Skip to main content
Log in

Deposition of extracellular matrix along the pathways of migrating fibroblasts

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

Summary

Fibroblasts from rat, mouse and chick embryos cultured on poly-lysine/fibronectin- or poly-lysine/laminin-coated dishes were stained with antibodies directed to extracellular matrix molecules. The staining showed that cells had migrated during culture and deposited extracellular matrix components along their migration trails. Depending on the antigen, the staining of the matrix revealed fibrils, spots or a diffuse smear along the migration pathways. The major matrix components were fibronectin and heparan sulfate proteoglycan; however, laminin nidogen, tenascin, glia-derived nexin (GDN) and chondroitin-4-sulfate proteoglycan were also found. The migration trails were also detectable by scanning electron microscopy. Here, the fibrils were the prominent structures. The deposition of matrix was independent from the substratum: fibronectin was deposited on laminin, plain poly-lysine, basal lamina and even on fibronectin. Functional assays using anti-fibronectin or an antiserum to embryonic pigment epithelium basement membrane disturbed the formation of matrix fibrils, but did not inhibit cell attachment and translocation. Likewise, heparin in the culture medium only partially inhibited cell migration, despite the fact that it disturbed the formation of proper matrix fibrils. Our results suggest that the deposition of extracellular matrix by cells may not be mandatory for attachment and translocation. However, the deposition of matrix along defined trails might be important for the pathfinding of cells or nerve fibers that appear later in development.

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

  • Ali JU, Hynes RO (1978) Effects of LETS glycoprotein on cell motility. Cell 14:439–446

    Google Scholar 

  • Bergman BL, Scott RW, Bajpa A, Watts Sh, Baker J (1986) Inhibition of tumor-cell mediated extracellular matrix destruction by a fibroblasts protease inhibitor protease nexin I. Proc Natl Acad Sci USA 83:996–1000

    Google Scholar 

  • Chen N-T, Chen J-M, Parson SJ, Parson JTh (1985) Focal degradation of fibronectin at sites of expression of the transforming gene product pp60\(\hat T\)src\(\hat T\). Nature 316:156–158

    Google Scholar 

  • Chiquet M, Fambrough D (1984) Chick myotendinous antigen. II. A novel extracellular glycoprotein complex consisting of large disulfide-linked subunits. J Cell Biol 98:1937–1946

    Google Scholar 

  • Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakagura T (1986) Tenascin: An extracellular matrix protein involved if tissue interaction during fetal development and oncogenesis. Cell 47:131–139

    Google Scholar 

  • Couchman JR, Rees A, Green MR, Smith CG (1982) Fibronectin has a dual role in locomotion and anchorage of primary chick fibroblasts and can promote entry into the division cycle. J Cell Biol 93:402–410

    Google Scholar 

  • Davis GE, Varon S, Engvall E, Manthorpe MC (1985) Substratum-binding neurite promoting factors: relationship to laminin. TINS 528–532

  • Engvall E, Ruoslahti E (1977) Binding of soluble form of fibroblasts surface protein, fibronectin, to collagen. Int J Cancer 20:1–5

    Google Scholar 

  • Halfter W (1988) Aberrant optic axons in the retinal pigment epithelium during chick and quail visual pathway development. J Comp Neurol 268:161–170

    Google Scholar 

  • Halfter W (1989) Antisera to basal lamina and glial endfeet disturb the normal extension of axons of retina and pigment epithelium basal lamina. Development 107:281–297

    Google Scholar 

  • Halfter W, Reckhaus W, Kroeger S (1987) Nondirected axonal growth of basal lamina from the embryonic avian retina. J Neurosci 7:3712–3722

    Google Scholar 

  • Halfter W, Diamantis I, Monard D (1988) Migratory behavior of cells or embryonic retina basal lamina. Dev Biol 130:259–275

    Google Scholar 

  • Halfter W, Reinhard E, Liverani D, Ortman R, Monard D (1989) Immunocytochemical localization of glia-derived nexin, laminin and fibronectin of the surface or extracellular matrix of C6 rat glioma cells, astrocytes and fibroblasts. Eur J Neurosci 1:297–308

    Google Scholar 

  • Hay ED (1981) Cell biology of extracellular matrix. Plenum Press, New York London

    Google Scholar 

  • Heasman J, Hynes RO, Swan AP, Thamas V, Wylie CC (1981) Primordial germ cells of Xenopus embryos: the role of fibronectin in their adhesion during migration. Cell 27:437–447

    Google Scholar 

  • Kirk D, Kagawa S, Narayan SK, Ohnuki Y (1985) Novel antigen system for tracking epithelial cell migration if serum-free culture. Exp Cell Res 160:221–229

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • Lagenauer C, Lemmon V (1987) A L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc Natl Acad Sci USA 84:7753–7757

    Google Scholar 

  • Laug WE, DeClerk YA, Jones PA (1983) Degradation of the subendothelial matrix by tumor cells. Cancer Res 43:1827–1834

    Google Scholar 

  • Majack RA, Clowes AW (1984) Inhibition of vascular smooth muscle cell migration by heparin-like glycosaminoglycans. J Cell Physiol 118:253–256

    Google Scholar 

  • Majack RA, Cook SC, Bornstein P (1885) Platelet-derived growth factor and heparin-like glycosaminoglycans regulate thrombospondin synthesis and deposition in the matrix of smooth muscle cells. J Cell Biol 101:1059–1070

