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The Migration of Neural Crest Cells and the Growth of Motor Axons Through the Rostral Half of the Chick Somite

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The Migration of Neural Crest Cells and the Growth of Motor Axons Through the Rostral Half of the Chick Somite /. Embryol. exp. Morph. 90, 437-455 (1985) 437 Printed in Great Britain © The Company of Biologists Limited 1985 The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite M. RICKMANN, J. W. FAWCETT The Salk Institute and The Clayton Foundation for Research, California division, P.O. Box 85800, San Diego, CA 92138, U.S.A. AND R. J. KEYNES Department of Anatomy, University of Cambridge, Downing St, Cambridge, CB2 3DY, U.K. SUMMARY We have studied the pathway of migration of neural crest cells through the somites of the developing chick embryo, using the monoclonal antibodies NC-1 and HNK-1 to stain them. Crest cells, as they migrate ventrally from the dorsal aspect of the neural tube, pass through the lateral part of the sclerotome, but only through that part of the sclerotome which lies in the rostral half of each somite. This migration pathway is almost identical to the path which pre- sumptive motor axons take when they grow out from the neural tube shortly after the onset of neural crest migration. In order to see whether the ventral root axons are guided along this pathway by neural crest cells, we surgically excised the neural crest from a series of embryos, and examined the pattern of axon outgrowth approximately 24 h later. In somites which contained no neural crest cells, ventral root axons were still found only in the rostral half of the somite, although axonal growth was slightly delayed. These axons were surrounded by sheath cells, which had presumably migrated out of the neural tube, to a point about 50 jan proximal to the growth cones. With appropriate antibodies we found that the extracellular matrix com- ponents fibronectin and laminin are evenly distributed between the rostral and caudal halves of the somite. Neither of these molecules therefore plays a critical role in determining the specific pathway of neural crest cells or motor axons through the rostral half of the somite. INTRODUCTION The cells of the neural crest are remarkable for the length and complexity of their migration pathway, and the number of cell types into which they differentiate (reviewed in Le Douarin, 1982). Perhaps the only comparable structures in terms of complexity of migratory behaviour are the growth cones of nerve fibres. It is hardly surprising, therefore, that the mechanisms controlling neural crest mi- gration and axon outgrowth have been two of the most intensively studied processes in embryogenesis. Over the years it has been possible to establish which tissues are derived from neural crest (Horstadius, 1950; Weston, 1963; Johnston, 1966; Noden, 1975), more Key words: neural crest, somite, axonal guidance, fibronectin, laminin. 438 M. RICKMANN, J. W. FAWCETT AND R. J. KEYNES recently with the technique of chimaeric grafting, in which quail cells are grafted into chick embryos (Le Douarin, 1973; Le Douarin & Teillet, 1974). The approxi- mate pathway of neural crest migration has also been elucidated, using this and a variety of other anatomical techniques. Recently, it has been possible to analyse the migration of crest cells with greater precision using immunohistochemical methods and monoclonal antibodies which bind selectively to the migrating neural crest cell surface (Vincent, Duband & Thiery, 1983; Vincent & Thiery, 1984), and it is a series of experiments using this technique which we report on here. Some progress has also been made in defining mechanisms which might be responsible for causing neural crest cells to migrate along their chosen pathways. In this respect much attention has focused over the last few years on the extra- cellular matrix component fibronectin, which is present in high concentration in the pathways followed by neural crest cells (Newgreen & Thiery, 1980; Mayer, Hay & Hynes, 1981; Duband & Thiery, 19826), is a good substrate for crest cell migration in culture (Rovasio et al. 1983), and, when coated onto microbeads, affects their transportation down the neural crest migration pathway (Bronner- Fraser, 1982). Shortly after truncal crest cells start to migrate ventrally past the neural tube, the presumptive motor axons begin to grow out from the neural tube into the somites. It has recently been reported that these motor nerve fibres grow only through the rostral half of each somite, and do so initially from only those portions of the neural tube immediately adjacent to the rostral half of each somite (Keynes & Stern, 1984). The specificity for this selective outgrowth lies in the cells of the somite itself, since in embryos with rostrocaudal rotations of the segmental plate the outgrowth of the motor nerve fibres is still restricted to the half of the somite which would, in an unoperated animal, have lain rostrally (Keynes & Stern, 1984). Moreover, ablating the somitic mesoderm with X irradiation results in motor axons growing out evenly along the length of the neural tube (Lewis, Chevallier, Kieny & Wolpert, 1981). In this paper we describe in detail the path taken by the neural crest cells through the somites, as revealed by staining them with the two monoclonal antibodies NC-1 (Vincent etal 1983) and HNK-1 (Tucker etal 1984). We report that neural crest cells demonstrate the same specificity as motor axons, and, like them, migrate through the rostral half of each somite. We also report the results of experiments in which we have ablated the neural crest, and examined the sub- sequent pathway of the motor nerve fibres through crest-free somites. We show that the motor fibres are not guided through the rostral half of the somite due to the presence of crest cells within it, since they still grow specifically through the rostral half when it is completely free of neural crest cells. We also describe the distribution of the extracellular matrix components fibronectin and laminin, and speculate on the possible roles of these molecules in guiding neural crest cells and nerve fibres. Neural crest migration and axon outgrowth 439 MATERIALS AND METHODS Immunocytochemistry The embryos were transferred from the egg into a dish filled with PBS (phosphate-buffered saline without Ca2+ and Mg2"1"), where they were carefully freed from the surrounding membranes, stretched out and pinned down. Thereafter, the embryos were fixed for 1 h at room temperature, in a fixative consisting of 1-25 % glutaraldehyde, 1 % paraformaldehyde and 3-5 % sucrose in O-lM-phosphate buffer at pH7-3. After rinsing in PBS the embryos were encap- sulated by placing them into a solution of 20 % BSA (bovine serum albumin) in 0-1 M-sodium phosphate at pH7-2 which was polymerized with 25 % glutaraldehyde (1 % in final volume). The resulting blocks were then hardened for 1 h in the original fixative. Since the blocks were transparent they could be easily trimmed for transverse, horizontal or parasagittal sectioning of the embryos. Sections were cut either on a vibratome at a thickness between 100 and 150 jum or, after soaking in 20% phosphate-buffered glycerol, on a freezing microtome at 50 to 100 fjm. They were collected in wells containing Tris-buffered saline (TBS: 50mmol Tris, 150mmol NaCl, pH7-6). The immunocytochemical method utilized the avidin-biotin-peroxidase pro- cedure. Free-floating sections were passed through the following incubation steps at room temperature, while being gently agitated. (1) Non-specific antibody binding was blocked by incubation for 2-3 h in 0-02 % sodium azide, 0-1 M-L-lysine., 1 % BSA and 1:10 serum (from the same species as the secondary antibody) in TBS. The same solution was used to dilute both the primary and secondary antibodies. (2) Without rinsing, the sections were transferred to the primary antibody for 12-24 h. The following dilutions were used for the various antibodies employed in this study. Goat anti-chicken fibronectin (Calbiochem, Lot 001428) was diluted 1:2000, rabbit anti-laminin serum (EY labs no. AT 2404, lot no. 020106) 1:100, prediluted hybridoma ascites containing anti-HNKl antibodies (Becton Dickinson anti Leu-7, no. 7390, lot no. 60914) 1:50 and monoclonal anti-NCI ascites 1:500. Normal serum and control ascites were used at the same concentrations as controls. (3) Sections were rinsed in TBS, three changes of 45min each, and then floated onto biotinylated secondary antibody (Vector laboratories), diluted 1:250, for 6-8h. (4) Rinsed three times in TBS and left in TBS overnight. (5) Endogenous peroxidase activity was blocked with 0-3% H2O2 in methanol for 30min. (6) Rinsed three times in TBS, 5min each change. The last two steps were omitted in some preparations in order to improve the structural preservation of the rather fragile sections. (7) Incubated with Avidin-coupled horseradish peroxidase complex (Vector laboratories) for 3 h at 1:100 dilution in 1 % BSA in TBS. (8) Rinsed four times, 1 h each change, in TBS. (9) 0-01 % 3,3'-diaminobenzidine tetrahydrochloride (DAB) and 0-03 % H2O2 in TBS for 10-15 min. (10) Rinsed four times, 10min each change, in TBS. (11) Transferred to PBS. At this stage of the procedure, some of the sections were mounted on gelatinized slides, air dried, dehydrated in ethanol and xylene and coverslipped in DPX. In order to obtain higher resolution and better tissue preservation, in some cases the reaction product was intensified and the sections were embedded in epoxy resin using the following procedure. (12) 0-01 % OsO4 in PBS for 15 min. (13) Rinsed four times, 10 min each, in PBS. Subsequently the sections were dehydrated in a graded series of ethanols and propylene oxide, and then infiltrated with Spurr's low viscosity embedding medium. The sections were flattened between glass slides, one of which was coated with a mould release compound, and polymerized at 70°C for one day.
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