Distinct interactions of Sox5 and Sox10 in fate specification of pigment cells in medaka and zebrafish

Nagao, Yusuke; Takada, Hiroyuki; Miyadai, Motohiro; Adachi, Tomoko; Seki, Ryohei; Kamei, Yasuhiro; Hara, Ikuyo; Taniguchi, Yoshihito; Naruse, Kiyoshi; Hibi, Masahiko; Kelsh, Robert N.; Hashimoto, Hisashi

doi:10.1371/journal.pgen.1007260

Cited by 55 publications

(66 citation statements)

References 69 publications

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“…This view is crystallised in the iconic Waddington landscape model of stem cell development (Waddington 1957). Consistent with this view, aside from the chromatoblast, these partially-restricted intermediates for pigment cells have been suggested to include bipotent Schwann cell precursors, capable of forming melanocytes as well as Schwann cells (Adameyko et al 2009;Adameyko and Lallemend 2010); bipotent melanoiridoblasts (Curran et al 2010), and bipotent xantholeucoblasts (Nagao et al 2014(Nagao et al , 2018.…”

Section: Introductionmentioning

confidence: 82%

A systems biology approach uncovers the core gene regulatory network governing iridophore fate choice from the neural crest

Petratou

Subkhankulova

Lister

et al. 2018

Preprint

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Multipotent neural crest (NC) progenitors generate an astonishing array of derivatives, including neuronal, skeletal components and pigment cells (chromatophores), but the molecular mechanisms allowing balanced selection of each fate remain unknown. In zebrafish, melanocytes, iridophores and xanthophores, the three chromatophore lineages, are thought to share progenitors and so lend themselves to investigating the complex gene regulatory networks (GRNs) underlying fate segregation of NC progenitors. Although the core GRN governing melanocyte specification has been previously established, those guiding iridophore and xanthophore development remain elusive. Here we focus on the iridophore GRN, where mutant phenotypes identify the transcription factors Sox10, Tfec and Mitfa and the receptor tyrosine kinase, Ltk, as key players. We present expression data, as well as loss and gain of function results, guiding the derivation of an initial iridophore specification GRN. Moreover, we use an iterative process of mathematical modelling, supplemented with a novel, Monte Carlo screening algorithm suited to the qualitative nature of the experimental data, to allow for rigorous predictive exploration of the GRN dynamics. Predictions were experimentally evaluated and testable hypotheses were derived to construct an improved version of the GRN, which we showed produced outputs consistent with experimentally observed gene expression dynamics. Our study reveals multiple important regulatory features, notably a sox10-dependent positive feedback loop between tfec and ltk driving iridophore specification; the molecular basis of sox10 maintenance throughout iridophore development; and the cooperation between sox10 and tfec in driving expression of pnp4a, a key differentiation gene. We also assess a candidate repressor of mitfa, a melanocyte-specific target of sox10. Surprisingly, our data challenge the reported role of Foxd3, an established mitfa repressor, in iridophore regulation. Our study builds upon our previous systems biology approach, by incorporating physiologically-relevant parameter values and rigorous evaluation of parameter values within a qualitative data framework, to establish for the first time the core GRN guiding specification of the iridophore lineage. Author SummaryMultipotent neural crest (NC) progenitors generate an astonishing array of derivatives, including neuronal, skeletal components and pigment cells, but the molecular mechanisms allowing balanced selection of each fate remain unknown. In zebrafish, melanocytes, iridophores and xanthophores, the three chromatophore lineages, are thought to share progenitors and so lend themselves to investigating the complex gene regulatory networks (GRNs) underlying fate segregation of NC progenitors. Although the core GRN governing melanocyte specification has been previously established, those guiding iridophore and xanthophore development remain elusive. Here we present expression data, as well as loss and gain of function results, guiding the derivation of a core irid...

