Network architecture and regulatory logic in neural crest development

Focus Article

Austin S. Hovland, Megan Rothstein, Marcos Simoes‐Costa

Published Online: Nov 08 2019

DOI: 10.1002/wsbm.1468

Full article on Wiley Online Library: HTML PDF

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Abstract The neural crest is an ectodermal cell population that gives rise to over 30 cell types during vertebrate embryogenesis. These stem cells are formed at the border of the developing central nervous system and undergo extensive migration before differentiating into components of multiple tissues and organs. Neural crest formation and differentiation is a multistep process, as these cells transition through sequential regulatory states before adopting their adult phenotype. Such changes are governed by a complex gene regulatory network (GRN) that integrates environmental and cell‐intrinsic inputs to regulate cell identity. Studies of neural crest cells in a variety of vertebrate models have elucidated the function and regulation of dozens of the molecular players that are part of this network. The neural crest GRN has served as a platform to explore the molecular control of multipotency, cell differentiation, and the evolution of vertebrates. In this review, we employ this genetic program as a stepping‐stone to explore the architecture and the regulatory principles of developmental GRNs. We also discuss how modern genomic approaches can further expand our understanding of genetic networks in this system and others. This article is categorized under: Physiology > Mammalian Physiology in Health and Disease Biological Mechanisms > Cell Fates Developmental Biology > Lineages Models of Systems Properties and Processes > Cellular Models

Stages of cranial neural crest development in the chicken embryo. (a). During gastrulation (Hamburger and Hamilton stage 5, HH5), the avian ectoderm is divided in three spatial domains: the neural plate, the nonneural ectoderm (NNE) and the neural plate border (NPB). The neural crest progenitor cells reside within the NPB, which elevate during the closure of the neural tube. (b). During neurulation (HH8), the neural crest cells are already specified and are positioned at the dorsal aspect of the neural tube. (c). At HH9‐10, cranial neural crest cells delaminate from the neural tube and begin migration along the dorsoventral pathway

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Regulatory sub‐circuits within the neural crest gene regulatory network. (a) Tfap2a, a key node within both the neural plate border (NPB) and neural crest specification modules, uses a coherent feed‐forward mechanism to activate other neural crest‐specific transcription factors. (b) A mutual cross‐repression circuit within the NPB. In this circuit, Pax7 promotes neural crest fate by activating Snai1/2 and repressing Sox2/3. In adjacent neural tissue, Sox2/3 represses Snai1/2. Similarly, preplacodal tissue express Six1/4 and Eya1/2, which repress Pax7. This promotes the spatial segregation of these domains. (c) Sox10 integrates many neural crest specification genes and utilizes a positive feedback loop to maintain neural crest identity during migration

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A gene regulatory network controls cranial neural crest development. This diagram depicts a simplified version of the cranial neural crest gene regulatory network across vertebrates. Gray boxes denote different regulatory modules. Nodes are represented as horizontal arrows, which are linked together by direct (solid) or indirect (dashed) regulatory links that are activating (ending in arrows) or repressive (ending in a T). (a) The neural plate border (NPB) is induced by signaling systems such as Wnts and BMPs. Adjacent neural and preplacodal region (PPR) cells express a distinct set of transcription factors, some of which form cross‐repressive circuitry with neural crest modules. Nodes within the NPB module activate the Specification module (b), which subsequently activates the genes that are part of the Migration module (c) of the network. (d) Different signals (TGF‐β, BMP, and Wnt) influence differentiation of neural crest cells into chondrocytes, sympathetic neurons, and melanocytes

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