Skip to main content
Log in

Calcium-dependent adhesion of Drosophila embryonic cells

  • Published:
Roux's archives of developmental biology Aims and scope Submit manuscript

Summary

By using an in vitro functional assay, we have shown that Drosophila embryonic cells possess Ca2+-dependent adhesive sites, which resemble in many respects those described for vertebrate cells and tissues. The cells, obtained by mechanical disruption of gastrulastage embryos, form aggregates within 30 min when maintained under constant rolling. The aggregation is completely dependent on the presence of Ca2+ in the medium. In its absence, the cells remain dispersed but the process is reversible by readdition of Ca2+. In addition the aggregation is temperature-dependent. No aggregation occurs at 4° C but it can be restored by raising the temperature to 25° C. These properties are characteristic of these cells: established cell lines do not aggregate under the same conditions and mixing of cell lines and embryonic cells does not result in chimeric aggregates, thus pointing towards cell-type selectivity with respect to aggregability. Observations in electron microscopy have shown that the embryonic cells in the aggregates tightly adhere to one another and form, as early as after 30 min, maculae adherens junctions. Drosophila embryonic cells have adhesion sites that are protected from trypsin proteolysis in the presence of Ca2+ and sensitive in its absence. The cells' aggregation can be inhibited by a mouse antiserum directed against cell-surface components and a good correlation exists between neutralization of the inhibitory activity of the antiserum and the presence of trypsin-sensitive sites on the cells. These data are in favour of cell-cell adhesion mediated by specific adhesion proteins.

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

  • Anderson H (1988) Drosophila adhesion molecules and neural development. Trends Neurosci 11:472–475

    Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–252

    Google Scholar 

  • Burt R, Gierer A (1979) Age specific cell sorting within aggregates of chick neural retina cells. Roux's Arch Dev Biol 187:367–373

    Google Scholar 

  • Choi YS, Gumbiner B (1989) Expression of cell adhesion molecule E-cadherin in Xenopus embryos begins at gastrulation and predominates in the ectoderm. J Cell Biol 108:2449–2458

    Google Scholar 

  • Cunningham BA, Hemperly JJ, Murray BA, Prediger EA, Brackenbury R, Edelman GM (1987) Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236:799–806

    Google Scholar 

  • Currie DA, Milner MJ, Evans CW (1988) The growth and differentiation in vitro of leg and wing imaginal disc cells from Drosophila melanogaster. Development 102:805–814

    Google Scholar 

  • Edelman GM (1986) Cell adhesion molecules in the regulation of animal form and tissue pattern. Annu Rev Cell Biol 2:81–117

    Google Scholar 

  • Edelman GM, Murray BA, Mege R, Cunningham BA, Gallin WJ (1987) Cellular expression of liver and neural cell adhesion molecules after transfection with their cDNAs results in specific cell-cell binding. Proc Natl Acad Sci USA 84:8502–8506

    Google Scholar 

  • Fausto-Sterling A, Hsieh L (1987) In vitro culture of Drosophila imaginal disc cells: aggregation, sorting out, and differentiation abilities. Dev Biol 120:284–293

    Google Scholar 

  • Fausto-Sterling A, Muckenthaler FA, Hsieh L, Rosenblatt PL (1985) Some determinants of cellular adhesiveness in an embryonic cell line from Drosophila melanogaster. J Exp Zool 234:47–55

    Google Scholar 

  • Fehon RG, Schubiger G (1985) Dissociation and sorting out of Drosophila imaginal disc cells. Dev Biol 108:465–473

    Google Scholar 

  • Furst A, Mahowald AP (1985) Differentiation of primary embryonic neuroblasts in purified neural cell cultures from Drosophila. Dev Biol 109:184–192

    Google Scholar 

  • Galewsky S, Rickoll WL (1989) 20-hydroxyecdysone induced aggregation of Drosophila S3 cells is inhibited by antibodies to a hormone-dependent extracellular glycoprotein. Roux's Arch Dev Biol 198:14–18

    Google Scholar 

  • Gauger A, Fehon RG, Schubiger G (1985) Preferential binding of imaginal disc cells to embryonic segments of Drosophila. Nature 313:395–397

    Google Scholar 

  • Gratecos D, Astier M, Sémériva M (1987) A new appproach to monoclonal antibody production. In vitro immunization with antigens on nitrocellulose using Drosophila myosin heavy chain as an example. J Immunol Methods 103:169–178

