scholarly journals The vertebrate-specific VENTX/NANOG gene empowers neural crest with ectomesenchyme potential

2020 ◽  
Vol 6 (18) ◽  
pp. eaaz1469 ◽  
Author(s):  
Pierluigi Scerbo ◽  
Anne H. Monsoro-Burq
Keyword(s):  
Neural Crest ◽  
Sensory Neuron ◽  
Neural Crest Cells ◽  
Neural Plate ◽  
Pigment Cells ◽  
Regulatory State ◽  
Neural Plate Border ◽  
Nanog Gene ◽  
Neural Ectoderm

During Cambrian, unipotent progenitors located at the neural (plate) border (NB) of an Olfactoria chordate embryo acquired the competence to form ectomesenchyme, pigment cells and neurons, initiating the rise of the multipotent neural crest cells (NC) specific to vertebrates. Surprisingly, the known vertebrate NB/NC transcriptional circuitry is a constrained feature also found in invertebrates. Therefore, evidence for vertebrate-specific innovations endowing vertebrate NC with multipotency is still missing. Here, we identified VENTX/NANOG and POU5/OCT4 as vertebrate-specific innovations. When VENTX was depleted in vivo and in directly-induced NC, the NC lost its early multipotent state and its skeletogenic potential, but kept sensory neuron and pigment identity, thus reminiscent of invertebrate NB precursors. In vivo, VENTX gain-of-function enabled NB specifiers to reprogram embryonic non-neural ectoderm towards early NC identity. We propose that skeletogenic NC evolved by acquiring VENTX/NANOG activity, promoting a novel multipotent progenitor regulatory state into the pre-existing sensory neuron/pigment NB program.

scholarly journals Bimodal function of chromatin remodeler Hmga1 in neural crest induction and Wnt-dependent emigration

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Shashank Gandhi ◽  
Erica J Hutchins ◽  
Krystyna Maruszko ◽  
Jong H Park ◽  
Matthew Thomson ◽  
...  
Keyword(s):  
Neural Crest ◽  
Neural Tube ◽  
Neural Crest Cells ◽  
Neural Plate ◽  
Chromatin Remodeler ◽  
Lineage Specification ◽  
Dorsal Neural Tube ◽  
Neural Crest Development ◽  
Neural Plate Border ◽  
Canonical Wnt

During gastrulation, neural crest cells are specified at the neural plate border, as characterized by Pax7 expression. Using single-cell RNA sequencing coupled with high-resolution in situ hybridization to identify novel transcriptional regulators, we show that chromatin remodeler Hmga1 is highly expressed prior to specification and maintained in migrating chick neural crest cells. Temporally controlled CRISPR-Cas9-mediated knockouts uncovered two distinct functions of Hmga1 in neural crest development. At the neural plate border, Hmga1 regulates Pax7-dependent neural crest lineage specification. At premigratory stages, a second role manifests where Hmga1 loss reduces cranial crest emigration from the dorsal neural tube independent of Pax7. Interestingly, this is rescued by stabilized ß-catenin, thus implicating Hmga1 as a canonical Wnt activator. Together, our results show that Hmga1 functions in a bimodal manner during neural crest development to regulate specification at the neural plate border, and subsequent emigration from the neural tube via canonical Wnt signaling.

scholarly journals Origins of the avian neural crest: the role of neural plate-epidermal interactions

Development ◽  
1995 ◽  
Vol 121 (2) ◽  
pp. 525-538 ◽  
Author(s):  
M.A. Selleck ◽  
M. Bronner-Fraser
Keyword(s):  
Neural Crest ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Neural Plate ◽  
Neural Tube Closure ◽  
Whole Embryo Culture ◽  
Early Stages ◽  
Tissue Interactions ◽  
Neural Ectoderm

We have investigated the lineage and tissue interactions that result in avian neural crest cell formation from the ectoderm. Presumptive neural plate was grafted adjacent to non-neural ectoderm in whole embryo culture to examine the role of tissue interactions in ontogeny of the neural crest. Our results show that juxtaposition of non-neural ectoderm and presumptive neural plate induces the formation of neural crest cells. Quail/chick recombinations demonstrate that both the prospective neural plate and the prospective epidermis can contribute to the neural crest. When similar neural plate/epidermal confrontations are performed in tissue culture to look at the formation of neural crest derivatives, juxtaposition of epidermis with either early (stages 4–5) or later (stages 6–10) neural plate results in the generation of both melanocytes and sympathoadrenal cells. Interestingly, neural plates isolated from early stages form no neural crest cells, whereas those isolated later give rise to melanocytes but not crest-derived sympathoadrenal cells. Single cell lineage analysis was performed to determine the time at which the neural crest lineage diverges from the epidermal lineage and to elucidate the timing of neural plate/epidermis interactions during normal development. Our results from stage 8 to 10+ embryos show that the neural plate/neural crest lineage segregates from the epidermis around the time of neural tube closure, suggesting that neural induction is still underway at open neural plate stages.