    Google Scholar 

  • Marusyk R (1980) Microdialysis of membrane filters. Anal Biochem 105:403–404

    Google Scholar 

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

    Google Scholar 

  • McDonald JA (1988) Extracellular matrix assembly. Ann Rev Cell Biol 4:183–207

    Google Scholar 

  • McKeown-Longo P, Mosher DF (1983) Binding of plasma fibronectin to cell layers of culture human fibroblasts. J Cell Biol 97:466–472

    Google Scholar 

  • McKeown-Longo P, Mosher DF (1985) Interaction of the 70000-mol-wt amino-terminal fragment of fibronectin with the matrixassembly receptor of fibroblasts. J Cell Biol 100:364–374

    Google Scholar 

  • Monard D (1989) Cell-derived proteases and protease inhibitors as regulators of neurite outgrowth. TINS 541–544

  • Morris RJ, Beach J (1984) Diferential expression of Thy1 of various components of connective tissue of rat nerve during postnatal development. Dev Biol 102:32–42

    Google Scholar 

  • Nakatsuji N, Johnson KE (1984) Experimental manipulation of a contact guidance system if amphibian gastrulation by mechanical tension. Nature 307:453–455

    Google Scholar 

  • Newgreen DF, Thiery J-P (1980) Fibronectin if early avian embryos: synthesis and distribution along migration pathways of neural crest cells. Cell Tissue Res 211:269–291

    Google Scholar 

  • Ocalan M, Goodman SL, Kuehl U, Hauschka SD, Mark K von der (1988) Laminin alters cell shape and stimulates motility and proliferation of murine skeletal myoblasts. Dev Biol 125:158–169

    Google Scholar 

  • Paulsson M, Aumally M, Deutzmann R, Timpl R, Beck K, Engel J (1987) Laminin-nidogen complex extraction with chelating agents and structural characterization. Eur J Biochem 166:11–19

    Google Scholar 

  • Polson A, Wechman MB, Regenmartel MHV van (1980) Isolation of viral IgY antibodies from yolks of immunized hens. Immun Comm 9:475–493

    Google Scholar 

  • Poste G, Doll J, Has JR, Fidler IJ (1980) If vivo selection of murine B16 melanoma variants with enhanced tissue invasive-properties. Cancer Res 40:1636–1644

    Google Scholar 

  • Presciotta-Peters DM, Mosher DF (1987) Localization of cell surface sites involved in fibronectin fibrillogenesis. J Cell Biol 104:121–130

    Google Scholar 

  • Reinhard E, Meier R, Halfter W, Rovelli G, Monard D (1988) Detection of glia-derived nexin if the olfactory system of the rat. Neuron 1:387–394

    Google Scholar 

  • Reynolds EJ (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–210

    Google Scholar 

  • Rijken DC, Collen D (1981) Purification and characterization of plasminogen activator secreted by human melanoma cells in culture. J Biol Chem 256:7035–7041

    Google Scholar 

  • Thiery JP, Duband JL, Tucker GC (1985) Cell migration in the vertebrate embryo. Role of cell adhesion and tissue environment in pattern formation. Ann Rev Cell Biol 1:91–113

    Google Scholar 

  • Timpl R, Rhode H, Robey PG, Rennard SI, Foidart JM, Martin GR (1979) Laminin: a glycoprotein from basement membranes. J Biol Chem 254:9933–9937

    Google Scholar 

  • Timpl R, Paulsson M, Dziadek M, Fujiwara S (1987) Basement membranes. Methods Enzymol 145:363–391

    Google Scholar 

  • Towbin H, Staehlin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Google Scholar 

  • Trinkaus JP (1984) Cells into organs: The Forces That Shape the Embryo. Prentice-Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Turner DC, Lawton J, Dollenmeier P, Ehrismann R, Chiquet M (1983) Guidance of myogenic cell migration by oriented deposits of fibronectin. Dev Biol 95:497–504

    Google Scholar 

  • Vardy PH, Fisher LR, Smith E, Williams KL (1980) Traction proteins in the extracellular matrix of Dictyostelium discoideum slugs. Nature XC:506–529

    Google Scholar 

  • Vigny M, Ollier-Hartmann MP, Lavigne M, Fayein N, Jeanny JC, Laurent M, Courtois Y (1988) Specific binding of basic fibroblast growth factor to basement membrane-like structures and to purified heparan sulfate proteoglycan of the EHS tumor. J Cell Physiol 137:321–328

    Google Scholar 

  • Vischer P, Volker W, Schmidt A, Sinclair N (1988) Association of trombospondin of endothelial cells with other matrix proteins, attachment sites and migration tracks. Eur J Cell Biol 47:36–46

    Google Scholar 

  • Yamada KM (1983) Cell surface interaction with extracellular material. Ann Rev Biochem 52:761–799

    Google Scholar 

  • Yamada KM, Yamada SS, Pastan I (1975) The major cell surface glycoprotein of embryo fibroblasts is an agglutinin. Proc Natl Acad Sci USA 72:3158–3162

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Halfter, W., Liverani, D., Vigny, M. et al. Deposition of extracellular matrix along the pathways of migrating fibroblasts. Cell Tissue Res 262, 467–481 (1990). https://doi.org/10.1007/BF00305243

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00305243

Key words

Navigation