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

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

doi:10.7554/elife.21231

Cited by 66 publications

(46 citation statements)

References 106 publications

(206 reference statements)

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“…Having revealed growth stem cells at the tip of each filament, we explored whether different cell types had a dedicated or a common stem cell during post-embryonic growth. Previous experiments in zebrafish on labelling cell populations at early embryonic stages revealed that neuro-endocrine cells (NECs) are derived from the endoderm (Hockman et al , 2017), while pillar cells have a neural crest origin (Mongera et al , 2013). We followed a holistic approach to address the potency of gill stem cells once the organ is formed, by using inducible ubiquitous drivers to potentially label all possible lineages within a gill filament.…”

Section: Resultsmentioning

confidence: 99%

“…Besides being the respiratory organ of fish, the gill has additional functions as a sensory and osmoregulatory organ (Sundin & Nilsson, 2002; Wilson & Laurent, 2002; Jonz & Nurse, 2005; Hockman et al , 2017). It contains oxygen sensing cells (Jonz et al , 2004), similar to those found in the mammalian carotid body although with a different lineage history (Hockman et al , 2017), and mitochondrial rich cells (MRCs) (Wilson & Laurent, 2002) that regulate ion uptake and excretion and are identified by a distinctive Na+, K+, ATPase activity. Other cell types include pavement cells (respiratory cells of the gills), pillar cells (structural support for lamellae), globe cells (mucous secretory cells), chondrocytes (skeleton of the filaments) and vascular cells.…”

Section: Introductionmentioning

confidence: 99%

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Hierarchical Stem Cell Topography Splits Growth and Homeostatic Functions in the Fish Gill

Stolper¹,

Ambrosio²,

Danciu³

et al. 2018

Preprint

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1While lower vertebrates contain adult stem cells (aSCs) that maintain homeostasis and drive un-2 exhaustive organismal growth, mammalian aSCs display mainly the homeostatic function. 3Understanding aSC-driven growth is of paramount importance to promote organ regeneration and 4 prevent tumor formation in mammals. Here we present a clonal approach to address common or 5 dedicated populations of aSCs for homeostasis and growth. Our functional assays on medaka gills 6 demonstrate the existence of separate homeostatic and growth aSCs, which are clonal but differ in 7 their topology. While homeostatic aSCs are fixed, embedded in the tissue, growth aSCs locate at the 8 expanding peripheral zone. Modifications in tissue architecture can convert the homeostatic zone 9 into a growth zone, indicating a leading role for the physical niche defining stem cell output. We 10 hypothesize that physical niches are main players to restrict aSCs to a homeostatic function in 11 animals with a fixed adult size.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Hierarchical Stem Cell Topography Splits Growth and Homeostatic Functions in the Fish Gill

Stolper¹,

Ambrosio²,

Danciu³

et al. 2018

Preprint

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“…Our reporter and lineage tracing data documents a close developmental relationship between endoderm and the LPM. Expression of the key vertebrate endoderm gene sox17 demarcates prospective endoderm progenitors also in zebrafish Sakaguchi et al, 2006), as evident by the exclusive endoderm lineage-labeling with sox17:creERT2 ( Fig S1C) (Hockman et al, 2017). We detected sox17/drl reporter double-positive cells throughout gastrulation that begin to separate from each other from tailbud stage (Fig 2A-D).…”

