Skip to main content
Log in

The distribution and movement of organelles in maturing growth cones: correlated video-enhanced and electron microscopic studies

  • Published:
Journal of Neurocytology

Summary

The morphology of growth cones from identified neurons ofAplysia californica was analysed both with video-enhanced contrast differential-interference contrast (VEC-DIC) microscopy, and through serial electron microscopic reconstructions of the same growth cones. The largest structures seen in the living growth cones, the large irregular refractile bodies (LIRBs), were shown in electron micrographs to be unique structures, composed predominantly of dense-core vesicles but including mitochondria and smooth membrane profiles. The LIRBs were stratified in the growth cones, occurring predominantly in sections distant from the substrate and relatively devoid of microtubules. VEC-DIC observations showed that LIRBs formed in the peripheral regions of the organelle-rich central growth cone, and grew in size through fusion with other LIRBs, accumulating into a large central mass in more proximal regions. The distribution of microtubules and LIRBs and the movements of LIRB suggest that there is an overall circulatory pattern in the growth cones, with the delivery of new vesicles occurring at distal areas close to the substrate, and the accumulation and retrograde processing of organelles occurring in more proximal areas away from adhesive contacts.

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

  • Aletta, J. M. &Greene, L. A. (1988) Growth cone configuration and advance: A time-lapse study using videoenhanced differential interference contrast microscopy.Journal of Neuroscience 8, 1425–35.

    Google Scholar 

  • Bailey, C. H., Kandel, P. &Chen, M. (1981) Active zone atAplysia synapses: Organization of presynaptic dense projections,Journal of Neurophysiology 46, 356–68.

    Google Scholar 

  • Bailey, C. H., Thompson, E. B., Castellucci, V. F. &Kandel, E. R. (1979) Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex inAplysia.Journal of Neurocytology 8, 415–44.

    Google Scholar 

  • Bray, D. (1987) Growth cones: do they pull or are they pushed?Trends in Neuroscience 10, 431–4.

    Google Scholar 

  • Bunge, M. B. (1973) Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture.Journal of Cell Biology 56, 713–35.

    Google Scholar 

  • Bunge, M. B., Bunge, R. P. &Peterson, E. R. (1967) The onset of synapse formation in spinal cord cultures as studied by electron microscopy.Brain Research 6, 728–49.

    Google Scholar 

  • Burmeister, D. W. &Goldberg, D. J. (1988) Micropruning: The mechanism of turning ofAplysia growth cones at substrate bordersin vitro.Journal of Neuroscience 8, 3151–59.

    Google Scholar 

  • Chen, M., Burmeister, D. W., Bailey, C. &Goldberg, D. J. (1987) Clusters of dense-core vesicles behave as autonomous bodies within the growth cones ofAplysia neuronsin vitro.Society for Neuroscience Abstracts 13, 259.

    Google Scholar 

  • Cheng, T. P. O. &Reese, T. S. (1985) Polarized compartmentalization of organelles in growth cones from developing optic tectum.Journal of Cell Biology 101, 1473–80.

    Google Scholar 

  • Cheng, T. P. O. &Reese, T. S. (1987) Recycling of plasmalemma in chick tectal growth cones.Journal of Neuroscience 7, 1752–9.

    Google Scholar 

  • Chiang, R. G. &Govind, C. K. (1986) Reorganization of synaptic ultrastructure at facilitated lobster neuromuscular terminals.Journal of Neurocytology 15, 63–74.

    Google Scholar 

  • Del Cerro, M. P. &Snider, R. S. (1968) Studies in developing cerebellum. Ultrastructure of growth cones.Journal of Comparative Neurology 133, 341–62.

    Google Scholar 

  • Flaster, M. S., Ambron, R. T. &Schacher, S. (1986) Growth cones isolated from identifiedAplysia neuronsin vitro: biochemical and morphological characterization.Developmental Biology 118, 577–86.

    Google Scholar 

  • Forscher, P., Kaczmarek, L. K., Buchanan, J. A. &Smith, S. J. (1987) Cyclic AMP induces changes in distribution and transport of organelles within growth cones ofAplysia bag cell neurons.Journal of Neuroscience 7, 3600–11.

    Google Scholar 

  • Goldberg, D. J. &Burmeister, D. W. (1986) Stages in axon formation: Observations of growth of Aplysia axons in culture using Video-enhanced contrast-Differential Interference contrast microscopy.Journal of Cell Biology 103, 1921–31.

    Google Scholar 

  • Goldberg, D. J. &Burmeister, D. W. (1988) Growth cone movement.Trends in Neuroscience 11, 257–8.

