scholarly journals Thyroid hormone regulates distinct paths to maturation in pigment cell lineages

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Lauren M Saunders ◽  
Abhishek K Mishra ◽  
Andrew J Aman ◽  
Victor M Lewis ◽  
Matthew B Toomey ◽  
...  
Keyword(s):  
Thyroid Hormone ◽  
Neural Crest ◽  
Developmental Trajectories ◽  
Pigment Cell ◽  
Cell Lineage ◽  
Population Expansion ◽  
Cell Types ◽  
Pigment Cells ◽  
Stripe Pattern ◽  
Yellow Orange

Thyroid hormone (TH) regulates diverse developmental events and can drive disparate cellular outcomes. In zebrafish, TH has opposite effects on neural crest derived pigment cells of the adult stripe pattern, limiting melanophore population expansion, yet increasing yellow/orange xanthophore numbers. To learn how TH elicits seemingly opposite responses in cells having a common embryological origin, we analyzed individual transcriptomes from thousands of neural crest-derived cells, reconstructed developmental trajectories, identified pigment cell-lineage specific responses to TH, and assessed roles for TH receptors. We show that TH promotes maturation of both cell types but in distinct ways. In melanophores, TH drives terminal differentiation, limiting final cell numbers. In xanthophores, TH promotes accumulation of orange carotenoids, making the cells visible. TH receptors act primarily to repress these programs when TH is limiting. Our findings show how a single endocrine factor integrates very different cellular activities during the generation of adult form.

scholarly journals Macromere cell fates during sea urchin development

Development ◽  
1991 ◽  
Vol 113 (4) ◽  
pp. 1085-1091 ◽  
Author(s):  
R.A. Cameron ◽  
S.E. Fraser ◽  
R.J. Britten ◽  
E.H. Davidson
Keyword(s):  
Sea Urchin ◽  
Pigment Cell ◽  
Cell Lineage ◽  
Cell Types ◽  
Cellular Migration ◽  
The Other ◽  
Pigment Cells ◽  
Basal Cells ◽  
Cell Fates ◽  
Gut Pigment

This paper examines the cell lineage relationships and cell fates in embryos of the sea urchin Strongylocentrotus purpuratus leading to the various cell types derived from the definitive vegetal plate territory or the veg2 tier of cells. These cell types are gut, pigment cells, basal cells and coelomic pouches. They are cell types that constitute embryonic structures through cellular migration or rearrangement unlike the relatively non-motile ectoderm cell types. For this analysis, we use previous knowledge of lineage to assign macromeres to one of four types: VOM, the oral macromere; VAM, the aboral macromere, right and left VLM, the lateral macromeres. Each of the four macromeres contributes progeny to all of the cell types that descend from the definitive vegetal plate. Thus in the gut each macromere contributes to the esophagus, stomach and intestine, and the stripe of labeled cells descendant from a macromere reflects the re-arrangement of cells that occurs during archenteron elongation. Pigment cell contributions exhibit no consistent pattern among the four macromeres, and are haphazardly distributed throughout the ectoderm. Gut and pigment cell contributions are thus radially symmetrical. In contrast, the VOM blastomere contributes to both of the coelomic pouches while the other three macromeres contribute to only one or the other pouch. The total of the macromere contribution amounts to 60% of the cells constituting the coelomic pouches.

scholarly journals Fate plasticity and reprogramming in genetically distinct populations of Danio leucophores

2019 ◽  
pp. 201901021 ◽  
Author(s):  
Victor M. Lewis ◽  
Lauren M. Saunders ◽  
Tracy A. Larson ◽  
Emily J. Bain ◽  
Samantha L. Sturiale ◽  
...  
Keyword(s):  
Evolutionary Biology ◽  
Pigment Cell ◽  
Cell Types ◽  
Pigment Cells ◽  
Chemical Compositions ◽  
White Pigment ◽  
Specific Chemical ◽  
Fundamental Goal ◽  
Yellow Orange ◽  
Cell Type Specific

