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Responses to cell contacts between growth cones, neurites and ganglionic non-neuronal cells

  • Published:
Journal of Neurocytology

Summary

The motility of growth cones of embryonic peripheral neurons is not inhibited by contact with the surfaces of neurites or of non-neuronal cells. Rather, growth cones and microspikes adhere to other cell surfaces and often respond with forward movement and elongation in contact with other cells, as they do on adhesive surfacesin vitro. Furthermore, non-neuronal cells do not display contact inhibition when they contact growth cones or neurites. If anything, surface motility and ruffling is stimulated by contact with a neuronal cell surface and some non-neuronal cells prefer to migrate along neurites rather than on the surface of the culture dish.

These observations on the contact behaviour of cells from peripheral nerve ganglia imply that the surfaces of embryonic neurons differ from those of non-neuronal cells in that the neuronal surfaces do not elicit the typical contact inhibition response.

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References

  • Abercrombie, M. (1967) Contact inhibition: The phenomenon and its biological implications.National Cancer Institute Monograph 26, 249–73.

    Google Scholar 

  • Abercrombie, M. A. &Dunn, G. A. (1975) Adhesions of fibroblasts to substratum during contact inhibition observed by interference reflection microscopy.Experimental Cell Research 92, 57–62.

    Google Scholar 

  • Albrecht-Buehler, G. (1976) Filopodia of spreading 3T3 cells.Journal of Cell Biology 69, 275–86.

    Google Scholar 

  • Albrecht-Buehler, G. &Goldman, R. D. (1976) Microspike mediate particle transport towards the cell body during early spreading of 3T3 cells.Experimental Cell Research 97, 329–39.

    Google Scholar 

  • Bell, P. B. (1977) Locomotory behavior, contact inhibition, and pattern formation of 3T3 and polyoma virus-transformed 3T3 cells in culture.Journal of Cell Biology 74, 963–82.

    Google Scholar 

  • Boyde, A., Grainger, F. &James, D. W. (1969) Scanning electron microscopic observations of chick embryo fibroblastsin vitro, with particular reference to the movement of cells under others.Zeitschrift für Zellforschung und mikroskopische Anatomie 94, 46–55.

    Google Scholar 

  • Bray, D. (1970) Surface movements during the growth of single explanted neurons.Proceedings of the National Academy of Sciences (U.S.A.) 65, 905–10.

    Google Scholar 

  • Bray, D. (1973a) Model for membrane movements in the neural growth cone.Nature 244, 93–6.

    Google Scholar 

  • Bray, D. (1973b) Branching patterns of individual sympathetic neurons in culture.Journal of Cell Biology 56, 702–12.

    Google Scholar 

  • Bray, D. &Bunge, M. B. (1973) The growth cone in neurite extension. InCiba Foundation Symposium, Vol. 14,Locomotion of Tissue Cells, pp. 195–209. Amsterdam: Associated Scientific Publishers.

    Google Scholar 

  • Bray, D., Thomas, C. &Shaw, G. (1978) Growth cone formation in cultures of sensory neurons.Proceedings of the National Academy of Sciences (U.S.A.) 75, 5226–9.

    Google Scholar 

  • Bunge, M. B. (1977) Initial endocytosis of peroxidase or ferritin by growth cones of cultured nerve cells.Journal of Neurocytology 6, 407–39.

    Google Scholar 

  • Di Pasquale, A. &Bell, P. B., Jr (1974) The upper cell surface: its inability to support active cell movement in culture.Journal of Cell Biology 62, 198–214.

    Google Scholar 

  • Di Pasquale, A. &Bell, P. B., Jr (1975) Comments on reported observations of cells spreading on the upper surfaces of other cells in culture.Journal of Cell Biology 66, 216–8.

    Google Scholar 

  • Dunn, G. A. (1971) Mutual contact inhibition of extension of chick sensory nerve fibersin vitro.Journal of Comparative Neurology 143, 491–508.

    Google Scholar 

  • Ebendal, T. (1976) The relative roles of contact inhibition and contact guidance in orientation of axons extending on aligned collagen fibrilsin vitro.Experimental Cell Research 98, 159–69.

