Control of pathfinding by the avian trunk neural crest

Development ◽  
1988 ◽  
Vol 103 (Supplement) ◽  
pp. 63-80 ◽  
Author(s):  
Carol A. Erickson

We have determined the pathways taken by the trunk neural crest of quail and examined the parameters that control these patterns of dispersion. Using antibodies that recognize migratory neural crest cells (HNK-1), we have found that the crest cells take three primary pathways: (1) between the ectoderm and somites, (2) within the intersomitic space and (3) through the anterior somite along the basal surface of the myotome. The parameters controlling dispersion patterns of neural crest cells are several. The pathways are filled with at least two adhesive molecules, laminin and fibronectin, to which neural crest cells adhere tenaciously in culture. The pattern of migration through the somite may be accounted for in part by the precocious development of the basal lamina of the dermamyotome in the anterior half of the somite; this basal lamina contains both fibronectin and laminin and the neural crest cells prefer to migrate on it. In contrast, the regions into which the crest cells do not invade are filled with relatively nonadhesive molecules such as chondroitin sulphate. Some of the pathways are filled with hyaluronic acid, which stimulates the migration of neural crest cells when they are cultured in three-dimensional gels, presumably by opening spaces. Neural crest cells are also constrained to stay within the pathways by basal laminae, which act as barriers and through which crest cells do not go. Therefore, crest pathways are probably defined by several redundant factors. The directionality of crest cell migration is probably due to contact inhibition, which can be demonstrated in tissue culture. Various grafting experiments have suggested that chemotaxis and haptotaxis do not play a role in controlling the dispersion of the crest cells away from the neural tube. We have documented the extraordinary ability of neural crest cells to disperse in the embryo, even when they are grafted into sites in which they would normally not migrate. We have evidence that the cells' production of plasminogen activator, a proteolytic enzyme, and also the minimal tractional force that crest cells exert on the substratum as they migrate, contribute to this migratory ability.

Development ◽  
1983 ◽  
Vol 74 (1) ◽  
pp. 97-118
Author(s):  
C. A. Erickson ◽  
J. A. Weston

The cellular morphology and migratory pathways of the trunk neural crest are described in normal mouse embryos, and in embryos homozygous for Patch in which neural crest derivatives develop abnormally. Trunk neural crest cells initially appear in 8½-day embryos as a unique cell population on the dorsal neural tube surface and are relatively rounded. Once they begin to migrate the cells flatten and orient somewhat tangentially to the neural tube, and advance ventrad between the somites and neural tube. At the onset of migration neural crest cells extend lamellipodia onto the surface of the tube while detaching their trailing processes from the lumenal surface. The basal lamina on the dorsal neural tube is discontinuous when cell migration begins in this region. As development proceeds, the basal lamina gradually becomes continuous from a lateral to dorsal direction and neural crest emigration is progressively confined to the narrowing region of discontinuous basal lamina. Cell separation from the neural tube ceases concomitant with completion of a continuous basement membrane. Preliminary observations of the mutant embryos reveal that abnormal extracellular spaces appear and patterns of crest migration are subsequently altered. We conclude that the extracellular matrix, extracellular spaces and basement membranes may delimit crest migration in the mouse.


1986 ◽  
Vol 102 (2) ◽  
pp. 432-441 ◽  
Author(s):  
R B Runyan ◽  
G D Maxwell ◽  
B D Shur

