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The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling
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 refer...
Autores principales: | , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2013
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3635870/ https://www.ncbi.nlm.nih.gov/pubmed/23537390 http://dx.doi.org/10.1186/1741-7007-11-27 |
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author | Khonsari, Roman H Seppala, Maisa Pradel, Alan Dutel, Hugo Clément, Gaël Lebedev, Oleg Ghafoor, Sarah Rothova, Michaela Tucker, Abigael Maisey, John G Fan, Chen-Ming Kawasaki, Maiko Ohazama, Atsushi Tafforeau, Paul Franco, Brunella Helms, Jill Haycraft, Courtney J David, Albert Janvier, Philippe Cobourne, Martyn T Sharpe, Paul T |
author_facet | Khonsari, Roman H Seppala, Maisa Pradel, Alan Dutel, Hugo Clément, Gaël Lebedev, Oleg Ghafoor, Sarah Rothova, Michaela Tucker, Abigael Maisey, John G Fan, Chen-Ming Kawasaki, Maiko Ohazama, Atsushi Tafforeau, Paul Franco, Brunella Helms, Jill Haycraft, Courtney J David, Albert Janvier, Philippe Cobourne, Martyn T Sharpe, Paul T |
author_sort | Khonsari, Roman H |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-3635870 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2013 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-36358702013-04-26 The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling Khonsari, Roman H Seppala, Maisa Pradel, Alan Dutel, Hugo Clément, Gaël Lebedev, Oleg Ghafoor, Sarah Rothova, Michaela Tucker, Abigael Maisey, John G Fan, Chen-Ming Kawasaki, Maiko Ohazama, Atsushi Tafforeau, Paul Franco, Brunella Helms, Jill Haycraft, Courtney J David, Albert Janvier, Philippe Cobourne, Martyn T Sharpe, Paul T BMC Biol Research Article 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. BioMed Central 2013-03-28 /pmc/articles/PMC3635870/ /pubmed/23537390 http://dx.doi.org/10.1186/1741-7007-11-27 Text en Copyright © 2013 Khonsari et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Article Khonsari, Roman H Seppala, Maisa Pradel, Alan Dutel, Hugo Clément, Gaël Lebedev, Oleg Ghafoor, Sarah Rothova, Michaela Tucker, Abigael Maisey, John G Fan, Chen-Ming Kawasaki, Maiko Ohazama, Atsushi Tafforeau, Paul Franco, Brunella Helms, Jill Haycraft, Courtney J David, Albert Janvier, Philippe Cobourne, Martyn T Sharpe, Paul T The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling |
title | The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling |
title_full | The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling |
title_fullStr | The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling |
title_full_unstemmed | The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling |
title_short | The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling |
title_sort | buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3635870/ https://www.ncbi.nlm.nih.gov/pubmed/23537390 http://dx.doi.org/10.1186/1741-7007-11-27 |
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