scholarly journals Spatiotemporal structure of cell fate decisions in murine neural crest

Science ◽  
2019 ◽  
Vol 364 (6444) ◽  
pp. eaas9536 ◽  
Author(s):  
Ruslan Soldatov ◽  
Marketa Kaucka ◽  
Maria Eleni Kastriti ◽  
Julian Petersen ◽  
Tatiana Chontorotzea ◽  
...  
Keyword(s):  
Neural Crest ◽  
Cell Fate ◽  
Single Cell Analysis ◽  
Neural Crest Cells ◽  
Cell Types ◽  
Phenotypic Traits ◽  
Cell Fate Decisions ◽  
Numerous Cell ◽  
Trunk Neural Crest ◽  
Cranial Neural Crest Cells

Neural crest cells are embryonic progenitors that generate numerous cell types in vertebrates. With single-cell analysis, we show that mouse trunk neural crest cells become biased toward neuronal lineages when they delaminate from the neural tube, whereas cranial neural crest cells acquire ectomesenchyme potential dependent on activation of the transcription factor Twist1. The choices that neural crest cells make to become sensory, glial, autonomic, or mesenchymal cells can be formalized as a series of sequential binary decisions. Each branch of the decision tree involves initial coactivation of bipotential properties followed by gradual shifts toward commitment. Competing fate programs are coactivated before cells acquire fate-specific phenotypic traits. Determination of a specific fate is achieved by increased synchronization of relevant programs and concurrent repression of competing fate programs.

scholarly journals Cyclic AMP Signaling Functions as a Bimodal Switch in Sympathoadrenal Cell Development in Cultured Primary Neural Crest Cells

2000 ◽  
Vol 20 (9) ◽  
pp. 3004-3014 ◽  
Author(s):  
Matthew L. Bilodeau ◽  
Theresa Boulineau ◽  
Ronald L. Hullinger ◽  
Ourania M. Andrisani
Keyword(s):  
Cyclic Amp ◽  
Neural Crest ◽  
Cell Fate ◽  
Bone Morphogenetic Proteins ◽  
Neural Crest Cells ◽  
Cell Types ◽  
Cell Development ◽  
Camp Signaling ◽  
Camp Signaling Pathway ◽  
Trunk Neural Crest

ABSTRACT Cells of the vertebrate neural crest (crest cells) are an invaluable model system to address cell fate specification. Crest cells are amenable to tissue culture, and they differentiate to a variety of neuronal and nonneuronal cell types. Earlier studies have determined that bone morphogenetic proteins (BMP-2, -4, and -7) and agents that elevate intracellular cyclic AMP (cAMP) stimulate the development of the sympathoadrenal (SA, adrenergic) lineage in neural crest cultures. To investigate whether interactive mechanisms between signaling pathways influence crest cell differentiation, we characterized the combinatorial effects of BMP-2 and cAMP-elevating agents on the development of quail trunk neural crest cells in primary culture. We report that the cAMP signaling pathway modulates both positive and negative signals influencing the development of SA cells. Specifically, we show that moderate activation of cAMP signaling promotes, in synergy with BMP-2, SA cell development and the expression of the SA lineage-determining gene Phox2a. By contrast, robust activation of cAMP signaling opposes, even in the presence of BMP-2, SA cell development and the expression of the SA lineage-determining ASH-1 and Phox2 genes. We conclude that cAMP signaling acts as a bimodal regulator of SA cell development in neural crest cultures.

scholarly journals Migrating neural crest cells in the trunk of the avian embryo are multipotent

Development ◽  
1991 ◽  
Vol 112 (4) ◽  
pp. 913-920 ◽  
Author(s):  
S.E. Fraser ◽  
M. Bronner-Fraser
Keyword(s):  
Neural Crest ◽  
Neural Tube ◽  
Sympathetic Neurons ◽  
Morphological Characteristics ◽  
Neural Crest Cells ◽  
Cell Types ◽  
Sympathetic Ganglia ◽  
Avian Embryo ◽  
Developmental Potential ◽  
Trunk Neural Crest