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Section: Introductionmentioning

confidence: 82%

A systems biology approach uncovers the core gene regulatory network governing iridophore fate choice from the neural crest

Petratou

Subkhankulova

Lister

et al. 2018

Preprint

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“…However, two previous studies are of particular interest in regards to this. The study by Nagao and colleagues [ 63 ] investigated the leucophore pigment cell type in the perciform lineage. Experimental evidence suggests that the origin of the leucophore in the perciform lineage was achieved by a change in the functional interaction between TFs already expressed in a precursor cell type.…”

Section: Discussionmentioning

confidence: 99%

The mammalian decidual cell evolved from a cellular stress response

et al. 2018

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Among animal species, cell types vary greatly in terms of number and kind. The number of cell types found within an organism differs considerably between species, and cell type diversity is a significant contributor to differences in organismal structure and function. These observations suggest that cell type origination is a significant source of evolutionary novelty. The molecular mechanisms that result in the evolution of novel cell types, however, are poorly understood. Here, we show that a novel cell type of eutherians mammals, the decidual stromal cell (DSC), evolved by rewiring an ancestral cellular stress response. We isolated the precursor cell type of DSCs, endometrial stromal fibroblasts (ESFs), from the opossum Monodelphis domestica. We show that, in opossum ESFs, the majority of decidual core regulatory genes respond to decidualizing signals but do not regulate decidual effector genes. Rather, in opossum ESFs, decidual transcription factors function in apoptotic and oxidative stress response. We propose that rewiring of cellular stress responses was an important mechanism for the evolution of the eutherian decidual cell type.

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“…Recent work has shown that the same gene can be involved in the development of the same pigment cell type but in different ways in various fish species. For instance, xanthophore differentiation requires the expression of sox5 in medaka whereas the repression of this gene is required in zebrafish [60].…”

Section: Box 1 Pigmentation Genesmentioning

confidence: 99%

Magic Traits in Magic Fish: Understanding Color Pattern Evolution Using Reef Fish

et al. 2019

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Color patterns provide easy access to phenotypic diversity and allow the questioning of the adaptive value of traits or the constraints acting on phenotypic evolution. Reef fish offer a unique opportunity to address such questions because they are ecologically and phylogenetically diverse and have the largest variety of pigment cell types known in vertebrates. In addition to recent development of their genetic resources, reef fish also constitute experimental models that allow the discrimination of ecological, developmental, and evolutionary processes at work. Here, we emphasize how the study of color patterns in reef fish can be integrated in an Eco/Evo/Devo (ecological evolutionary developmental) perspective and we illustrate that such an approach can bring new insights on the evolution of complex phenotypes. Why Study Reef Fish and Their Color Patterns?Questions regarding the diversity, evolution, and ecological significance of color patterns (see Glossary) have caught scientists' attention for centuries [1]. Pigmentation has been studied using a wide variety of animal models from hexapods to vertebrates [1,2]. Fruit flies and mice are still important models to study pigmentation genes [3] but, over the last few years, teleost fish have also became efficient systems for addressing questions related to color patterns. Zebrafish and medaka are helpful models for combining genetic manipulations with live imaging, and their study has provided new insights on the cellular and molecular mechanisms that drive the development of color patterns [4]. Other fish such as cichlids and guppies have also provided valuable insight into genes and molecular mechanisms underlying specific traits (egg spots and stripes) and various color ornaments [5][6][7].While mammals only possess melanocytes, the teleost lineage harbors the highest number of pigment cell typesalso called chromatophores (e.g., melanophores, xanthophores, and iridophores) [8]. This diversity can explain the diversity of color and their patterns and implies the involvement of many pigmentation genes. The list of identified genes has increased in recent years (Box 1) and the whole genome duplication that occurred at the basis of the teleost lineage has been identified as a major contributor to this diversity [9].To be able to fully understand the evolution of traits such as those displayed in color patterns and the genetic mechanisms underlying the responses of organisms to their natural environment, it is important to perform Eco/Evo/Devo approaches. However, ecological and behavioral roles of color patterns have not been studied in the model organisms cited above, leading to a black box concerning how proximate factors shape color patterns and their diversity over evolution. Reef fish offer promising models to address such questions because they do express much of the amazing diversity of color patterns as well as associated behavioral and ecological variation. Their original color patterns include dark or conspicuous colors, and can be made of a diverse combin...

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Distinct interactions of Sox5 and Sox10 in fate specification of pigment cells in medaka and zebrafish

Cited by 55 publications

References 69 publications

A systems biology approach uncovers the core gene regulatory network governing iridophore fate choice from the neural crest

A systems biology approach uncovers the core gene regulatory network governing iridophore fate choice from the neural crest

The mammalian decidual cell evolved from a cellular stress response

Magic Traits in Magic Fish: Understanding Color Pattern Evolution Using Reef Fish

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