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

Dorit Hockman, Alan J. Burns, Gerhard Schlosser, Keith P. Gates, Benjamin Jevans, Alessandro Mongera, Shannon Fisher, Gokhan Unlu, Ela W. Knapik, Charles K. Kaufman, Christian Mosimann, Leonard I. Zon, Joseph J. Lancman, P. Duc S. Dong, Heiko Lickert, Abigail S. Tucker, Clare V.H. Baker

Research output: Contribution to journalArticlepeer-review

34 Scopus citations

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.

Original languageEnglish
Article numbere21231
JournaleLife
Volume6
DOIs
StatePublished - Apr 7 2017

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