Insights from the amphioxus genome on the origin of vertebrate neural crest

Yu, Jr-Kai; Meulemans, Daniel; McKeown, Sonja J.; Bronner‐Fraser, Marianne

doi:10.1101/gr.076208.108

Cited by 148 publications

(142 citation statements)

References 37 publications

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“…2, more detailed expression patterns are shown in Figs. S3-S7) (8,9). Interestingly, only FGF8/17/18, FGFA, and FGFE show transient expression in the presumptive mesoderm.…”

Section: Resultsmentioning

confidence: 97%

Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits

Bertrand

Camasses

Somorjai

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

100

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FGF signaling is one of the few cell-cell signaling pathways conserved among all metazoans. The diversity of FGF gene content among different phyla suggests that evolution of FGF signaling may have participated in generating the current variety of animal forms. Vertebrates possess the greatest number of FGF genes, the functional evolution of which may have been implicated in the acquisition of vertebrate-specific morphological traits. In this study, we have investigated the roles of the FGF signal during embryogenesis of the cephalochordate amphioxus, the best proxy for the chordate ancestor. We first isolate the full FGF gene complement and determine the evolutionary relationships between amphioxus and vertebrate FGFs via phylogenetic and synteny conservation analysis. Using pharmacological treatments, we inhibit the FGF signaling pathway in amphioxus embryos in different time windows. Our results show that the requirement for FGF signaling during gastrulation is a conserved character among chordates, whereas this signal is not necessary for neural induction in amphioxus, in contrast to what is known in vertebrates. We also show that FGF signal, acting through the MAPK pathway, is necessary for the formation of the most anterior somites in amphioxus, whereas more posterior somite formation is not FGF-dependent. This result leads us to propose that modification of the FGF signal function in the anterior paraxial mesoderm in an amphioxus-like vertebrate ancestor might have contributed to the loss of segmentation in the preotic paraxial mesoderm of the vertebrate head.O nly a few cell-cell signaling molecules are known to play a major role during metazoan embryonic development. Among them, the FGFs were discovered in the mid-1970s in vertebrates. FGFs are small proteins, generally secreted, characterized by a conserved functional domain and acting through binding to their transmembrane receptors [FGF receptors (FGFRs)], causing them to homodimerize. This leads to intracellular autophosphorylation and further activation of cytoplasmic signaling cascades, such as the MAPK and the PI3K pathways (1).Sequencing of several complete metazoan genomes has shown that FGF and FGFR genes were already present in the common ancestor of diploblastic and bilaterian animals (2). In vertebrates, at least 22 genes coding for FGFs and 4 coding for their FGFRs are known. In contrast, only 3 genes coding for FGFs and 2 coding for FGFRs have been described in Drosophila (2). In the urochordate Ciona intestinalis, a member of the sister group of vertebrates, only 6 FGF genes are present, for which some orthology relationships with vertebrate FGFs are still not resolved (3). This large number of FGFs and FGFRs in vertebrates raises the question of their implication in the evolution of vertebrate-specific morphological characteristics.In vertebrates, FGF signaling is involved in different developmental processes, among which are neural and mesoderm induction in the early embryo, and somitogenesis and limb bud formation at later stages (4)....

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“…2, more detailed expression patterns are shown in Figs. S3-S7) (8,9). Interestingly, only FGF8/17/18, FGFA, and FGFE show transient expression in the presumptive mesoderm.…”

Section: Resultsmentioning

confidence: 97%

Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits

Bertrand

Camasses

Somorjai

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

100

View full text Add to dashboard Cite

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“…These findings suggest that initial formation of the neural plate border may occur via a mechanisms conserved between cephalochordates and vertebrates. Support for this idea comes from experimental manipulations in which inhibition of BMP signaling has similar effects in amphioxus as in vertebrates (Yu et al, 2008).…”

Section: Nonvertebrate Chordatesmentioning

confidence: 99%

Evolution of the neural crest viewed from a gene regulatory perspective

Sauka‐Spengler

Bronner‐Fraser

2008

Genesis

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Summary: Neural crest cells are a vertebrate innovation and form a wide variety of embryonic cell types as diverse as peripheral neurons and facial skeleton. They undergo complex migration and differentiation processes from their site of origin in the developing central nervous system to their final destinations in the periphery. In this review, we summarize recent data on the current formulation of a gene regulatory network underlying neural crest formation and its roots at the base of the vertebrate lineage. Analyzing neural crest formation from a gene regulatory viewpoint provides insights into both the developmental mechanisms and evolutionary origins of this vertebrate-specific cell type. genesis 46:673-682,

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“…Recently, a more comprehensive functional analysis of multiple components with the network was systematically tested in a single species (7). The results suggested that much of the NC-GRN is highly conserved across vertebrates (7), contrasting with nonvertebrate chordates (6,(8)(9)(10)(11)(12)(13)(14)(15), which appear to lack a module involved in neural crest specification (16). However, proximal portions of this network appear conserved to the base of the chordate lineage (17).…”

mentioning

confidence: 99%

Dissecting early regulatory relationships in the lamprey neural crest gene network

Nikitina

Sauka‐Spengler²,

Bronner‐Fraser³

2008

Proc. Natl. Acad. Sci. U.S.A.

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The neural crest, a multipotent embryonic cell type, originates at the border between neural and nonneural ectoderm. After neural tube closure, these cells undergo an epithelial-mesenchymal transition, migrate to precise, often distant locations, and differentiate into diverse derivatives. Analyses of expression and function of signaling and transcription factors in higher vertebrates has led to the proposal that a neural crest gene regulatory network (NC-GRN) orchestrates neural crest formation. Here, we interrogate the NC-GRN in the lamprey, taking advantage of its slow development and basal phylogenetic position to resolve early inductive events, 1 regulatory step at the time. To establish regulatory relationships at the neural plate border, we assess relative expression of 6 neural crest network genes and effects of individually perturbing each on the remaining 5. The results refine an upstream portion of the NC-GRN and reveal unexpected order and linkages therein; e.g., lamprey AP-2 appears to function early as a neural plate border rather than a neural crest specifier and in a pathway linked to MsxA but independent of ZicA. These findings provide an ancestral framework for performing comparative tests in higher vertebrates in which network linkages may be more difficult to resolve because of their rapid development.neural plate border ͉ transcription factor ͉ agnathan

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Insights from the amphioxus genome on the origin of vertebrate neural crest

Cited by 148 publications

References 37 publications

Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits

Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits

Evolution of the neural crest viewed from a gene regulatory perspective

Dissecting early regulatory relationships in the lamprey neural crest gene network

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