The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling

Roman H. Khonsari (1) , Maisa Seppala (2, 1) , Alan Pradel (3) , Hugo Dutel (4, 5) , Gael Clement (4) , Oleg Lebedev (6) , Sarah Ghafoor (1) , Michaela Rothova (7, 1) , Abigael Tucker (1) , John G. Maisey (3) , Chen-Ming Fan (8) , Maiko Kawasaki (1) , Atsushi Ohazama (1) , Paul Tafforeau (9) , Brunella Franco (10) , Jill Helms (11) , Courtney J. Haycraft (12) , Albert David (13) , Philippe Janvier (4) , Martyn T. Cobourne (2, 1) , Paul T. Sharpe (1)

1 Kings Coll London, Inst Dent, Comprehens Biomed Res Ctr, Dept Craniofacial Dev & Stem Cell Res, London WC2R 2LS, England
2 Kings Coll London, Guys Hosp, Inst Dent, Dept Orthodont, London WC2R 2LS, England
3 AMNH - American Museum of Natural History [New York, USA] = Musée américain d'histoire naturelle [New York, USA]
4 CR2P - Centre de recherche sur la Paléobiodiversité et les Paléoenvironnements
5 Mécanismes adaptatifs : des organismes aux communautés
6 Russian Acad Sci, Inst Paleontol, Moscow V71, Russia
7 Acad Sci Czech Republic, Inst Expt Med, Prague, Czech Republic
8 Carnegie Institution for Science
9 ESRF - European Synchrotron Radiation Facility
10 University of Naples Federico II = Università degli studi di Napoli Federico II
11 Stanford University
12 MUSC - Medical University of South Carolina [Charleston]
13 Hôtel-Dieu de Nantes

Background: The pituitary gland is formed by the juxtaposition of two tissues: neuroectoderm arising from the basal diencephalon, and oral epithelium, which invaginates towards the central nervous system from the roof of the mouth. The oral invagination that reaches the brain from the mouth is referred to as Rathke's pouch, with the tip forming the adenohypophysis and the stalk disappearing after the earliest stages of development. In tetrapods, formation of the cranial base establishes a definitive barrier between the pituitary and oral cavity; however, numerous extinct and extant vertebrate species retain an open buccohypophyseal canal in adulthood, a vestige of the stalk of Rathke's pouch. Little is currently known about the formation and function of this structure. Here we have investigated molecular mechanisms driving the formation of the buccohypophyseal canal and their evolutionary significance. Results: We show that Rathke's pouch is located at a boundary region delineated by endoderm, neural crest-derived oral mesenchyme and the anterior limit of the notochord, using CD1, R26R-Sox17-Cre and R26R-Wnt1-Cre mouse lines. As revealed by synchrotron X-ray microtomography after iodine staining in mouse embryos, the pouch has a lobulated three-dimensional structure that embraces the descending diencephalon during pituitary formation. Polaris(fl/fl); Wnt1-Cre, Ofd1(-/-) and Kif3a(-/-) primary cilia mouse mutants have abnormal sonic hedgehog (Shh) signaling and all present with malformations of the anterior pituitary gland and midline structures of the anterior cranial base. Changes in the expressions of Shh downstream genes are confirmed in Gas1(-/-) mice. From an evolutionary perspective, persistence of the buccohypophyseal canal is a basal character for all vertebrates and its maintenance in several groups is related to a specific morphology of the midline that can be related to modulation in Shh signaling. Conclusion: These results provide insight into a poorly understood ancestral vertebrate structure. It appears that the opening of the buccohypophyseal canal depends upon Shh signaling and that modulation in this pathway most probably accounts for its persistence in phylogeny

Mots clés: Buccohypophyseal canal; Chondrichthyans; Coelacanth; Endoderm; Knock-out mouse; Midline; Neural crest; Primary cilia; Shh

Domaines: Sciences du Vivant [q-bio]; Biologie du développement

Roman H. Khonsari, Maisa Seppala, Alan Pradel, Hugo Dutel, Gael Clement, et al.. The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling. BMC Biology, 2013, 11 (1), 15 p. ⟨10.1186/1741-7007-11-27⟩. ⟨hal-01572918⟩