Skip to main content
Log in

Morphogenesis of sclerotome and neural crest in avian embryos

In vivo and in vitro studies on the role of notochordal extracellular material

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The distribution of sclerotome and neural crest cells of avian embryos was studied by light and electron microscopy. Sclerotome cells radiated from the somites towards the notochord, to occupy the perichordal space. Neural crest cells, at least initially, also entered cell-free spaces. At the cranial somitic levels they moved chiefly dorsal to the somites, favouring the rostral part of each somite. These cells did not approach the perichordal space. More caudally (i.e. trunk levels), neural crest cells initially moved ventrally between the somites and neural tube. Adjacent to the caudal half of each somite, these cells penetrated no further than the myosclerotomal border, but opposite the rostral somite half, they were found next to the sclerotome almost as far ventrally as the notochord. However, they did not appear to enter the perichordal space, in contrast to sclerotome cells.

When tested in vitro, sclerotome cells migrated towards notochords co-cultured on fibronectin-rich extracellular material, and on collagen gels. In contrast, neural crest cells avoided co-cultured notochords. This avoidance was abolished by inclusion of testicular hyaluronidase and chondroitinase ABC in the culture medium, but not by hyaluronidase from Streptomyces hyalurolyticus. The results suggest that sclerotome and neural crest mesenchyme cells have a different distribution with respect to the notochord, and that differential responses to notochordal extracellular material, possibly chondroitin sulphate proteoglycan, may be responsible for this.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allan IJ, Newgreen DF (1977) Catecholamine accumulation in neural crest cells and the primary sympathetic chain. Am J Anat 149:413–421

    Google Scholar 

  • Anderson CB, Meier S (1981) The influence of the metameric pattern in the mesoderm on migration of cranial neural crest cells in the chick embryo. Dev Biol 85:385–402

    Google Scholar 

  • Bancroft M, Bellairs R (1976) The neural crest cells of the trunk region of the chick embryo studies by SEM and TEM. Zoon 4:73–85

    Google Scholar 

  • Bornstein M (1958) Rat-tail collagen as a substrate. Lab Invest 7:134–137

    Google Scholar 

  • Boucaut J-C, Darribère T, Poole TJ, Aoyama H, Yamada K, Thiery JP (1984) Biologically active synthetic peptides as probes of embryonic development: A competitive peptide inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest cell migration in avian embryos. J Cell Biol 99:1822–1830

    Google Scholar 

  • Brauer PR, Bolender DL, Markwald RR (1985) The migratory pathway utilized by cephalic neural crest: Distribution and spatial organization of the extracellular matrix encountered by neural crest cells. Anat Rec 211:57–68

    Google Scholar 

  • Bronner-Fraser M (1982) Distribution of latex beads and retinal pigment epithelial cells along the ventral neural crest pathway. Dev Biol 91:50–63

    Google Scholar 

  • Caputo DB, Schrode J, Kimura JH, Hascall VC (1980) Removal of protease from streptomyces hyaluronidase by affinity chromatography. Anal Biochem 105:468–475

    Google Scholar 

  • Chernoff EAG, Lash JW (1981) Cell movement in somite formation and development in the chick: Inhibition of segmentation. Dev Biol 87:212–219

    Google Scholar 

  • Derby MA (1978) Analysis of glycosaminoglycans within the extracellular environments encountered by migrating neural crest cells. Dev Biol 66:321–336

    Google Scholar 

  • Derby MA, Newgreen DF (1982) Differentiation of avian neural crest cells in vitro: Absence of a developmental bias towards melanogenesis. Cell Tissue Res 225:365–378

    Google Scholar 

  • Ebendal T (1977) Extracellular matrix fibrils and cell contacts in the chick embryo. Possible roles in orientation of cell migration and axon extension. Cell Tissue Res 175:439–458

    Google Scholar 

  • Elsdale T, Bard J (1972) Collagen structure for studies on cell behaviour. J Cell Biol 54:626–637

    Google Scholar 

  • Erickson CA, Turley EA (1983) Substrata formed by combinations of extracellular matrix components alter neural crest cell motility in vitro. J Cell Sci 61:299–323

    Google Scholar 

  • Frederickson RG, Low FN (1971) The fine structure of perinotochordal microfibils in control and enzyme-treated chick embryos. Am J Anat 130:347–376

    Google Scholar 

  • Gasser RF (1979) Evidence that sclerotomal cells do not migrate medially during normal development of the rat. Am J Anat 154:509–524

    Google Scholar 

  • Grinnell F, Feld M, Minter D (1980) Fibroblast adhesion to fibrinogen and fibrin substrata: Requirement for cold-insoluble globulin (plasma fibronectin). Cell 19:517–525