Trunk neural crest cells migrate extensively and give rise to diverse cell types, including cells of the sensory and autonomic nervous systems. Previously, we demonstrated that many premigratory trunk neural crest cells give rise to descendants with distinct phenotypes in multiple neural crest derivatives. The results are consistent with the idea that neural crest cells are multipotent prior to their emigration from the neural tube and become restricted in phenotype after leaving the neural tube either during their migration or at their sites of localization. Here, we test the developmental potential of migrating trunk neural crest cells by microinjecting a vital dye, lysinated rhodamine dextran (LRD), into individual cells as they migrate through the somite. By two days after injection, the LRD-labelled clones contained from 2 to 67 cells, which were distributed unilaterally in all embryos. Most clones were confined to a single segment, though a few contributed to sympathetic ganglia over two segments. A majority of the clones gave rise to cells in multiple neural crest derivatives. Individual migrating neural crest cells gave rise to both sensory and sympathetic neurons (neurofilament-positive), as well as cells with the morphological characteristics of Schwann cells, and other non-neuronal cells (both neurofilament-negative). Even those clones contributing to only one neural crest derivative often contained both neurofilament-positive and neurofilament-negative cells. Our data demonstrate that migrating trunk neural crest cells can be multipotent, giving rise to cells in multiple neural crest derivatives, and contributing to both neuronal and non-neuronal elements within a given derivative.(ABSTRACT TRUNCATED AT 250 WORDS)

scholarly journals Neuromesodermal progenitor origin of trunk neural crest in vivo

2021 ◽  
Author(s):  
Martyna Lukoseviciute ◽  
Sarah Mayes ◽  
Tatjana Sauka-Spengler
Keyword(s):  
Neural Crest ◽  
Single Cell Analysis ◽  
Neuronal Cell ◽  
Cell Types ◽  
Neural Cells ◽  
Embryonic Cells ◽  
Cell Fates ◽  
Trunk Neural Crest ◽  
Bona Fide

AbstractNeural crest (NC) is a vertebrate-specific population of multipotent embryonic cells predisposed to particular derivatives along the anteroposterior (A-P) axis. While only cranial NC progenitors give rise to ectomesenchymal cell types, trunk NC is biased for neuronal cell fates. By integrating multimodal single-cell analysis we uncovered heterogenous NC cells across the entire A-P axis expressing NC regulator foxd3. We pinpointed to its specific cranial and trunk auto-regulated enhancers. The trunk foxd3 enhancer, however, did not mark the bona fide NC, but bipotent tailbud neuromesodermal progenitors (NMps). A subset of these NMp-derived pro-neural cells appeared to give rise to neuronal trunk NC in amniotes in vivo, suggesting that at least a portion of trunk NC progenitors with a bias for neuronal fates originated from NMps in vivo.

Restriction of neural crest cell fate in the trunk of the embryonic zebrafish

Development ◽  
1994 ◽  
Vol 120 (3) ◽  
pp. 495-503 ◽  
Author(s):  
D.W. Raible ◽  
J.S. Eisen
Keyword(s):  
Neural Crest ◽  
Cell Fate ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Multiple Phenotypes ◽  
Trunk Neural Crest ◽  
Cell Type Specific ◽  
Derivatives Of ◽  
Crest Cell ◽  
Do So

To learn when cell fate differences first arise in the zebrafish trunk neural crest, individual premigratory crest cells were labeled intracellularly with fluorescent vital dyes, followed in living embryos and complete lineages recorded. Although some of the earliest cells to migrate produced derivatives of multiple phenotypes, most zebrafish trunk neural crest cells appear to be lineage-restricted, generating type-restricted precursors that produce single kinds of derivatives. Further, cells that produce derivatives of multiple phenotypes appear to do so by first generating type-restricted precursors. Among the various types of derivatives, sensory and sympathetic cells arise only from early migrating crest cells. Some type-restricted precursors display cell-type-specific characteristics while still migrating. Taken together, these observations suggest that some trunk neural crest cells are specified before reaching their final locations.

The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate

Development ◽  
2001 ◽  
Vol 128 (21) ◽  
pp. 4127-4138 ◽  
Author(s):  
Mirella Dottori ◽  
Michael K. Gross ◽  
Patricia Labosky ◽  
Martyn Goulding
Keyword(s):  
Transcription Factor ◽  
Neural Crest ◽  
Cell Fate ◽  
Neural Tube ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Cell Types ◽  
Winged Helix ◽  
Multiple Cell ◽  
Winged Helix Transcription Factor