    Google Scholar 

  • Ebendal, T. (1977) Extracellular matrix fibrils and cell contacts in the chick embryo.Cell and Tissue Research 175, 439–58.

    Google Scholar 

  • Gail, M. H. &Boone, C. W. (1972) Cell-substrate adhesivity.Experimental Cell Research 70, 33–40.

    Google Scholar 

  • Harris, A. (1973) Behaviour of cultured cells on substrata of variable adhesiveness.Experimental Cell Research 77, 285–97.

    Google Scholar 

  • Harris, A. (1974) Contact inhibition of cell locomotion. InCell Communication (edited byCox, R. P.), pp. 147–185. New York: Wiley.

    Google Scholar 

  • Harris, A. &Dunn, G. A. (1972) Centripetal transport of attached particles on both surfaces of moving fibroblasts.Experimental Cell Research 73, 519–22.

    Google Scholar 

  • Heaysman, J. E. M. (1978) Contact inhibition of locomotion: a reappraisal.International Review of Cytology 55, 49–66.

    Google Scholar 

  • Heaysman, J. E. M. &Pegrum, S. M. (1973) Early contact between fibroblasts. An ultrastructural study.Experimental Cell Research 78, 71–8.

    Google Scholar 

  • Helfand, S. L., Smith, G. A. &Wessells, N. K. (1976) Survival and development in culture of dissociated parasympathetic neurons from ciliary ganglia.Developmental Biology 50, 541–7.

    Google Scholar 

  • Jacobson, M. (1978)Developmental Neurobiology. 2nd edn. New York: Holt, Rhinehart, Winston.

    Google Scholar 

  • Letourneau, P. C. (1975a) Possible roles for cell-to-substratum adhesion in neuronal morphogenesis.Developmental Biology 44, 77–91.

    Google Scholar 

  • Letourneau, P. C. (1975b) Cell-to-substratum adhesion and guidance of axonal elongation.Developmental Biology 44, 92–101.

    Google Scholar 

  • Letourneau, P. C. (1979) Cell-substratum adhesion of neurite growth cones, and its role in neurite elongation.Experimental Cell Research 124, 127–38.

    Google Scholar 

  • Lopresti, V., Macagno, E. R. &Levinthal, C. (1973) Structure and development of neural connections in isogenous organisms: Cellular interactions in the development of the optic lamina ofDaphnia.Proceedings of the National Academy of Sciences (U.S.A.) 70, 433–7.

    Google Scholar 

  • Ludueña, M. A. (1973a) Nerve cell differentiationin vitro.Developmental Biology 33, 268–4.

    Google Scholar 

  • Luduena, M. A. (1973b) The growth of spinal ganglion neurons in serum-free medium.Developmental Biology 33, 470–6.

    Google Scholar 

  • Ludueña, M. A. &Wessells, N. K. (1973) Cell locomotion, nerve elongation and microfilaments.Developmental Biology 30, 427–40.

    Google Scholar 

  • Nakai, J. (1956) Dissociated dorsal root ganglia in tissue culture.American Journal of Anatomy 99, 81–130.

    Google Scholar 

  • Nakai, J. (1960) Studies on the mechanism determining the course of nerve fibers in tissue culture. II. The mechanism of fasciculation.Zeitschrift für Zellforschung und mikroskopische Anatomie 52, 427–49.

    Google Scholar 

  • Nakai, J. &Kawasaki, Y. (1959) Studies on the mechanism determining the course of nerve fibers in tissue culture. I. The reactions of the growth cone to various obstructions.Zeitschrift für Zellforschung und mikroskopische Anatomie 51, 108–22.

    Google Scholar 

  • Nakajima, S. (1965) Selectivity in fasciculation of nerve fibersin vitro.Journal of Comparative Neurology 125, 193–204.

    Google Scholar 

  • Parkinson, E. K. &Edwards, S. G. (1978) Non-reciprocal contact inhibition of locomotion of chick embryonic choroid fibroblasts by pigmented retina epithelial cells.Journal of Cell Science 33, 103–20.

