Evolution of the hypoxia-sensitive cells involved in amniote respiratory reflexes
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.
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.
Reviewing Editor
- Robb Krumlauf, Stowers Institute for Medical Research, United States
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.
Metrics
-
- 2,935
- Page views
-
- 643
- Downloads
-
- 43
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Developmental Biology
A growing body of evidence suggests that cell division and basement membrane invasion are mutually exclusive cellular behaviors. How cells switch between proliferative and invasive states is not well understood. Here, we investigated this dichotomy in vivo by examining two cell types in the developing Caenorhabditis elegans somatic gonad that derive from equipotent progenitors, but exhibit distinct cell behaviors: the post-mitotic, invasive anchor cell and the neighboring proliferative, non-invasive ventral uterine (VU) cells. We show that the fates of these cells post-specification are more plastic than previously appreciated and that levels of NHR-67 are important for discriminating between invasive and proliferative behavior. Transcription of NHR-67 is downregulated following post-translational degradation of its direct upstream regulator, HLH-2 (E/Daughterless) in VU cells. In the nuclei of VU cells, residual NHR-67 protein is compartmentalized into discrete punctae that are dynamic over the cell cycle and exhibit liquid-like properties. By screening for proteins that colocalize with NHR-67 punctae, we identified new regulators of uterine cell fate maintenance: homologs of the transcriptional co-repressor Groucho (UNC-37 and LSY-22), as well as the TCF/LEF homolog POP-1. We propose a model in which the association of NHR-67 with the Groucho/TCF complex suppresses the default invasive state in non-invasive cells, which complements transcriptional regulation to add robustness to the proliferative-invasive cellular switch in vivo.
-
- Chromosomes and Gene Expression
- Developmental Biology
Imaging experiments reveal the complex and dynamic nature of the transcriptional hubs associated with Notch signaling.