Migrating embryonic cells have high levels of cell surface galactosyltransferase (GalTase) activity. It has been proposed that GalTase participates during migration by recognizing and binding to terminal N-acetylglucosamine (GlcNAc) residues on glycoconjugates within the extracellular matrix (Shur, B. D., 1982, Dev. Biol. 91:149-162). We tested this hypothesis using migrating neural crest cells as an in vitro model system. Cell surface GalTase activity was perturbed using three independent sets of reagents, and the effects on cell migration were analyzed by time-lapse microphotography. The GalTase modifier protein, alpha-lactalbumin (alpha-LA), was used to inhibit surface GalTase binding to terminal GlcNAc residues in the underlying substrate. alpha-LA inhibited neural crest cell migration on basal lamina-like matrices in a dose-dependent manner, while under identical conditions, alpha-LA had no effect on cell migration on fibronectin. Control proteins, such as lysozyme (structurally homologous to alpha-LA) and bovine serum albumin, did not effect migration on either matrix. Second, the addition of competitive GalTase substrates significantly inhibited neural crest cell migration on basal lamina-like matrices, but as above, had no effect on migration on fibronectin. Comparable concentrations of inappropriate sugars also had no effect on cell migration. Third, addition of the GalTase catalytic substrate, UDPgalactose, produced a dose-dependent increase in the rate of cell migration. Under identical conditions, the inappropriate sugar nucleotide, UDPglucose, had no effect. Quantitative enzyme assays confirmed the presence of GalTase substrates in basal lamina matrices, their absence in fibronectin matrices, and the ability of alpha-LA to inhibit GalTase activity towards basal lamina substrates. Laminin was found to be a principle GalTase substrate in the basal lamina, and when tested in vitro, alpha-LA inhibited cell migration on laminin. Together, these experiments show that neural crest cells have at least two distinct mechanisms for interacting with the substrate during migration, one that is fibronectin-dependent and one that uses GalTase recognition of basal lamina glycoconjugates.


Development ◽  
1994 ◽  
Vol 120 (3) ◽  
pp. 495-503 ◽  
Author(s):  
D.W. Raible ◽  
J.S. Eisen

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.


Development ◽  
1989 ◽  
Vol 106 (4) ◽  
pp. 787-798
Author(s):  
G. Morriss-Kay ◽  
F. Tuckett

Studies on cell behaviour in vitro have indicated that the chondroitin sulphate proteoglycan (CSPG) family of molecules can participate in the control of cell proliferation, differentiation and adhesion, but its morphogenetic functions had not been investigated in intact embryos. Chondroitin/chondroitin sulphates have been identified in rat embryos at low levels at the start of neurulation (day 9) and at much higher levels on day 10. In this study we have sought evidence for the morphogenetic functions of CSPGs in rat embryos during the period of neurulation and neural crest cell migration by a combination of two approaches: immunocytochemical localization of CSPG by means of an antibody, CS-56, to the chondroitin sulphate component of CSPG, and exposure of embryos to the enzyme chondroitinase ABC. Staining of the CS-56 epitope was poor at the beginning of cranial neurulation; bright staining was at first confined to the primary mesenchyme under the convex neural folds late on day 9. In day 10 embryos, all mesenchyme cells were stained, but at different levels of intensity, so that primary mesenchyme, neural crest and sclerotomal cells could be distinguished from each other. Basement membranes were also stained, particularly bright staining being present where two epithelial were basally apposed, e.g., neural/surface ectoderms, dorsal aorta/neural tube, prior to migration of a population of cells between them. Staining within the neural epithelium was first confined to the dorsolateral edge region, and associated with the onset of neural crest cell emigration; after neural tube closure, neuroepithelial staining was more general. Neural crest cells were stained during migration, but the reaction was absent in areas associated with migration end-points (trigeminal ganglion anlagen, frontonasal mesenchyme). Embryos exposed to chondroitinase ABC in culture showed no abnormalities until early day 10, when cranial neural crest cell emigration from the neural epithelium was inhibited and neural tube closure was retarded. Sclerotomal cells failed to take their normal pathway between the dorsal aorta and neural tube. Correlation of the results of these two methods suggests: (1) that by decreasing adhesiveness within the neural epithelium at specific stages, CSPG facilitates the emigration of neural crest cells and the migratory movement of neuroblasts, and may also provide increased flexibility during the generation of epithelial curvatures; (2) that by decreasing the adhesiveness of fibronectin-containing extracellular matrices, CSPG facilitates the migration of neural crest and sclerotomal cells. This second function is particularly important when migrating cells take pathways between previously apposed tissues.


2020 ◽  
Author(s):  
Ezra Lencer ◽  
Rytis Prekeris ◽  
Kristin Bruk Artinger

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.


