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Morphogenesis and morphometric scaling of lung airway development follows phylogeny in chicken, quail, and duck embryos

BACKGROUND: New branches within the embryonic chicken lung form via apical constriction, in which epithelial cells in the primary bronchus become trapezoidal in shape. These branches form at precise locations along the primary bronchus that scale relative to the size of the organ. Here, we examined...

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Autores principales: Tzou, Daniel, W. Spurlin, James, Pavlovich, Amira L., Stewart, Carolyn R., Gleghorn, Jason P., Nelson, Celeste M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4882856/
https://www.ncbi.nlm.nih.gov/pubmed/27239263
http://dx.doi.org/10.1186/s13227-016-0049-3
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author Tzou, Daniel
W. Spurlin, James
Pavlovich, Amira L.
Stewart, Carolyn R.
Gleghorn, Jason P.
Nelson, Celeste M.
author_facet Tzou, Daniel
W. Spurlin, James
Pavlovich, Amira L.
Stewart, Carolyn R.
Gleghorn, Jason P.
Nelson, Celeste M.
author_sort Tzou, Daniel
collection PubMed
description BACKGROUND: New branches within the embryonic chicken lung form via apical constriction, in which epithelial cells in the primary bronchus become trapezoidal in shape. These branches form at precise locations along the primary bronchus that scale relative to the size of the organ. Here, we examined the extent to which this scaling relationship and branching mechanism are conserved within lungs of three species of birds. FINDINGS: Analyzing the development of embryonic lungs from chicken, quail, and duck, as well as lungs explanted and cultured ex vivo, revealed that the patterns of branching are remarkably conserved. In particular, secondary bronchi form at identical positions in chicken and quail, the patterns of which are indistinguishable, consistent with the close evolutionary relationship of these two species. In contrast, secondary bronchi form at slightly different positions in duck, the lungs of which are significantly larger than those of chicken and quail at the same stage of development. Confocal analysis of fixed specimens revealed that each secondary bronchus forms by apical constriction of the dorsal epithelium of the primary bronchus, a morphogenetic mechanism distinct from that used to create branches in mammalian lungs. CONCLUSIONS: Our findings suggest that monopodial branching off the primary bronchus is driven by apical constriction in lungs of chicken, quail, and duck. The relative positions at which these branches form are also conserved relative to the evolutionary relationship of these species. It will be interesting to determine whether these mechanisms hold in more distant species of birds, and why they differ so significantly in mammals.
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spelling pubmed-48828562016-05-28 Morphogenesis and morphometric scaling of lung airway development follows phylogeny in chicken, quail, and duck embryos Tzou, Daniel W. Spurlin, James Pavlovich, Amira L. Stewart, Carolyn R. Gleghorn, Jason P. Nelson, Celeste M. EvoDevo Short Report BACKGROUND: New branches within the embryonic chicken lung form via apical constriction, in which epithelial cells in the primary bronchus become trapezoidal in shape. These branches form at precise locations along the primary bronchus that scale relative to the size of the organ. Here, we examined the extent to which this scaling relationship and branching mechanism are conserved within lungs of three species of birds. FINDINGS: Analyzing the development of embryonic lungs from chicken, quail, and duck, as well as lungs explanted and cultured ex vivo, revealed that the patterns of branching are remarkably conserved. In particular, secondary bronchi form at identical positions in chicken and quail, the patterns of which are indistinguishable, consistent with the close evolutionary relationship of these two species. In contrast, secondary bronchi form at slightly different positions in duck, the lungs of which are significantly larger than those of chicken and quail at the same stage of development. Confocal analysis of fixed specimens revealed that each secondary bronchus forms by apical constriction of the dorsal epithelium of the primary bronchus, a morphogenetic mechanism distinct from that used to create branches in mammalian lungs. CONCLUSIONS: Our findings suggest that monopodial branching off the primary bronchus is driven by apical constriction in lungs of chicken, quail, and duck. The relative positions at which these branches form are also conserved relative to the evolutionary relationship of these species. It will be interesting to determine whether these mechanisms hold in more distant species of birds, and why they differ so significantly in mammals. BioMed Central 2016-05-26 /pmc/articles/PMC4882856/ /pubmed/27239263 http://dx.doi.org/10.1186/s13227-016-0049-3 Text en © The Author(s) 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Short Report
Tzou, Daniel
W. Spurlin, James
Pavlovich, Amira L.
Stewart, Carolyn R.
Gleghorn, Jason P.
Nelson, Celeste M.
Morphogenesis and morphometric scaling of lung airway development follows phylogeny in chicken, quail, and duck embryos
title Morphogenesis and morphometric scaling of lung airway development follows phylogeny in chicken, quail, and duck embryos
title_full Morphogenesis and morphometric scaling of lung airway development follows phylogeny in chicken, quail, and duck embryos
title_fullStr Morphogenesis and morphometric scaling of lung airway development follows phylogeny in chicken, quail, and duck embryos
title_full_unstemmed Morphogenesis and morphometric scaling of lung airway development follows phylogeny in chicken, quail, and duck embryos
title_short Morphogenesis and morphometric scaling of lung airway development follows phylogeny in chicken, quail, and duck embryos
title_sort morphogenesis and morphometric scaling of lung airway development follows phylogeny in chicken, quail, and duck embryos
topic Short Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4882856/
https://www.ncbi.nlm.nih.gov/pubmed/27239263
http://dx.doi.org/10.1186/s13227-016-0049-3
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