Summary
In response to concanavalin A (Con A), neuroblastoma cells undergo marked morphological changes which involve the retraction of neurites and the induction of broad and extensive lamellar regions around the cell periphery. From the use of FITC-Con A it was shown that the membrane formed on the induced lamellar regions lacked receptors to Con A from the onset of lamella formation. These receptors were confined to the cell body; they initially showed a uniform distribution and were subsequently collected into patches and finally into aggregates or caps. When the aggregates occurred on the cell periphery their position coincided with areas free of lamellae.
Investigations of the lamellar regions in Triton-extracted cell monolayers showed them to consist of a meshwork of actin filaments containing radiating thin filament bundles or microspikes. With increasing time in the presence of Con A there was a progressive increase in the number of radiating microspikes. Previous studies have shown the actin in these lamellar regions to be singly polarized with respect to the cell body.
From the segregation of Con A receptors away from areas of actin polymerization in the lamellae it is concluded that actin is involved in some indirect way in surface receptor movement.
Similar content being viewed by others
References
Abercrombie, M., Heaysman, J. E. M. andPegrum, S. M. (1970) The locomotion of fibroblasts in culture. III. Movements of particles on the dorsal surface of the leading lamella.Experimental Cell Research 62, 389–98.
Abercrombie, M., Heaysman, J. E. M. andPegrum, S. M. (1972) Locomotion of fibroblasts in culture. V. Surface marking with Concanavalin A.Experimental Cell Research 73, 536–9.
Albertini, D. F., Berlin, R. D. andOliver, J. M. (1977) The mechanism of Concanavalin A cap formation in leucocytes.Journal of Cell Science 26, 57–75.
Bourguignon, L. Y. W. andSinger, S. J. (1977) Transmembrane interactions and the mechanism of capping of surface receptors by their specific ligands.Proceedings of the National Academy of Sciences, U.S.A. 74, 5031–5.
Bretscher, M. S. (1976) Directed lipid flow in cell membranes.Nature 260, 21–3.
De Petris, S. (1977) Distribution and mobility of plasma membrane components on lymphocytes. InCell Surface Reviews (edited byPoste, G. andNicholson, G. L.) pp. 643–728. Amsterdam: North Holland.
De Petris, S. andRaff, M. C. (1972) Distribution of immunoglobulin on the surface of mouse lymphoid cells as determined by immunoferritin electron microscopy. Antibody-induced, temperature-dependent redistribution and its implications for membrane structure.European Journal of Immunology 2, 523–35.
De Petris, S. andRaff, M. C. (1973) Fluidity of the plasma membrane and its implications for cell movement. InLocomotion of Tissue Cells (CIBA Foundation Symposium No. 14) (edited byPorter, R. andFitzsimmons, D. W.), pp. 27–41. Amsterdam: Excerpta Medica.
Domnina, L. V., Pletyushkina, O. Y., Vasiliev, J. M. andGelfand, I. M. (1977) Effects of antitubulins on the redistribution of cross-linked receptors on the surface of fibroblasts and epithelial cells.Proceedings of the National Academy of Sciences, U.S.A. 74, 2865–8.
Edelman, G. M. (1976). Surface modulation in cell recognition and cell growth.Science 192, 218–26.
Gabbiani, G., Chaponnier, C., Zumbe, A. andVassalli, P. (1977) Actin and tubulin co-cap with surface immunoglobulins in mouse B lymphocytes.Nature 269, 697–8.
Goldacre, R. J. (1961) The role of the cell membrane in the locomotion of amoebae, and the source of the motive force and its control by feedback.Experimental Cell Research Suppl. 1–16.
Graham, R. C. andKarnovsky, M. J. (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: Ultrastructural cytochemistry, a new technique.Journal of Histochemistry and Cytochemistry 14, 291–302.
Harris, A. K. (1973) Cell surface movements related to cell locomotion. InLocomotion of Tissue Cells (CIBA Foundation Symposium No. 14) (edited byPorter, R. andFitzsimmons, D. W.) pp. 3–26. Amsterdam: Excerpta Medica.
Harris, A. K. (1976) Recycling of dissolved plasma membrane components as an explanation of the capping phenomenon.Nature 264, 411.