The neural crest is a migratory cell population that gives rise to multiple cell types in the vertebrate embryo. The intrinsic determinants that segregate neural crest cells from multipotential dorsal progenitors within the neural tube are poorly defined. In this study, we show that the winged helix transcription factor Foxd3 is expressed in both premigratory and migratory neural crest cells. Foxd3 is genetically downstream of Pax3 and is not expressed in regions of Pax3 mutant mice that lack neural crest, implying that Foxd3 may regulate aspects of the neural crest differentiation program. We show that misexpression of Foxd3 in the chick neural tube promotes a neural crest-like phenotype and suppresses interneuron differentiation. Cells that ectopically express Foxd3 upregulate HNK1 and Cad7, delaminate and emigrate from the neural tube at multiple dorsoventral levels. Foxd3 does not induce Slug and RhoB, nor is its ability to promote a neural crest-like phenotype enhanced by co-expression of Slug. Together these results suggest Foxd3 can function independently of Slug and RhoB to promote the development of neural crest cells from neural tube progenitors.

scholarly journals Single cell RNA analysis of trunk neural crest cells in zebrafish identifies pre-migratory populations expressing markers of differentiated derivatives

2020 ◽  
Author(s):  
Ezra Lencer ◽  
Rytis Prekeris ◽  
Kristin Bruk Artinger
Keyword(s):  
Neural Crest ◽  
Single Cell ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Cell Types ◽  
Vertebrate Development ◽  
Multiple Traits ◽  
Transcriptional Changes ◽  
Trunk Neural Crest ◽  
Crest Cell

AbstractThe neural crest is a migratory population of stem-like cells that contribute to multiple traits including the bones of the skull, peripheral nervous system, and pigment. How neural crest cells differentiate into diverse cell types is a fundamental question in the study of vertebrate biology. Here, we use single cell RNA sequencing to characterize transcriptional changes associated with neural crest cell development in the zebrafish trunk during the early stages of migration. We show that neural crest cells are transcriptionally diverse, and identify pre-migratory populations already expressing genes associated with differentiated derivatives. Further, we identify a population of Rohon-Beard neurons that are shown to be sources of Fgf signaling in the zebrafish trunk. The data presented identify novel genetic markers for multiple trunk neural crest cell populations and Rohon-Beard neurons providing insight into previously uncharacterized genes critical for vertebrate development.

scholarly journals Cell lineage analysis of the avian neural crest

Development ◽  
1991 ◽  
Vol 113 (Supplement_2) ◽  
pp. 17-22 ◽  
Author(s):  
Marianne Bronner-Fraser ◽  
Scott E. Fraser
Keyword(s):  
Neural Crest ◽  
Cell Fate ◽  
Neural Tube ◽  
Sympathetic Neurons ◽  
Cell Lineage ◽  
Morphological Characteristics ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Developmental Potential ◽  
Trunk Neural Crest

Neural crest cells migrate extensively and give rise to diverse cell types, including cells of the sensory and autonomic nervous systems. A major unanswered question concerning the neural crest is when and how the neural crest cells become determined to adopt a particular fate. We have explored the developmental potential of trunk neural crest cells in avian embryos by microinjecting a vital dye, lysinated rhodamine dextran (LRD), into individual cells within the dorsal neural tube. We find that premigratory and emigrating neural crest cells give rise to descendants with distinct phenotypes in multiple neural crest derivatives. These results are consistent with the idea that neural crest cells are multipotent prior to their emigration from the neural tube and become restricted in phenotype after emigration from the neural tube either during their migration or at their sites of localization. To determine whether neural crest cells become restricted during their migration, we have microinjected individual trunk neural crest cells with dye shortly after they leave the neural tube or as they migrate through the somite. We find that a majority of the clones derived from migrating neural crest cells appear to be multipotent; individual migrating neural crest cells gave rise to both sensory and sympathetic neurons, as well as cells with the morphological characteristics of Schwann cells, and other nonneuronal cells. Even those clones contributing to only one neural crest derivative often contained both neurofilament-positive and neurofilament-negative cells. These data demonstrate that migrating trunk neural crest cells, like their premigratory progenitors, can be multipotent. They give rise to cells in multiple neural crest derivatives and contribute to both neuronal and non-neuronal elements within a given derivative. Thus, restriction of neural crest cell fate must occur relatively late in migration or at the final destinations.

scholarly journals Trunk neural crest origin of dermal denticles in a cartilaginous fish

