Gene tracing analysis reveals the contribution of neural crest‐derived cells in pituitary development

The anterior pituitary originates from the adenohypophyseal placode. Both the preplacode region and neural crest (NC) derive from subdivision of the neural border region, and further individualization of the placode domain is established by a reciprocal interaction between placodal precursors and NC...

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Published inJournal of anatomy Vol. 230; no. 3; pp. 373 - 380
Main Authors Ueharu, Hiroki, Yoshida, Saishu, Kikkawa, Takako, Kanno, Naoko, Higuchi, Masashi, Kato, Takako, Osumi, Noriko, Kato, Yukio
Format Journal Article
LanguageEnglish
Published England Wiley Subscription Services, Inc 01.03.2017
John Wiley and Sons Inc
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Abstract The anterior pituitary originates from the adenohypophyseal placode. Both the preplacode region and neural crest (NC) derive from subdivision of the neural border region, and further individualization of the placode domain is established by a reciprocal interaction between placodal precursors and NC cells (NCCs). It has long been known that NCCs are present in the adenohypophysis as interstitial cells. A recent report demonstrated that NCCs also contribute to the formation of pericytes in the developing pituitary. Here, we attempt to further clarify the role of NCCs in pituitary development using P0‐Cre/EGFP reporter mice. Spatiotemporal analyses revealed that GFP‐positive NCCs invaded the adenohypophysis in a stepwise manner. The first wave was detected on mouse embryonic day 9.5 (E9.5), when the pituitary primordium begins to be formed by adenohypophyseal placode cells; the second wave occurred on E14.5, when vasculogenesis proceeds from Atwell's recess. Finally, fate tracing of NCCs demonstrated that NC‐derived cells in the adenohypophysis terminally differentiate into all hormone‐producing cell lineages as well as pericytes. Our data suggest that NCCs contribute to pituitary organogenesis and vasculogenesis in conjunction with placode‐derived pituitary stem/progenitor cells.
AbstractList The anterior pituitary originates from the adenohypophyseal placode. Both the preplacode region and neural crest ( NC ) derive from subdivision of the neural border region, and further individualization of the placode domain is established by a reciprocal interaction between placodal precursors and NC cells ( NCC s). It has long been known that NCC s are present in the adenohypophysis as interstitial cells. A recent report demonstrated that NCC s also contribute to the formation of pericytes in the developing pituitary. Here, we attempt to further clarify the role of NCC s in pituitary development using P0‐Cre/ EGFP reporter mice. Spatiotemporal analyses revealed that GFP ‐positive NCC s invaded the adenohypophysis in a stepwise manner. The first wave was detected on mouse embryonic day 9.5 (E9.5), when the pituitary primordium begins to be formed by adenohypophyseal placode cells; the second wave occurred on E14.5, when vasculogenesis proceeds from Atwell's recess. Finally, fate tracing of NCC s demonstrated that NC ‐derived cells in the adenohypophysis terminally differentiate into all hormone‐producing cell lineages as well as pericytes. Our data suggest that NCC s contribute to pituitary organogenesis and vasculogenesis in conjunction with placode‐derived pituitary stem/progenitor cells.
The anterior pituitary originates from the adenohypophyseal placode. Both the preplacode region and neural crest (NC) derive from subdivision of the neural border region, and further individualization of the placode domain is established by a reciprocal interaction between placodal precursors and NC cells (NCCs). It has long been known that NCCs are present in the adenohypophysis as interstitial cells. A recent report demonstrated that NCCs also contribute to the formation of pericytes in the developing pituitary. Here, we attempt to further clarify the role of NCCs in pituitary development using P0-Cre/EGFP reporter mice. Spatiotemporal analyses revealed that GFP-positive NCCs invaded the adenohypophysis in a stepwise manner. The first wave was detected on mouse embryonic day 9.5 (E9.5), when the pituitary primordium begins to be formed by adenohypophyseal placode cells; the second wave occurred on E14.5, when vasculogenesis proceeds from Atwell's recess. Finally, fate tracing of NCCs demonstrated that NC-derived cells in the adenohypophysis terminally differentiate into all hormone-producing cell lineages as well as pericytes. Our data suggest that NCCs contribute to pituitary organogenesis and vasculogenesis in conjunction with placode-derived pituitary stem/progenitor cells.
