Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head

Development ◽  
2002 ◽  
Vol 129 (4) ◽  
pp. 1061-1073 ◽  
Author(s):  
Gérard Couly ◽  
Sophie Creuzet ◽  
Selim Bennaceur ◽  
Christine Vincent ◽  
Nicole M. Le Douarin
Keyword(s):  
Neural Crest ◽  
Hox Genes ◽  
Neural Crest Cells ◽  
Facial Skeleton ◽  
Facial Bones ◽  
Embryonic Axes ◽  
Branchial Arches ◽  
Upper Face ◽  
Neural Crest Origin ◽  
Foregut Endoderm

The vertebrate face contains bones that differentiate from mesenchymal cells of neural crest origin, which colonize the median nasofrontal bud and the first branchial arches. The patterning of individual facial bones and their relative positions occurs through mechanisms that remained elusive. During the early stages of head morphogenesis, an endodermal cul-de-sac, destined to become Sessel’s pouch, underlies the nasofrontal bud. Reiterative outpocketings of the foregut then form the branchial pouches. We have tested the capacity of endoderm of the avian neurula to specify the facial skeleton by performing ablations or grafts of defined endodermal regions. Neural crest cells that do not express Hox genes respond to patterning cues produced regionally in the anterior endoderm to yield distinct skeletal components of the upper face and jaws. However, Hox-expressing neural crest cells do not respond to these cues. Bone orientation is likewise dependent on the position of the endoderm relative to the embryonic axes. Our findings thus indicate that the endoderm instructs neural crest cells as to the size, shape and position of all the facial skeletal elements, whether they are cartilage or membrane bones.

The developmental fate of the cephalic mesoderm in quail-chick chimeras

Development ◽  
1992 ◽  
Vol 114 (1) ◽  
pp. 1-15 ◽  
Author(s):  
G.F. Couly ◽  
P.M. Coltey ◽  
N.M. Le Douarin
Keyword(s):  
Neural Crest ◽  
Neural Crest Cells ◽  
Paraxial Mesoderm ◽  
Avian Embryo ◽  
Facial Skeleton ◽  
Developmental Fate ◽  
Prechordal Mesoderm ◽  
The Face ◽  
Neural Crest Origin ◽  
Neurula Stage

The developmental fate of the cephalic paraxial and prechordal mesoderm at the late neurula stage (3-somite) in the avian embryo has been investigated by using the isotopic, isochronic substitution technique between quail and chick embryos. The territories involved in the operation were especially tiny and the size of the transplants was of about 150 by 50 to 60 microns. At that stage, the neural crest cells have not yet started migrating and the fate of mesodermal cells exclusively was under scrutiny. The prechordal mesoderm was found to give rise to the following ocular muscles: musculus rectus ventralis and medialis and musculus oblicus ventralis. The paraxial mesoderm was separated in two longitudinal bands: one median, lying upon the cephalic vesicles (median paraxial mesoderm—MPM); one lateral, lying upon the foregut (lateral paraxial mesoderm—LPM). The former yields the three other ocular muscles, contributes to mesencephalic meninges and has essentially skeletogenic potencies. It contributes to the corpus sphenoid bone, the orbitosphenoid bone and the otic capsules; the rest of the facial skeleton is of neural crest origin. At 3-somite stage, MPM is represented by a few cells only. The LPM is more abundant at that stage and has essentially myogenic potencies with also some contribution to connective tissue. However, most of the connective cells associated with the facial and hypobranchial muscles are of neural crest origin. The more important result of this work was to show that the cephalic mesoderm does not form dermis. This function is taken over by neural crest cells, which form both the skeleton and dermis of the face. If one draws a parallel between the so-called “somitomeres” of the head and the trunk somites, it appears that skeletogenic potencies are reduced in the former, which in contrast have kept their myogenic capacities, whilst the formation of skeleton and dermis has been essentially taken over by the neural crest in the course of evolution of the vertebrate head.

The regeneration of the cephalic neural crest, a problem revisited: the regenerating cells originate from the contralateral or from the anterior and posterior neural fold

Development ◽  
1996 ◽  
Vol 122 (11) ◽  
pp. 3393-3407 ◽  
Author(s):  
G. Couly ◽  
A. Grapin-Botton ◽  
P. Coltey ◽  
N.M. Le Douarin
Keyword(s):  
Neural Crest ◽  
Neural Tube ◽  
Hox Genes ◽  
Experimental Situation ◽  
Neural Crest Cells ◽  
Fate Map ◽  
Somite Stage ◽  
Dorsal Neural Tube ◽  
Ventral Neural Tube ◽  
Branchial Arches