Section: The Lpm As Early Established Specialized Mesodermmentioning

confidence: 73%

A conserved regulatory program drives emergence of the lateral plate mesoderm

Hess

Nieuwenhuize

et al. 2018

Preprint

Self Cite

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Abstract:Cardiovascular cell lineages emerge with kidney, smooth muscle, and limb skeleton progenitors from the lateral plate mesoderm (LPM). How the LPM emerges during development and how it has evolved to form key lineages of the vertebrate body plan remain unknown. Here, we captured LPM formation by transgenic in toto imaging and lineage tracing using the first pan-LPM enhancer element from the zebrafish gene draculin (drl). drl LPM enhancer-based reporters are specifically active in LPM-corresponding territories of several chordate species, uncovering a universal LPM-specific gene program. Distinct from other mesoderm, we identified EomesA, FoxH1, and MixL1 with BMP/Nodal-controlled Smad activity as minimally required factors to drive drl-marked LPM formation. Altogether, our work provides a developmental and mechanistic framework for LPM emergence and the in vitro differentiation of cardiovascular cell types. Our findings suggest that the LPM may represent an ancient cell fate domain that predates ancestral vertebrates.. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/261115 doi: bioRxiv preprint first posted online Feb. 7, 2018; 2 Main Text:Following gastrulation, mesoderm in vertebrates is classically described to partition into axial, paraxial, and lateral domains (Gurdon, 1995). The ventrally forming lateral plate mesoderm (LPM) is composed of highly mobile cells and is mainly defined by its position adjacent to the somite-forming paraxial mesoderm (Hatada and Stern, 1994). Transplantation and lineage tracing experiments in several species have shown that the LPM contains progenitor cells of the circulatory system, smooth muscle lineages, the kidneys (often demarcated as dedicated intermediate mesoderm), and the limb anlagen (Chal and Pourquié, 2017; Gurdon, 1995; Takasato and Little, 2015). Several transcription factors including Hand1/2, Tbx5, Osr1, FoxF1, Prrx1, Mesp1, and Etv2 are expressed in LPM territories and play overlapping roles in cell fate determination (Chal and Pourquié, 2017;Davidson and Zon, 2004; Takasato and Little, 2015), albeit not always with conserved function (Yabe et al., 2016). Anterior-to-posterior expression domains of select transcription factors including Tbx1/10 and Hand are conserved in lampreys and even in the basal cephalochordate amphioxus that lacks major LPM-derived organ systems (Onimaru et al., 2011). These observations raise the possibility of the existence of an ancient upstream program that delineates the prospective LPM domain.In zebrafish, the LPM emerges from the ventral half of the embryo and becomes readily detectable as a patchwork of bilateral gene expression domains at the end of gastrulation (Davidson and Zon, 2004). hand2 expression marks in the anterior LPM (ALPM) the heart field and pectoral fin precursors, and a lateral-most domain within the posterior LPM (PLPM) (Perens et al., 2016; Yelon et al., 2000), wh...

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“…We also captured a cluster marked by Mpz and Plp1 , which are expressed in Schwann cells derived from the neural crest (Dyachuk et al, 2014;Espinosa-Medina et al, 2014;Feltri et al, 1999), as well as a small cluster distinguished by Snap25 , Ascl1 , Chga , which are molecular signatures for neuroendocrine cells (Nec) present in the adult mouse trachea (Montoro et al, 2018;Plasschaert et al, 2018) (Figures 1C and S1G). These Nec express transcription factors Phox2a and Phox2b required for cell fate specification in the parasympathetic ganglia ( Figure S1G) (Dyachuk et al, 2014;Espinosa-Medina et al, 2014), indicating that trachea Nec may originate from a lineage different from the pulmonary Nec found in the vertebrate lung (Hockman et al, 2017).…”

Section: Molecular Taxonomy Of Mesenchymal Cells Of the Developing Momentioning

confidence: 99%

Single Cell RNAseq Reveals A Critical Role of Chloride Channels in Airway Development

He¹,

et al. 2019

Preprint

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Word count: 154 SUMMARYThe conducting airway forms a protective mucosal barrier and is the primary target of airway disorders. To better understand how airway developmental programs are established to support air breathing and barrier functions, we constructed a single-cell atlas of the human and mouse developing trachea. In this study, we uncover hitherto unrecognized heterogeneity of cell states with distinct differentiation programs and immune features of the developing airway. In addition, we find ubiquitous expression of CFTR and ANO1/TMEM16A chloride channels in the embryonic airway epithelium. We show that genetic inactivation of TMEM16A leads to airway defects commonly seen in cystic fibrosis patients with deficient CFTR, alters the differentiation trajectory of airway basal progenitors, and results in mucus cell hyperplasia and aberrant epithelial antimicrobial expression. Together, our study illuminates conserved developmental features of the mammalian airway and implicates chloride homeostasis as a key player in regulating mucosal barrier formation and function relevant to early onset airway diseases.

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

Cited by 66 publications

References 106 publications

Hierarchical Stem Cell Topography Splits Growth and Homeostatic Functions in the Fish Gill

Hierarchical Stem Cell Topography Splits Growth and Homeostatic Functions in the Fish Gill

A conserved regulatory program drives emergence of the lateral plate mesoderm

Single Cell RNAseq Reveals A Critical Role of Chloride Channels in Airway Development

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