Skip to main content

Factors Affecting Neurite Outgrowth in Cell Culture

  • Chapter
Current Aspects of the Neurosciences
  • 14 Accesses

Abstract

A major challenge in developmental neurobiology is the characterization of the epigenetic factors controlling axonal outgrowth towards or within a given target tissue. Important factors are likely to include the expression of receptors for, and availability of, soluble neurotrophic factors such as nerve growth factor (NGF). In addition, the expression of receptors for extracellular matrix components and cell adhesion molecules is likely to directly control growth cone interaction with the local microenvironment. Primary cell cultures of peripheral and central nervous tissue, together with well-characterized ‘neuronal’ cell lines have proved to be a convenient means of identifying some of the factors that may influence neurite outgrowth during development. However, it should be remembered that in vitro observations rarely constitute direct evidence of a physiological function, with the latter normally only established by use of a variety of strategies. The starting point for a study of the factors that affect neurite outgrowth in vitro is generally the isolation of viable healthy neurons from the central or peripheral nervous system. In many instances well-characterized neuronal cell lines offer positive advantages over primary neurons in terms of homogeneity of the population and the large numbers of cells that can be obtained for biochemical analysis. These cells also have disadvantages that limit the conclusions that can be deduced.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

  • Acheson, A., Edgar, D., Timpl, R. and Thoenen, H. (1986). Laminin increases both levels and activity of tyrosine hydroxylase in calf adrenal chromaffin cells. J. Cell. Biol., 102, 151–159

    Google Scholar 

  • Aloe, L. and Levi-Montalcini, R. (1979). Nerve growth factor induced transformation of immature chromaffin cells in vivo to sympathetic neurons: effect of antiserum to nerve growth factor. Proc. NatlAcad. Sci. USA, 76,1246–1250

    Google Scholar 

  • Barde, Y.-A., Edgar, D. and Thoenen, H. (1980). Sensory neurons in culture: changing requirements for survival factors during embryonic development. Proc. Natl Acad. Sci. USA, 77,1199–1203

    Google Scholar 

  • Barnstable, C. J. and Drager, U.C. (1984). Thy-1 antigen: a ganglion cell specific marker in rodent retina. Neuroscience, 11, 847–855

    Google Scholar 

  • Bixby, J. L., Pratt, R. S., Lilien, J. and Reichardt, L. F. (1987). Neurite outgrowth on muscle cell surfaces involves extracellular matrix receptors as well as Ca2+-dependent and -independent cell adhesion molecules. Proc. NatlAcad. Sci. USA, 84, 2555–2559

    Google Scholar 

  • Bottenstein, J. E. (1984). Growth and differentiation of neural cells in defined media. In Cell Culture in the Neurosciences (ed. J. E. Bottenstein and G. Sato). Plenum Press, New York, London

    Google Scholar 

  • Carbonetto, S., Gruver, M. M. and Turner, D. C. (1982). Nerve fibre growth in culture on fibronectin, collagen and glycosaminoglycan substrates. J. Neurosci., 3, 2324–2335

    Google Scholar 

  • Chiu, A. Y., Matthew, W. D. and Patterson, P. H. (1986). A monoclonal antibody blocks the activity of a neurite regeneration-promoting factor: studies on the binding site and its localisation in vivo. J. Cell. Biol, 103,1383–1398

    Google Scholar 

  • Cohen, J., Burne, J. F., McKinlay, C. and Winter, J. (1987). The role of laminin and the laminin/fibronectin receptor complex in the outgrowth of retinal ganglion cell axons. Dev. Biol, 122, 407–418

    Google Scholar 

  • Collins, F. (1988). Developmental time course of the effect of nerve growth factor on the parasympathetic ciliary ganglion. Dev. Brain Res., 39,111–116

    Google Scholar 

  • Davies, A. M. (1987). Molecular and cellular aspects of patterning sensory neurone connections in the vertebrate nervous system. Development, 101,185–208

    Google Scholar 

  • Davies, A. M. (1988). The emerging generality of the neurotrophic hypothesis. Trends Neurosci., 11, 243–244

    Google Scholar 

  • Davies, A. M. and Lindsay, R. M. (1985). The cranial sensory ganglia in culture: differences in the response of placode-derived and neural crest-derived neurons to nerve growth factor. Dev. Biol, 111, 62–72

