Evolution of the hypoxia-sensitive cells involved in amniote respiratory reflexes
- University of Oxford, United Kingdom
- UCL Great Ormond Street Institute of Child Health, United Kingdom
- National University of Ireland, Ireland
- Sanford Burnham Prebys Medical Discovery Institute, United States
- University of California, California NanoSystem Institute, United States
- Boston University School of Medicine, United States
- Vanderbilt University Medical Center, United States
- Washington University School of Medicine, United States
- University of Zürich, Switzerland
- Howard Hughes Medical Institute, Harvard Medical School, United States
- Helmholtz Zentrum München, Germany
- King's College London, United Kingdom
- University of 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.
Article and author information
Author details
Funding
Wellcome (086804/Z/08/Z)
- Dorit Hockman
Wellcome (102889/Z/13/Z)
- Abigail S Tucker
National Institute of Dental and Craniofacial Research (R01-DE018477)
- Ela W Knapik
National Institute of Diabetes and Digestive and Kidney Diseases (1DP2DK098092)
- P Duc S Dong
Human Frontier Science Program (Long-Term Fellowship)
- Christian Mosimann
Helmholtz-Gemeinschaft (Helmholtz Portfolio Theme 'Metabolic Dysfunction and Common Disease')
- Heiko Lickert
Helmoltz Alliance (Imaging and Curing Environmental Metabolic Disease)
- Heiko Lickert
German Center for Diabetes Research
- Heiko Lickert
National Institutes of Health (R01-HL092217)
- Ela W Knapik
National Institute of Dental and Craniofacial Research (R21-DE021509)
- Shannon Fisher
Zebrafish Initiative of the Vanderbilt University Venture Capital Fund
- Ela W Knapik
Vanderbilt International Scholar Program (Graduate Student Scholarship)
- Gokhan Unlu
Swiss National Science Foundation (Advanced Postdoctoral Fellowship and Professorship)
- Christian Mosimann
Cambridge Trusts (Graduate Student Scholarship)
- Dorit Hockman
Cambridge Philosophical Society (Graduate Student Scholarship)
- Dorit Hockman
Oppenheimer Memorial Trust (Graduate Student Scholarship)
- Dorit Hockman
Trinity College Oxford (Junior Research Fellowship)
- Dorit Hockman
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Robb Krumlauf, Stowers Institute for Medical Research, United States
Ethics
Animal experimentation: Experiments using Tg(-4.9sox10:creERT2);Tg(βactin:loxP-SuperStop-loxP-DsRed) zebrafish were conducted in compliance with the regulations of the Regierungspräsidium Tübingen and the Max Planck Society. Experiments using all other zebrafish lines were conducted according to protocols approved by the Institutional Animal Care and Use Committees in facilities accredited by the Association for Assessment and Accreditation of Laboratory Animal Care International (AAALAC).Experiments using Xenopus laevis were conducted in accordance with the UK Animals (Scientific Procedures) Act 1986, with appropriate personal and project licences in place where necessary.Experiments using sea lamprey (Petromyzon marinus) were conducted according to protocols approved by the California Institute of Technology Institutional Animal Care and Use Committee.Experiments using transgenic mice were conducted in accordance with the UK Animals (Scientific Procedures) Act 1986, with appropriate personal and project licences in place.Experiments using chicken (Gallus gallus domesticus) embryos were conducted in accordance with the UK Animals (Scientific Procedures) Act 1986, with appropriate personal and project licences in place where necessary.
Version history
- Received: September 3, 2016
- Accepted: April 7, 2017
- Accepted Manuscript published: April 7, 2017 (version 1)
- Accepted Manuscript updated: April 11, 2017 (version 2)
- Version of Record published: May 19, 2017 (version 3)
Copyright
© 2017, Hockman et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Evolution of the hypoxia-sensitive cells involved in amniote respiratory reflexes
eLife 6:e21231.
https://doi.org/10.7554/eLife.21231
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