Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii

Demilly, Adrien; Steinmetz, Patrick R. H.; Gazave, Eve; Marchand, Lauriane; Vervoort, Michel

doi:10.1038/ncomms2915

Cited by 45 publications

(75 citation statements)

References 59 publications

(71 reference statements)

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“…In P. dumerilii , an anterior and a posterior-ventral subdomain within the ectoderm, which give rise to the brain and ventral nerve cord, respectively, express SoxB (Kerner et al, 2009). Smaller, segmentally arranged expression domains of the proneural genes ASH, ATO and Olig are nested within the neuroectoderm, which consists of rapidly proliferating neural precursors (Simionato et al, 2008; Demilly et al, 2013; Fig. 2D, top).…”

Section: Introductionmentioning

confidence: 99%

The Evolution of Early Neurogenesis

2015

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The foundation for the complex architecture of the brain is laid by means of a highly stereotyped pattern of proliferation and migration of neural progenitors during embryonic development. This process, termed early neurogenesis, is controlled by genetic mechanisms that have been studied in a number of experimentally amenable vertebrate and invertebrate model systems. Despite of the fact that many of these genetic mechanisms are highly conserved, fundamental structural aspects of early neurogenesis are different in the model systems used. The vertebrate brain is formed by layers of neurons that arise from large numbers of apical and basal progenitors embedded in an invaginated neuroepithelium (neural tube). By contrast, neurons in Drosophila or C. elegans descend from a relatively small number of invariant progenitors which divide in an asymmetric, stem cell-like pattern to create fixed lineages. In order to achieve a better understanding of neurogenesis it is beneficial to explore the evolution of this process. The use of molecular markers and experimental approaches spawned by the model systems has made it possible to study early neurogenesis in other animals, representing a variety of different clades, and our review attempts to provide a survey of this body of work. We divide the neurogenetic process into discrete elements, including origin, pattern, proliferation, and movement of neuronal progenitors, and compare these elements (the “toolkit” of early neurogenesis) in animals that represent the different clades. In cnidarians and many basal bilaterians the entire embryonic ectoderm produces neural precursors that differentiate within the epithelium or delaminate, and form a diffuse basiepithelial nerve net. In addition, one can distinguish in most basal bilaterians ectodermal subdomains (neuroectoderm), defined by conserved regulatory genes and signaling pathways, that contain neural progenitors at higher density, and with increased proliferatory activity. These neuroectodermal progenitors remain at the surface in the (few) basal lophotrochozoans (polychaetes) for which data exist; progenitors become internalized by a combination of delamination and invagination in basal ecdysozoans (onychophorans) and deuterostomes (hemichordates, cephalochordates). In more evolved bilaterians, larger nervous systems are realized by increasing the volume of invaginated neural progenitors (vertebrates, chelicerates), and/or advancing neural proliferation by switching to a mode of asymmetric, self-renewing mitosis (insects, crustaceans, derived annelids, vertebrates). In addition, the pattern of distribution and proliferation of neural progenitors is more precisely controlled, resulting in nervous systems with invariant neuronal architecture (annelids, arthropods, nematodes). Given their limited occurrence in derived clades, these aspects of neurogenesis have likely evolved independently multiple times.

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Section: Introductionmentioning

confidence: 99%

The Evolution of Early Neurogenesis

2015

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“…We observed that Pdu-Hes1, Pdu-Hes6, Pdu-Hes8 and Pdu-Stich are expressed there (Figures 6, 11, 12 and Additional file 5). Previous studies reported the specific expression of several genes in the larvae ventral midline cells such as slit, sim and netrin [90] but also a wnt gene ( Wnt 4 , [57]), two upstream regulators of the core PCP proteins ( fat and four-jointed , [91]) and a microRNA ( mir92 , [92]). In Drosophila , m3, m7, m γ, and m δ ( E(spl) genes) are specifically expressed in the embryonic midline and m7 transcripts are present in the midline until the condensation of the nerve chord [93].…”

Section: Resultsmentioning

confidence: 99%

“…Functionally, the structure serves as an organizer sending a ventralizing signal to the neural tube, as well as to guide neuronal positioning and differentiation along the dorsoventral axis of the neural tube. Recently, it was proposed that Platynereis ventral midline may also act as an organizing center, which produces signals important for neuron production and the proper scaffolding of the VNC [91]. …”

Section: Resultsmentioning

confidence: 99%

History of a prolific family: the Hes/Hey-related genes of the annelid Platynereis

Gazave

Guillou

Balavoine

2014

EvoDevo

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BackgroundThe Hes superfamily or Hes/Hey-related genes encompass a variety of metazoan-specific bHLH genes, with somewhat fuzzy phylogenetic relationships. Hes superfamily members are involved in a variety of major developmental mechanisms in metazoans, notably in neurogenesis and segmentation processes, in which they often act as direct effector genes of the Notch signaling pathway.ResultsWe have investigated the molecular and functional evolution of the Hes superfamily in metazoans using the lophotrochozoan Platynereis dumerilii as model. Our phylogenetic analyses of more than 200 Metazoan Hes/Hey-related genes revealed the presence of five families, three of them (Hes, Hey and Helt) being pan-metazoan. Those families were likely composed of a unique representative in the last common metazoan ancestor. The evolution of the Hes family was shaped by many independent lineage specific tandem duplication events. The expression patterns of 13 of the 15 Hes/Hey-related genes in Platynereis indicate a broad functional diversification. Nevertheless, a majority of these genes are involved in two crucial developmental processes in annelids: neurogenesis and segmentation, resembling functions highlighted in other animal models.ConclusionsCombining phylogenetic and expression data, our study suggests an unusual evolutionary history for the Hes superfamily. An ancestral multifunctional annelid Hes gene may have undergone multiples rounds of duplication-degeneration-complementation processes in the lineage leading to Platynereis, each gene copies ensuring their maintenance in the genome by subfunctionalisation. Similar but independent waves of duplications are at the origin of the multiplicity of Hes genes in other metazoan lineages.

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“…These cells are distinct from the surrounding cells by the presence of nuclear β-catenin, a marker of the Wnt ⁄β-catenin signalling pathway which is involved in neurogenesis (see, e.g., Zhang et al 2011 ;Demilly et al 2013 ). In general, these cells are post-mitotic immature neurons/glial cells that immigrate into the embryo as group of neural precursor ("cell internalisation sites" sensu Brenneis et al 2013 ), composed of fi ve to nine subapical, fl ask-shaped cells.…”

mentioning

confidence: 98%

Myriapoda

Brena

2015

Evolutionary Developmental Biology of Invertebrates 3

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Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii

Cited by 45 publications

References 59 publications

The Evolution of Early Neurogenesis

The Evolution of Early Neurogenesis

History of a prolific family: the Hes/Hey-related genes of the annelid Platynereis

Myriapoda

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