    Google Scholar 

  • Davies, A. M., Thoenen, H. and Barde, Y. A. (1986). The response of chick sensory neuron to brain-derived neurotrophic factor. J. Neurosci., 6, 1897–1904

    Google Scholar 

  • Dickson, J. G., Flanigan, T. P. and Walsh, F. S. (1982). Cell surface antigens of human foetal brain and dorsal root ganglion cells in tissue culture. In Human Motor Neuron Diseases (ed. L. P. Rowland). Raven Press, New York, pp. 435–451

    Google Scholar 

  • Doherty, P., Dickson, J. G., Flanigan, T. P. and Walsh, F. S. (1984a). Quantitative evaluation of neurite outgrowth in cultures of human foetal brain and dorsal root ganglion cells using an enzyme-linked immunoadsorbent assay for human neurofilament protein. J. Neurochem., 42, 1116–1122

    Google Scholar 

  • Doherty, P., Dickson, J. G., Flanigan, T. P. and Walsh, F. S. (1984b). The effect of nerve growth factor and its antibodies on neurofilament protein expression in primary cultures of sensory and spinal neurons. Neruosci. Lett., 51, 55–60

    Google Scholar 

  • Doherty, P., Dickson, J. G., Flanigan, T. P., Leon, A., Toffano, G. and Walsh, F. S. (1985a). Molecular specificity of ganglioside effects on neurite regeneration of sensory neurons in vitro. Neurosci. Lett., 62, 193–198

    Google Scholar 

  • Doherty, P., Dickson, J. G., Flanigan, T. P. and Walsh, F. S. (1985b). Ganglioside GM1 does not initiate, but enhances neurite regeneration of nerve-growth factor-dependent sensory neurones. J. Neurochem., 41, 1259–1265

    Google Scholar 

  • Doherty, P., Mann, D. A. and Walsh, F. S. (1987). Cell-cell interactions modulate the responsiveness of PC12 cells to nerve growth factor. Development, 101, 605–615

    Google Scholar 

  • Doherty, P., Mann, D. A. and Walsh, F. S. (1988a). Comparison of the effects of NGF, activators of protein kinase C, and a calcium ionophore on the expression of Thy-1 and N-CAM in PC12 cell cultures. J. Cell Biol., 107, 333–340

    Google Scholar 

  • Doherty, P., Robinson, E. and Walsh, F. S. (1988b). Analysis of PC12 cell adhesion to muscle and non-muscle cells and components of the extracellular matrix. Exp. Cell. Res., 179,233–242 Doherty, P. and Walsh, F. S. (1987). Ganglioside GM1 antibodies and β-cholera toxin bind specifically to embryonic chick dorsal root ganglion neurons but do not modulate neurite regeneration. J. Neurochem., 48, 1237–1244

    Google Scholar 

  • Doherty, P. and Walsh, F. S. (1989). K-252a specifically inhibits the survival and morphological differentiation of NGF-dependent neurons in primary cultures of human dorsal root ganglia. Neuroscience Lett., 96, 1–6

    Google Scholar 

  • Dohrmann, U., Edgar, D. and Thoenen, H. (1987). Distinct neurotrophic factors from skeletal muscle and the central nervous system interact synergistically to support the survival of cultured embryonic spinal motor neurons. Dev. Biol., 124,145–152

    Google Scholar 

  • Edgar, D., Timpl, R. and Thoenen, H. (1984). The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. EMBO Jl., 3,1463–1468 Fallon, J. R. (1985). Neurite guidance by non-neuronal cells in culture: preferential outgrowth of peripheral neurites on glial as composed to nonglial cell surfaces. J. Neurosci., 12, 3169–3177 Flanigan, T. P., Dickson, J. G. and Walsh, F. S. (1985). Cell survival characteristics and choline acetyltransferase activity in neuron-enriched cultures from chick embryo spinal cord. J. Neurochem., 45, 1323–1326

    Google Scholar 

  • Gorio, A., Marini, P. and Zanoni, R. (1983). Motor neuron sprouting capacity enhancement by exogenous gangliosides. Neruoscience, 8, 417–429

    Google Scholar 

  • Greene, L. A. (1984). The importance of both early and delayed responses in the biological actions of nerve growth factor. Trends Neurosci., 7, 91–94

    Google Scholar 

  • Grumet, M. and Edelman, G. M. (1988). Neuron-glia adhesion molecule interacts with neurons and astroglia via different binding mechanisms. J. Cell. Biol., 106, 487–504