Development ◽  
1991 ◽  
Vol 111 (1) ◽  
pp. 15-22 ◽  
Author(s):  
B. Ranscht ◽  
M. Bronner-Fraser

Trunk neural crest cells and motor axons move in a segmental fashion through the rostral (anterior) half of each somitic sclerotome, avoiding the caudal (posterior) half. This metameric migration pattern is thought to be caused by molecular differences between the rostral and caudal portions of the somite. Here, we describe the distribution of T-cadherin (truncated-cadherin) during trunk neural crest cell migration. T-cadherin, a novel member of the cadherin family of cell adhesion molecules was selectively expressed in the caudal half of each sclerotome at all times examined. T-cadherin immunostaining appeared graded along the rostrocaudal axis, with increasing levels of reactivity in the caudal halves of progressively more mature (rostral) somites. The earliest T-cadherin expression was detected in a small population of cells in the caudal portion of the somite three segments rostral to last-formed somite. This initial T-cadherin expression was observed concomitant with the invasion of the first neural crest cells into the rostral portion of the same somite in stage 16 embryos. When neural crest cells were ablated surgically prior to their emigration from the neural tube, the pattern of T-cadherin immunoreactivity was unchanged compared to unoperated embryos, suggesting that the metameric T-cadherin distribution occurs independent of neural crest cell signals. This expression pattern is consistent with the possibility that T-cadherin plays a role in influencing the pattern of neural crest cell migration and in maintaining somite polarity.


Development ◽  
1992 ◽  
Vol 116 (3) ◽  
pp. 531-541 ◽  
Author(s):  
T. Lallier ◽  
G. Leblanc ◽  
K.B. Artinger ◽  
M. Bronner-Fraser

We have used a quantitative cell attachment assay to compare the interactions of cranial and trunk neural crest cells with the extracellular matrix (ECM) molecules fibronectin, laminin and collagen types I and IV. Antibodies to the beta 1 subunit of integrin inhibited attachment under all conditions tested, suggesting that integrins mediate neural crest cell interactions with these ECM molecules. The HNK-1 antibody against a surface carbohydrate epitope under certain conditions inhibited both cranial and trunk neural crest cell attachment to laminin, but not to fibronectin. An antiserum to alpha 1 intergrin inhibited attachment of trunk, but not cranial, neural crest cells to laminin and collagen type I, though interactions with fibronectin or collagen type IV were unaffected. The surface properties of trunk and cranial neural crest cells differed in several ways. First, trunk neural crest cells attached to collagen types I and IV, but cranial neural crest cells did not. Second, their divalent cation requirements for attachment to ECM molecules differed. For fibronectin substrata, trunk neural crest cells required divalent cations for attachment, whereas cranial neural crest cells bound in the absence of divalent cations. However, cranial neural crest cells lost this cation-independent attachment after a few days of culture. For laminin substrata, trunk cells used two integrins, one divalent cation-dependent and the other divalent cation-independent (Lallier, T. E. and Bronner-Fraser, M. (1991) Development 113, 1069–1081). In contrast, cranial neural crest cells attached to laminin using a single, divalent cation-dependent receptor system. Immunoprecipitations and immunoblots of surface labelled neural crest cells with HNK-1, alpha 1 integrin and beta 1 integrin antibodies suggest that cranial and trunk neural crest cells possess biochemically distinct integrins. Our results demonstrate that cranial and trunk cells differ in their mechanisms of adhesion to selected ECM components, suggesting that they are non-overlapping populations of cells with regard to their adhesive properties.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Ezra Lencer ◽  
Rytis Prekeris ◽  
Kristin Bruk Artinger

The 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, specifically in the xanthophore lineage. Further, we identify a population of Rohon–Beard neurons in the data. 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.


PLoS ONE ◽  
2014 ◽  
Vol 9 (1) ◽  
pp. e84072 ◽  
Author(s):  
Kunie Hagiwara ◽  
Takeshi Obayashi ◽  
Nobuyuki Sakayori ◽  
Emiko Yamanishi ◽  
Ryuhei Hayashi ◽  
...  

2010 ◽  
Vol 344 (1) ◽  
pp. 531
Author(s):  
Judith A. Cebra-Thomas ◽  
James Robinson ◽  
Melinda Yin ◽  
James McCarthy ◽  
Sonal Shah ◽  
...  

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