Summary
In avian embryos, the migration behaviour of several cell populations, melanoblasts, Schwann cells, myogenic cells and axons after application of antibodies directed against the cell-attachment fragment of fibronectin (α-CAF) was investigated. The migration of the different cell types was influenced in different ways. 1. Epidermal melanoblasts did not colonize areas into which the antibody had been injected, i.e. distal to the grafting site. They frequently spread proximally to the back and neck, sometimes even as far as to the ipsilateral leg. When grafted to the dorsal side of the wing bud, melanoblasts never spread to the ventral side after injection of the antibody. Non-epidermal melanoblasts continued to migrate distally. 2. Grafted Schwann cells and host axons were not noticeably affected by the antibody injections. Both were found proximally and far distally to the grafting site, i.e. also within the injected area. 3. Myogenic cells were immobilized near the grafting site, where they differentiated biochemically, but sometimes only partially underwent fusion into myotubes. They participated in the formation of host muscle blastemas only immediately adjacent to the non-migratory cell population of the graft such as fibroblasts and cartilage. 4. The injected antibody could be localized up to 5 h after the application in the distal third of the limb bud. We conclude that migrating cell populations show differences in their fibronectin-dependence which probably reflect their use of fibronectin during migration.
Similar content being viewed by others
References
Al-Ghaith LK, Lewis JH (1982) Pioneer growth cones in virgin mesenchyme: an electron-microscope study in the developing chick wing. J Embryol Exp Morphol 68:149–160
Ali IU, Hynes RO (1978) Effects of LETS glycoprotein on cell motility. Cell 14:439–446
Argraves WS, Gehlsen KR (1991) Cellular interactions with fibronectin as a model for redundant binding of cells to other extra-cellular matrix proteins. In vivo 5:489–492
Bogusch G (1992) Electron microscopic investigations on the growing tip of nerve fibres in the developing distal forelimb of the mouse. Anat Embryol 185:201–206
Boucaut JC, Darribère T (1983) Fibronectin in early amphibian embryos. Cell Tissue Res 234:135–145
Boucaut JC, Darribère T, Poole TJ, Aoyama H, Yamada KM, 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
Brand-Saberi B (1991) Befunde zur Kontrolle der gerichteten Zell-migration myogener Zellen in der Vogelextremität. Verh Anat Ges 85:479–481
Brand-Saberi B, Krenn V (1991) Observations concerning the control of directed myogenic cell migration. NATO ASI Series. Hinchliffe JR, Hurle J, Summerbell D (eds) Plenum Publishing Company, New York, pp 273–284
Brand-Saberi B, Krenn V, Christ B (1989) The control of directed myogenic cell migration in the avian limb bud. Anat Embryol 180:555–556
Bronner-Fraser M (1986) An antibody to a receptor for fibronectin and laminin perturbs cranial neural crest development in vivo. Dev Biol 117:528–536
Carpenter EM, Hollyday M (1992) The distribution of neural crest-derived Schwann cells from subsets of brachial spinal segments into the peripheral nerves innervating the chick forelimb. Dev Biol 150:160–170
Chammas R, Brentani R (1991) Integrins and metastases: an overview. Tumor Biol 12:309–320
Chiquet M, Eppenberger HM, Turner DC (1981) Muscle morphogenesis: evidence for an organizing function of exogenous fibronectin. Dev Biol 88:220–235
Christ B, Epperlein HH, Flöel H, Grim M, Kaehn K, Wilting J (1991) Somitendifferenzierung und Muskelentwicklung bei Vogelembryonen. Verh Anat Ges 86:50
Cordell JL, Falini B, Erber WN, Ghosh AK, Abdulaziz Z, MacDonald S, Pulford KAF, Stein H, Mason DY (1984) Immunoenzymatic labeling of monoclonal antibodies using immune complexes of alkaline phosphatase and monoclonal anti-alkaline phosphatase (APAAP complexes). J Histochem Cytochem 32:219–229
Critchley DR, England MA, Wakely J, Hynes RO (1979) Distribution of fibronectin in the ectoderm of gastrulating chick embryos. Nature 280:498–500
Dufour S, Duband JL, Humphries MJ, Obara M, Yamada KM, Thiery JP (1988) Attachment, spreading and locomotion of avian neural crest cells are mediated by multiple adhesion sites on fibronectin molecules. EMBO J 7:2661–2671
