Skip to main content
SpringerLink
Log in

Peptide Modulation of Neuronal Differentiation in Culture

  • Chapter
Model Systems of Development and Aging of the Nervous System

Abstract

In attempts at the analysis of the highly complex process of development, particularly of the mammalian central nervous system (CNS), there are two equal and opposite imperatives: complexity (to capture what are undoubtedly complicated interactions between the multiple components of the intact system) and simplicity (to permit coherent and comprehensible results). Clearly, a clever choice of preparation is required such that the level of questions and their resolution is matched to the possibilities inherent in the system. For some questions, only a behaviorally intact animal will be an appropriate preparation, while for others a single, cloned gene may be best. We have chosen dissociated cell cultures prepared from the fetal mammalian central nervous system (Ransom et al., 1977) as a useful model for study of mechanisms of central synaptic action and the role of electrical activity in neuronal development. In this chapter, we deal in a general way with the properties of such system, including some of the advantages and disadvantages, and then present in some detail the results of using the dissociated spinal cord cultures in analyzing an important role that vasoactive intestinal peptide (VIP) has in mediating activity-dependent regulation of neuronal development. In addition, we examine general considerations for investigating developmental effects of neuropeptides and finally present a model for activity-dependent influences on neuronal survival.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Banker, G.A. (1980) Trophic interactions between astroglial cells and hippocampal neurons in cultures. Science 209:809–810.

    Article  PubMed  CAS  Google Scholar 

  • Ben Ari, Y., Krnjevic, K., Reinhardt, W., and Ropert, N. (1981) Intracellular observations on the disinhibitory action of acetylcholine in the hippocampus. Neuroscience 6:2475–2484.

    Article  PubMed  CAS  Google Scholar 

  • Bignami, A., Eng. L.F., Dahl, D., and Uyeda, C.T. (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 43:429–435.

    Article  PubMed  CAS  Google Scholar 

  • Bissonnette, B.M., Collen, M.J., Adachi, H., Jensen, R.T., and Gardner, J.D. (1984) Receptors for vasoactive intestinal peptide and secretin on rat pancreatic acini. Am. J. Physiol. 246:G710-G717.

    PubMed  CAS  Google Scholar 

  • Bottenstein, J., Skaper, S., Varon, S., and Sato, G. (1980) Selective survival of neurons from chick embryo sensory ganglionic dissociates utilizing serum-free supplemented medium. Exp. Cell Res. 125:183–190.

    Article  PubMed  CAS  Google Scholar 

  • Brenneman, D.E. (1986) Role of electrical activity and trophic factors during cholinergic development in dissociated cultures. Can. J. Physiol. Pharmacol. 64:356–362.

    Article  PubMed  CAS  Google Scholar 

  • Brenneman, D.E., and Eiden, L.E. (1986) Vasoactive intestinal peptide and electrical activity influence neuronal survival. Proc. Natl. Acad. Sci. USA 83:1159–1162.

    Article  PubMed  CAS  Google Scholar 

  • Brenneman, D.E., and Nelson (1985) Neuronal development in culture: role of electrical activity. In: Bottenstein, J.E., and Sato, G. (eds.) Cell culture in the neurosciences. New York: Plenum, pp. 289–316.

    Google Scholar 

  • Brenneman, D.E., Neale, E.A., Habig, W.H., Bowers, L.M., and Nelson, P.G. (1983) Developmental and neurochemical specificity of neurochemical deficits produced by electrical impulse blockade in dissociated spinal cord cultures. Dev. Brain Res. 9:13–27.

    Article  Google Scholar 

  • Brenneman, D.E., Fitzgerald, S., and Nelson, P.G. (1984) Interaction between trophic action and electrical activity in spinal cord cultures. Dev. Brain Res. 15:211–217.

    Article  Google Scholar 

  • Brenneman, D.E., d’Autremont, S.W., and Neale, E.A., (1985a) Non-neuronal cells mediate VIP stimulation of neuronal survival during development. Neurosci. Soc. Abstr. 11:1148.

    Google Scholar 

  • Brenneman, D.E., Eiden, L.E., and Siegel, R.E. (1985b) Neurotrophic action of VIP on spinal cord cultures. Peptides 6:35–39.

    Article  PubMed  CAS  Google Scholar 

  • Brenneman, D.E., Fitzgerald, S., and Litzinger, M.J. (1985c) Neuronal survival during electrical blockade is increased by 8-bromo cyclic adenosine 3’, 5’ monophosphate, J. Pharmacol. Exp. Ther. 233:402–408.

