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Peptide-containing neurons in explant cultures of guinea-pig myenteric plexus during development in vitro: Gross morphology and growth patterns

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Summary

The gross morphology and growth patterns of substance P, enkephalin-, somatostatin and vasoactive intestinal peptide-immunoreactive neurons have been studied in explant cultures of the myenteric plexus taken from beneath the newborn guinea-pig taenia coli, grown for up to 4 weeks in vitro. Substance P and enkephalin-immuno-reactive neurons were more abundant than somatostatin and vasoactive intestinal peptide-immunoreactive neurons. The peptide-containing neuronal cell bodies were clearly visible in culture and exhibited characteristic gross morphologies similar to those described in situ, although some overlap of shape between populations containing different peptides was seen. All four types of peptide-containing fibres were found in the outgrowth and central areas of the cultures. In the case of substance P and somatostatin, the density and pattern of labelling in the central, neuronal area of the cultures resembled that previously seen in the myenteric plexus of the newborn guinea-pig caecum in situ, while the density of the enkephalin-immunoreactive fibres was greater, and that of the vasoactive intestinal peptide-immunoreactive fibres less than that seen in situ. These observations suggest that subpopulations of myenteric neurons containing different peptides may be differentially affected by the culture environment. Possible contributory factors are discussed.

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References

  • Baluk PLJ (1982) The enteric nervous system: morphology and development in vivo and in vitro. PhD Thesis, University of London

  • Black IB (1978) Regulation of autonomic development. Ann Rev Neurosci 1:183–214

    Google Scholar 

  • Black IB (1982) Stages of neurotransmitter development in autonomic neurons. Science 215:1198–1204

    Google Scholar 

  • Costa M, Furness JB (1983) The origins, pathways and terminations of neurons with VIP-like immunoreactivity in the guineapig small intestine. Neuroscience 8:665–676

    Google Scholar 

  • Costa M, Buffa R, Furness JB, Solcia EL (1980a) Immunohistochemical localization of polypeptides in peripheral autonomic nerves using whole-mount preparations. Histochemistry 65:157–165

    Google Scholar 

  • Costa M, Furness JB, Buffa R, Said SI (1980b) Distribution of enteric nerve cell bodies and axons showing immunoreactivity for vasoactive intestinal polypeptide in the guinea-pig intestine. Neuroscience 5:587–596

    Google Scholar 

  • Costa M, Furness JB, Llewellyn-Smith IJ, Davies B, Oliver J (1980c) An immunohistochemical study of the projections of somatostatin containing neurons in the guinea-pig intestine. Neuroscience 5:841–852

    Google Scholar 

  • Costa M, Furness JB, Llewellyn-Smith IJ, Cuello C (1981) Projections of substance P containing neurons within the guinea-pig small intestine. Neuroscience 6:411–424

    Google Scholar 

  • Costa M, Furness JB, Cuello AC (1985) Separate populations of opioid containing neurons in the guinea-pig intestine. Neuropeptides 5:445–448

    Google Scholar 

  • Costa M, Furness JB, Gibbins IL (1986) Chemical coding of enteric neurons. In: Hökfelt T, Fuxe K, Pernow B (eds) Progress in brain research. Vol 68. Elsevier, Amsterdam, pp 217–239

    Google Scholar 

  • Costa M, Furness JB, Llewellyn-Smith IJ (1987) Histochemistry of the enteric nervous system. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Second Edition. Raven Press, New York, pp 1–40

    Google Scholar 

  • Cuello AC, Galfré G, Milstein C (1979) Detection of substance P in the central nervous system by a monoclonal antibody. Proc Natl Acad Sci USA 76:3532–3536

    Google Scholar 

  • Furness JB, Costa M (1982) Identification of gastrointestinal neurotransmitters. Handb Exp Pharmacol 59:383–460

    Google Scholar 

  • Furness JB, Costa M (1987) The enteric nervous system. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Furness JB, Costa M, Walsh JH (1981) Evidence for significance of the projection of VIP neurons from the myenteric plexus to the taenia coli in the guinea-pig. Gastroenterology 80:1557–1561

    Google Scholar 

  • Furness JB, Costa M, Miller RJ (1983) Distribution and projections of nerves with enkephalin-like immunoreactivity in the guinea-pig small intestine. Neuroscience 8:653–664

