scholarly journals Embryonic origin and serial homology of gill arches and paired fins in the skate (Leucoraja erinacea)

2020 ◽  
Author(s):  
Victoria A. Sleight ◽  
J. Andrew Gillis
Keyword(s):  
Neural Crest ◽  
Cell Lineage ◽  
Body Plan ◽  
Lineage Tracing ◽  
Germ Layers ◽  
Axial Patterning ◽  
Serial Homology ◽  
Embryonic Origin ◽  
Dual Origin ◽  
Derivatives Of

AbstractPaired fins are a defining feature of the jawed vertebrate body plan, but their evolutionary origin remains unresolved. Gegenbaur proposed that paired fins evolved as gill arch serial homologues, but this hypothesis is now widely discounted, owing largely to the presumed distinct embryonic origins of these structures from mesoderm and neural crest, respectively. Here, we use cell lineage tracing to test the embryonic origin of the pharyngeal and paired fin skeleton in the skate (Leucoraja erinacea). We find that while the jaw and hyoid arch skeleton derive from neural crest, and the pectoral fin skeleton from mesoderm, the gill arches are of dual origin, receiving contributions from both germ layers. We propose that gill arches and paired fins are serially homologous as derivatives of a continuous, dual-origin mesenchyme with common skeletogenic competence, and that this serial homology accounts for their parallel anatomical organization and shared responses to axial patterning signals.

scholarly journals Embryonic origin and serial homology of gill arches and paired fins in the skate, Leucoraja erinacea

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Victoria A Sleight ◽  
J Andrew Gillis
Keyword(s):  
Neural Crest ◽  
Cell Lineage ◽  
Body Plan ◽  
Lineage Tracing ◽  
Germ Layers ◽  
Axial Patterning ◽  
Serial Homology ◽  
Embryonic Origin ◽  
Dual Origin ◽  
Derivatives Of

Paired fins are a defining feature of the jawed vertebrate body plan, but their evolutionary origin remains unresolved. Gegenbaur proposed that paired fins evolved as gill arch serial homologues, but this hypothesis is now widely discounted, owing largely to the presumed distinct embryonic origins of these structures from mesoderm and neural crest, respectively. Here, we use cell lineage tracing to test the embryonic origin of the pharyngeal and paired fin skeleton in the skate (Leucoraja erinacea). We find that while the jaw and hyoid arch skeleton derive from neural crest, and the pectoral fin skeleton from mesoderm, the gill arches are of dual origin, receiving contributions from both germ layers. We propose that gill arches and paired fins are serially homologous as derivatives of a continuous, dual-origin mesenchyme with common skeletogenic competence, and that this serial homology accounts for their parallel anatomical organization and shared responses to axial patterning signals.

scholarly journals Embryonic origin of the gnathostome vertebral skeleton

2017 ◽  
Vol 284 (1867) ◽  
pp. 20172121 ◽  
Author(s):  
Katharine E. Criswell ◽  
Michael I. Coates ◽  
J. Andrew Gillis
Keyword(s):  
Vertebral Column ◽  
Bone Matrix ◽  
Cell Lineage ◽  
Body Plan ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Paraxial Mesoderm ◽  
Teleost Fishes ◽  
Embryonic Origin

The vertebral column is a key component of the jawed vertebrate (gnathostome) body plan, but the primitive embryonic origin of this skeleton remains unclear. In tetrapods, all vertebral components (neural arches, haemal arches and centra) derive from paraxial mesoderm (somites). However, in teleost fishes, vertebrae have a dual embryonic origin, with arches derived from somites, but centra formed, in part, by secretion of bone matrix from the notochord. Here, we test the embryonic origin of the vertebral skeleton in a cartilaginous fish (the skate, Leucoraja erinacea ) which serves as an outgroup to tetrapods and teleosts. We demonstrate, by cell lineage tracing, that both arches and centra are somite-derived. We find no evidence of cellular or matrix contribution from the notochord to the skate vertebral skeleton. These findings indicate that the earliest gnathostome vertebral skeleton was exclusively of somitic origin, with a notochord contribution arising secondarily in teleosts.