The mesencephalic and rhombencephalic levels of origin of the hypobranchial skeleton (lower jaw and hyoid bone) within the neural fold have been determined at the 5-somite stage with a resolution corresponding to each single rhombomere, by means of the quail-chick chimera technique. Expression of certain Hox genes (Hoxa-2, Hoxa-3 and Hoxb-4) was recorded in the branchial arches of chick and quail embryos at embryonic days 3 (E3) and E4. This was a prerequisite for studying the regeneration capacities of the neural crest, after the dorsal neural tube was resected at the mesencephalic and rhombencephalic level. We found first that excisions at the 5-somite stage extending from the midmesencephalon down to r8 are followed by the regeneration of neural crest cells able to compensate for the deficiencies so produced. This confirmed the results of previous authors who made similar excisions at comparable (or older) developmental stages. When a bilateral excision was followed by the unilateral homotopic graft of the dorsal neural tube from a quail embryo, thus mimicking the situation created by a unilateral excision, we found that the migration of the grafted unilateral neural crest (quail-labelled) is bilateral and compensates massively for the missing crest derivatives. The capacity of the intermediate and ventral neural tube to yield neural crest cells was tested by removing the chick rhombencephalic neural tube and replacing it either uni- or bilaterally with a ventral tube coming from a stage-matched quail. No neural crest cells exited from the ventral neural tube but no deficiency in neural crest derivatives was recorded. Crest cells were found to regenerate from the ends of the operated region. This was demonstrated by grafting fragments of quail neural fold at the extremities of the excised territory. Quail neural crest cells were seen migrating longitudinally from both the rostral and caudal ends of the operated region and filling the branchial arches located inbetween. Comparison of the behaviour of neural crest cells in this experimental situation with that showed by their normal fate map revealed that crest cells increase their proliferation rate and change their migratory behaviour without modifying their Hox code.

scholarly journals A novel spalt gene expressed in branchial arches affects the ability of cranial neural crest cells to populate sensory ganglia

2004 ◽  
Vol 1 (1) ◽  
pp. 57-63 ◽  
Author(s):  
MEYER BAREMBAUM ◽  
MARIANNE BRONNER-FRASER
Keyword(s):  
Neural Crest ◽  
Trigeminal Ganglion ◽  
Neural Tube ◽  
Cell Lineage ◽  
Neural Crest Cells ◽  
Cranial Neural Crest ◽  
Facial Skeleton ◽  
Differentiation Markers ◽  
Branchial Arches ◽  
Cranial Neural Crest Cells

Cranial neural crest cells differentiate into diverse derivatives including neurons and glia of the cranial ganglia, and cartilage and bone of the facial skeleton. Here, we explore the function of a novel transcription factor of the spalt family that might be involved in early cell-lineage decisions of the avian neural crest. The chicken spalt4 gene (csal4) is expressed in the neural tube, migrating neural crest, branchial arches and, transiently, in the cranial ectoderm. Later, it is expressed in the mesectodermal, but not neuronal or glial, derivatives of midbrain and hindbrain neural crest. After over-expression by electroporation into the cranial neural tube and neural crest, we observed a marked redistribution of electroporated neural crest cells in the vicinity of the trigeminal ganglion. In control-electroporated embryos, numerous, labeled neural crest cells (∼80% of the population) entered the ganglion, many of which differentiated into neurons. By contrast, few (∼30% of the population) spalt-electroporated neural crest cells entered the trigeminal ganglion. Instead, they localized in the mesenchyme around the ganglionic periphery or continued further ventrally to the branchial arches. Interestingly, little or no expression of differentiation markers for neurons or other cell types was observed in spalt-electroporated neural crest cells.

Jaw and branchial arch mutants in zebrafish I: branchial arches

Development ◽  
1996 ◽  
Vol 123 (1) ◽  
pp. 329-344 ◽  
Author(s):  
T.F. Schilling ◽  
T. Piotrowski ◽  
H. Grandel ◽  
M. Brand ◽  
C.P. Heisenberg ◽  
...  
Keyword(s):  
Neural Crest ◽  
Zebrafish Embryo ◽  
Neural Crest Cells ◽  
Branchial Arch ◽  
Pigment Cells ◽  
Pharyngeal Arches ◽  
Pectoral Fins ◽  
Branchial Arches ◽  
Group Members ◽  
The Brain