    Google Scholar 

  • Gundersen, R. W. and Barrett, J. N. (1978). Neuronal chemotaxis: chick dorsal-root axons turn toward high concentration of nerve growth factor. Science, N.Y., 206,1079–1080

    Google Scholar 

  • Hamburger, V. (1958). Regression versus peripheral control of differentiation in motor hypoplasia. Am. J. Anat., 102, 365–410

    Google Scholar 

  • Hamburger, V. and Oppenheim, R. W. (1982). Naturally occurring neuronal death in vertebrates. Neurosci. Commentaries, 1, 39–55

    Google Scholar 

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

    Google Scholar 

  • Hefti, F., Hartikka, J., Eckenstein, F., Gnahn, H., Neumann, R. and Schwab, M. (1985). Nerve growth factor increases choline acetyltransferase but not survival of fibre outgrowth of cultured foetal septal cholinergic neurons. Neuroscience, 14, 55–68

    Google Scholar 

  • Henderson, C. E. (1988). The role of muscle in the development and differentiation of spinal

    Google Scholar 

  • motorneurons: in vitro studies. In Plasticity of the Neuromuscular System, Ciba Foundation Symposium 138. Wiley, Chichester, pp. 172–191

    Google Scholar 

  • Hilbig, R., Lanke, G. and Rohman, H. (1983). Brain gangliosides during the life span (embryogenesis to senescence) of the rat. Dev. Neurosci., 6, 260–270

    Google Scholar 

  • Hofer, M. M. and Barde, Y.-A. (1988). Brain-derived neurotrophic factor prevents neuronal death in vivo. Nature, 331, 261–262

    Google Scholar 

  • Hollyday, M. and Hamburger, V. (1976). Reduction of the naturally occurring motor neuron loss by enlargement of the periphery. J. Comp. Neurol., 170, 311–320

    Google Scholar 

  • Horwitz, A., Duggan, K., Greggs, R., Decker, C. and Buck, C. (1985). The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J. Cell. Biol, 101, 2134–2144 Hynes, R. O. (1987). Integrins: a family of cell surface receptors. Cell, 48, 549–554

    Google Scholar 

  • Johnson, J. E., Barde, Y.-A., Schwab, M. and Thoenen, H. (1986). Brain-derived neurotrophic factor supports the survival of cultured rat retinal ganglion cells. J. Neurosci., 6, 3031–3038

    Google Scholar 

  • Lander, A. D., Fujii, D. K. and Reichasdt, L. F. (1985). Purification of a factor that promotes neurite outgrowth: isolation of laminin and associated molecules. J. Cell. Biol., 101, 898–913

    Google Scholar 

  • Lasek, R. J. (1982). Translocation of the neuronal cytoskeleton and axonal locomotion. Phil. Trans. R. Soc. Lond. (Biol.), 299, 313–327

    Google Scholar 

  • Levi-Montalcini, R. (1987). The nerve growth factor 35 years later. Science, N.Y., 237, 1154–1162

    Google Scholar 

  • Lindsay, R. M., Thoenen, H. and Barde, Y.-A. (1985). Placode and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor (BDNF). Dev. Biol., 112, 319–328

    Google Scholar 

  • Manthorpe, M., Engvall, E., Ruoslahti, E., Longo, F. M., Davis, G. E. and Varon, S. (1983). Laminin promotes neurite regeneration from cultured peripheral and central neurons. J. Cell. Biol., 97, 1882–1890

    Google Scholar 

  • Matsunaga, M., Hatta, H., Nagafuchi, A. and Takeichi, M. (1988). Guidance of optic nerve fibres by N-cadherin adhesion molecules. Nature, 334, 62–64

    Google Scholar 

  • Noble, M., Fok-Seang, J. and Cohen, J. (1984). Glia are a unique substrate for the in vitro growth of central nervous system neurons. J. Neurosci., 4, 1892–1903

    Google Scholar 

  • Oppenheim, R. W., Haverkamp, L. J., Prevette, D., McManaman, J. L. and Appel, S. H. (1988). Reduction of naturally occurring motoneuron death in vivo by a target-derived neurotrophic factor. Science, N. Y., 240, 919–922