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

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Dorit Hockman ◽  
Alan J Burns ◽  
Gerhard Schlosser ◽  
Keith P Gates ◽  
Benjamin Jevans ◽  
...  
Keyword(s):  
Neural Crest ◽  
Blood Vessels ◽  
Carotid Body ◽  
Lineage Tracing ◽  
Neuroendocrine Cells ◽  
Genetic Lineage ◽  
Glomus Cells ◽  
Evolutionary Origins ◽  
Embryonic Origin ◽  
Respiratory Reflexes

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.

scholarly journals Resegmentation is an ancestral feature of the gnathostome vertebral skeleton

2019 ◽  
Author(s):  
Katharine E. Criswell ◽  
J. Andrew Gillis
Keyword(s):  
Cell Lineage ◽  
Body Plan ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Teleost Fishes ◽  
Body Segment ◽  
The Relationship

AbstractThe vertebral skeleton is a defining feature of vertebrate animals. However, the mode of vertebral segmentation varies considerably between major lineages. In tetrapods, adjacent somite halves recombine to form a single vertebra through the process of “resegmentation”. However, in teleost fishes, there is considerable mixing between cells of the anterior and posterior somite halves, without clear resegmentation. To determine whether resegmentation is a tetrapod novelty, or an ancestral feature of jawed vertebrates, we tested the relationship between somites and vertebrae in a cartilaginous fish, the skate (Leucoraja erinacea). Using cell lineage tracing, we show that skate trunk vertebrae arise through tetrapod-like resegmentation, with anterior and posterior halves of each vertebra deriving from adjacent somites. We further show that tail vertebrae also arise through resegmentation, despite a duplication of the number of vertebrae per body segment. These findings resolve axial resegmentation as an ancestral feature of the jawed vertebrate body plan.

scholarly journals Neural crest lineage analysis: from past to future trajectory

Development ◽  
2020 ◽  
Vol 147 (20) ◽  
pp. dev193193 ◽  
Author(s):  
Weiyi Tang ◽  
Marianne E. Bronner
Keyword(s):  
Neural Crest ◽  
Cell Fate ◽  
Single Molecule ◽  
Cell Lineage ◽  
Neural Crest Cell ◽  
Cell Types ◽  
Lineage Tracing ◽  
Migration Routes ◽  
Developmental Potential ◽  
Lineage Analysis

ABSTRACTSince its discovery 150 years ago, the neural crest has intrigued investigators owing to its remarkable developmental potential and extensive migratory ability. Cell lineage analysis has been an essential tool for exploring neural crest cell fate and migration routes. By marking progenitor cells, one can observe their subsequent locations and the cell types into which they differentiate. Here, we review major discoveries in neural crest lineage tracing from a historical perspective. We discuss how advancing technologies have refined lineage-tracing studies, and how clonal analysis can be applied to questions regarding multipotency. We also highlight how effective progenitor cell tracing, when combined with recently developed molecular and imaging tools, such as single-cell transcriptomics, single-molecule fluorescence in situ hybridization and high-resolution imaging, can extend the scope of neural crest lineage studies beyond development to regeneration and cancer initiation.

scholarly journals Trunk neural crest origin of dermal denticles in a cartilaginous fish

2017 ◽  
Vol 114 (50) ◽  
pp. 13200-13205 ◽  
Author(s):  
J. Andrew Gillis ◽  
Els C. Alsema ◽  
Katharine E. Criswell
Keyword(s):  
Neural Crest ◽  
Cell Lineage ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Skeletal Tissue ◽  
Trunk Neural Crest ◽  
Neural Crest Origin ◽  
Cranial Neural Crest Cells

Cartilaginous fishes (e.g., sharks and skates) possess a postcranial dermal skeleton consisting of tooth-like “denticles” embedded within their skin. As with teeth, the principal skeletal tissue of dermal denticles is dentine. In the head, cranial neural crest cells give rise to the dentine-producing cells (odontoblasts) of teeth. However, trunk neural crest cells are generally regarded as nonskeletogenic, and so the embryonic origin of trunk denticle odontoblasts remains unresolved. Here, we use expression of FoxD3 to pinpoint the specification and emigration of trunk neural crest cells in embryos of a cartilaginous fish, the little skate (Leucoraja erinacea). Using cell lineage tracing, we further demonstrate that trunk neural crest cells do, in fact, give rise to odontoblasts of trunk dermal denticles. These findings expand the repertoire of vertebrate trunk neural crest cell fates during normal development, highlight the likely primitive skeletogenic potential of this cell population, and point to a neural crest origin of dentine throughout the ancestral vertebrate dermal skeleton.