2017 ◽  
Vol 114 (50) ◽  
pp. 13200-13205 ◽  
Author(s):  
J. Andrew Gillis ◽  
Els C. Alsema ◽  
Katharine E. Criswell
Keyword(s):  
Neural Crest ◽  
Cell Lineage ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Skeletal Tissue ◽  
Trunk Neural Crest ◽  
Neural Crest Origin ◽  
Cranial Neural Crest Cells

Cartilaginous fishes (e.g., sharks and skates) possess a postcranial dermal skeleton consisting of tooth-like “denticles” embedded within their skin. As with teeth, the principal skeletal tissue of dermal denticles is dentine. In the head, cranial neural crest cells give rise to the dentine-producing cells (odontoblasts) of teeth. However, trunk neural crest cells are generally regarded as nonskeletogenic, and so the embryonic origin of trunk denticle odontoblasts remains unresolved. Here, we use expression of FoxD3 to pinpoint the specification and emigration of trunk neural crest cells in embryos of a cartilaginous fish, the little skate (Leucoraja erinacea). Using cell lineage tracing, we further demonstrate that trunk neural crest cells do, in fact, give rise to odontoblasts of trunk dermal denticles. These findings expand the repertoire of vertebrate trunk neural crest cell fates during normal development, highlight the likely primitive skeletogenic potential of this cell population, and point to a neural crest origin of dentine throughout the ancestral vertebrate dermal skeleton.

TGF-β Signaling and its Functional Significance in Regulating the Fate of Cranial Neural Crest Cells

2003 ◽  
Vol 14 (2) ◽  
pp. 78-88 ◽  
Author(s):  
Y. Chai ◽  
Y. Ito ◽  
J. Han
Keyword(s):  
Neural Crest ◽  
Transforming Growth Factor ◽  
Neural Crest Cells ◽  
Transforming Growth Factor Β ◽  
Cell Types ◽  
Cranial Neural Crest ◽  
Multipotent Progenitors ◽  
Smad Proteins ◽  
Β Receptor ◽  
Cranial Neural Crest Cells

Members of the transforming growth factor-β (TGF-β) superfamily regulate cell proliferation, differentiation, and apoptosis, and control the development and maintenance of most tissues. TGF-β signal is transmitted through the phosphorylation of Smad proteins by TGF-β receptor serine/threonine kinase. During craniofacial development, TGF-β may regulate the fate specification of cranial neural crest cells. These cells are multipotent progenitors and capable of producing diverse cell types upon differentiation. Here we summarize evidence that TGF-β ligands and their signaling intermediates have significant roles in patterning and specification of cranial neural crest cells. The biological function of TGF-β is carried out through the regulation of transcriptional factors during embryogenesis.

scholarly journals Clonal analysis and dynamic imaging identify multipotency of individual Gallus gallus caudal hindbrain neural crest cells toward cardiac and enteric fates

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Weiyi Tang ◽  
Yuwei Li ◽  
Ang Li ◽  
Marianne E. Bronner
Keyword(s):  
Neural Crest ◽  
Single Cell ◽  
Cell Fate ◽  
Neural Crest Cells ◽  
Time Lapse ◽  
Cell Types ◽  
Clonal Analysis ◽  
Dynamic Imaging ◽  
Lineage Tracing ◽  
Enteric Ganglia

AbstractNeural crest stem cells arising from caudal hindbrain (often called cardiac and posterior vagal neural crest) migrate long distances to form cell types as diverse as heart muscle and enteric ganglia, abnormalities of which lead to common congenital birth defects. Here, we explore whether individual caudal hindbrain neural crest precursors are multipotent or predetermined toward these particular fates and destinations. To this end, we perform lineage tracing of chick neural crest cells at single-cell resolution using two complementary approaches: retrovirally mediated multiplex clonal analysis and single-cell photoconversion. Both methods show that the majority of these neural crest precursors are multipotent with many clones producing mesenchymal as well as neuronal derivatives. Time-lapse imaging demonstrates that sister cells can migrate in distinct directions, suggesting stochasticity in choice of migration path. Perturbation experiments further identify guidance cues acting on cells in the pharyngeal junction that can influence this choice; loss ofCXCR4signaling results in failure to migrate to the heart but no influence on migration toward the foregut, whereas loss ofRETsignaling does the opposite. Taken together, the results suggest that environmental influences rather than intrinsic information govern cell fate choice of multipotent caudal hindbrain neural crest cells.

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