Harris, A. K. andDunn, G. (1972) Centripetal transport of attached particles on both surfaces of moving fibroblasts.Experimental Cell Research 73, 519–23.
Ingram, V. M. (1969) A side view of moving fibroblasts.Nature 222, 641–4.
Isenberg, G., Rathke, P. C., Hülsmann, N., Franke, W. W. andWohlfarth-Bottermann, K. E. (1976) Cytoplasmic actomyosin fibrils in tissue culture cells-Direct proof of contractility by visualization of ATP-induced contraction of fibrils isolated by laser microbeam dissection.Cell and Tissue Research 166, 427–43.
Isenberg, G., Rieske, E. andKreutzberg, G. W. (1977) Distribution of actin and tubulin in neuroblastoma cells.Cytobiologie 15, 382–9.
Isenberg, G. andSmall, J. V. (1978) Filamentous actin, 100 Å filaments and microtubules in neuroblastoma cells: Their distribution in relation to sites of movement and neuronal transport.Cytobiologie 16, 326–44.
Kushida, H. (1961) A styrene methacrylate resin embedding method for ultrathin sectioning.Journal of Electron Microscopy 10, 16–9.
Luftig, R. B., Mcmillan, P. N., Weatherbee, J. A. andWeihing, R. R. (1977) Increased visualization of microtubules by an improved fixation procedure.Journal of Histochemistry and Cytochemistry 25, 175–87.
Nicolson, G. L. (1976a) Transmembrane control of the receptors on normal and tumor cells, I. Cytoplasmic influence over cell surface components.Biochimica et Biophysica Acta 457, 57–108.
Nicolson, G. L. (1976b) Transmembrane control of the receptors on normal and tumor cells. II. Surface changes associated with transformation and malignancy.Biochimica et Biophysica Acta 458, 1–72.
Nicolson, G. L. andPoste, G. (1976) The cancer cell: Dynamic aspects and modifications in cell-surface organization.New England Journal of Medicine 295, 197–203 (Part 1); 253–8 (Part 2)
Nicolson, G. L., Poste, G., andJi, T. H. (1977) The dynamics of cell membrane organization. InCell Surface Reviews (edited byPoste, G. andNicolson, G. L.) Vol. 3. pp. 1–73. Amsterdam: North Holland.
Oliver, J. M., Lalchandani, R. andBecker, E. L. (1977) Actin redistribution during Concanavalin A cap formation in rabbit neutrophils.Journal of the Reticuloendothelial Society 21, 359–64.
Schreiner, G. F. andUnanue, E. R. (1976) Membrane and cytoplasmic changes in B lymphocytes induced by ligand-surface immunoglobulin interaction.Advances in Immunology 24, 38–165.
Small, J. V. andCelis, J. E. (1978) Filament arrangements in negatively stained cultured cells. I. The organization of actin.Cytobiologie 16, 308–25.
Small, J. V., Isenberg, G. andCelis, J. E. (1978). Polarity of actin at the leading edge of cultured cells.Nature 272, 638–9.
Storrie, B. andEdelson, P. J. (1977) Distribution of Concanavalin A in fibroblasts: Direct endocytosis versus surface capping.Cell 11, 707–17.
Taylor, R. B., Duffus, W. P. H., Raff, M. C. andDe Petris, S. (1971) Redistribution and pinocytosis of lymphocyte surface immunoglobulin molecules induced by anti-immunoglobulin antibody.Nature New Biology 233, 225–9.
Toh, B. H. andHard, G. C. (1977) Actin co-caps with Concanavalin A receptors.Nature 269, 695–6.
Vasiliev, J. M., Gelfand, I. M., Domnina, L. V., Dorfman, N. A. andPletyushkina, O. Y. (1976) Active cell edge and movements of Concanavalin A receptors of the surface of epithelial and fibroblastic cells.Proceedings of the National Academy of Sciences, U.S.A. 73, 4085–9.
Vasiliev, J. M. andGelfand, I. M. (1977) Mechanisms of morphogenesis in cell cultures.International Review of Cytology 50, 159–274.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Isenberg, G., Small, J.V. & Kreutzberg, G.W. Correlation between actin polymerization and surface receptor segregation in neuroblastoma cells treated with concanavalin A. J Neurocytol 7, 649–661 (1978). https://doi.org/10.1007/BF01260896
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01260896