Understanding genetic and cellular bases of adult form remains a fundamental goal at the intersection of developmental and evolutionary biology. The skin pigment cells of vertebrates, derived from embryonic neural crest, are a useful system for elucidating mechanisms of fate specification, pattern formation, and how particular phenotypes impact organismal behavior and ecology. In a survey of Danio fishes, including the zebrafish Danio rerio, we identified two populations of white pigment cells—leucophores—one of which arises by transdifferentiation of adult melanophores and another of which develops from a yellow–orange xanthophore or xanthophore-like progenitor. Single-cell transcriptomic, mutational, chemical, and ultrastructural analyses of zebrafish leucophores revealed cell-type–specific chemical compositions, organelle configurations, and genetic requirements. At the organismal level, we identified distinct physiological responses of leucophores during environmental background matching, and we showed that leucophore complement influences behavior. Together, our studies reveal independently arisen pigment cell types and mechanisms of fate acquisition in zebrafish and illustrate how concerted analyses across hierarchical levels can provide insights into phenotypes and their evolution.

scholarly journals Fate plasticity and reprogramming in genetically distinct populations of Danio leucophores

2019 ◽  
Author(s):  
Victor Lewis ◽  
Lauren Saunders ◽  
Tracy A Larson ◽  
Emily Bain ◽  
Samantha Sturiale ◽  
...  
Keyword(s):  
Evolutionary Biology ◽  
Pigment Cell ◽  
Cell Types ◽  
Pigment Cells ◽  
Chemical Compositions ◽  
White Pigment ◽  
Specific Chemical ◽  
Fundamental Goal ◽  
Yellow Orange ◽  
Cell Type Specific

Understanding genetic and cellular bases of adult form remains a fundamental goal at the intersection of developmental and evolutionary biology. The skin pigment cells of vertebrates, derived from embryonic neural crest, are a useful system for elucidating mechanisms of fate specification, pattern formation, and how particular phenotypes impact organismal behavior and ecology. In a survey of Danio fishes, including zebrafish Danio rerio, we identified two populations of white pigment cells--leucophores--one of which arises by transdifferentiation of adult melanophores and another that develops from a yellow/orange xanthophore-like progenitor. Single-cell transcriptomic, mutational, chemical and ultrastructural analyses of zebrafish leucophores revealed cell-type specific chemical compositions, organelle configurations and genetic requirements. At the organismal level, we identified distinct physiological responses of leucophores during environmental background matching and we show that leucophore complement influences behavior. Together, our studies revealed new, independently arisen pigment cell types and mechanisms of fate acquisition in zebrafish, and illustrate how concerted analyses across hierarchical levels can provide insights into phenotypes and their evolution.

scholarly journals Cell Fate Decisions in the Neural Crest, from Pigment Cell to Neural Development

2021 ◽  
Vol 22 (24) ◽  
pp. 13531
Author(s):  
Jonathan H. P. Dawes ◽  
Robert N. Kelsh
Keyword(s):  
Neural Crest ◽  
Cell Fate ◽  
Neural Development ◽  
Pigment Cell ◽  
Dynamic Modelling ◽  
Cell Types ◽  
Pigment Cells ◽  
Cell Fate Decisions ◽  
Modelling Studies ◽  
Novel Model

The neural crest shows an astonishing multipotency, generating multiple neural derivatives, but also pigment cells, skeletogenic and other cell types. The question of how this process is controlled has been the subject of an ongoing debate for more than 35 years. Based upon new observations of zebrafish pigment cell development, we have recently proposed a novel, dynamic model that we believe goes some way to resolving the controversy. Here, we will firstly summarize the traditional models and the conflicts between them, before outlining our novel model. We will also examine our recent dynamic modelling studies, looking at how these reveal behaviors compatible with the biology proposed. We will then outline some of the implications of our model, looking at how it might modify our views of the processes of fate specification, differentiation, and commitment.

scholarly journals Thyroid hormone regulates distinct paths to maturation in pigment cell lineages

2019 ◽  
Author(s):  
Lauren Saunders ◽  
Abhishek Mishra ◽  
Andrew J Aman ◽  
Victor Lewis ◽  
Matthew B Toomey ◽  
...  
Keyword(s):  
Thyroid Hormone ◽  
Embryonic Development ◽  
Developmental Trajectories ◽  
Pigment Cell ◽  
Developmental Time ◽  
Pigment Cells ◽  
Cell Lineages ◽  
Cellular Processes ◽  
Global Factor ◽  
Endocrine Factors

Circulating endocrine factors are critical for orchestrating complex developmental processes during the generation of adult form. One such factor, thyroid hormone, regulates diverse cellular processes during post-embryonic development and can drive disparate morphological outcomes through mechanisms that remain essentially unknown. We sought to define how thyroid hormone elicits opposite responses in the abundance of two pigment cell classes during development of the zebrafish adult pigment pattern. By profiling individual transcriptomes from thousands of neural crest derived cells, including pigment cells, we reconstructed developmental trajectories and identified lineage-specific changes in response to thyroid hormone. Our findings show that thyroid hormone and its receptors regulate distinct events of cellular maturation across lineages, and illustrate how a single, global factor integrates seemingly divergent morphogenetic outcomes across developmental time.

