Prickle1 is required for EMT and migration of zebrafish cranial neural crest

Ahsan, Kamil; Singh, Noor; Rocha, Manuel; Huang, Christina; Prince, Victoria

doi:10.1016/j.ydbio.2019.01.018

Cited by 23 publications

(20 citation statements)

References 98 publications

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“…PRICKLE1 was strongly up-regulated during duct formation. This gene encodes a nuclear receptor that localises to the nuclear membrane and is implicated in planar cell polarity, inhibition of the Wnt/β-catenin signaling pathway, EMT and neuronal cell migration [ 86 ]. In the chicken embryo, PRICKLE1 is expressed in a developmentally restricted fashion, in the primitive streak, ventral neural tube, and foregut at early stages and later in differentiating myotomes [ 87 ].…”

Section: Discussionmentioning

confidence: 99%

Transcriptional landscape of the embryonic chicken Müllerian duct

et al. 2020

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Background Müllerian ducts are paired embryonic tubes that give rise to the female reproductive tract in vertebrates. Many disorders of female reproduction can be attributed to anomalies of Müllerian duct development. However, the molecular genetics of Müllerian duct formation is poorly understood and most disorders of duct development have unknown etiology. In this study, we describe for the first time the transcriptional landscape of the embryonic Müllerian duct, using the chicken embryo as a model system. RNA sequencing was conducted at 1 day intervals during duct formation to identify developmentally-regulated genes, validated by in situ hybridization. Results This analysis detected hundreds of genes specifically up-regulated during duct morphogenesis. Gene ontology and pathway analysis revealed enrichment for developmental pathways associated with cell adhesion, cell migration and proliferation, ERK and WNT signaling, and, interestingly, axonal guidance. The latter included factors linked to neuronal cell migration or axonal outgrowth, such as Ephrin B2, netrin receptor, SLIT1 and class A semaphorins. A number of transcriptional modules were identified that centred around key hub genes specifying matrix-associated signaling factors; SPOCK1, HTRA3 and ADGRD1. Several novel regulators of the WNT and TFG-β signaling pathway were identified in Müllerian ducts, including APCDD1 and DKK1, BMP3 and TGFBI. A number of novel transcription factors were also identified, including OSR1, FOXE1, PRICKLE1, TSHZ3 and SMARCA2. In addition, over 100 long non-coding RNAs (lncRNAs) were expressed during duct formation. Conclusions This study provides a rich resource of new candidate genes for Müllerian duct development and its disorders. It also sheds light on the molecular pathways engaged during tubulogenesis, a fundamental process in embryonic development.

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Section: Discussionmentioning

confidence: 99%

Transcriptional landscape of the embryonic chicken Müllerian duct

et al. 2020

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“…This dlx5a recovery phenomenon is not observed in edn1 mutants indicating only some craniofacial mutants can recover over time [31]. Other mutations affecting neural crest cells, like those in prickle1 , also exhibit early phenotypes that are later overcome [65]. Therefore, we propose that the ability of some mutants to overcome a deleterious mutation truly is a form of resilience, defined as the ability to recover from or adjust to misfortune or change over time [66].…”

Section: Discussionmentioning

confidence: 99%

Selective breeding modifies mef2ca mutant incomplete penetrance by tuning the opposing Notch pathway

et al. 2019

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Deleterious genetic mutations allow developmental biologists to understand how genes control development. However, not all loss of function genetic mutants develop phenotypic changes. Many deleterious mutations only produce a phenotype in a subset of mutant individuals, a phenomenon known as incomplete penetrance. Incomplete penetrance can confound analyses of gene function and our understanding of this widespread phenomenon remains inadequate. To better understand what controls penetrance, we capitalized on the zebrafish mef2ca mutant which produces craniofacial phenotypes with variable penetrance. Starting with a characterized mef2ca loss of function mutant allele, we used classical selective breeding methods to generate zebrafish strains in which mutant-associated phenotypes consistently appear with low or high penetrance. Strikingly, our selective breeding for low penetrance converted the mef2ca mutant allele behavior from homozygous lethal to homozygous viable. Meanwhile, selective breeding for high penetrance converted the mef2ca mutant allele from fully recessive to partially dominant. Comparing the selectively-bred low- and high-penetrance strains revealed that the strains initially respond similarly to the mutation, but then gene expression differences between strains emerge during development. Thus, altered temporal genetic circuitry can manifest through selective pressure to modify mutant penetrance. Specifically, we demonstrate differences in Notch signaling between strains, and further show that experimental manipulation of the Notch pathway phenocopies penetrance changes occurring through selective breeding. This study provides evidence that penetrance is inherited as a liability-threshold trait. Our finding that vertebrate animals can overcome a deleterious mutation by tuning genetic circuitry complements other reported mechanisms of overcoming deleterious mutations such as transcriptional adaptation of compensatory genes, alternative mRNA splicing, and maternal deposition of wild-type transcripts, which are not observed in our system. The selective breeding approach and the resultant genetic circuitry change we uncovered advances and expands our current understanding of genetic and developmental resilience.

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“…113 EMT occurs in multiple contexts, and its roles in collective cell migrations, morphogenesis, and cancer have been broadly investigated. [114][115][116][117][118] However, the manner in which EMT has typically been discussed-as a "binary switch" from tightly-packed, highly adhesive epithelial cells to dispersed, loosely-packed mesenchymal cells-has recently been called into question, both in the context of zebrafish neural crest, 81,[119][120][121] and beyond. 122,123 A growing body of evidence indicates that EMT is not in fact a binary switch, but is instead a more gradual process, during which cells pass through a spectrum of morphologies that are neither entirely epithelial nor entirely mesenchymal.…”

Section: The Epithelial-to-mesenchymal Transitionmentioning

confidence: 99%

Neural crest development: insights from the zebrafish

Rocha

Singh

Ahsan

et al. 2019

Developmental Dynamics

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Our understanding of the neural crest, a key vertebrate innovation, is built upon studies of multiple model organisms. Early research on neural crest cells (NCCs) was dominated by analyses of accessible amphibian and avian embryos, with mouse genetics providing complementary insights in more recent years. The zebrafish model is a relative newcomer to the field, yet it offers unparalleled advantages for the study of NCCs. Specifically, zebrafish provide powerful genetic and transgenic tools, coupled with rapidly developing transparent embryos that are ideal for high-resolution real-time imaging of the dynamic process of neural crest development. While the broad principles of neural crest development are largely conserved across vertebrate species, there are critical differences in anatomy, morphogenesis, and genetics that must be considered before information from one model is extrapolated to another. Here, our goal is to provide the reader with a helpful primer specific to neural crest development in the zebrafish model. We focus largely on the earliest events-specification, delamination, and migrationdiscussing what is known about zebrafish NCC development and how it differs from NCC development in non-teleost species, as well as highlighting current gaps in knowledge.

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Prickle1 is required for EMT and migration of zebrafish cranial neural crest

Cited by 23 publications

References 98 publications

Transcriptional landscape of the embryonic chicken Müllerian duct

Transcriptional landscape of the embryonic chicken Müllerian duct

Selective breeding modifies mef2ca mutant incomplete penetrance by tuning the opposing Notch pathway

Neural crest development: insights from the zebrafish

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