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

BMC Biology

Research Article

Alan Pradel¹  John G Maisey¹  Gaël Clément²  Philippe Janvier²  Hugo Dutel³  Courtney J Haycraft⁴  Atsushi Ohazama⁵  Abigael Tucker⁵  Maiko Kawasaki⁵  Sarah Ghafoor⁵  Paul T Sharpe⁵  Maisa Seppala⁶  Martyn T Cobourne⁶  Michaela Rothova⁷  Roman H Khonsari⁸  Chen-Ming Fan⁹  Brunella Franco^1,10  Jill Helms^1,11  Paul Tafforeau^1,12  Oleg Lebedev^1,13  Albert David^1,14 

[1] American Museum of Natural History, New York City, NY, USA;CNRS-UMR, Muséum National d’Histoire Naturelle, 7207, Paris, France;CNRS-UMR, Muséum National d’Histoire Naturelle, 7207, Paris, France;CNRS-UMR, Muséum National d’Histoire Naturelle, 7179, Paris, France;College of Dental Medicine, Craniofacial Biology, Medical University of South Carolina, Carolina, SC, USA;Department of Craniofacial Development and Stem Cell Research, Comprehensive Biomedical Research Center, Dental Institute, King’s College London, London, UK;Department of Craniofacial Development and Stem Cell Research, Comprehensive Biomedical Research Center, Dental Institute, King’s College London, London, UK;Department of Orthodontics, Dental Institute, King’s College London, Guy’s Hospital, London, UK;Department of Craniofacial Development and Stem Cell Research, Comprehensive Biomedical Research Center, Dental Institute, King’s College London, London, UK;Institute of Experimental Medicine, Academy of Sciences of the Czech Republic, Prague, Czech Republic;Department of Craniofacial Development and Stem Cell Research, Comprehensive Biomedical Research Center, Dental Institute, King’s College London, London, UK;Service de Chirurgie Maxillo-Faciale, Centre Hospitalier Universitaire Hôtel-Dieu, Nantes, France;Department of Embryology, Carnegie Institution of Washington, Baltimore, USA;Department of Pediatrics, Università degli Studi di Napoli Federico II, Naples, Italy;Department of Surgery, Stanford University, Palo Alto, CA, USA;European Synchrotron Radiation Facility, Grenoble, France;Paleontological Institute of Russian Academy of Science, Moscow, Russian Federation;Service de Génétique Clinique, Centre Hospitalier Universitaire Hôtel-Dieu, Nantes, France;

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

DOI  :  10.1186/1741-7007-11-27

 received in 2012-12-25, accepted in 2013-03-19,  发布年份 2013

来源: Springer

【 摘 要 】

BackgroundThe 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.ResultsWe 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. Polarisfl/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.ConclusionThese 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.

【 授权许可】

CC BY   
© Khonsari et al.; licensee BioMed Central Ltd. 2013