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Published 30 August 2004. doi:10.1083/jcb.200401077
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 166, Number 5, 673-684
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Article

 Sonic hedgehog regulates the proliferation, differentiation, and migration of enteric neural crest cells in gut

Ming Fu1, Vincent Chi Hang Lui1, Mai Har Sham2, Vassilis Pachnis3, and Paul Kwong Hang Tam1

1 Department of Surgery, The University of Hong Kong, Pokfulam, Hong Kong, HKSAR China
2 Department of Biochemistry, The University of Hong Kong, Pokfulam, Hong Kong, HKSAR China
3 Division of Molecular Neurobiology, Medical Research Council National Institute for Medical Research, The Ridgeway, Mill Hill, London NW7 1AA, England, UK

Address correspondence to Vincent Chi Hang Lui, Dept. of Surgery, The University of Hong Kong, 21 Sassoon Rd., Pokfulam, Hong Kong, HKSAR China. Tel.: (852) 28199607. Fax: (852) 28199621. email: vchlui{at}hkucc.hku.hk; or Paul Kwong Hang Tam, Tel.: (852) 28554850. Fax: (852) 28173155. email: paultam{at}hkucc.hku.hk

Enteric neural crest cells (NCCs) migrate and colonize the entire gut and proliferate and differentiate into neurons and glia of the enteric nervous system in vertebrate embryos. We have investigated the mitogenic and morphogenic functions of Sonic hedgehog (Shh) on enteric NCCs in cell and organ culture. Enteric NCCs expressed Shh receptor Patched and transcripts encoding the Shh signal transducer (Gli1). Shh promoted the proliferation and inhibited the differentiation of NCCs. The pro-neurogenic effect of glial cell line–derived neurotrophic factor (GDNF) on NCCs was abolished by Shh. In gut explants, NCCs migrated from the explants onto the adjacent substratum if GDNF was added, whereas addition of Shh abolished this migration. Neuronal differentiation and coalescence of neural crest–derived cells into myenteric plexuses in explants was repressed by the addition of Shh. Our data suggest that Shh controls the proliferation and differentiation of NCCs and modulates the responsiveness of NCCs toward GDNF inductions.

Key Words: Sonic hedgehog; enteric nervous system; neural plexuses; neurogenesis; glial cell-line derived neurotrophic factor

M. Fu and V.C.H. Lui contributed equally to this paper.

Abbreviations used in this paper: EDN3; endothelin 3; EDNRB; endothelin receptor-B; ENS, enteric nervous system; GDNF, glial cell line–derived neurotrophic factor; NCAM, neural cell adhesion molecule; NCC, neural crest cell; Ptc1, Patched; Ret, rearrangement during transformation; Shh, Sonic hedgehog; SMA, smooth muscle {alpha}-actin; TH, tyrosine hydroxylase; TUJ1, neuron-specific ß-tubulin.


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