    Google Scholar 

  • Rakic, P. (1971) Neuron-glia relationship during granule cell migration in developing cerebellar cortex, a Golgi and EM study inMacacus rhesus.Journal of Comparative Neurology 141, 283–312.

    Google Scholar 

  • Speidel, C. C. (1933) Studies of living nerves. II. Activities of ameboid growth cones, sheath cells, and myelin segments, as revealed by prolonged observation of individual nerve fibers in frog tadpoles.American Journal of Anatomy 52, 1–79.

    Google Scholar 

  • Spooner, B. S., Ludueña, M. A. &Wessells, N. K. (1974) Membrane fusion in the growth cone-microspike region of embryonic nerve cells undergoing axon elongation in cell culture.Tissue and Cell 6, 399–409.

    Google Scholar 

  • Stephenson, E. M. &Stephenson, N. G. (1978) Invasive locomotory behaviour between malignant human melanoma cells and normal fibroblasts filmedin vitro.Journal of Cell Science 32, 389–412.

    Google Scholar 

  • Tosney, K. W. (1978) The early migration of neural crest cells in the trunk region of the avian embryo: An electron microscopic study.Developmental Biology 62, 317–33.

    Google Scholar 

  • Trinkaus, J. P. (1976) On the mechanism of metazoan cell movements. InThe Cell Surface in Animal Embryogenesis and Development (edited byPoste, G. andNicolson, G. L.), pp. 225–329. Amsterdam: North-Holland.

    Google Scholar 

  • Trinkaus, J. P., Betchaku, T. &Krulikowski, L. S. (1971) Local inhibition of ruffling during contact inhibition of cell movement.Experimental Cell Research 64, 291–300.

    Google Scholar 

  • Weiss, P. (1941)Nerve Patterns: the Mechanics of Nerve Growth. 3rd Growth Symposium, Vol. 5, pp. 163–203.

    Google Scholar 

  • Wessells, N. K., Johnson, S. R. &Nuttall, R. P. (1978) Axon initiation and growth cone regeneration in cultured motor neurons.Experimental Cell Research 117, 335–45.

    Google Scholar 

  • Wessells, N. K. &Nuttall, R. P. (1978) Normal branching, induced branching and steering of cultured parasympathetic motor neuronsin vitro.Experimental Cell Research 115, 111–22.

    Google Scholar 

  • Wessells, N. K., Nuttall, R. P., Wrenn, J. T. &Johnson, S. (1976) Differential labeling of the cell surface of single ciliary ganglion neuronsin vitro.Proceedings of the National Academy of Sciences (U.S.A.) 73, 4100–4.

    Google Scholar 

  • Wood, P. M. (1976) Separation of functional Schwann cells and neurons from normal peripheral nerve tissue.Brain Research 115, 361–75.

    Google Scholar 

  • Yamada, K. M., Spooner, B. S. &Wessells, N. K. (1971) Ultrastructure and function of growth cones and axons of cultured nerve cells.Journal of Cell Biology 49, 614–35.

    Google Scholar 

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Authors and Affiliations

  1. Department of Biological Sciences, Stanford University, 94305, Stanford, California, USA

    Norman K. Wessells, Marilyn Ludueña-Anderson & Jeremy M. Geiduschek

  2. Department of Anatomy, University of Minnesota, 4-135 Jackson Hall, 55455, Minneapolis, Minnesota, USA

    Paul C. Letourneau

  3. Department of Biology, Emory University, 30322, Atlanta, Georgia, USA

    Robert P. Nuttall

Authors
  1. Norman K. Wessells
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  2. Paul C. Letourneau
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  3. Robert P. Nuttall
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  4. Marilyn Ludueña-Anderson
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  5. Jeremy M. Geiduschek
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Wessells, N.K., Letourneau, P.C., Nuttall, R.P. et al. Responses to cell contacts between growth cones, neurites and ganglionic non-neuronal cells. J Neurocytol 9, 647–664 (1980). https://doi.org/10.1007/BF01205031

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  • DOI: https://doi.org/10.1007/BF01205031

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