Jaws and branchial arches together are a basic, segmented feature of the vertebrate head. Seven arches develop in the zebrafish embryo (Danio rerio), derived largely from neural crest cells that form the cartilaginous skeleton. In this and the following paper we describe the phenotypes of 109 arch mutants, focusing here on three classes that affect the posterior pharyngeal arches, including the hyoid and five gill-bearing arches. In lockjaw, the hyoid arch is strongly reduced and subsets of branchial arches do not develop. Mutants of a large second class, designated the flathead group, lack several adjacent branchial arches and their associated cartilages. Five alleles at the flathead locus all lead to larvae that lack arches 4–6. Among 34 other flathead group members complementation tests are incomplete, but at least six unique phenotypes can be distinguished. These all delete continuous stretches of adjacent branchial arches and unpaired cartilages in the ventral midline. Many show cell death in the midbrain, from which some neural crest precursors of the arches originate. lockjaw and a few mutants in the flathead group, including pistachio, affect both jaw cartilage and pigmentation, reflecting essential functions of these genes in at least two neural crest lineages. Mutants of a third class, including boxer, dackel and pincher, affect pectoral fins and axonal trajectories in the brain, as well as the arches. Their skeletal phenotypes suggest that they disrupt cartilage morphogenesis in all arches. Our results suggest that there are sets of genes that: (1) specify neural crest cells in groups of adjacent head segments, and (2) function in common genetic pathways in a variety of tissues including the brain, pectoral fins and pigment cells as well as pharyngeal arches.

Participation of neural crest-derived cells in the genesis of the skull in birds

Development ◽  
1978 ◽  
Vol 47 (1) ◽  
pp. 17-37
Author(s):  
Christiane S. Le Lièvre
Keyword(s):  
Neural Crest ◽  
Nuclear Dna ◽  
Neural Crest Cells ◽  
Frontal Bone ◽  
Skeletal Tissue ◽  
Nasal Process ◽  
Branchial Arches ◽  
Mesodermal Origin ◽  
Mixed Origin ◽  
Dual Origin

The differentiation of cephalic neural crest cells into skeletal tissue in birds has been observed using the quail —chick nuclear marking system, which is based on specific differences in the distribution of the nuclear DNA. Chimaeras were formed by replacing a fragment of cephalic neural primordium of a 2- to 12-somite chicken embryo by the corresponding fragment isolated from an equivalent quail embryo. The participation of the graft-derived cells in the formation of the skull of these embryos was studied on histological sections after Feulgen and Rossenbeck staining. Cells from the pirosencephalic neural crest migrate into the frontal nasal process and mix with the mesencephalic neural crest cells in the lateral nasal processes, around the optic cupule and beneath the diencephalon. In addition, the mesencephalic neural crest cells form the bulk of the mesenchyme of the maxillary processes and mandibular arch, whereas the rhombencephalic neural crest cells become located in the branchial arches. The origin of cartilages of the chondrocranium and bones of the neurocranium and viscerocranium has been shown in the chimaeric embryos: the basal plate cartilages, occipital bones, sphenoid bones and the cranial vault are mainly of mesodermal origin. However some parts have a dual origin: rhombo-mesencephalic neural crest cells are found in the otic capsule, and the frontal bone, the rostrum of parasphenoid and the orbital cartilages contain diverse amounts of prosencephalo-mesencephalic neural crest cells. The squamosals and the columella auris are formed from mesectodermic cells as are the nasal skeleton, the palatines and the maxillar bones. The mesectodermal origin of mandibular and hyoid bones and cartilages was already known. From these results it appears that the cephalic neural crest is particularly important in the formation of the facial part of the skull, while the vault and dorsal part are mesodermal and cartilages and bones found in the intermediary region are of mixed origin. The presence of mixed structures implies that the mesoderm and the mesectoderm are equally competent towards the specific inducers of these bones and cartilages. This correlates with the equivalence in differentiation capacities already shown for cephalic mesodeimal and mesectodermal mesenchymes.

An experimental study on neural crest migration in Barbus conchonius (Cyprinidae, Teleostei), with special reference to the origin of the enteroendocrine cells

Development ◽  
1981 ◽  
Vol 62 (1) ◽  
pp. 309-323
Author(s):  
C. H. J. Lamers ◽  
J. W. H. M. Rombout ◽  
L. P. M. Timmermans
Keyword(s):  
Neural Crest ◽  
Neural Tube ◽  
Ganglion Cells ◽  
Neural Crest Cells ◽  
Enteroendocrine Cells ◽  
Pigment Cells ◽  
Transplantation Technique ◽  
Spinal Ganglion Cells ◽  
Neural Crest Origin ◽  
Neural Crest Migration