    PubMed  CAS  Google Scholar 

  • Campenot, R.B. (1981) Regeneration of neurites in long-term cultures of sympathetic neurons deprived of nerve growth factor. Science 214:579–581.

    Article  PubMed  CAS  Google Scholar 

  • Changeux, J.-P., Courrege, P., and Danchin, A. (1973) A theory of the epigenesis of neuronal networks by selective stabilization of synapses. Proc. Natl. Acad. Sci. USA 70:2974–2978.

    Article  PubMed  CAS  Google Scholar 

  • Creazzo, T.L., and Sohal, G.S. (1979) Effects of chronic injections of a-bungarotoxin on embryonic cell death. Exp. Neurol. 66:135–145.

    Article  PubMed  CAS  Google Scholar 

  • Dahl, D., and Bignami, A. (1977) Preparation of antisera to neurofilament protein from chicken brain and human sciatic nerve. J. Comp. Neurol. 176:645–658.

    Article  PubMed  CAS  Google Scholar 

  • Delfs, J.R., and Dichter, M.A. (1983) Effects of somatostatin on mammalian cortical neurons in culture: physiological actions and unusual dose response characteristics. J. Neurosci. 3:1176–1188.

    PubMed  CAS  Google Scholar 

  • Dodd, J., Dingledine, R., and Kelly, J.S. (1981) The excitatory action of acetylcholine on hippocampal neurons of the guinea pig and rat maintained in vitro. Brain Res. 207:109–127.

    Article  PubMed  CAS  Google Scholar 

  • Eagleson, K.L., Raju, T.R., and Bennett, M.R., (1985) Motoneurone survival is induced by immature astrocytes from developing avian spinal cord. Dev. Brain Res. 17:95–104.

    Article  Google Scholar 

  • Eccleston, P.A., and Silberberg, D.H. (1984) The differentiation of oligodendrocytes in a serum-free hormone-supplemented medium. Dev. Brain Res. 16:1–9.

    Article  CAS  Google Scholar 

  • Eckenstein, F., and Baughman, R.W. (1984) Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide. Nature 309:153–155.

    Article  PubMed  CAS  Google Scholar 

  • Eiden, L.E., Nilaver, G., and Palkovits, M. (1982) Distribution of vasoactive intestinal polypeptide (VIP) in the rat brain stem nuclei. Brain Res. 231:472–477.

    Article  PubMed  CAS  Google Scholar 

  • Giulian, D., Tomozawa, Y., Hindman, H., and Allen, R.L. (1985) Peptides from regenerating central nervous system promote specific populations of macroglia. Proc. Natl. Acad. Sci. USA 82:4287–4290.

    Article  PubMed  CAS  Google Scholar 

  • Go, V.L.W., and Yaksh, T.L. (1980) Vasoactive intestinal peptide (VIP) and cholecystokinin CCK-8 in cat spinal cord and dorsal root ganglion: release from cord by peripheral nerve stimulation. Regul. Pept. 1:43.

    Article  Google Scholar 

  • Hamburger, V. (1975) Cell death in the development of the lateral motor column of chick embryo. J. Comp. Neurol. 160:535–546.

    Article  PubMed  CAS  Google Scholar 

  • Hendry, I. A., and Hill, C.E. (1980) Retrograde axonal transport of target tissue-derived macro-molecules. Nature 287:647–649.

    Article  PubMed  CAS  Google Scholar 

  • Hirayama, M., Silberberg, D.H., Lisak, R.P., and Pleasure, D.E. (1983) Long-term culture of oligodendrocytes isolated from rat corpus callosum by Percoll density gradient: lysis by polyclonal antigalactocerebroside serum. J. Neuropathol. Exp. Neurol. 42:16–28.

    Article  PubMed  CAS  Google Scholar 

  • Hsu, S.-M., Raine, L., and Fanger, H. (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase technique: a comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29:577–580.

    Article  PubMed  CAS  Google Scholar 

  • James, R., and Bradshaw, R.A. (1984) Polypeptide growth factors. Annu. Rev. Biochem. 53:259–292.

    Article  PubMed  CAS  Google Scholar 

  • Keltz, T.N., Straus, E., and Yalow, R.S. (1980) Degradation of vasoactive intestinal polypeptide by tissue homogenates. Biochem. Biophys. Res. Commum. 92:669–674.

    Article  CAS  Google Scholar 

  • Kessler, J.A., Adler, J.E., and Black, I.B. (1983) Substance P and somatostatin regulate sympathetic noradrenergic function. Science 221:1059–1061.

    Article  PubMed  CAS  Google Scholar 

  • Koh, S.-W.M., Kyritsis, A., and Chader, G.J. (1984) Interaction of neuropeptides and cultured glial (Muller) cells of the chick retina: elevation of intracellular cyclic AMP by vasoactive intestinal peptide and glucagon. J. Neurochem. 43:199–203.

    Article  PubMed  CAS  Google Scholar 

  • Landmesser, L., and Pilar, G. (1974) Synaptic transmission and cell death during normal ganglionic development. J. Physiol. 241:737–749.

    PubMed  CAS  Google Scholar 

  • Loren, I., Emson, P.C., Fahrenkrug, J., Bjorklund, A., Alumets, J., Hakanson, R., and Sundler, F. (1979) Distribution of vasoactive intestinal polypeptide in the rat and mouse brain. Neuroscience 4:1953–1976.

    Article  PubMed  CAS  Google Scholar 

  • Luine, V.N., Rostene, W., Rhodes, J., and Mwen, B.S. (1984) Activation of choline acetyl-transferase by vasoactive intestinal peptide. J. Neurochem. 42:1131–1134.

    Article  PubMed  CAS  Google Scholar 

  • Lundberg, J.M., Anggard, A., Emson, P., Fahrenkrug, J., and Hokfelt, T. (1981) Vasoactive intestinal polypeptide and cholinergic mechanisms in cat nasal mucosa: studies on choline acetyltransferase and release of vasoactive intestinal peptide. Proc. Natl. Acad. Sci. USA 78:5255–5259.

    Article  PubMed  CAS  Google Scholar 

  • Magistretti, P.J., Manthorpe, M., Bloom, F.E., and Varon, S. (1983) Functional receptors for vasoactive intestinal polypeptide in cultured astroglia from neonatal rat brain. Regul. Pept. 6:71–80.

    Article  PubMed  CAS  Google Scholar 

  • McCarthy, K.D., and De Vellis, J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85:890–902.

    Article  PubMed  CAS  Google Scholar 

  • Marthy, K., and Partlow, L. (1976) Separation of pure neuronal and non-neuronal cultures from embryonic chick sympathetic ganglia: a new method based on both differential cell adhesion and the formation of homotypic neuronal aggregates. Brain Res. 114:391–414.

    Article  PubMed  CAS  Google Scholar 

  • Manaman, J.L., Smith, R.G., and Appel, S.H. (1985) Low-molecular-weight peptide stimulates cholinergic development in ventral spinal cord cultures. Dev. Biol. 112:248–252.

    Article  Google Scholar 

  • Muller, H.W., Beckh, S., and Seifert, W. (1984) Neurotrophic factor for central neurons. Proc. Natl. Acad. Sci. USA 81:1248–1252.

    Article  PubMed  CAS  Google Scholar 

  • Neale, E.A., Matthew, E., Zimmerman, E.A., and Nelson, P.G. (1982) Substance P-like immunoreactivity in neurons in dissociated cell cultures of mammalian spinal cord and dorsal root ganglia. J. Neurosci. 2:169–177.

    PubMed  CAS  Google Scholar 

  • Neale, E.A., Oertel, W.H., Bowers, L.M., and Weise, V.K. (1983) Glutamate decarboxylase immunoreactivity and γ-(3H) aminobutyric acid accumulation within the same neurons in dissociated cell cultures of cerebral cortex. J. Neurosci. 3:376–382.

    PubMed  CAS  Google Scholar 

  • Neale, E.A, Bruce, G., Matthew, E., d’Autremont, S.W., Strauss, W., Hersh, L.B., and Nelson, P.G. (1985) Cholinergic neurons demonstrated by immunohistochemistry in mouse spinal cord cultures. Neurosci Soc. Abstr. 11:862.

    Google Scholar 

  • Pickel, V.M., Reis, D.J., Marangos, P.J., and Zomzely-Neurath, C. (1975) Immunocyto-chemical localization of nervous system-specific protein (NSP-R) in rat brain. Brain Res. 105:184–187.

    Article  Google Scholar 

  • Pittman, R.H., and Oppenheim, R.W. (1978) Neuromuscular blockade increases motoneurone survival during normal cell death in the chick embryo. Nature 271:364–366.

    Article  PubMed  CAS  Google Scholar 

  • Pun, R.Y.K., Marshall, K.C., Hendelman, W.J., Guthrie, P.B., and Nelson, P.G. (1985) Noradrenergic responses of spinal neurons in locus coeruleus-spinal cord co-cultures. J. Neurosci. 5:181–191.

    PubMed  CAS  Google Scholar 

  • Raff, M.C., Mirsky, R., Fields, K.L., Lisak, R.P., Dorfman, S.H., Silberberg, D.H., Gregson, N.A., Leibowitz, S., and Kennedy, M. (1978) Galactocerebroside is a specific cell-surface antigenic marker for oligodendrocytes in culture. Nature 274:813–816.

    PubMed  CAS  Google Scholar 

  • Raju, T.R., Bignami, A., and Dahl, D. (1981) In vivo and in vitro differentiation of neurones and astrocytes in the rat embryo: immunofluorescence study with neurofilament and glial filament antisera. Dev. Biol. 85:344–357.

    Article  PubMed  CAS  Google Scholar 

  • Ransom, B.R., Neale, E., Henkart, M., Bullock, P.N., and Nelson, P.G. (1977) Mouse spinal cord in cell culture. I. Morphology and intrinsic neuronal electrophysiological properties. J. Neurophysiol. 40:1132–1150.

    PubMed  CAS  Google Scholar 

  • Rostene, W.H., Fischette, C.T., and McEwen, B.S. (1983) Modulation by vasoactive intestinal peptide (VIP) of serotonin1 receptors in membranes from rat hippocampus. J. Neurosci. 3:2414–2419.

    PubMed  CAS  Google Scholar 

  • Rougon, G., Noble, M., and Mudge, A.W. (1983) Neuropeptides modulate the ß-adrenergic response of purified astrocytes in vitro. Nature 305:715–717.

    Article  PubMed  CAS  Google Scholar 

  • Rudge, J.S., Manthorpe, M., and Varon, S. (1985) The output of neuronotrophic and neurite-promoting agents from rat brain astroglial cells: a microculture method for screening potential regulatory molecules. Dev. Brain Res. 19:161–172.

    Article  CAS  Google Scholar 

  • Segal, M. (1983) Rat hippocampal neurons in culture: responses to electrical and chemical stimuli. J. Neurophysiol. 50:1249–1264.

    PubMed  CAS  Google Scholar 

  • Turner, J.T., Ray-Prenger, C.J., and Bylund, D.B. (1985) VIP(10–28) is an antagonist of VIP adenylate cyclase stimulation of HT29 cells. Neurosci. Soc. Abstr. 11:414.

    Google Scholar 

  • Varon, S., Skaper, S.D., Barbin G., Selak, I., and Manthorpe, M. (1984) Low molecular weight agents support survival of cultured neurons from the central nervous system. J. Neurosci. 4:654–658.

    PubMed  CAS  Google Scholar 

  • Vernadakis, A., and Arnold, E.B. (1980) Age-related changes in neuronal and glial enzyme activites. In: Fedoroff, S., and Hertz, L. (eds.) Advances in cellular neurobiology. New York: Academic Press, pp. 229–283.

    Google Scholar 

  • Watling, K.J., and Dowling, J.E. (1983) Effects of vasoactive intestinal peptide and other peptides on cyclic AMP accumulation in intact pieces and isolated horizontal cells of the teleost retina. J. Neurochem. 41:1205–1213.

    Article  PubMed  CAS  Google Scholar 

  • Westbrook, G.L., and Brenneman, D.E. (1984) The development of spontaneous electrical activity in spinal cord cultures In: Caciagli, E., Giacobini, E., and Paoletti, R. (eds.) Developmental neurosciences: physiological, pharmacological and clinical aspects. Amsterdam: Elsevier, pp. 11–17.

    Google Scholar 

Download references

Authors
  1. Douglas E. Brenneman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Phillip G. Nelson
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Departments of Psychiatry and Pharmacology, University of Colorado School of Medicine, 4200 East 9th Avenue, 80262, Denver, CO, USA

    Antonia Vernadakis

  2. Neurobiologie du Développement, INSERM U249, F-34060, Montpellier Cedex, France

    Alain Privat

  3. Department of Anatomy, University of North Carolina School of Medicine, 27514, Chapel Hill, NC, USA

    Jean M. Lauder

  4. Department of Physiology-Anatomy, University of California, 94720, Berkeley, CA, USA

    Paola S. Timiras

  5. Department of Pharmacology, Southern Illinois University School of Medicine, PO Box 3926, 62708, Springfield, IL, USA

    Ezio Giacobini

Rights and permissions

Reprints and permissions

Copyright information

© 1987 Martinus Nijhoff Publishing, Boston

About this chapter

Cite this chapter

Brenneman, D.E., Nelson, P.G. (1987). Peptide Modulation of Neuronal Differentiation in Culture. In: Vernadakis, A., Privat, A., Lauder, J.M., Timiras, P.S., Giacobini, E. (eds) Model Systems of Development and Aging of the Nervous System. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2037-1_18

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-2037-1_18

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-9212-8

  • Online ISBN: 978-1-4613-2037-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation