scholarly journals Completion of neural crest cell production and emigration is regulated by retinoic acid-dependent inhibition of BMP signaling

2021 ◽  
Author(s):  
Dina Rekler ◽  
Chaya Kalcheim
Keyword(s):  
Retinoic Acid ◽  
Neural Crest ◽  
Neural Tube ◽  
Single Cells ◽  
Neural Crest Cell ◽  
Bmp Signaling ◽  
Retinoic Acid Signaling ◽  
Molecular Architecture ◽  
Roof Plate ◽  
Dependent Inhibition

Production and emigration of neural crest cells is a transient process followed by the emergence of the definitive roof plate. The mechanisms regulating the end of neural crest ontogeny are poorly understood. Whereas early crest development is stimulated by mesoderm-derived retinoic acid, we report that the end of the neural crest period is regulated by retinoic acid synthesized in the dorsal neural tube. Inhibition of retinoic acid signaling in the neural tube prevents the normal upregulation of BMP inhibitors in the nascent roof plate and prolongs the period of BMP responsiveness which otherwise ceases close to roof plate establishment. Consequently, neural crest production and emigration are extended well into the roof plate stage. Although several roof plate-specific genes are normally expressed in the absence of retinoic acid signaling, roof plate and crest markers are co-expressed in single cells and this domain also contains dorsal interneurons. Hence, the cellular and molecular architecture of the roof plate is compromised. Collectively, our results demonstrate that neural tube-derived retinoic acid, via inhibition of BMP signaling, is an essential factor responsible for the end of neural crest generation and the proper segregation of dorsal neural lineages.

scholarly journals Vital dye labelling of Xenopus laevis trunk neural crest reveals multipotency and novel pathways of migration

Development ◽  
1993 ◽  
Vol 118 (2) ◽  
pp. 363-376 ◽  
Author(s):  
A. Collazo ◽  
M. Bronner-Fraser ◽  
S.E. Fraser
Keyword(s):  
Xenopus Laevis ◽  
Neural Crest ◽  
Neural Tube ◽  
Single Cells ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Pigment Cells ◽  
Spinal Ganglia ◽  
Posterior Portion ◽  
Precise Position

Although the Xenopus embryo has served as an important model system for both molecular and cellular studies of vertebrate development, comparatively little is known about its neural crest. Here, we take advantage of the ease of manipulation and relative transparency of Xenopus laevis embryos to follow neural crest cell migration and differentiation in living embryos. We use two techniques to study the lineage and migratory patterns of frog neural crest cells: (1) injections of DiI or lysinated rhodamine dextran (LRD) into small populations of neural crest cells to follow movement and (2) injections of LRD into single cells to follow cell lineage. By using non-invasive approaches that allow observations in living embryos and control of the time and position of labelling, we have been able to expand upon the results of previous grafting experiments. Migration and differentiation of the labelled cells were observed over time in individual living embryos, and later in sections to determine precise position and morphology. Derivatives populated by the neural crest are the fins, pigment stripes, spinal ganglia, adrenal medulla, pronephric duct, enteric nuclei and the posterior portion of the dorsal aorta. In the rostral to mid-trunk levels, most neural crest cells migrate along two paths: a dorsal pathway into the fin, followed by presumptive fin cells, and a ventral pathway along the neural tube and notochord, followed by presumptive pigment, sensory ganglion, sympathetic ganglion and adrenal medullary cells. In the caudal trunk, two additional paths were noted. One group of cells moves circumferentially within the fin, in an arc from dorsal to ventral; another progresses ventrally to the anus and subsequently populates the ventral fin. By labelling individual precursor cells, we find that neural tube and neural crest cells often share a common precursor. The majority of clones contain labelled progeny cells in the dorsal fin. The remainder have progeny in multiple derivatives including spinal ganglion cells, pigment cells, enteric cells, fin cells and/or neural tube cells in all combinations, suggesting that many premigratory Xenopus neural crest precursors are multipotent.

A role for rhoB in the delamination of neural crest cells from the dorsal neural tube

Development ◽  
1998 ◽  
Vol 125 (24) ◽  
pp. 5055-5067 ◽  
Author(s):  
J.P. Liu ◽  
T.M. Jessell
Keyword(s):  
Neural Crest ◽  
Cell Fate ◽  
Neural Tube ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Bmp Signaling ◽  
Dorsal Neural Tube ◽  
Rho Family ◽  
Neural Crest Differentiation ◽  
Crest Cell

The differentiation of neural crest cells from progenitors located in the dorsal neural tube appears to involve three sequential steps: the specification of premigratory neural crest cell fate, the delamination of these cells from the neural epithelium and the migration of neural crest cells in the periphery. BMP signaling has been implicated in the specification of neural crest cell fate but the mechanisms that control the emergence of neural crest cells from the neural tube remain poorly understood. To identify molecules that might function at early steps of neural crest differentiation, we performed a PCR-based screen for genes induced by BMPs in chick neural plate cells. We describe the cloning and characterization of one gene obtained from this screen, rhoB, a member of the rho family GTP-binding proteins. rhoB is expressed in the dorsal neural tube and its expression persists transiently in migrating neural crest cells. BMPs induce the neural expression of rhoB but not the more widely expressed rho family member, rhoA. Inhibition of rho activity by C3 exotoxin prevents the delamination of neural crest cells from neural tube explants but has little effect on the initial specification of premigratory neural crest cell fate or on the later migration of neural crest cells. These results suggest that rhoB has a role in the delamination of neural crest cells from the dorsal neural tube.

scholarly journals Developmental potential of trunk neural crest cells in the mouse

Development ◽  
1994 ◽  
Vol 120 (7) ◽  
pp. 1709-1718 ◽  
Author(s):  
G.N. Serbedzija ◽  
M. Bronner-Fraser ◽  
S.E. Fraser
Keyword(s):  
Neural Crest ◽  
Neural Tube ◽  
Mouse Embryo ◽  
Dorsal Root ◽  
Single Cells ◽  
Neural Crest Cell ◽  
Experimental System ◽  
Neural Crest Cells ◽  
Pigment Cells ◽  
Developmental Potential

The availability of naturally occurring and engineered mutations in mice which affect the neural crest makes the mouse embryo an important experimental system for studying neural crest cell differentiation. Here, we determine the normal developmental potential of neural crest cells by performing in situ cell lineage analysis in the mouse by microinjecting lysinated rhodamine dextran (LRD) into individual dorsal neural tube cells in the trunk. Labeled progeny derived from single cells were found in the neural tube, dorsal root ganglia, sympathoadrenal derivatives, presumptive Schwann cells and/or pigment cells. Most embryos contained labeled cells both in the neural tube and at least one neural crest derivative, and numerous clones contributed to multiple neural crest derivatives. The time of injection influenced the derivatives populated by the labeled cells. Injections at early stages of migration yielded labeled progeny in both dorsal and ventral neural crest derivatives, whereas those performed at later stages had labeled cells only in more dorsal neural crest derivatives, such as dorsal root ganglion and presumptive pigment cells. The results suggest that in the mouse embryo: (1) there is a common precursor for neural crest and neural tube cells; (2) some neural crest cells are multipotent; and (3) the timing of emigration influences the range of possible neural crest derivatives.

Retinoid-binding protein distribution in the developing mammalian nervous system

Development ◽  
1990 ◽  
Vol 109 (1) ◽  
pp. 75-80 ◽  
Author(s):  
M. Maden ◽  
D.E. Ong ◽  
F. Chytil
Keyword(s):  
Nervous System ◽  
Retinoic Acid ◽  
Neural Crest ◽  
Motor Neurons ◽  
Neural Tube ◽  
Binding Protein ◽  
Sympathetic Ganglia ◽  
Retinol Binding Protein ◽  
Otic Vesicle ◽  
Protein Distribution

We have analysed the distribution of cellular retinol-binding protein (CRBP) and cellular retinoic acid-binding protein (CRABP) in the day 8.5-day 12 mouse and rat embryo. CRBP is localised in the heart, gut epithelium, notochord, otic vesicle, sympathetic ganglia, lamina terminalis of the brain, and, most strikingly, in a ventral stripe across the developing neural tube in the future motor neuron region. This immunoreactivity remains in motor neurons and, at later stages, motor axons are labelled in contrast to unlabelled sensory axons. CRABP is localised to the neural crest cells, which are particularly noticeable streaming into the branchial arches. At later stages, neural crest derivatives such as Schwann cells, cells in the gut wall and sympathetic ganglia are immunoreactive. An additional area of CRABP-positive cells are neuroblasts in the mantle layer of the neural tube, which subsequently appear to be the axons and cell bodies of the commissural system. Since retinol and retinoic acid are the endogenous ligands for these binding proteins, we propose that retinoids may play a role in the development and differentiation of the mammalian nervous system and may interact with certain homoeobox genes whose transcripts have also been localised within the nervous system.