    Google Scholar 

  • Goldberg, D. J. &Schacher, S. (1987) Differential growth of the branches of a regenerating bifurcate axon is associated with differential axonal transport of organelles.Developmental Biology 124, 35–40.

    Google Scholar 

  • Giller, E. L., Breakefield, X. O., Christian, C. N., Neale, E. A. &Nelson, P. G. (1975) Expression of neuronal characteristics in culture: some pros and cons of primary cultures and continuous cell lines. InGolgi Centennial Symposium, Pavia and Milan, 1973 (edited bySantini, M.), New York: Raven Press.

    Google Scholar 

  • Heuser, J. E. &Reese, T. J. (1977) Structure of the synapse. InHandbook of Physiology, Vol. 1,The Nervous System, Part 1 (edited byKandel, E. R.), pp. 261–94. Bethesda, MD: American Physiological Society.

    Google Scholar 

  • Hollenbeck, P. J. &Bray, D. (1987) Rapidly transported organelles containing membrane and cytoskeletal components: their relation to axonal growth.Journal of Cell Biology 106, 2827–35.

    Google Scholar 

  • Koenig, E., Kinsman, S., Repasky, E. &Sultz, L. (1985) Rapid mobility of motile varicosities and inclusions containing -spectrin, actin, and calmodulin in regenerating axonsin vitro.Journal of Neuroscience 5, 715–29.

    Google Scholar 

  • Kreiner, T., Sossin, W. &Scheller, R. H. (1986) Localization ofAplysia neurosecretory peptide to multiple populations of dense core vesicles.Journal of Cell Biology 102, 769–82.

    Google Scholar 

  • Landis, S. C. (1978) Growth cones of cultured sympathetic neurons contain adrenergic vesicles.Journal of Cell Biology 78, R8-R14.

    Google Scholar 

  • Letourneau, P. C., Shattuck, T. A. &Ressler, A. H. (1986) Branching of sensory and sympathetic neuritesin vitro is inhibited by treatment with taxol.Journal of Neuroscience 6 1912–17.

    Google Scholar 

  • Letourneau, P. C., Shattuck, T. A. &Ressler, A. H. (1987) “Pull” and “Push” in neurite elongation: observations on the effects of different concentrations of cytochalasin B and taxol.Cell Motility and the Cytoskeleton 8, 193–209.

    Google Scholar 

  • Moore, M. J. (1975) Removal of glass coverslips from cultures flat embedded in epoxy resins using hydrofluoric acid.Journal of Microscopy 104, 205–7.

    Google Scholar 

  • Nuttall, R. P. &Wessells, N. K. (1979) Veils, mounds, and vesicle aggregates in neurons elongating in vitro.Experimental Cell Research 119, 163–74.

    Google Scholar 

  • Pappas, G. D. &Waxman, S. G. (1972) Synaptic fine structure — morphological correlates of chemical and electrotonic transmission. InStructure and Function of Synapses (edited byPappas, G. D. &Purpura, D. P.). New York: Raven Press.

    Google Scholar 

  • Peters, A., Palay, S. L. &Webster, H. DeF. (1976)The Fine Structure of the Nervous System: The Neurons and Their Supporting Cells, Philadelphia: Saunders.

    Google Scholar 

  • Pfenninger, K. H. (1982) Axonal transport in the sprouting neuron: Transfer of newly synthesized membrane components to the cell surface. InAxoplasmic Transport in Physiology and Pathology (edited byWeiss, D. G. &Gorio, A.) Berlin: Springer-Verlag.

    Google Scholar 

  • Pfenninger, K. H. (1984) Molecular biology of the nerve growth cone: A perspective.Advances in Experimental Medicine and Biology 181, 1–14.

    Google Scholar 

  • Reed, W., Weiss, K. R., Lloyd, P. E., Kupferman, I., Chen, M. &Bailey, C. H. (1988) Association of neuroactive peptides with the protein secretory pathway in identified neurons ofAplysia californica. Immunolocalization of SCPA and SCPB to the contents of dense core vesicles and the trans face of the Golgi apparatus.Journal of Comparative Neurology 272, 358–69.

    Google Scholar 

  • Rees, R. P. &Reese, T. S. (1981) New structural features of freeze-substituted neuritic growth cones.Neuroscience 6, 247–54.

    Google Scholar 

  • Tosney, K. W. &Wessells, N. K. (1983) Neuronal motility: the ultrastructure of veils and microspikes correlates with their motile activities.Journal of Cell Science 61, 389–411.

    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 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Burmeister, D.W., Chen, M., Bailey, C.H. et al. The distribution and movement of organelles in maturing growth cones: correlated video-enhanced and electron microscopic studies. J Neurocytol 17, 783–795 (1988). https://doi.org/10.1007/BF01216706

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01216706

Keywords

Navigation