    Google Scholar 

  • Rogers, S. L., Letourneau, P.-C, Palm, S. L., McCarthy, J. and Furcht, L. T. (1983). Neurite extension by peripheral and central nervous system neurons in response to substratum-bound fibronectin and laminin. Dev. Biol, 98, 212–220

    Google Scholar 

  • Roisen, F. J., Bartfeld, H., Nagele, L. and Yorke, G. (1981). Ganglioside stimulation of axonal sprouting in vitro. Science, N.Y., 214, 577–578

    Google Scholar 

  • Sandrock, A. W. and Matthew, W. D. (1987). An in vitro neurite-promoting antigen functions in axonal regeneration in vivo. Science, N.Y., 237, 1605–1608

    Google Scholar 

  • Schwartz, M. and Spirman, N. (1982). Sprouting from chicken embryo dorsal root ganglia induced by nerve growth factor is specifically inhibited by affinity-purified antiganglioside antibodies. Proc. NatlAcad. Sci. USA, 79, 6080–6083

    Google Scholar 

  • Seilheimer, B. and Schachner, M. (1988). Studies of adhesion molecules mediating interactions between cells of peripheral nervous system indicate a major role for LI in mediating sensory neuron growth on Schwann cells in culture. J. Cell. Biol., 107, 341–351

    Google Scholar 

  • Smith, G. R. and Appel, S. H. (1983). Extracts of skeletal muscle increase neurite outgrowth and cholinergic activity of foetal rat spinal motor neurons. Science, N. Y., 219, 1079–1081

    Google Scholar 

  • Thoenen, H. and Barde, Y.-A. (1980). Physiology of nerve growth factor. Physiol. Rev., 60, 1284–1335

    Google Scholar 

  • Toffano, G., Savoini, G., Moroni, F., Lombardi, G., Calza, L. and Agnati, L. F. (1983). GM1 ganglioside stimulates the regeneration of dopaminergic neurons in the central nervous system. Brain Res., 261, 163–168

    Google Scholar 

  • Tomaselli, K. J., Neugebauer, K. M., Bixby, J. L., Lilien, J. and Reichardt, L. F. (1988). Ncadherin and integrins: two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron, 1, 33–43

    Google Scholar 

  • Tomaselli, K. J., Reichardt, L. F. and Bixby, J. L. (1986). Distinct molecular interactions mediate neuronal process outgrowth on non-neuronal cell surfaces and extracellular matrices. J. Cell. Biol, 103, 2659–2672

    Google Scholar 

  • Tsusi, S., Arita, M. and Nagai, Y. (1983). GQ1b, a bioactive ganglioside that exhibits novel nerve growth factor (NGF)-like activities in two neuroblastoma cell lines. J. Biochem. (Tokyo), 94, 303

    Google Scholar 

  • Turner, D. C., Flier, L. A. and Carbonetto, S. (1987). Magnesium-dependent attachment and neurite outgrowth by PC12 cells on collagen and laminin substrata. Dev. Biol., 121, 510–525 Unsicker, K., Krisch, B., Otten, U. and Thoenen, H. (1978). Nerve growth factor-induced fibre outgrowth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids. Proc. NatlAcad. Sci. USA, 75, 3498–3502

    Google Scholar 

  • Vaccarino, F., Guidotti, A. and Costa, E. (1987). Ganglioside inhibition of glutamate-mediated protein kinase C translocation in primary cultures of cerebellar neurons. Proc. Natl Acad. Sci. USA, 84, 8707–8711

    Google Scholar 

  • Walsh, F. S. (1988). The N-CAM gene in a complex transcriptional unit. Neurochem. Int., 12, 263–267

    Google Scholar 

  • Yankner, B. A. and Shooter, E. M. (1982). The biology and mechanism of action of nerve growth factor. Ann. Rev. Biochem., 51, 845–868

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Copyright information

© 1990 Macmillan Publishers Limited

About this chapter

Cite this chapter

Doherty, P., Walsh, F.S. (1990). Factors Affecting Neurite Outgrowth in Cell Culture. In: Osborne, N.N. (eds) Current Aspects of the Neurosciences. Palgrave, London. https://doi.org/10.1007/978-1-349-10997-5_4

Download citation

  • DOI: https://doi.org/10.1007/978-1-349-10997-5_4

  • Publisher Name: Palgrave, London

  • Print ISBN: 978-1-349-10999-9

  • Online ISBN: 978-1-349-10997-5

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics