Epithelial morphogenesis, tubulogenesis and forces in organogenesis

Shaye, Daniel D.; Soto, Martha C.

doi:10.1016/bs.ctdb.2020.12.012

Cited by 12 publications

(15 citation statements)

References 218 publications

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“…Here we focus on studying the uncommon supernumerary excretory canals defect, as it offers the unique opportunity to investigate the mechanisms that restrict the number of cellular extensions. The excretory cell is an ideal model to address this question as its development has been characterised in detail 11,24,25 , and its outgrowth and guidance are regulated by pathways shared with neurons 4,23,26 .…”

Section: Resultsmentioning

confidence: 99%

“…Similarities in the cytoskeletal organisation exist between the growth cone of a developing neuron 11 and the tip of a growing canal, where actin and microtubules need to be tightly regulated for proper development 11,25 . CED-10/Rac and MIG-2/RhoG are two Rho-GTPases that regulate cytoskeletal organisation in numerous biological processes 10,11 . Of particular interest, they regulate the actin cytoskeleton downstream of the UNC-6/Netrin guidance pathways in the growth cone of axons 6,53 .…”

Section: Discussionmentioning

confidence: 99%

“…MIG-2/RHOG and CED-10/Rac are also required for proper extension outgrowth of other cells such as those of the excretory canal cell in C . elegans 11 . Besides their role in guidance, these regulators also modulate the cytoskeleton during the earliest phase of cell extension or axonal specification 12 .…”

Section: Introductionmentioning

confidence: 99%

“…MIG-2/RHOG and CED-10/Rac are two small Rho-GTPases members of the Rac-like GTPases subfamily that function in the UNC-6/Netrin guidance pathway, to regulate the growth cone's cytoskeleton dynamics 10 . MIG-2/RHOG and CED-10/Rac are also required for proper extension outgrowth of other cells such as those of the excretory canal cell in C. elegans 11 . Besides their role in guidance, these regulators also modulate the cytoskeleton during the earliest phase of cell extension or axonal specification 12 .…”

Section: Introductionmentioning

confidence: 99%

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Syndecan Regulates Cellular Morphogenesis in Cooperation with the Netrin Guidance Pathway and Rho-family GTPases

Dima¹,

Tahe²,

Chabi³

et al. 2022

Preprint

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The establishment of complex cell shapes is essential for specific cellular functions, and thus critical in animal development and physiology. Heparan sulfate proteoglycans (HSPGs) are conserved glycoproteins that regulate interactions between extracellular signals and their receptors, to orchestrate morphogenetic events and elicit cellular responses. Although HSPG-regulated pathways have been implicated in regulating the guidance of neuronal migrations, whether HSPGs regulate earlier aspects of cellular development that dictate cell shape remains unknown. HSPGs consist of a protein core (e.g., Syndecan, Perlecan, Glypican, etc.) with attached heparan sulfate (HS) glycosaminoglycan chains, which are synthesized by glycosyltransferases of the exostosin family. Using mutations in the two C. elegans HS glycosyltransferases genes, rib-1 and rib-2, we reveal that HSPGs control the number of cellular projections in the epithelial excretory canal cell, which can form more than its normal four canals in these mutants. We identify SDN-1/Syndecan as the key HSPG that regulates the number of excretory canal cell projections in a cell-autonomous manner. We also find that Syndecan and guidance receptors for Netrin function in the same pathway to restrict the number of cellular projections. Furthermore, we show that the formation of extra projections in the absence of Syndecan requires the conserved Rho-family GTPases CED-10/Rac and MIG-2/RhoG. Our findings not only contribute to understanding the roles of conserved HSPGs in cellular morphogenetic events, but also reveal the existence of an HSPG-regulated system operating to guarantee that a precise number of cellular projections is established during cell development. Given the evolutionary conservation of developmental mechanisms and the molecules implicated, this work provides information relevant to understanding the cellular and molecular bases of the development of precise cellular morphologies in varied cell types across animals.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Syndecan Regulates Cellular Morphogenesis in Cooperation with the Netrin Guidance Pathway and Rho-family GTPases

Dima¹,

Tahe²,

Chabi³

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Besides being a barrier, during mid-embryogenesis, it regulates morphogenetic processes like embryonic elongation ( Priess and Hirsh, 1986 ; Williams-Masson et al, 1997 ; Costa et al, 1998 ), cell and axon guidance ( Hedgecock et al, 1990 ), it secretes basement membrane material that separates it from underlying body wall muscles ( Francis and Waterston, 1991 ), and eliminates apoptotic cells and synapses via phagocytosis ( Robertson and Thomson, 1982 ; Chung et al, 2000 ). Importantly, epidermal cells provide the force that drives body elongation ( Priess and Hirsh, 1986 ; Shelton et al, 1999 ; Wissmann et al, 1999 ; Piekny et al, 2003 ; Gally et al, 2009 ; Vuong-Brender et al, 2016 ; Shaye and Soto, 2021 ). The different stages of embryonic elongation in C. elegans have been coined with names that reflect the overall shape or elongation progress ( Figure 1A ), while the invariantly numbered and positioned epidermal cells also have a specific nomenclature (also see Figure 1A ).…”

Section: Introductionmentioning

confidence: 99%

A Maternal-Effect Toxin Affects Epithelial Differentiation and Tissue Mechanics in Caenorhabditis elegans

Lehmann

Pohl

2021

Front. Cell Dev. Biol.

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Selfish genetic elements that act as post-segregation distorters cause lethality in non-carrier individuals after fertilization. Two post-segregation distorters have been previously identified in Caenorhabditis elegans, the peel-1/zeel-1 and the sup-35/pha-1 elements. These elements seem to act as modification-rescue systems, also called toxin/antidote pairs. Here we show that the maternal-effect toxin/zygotic antidote pair sup-35/pha-1 is required for proper expression of apical junction (AJ) components in epithelia and that sup-35 toxicity increases when pathways that establish and maintain basal epithelial characteristics, die-1, elt-1, lin-26, and vab-10, are compromised. We demonstrate that pha-1(e2123) embryos, which lack the antidote, are defective in epidermal morphogenesis and frequently fail to elongate. Moreover, seam cells are frequently misshaped and mispositioned and cell bond tension is reduced in pha-1(e2123) embryos, suggesting altered tissue material properties in the epidermis. Several aspects of this phenotype can also be induced in wild-type embryos by exerting mechanical stress through uniaxial loading. Seam cell shape, tissue mechanics, and elongation can be restored in pha-1(e2123) embryos if expression of the AJ molecule DLG-1/Discs large is reduced. Thus, our experiments suggest that maternal-effect toxicity disrupts proper development of the epidermis which involves distinct transcriptional regulators and AJ components.

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Context matters: Lessons in epithelial polarity from the Caenorhabditis elegans intestine and other tissues

Naturale¹,

Pickett²,

Feldman³

2023

Current Topics in Developmental Biology

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Epithelial morphogenesis, tubulogenesis and forces in organogenesis

Cited by 12 publications

References 218 publications

Syndecan Regulates Cellular Morphogenesis in Cooperation with the Netrin Guidance Pathway and Rho-family GTPases

Syndecan Regulates Cellular Morphogenesis in Cooperation with the Netrin Guidance Pathway and Rho-family GTPases

A Maternal-Effect Toxin Affects Epithelial Differentiation and Tissue Mechanics in Caenorhabditis elegans

Context matters: Lessons in epithelial polarity from the Caenorhabditis elegans intestine and other tissues

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