scholarly journals Review: The Role of Wnt/β-Catenin Signalling in Neural Crest Development in Zebrafish

2021 ◽  
Vol 9 ◽  
Author(s):  
Gemma Sutton ◽  
Robert N. Kelsh ◽  
Steffen Scholpp
Keyword(s):  
Neural Crest ◽  
Pigment Cell ◽  
Model Organism ◽  
Neural Plate ◽  
The Body ◽  
Signalling Pathway ◽  
Border Region ◽  
Pigment Cells ◽  
Neural Plate Border

The neural crest (NC) is a multipotent cell population in vertebrate embryos with extraordinary migratory capacity. The NC is crucial for vertebrate development and forms a myriad of cell derivatives throughout the body, including pigment cells, neuronal cells of the peripheral nervous system, cardiomyocytes and skeletogenic cells in craniofacial tissue. NC induction occurs at the end of gastrulation when the multipotent population of NC progenitors emerges in the ectodermal germ layer in the neural plate border region. In the process of NC fate specification, fate-specific markers are expressed in multipotent progenitors, which subsequently adopt a specific fate. Thus, NC cells delaminate from the neural plate border and migrate extensively throughout the embryo until they differentiate into various cell derivatives. Multiple signalling pathways regulate the processes of NC induction and specification. This review explores the ongoing role of the Wnt/β-catenin signalling pathway during NC development, focusing on research undertaken in the Teleost model organism, zebrafish (Danio rerio). We discuss the function of the Wnt/β-catenin signalling pathway in inducing the NC within the neural plate border and the specification of melanocytes from the NC. The current understanding of NC development suggests a continual role of Wnt/β-catenin signalling in activating and maintaining the gene regulatory network during NC induction and pigment cell specification. We relate this to emerging models and hypotheses on NC fate restriction. Finally, we highlight the ongoing challenges facing NC research, current gaps in knowledge, and this field’s potential future directions.

scholarly journals Regulation of melanocyte development by ligand-dependent BMP signaling underlies oncogenic BMP signaling in melanoma

2019 ◽  
Author(s):  
Alec K. Gramann ◽  
Arvind M. Venkatesan ◽  
Melissa Guerin ◽  
Craig J. Ceol
Keyword(s):  
Neural Crest ◽  
Pigment Cell ◽  
Terminal Differentiation ◽  
Melanoma Cells ◽  
Cell Development ◽  
Bmp Signaling ◽  
Pigment Cells ◽  
Cell Type ◽  
Neural Crest Development ◽  
Direct Regulation

AbstractPreventing terminal differentiation is important in the development and progression of many cancers including melanoma. Recent identification of the BMP ligand GDF6 as a novel melanoma oncogene showed GDF6-activated BMP signaling suppresses differentiation of melanoma cells. Previous studies have identified roles for GDF6 orthologs during early embryonic and neural crest development, but have not identified direct regulation of melanocyte development by GDF6. Here, we investigate the BMP ligand gdf6a, a zebrafish ortholog of human GDF6, during the development of melanocytes from the neural crest. We establish that the loss of gdf6a or inhibition of BMP signaling during neural crest development disrupts normal pigment cell development, leading to an increase in the number of melanocytes and a corresponding decrease in iridophores, another neural crest-derived pigment cell type in zebrafish. This shift occurs as pigment cells arise from the neural crest and depends on mitfa, an ortholog of MITF, a key regulator of melanocyte development that is also targeted by oncogenic BMP signaling. Together, these results indicate that the oncogenic role ligand-dependent BMP signaling plays in suppressing differentiation in melanoma is a reiteration of its physiological roles during melanocyte development.