    Google Scholar 

  • Gabella G (1979) Innervation of the gastrointestinal tract. Int Rev Cytol 59:129–193

    Google Scholar 

  • Gabella G (1981) Structure of muscles and nerves in the gastrointestinal tract. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven Press, New York, pp 197–241

    Google Scholar 

  • Gershon MD, Rothman TP (1984) Experimental and genetic approaches to the study of the development of the enteric nervous system. Trends Neurosci 7:150–155

    Google Scholar 

  • Gershon MD, Payette RF, Rothman TP (1983) Development of the enteric nervous system. Fed Proc 42:1620–1625

    Google Scholar 

  • Jessen KR (1982) A new approach in research on gut neurons: applications for studies on neuropeptides and related substances. In: Bloom SR, Polak JM, Lindenlaub E (eds) Systemic role of regulatory peptides. Symposia Medica Hoechst 18. Schattauer, Stuttgart New York, pp 36–53

    Google Scholar 

  • Jessen KR, Polak JM, Van Noorden S, Bloom SR, Burnstock G (1980a) Peptide-containing neurons connect the two ganglionated plexuses of the enteric nervous system. Nature 283:391–393

    Google Scholar 

  • Jessen KR, Saffrey MJ, Van Noorden S, Bloom SR, Polak JM, Burnstock G (1980b) Immunohistochemical studies of the enteric nervous system in tissue culture and in situ: localization of vasoactive intestinal polypeptide (VIP), substance P and enkephalin immunoreactive nerves in the guinea-pig gut. Neuroscience 5:1717–1735

    Google Scholar 

  • Jessen KR, Saffrey MJ, Burnstock G (1983) The enteric nervous system in tissue culture. I. Cell types and their interactions in explants of the myenteric and submucous plexuses from guinea-pig, rabbit and rat. Brain Res 262:1–35

    Google Scholar 

  • Kessler JA, Black IB (1982) Regulation of substance P in adult rat sympathetic ganglia. Brain Res 234:182–187

    Google Scholar 

  • Kessler JA, Adler JE, Bell WO, Black IB (1983) Substance P and somatostatin metabolism in sympathetic and special sensory ganglia in vitro. Neuroscience 9:309–318

    Google Scholar 

  • Leander S, Håkanson R, Sundler F (1981) Nerves containing substance P, vasoactive intestinal polypeptide, enkephalin or somatostatin in the guinea-pig taenia coli: distribution, ultrastructure and possible functions. Cell Tissue Res 215:21–39

    Google Scholar 

  • Le Douarin N (1982) The Neural Crest. Cambridge University Press, London

    Google Scholar 

  • Mudge AW (1981a) Effect of chemical enviroment on levels of substance P and somatostatin in cultured sensory neurons. Nature 292:764–767

    Google Scholar 

  • Mudge AW (1981b) Effect of non-neuronal cells on peptide content of cultured sensory neurons. J Exp Biol 95:195–203

    Google Scholar 

  • Nishi R, Willard AL (1985) Neurons dissociated from rat myenteric plexus retain differentiated properties when grown in cell culture. I. Morphological properties and immunocytochemical localization of transmitter candidates. Neuroscience 16:187–199

    Google Scholar 

  • Saffrey MJ, Burnstock G (1988) Distribution of peptide-immunoreactive nerves in the foetal and newborn guinea-pig caecum. Cell Tisse Res (in press)

  • Schultzberg M, Hökfelt T, Nilsson T, Terenius L, Rehfeld JF, Brown M, Goldstein M, Said S (1980) Distribution of peptide and catecholamine-containing neurons in the gastrointestinal tract of the rat and guinea-pig: immunohistochemical studies with antisera to substance-P, vasoactive intestinal polypeptide, enkephalins, somatostatin, gastrin/cholecystokinin, neurotensin and dopamine beta-hydroxylase. Neuroscience 5:689–744

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Saffrey, M.J., Burnstock, G. Peptide-containing neurons in explant cultures of guinea-pig myenteric plexus during development in vitro: Gross morphology and growth patterns. Cell Tissue Res. 254, 167–176 (1988). https://doi.org/10.1007/BF00220030

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