The anterior pituitary originates from the adenohypophyseal placode. Both the preplacode region and neural crest (NC) derive from subdivision of the neural border region, and further individualization of the placode domain is established by a reciprocal interaction between placodal precursors and NC cells (NCCs). It has long been known that NCCs are present in the adenohypophysis as interstitial cells. A recent report demonstrated that NCCs also contribute to the formation of pericytes in the developing pituitary. Here, we attempt to further clarify the role of NCCs in pituitary development using P0-Cre/EGFP reporter mice. Spatiotemporal analyses revealed that GFP-positive NCCs invaded the adenohypophysis in a stepwise manner. The first wave was detected on mouse embryonic day 9.5 (E9.5), when the pituitary primordium begins to be formed by adenohypophyseal placode cells; the second wave occurred on E14.5, when vasculogenesis proceeds from Atwell's recess. Finally, fate tracing of NCCs demonstrated that NC-derived cells in the adenohypophysis terminally differentiate into all hormone-producing cell lineages as well as pericytes. Our data suggest that NCCs contribute to pituitary organogenesis and vasculogenesis in conjunction with placode-derived pituitary stem/progenitor cells.The anterior pituitary originates from the adenohypophyseal placode. Both the preplacode region and neural crest (NC) derive from subdivision of the neural border region, and further individualization of the placode domain is established by a reciprocal interaction between placodal precursors and NC cells (NCCs). It has long been known that NCCs are present in the adenohypophysis as interstitial cells. A recent report demonstrated that NCCs also contribute to the formation of pericytes in the developing pituitary. Here, we attempt to further clarify the role of NCCs in pituitary development using P0-Cre/EGFP reporter mice. Spatiotemporal analyses revealed that GFP-positive NCCs invaded the adenohypophysis in a stepwise manner. The first wave was detected on mouse embryonic day 9.5 (E9.5), when the pituitary primordium begins to be formed by adenohypophyseal placode cells; the second wave occurred on E14.5, when vasculogenesis proceeds from Atwell's recess. Finally, fate tracing of NCCs demonstrated that NC-derived cells in the adenohypophysis terminally differentiate into all hormone-producing cell lineages as well as pericytes. Our data suggest that NCCs contribute to pituitary organogenesis and vasculogenesis in conjunction with placode-derived pituitary stem/progenitor cells.
Author Kikkawa, Takako
Kanno, Naoko
Osumi, Noriko
Kato, Yukio
Ueharu, Hiroki
Higuchi, Masashi
Kato, Takako
Yoshida, Saishu
AuthorAffiliation 4 Department of Life Science School of Agriculture Meiji University Kawasaki Kanagawa Japan
1 Division of Life Science Graduate School of Agriculture Meiji University Kawasaki Kanagawa Japan
2 Institute for Reproduction and Endocrinology Meiji University Kawasaki Kanagawa Japan
3 Department of Developmental Neuroscience Center for Translational and Advanced Animal Research Tohoku University Graduate School of Medicine Sendai Miyagi Japan
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Keywords SOX2
pituitary development
PROP1
neural crest cell
stem/progenitor cell
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2016 The Authors. Journal of Anatomy published by John Wiley & Sons Ltd on behalf of Anatomical Society.
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Snippet The anterior pituitary originates from the adenohypophyseal placode. Both the preplacode region and neural crest (NC) derive from subdivision of the neural...
The anterior pituitary originates from the adenohypophyseal placode. Both the preplacode region and neural crest ( NC ) derive from subdivision of the neural...
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SubjectTerms Animals
Embryo, Mammalian
Immunohistochemistry
Mice
Mice, Transgenic
Models, Animal
Neural Crest - growth & development
neural crest cell
Organogenesis - physiology
Original
pituitary development
Pituitary Gland - embryology
PROP1
Rodents
SOX2
stem/progenitor cell
Title Gene tracing analysis reveals the contribution of neural crest‐derived cells in pituitary development
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fjoa.12572
https://www.ncbi.nlm.nih.gov/pubmed/28026856
https://www.proquest.com/docview/1868949957
https://www.proquest.com/docview/1853347852
https://www.proquest.com/docview/1881769055
https://pubmed.ncbi.nlm.nih.gov/PMC5314385
Volume 230
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