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Elife. 2017 Apr 7;6. pii: e21231. doi: 10.7554/eLife.21231.

Evolution of the hypoxia-sensitive cells involved in amniote respiratory reflexes.

Author information

1
Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, United Kingdom.
2
Stem Cells and Regenerative Medicine, UCL Great Ormond Street Institute of Child Health, London, United Kingdom.
3
School of Natural Sciences, National University of Ireland, Galway, Ireland.
4
Human Genetics Program, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, United States.
5
Department of Mechanical Engineering, University of California, California NanoSystem Institute, Santa Barbara, United States.
6
Department of Pharmacology and Experimental Therapeutics, Boston University School of Medicine, Boston, United States.
7
Department of Medicine, Division of Genetic Medicine, Vanderbilt University Medical Center, Nashville, United States.
8
Department of Medicine, Division of Oncology, Washington University School of Medicine, St. Louis, United States.
9
Institute of Molecular Life Sciences, University of Zürich, Zürich, Switzerland.
10
Children's Hospital Boston, Howard Hughes Medical Institute, Harvard Medical School, Boston, United States.
11
Institute of Diabetes and Regeneration Research, Helmholtz Zentrum München, Neuherberg, Germany.
12
Department of Craniofacial Development and Stem Cell Biology, King's College London, London, United Kingdom.
13
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom.

Abstract

The evolutionary origins of the hypoxia-sensitive cells that trigger amniote respiratory reflexes - carotid body glomus cells, and 'pulmonary neuroendocrine cells' (PNECs) - are obscure. Homology has been proposed between glomus cells, which are neural crest-derived, and the hypoxia-sensitive 'neuroepithelial cells' (NECs) of fish gills, whose embryonic origin is unknown. NECs have also been likened to PNECs, which differentiate in situ within lung airway epithelia. Using genetic lineage-tracing and neural crest-deficient mutants in zebrafish, and physical fate-mapping in frog and lamprey, we find that NECs are not neural crest-derived, but endoderm-derived, like PNECs, whose endodermal origin we confirm. We discover neural crest-derived catecholaminergic cells associated with zebrafish pharyngeal arch blood vessels, and propose a new model for amniote hypoxia-sensitive cell evolution: endoderm-derived NECs were retained as PNECs, while the carotid body evolved via the aggregation of neural crest-derived catecholaminergic (chromaffin) cells already associated with blood vessels in anamniote pharyngeal arches.

KEYWORDS:

carotid body; chicken; developmental biology; endoderm; fate-mapping; mouse; neural crest; neuroepithelial cells; sea lamprey (Petromyzon marinus); stem cells; xenopus; zebrafish

PMID:
28387645
PMCID:
PMC5438250
DOI:
10.7554/eLife.21231
[Indexed for MEDLINE]
Free PMC Article

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