    Google Scholar 

  • Grinnell F, Billingham RE, Burgess L (1981) Distribution of fibronectin during wound healing in vivo. J Invest Dermatol 76:181–189

    Google Scholar 

  • Hay ED (1978) Fine structure of embryonic matrices and their relation to the cell surface in ruthenium-red fixed tissue. Growth 42:399–423

    Google Scholar 

  • Hay ED, Meier S (1974) Glycosaminoglycan synthesis by embryonic inductors: Neural tube, notochord and lens. J Cell Biol 62:889–898

    Google Scholar 

  • Hedman K, Kurkinen M, Alitalo K, Vaheri A, Johansson S, Höök M (1979) Isolation of the pericellular matrix of human fibroblast cultures. J Cell Biol 81:83–91

    Google Scholar 

  • Hedman K, Johansson S, Vartio T, Kjellen L, Vaheri A, Höök M (1982) Structure of the pericellular matrix: Association of heparan and chondroitin sulphates with fibronectin-procollagen fibres. Cell 28:663–671

    Google Scholar 

  • Holmdahl DE (1928) Die Entstehung und weitere Entwicklung der Neuralleiste (Ganglienleiste) bei Vögeln und Säugetieren. Z Mikrosk Anat Forsch 14:99–298

    Google Scholar 

  • Jacob M, Jacob HJ, Christ B (1975) Die frühe Differenzierung des chordanahen Bindegewebes. Raster- und transmissionelek-tronenmikroskopische Untersuchungen an Hühnerembryonen. Experientia 31:1083–1086

    CAS  PubMed  Google Scholar 

  • Kenney MC, Carlson EC (1978) Ultrastrutural identification of collagen and glycosaminoglycans in notochord extracellular matrix in vivo and in vitro. Anat Rec 190:827–850

    Google Scholar 

  • Kvist TN, Finnegan CV (1970) The distribution of glycosaminoglycans in the axial region of the developing chick embryo. 1. Histochemical analysis. J Exp Zool 175:221–240

    Google Scholar 

  • Le Douarin N (1973) A biological cell labelling technique and its use in experimental embryology. Dev Biol 30:217–222

    PubMed  Google Scholar 

  • Le Douarin NM (1982) The neural crest. Cambridge University Press, Cambridge

    Google Scholar 

  • Le Douarin NM, Cochard P (1983) Embryonic development of the autonomic system. In: Burnstock G (ed) Somatic and autonomic nerve-muscle interactions. Elsevier Science Publishing B.V. Amsterdam, pp 1–33

    Google Scholar 

  • Mark H svon der, Mark K von der, Gay S (1976) Study of differential collagen synthesis during development of the chick embryo by immunofluorescence. Dev Biol 48:237–249

    Google Scholar 

  • Mayer BW Jr, Hay ED, Hynes RO (1981) Immunocytochemical localization of fibronectin in embryonic chick trunk and area vasculosa. Dev Biol 82:267–286

    Google Scholar 

  • Nawar G (1956) Experimental analysis of the origin of the autonomic ganglia in the chick embryo. Am J Anat 99:473–498

    Google Scholar 

  • Newgreen DF (1982) Adhesion to extracellular materials by neural crest cells at the stage of initial migration. Cell Tissue Res 227:297–317

    Google Scholar 

  • Newgreen DF (1984) Spreading of expiants of embryonic chick mesenchymes and epithelia on fibronectin and laminin. Cell Tissue Res 236:265–277

    Google Scholar 

  • Newgreen D, Thiery J-P (1980) Fibronectin in early avian embryos: synthesis and distribution along migration pathways of neural crest cells. Cell Tissue Res 221:269–291

    Google Scholar 

  • Newgreen DF, Ritterman M, Peters EA (1979) Morphology and behaviour of neural crest cells of chick embryo in vitro. Cell Tissue Res 203:115–140

    Google Scholar 

  • Newgreen DF, Gibbins IL, Sauter J, Wallenfels B, Wutz R (1982) Ultrastructural and tissue culture studies on the role of fibronectin, collagen and glycosaminoglycans in the migration of neural crest cells in the fowl embryo. Cell Tissue Res 221:521–549

    Google Scholar 

  • Noden DM (1978) Interactions directing the migration and cytodifferentiation of avian neural crest cells. In: Garrod D (ed) The specificity of embryonic interactions. Chapman and Hall, London, pp 3–49

    Google Scholar 

  • Oettinger HF, Thal G, Sasse J, Holtzer H, Pacifici M (1985) Immunological analysis of chick notochord and cartilage matrix development with antisera to cartilage matrix macromolecules. Dev Biol 109:63–71

