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First published online June 6, 2008
doi: 10.1242/10.1242/dev.020123

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Sonic hedgehog signalling from foregut endoderm patterns the avian nasal capsule

Laurence Benouaiche^1,2,*, Yorick Gitton^1,*, Christine Vincent³, Gérard Couly^1,2, and Giovanni Levi^1,

¹ Evolution des Régulations Endocriniennes, CNRS UMR 5166, Muséum National d'Histoire Naturelle, Paris, France.
² Service de Chirurgie Plastique, Maxillofaciale et Stomatologie, Hôpital Necker-Enfants Malades, 149, rue de Sèvres, 75015 Paris, France.
³ Biologie du Développement, CNRS UMR 7622, Université Pierre et Marie Curie, Paris, France.

View larger version (80K): [in this window] [in a new window]   Fig. 1. Endoderm zone I ablation prevents mesethmoid formation. (A-B') Frontal (A) and lateral (B) views of the cephalic skeleton of a chick embryo at 9 days (HH35) with corresponding drawings (A',B'), highlighting the elements of the nasal capsule: blue, mesethmoid (mes); red, ectethmoid (ect); green, infraorbital septum (is). Mc, Meckel's cartilage. (C) Schematic of the surgical procedure of endoderm zone I (EZ-I) ablation. I and II, endoderm zones I and II; r1-r8, rhombomeres 1 to 8. (D) Lateral view of the chondrochranium of a representative HH35 embryo in which EZ-I has been ablated at the 5-somite stage. (Upper inset) The same embryo before skeletal preparation. (Lower inset) Frontal view of the same embryo showing the normal size and shape of the ectethmoid. (D') Drawing corresponding to D, using the same colour code as above. Note the absence of the mesethmoid, whereas the ectethmoid and the infraorbital septum are still present.

View larger version (53K): [in this window] [in a new window]   Fig. 2. Supernumerary EZ-I graft in the cephalic region induces an ectopic mesethmoid. (A) Dorsal schematic view of 5-somite quail and chick embryos showing the dissection of EZ-I from a quail embryo and its transplantation into the lateral anterior mesenchyme of a chick embryo. (B) Ventral view at HH35 of the chondrochranium of an operated embryo. A supernumerary mesethmoid develops within the nasofrontal region perpendicularly to the host nasal capsule, which develops normally. (B') Drawing corresponding to B, with the same colour code as in Fig. 1. (C) Transplantation of a quail EZ-I into the mesenchyme of the presumptive first PA of a recipient chick embryo. (D) Lateral view of a skeletal preparation from a 12-day (HH38) operated embryo. A supernumerary mesethmoid can be seen developing within the maxillary arch under the native Meckel's cartilage. ect, ectethmoid; I and II, endoderm zones I and II; Mc, Meckel's cartilage; mes, mesethmoid; mes*, supernumerary mesethmoid.

View larger version (119K): [in this window] [in a new window]   Fig. 3. Shh is expressed in EZ-I and can rescue the mesethmoid loss induced by EZ-I ablation. (A-C) This HH14 chick embryo simultaneously received two quail grafts at the 5-somite stage. One was a homotopic substitution of the anterior neural crest and the other a supernumerary EZ-1 graft in the mesenchyme of the presumptive first PA. (A,B) Frontal section analysed by in situ hybridisation with a Shh probe, showing strong expression in the floor plate, in the notochord and in the grafted EZ-I (boxed). (C) Immunodetection of quail nuclei confirms the quail origin of the grafted endoderm and of the neighbouring CNCCs. (D) Dorsal schematic view of a 5-somite chick embryo showing the strategy of Shh rescue. After EZ-I ablation (Step 1), a Shh-loaded bead was implanted in the vacant region (Step 2). (E) Representative rescued embryo (HH35) showing almost normal development of the mesethmoid. (E') The same embryo before skeletal preparation showing the development of an upper beak. 1stpa, first pharyngeal arch; I and II, endoderm zones I and II; ect, ectethmoid; en*, supernumerary graft of EZ-I; fp, floor plate; Mc, Meckel's cartilage; mes, mesethmoid; n, neural tube; nt, notochord; QNCC, quail neural crest cells; r1-r8, rhombomeres 1-8.

View larger version (83K): [in this window] [in a new window]   Fig. 4. The Shh-Gli1 pathway mediates the interaction between EZ-I and CNCCs. (A) Explant assay. Fragments were dissected from EZ-I and anterior apical neural crest ridges (see also Fig. S1 in the supplementary material) and were either cultured alone or co-cultured. (Right panel) RT-PCR for Gapdh, Shh and Gli1 in untreated explants (-), after treatment with 10 µM cyclopamine (Cyc) or 10 µM Shh-N (Shh). The forehead of a 13-somite embryo was used as a control (whole head). Note the strong, cyclopamine-sensitive induction of Gli1 expression occurring only in the co-cultures. (B) CNCC-endoderm interaction. Frontal section of a 13-somite chicken head grafted with 5-somite quail CNCCs and processed for QCPN immunodetection (dark nuclei). (Inset) Post-migratory donor CNCCs (green) contact the ventral aspect of the host endoderm (red) triggering a mutual exchange of inductive signals (arrows). (C) Endodermal fate map indicating the induction by EZ-I of the mesethmoid cartilage (blue). The 150 µm EZ-I domain is adjacent to the EZ-II domain, which drives Meckel's cartilage morphogenesis (Couly et al., 2002). I and II, endoderm zones I and II; AIP, anterior intestinal portal; en, endoderm; Mc, Meckel's cartilage; mes, mesethmoid; n, neural tube; nc, neural crest; r1-r8, rhombomeres 1-8.

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