CDON contributes to Hedgehog-dependent patterning and growth of the developing limb

Echevarría-Andino, Martha L.; Franks, Nicole E.; Schrader, Hannah E.; Hong, Mingi; Krauss, Robert M.; Allen, Benjamin L.

doi:10.1016/j.ydbio.2022.09.011

Cited by 8 publications

(9 citation statements)

References 66 publications

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“…Gas1 mutant embryos display genetic background-dependent phenotypes in other tissues during development (Allen et al, 2007; Echevarria-Andino and Allen, 2020; Echevarria-Andino et al, 2022; Martinelli and Fan, 2007a; Seppala et al, 2007; Seppala et al, 2014). Thus, we collected kidneys from wildtype (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…However, the successful development of conditional alleles for both Cdon and Gas1 (Bae et al, 2020; Jin et al, 2015) provides an opportunity to assess their combined contribution in the kidney mesenchyme. These will be particularly informative experiments since Gas1 deletion does not completely abrogate HH pathway activity during mesonephros development, and since a role for Cdon in HH-dependent digit specification was only revealed in a Gas1;Boc null background (Echevarria-Andino et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

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Hedgehog-dependent and Hedgehog-independent roles for Growth Arrest Specific 1 in mammalian kidney morphogenesis

Franks,

Allen

2024

Preprint

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Growth arrest specific 1 (GAS1) is a key regulator of mammalian embryogenesis, best known for its role in Hedgehog (HH) signaling, but with additional described roles in the FGF, RET, and NOTCH pathways. Previous work indicated a later role for GAS1 in kidney development through FGF pathway modulation. Here, we demonstrate that GAS1 is essential for both mesonephrogenesis and metanephrogenesis- most notably, Gas1 deletion in mice results in renal agenesis in a genetic background-dependent fashion. Mechanistically, GAS1 promotes mesonephrogenesis in a HH-dependent fashion, performing a unique co-receptor function, while promoting metanephrogenesis in a HH-independent fashion, acting as a putative secreted RET co-receptor. Our data indicate that Gas1 deletion leads to renal agenesis through a transient reduction in metanephric mesenchyme proliferation- a phenotype that can be rescued by exogenous RET pathway stimulation. Overall, this study indicates that GAS1 contributes to early kidney development through the integration of multiple different signaling pathways.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Hedgehog-dependent and Hedgehog-independent roles for Growth Arrest Specific 1 in mammalian kidney morphogenesis

Franks,

Allen

2024

Preprint

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“…The role of Cdon in organ development and function had been reported in many literatures, including the role in neural differentiation, migration and survival (Jeong et al, 2014; Kim et al, 2023; Powell et al, 2015; Uluca et al, 2022; Wang et al, 2017), cardiac remodeling and fibrosis (Jeong et al, 2017) and myoblast fusion (Castiglioni et al, 2018). More recently, in zebrafish cdon was reported being involved in trunk neural crest cell migration and slow-twitch muscle development (Lencer et al, 2023) and limb growth (Echevarria-Andino et al, 2023). While in more early stage whether it plays a critical role in organ LR patterning is not reported.…”

Section: Discussionmentioning

confidence: 99%

Cdonis required for organ Left-Right patterning via regulating DFCs migration and the sequential ciliogenesis

Deng,

Chang,

et al. 2024

Preprint

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Cdon and boc are members of the cell adhesion molecule subfamily III Ig/fibronectin. Although they were reported to be involved in muscle and neural development at late developmental stage, while their early roles in embryonic development are unknown. Here we discovered that zebrafish cdon but not boc was expressed in dorsal forerunner cells (DFCs) and epitheliums of Kupffer's vesicle (KV), implying the possible role of cdon in organ LR patterning. Further data showed that the liver and heart LR patterning was disturbed in cdon morphants and cdon mutants. Mechanically, we found that cdon loss of function led to dispersed DFCs migration, smaller KV and defective ciliogenesis, which resulting in randomized Nodal/spaw signaling and the sequential organ LR patterning defect. Finally, predominant distribution of a cdon MO in DFCs led to defects in DFCs migration, KV morphogenesis/ciliogenesis, Nodal/spaw signaling and organ LR asymmetry, being similar to those in cdon morphants and cdon-/- embryos, indicating a cell-autonomous role of cdon in regulating KV formation and ciliogenesis during LR patterning. In conclusion, our data demonstrated that, during gastrulation stage and early somitogenesis stage, cdon is required for proper DFCs migration, KV formation and ciliogenesis, thus playing an important role in setting up organ LR asymmetry.

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“…Cooperation between Gas1 and Cdon was not observed during limb development (19), even though they are expressed in overlapping domains in the limb (62, 63). Recently, it has been shown that embryonic Cdon deletion does not affect HH signaling; however, when combined with Gas1 deletion, it leads to the elimination of HH signaling (60). Co-expression of Gas1 and Cdon in FILIF along with simultaneous reduction of HH signaling suggests the latter antagonistic roles may be dependent on the concurrent presence of Gas1 .…”

Section: Discussionmentioning

confidence: 99%

Distinct expression patterns of Hedgehog signaling components In mouse gustatory system during postnatal tongue development and adult homeostasis

Kumari,

Franks,

et al. 2023

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It is well established that the Hedgehog (HH) pathway regulates embryonic development of anterior tongue taste fungiform papilla (FP) and the posterior circumvallate (CVP) and foliate (FOP) taste papillae, and taste organ maintenance and regeneration in adults. However, there are knowledge gaps in determining HH signaling regulation in postnatal taste organ differentiation and maturation. Importantly, the HH transcription factors GLI1, GLI2 and GLI3 have not been investigated in early postnatal stages; and, the receptors PTCH1, GAS1, CDON and HHIP, required to either drive HH pathway activation or antagonism, remain unexplored. UsinglacZreporter mouse models, we mapped expression of the HH ligand SHH, receptors, and transcription factors in FP, CVP and FOP in early and late postnatal and adult stages. In adults we also studied the soft palate, and the geniculate and trigeminal ganglia which extend afferent fibers to the anterior tongue.ShhandGas1are the only components that were consistently expressed within taste buds of all three papillae and the soft palate. In the first postnatal week, we observed a broad expression of HH signaling components in FP and adjacent, non-taste filiform (FILIF) papillae in epithelium or stroma and tongue muscles. Remarkably, we observed elimination ofGli1in FILIF andGas1in muscles, and downregulation ofPtch1in lingual epithelium and ofCdon,Gas1andHhipin stroma from late postnatal stage. Further, HH receptor expression patterns in CVP and FOP epithelium differed from anterior FP. Among all the components, only known positive regulators of HH signaling, SHH,Ptch1,Gli1andGli2, were expressed in the ganglia. Our studies emphasize differential regulation of HH signaling in distinct postnatal developmental periods and in anterior versus posterior taste organs, and lay the foundation for functional studies to understand the roles of numerous HH signaling components in postnatal tongue development.

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CDON contributes to Hedgehog-dependent patterning and growth of the developing limb

Cited by 8 publications

References 66 publications

Hedgehog-dependent and Hedgehog-independent roles for Growth Arrest Specific 1 in mammalian kidney morphogenesis

Hedgehog-dependent and Hedgehog-independent roles for Growth Arrest Specific 1 in mammalian kidney morphogenesis

Cdonis required for organ Left-Right patterning via regulating DFCs migration and the sequential ciliogenesis

Distinct expression patterns of Hedgehog signaling components In mouse gustatory system during postnatal tongue development and adult homeostasis

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