    Google Scholar 

  • Ohya T, Kaneko Y (1970) Novel hyaluronidase from streptomyces. Biochim Biophys Acta 198:607–609

    Google Scholar 

  • Ostrovsky D, Cheney C, Seitz AW, Lash JW (1983) Fibronectin distribution during somitogenesis in the chick embryo. Cell Differ 13:217–223

    Google Scholar 

  • Pintar JE (1978) Distribution and synthesis of glycosaminoglycans during quail neural crest morphogenesis. Dev Biol 67:444–464

    Google Scholar 

  • Rodén L (1980) Structure and metabolism of connective tissue proteoglycans. In: Lennarz WJ (ed) The biochemistry of glycoproteins and proteoglycans. Plenum Press, New York, London, pp 267–371

    Google Scholar 

  • Rose GG, Pomerat CM, Shindler TO, Trunnel JB (1958) A cellophanestrip technique for culturing tissue in multipurpose culture chambers. J Biophys Biochem Cytol 4:761–764

    Google Scholar 

  • Rubin H (1973) Chick embryo cells. In: Kruse PF Jr, Patterson MK Jr (eds) Tissue culture: Methods and applications. Adademic Press, London, pp 119–122

    Google Scholar 

  • Ruggeri A (1972) Ultrastructural histochemical and autoradiographic studies of the developing chick notochord. Z Anat Entwickl 138:20–33

    Google Scholar 

  • Sanders EJ, Prasad S (1983) The culture of chick embryo mesoderm cells in hydrated collagen gels. J Exp Zool 226:81–92

    Google Scholar 

  • Solursh M, Fisher M, Meier S, Singley CT (1979) The role of extracellular matrix in the formation of the sclerotome. J Embryol Exp Morphol 54:75–98

    Google Scholar 

  • Strudel G (1971) Matériel extracellulaire et chondrogenèse vertebrale. CR Acad Sci Paris Sér D272:473–476

    Google Scholar 

  • Thiery JP, Duband JL, Delouvée A (1982) Pathways and mechanisms of avian trunk neural crest cell migration and localization. Dev Biol 93:324–343

    Google Scholar 

  • Tosney KW (1978) The early migration of neural crest cells in the trunk region of the avian embryo: An electron microscopic study. Dev Biol 62:317–333

    Google Scholar 

  • Trelstad RL (1977) Mesenchymal cell polarity and morhogenesis of chick cartilage. Dev Biol 59:153–163

    CAS  PubMed  Google Scholar 

  • Tucker RP, Erickson CA (1984) Morphological behaviour of quail crest cells in artificial three-dimensional extracellular matrixes. Dev Biol 104:390–405

    Google Scholar 

  • Vasan N (1981) Analysis of perinotochordal materials. I. Studies on proteoglycan synthesis. J Exp Zool 215:229–233

    Google Scholar 

  • Venable JH, Coggeshall R (1965) A simplified lead citrate stain for use in electron microscopy. J Cell Biol 25:407–408

    Article  CAS  PubMed  Google Scholar 

  • Vincent M, Thiery J-P (1984) A cell surface marker for neural crest and placodal cells: Further evolution in peripheral and central nervous system. Dev Biol 103:468–481

    Google Scholar 

  • Weston JA (1963) A radioautographic analysis of the migration and localization of trunk neural crest cells in the chick. Dev Biol 6:279–310

    Google Scholar 

  • Weston JA (1982) Motile and social behavior of neural crest cells. In: Bellairs R, Curtis A, Dunn G (eds) rCell behaviour. Cambridge University Press, Cambridge, pp 429–470

    Google Scholar 

  • Wight TN, Ross R (1975) Proteoglycans in primate arteries. I. Ultrastructural localization and distribution in the intima. J Cell Biol 67:660–674

    Google Scholar 

  • Williams LW (1910) The somites of the chick. Am J Anat 2:55–100

    Google Scholar 

  • Yamagata T, Saito H, Habuchi O, Suzuki S (1968) Purification and properties of bacterial chondroitinases and chondrosulfatases. J Biol Chem 243:1523–1535

    Google Scholar 

  • Yntema Cl, Hammond WS (1945) Depletions and abnormalities in the cervical sympathetic system of the chick following extirpation of neural crest. J Exp Zool 100:237–263

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Newgreen, D.F., Scheel, M. & Kastner, V. Morphogenesis of sclerotome and neural crest in avian embryos. Cell Tissue Res. 244, 299–313 (1986). https://doi.org/10.1007/BF00219205

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00219205

Key words

Navigation