 49 publications

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“…2Ba,b). This organization is identical to that of the E-cadherin/Lgl localization (Denker et al, 2013), suggesting myosin is present in the same area as the E-cadherin. Furthermore, we found little overlap between myosin and ZO1 (Fig.…”

Section: Myosin Is Strongly Accumulated At the Lateral Domainmentioning

confidence: 53%

“…2Ba,b). They also contained ZO1, and the polarity protein Par6, which is normally co-localized with ZO1 at the apical/ lateral junction in normal notochord cells (Denker et al, 2013). Both proteins were concentrated into a single discrete patch (arrowheads in Fig.…”

Section: Increasing Myosin Activity Counteracts Lumen Expansionmentioning

confidence: 95%

“…The growing lumen is sealed by a de novoformed ring of tight junctions (ZO-1 positive) at the place where two apical domains juxtapose. As the lumen expands, the lateral domains reduce and the tight junction ring concurrently enlarges (Denker et al, 2013). Once the lumen pockets have reached a crucial size, they tilt in alternate directions as a result of extensive cell shape changes, and eventually contact each other to form a continuous lumen (Fig.…”

Section: Lumen Growth Is a Non-linear Processmentioning

confidence: 99%

“…The density of myosin became lower in the region away from the apical domain (region 2), and was undetectable in the distal region next to the basal domain, where only actin is present (region 3). As the lateral domain is the site of E-cadherin-positive adherens junctions and, more proximally, of ZO1-positive tight junctions at the apical/lateral transition (Denker et al, 2013;Dong et al, 2009), we examined in which specific junctional domain the MRLC is present. Co-expression analysis with the basolateral marker Lgl showed a tripartite expression pattern, with a myosin-only proximal domain, an Lgl/MRLC overlapping domain centrally and a distal Lgl-only domain (Fig.…”

Section: Myosin Is Strongly Accumulated At the Lateral Domainmentioning

confidence: 99%

“…The formation of an individual lumen represents the simplest model system for multicellular tube formation, as the lumen is produced and enclosed by only two cells. The surface of the lumen is thus interrupted by a ring of cell-cell junctions (apical/ lateral junction) connecting the apical membranes of the two adjacent cells (Denker and Jiang, 2012;Denker et al, 2013) (Fig. 1B).…”

Section: Introductionmentioning

confidence: 99%

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Regulation by a TGFβ-ROCK-actomyosin axis secures a non-linear lumen expansion that is essential for tubulogenesis

et al. 2015

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Regulation of lumen growth is crucial to ensure the correct morphology, dimensions and function of a tubular structure. How this is controlled is still poorly understood. During Ciona intestinalis notochord tubulogenesis, single extracellular lumen pockets grow between pairs of cells and eventually fuse into a continuous tube. Here, we show that lumen growth exhibits a lag phase, during which the luminal membranes continue to grow but the expansion of the apical/lateral junction pauses for ∼30 min. Inhibition of non-muscle myosin II activity abolishes this lag phase and accelerates expansion of the junction, resulting in the formation of narrower lumen pockets partially fusing into a tube of reduced size. Disruption of actin dynamics, conversely, causes a reversal of apical/lateral junction expansion, leading to a dramatic conversion of extracellular lumen pockets to intracellular vacuoles and a tubulogenesis arrest. The onset of the lag phase is correlated with a de novo accumulation of actin that forms a contractile ring at the apical/lateral junctions. This actin ring actively restricts the opening of the lumen in the transverse plane, allowing sufficient time for lumen growth via an osmotic process along the longitudinal dimension. The dynamics of lumen formation is controlled by the TGFβ pathway and ROCK activity. Our findings reveal a TGFβ-ROCKactomyosin contractility axis that coordinates lumen growth, which is powered by the dynamics of luminal osmolarity. The regulatory system may function like a sensor/checkpoint that responds to the change of luminal pressure and fine-tunes actomyosin contractility to effect proper tubulogenesis.

