Insights into neural crest development and evolution from genomic analysis

Simões-Costa, Marcos; Bronner‐Fraser, Marianne

doi:10.1101/gr.157586.113

Cited by 112 publications

(119 citation statements)

References 119 publications

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“…Advances in molecular biology in the last two decades have greatly elaborated our knowledge of the genetic control of different events in neural crest development (Simoes-Costa and Bronner, 2013). Numerous studies have resulted in the identification of many transcription factors important for neural crest formation, as well as some of the regulatory links between these regulators.…”

Section: The Neural Crest Gene Regulatory Networkmentioning

confidence: 99%

“…This raises the interesting possibility that WNTs could act as permissive factors in neural crest specification. However, cis-regulatory analysis has failed to uncover many direct TCF/LEF binding sites that are crucial for neural crest specifier expression (Betancur et al, 2010b;Barembaum and Bronner, 2013;Simoes-Costa and Bronner, 2013). The exception seems to be Snai2, which has a proximal enhancer that is directly activated by TCF/LEF and β-catenin (Vallin et al, 2001).…”

Section: Induction and Formation Of The Neural Plate Bordermentioning

confidence: 99%

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Establishing neural crest identity: a gene regulatory recipe

2015

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The neural crest is a stem/progenitor cell population that contributes to a wide variety of derivatives, including sensory and autonomic ganglia, cartilage and bone of the face and pigment cells of the skin. Unique to vertebrate embryos, it has served as an excellent model system for the study of cell behavior and identity owing to its multipotency, motility and ability to form a broad array of cell types. Neural crest development is thought to be controlled by a suite of transcriptional and epigenetic inputs arranged hierarchically in a gene regulatory network. Here, we examine neural crest development from a gene regulatory perspective and discuss how the underlying genetic circuitry results in the features that define this unique cell population.

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Section: The Neural Crest Gene Regulatory Networkmentioning

confidence: 99%

Section: Induction and Formation Of The Neural Plate Bordermentioning

confidence: 99%

Establishing neural crest identity: a gene regulatory recipe

2015

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“…A longstanding question concerns the nature of the mechanisms that regulate the persistence of direction and cohesion of multicellular streams. Large-scale genomic analyses of premigratory or migrating embryonic cells, such as the neural crest (NC), have shed light on the genes expressed in migratory versus non-migratory cells during embryonic development Bronner-Fraser, 2002, 2003;Molyneaux et al, 2004;Adams et al, 2008;Gallardo et al, 2010;Simoes-Costa and Bronner, 2013;Simoes-Costa et al, 2014). However, what remains unclear is how gene expression varies as migrating cells respond to different microenvironments and how this transduces into observed cell behaviors.…”

Section: Introductionmentioning

confidence: 99%

Neural crest migration is driven by a few trailblazer cells with a unique molecular signature narrowly confined to the invasive front

et al. 2015

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Neural crest (NC) cell migration is crucial to the formation of peripheral tissues during vertebrate development. However, how NC cells respond to different microenvironments to maintain persistence of direction and cohesion in multicellular streams remains unclear. To address this, we profiled eight subregions of a typical cranial NC cell migratory stream. Hierarchical clustering showed significant differences in the expression profiles of the lead three subregions compared with newly emerged cells. Multiplexed imaging of mRNA expression using fluorescent hybridization chain reaction (HCR) quantitatively confirmed the expression profiles of lead cells. Computational modeling predicted that a small fraction of lead cells that detect directional information is optimal for successful stream migration. Single-cell profiling then revealed a unique molecular signature that is consistent and stable over time in a subset of lead cells within the most advanced portion of the migratory front, which we term trailblazers. Model simulations that forced a lead cell behavior in the trailing subpopulation predicted cell bunching near the migratory domain entrance. Misexpression of the trailblazer molecular signature by perturbation of two upstream transcription factors agreed with the in silico prediction and showed alterations to NC cell migration distance and stream shape. These data are the first to characterize the molecular diversity within an NC cell migratory stream and offer insights into how molecular patterns are transduced into cell behaviors.

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“…Dct enzyme and Ret transmembrane receptor) is finally activated during the migration of NCCs in order to control their tissue-specific homing and differentiation. Comparative analysis of the cranial NC GRN from basal chordates to vertebrates suggests that many regulatory circuits are conserved across chordates (Green and Bronner, 2013;Simoes-Costa and Bronner, 2013). However, the exact way in which the NC GRN is wired downstream of the signaling inputs is expected to differ between the cranial and trunk regions, and between species (Barriga et al, 2015;Simoes-Costa and Bronner, 2013).…”

Section: Introductionmentioning

confidence: 99%

A direct role for murine Cdx proteins in the trunk neural crest-gene regulatory network

et al. 2016

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Numerous studies in chordates and arthropods currently indicate that Cdx proteins have a major ancestral role in the organization of posthead tissues. In urochordate embryos, Cdx loss-of-function has been shown to impair axial elongation, neural tube (NT) closure and pigment cell development. Intriguingly, in contrast to axial elongation and NT closure, a Cdx role in neural crest (NC)-derived melanocyte/ pigment cell development has not been reported in any other chordate species. To address this, we generated a new conditional pan-Cdx functional knockdown mouse model that circumvents Cdx functional redundancy as well as the early embryonic lethality of Cdx mutants. Through directed inhibition in the neuroectoderm, we provide in vivo evidence that murine Cdx proteins impact melanocyte and enteric nervous system development by, at least in part, directly controlling the expression of the key early regulators of NC ontogenesis Pax3, Msx1 and Foxd3. Our work thus reveals a novel role for Cdx proteins at the top of the trunk NC gene regulatory network in the mouse, which appears to have been inherited from their ancestral ortholog.

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Insights into neural crest development and evolution from genomic analysis

Cited by 112 publications

References 119 publications

Establishing neural crest identity: a gene regulatory recipe

Establishing neural crest identity: a gene regulatory recipe

Neural crest migration is driven by a few trailblazer cells with a unique molecular signature narrowly confined to the invasive front

A direct role for murine Cdx proteins in the trunk neural crest-gene regulatory network

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