Abstract 323: Loss of Gravity Impairs Cardiac Neural Crest Cell Lineage Development and Function

2016 ◽  
Vol 119 (suppl_1) ◽  
Author(s):  
Konstantinos E Hatzistergos ◽  
Krystalenia Valasaki ◽  
Zhijie Jiang ◽  
Lauro M Takeuchi ◽  
Wayne Balkan ◽  
...  
Keyword(s):  
Neural Crest ◽  
Molecular Mechanisms ◽  
Cell Lineage ◽  
Neural Crest Cell ◽  
Lineage Tracing ◽  
Embryoid Bodies ◽  
Egfp Expression ◽  
Cardiac Neural Crest ◽  
Induced Pluripotent ◽  
And Function

Introduction: A multitude of structural, haemodynamic and electromechanical cardiovascular disorders have been observed in humans following space-travel. These abnormalities are thought to emerge from transient alterations in autonomic nervous system (ANS). However, since the ANS is cardiac neural crest (CNC)-derived, whether microgravity-induced cardiomyopathies reflect CNC dysfunction, is unknown. Hypothesis: Impairment of CNCs underlies microgravity-induced cardiomyopathies. Methods: Myocardial explants from adult cKit CreERT2/+ ;IRG mice (n=5/group), as well as cKit CreERT2/+ ;IRG- derived (iPSC Kit-Cre ; n=6/group) and Wnt1-Cre;tdTomato -derived (iPSC Wnt1-Cre ; n=18/group) induced pluripotent stem cells, were cultured under static (SC) or simulated microgravity conditions (rotary cell-culture system; RCCS). Results: CNC lineage-tracing in cardiac explants illustrated that, compared to SC, RCCS abolished the pool of cKit + CNCs in adult hearts, indicated by quantitation of cKit CreERT2 - mediated EGFP expression ( p <0.05). Cardiogenesis modeling experiments with iPSC Kit-Cre yielded fewer beating EBs ( p =0.0005), and ~10-fold reduction in EGFP + cardiomyocytes ( p =0.01), in RCCS vs . SC. Microarray analyses suggested that RCCS-mediated alterations in BMP and Wnt/β-catenin pathways, downregulated ANS and CNC-related gene programs, and enhanced vasculogenic differentiation without affecting the expression of cardiac mesoderm-related genes. Differences were verified by quantitative PCR. Modeling CNC development in iPSC Wnt1-Cre further confirmed an RCCS-mediated dramatic impairment in development and function of CNCs, indicated by quantitation of tdTomato expression in day-10 and day-21 beating embryoid bodies ( p <0.0001). Intriguingly, the effect of RCCS in CNCs could be only partially rescued upon transfer to SC. Conclusions: Together these data indicate that microgravity negatively regulates the development and function of CNCs, thus partly explaining the cellular and molecular mechanisms of microgravity-induced cardiomyopathies. Moreover, these findings are expected to have important implications in space exploration, since they suggest an essential role for gravity in vertebrate development.

scholarly journals Resegmentation is an ancestral feature of the gnathostome vertebral skeleton

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Katharine E Criswell ◽  
J Andrew Gillis
Keyword(s):  
Cell Lineage ◽  
Body Plan ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Teleost Fishes ◽  
Body Segment ◽  
The Relationship

The vertebral skeleton is a defining feature of vertebrate animals. However, the mode of vertebral segmentation varies considerably between major lineages. In tetrapods, adjacent somite halves recombine to form a single vertebra through the process of ‘resegmentation’. In teleost fishes, there is considerable mixing between cells of the anterior and posterior somite halves, without clear resegmentation. To determine whether resegmentation is a tetrapod novelty, or an ancestral feature of jawed vertebrates, we tested the relationship between somites and vertebrae in a cartilaginous fish, the skate (Leucoraja erinacea). Using cell lineage tracing, we show that skate trunk vertebrae arise through tetrapod-like resegmentation, with anterior and posterior halves of each vertebra deriving from adjacent somites. We further show that tail vertebrae also arise through resegmentation, though with a duplication of the number of vertebrae per body segment. These findings resolve axial resegmentation as an ancestral feature of the jawed vertebrate body plan.

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