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

• Published in: eLife Vol. 6
• Main Authors: Hockman, Dorit, Burns, Alan J, Schlosser, Gerhard, Gates, Keith P, Jevans, Benjamin, Mongera, Alessandro, Fisher, Shannon, Unlu, Gokhan, Knapik, Ela W, Kaufman, Charles K, Mosimann, Christian, Zon, Leonard I, Lancman, Joseph J, Dong, P Duc S, Lickert, Heiko, Tucker, Abigail S, Baker, Clare Vh
• Format: Journal Article
• Language: English
• Published: England eLife Science Publications, Ltd 07.04.2017; eLife Sciences Publications Ltd; eLife Sciences Publications, Ltd
• Subjects: Amniotes; Animals; Anura; Biological Evolution; Biology; Blood vessels; Cameras; Carotid arteries; Carotid body; Cell fate; Cell Hypoxia; Cell Lineage; Danio rerio; Deficient mutant; Developmental Biology and Stem Cells; Embryos; Endoderm; Evolution; Fate maps; fate-mapping; Gene mapping; Genetics; Gills; Glomus cells; Health aspects; Homology; Hypotheses; Hypoxia; Lampreys; Medicine; Neural crest; Neuroendocrine Cells; Neuroepithelial Cells; Pharynx; Reflexes; Respiratory tract; sea lamprey (Petromyzon marinus); Serotonin; Software; Veins & arteries; Zebrafish; mouse; stem cells; chicken; neuroepithelial cells; endoderm; sea lamprey (Petromyzon marinus); developmental biology; neural crest; xenopus; carotid body; fate-mapping; zebrafish
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/elife.21231

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.