Ancient Evolutionary Origin of the Neural Crest Gene Regulatory Network

Division of Biology 139-74, California Institute of Technology, Pasadena, CA 91125, USA.
Developmental Cell (Impact Factor: 9.71). 10/2007; 13(3):405-20. DOI: 10.1016/j.devcel.2007.08.005
Source: PubMed


The vertebrate neural crest migrates from its origin, the neural plate border, to form diverse derivatives. We previously hypothesized that a neural crest gene regulatory network (NC-GRN) guides neural crest formation. Here, we investigate when during evolution this hypothetical network emerged by analyzing neural crest formation in lamprey, a basal extant vertebrate. We identify 50 NC-GRN homologs and use morpholinos to demonstrate a critical role for eight transcriptional regulators. The results reveal conservation in deployment of upstream factors, suggesting that proximal portions of the network arose early in vertebrate evolution and have been conserved for >500 million years. We found biphasic expression of neural crest specifiers and differences in deployment of some specifiers and effectors expected to confer species-specific properties. By testing the collective expression and function of neural crest genes in a single, basal vertebrate, we reveal the ground state of the NC-GRN and resolve ambiguities between model organisms.

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Available from: Tatjana Sauka-Spengler, Feb 02, 2014
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    • "For linearised plasmid injection, the pm3285_cfos_EGFP plasmid, consisting of the lamprey homolog of CNE 3285 cloned into the pGW_cfosEGFP vector, was linearised with KpnI (NEB), purified with a Qiagen PCR purification kit and eluted in distilled water. Lamprey embryos were obtained as described previously [6] and injected with approximately 2–3 nl of linearised plasmid at a concentration of 100 ngμl−1 during the first cell division. Circular plasmid injection was performed at a concentration of 50 ngµl−1. "
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    ABSTRACT: The sea lamprey is an important model organism for investigating the evolutionary origins of vertebrates. As more vertebrate genome sequences are obtained, evolutionary developmental biologists are becoming increasingly able to identify putative gene regulatory elements across the breadth of the vertebrate taxa. The identification of these regions makes it possible to address how changes at the genomic level have led to changes in developmental gene regulatory networks and ultimately to the evolution of morphological diversity. Comparative genomics approaches using sea lamprey have already predicted a number of such regulatory elements in the lamprey genome. Functional characterisation of these sequences and other similar elements requires efficient reporter assays in lamprey. In this report, we describe the development of a transient transgenesis method for lamprey embryos. Focusing on conserved non-coding elements (CNEs), we use this method to investigate their functional conservation across the vertebrate subphylum. We find instances of both functional conservation and lineage-specific functional evolution of CNEs across vertebrates, emphasising the utility of functionally testing homologous CNEs in their host species.
    PLoS ONE 01/2014; 9(1):e85492. DOI:10.1371/journal.pone.0085492 · 3.23 Impact Factor
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    • "The neural crest gene regulatory network is conserved among vertebrates, including cyclostomes [15,33]. As one could expect for a conserved regulatory network, some of its parts are present in other chordate groups, i.e., tunicates and cephalochordates [15,34,35]. "
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    ABSTRACT: Background The vertebrate head is a highly derived trait with a heavy concentration of sophisticated sensory organs that allow complex behaviour in this lineage. The head sensory structures arise during vertebrate development from cranial placodes and the neural crest. It is generally thought that derivatives of these ectodermal embryonic tissues played a central role in the evolutionary transition at the onset of vertebrates. Despite the obvious importance of head sensory organs for vertebrate biology, their evolutionary history is still uncertain. Results To give a fresh perspective on the adaptive history of the vertebrate head sensory organs, we applied genomic phylostratigraphy to large-scale in situ expression data of the developing zebrafish Danio rerio. Contrary to traditional predictions, we found that dominant adaptive signals in the analyzed sensory structures largely precede the evolutionary advent of vertebrates. The leading adaptive signals at the bilaterian-chordate transition suggested that the visual system was the first sensory structure to evolve. The olfactory, vestibuloauditory, and lateral line sensory organs displayed a strong link with the urochordate-vertebrate ancestor. The only structures that qualified as genuine vertebrate innovations were the neural crest derivatives, trigeminal ganglion and adenohypophysis. We also found evidence that the cranial placodes evolved before the neural crest despite their proposed embryological relatedness. Conclusions Taken together, our findings reveal pre-vertebrate roots and a stepwise adaptive history of the vertebrate sensory systems. This study also underscores that large genomic and expression datasets are rich sources of macroevolutionary information that can be recovered by phylostratigraphic mining.
    Frontiers in Zoology 04/2013; 10(1):18. DOI:10.1186/1742-9994-10-18 · 3.05 Impact Factor
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    • "Recent research revealed that at the level of cyclostomes neural crest formation is already governed by a group of evolutionarily conserved molecules organized into the so-called neural crest gene regulatory network (NC-GRN) [15]. These molecules orchestrate the formation of the neural crest in all vertebrates and include neural plate inducers and border specifiers (FGF, BMP, Wnt, Dlx, Msx1/2, Pax3/7, Zic), neural crest specifiers (Slug/Snail, FoxD3, AP-2, Twist, Id, c-Myc, members of SoxE family), neural crest delamination and migration controllers (RhoB, Cadherins), and, finally, neural crest effectors (MITF, Kit, Col2a, cRet, Erbb3) [15-17]. "
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    ABSTRACT: The neural crest represents a highly multipotent population of embryonic stem cells found only in vertebrate embryos. Acquisition of the neural crest during the evolution of vertebrates was a great advantage, providing Chordata animals with the first cellular cartilage, bone, dentition, advanced nervous system and other innovations. Today not much is known about the evolutionary origin of neural crest cells. Here we propose a novel scenario in which the neural crest originates from neuroectodermal progenitors of the pigmented ocelli in Amphioxus-like animals. We suggest that because of changes in photoreception needs, these multipotent progenitors of photoreceptors gained the ability to migrate outside of the central nervous system and subsequently started to give rise to neural, glial and pigmented progeny at the periphery.
    EvoDevo 04/2013; 4(1):12. DOI:10.1186/2041-9139-4-12 · 3.03 Impact Factor
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