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

TY - JOUR

T1 - The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling

AU - Khonsari, Roman H.

AU - Seppala, Maisa

AU - Pradel, Alan

AU - Dutel, Hugo

AU - Clement, Gael

AU - Lebedev, Oleg

AU - Ghafoor, Sarah

AU - Rothova, Michaela

AU - Tucker, Abigael

AU - Maisey, John G.

AU - Fan, Chen-Ming

AU - Kawasaki, Maiko

AU - Ohazama, Atsushi

AU - Tafforeau, Paul

AU - Franco, Brunella

AU - Helms, Jill

AU - Haycraft, Courtney J.

AU - David, Albert

AU - Janvier, Philippe

AU - Cobourne, Martyn T.

AU - Sharpe, Paul T.

PY - 2013/3/28

Y1 - 2013/3/28

N2 - 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.

AB - 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.

KW - Buccohypophyseal canal

KW - Chondrichthyans

KW - Coelacanth

KW - Endoderm

KW - Knock-out mouse

KW - Midline

KW - Neural crest

KW - Primary cilia

KW - Shh

KW - PITUITARY-GLAND DEVELOPMENT

KW - PRIMARY CILIA

KW - CRANIAL BASE

KW - DEVELOPMENTAL BIOLOGY

KW - CRE RECOMBINASE

KW - EVOLUTION

KW - ORIGINS

KW - BRAINCASE

KW - ENDODERM

KW - GROWTH

U2 - 10.1186/1741-7007-11-27

DO - 10.1186/1741-7007-11-27

M3 - Article

SN - 1741-7007

VL - 11

JO - BMC Biology

JF - BMC Biology

M1 - 27

ER -