Erickson CA, Tosney KW, Weston JA (1980) Analysis of migratory behavior of neural crest and fibroblastic cells in embryonic tissues. Dev Biol 77:142–156
Feulgen R, Rossenbeck H (1924) Mikroskopisch-chemischer Nachweis einer Nucleinsäure vom Typ der Thymonucleinsäure und die darauf beruhende elektive Färbung von Zellkernen in mikroskopischen Präparaten. Hoppe Seylers Z Physiol Chem 135:203–252
Gehlsen KR, Argraves WS, Pierschbacher MD, Ruoslahti E (1988) Inhibition of in vitro tumor cell invasion by Arg-Gly-Asp-containing synthetic peptides. J Cell Biol 106:925–930
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92
Humphries MJ, Olden K, Yamada KM (1986) A synthetic peptide from fibronectin inhibits experimental metastasis of murine melanoma cells. Science 233:467–470
Hynes RO (1981) Fibronectin and its relation to cellular structure and behavior. In: Hay ED (ed) Cell biology of extracellular matrix. Plenum Press, New York, pp 295–333
Hynes RO, Yamada KM (1982) Fibronectins: multifunctional modular glycoproteins. J Cell Biol 95:369–377
Jacob M, Christ B, Jacob HJ (1978) On the migration of myogenic stem cells into the prospective wing region of chick embryos. A scanning and transmission electron microscope study. Anat Embryol 153:179–193
Jaffredo T, Horwitz AF, Buck CA, Rong PM, Dieterlen-Lièvre F (1988) Myoblast migration specifically inhibited in the chick embryo by grafted CSAT hybridoma cells secreting an antiintegrin antibody. Development 103:431–446
Katayama M, Hino F, Odate Y, Goto S, Kimizuka F, Kato I, Titani K, Sekiguchi K (1989) Isolation and characterization of two monoclonal antibodies that recognize remote epitopes on the cell-binding domain of human fibronectin. Exp Cell Res 185:229–236
Kosher RA, Walker KH, Ledger PW (1982) Temporal and spatial distribution of fibronectin during development of the embryonic chick limb bud. Cell Differ 11:217–228
Krenn V, Brand-Saberi B, Wachtler F (1991) Hyaluronic acid influences the migration of myoblasts within the avian embryonic wing bud. Am J Anat 192:400–406
Mackie EJ, Tucker RP, Halfter W, Chiquet-Ehrismann R, Epperlein HH (1988) The distribution of tenascin coincides with pathways of neural crest cell migration. Development 102:237–250
Melnick M, Jaskoll T, Brownell AG, MacDougall M, Bessern C, Slavkin HC (1981) Spatiotemporal patterns of fibronectin distribution during embryonic development. I. Chick limbs. J Embryol Exp Morphol 63:193–206
Newgreen DF, Thiery JP (1980) Fibronectin in early avian embryos: synthesis and distribution along the migration pathways of neural crest cells. Cell Tissue Res 211:269–291
Pierschbacher MD, Ruoslahti E (1984) Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309:30–33
Pierschbacher MD, Haymann EG, Ruoslahti E (1983) Synthetic peptide with cell attachment activity of fibronectin. Proc Natl Acad Sci USA 80:1224–1227
Ruoslahti R (1984) Fibronectin in cell adhesion and invasion. Canc Metastasis Rev 3:43–51
Spiegel E, Burger M, Spiegel M (1980) Fibronectin in the developing sea urchin embryo. J Cell Biol 87:309–313
Tanaka H, Kinutani M, Agata A, Takashima Y, Obata K (1990) Pathfinding during spinal tract formation in the chick-quail chimera analysed by species-specific monoclonal antibodies. Development 110:565–571
Tomasek JJ, Mazurkiewicz JE, Newman SA (1982) Nonuniform distribution of fibronectin during avian limb development. Dev Biol 90:118–126
Wachtler F (1984) On the migration of epidermal melanoblasts in the avian embryonic wing bud. Anat Embryol 170:307–312
Wylie CC, Heasman J (1982) Effects of the substratum on the migration of primordial germ cells. Philos Trans R Soc Lond [Biol] 299:177–183
Wylie CC, Heasman J, Swan AP, Anderton BH (1979) Evidence for substrate guidance of primordial germ cells. Exp Cell Res 121:315–324
Yamada KM (1983) Cell surface interactions with extracellular materials. Annu Rev Biochem 52:761–799
Author information
Authors and Affiliations
Additional information
Fellow of the FWF (Erwin-Schrödinger-scholarship)
Rights and permissions
About this article
Cite this article
Brand-Saberi, B., Krenn, V., Grim, M. et al. Differences in the fibronectin-dependence of migrating cell populations. Anat Embryol 187, 17–26 (1993). https://doi.org/10.1007/BF00208193
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00208193