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

AUTHORS

Hockman DDorit , Burns AJAlan J , Schlosser GGerhard , Gates KPKeith P , Jevans BBenjamin , Mongera AAlessandro , Fisher SShannon , Unlu GGokhan , Knapik EWEla W , Kaufman CKCharles K , Mosimann CChristian , Zon LILeonard I , Lancman JJJoseph J , Dong PDSP Duc S , Lickert HHeiko , Tucker ASAbigail S , Baker CVClare Vh . eLife. 2017 4 7; 6().

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.