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Section: Myosin Is Strongly Accumulated At the Lateral Domainmentioning

confidence: 53%

Section: Increasing Myosin Activity Counteracts Lumen Expansionmentioning

confidence: 95%

Section: Lumen Growth Is a Non-linear Processmentioning

confidence: 99%

Section: Myosin Is Strongly Accumulated At the Lateral Domainmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Regulation by a TGFβ-ROCK-actomyosin axis secures a non-linear lumen expansion that is essential for tubulogenesis

et al. 2015

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Proteomic identification of intracellular vesicle trafficking and protein glycosylation requirements for lumen inflation in Ciona notochord

et al. 2023

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Lumen formation and inflation are crucial steps for tubular organ morphogenesis, yet the underling mechanism remains largely unrevealed. Here, we applied 4D proteomics to screen the lumenogenesis‐related proteins and revealed the biological pathways potentially that are involved in lumen inflation during notochord lumen formation in the ascidian Ciona savignyi. In total, 910 differentiated expressed proteins (DEPs) were identified before and after notochord lumen formation utilizing Mfuzz analysis. Those DEPs were grouped into four upregulated clusters based on their quantitative expression patterns; the functions of these proteins were enriched in protein metabolic and biosynthetic process, the establishment of localization, and vesicle‐mediated transport. We analyzed the vesicle trafficking cluster and focused on several vesicle transport hub proteins. In vivo function‐deficient experiments showed that mutation of vesicle transport proteins resulted in an abnormal lumen in notochord development, demonstrating the crucial role of intracellular trafficking for lumen formation. Moreover, abundant extracellular matrix proteins were identified, the majority of which were predicted to be glycosylated proteins. Inhibition of glycosylation markedly reduced the lumen expansion rate in notochord cells, suggesting that protein glycosylation is essential for lumenogenesis. Overall, our study provides an invaluable resource and reveals the crucial mechanisms in lumen formation and expansion.

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Asymmetric and Unequal Cell Divisions in Ascidian Embryos

Negishi

Nishida

2017

Results and Problems in Cell Differentiation

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Asymmetric cell division during embryogenesis contributes to cell diversity by generating daughter cells that adopt distinct developmental fates. In this chapter, we summarize current knowledge of three examples of asymmetric cell division occurring in ascidian early embryos: (1) Three successive cell divisions that are asymmetric in terms of cell fate and unequal in cell size in the germline lineage at the embryo posterior pole. A subcellular structure, the centrosome-attracting body (CAB), and maternal PEM mRNAs localized within it control both the positioning of the cell division planes and segregation of the germ cell fates. (2) Asymmetric cell divisions involving endoderm and mesoderm germ layer separation. Asymmetric partitioning of zygotically expressed mRNA for Not, a homeodomain transcription factor, promotes the mesoderm fate and suppresses the endoderm fate. This asymmetric partitioning is mediated by transient nuclear migration toward the mesodermal pole of the mother cell, where the mRNA is delivered. In this case, there is no special regulation of cleavage plane orientation. (3) Asymmetric cell divisions in the marginal region of the vegetal hemisphere. The directed extracellular FGF and ephrin signals polarize the mother cells, inducing distinct fates in a pair of daughter cells (nerve versus notochord and mesenchyme versus muscle). The directions of cell division are regulated and oriented but independently of FGF and ephrin signaling. In these examples, polarization of the mother cells is facilitated by localized maternal factors, by delivery of transcripts from the nucleus to one pole of each cell, and by directed extracellular signals. Two cellular processes-asymmetric fate allocation and orientation of the cell division plane-are coupled by a single factor in the first example, but these processes are regulated independently in the third example. Thus, various modes of asymmetric cell division operate even at the early developmental stages in this single type of organism.

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

Cited by 36 publications

References 49 publications

Regulation by a TGFβ-ROCK-actomyosin axis secures a non-linear lumen expansion that is essential for tubulogenesis

Regulation by a TGFβ-ROCK-actomyosin axis secures a non-linear lumen expansion that is essential for tubulogenesis

Proteomic identification of intracellular vesicle trafficking and protein glycosylation requirements for lumen inflation in Ciona notochord

Asymmetric and Unequal Cell Divisions in Ascidian Embryos

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