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

Autor: Gaël Clément, Oleg V. Lebedev, Alan Pradel, Courtney J. Haycraft, Paul T. Sharpe, Brunella Franco, Maisa Seppala, Jill A. Helms, Albert David, Philippe Janvier, Michaela Rothova, Roman Hossein Khonsari, Paul Tafforeau, Sarah Ghafoor, Hugo Dutel, Atsushi Ohazama, Chen-Ming Fan, John G. Maisey, Abigael Tucker, Martyn T. Cobourne
Přispěvatelé: Kings Coll London, Inst Dent, Comprehens Biomed Res Ctr, Dept Craniofacial Dev & Stem Cell Res, London WC2R 2LS, England, Kings Coll London, Guys Hosp, Inst Dent, Dept Orthodont, London WC2R 2LS, England, American Museum of Natural History (AMNH), Centre de recherche sur la Paléobiodiversité et les Paléoenvironnements (CR2P), Muséum national d'Histoire naturelle (MNHN)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Mécanismes adaptatifs : des organismes aux communautés, Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS), Russian Acad Sci, Inst Paleontol, Moscow V71, Russia, Acad Sci Czech Republic, Inst Expt Med, Prague, Czech Republic, Carnegie Institution for Science [Washington], European Synchrotron Radiation Facility (ESRF), Univ Naples Federico II, Dept Pediat, Naples, Italy, Stanford University, Medical University of South Carolina [Charleston] (MUSC), Hôtel-Dieu de Nantes, Khonsari, Rh, Seppala, M, Pradel, A, Dutel, H, Clément, G, Lebedev, O, Ghafoor, S, Rothova, M, Tucker, A, Maisey, Jg, Fan, Cm, Kawasaki, M, Ohazama, A, Tafforeau, P, Franco, Brunella, Helms, J, Haycraft, Cj, David, A, Janvier, P, Cobourne, Mt, Sharpe, Pt, Carnegie Institution for Science, University of Naples Federico II = Università degli studi di Napoli Federico II, Centre de Recherche en Paléontologie - Paris (CR2P), Muséum national d'Histoire naturelle (MNHN)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)
Jazyk: angličtina
Rok vydání: 2013
Předmět:
Pituitary gland
Coelacanth
Midline
Physiology
[SDV]Life Sciences [q-bio]
Cell Cycle Proteins
Ectoderm
Plant Science
Shh
Mice
Neural crest
0302 clinical medicine
Primary cilia
Structural Biology
Sonic hedgehog
[SDV.BDD]Life Sciences [q-bio]/Development Biology
ComputingMilieux_MISCELLANEOUS
Phylogeny
0303 health sciences
Agricultural and Biological Sciences(all)
Fossils
Endoderm
Fishes
Gene Expression Regulation
Developmental

Vertebrate
Anatomy
Hedgehog signaling pathway
medicine.anatomical_structure
Pituitary Gland
Vertebrates
embryonic structures
General Agricultural and Biological Sciences
Research Article
Signal Transduction
Biotechnology
animal structures
Buccohypophyseal canal
Biology
Extinction
Biological

GPI-Linked Proteins
Chondrichthyans
General Biochemistry
Genetics and Molecular Biology

03 medical and health sciences
Anterior pituitary
biology.animal
Notochord
medicine
Animals
Hedgehog Proteins
Cilia
Ecology
Evolution
Behavior and Systematics

030304 developmental biology
Mouth
Neuroectoderm
Biochemistry
Genetics and Molecular Biology(all)

Skull
Cell Biology
Knock-out mouse
Jaw
Mutation
biology.protein
030217 neurology & neurosurgery
Developmental Biology
Zdroj: BMC Biology
BMC Biology, BioMed Central, 2013, 11 (1), 15 p. ⟨10.1186/1741-7007-11-27⟩
'BMC Biology ', vol: 11, pages: 27-1-27-15 (2013)
BMC Biology, 2013, 11 (1), 15 p. ⟨10.1186/1741-7007-11-27⟩
BMC Biology, BioMed Central, 2013, 11 (1), ⟨10.1186/1741-7007-11-27⟩
ISSN: 1741-7007
Popis: 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. 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. 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.
Databáze: OpenAIRE