Common precursors for neural and mesectodermal derivatives in the cephalic neural crest

Development ◽  
1991 ◽  
Vol 112 (1) ◽  
pp. 301-305 ◽  
Author(s):  
A. Baroffio ◽  
E. Dupin ◽  
N.M. Le Douarin
Keyword(s):  
Neural Crest ◽  
Cell Types ◽  
Culture Conditions ◽  
Pigment Cells ◽  
Stem Cell Population ◽  
Multipotent Cells ◽  
Clonal Cultures ◽  
Vertebrate Embryos ◽  
Derivatives Of

The cephalic neural crest (NC) of vertebrate embryos yields a variety of cell types belonging to the neuronal, glial, melanocytic and mesectodermal lineages. Using clonal cultures of quail migrating cephalic NC cells, we demonstrated that neurons and glial cells of the peripheral nervous system can originate from the same progenitors as cartilage, one of the mesectodermal derivatives of the NC. Moreover, we obtained evidence that the migrating cephalic NC contains a few highly multipotent precursors that are common to neurons, glia, cartilage and pigment cells and which we interprete as representative of a stem cell population. In contrast, other NC cells, although provided with identical culture conditions, give rise to clones composed of only one or some of these cell types. These cells thus appear restricted in their developmental potentialities compared to multipotent cells. It is therefore proposed that, in vivo, the active proliferation of pluripotent NC cells during the migration process generates distinct subpopulations of cells that become progressively committed to different developmental fates.

nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate

Development ◽  
1999 ◽  
Vol 126 (17) ◽  
pp. 3757-3767 ◽  
Author(s):  
J.A. Lister ◽  
C.P. Robertson ◽  
T. Lepage ◽  
S.L. Johnson ◽  
D.W. Raible
Keyword(s):  
Transcription Factor ◽  
Retinal Pigment Epithelium ◽  
Neural Crest ◽  
Cell Fate ◽  
Pigment Cell ◽  
Pigment Epithelium ◽  
Retinal Pigment ◽  
Pigment Cells ◽  
Evolutionary Divergence ◽  
Wild Type

We report the isolation and identification of a new mutation affecting pigment cell fate in the zebrafish neural crest. Homozygous nacre (nac(w2)) mutants lack melanophores throughout development but have increased numbers of iridophores. The non-crest-derived retinal pigment epithelium is normal, suggesting that the mutation does not affect pigment synthesis per se. Expression of early melanoblast markers is absent in nacre mutants and transplant experiments suggested a cell-autonomous function in melanophores. We show that nac(w2) is a mutation in a zebrafish gene encoding a basic helix-loop-helix/leucine zipper transcription factor related to microphthalmia (Mitf), a gene known to be required for development of eye and crest pigment cells in the mouse. Transient expression of the wild-type nacre gene restored melanophore development in nacre(−/−) embryos. Furthermore, misexpression of nacre induced the formation of ectopic melanized cells and caused defects in eye development in wild-type and mutant embryos. These results demonstrate that melanophore development in fish and mammals shares a dependence on the nacre/Mitf transcription factor, but that proper development of the retinal pigment epithelium in the fish is not nacre-dependent, suggesting an evolutionary divergence in the function of this gene.

Zebrafish Pigment Pattern Formation: Insights into the Development and Evolution of Adult Form

2019 ◽  
Vol 53 (1) ◽  
pp. 505-530 ◽  
Author(s):  
Larissa B. Patterson ◽  
David M. Parichy
Keyword(s):  
Pattern Formation ◽  
Pigment Cell ◽  
Cell Lineage ◽  
Pigment Cells ◽  
Cellular Interactions ◽  
Lineage Specification ◽  
Pigment Pattern ◽  
Adult Form ◽  
Pattern Development ◽  
Pigment Patterns

Vertebrate pigment patterns are diverse and fascinating adult traits that allow animals to recognize conspecifics, attract mates, and avoid predators. Pigment patterns in fish are among the most amenable traits for studying the cellular basis of adult form, as the cells that produce diverse patterns are readily visible in the skin during development. The genetic basis of pigment pattern development has been most studied in the zebrafish, Danio rerio. Zebrafish adults have alternating dark and light horizontal stripes, resulting from the precise arrangement of three main classes of pigment cells: black melanophores, yellow xanthophores, and iridescent iridophores. The coordination of adult pigment cell lineage specification and differentiation with specific cellular interactions and morphogenetic behaviors is necessary for stripe development. Besides providing a nice example of pattern formation responsible for an adult trait of zebrafish, stripe-forming mechanisms also provide a conceptual framework for posing testable hypotheses about pattern diversification more broadly. Here, we summarize what is known about lineages and molecular interactions required for pattern formation in zebrafish, we review some of what is known about pattern diversification in Danio, and we speculate on how patterns in more distant teleosts may have evolved to produce a stunningly diverse array of patterns in nature.

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