The relationship between emerging neural crest cells and basement membranes in the trunk of the mouse embryo: a TEM and immunocytochemical study

Development ◽  
1986 ◽  
Vol 98 (1) ◽  
pp. 251-268
Author(s):  
J. Sternberg ◽  
S. J. Kimber
Keyword(s):  
Neural Crest ◽  
Neural Tube ◽  
Cell Shape ◽  
Type Iv Collagen ◽  
Neural Crest Cell ◽  
Basement Membranes ◽  
Type Iv ◽  
Transmission Electron ◽  
The Relationship ◽  
Crest Cell

The earliest stage of neural crest cell (NCC) migration is characterized by an epitheliomesenchymal transformation, as the cells leave the neural tube. There is evidence that in a number of cell systems this transformation is accompanied by alteration or depletion of associated basement membranes. This study examines the ultrastructural relationship between mouse NCCs and adjacent basement membranes during the earliest stages of migration from the neural tube. Basement membranes were identified by transmission electron microscopy (TEM) and immunofluorescence using antibodies to type-IV collagen. The ultrastructural features of NCCs and their relationship with surrounding tissues were also examined using TEM. In the dorsal region of the neural tube, from which NCCs originate, the basement membrane was depleted or absent, and with the immunofluorescence technique it was shown that this pattern was reflected in a deficit of type-IV collagen. TEM observations indicated that ultrastructurally NCCs differ from their neuroepithelial neighbours only in overall cell shape and their relationship to other cells and the extracellular matrix.

scholarly journals Role of FGF signalling in neural crest cell migration during early chick embryo development

Zygote ◽  
2018 ◽  
Vol 26 (6) ◽  
pp. 457-464 ◽  
Author(s):  
Xiao-tan Zhang ◽  
Guang Wang ◽  
Yan Li ◽  
Manli Chuai ◽  
Kenneth Ka Ho Lee ◽  
...  
Keyword(s):  
Neural Crest ◽  
Neural Tube ◽  
Neural Crest Cell ◽  
Dominant Negative ◽  
Neural Tubes ◽  
Dorsal Neural Tube ◽  
Neural Crest Cell Migration ◽  
Fgf Signalling ◽  
Crest Cell

SummaryFibroblast growth factor (FGF) signalling acts as one of modulators that control neural crest cell (NCC) migration, but how this is achieved is still unclear. In this study, we investigated the effects of FGF signalling on NCC migration by blocking this process. Constructs that were capable of inducing Sprouty2 (Spry2) or dominant-negative FGFR1 (Dn-FGFR1) expression were transfected into the cells making up the neural tubes. Our results revealed that blocking FGF signalling at stage HH10 (neurulation stage) could enhance NCC migration at both the cranial and trunk levels in the developing embryos. It was established that FGF-mediated NCC migration was not due to altering the expression of N-cadherin in the neural tube. Instead, we determined that cyclin D1 was overexpressed in the cranial and trunk levels when Sprouty2 was upregulated in the dorsal neural tube. These results imply that the cell cycle was a target of FGF signalling through which it regulates NCC migration at the neurulation stage.

scholarly journals A vital dye analysis of the timing and pathways of avian trunk neural crest cell migration

Development ◽  
1989 ◽  
Vol 106 (4) ◽  
pp. 809-816 ◽  
Author(s):  
G.N. Serbedzija ◽  
M. Bronner-Fraser ◽  
S.E. Fraser
Keyword(s):  
Neural Crest ◽  
Neural Tube ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Sympathetic Ganglia ◽  
Pigment Cells ◽  
Root Cells ◽  
Vital Dye ◽  
Rostral Portion ◽  
Crest Cell

