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

Nandor Nagy1, Csilla Barad2, Hannah K Graham3

  • 1Department of Pediatric Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA Department of Human Morphology and Developmental Biology, Faculty of Medicine, Semmelweis University, Budapest 1094, Hungary nagy.nandor@med.semmelweis-univ.hu.

Development (Cambridge, England)
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PubMed
Summary
This summary is machine-generated.

Epithelial Sonic hedgehog (Shh) signaling influences enteric nervous system (ENS) development by altering the gut microenvironment. Shh regulates neural crest cell migration and differentiation, impacting ENS formation and ganglia patterning.

Keywords:
ChickEnteric nervous systemEnteric neural crest cellsEpitheliumExtracellular matrixHirschsprung diseaseMousePatchedPtchQuailSonic hedgehog

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Area of Science:

  • Developmental biology
  • Neuroscience
  • Gastroenterology

Background:

  • The enteric nervous system (ENS) originates from neural crest cells migrating into the developing gut.
  • Epithelial-mesenchymal interactions are crucial for gut development, but their role in ENS formation is unclear.

Purpose of the Study:

  • To investigate the role of epithelial-derived Sonic hedgehog (Shh) signaling in regulating enteric nervous system (ENS) development.
  • To elucidate the mechanisms by which Shh influences neural crest cell behavior and gut microenvironment composition.

Main Methods:

  • Avian epithelial-mesenchymal recombination assays using hindgut mesenchyme and non-intestinal epithelium.
  • Manipulation of Shh signaling via cyclopamine, function-blocking antibodies, retroviral overexpression, and recombinant protein.
  • Analysis of gene expression (versican, collagen type IX, Gdnf) and cell behavior (proliferation, differentiation, migration).

Main Results:

  • Epithelial-mesenchymal recombinations with non-intestinal epithelium resulted in abnormal ganglia formation.
  • Shh inhibition led to large, ectopic ganglia, while Shh overexpression caused intestinal aganglionosis.
  • Shh modulated the expression of chondroitin sulfate proteoglycans, inhibited enteric neural crest-derived cell (ENCC) proliferation, promoted neuronal differentiation, and reduced Gdnf expression.

Conclusions:

  • Epithelial-derived Shh plays a critical, indirect role in ENS development.
  • Shh regulates the intestinal microenvironment, influencing neural crest cell migration, proliferation, and differentiation.
  • These findings highlight Shh as a key mediator of epithelial-mesenchymal interactions in ENS formation.