A neural crest transplantation technique is described for fish. As in other classes ofvertebrates, two pathways of neural crest migration can be distinguished: a lateroventral pathway between somites and ectoderm, and a medioventral pathway between somites and neural tube/notochord. In this paper evidence is presented for a neural crest origin of spinal ganglion cells and pigment cells, and indication for such an origin is obtained for sympathetic and enteric ganglion cells and for cells that are probably homologues to adrenomedullary and paraganglion cells in the future kidney area. The destiny of neural crest cells near the developing lateral-line sense organs is discussed. When grafted into the yolk, neural crest cells or neural tube cells appear to differentiate into ‘periblast cells’; this suggests a highly activating influence of the yolk. Many neural crest cells are found around the urinary ducts and, when grafted below the notochord, even within the urinary duct epithelium. These neural crest cells do not invade the gut epithelium, even when grafted adjacent to the developing gut. Consequently enteroendocrine cells in fish are not likely to have a trunkor rhombencephalic neural crest origin. Another possible origin of these cells will be proposed.

Pax3 is required for cardiac neural crest migration in the mouse: evidence from the splotch (Sp2H) mutant

Development ◽  
1997 ◽  
Vol 124 (2) ◽  
pp. 505-514 ◽  
Author(s):  
S.J. Conway ◽  
D.J. Henderson ◽  
A.J. Copp
Keyword(s):  
Neural Crest ◽  
Neural Tube ◽  
Neural Crest Cells ◽  
Outflow Tract ◽  
Avian Embryo ◽  
Cardiac Neural Crest ◽  
Branchial Arches ◽  
Aortic Arches ◽  
Cardiac Outflow

Neural crest cells originating in the occipital region of the avian embryo are known to play a vital role in formation of the septum of the cardiac outflow tract and to contribute cells to the aortic arches, thymus, thyroid and parathyroids. This ‘cardiac’ neural crest sub-population is assumed to exist in mammals, but without direct evidence. In this paper we demonstrate, using RT-PCR and in situ hybridisation, that Pax3 expression can serve as a marker of cardiac neural crest cells in the mouse embryo. Cells of this lineage were traced from the occipital neural tube, via branchial arches 3, 4 and 6, into the aortic sac and aorto-pulmonary outflow tract. Confirmation that these Pax3-positive cells are indeed cardiac neural crest is provided by experiments in which hearts were deprived of a source of colonising neural crest, by organ culture in vitro, with consequent lack of up-regulation of Pax3. Occipital neural crest cell outgrowths in vitro were also shown to express Pax3. Mutation of Pax3, as occurs in the splotch (Sp2H) mouse, results in development of conotruncal heart defects including persistent truncus arteriosus. Homozygotes also exhibit defects of the aortic arches, thymus, thyroid and parathyroids. Pax3-positive neural crest cells were found to emigrate from the occipital neural tube of Sp2H/Sp2H embryos in a relatively normal fashion, but there was a marked deficiency or absence of neural crest cells traversing branchial arches 3, 4 and 6, and entering the cardiac outflow tract. This decreased expression of Pax3 in Sp2H/Sp2H embryos was not due to down-regulation of Pax3 in neural crest cells, as use of independent neural crest markers, Hoxa-3, CrabpI, Prx1, Prx2 and c-met also revealed a deficiency of migrating cardiac neural crest cells in homozygous embryos. This work demonstrates the essential role of the cardiac neural crest in formation of the heart and great vessels in the mouse and, furthermore, shows that Pax3 function is required for the cardiac neural crest to complete its migration to the developing heart.

Head morphogenesis in embryonic avian chimeras: evidence for a segmental pattern in the ectoderm corresponding to the neuromeres

Development ◽  
1990 ◽  
Vol 108 (4) ◽  
pp. 543-558 ◽  
Author(s):  
G. Couly ◽  
N.M. Le Douarin
Keyword(s):  
Spatial Distribution ◽  
Neural Crest ◽  
Developmental Stage ◽  
Neural Tube ◽  
Neural Crest Cells ◽  
Chick Embryos ◽  
Quail Embryo ◽  
Branchial Arches ◽  
Developmental Unit

Areas of the superficial cephalic ectoderm, including or excluding the neural fold at the same level, were surgically removed from 3-somite chick embryos and replaced by their counterparts excised from a quail embryo at the same developmental stage. Strips of ectoderm corresponding to the presumptive branchial arches were delineated, thus defining anteroposterior ‘segments’ (designated here as ‘ectomeres’) that coincided with the spatial distribution of neural crest cells arising from the adjacent levels of the neural fold. This discrete ectodermal metamerisation parallels the segmentation of the hindbrain into rhombomeres. It seems, therefore, that not only is the neural crest patterned according to its rhombomeric origin but that the superficial ectoderm covering the branchial arches may be part of a larger developmental unit that includes the entire neurectoderm, i.e., the neural tube and the neural crest.

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