scholarly journals Review: The Role of Wnt/β-Catenin Signalling in Neural Crest Development in Zebrafish

2021 ◽  
Vol 9 ◽  
Author(s):  
Gemma Sutton ◽  
Robert N. Kelsh ◽  
Steffen Scholpp
Keyword(s):  
Neural Crest ◽  
Pigment Cell ◽  
Model Organism ◽  
Neural Plate ◽  
The Body ◽  
Signalling Pathway ◽  
Border Region ◽  
Pigment Cells ◽  
Neural Plate Border

The neural crest (NC) is a multipotent cell population in vertebrate embryos with extraordinary migratory capacity. The NC is crucial for vertebrate development and forms a myriad of cell derivatives throughout the body, including pigment cells, neuronal cells of the peripheral nervous system, cardiomyocytes and skeletogenic cells in craniofacial tissue. NC induction occurs at the end of gastrulation when the multipotent population of NC progenitors emerges in the ectodermal germ layer in the neural plate border region. In the process of NC fate specification, fate-specific markers are expressed in multipotent progenitors, which subsequently adopt a specific fate. Thus, NC cells delaminate from the neural plate border and migrate extensively throughout the embryo until they differentiate into various cell derivatives. Multiple signalling pathways regulate the processes of NC induction and specification. This review explores the ongoing role of the Wnt/β-catenin signalling pathway during NC development, focusing on research undertaken in the Teleost model organism, zebrafish (Danio rerio). We discuss the function of the Wnt/β-catenin signalling pathway in inducing the NC within the neural plate border and the specification of melanocytes from the NC. The current understanding of NC development suggests a continual role of Wnt/β-catenin signalling in activating and maintaining the gene regulatory network during NC induction and pigment cell specification. We relate this to emerging models and hypotheses on NC fate restriction. Finally, we highlight the ongoing challenges facing NC research, current gaps in knowledge, and this field’s potential future directions.

scholarly journals Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo

Development ◽  
1999 ◽  
Vol 126 (8) ◽  
pp. 1715-1728 ◽  
Author(s):  
S.E. Perez ◽  
S. Rebelo ◽  
D.J. Anderson
Keyword(s):  
Neural Crest ◽  
Sensory Neuron ◽  
Ectopic Expression ◽  
Neural Crest Cells ◽  
Sensory Ganglia ◽  
Helix Loop Helix ◽  
Autonomic Neurons ◽  
And Function ◽  
Bhlh Transcription Factors

The generation of sensory and autonomic neurons from the neural crest requires the functions of two classes of basic helix-loop-helix (bHLH) transcription factors, the Neurogenins (NGNs) and MASH-1, respectively (Fode, C., Gradwohl, G., Morin, X., Dierich, A., LeMeur, M., Goridis, C. and Guillemot, F. (1998) Neuron 20, 483–494; Guillemot, F., Lo, L.-C., Johnson, J. E., Auerbach, A., Anderson, D. J. and Joyner, A. L. (1993) Cell 75, 463–476; Ma, Q., Chen, Z. F., Barrantes, I. B., de la Pompa, J. L. and Anderson, D. J. (1998 Neuron 20, 469–482). We have cloned two chick NGNs and found that they are expressed in a subset of neural crest cells early in their migration. Ectopic expression of the NGNs in vivo biases migrating neural crest cells to localize in the sensory ganglia, and induces the expression of sensory neuron-appropriate markers in non-sensory crest derivatives. Surprisingly, the NGNs can also induce the expression of multiple pan-neuronal and sensory-specific markers in the dermomyotome, a mesodermal derivative. Taken together, these data suggest that a subset of neural crest cells may already be specified for a sensory neuron fate early in migration, as a consequence of NGN expression.

scholarly journals Effects of Shh and Noggin on neural crest formation demonstrate that BMP is required in the neural tube but not ectoderm

Development ◽  
1998 ◽  
Vol 125 (24) ◽  
pp. 4919-4930 ◽  
Author(s):  
M.A. Selleck ◽  
M.I. Garcia-Castro ◽  
K.B. Artinger ◽  
M. Bronner-Fraser
Keyword(s):  
Neural Crest ◽  
Sonic Hedgehog ◽  
Neural Tube ◽  
Neural Crest Cells ◽  
Neural Plate ◽  
Bmp Signaling ◽  
Neural Tube Closure ◽  
Dorsal Neural Tube ◽  
Neural Ectoderm ◽  
Tube Closure

