Endoderm-derived Sonic hedgehog and mesoderm Hand2 expression are required for enteric nervous system development in zebrafish

Reichenbach, Bettina; Delalande, Jean-Marie; Kolmogorova, Ekaterina; Prier, Abigail; Nguyen, Tu; Smith, Chelsey M.; Holzschuh, Jochen; Shepherd, Iain T.

doi:10.1016/j.ydbio.2008.02.061

Cited by 77 publications

(84 citation statements)

References 113 publications

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“…Studies have demonstrated that endodermal Hh signaling is required for both the patterning and differentiation of the gut mesenchyme (Ramalho-Santos et al, 2000;Sukegawa et al, 2000;Reichenbach et al, 2008;Mao et al, 2010;Liu and Ngan, 2014), presumably through the regulation of the Notch signaling activity (Kim et al, 2011). In this study, we show that vENCCs participate in stomach patterning and differentiation through the regulation of Notch activity.…”

Section: Discussionsupporting

confidence: 63%

“…In this study, we show that vENCCs participate in stomach patterning and differentiation through the regulation of Notch activity. Interestingly, it has been shown that endodermal Hh signaling regulates ENS development (Ramalho-Santos et al, 2000;Sukegawa et al, 2000;Reichenbach et al, 2008;Mao et al, 2010;Liu and Ngan, 2014). Accordingly, vENCCs express the Hh receptor Patched and Hh signaling specifically regulates their proliferation, migration and differentiation (Fu et al, 2004;Reichenbach et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

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Enteric neural crest cells regulate vertebrate stomach patterning and differentiation

et al. 2015

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In vertebrates, the digestive tract develops from a uniform structure where reciprocal epithelial-mesenchymal interactions pattern this complex organ into regions with specific morphologies and functions. Concomitant with these early patterning events, the primitive GI tract is colonized by the vagal enteric neural crest cells (vENCCs), a population of cells that will give rise to the enteric nervous system (ENS), the intrinsic innervation of the GI tract. The influence of vENCCs on early patterning and differentiation of the GI tract has never been evaluated. In this study, we report that a crucial number of vENCCs is required for proper chick stomach development, patterning and differentiation. We show that reducing the number of vENCCs by performing vENCC ablations induces sustained activation of the BMP and Notch pathways in the stomach mesenchyme and impairs smooth muscle development.

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Section: Discussionsupporting

confidence: 63%

Section: Discussionmentioning

confidence: 99%

Enteric neural crest cells regulate vertebrate stomach patterning and differentiation

et al. 2015

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“…Reichenbach et al (2008) similarly found Ptc1 expressed by Phox2b-expressing ENCCs in zebrafish. By contrast, however, reporter mice expressing β-galactosidase driven by Ptc1, Gli1 or Gli2 showed no lacZ expression in ENCCs (Washington Smoak et al, 2005;Kolterud et al, 2009), suggesting that these Hh pathway genes are not expressed.…”

Section: Discussionmentioning

confidence: 72%

Sonic hedgehog controls enteric nervous system development by patterning the extracellular matrix

et al. 2015

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The enteric nervous system (ENS) develops from neural crest cells that migrate along the intestine, differentiate into neurons and glia, and pattern into two plexuses within the gut wall. Inductive interactions between epithelium and mesenchyme regulate gut development, but the influence of these interactions on ENS development is unknown. Epithelial-mesenchymal recombinations were constructed using avian hindgut mesenchyme and nonintestinal epithelium from the bursa of Fabricius. These recombinations led to abnormally large and ectopically positioned ganglia. We hypothesized that sonic hedgehog (Shh), a secreted intestinal epithelial protein not expressed in the bursa, mediates this effect. Inhibition of Shh signaling, by addition of cyclopamine or a function-blocking antibody, resulted in large, ectopic ganglia adjacent to the epithelium. Shh overexpression, achieved in ovo using Shhencoding retrovirus and in organ culture using recombinant protein, led to intestinal aganglionosis. Shh strongly induced the expression of versican and collagen type IX, whereas cyclopamine reduced expression of these chondroitin sulfate proteoglycans that are known to be inhibitory to neural crest cell migration. Shh also inhibited enteric neural crest-derived cell (ENCC) proliferation, promoted neuronal differentiation, and reduced expression of Gdnf, a key regulator of ENS formation. Ptc1 and Ptc2 were not expressed by ENCCs, and migration of isolated ENCCs was not inhibited by Shh protein. These results suggest that epithelial-derived Shh acts indirectly on the developing ENS by regulating the composition of the intestinal microenvironment.

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“…As hand2 is also expressed in neural crest derivatives and is required for the development of neural crest-derived neurons (Olden et al, 2008;Reichenbach et al, 2008), we concluded these cells are enteric neurons. Taken together, our observations confirm and extend previous reports that hand2-expressing bilateral LPM cells give rise to the iSMC layer surrounding the developing gut tube.…”

Section: Lateral Plate Mesoderm Gives Rise To Intestinal Smcsmentioning

confidence: 78%

An exclusive cellular and molecular network governs intestinal smooth muscle cell differentiation in vertebrates

et al. 2017

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Intestinal smooth muscle cells (iSMCs) are a crucial component of the adult gastrointestinal tract and support intestinal differentiation, peristalsis and epithelial homeostasis during development. Despite these crucial roles, the origin of iSMCs and the mechanisms responsible for their differentiation and function remain largely unknown in vertebrates. Here, we demonstrate that iSMCs arise from the lateral plate mesoderm (LPM) in a stepwise process. Combining pharmacological and genetic approaches, we show that TGFβ/Alk5 signaling drives the LPM ventral migration and commitment to an iSMC fate. The Alk5-dependent induction of zeb1a and foxo1a is required for this morphogenetic process: zeb1a is responsible for driving LPM migration around the gut, whereas foxo1a regulates LPM predisposition to iSMC differentiation. We further show that TGFβ, zeb1a and foxo1a are tightly linked together by miR-145. In iSMC-committed cells, TGFβ induces the expression of miR-145, which in turn is able to downregulate zeb1a and foxo1a. The absence of miR-145 results in only a slight reduction in the number of iSMCs, which still express mesenchymal genes but fail to contract. Together, our data uncover a cascade of molecular events that govern distinct morphogenetic steps during the emergence and differentiation of vertebrate iSMCs.

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Endoderm-derived Sonic hedgehog and mesoderm Hand2 expression are required for enteric nervous system development in zebrafish

Cited by 77 publications

References 113 publications

Enteric neural crest cells regulate vertebrate stomach patterning and differentiation

Enteric neural crest cells regulate vertebrate stomach patterning and differentiation

Sonic hedgehog controls enteric nervous system development by patterning the extracellular matrix

An exclusive cellular and molecular network governs intestinal smooth muscle cell differentiation in vertebrates

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