    Google Scholar 

  • Gratecos D, Naidet C, Astier M, Thiery JP, Sémériva M (1988) Drosophila fibronectin: a protein that shares properties similar to those of its mammalian homologue. EMBO J 7:215–223

    Google Scholar 

  • Harrelson AL, Goodman CS (1988) Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily. Science 242:700–708

    Google Scholar 

  • Hatta K, Nose A, Nagafuchi A, Takeichi M (1988) Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family. J Cell Biol 106:873–881

    Google Scholar 

  • Hay ED (1968) Organization and fine structure of epithelium and mesenchyme in the developing chick embryo. In: Fleishmajer R, Billingham R (eds) ‘Epithelial-mesenchymal interactions’. Williams and Wilkins, Baltimore, Maryland, pp 31–55

    Google Scholar 

  • Hubbard AL, Cohn ZA (1972) The enzymatic iodination of the cell membrane. J Cell Biol 55:390–405

    Google Scholar 

  • Klämbt C, Müller S, Lützelschwab R, Rossa R, Totzke F, Schmidt O (1989) The Drosophila melanogaster l(2)gl gene encodes a protein homologous to the cadherin cell adhesion molecule family. Dev Biol 133:425–436

    Google Scholar 

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

    Google Scholar 

  • Moscona A, Moscona H (1952) Dissociation and aggregation of cells from organ rudiments of the early chick embryos. J Anat 86:287–301

    Google Scholar 

  • Nagafuchi A, Shirayoshi Y, Okazaki K, Yasuda K, Takeichi M (1987) Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA. Nature 329:341–343

    Google Scholar 

  • Nose A, Nagafuchi A, Takeichi M (1988) Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54:993–1001

    Google Scholar 

  • Ozawa M, Baribault H, Kemler R (1989) The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8:1711–1717

    Google Scholar 

  • Rickoll WL, Counce SJ (1980) Morphogenesis in the embryo of Drosophila melanogaster. Germ band extension. Roux's Arch Dev Biol 188:163–177

    Google Scholar 

  • Sang JH (1981) Drosophila cells and cell lines. Adv Cell Cult 1:125–182

    Google Scholar 

  • Seecof RL (1979) Preparation of cell cultures from Drosophila melanogaster embryos. TCA Man 5:1019–1022

    Google Scholar 

  • Seecof RL, Alleaume N, Teplitz RL, Gerson I (1971) Differentiation of neurons and myocytes in cell cultures made from Drosophila gastrulae. Exp Cell Res 69:161–173

    Google Scholar 

  • Seecof RL, Donady JJ, Teplitz RL (1973) Differentiation of Drosophila neuroblasts to form ganglion-like clusters of neurons in vitro. Cell Differ 2:143–149

    Google Scholar 

  • Seeger MA, Haffley L, Kaufman TC (1988) Characterization of amalgam: a member of the immunoglobulin superfamily of Drosophila. Cell 55:589–600

    Google Scholar 

  • Sémériva M, Naidet C, Krejci E, Gratecos D (1989) Towards the molecular biology of cell adhesion in Drosophila. Trends Genet 5:24–28

    Google Scholar 

  • Shields G, Sang JH (1977) An improved medium for the cultivation of Drosophila cells. Drosophila Inf Ser 52:161

    Google Scholar 

  • Takeichi M (1977) Functional correlation between cell adhesive properties and some cell surface proteins. J Cell Biol 75:464–474

    Google Scholar 

  • Takeichi M (1988) The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102:639–655

    Google Scholar 

  • Takeichi M, Hatta K, Nagafuchi A (1985) Selective cell-adhesion mechanism: role of the calcium-dependent cell adhesion system. In: Edelman GM (ed) Molecular determinants of animal form. AR Liss, New-York, pp 223–233

    Google Scholar 

  • Townes PL, Holtfreter J (1955) Directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool 128:53–120

    Google Scholar 

  • Trinkaus JP (1984) Cells into organs, Prentice Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Ui K, Ueda R, Miyake T (1988) In vitro cultures of cells from different kinds of imaginal discs of Drosophila melanogaster. Jpn J Genet 63:33–41

    Google Scholar 

  • Wu CF, Suzuki N, Poo MM (1983) Dissociated neurons from normal and mutant Drosophila larval central nervous system in cell culture. J Neurosci 3:1888–1899

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gratecos, D., Krejci, E. & Sémériva, M. Calcium-dependent adhesion of Drosophila embryonic cells. Roux's Arch Dev Biol 198, 411–419 (1990). https://doi.org/10.1007/BF00376160

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00376160

Key words

Navigation