To permit a more detailed analysis of neural crest cell migratory pathways in the chick embryo, neural crest cells were labelled with a nondeleterious membrane intercalating vital dye, DiI. All neural tube cells with endfeet in contact with the lumen, including premigratory neural crest cells, were labelled by pressure injecting a solution of DiI into the lumen of the neural tube. When assayed one to three days later, migrating neural crest cells, motor axons, and ventral root cells were the only cells types external to the neural tube labelled with DiI. During the neural crest cell migratory phase, distinctly labelled cells were found along: (1) a dorsolateral pathway, under the epidermis, as well adjacent to and intercalating through the dermamyotome; and (2) a ventral pathway, through the rostral portion of each sclerotome and around the dorsal aorta as described previously. In contrast to those cells migrating through the sclerotome, labelled cells on the dorsolateral pathway were not segmentally arranged along the rostrocaudal axis. DiI-labelled cells were observed in all truncal neural crest derivatives, including subepidermal presumptive pigment cells, dorsal root ganglia, and sympathetic ganglia. By varying the stage at which the injection was performed, neural crest cell emigration at the level of the wing bud was shown to occur from stage 13 through stage 22. In addition, neural crest cells were found to populate their derivatives in a ventral-to-dorsal order, with the latest emigrating cells migrating exclusively along the dorsolateral pathway.

The distribution of fibronectin and tenascin along migratory pathways of the neural crest in the trunk of amphibian embryos

Development ◽  
1988 ◽  
Vol 103 (4) ◽  
pp. 743-756 ◽  
Author(s):  
H.H. Epperlein ◽  
W. Halfter ◽  
R.P. Tucker
Keyword(s):  
Cell Migration ◽  
Neural Crest ◽  
Neural Tube ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Pigment Cells ◽  
Dorsal Fin ◽  
Amphibian Embryos ◽  
Neural Crest Cell Migration ◽  
Crest Cell

It is generally assumed that in amphibian embryos neural crest cells migrate dorsally, where they form the mesenchyme of the dorsal fin, laterally (between somites and epidermis), where they give rise to pigment cells, and ventromedially (between somites and neural tube), where they form the elements of the peripheral nervous system. While there is agreement about the crest migratory routes in the axolotl (Ambystoma mexicanum), different opinions exist about the lateral pathway in Xenopus. We investigated neural crest cell migration in Xenopus (stages 23, 32, 35/36 and 41) using the X. laevis-X. borealis nuclear marker system and could not find evidence for cells migrating laterally. We have also used immunohistochemistry to study the distribution of the extracellular matrix (ECM) glycoproteins fibronectin (FN) and tenascin (TN), which have been implicated in directing neural crest cells during their migrations in avian and mammalian embryos, in the neural crest migratory pathways of Xenopus and the axolotl. In premigratory stages of the crest, both in Xenopus (stage 22) and the axolotl (stage 25), FN was found subepidermally and in extracellular spaces around the neural tube, notochord and somites. The staining was particularly intense in the dorsal part of the embryo, but it was also present along the visceral and parietal layers of the lateral plate mesoderm. TN, in contrast, was found only in the anterior trunk mesoderm in Xenopus; in the axolotl, it was absent. During neural crest cell migration in Xenopus (stages 25–33) and the axolotl (stages 28–35), anti-FN stained the ECM throughout the embryo, whereas anti-TN staining was limited to dorsal regions. There it was particularly intense medially, i.e. in the dorsal fin, around the neural tube, notochord, dorsal aorta and at the medial surface of the somites (stage 35 in both species). During postmigratory stages in Xenopus (stage 40), anti-FN staining was less intense than anti-TN staining. In culture, axolotl neural crest cells spread differently on FN- and TN-coated substrata. On TN, the onset of cellular outgrowth was delayed for about 1 day, but after 3 days the extent of outgrowth was indistinguishable from cultures grown on FN. However, neural crest cells in 3-day-old cultures were much more flattened on FN than on TN. We conclude that both FN and TN are present in the ECM that lines the neural crest migratory pathways of amphibian embryos at the time when the neural crest cells are actively migrating. FN is present in the embryonic ECM before the onset of neural crest migration.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals BMP signaling is necessary for neural crest cell migration and ganglion formation in the enteric nervous system

2005 ◽  
Vol 122 (6) ◽  
pp. 821-833 ◽  
Author(s):  
Allan M. Goldstein ◽  
Katherine C. Brewer ◽  
Adele M. Doyle ◽  
Nandor Nagy ◽  
Drucilla J. Roberts
Keyword(s):  
Nervous System ◽  
Cell Migration ◽  
Neural Crest ◽  
Enteric Nervous System ◽  
Neural Crest Cell ◽  
Bmp Signaling ◽  
Neural Crest Cell Migration ◽  
Crest Cell
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