To define the timing of neural crest formation, we challenged the fate of presumptive neural crest cells by grafting notochords, Sonic Hedgehog- (Shh) or Noggin-secreting cells at different stages of neurulation in chick embryos. Notochords or Shh-secreting cells are able to prevent neural crest formation at open neural plate levels, as assayed by DiI-labeling and expression of the transcription factor, Slug, suggesting that neural crest cells are not committed to their fate at this time. In contrast, the BMP signaling antagonist, Noggin, does not repress neural crest formation at the open neural plate stage, but does so if injected into the lumen of the closing neural tube. The period of Noggin sensitivity corresponds to the time when BMPs are expressed in the dorsal neural tube but are down-regulated in the non-neural ectoderm. To confirm the timing of neural crest formation, Shh or Noggin were added to neural folds at defined times in culture. Shh inhibits neural crest production at early stages (0-5 hours in culture), whereas Noggin exerts an effect on neural crest production only later (5-10 hours in culture). Our results suggest three phases of neurulation that relate to neural crest formation: (1) an initial BMP-independent phase that can be prevented by Shh-mediated signals from the notochord; (2) an intermediate BMP-dependent phase around the time of neural tube closure, when BMP-4 is expressed in the dorsal neural tube; and (3) a later pre-migratory phase which is refractory to exogenous Shh and Noggin.

scholarly journals Segregation of neural crest specific lineage trajectories from a heterogeneous neural plate border territory only emerges at neurulation

2021 ◽  
Author(s):  
Ruth Williams ◽  
Martyna Lukoseviciute ◽  
Tatjana Sauka-Spengler ◽  
Marianne E Bronner
Keyword(s):  
Neural Crest ◽  
Neural Plate ◽  
Developmental Trajectory ◽  
Rna Seq ◽  
Transcriptional Signature ◽  
Transcriptional Changes ◽  
Neural Plate Border ◽  
Neural Ectoderm ◽  
Vertebrate Embryos

The epiblast of vertebrate embryos is comprised of neural and non-neural ectoderm, with the border territory at their intersection harbouring neural crest and cranial placode progenitors. Here we profile avian epiblast cells as a function of time using single-cell RNA-seq to define transcriptional changes in the emerging ‘neural plate border’. The results reveal gradual establishment of heterogeneous neural plate border signatures, including novel genes that we validate by fluorescent in situ hybridisation. Developmental trajectory analysis shows that segregation of neural plate border lineages only commences at early neurulation, rather than at gastrulation as previously predicted. We find that cells expressing the prospective neural crest marker Pax7 contribute to multiple lineages, and a subset of premigratory neural crest cells shares a transcriptional signature with their border precursors. Together, our results suggest that cells at the neural plate border remain heterogeneous until early neurulation, at which time progenitors become progressively allocated toward defined lineages.

scholarly journals In vivo regeneration of rat laryngeal cartilage with mesenchymal stem cells derived from human induced pluripotent stem cells via neural crest cells

2021 ◽  
Vol 52 ◽  
pp. 102233
Author(s):  
Masayoshi Yoshimatsu ◽  
Hiroe Ohnishi ◽  
Chengzhu Zhao ◽  
Yasuyuki Hayashi ◽  
Fumihiko Kuwata ◽  
...  
Keyword(s):  
Stem Cells ◽  
Mesenchymal Stem Cells ◽  
Neural Crest ◽  
Induced Pluripotent Stem Cells ◽  
Pluripotent Stem Cells ◽  
Neural Crest Cells ◽  
Laryngeal Cartilage ◽  
Induced Pluripotent

scholarly journals Migrating into Genomics with the Neural Crest

2014 ◽  
Vol 2014 ◽  
pp. 1-8 ◽  
Author(s):  
Marianne E. Bronner
Keyword(s):  
Neural Crest ◽  
Gene Regulatory Network ◽  
Regulatory Network ◽  
Neural Crest Cells ◽  
Embryonic Cell ◽  
Putative Gene ◽  
Peripheral Neurons ◽  
Neural Plate Border ◽  
The Central Nervous System ◽  
Gene Regulatory

Neural crest cells are a fascinating embryonic cell type, unique to vertebrates, which arise within the central nervous system but emigrate soon after its formation and migrate to numerous and sometimes distant locations in the periphery. Following their migratory phase, they differentiate into diverse derivatives ranging from peripheral neurons and glia to skin melanocytes and craniofacial cartilage and bone. The molecular underpinnings underlying initial induction of prospective neural crest cells at the neural plate border to their migration and differentiation have been modeled in the form of a putative gene regulatory network. This review describes experiments performed in my laboratory in the past few years aimed to test and elaborate this gene regulatory network from both an embryonic and evolutionary perspective. The rapid advances in genomic technology in the last decade have greatly expanded our knowledge of important transcriptional inputs and epigenetic influences on neural crest development. The results reveal new players and new connections in the neural crest gene regulatory network and suggest that it has an ancient origin at the base of the vertebrate tree.

Cell cycle of neural crest cells in the early migratory stage in vivo

1994 ◽  
Vol 27 (9) ◽  
pp. 571-578 ◽  
Author(s):  
M. G. Paglini ◽  
R. A. Rovasio
Keyword(s):  
Cell Cycle ◽  
Neural Crest ◽  
Neural Crest Cells
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