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Distinct distribution of CGRP-, enkephalin-, galanin-, neuromedin U-, neuropeptide Y-, somatostatin-, substance P-, VIP- and serotonin-containing neurons in the two submucosal ganglionic neural networks of the porcine small intestine

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Summary

In addition to differences between the two submucosal ganglionic neural networks, i.e., the plexus submucosus externus (Schabadasch) and the plexus submucosus internus (Meissner), with respect to the occurrence and distribution of serotonin as neurotransmitter, immunocytochemistry also revealed a distinct distribution for various neuropeptides in these two plexuses. Immunoreactivity for galanin, vasoactive intestinal polypeptide, calcitonin gene-related peptide, substance P, neuromedin U, enkephalin, somatostatin and neuropeptide Y was found in varicose and non-varicose nerve fibres of both submucosal ganglionic plexuses, albeit with a distinct distributional pattern. The difference in neurotransmitter and/or neuromodulator content between both neural networks became even more obvious when attention was focussed on the immunoreactivity of the nerve cell bodies for these substances. Indeed, neuropeptide Y, enkephalin-and somatostatin-immunoreactive neuronal perikarya as well as serotonergic neuronal cell bodies appear solely in the plexus submucosus externus. Neuromedin U-immunoreactive perikarya, mostly coexisting with substance P, are observed in large numbers in the plexus submucosus internus, whilst they are rare in the plexus submucosus externus. Double-labelling immunostaining for substance P with CGRP and galanin revealed a different coexistence pattern for the two submucosal ganglionic plexuses. The differing chemical content of the neuronal populations supports the hypothesis that the existence of the two submucosal ganglionic plexuses, present in most large mammals including man, not only reflects a morphological difference but also points to differentiated functions.

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References

  • Ballesta J, Carlei F, Bishop AE, Steel JH, Gibson SJ, Fahey M, Hennessey R, Domin J, Bloom SR, Polak JM (1988) Occurrence and developmental pattern of neuromedin U-immunoreactive nerves in the gastrointestinal tract and brain of the rat. Neuroscience 25:797–816

    Google Scholar 

  • Billroth T (1858) Einige Beobachtungen über das ausgedehnte Vorkommen von Nervenanastomosen im Tractus intestinalis. Arch Anat Physiol 2:148–158

    Google Scholar 

  • Bishop AE, Polak JM, Bauer FE, Christofides ND, Carlei F, Bloom SR (1986) Occurrence and distribution of a newly discovered peptide, galanin, in the mammalian enteric nervous system. Gut 27:849–857

    Google Scholar 

  • Costa M, Cuello AC, Furness JB, Franco R (1980a) Distribution of enteric neurons showing immunoreactivity for substance P in the guinea-pig ileum. Neuroscience 5:323–331

    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 

  • Daniel EE, Costa M, Furness JB, Keast JR (1985) Peptide neurons in the canine small intestine. J Comp Neurol 237:227–238

    Google Scholar 

  • Domin J, Ghatei MA, Chohan P, Bloom SR (1987) Neuromedin U. A study of its distribution in the rat. Peptides 8:779–784

    Google Scholar 

  • Domoto T, Gonda T, Oki M, Yanaihara N (1984) Coexistence of substance P- and methionine5-enkephalin-like immunoreactivity in nerve cells of the myenteric ganglia in the cat ileum. Neurosci Lett 47:9–13

    Google Scholar 

  • Ekblad E, Rökaeus Å, Håkanson R, Sundler F (1985) Galanin nerve fibres in the rat gut: distribution, origin and projections. Neuroscience 16:355–363

    Google Scholar 

  • Elde R, Hökfelt T, Johansson O, Terenius L (1976) Immunohistochemical studies using antibodies to leucine-enkephalin: initial observations on the nervous system of the rat. Neuroscience 1:349–351

    Google Scholar 

  • Furness JB, Costa M (1982) Neurons with 5-hydroxytryptamine-like immunoreactivity in the enteric nervous system: their projections in the guinea-pig small intestine. Neuroscience 7:341–349

    Google Scholar 

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

    Google Scholar 

  • Furness JB, Costa M, Emson PC, Håkanson R, Moghimzadeh E, Sundler F, Taylor IL, Chance RE (1983a) Distribution, pathways and reactions to drug treatment of nerves with neuropeptide Y- and pancreatic polypeptide-like immunoreactivity in the guinea-pig digestive tract. Cell Tissue Res 234:71–92

    Google Scholar 

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

    Google Scholar 

  • Furness JB, Costa B, Rökaeus Å, McDonald TJ, Brooks B (1987) Galanin-immunoreactive neurons in the guinea-pig small intestine: their projections and relationships to other enteric neurons. Cell Tissue Res 250:607–615

    Google Scholar 

  • Griffith SG, Burnstock G (1983) Serotoninergic neurons in human fetal intestine: an immunohistochemical study. Gastroenterology 85:929–937

    Google Scholar 

  • Gunn M (1968) Histological and histochemical observations on the myenteric and submucous plexuses of mammals. J Anat 102:223–239

    Google Scholar 

  • Hirst GDS, McKirdy HC (1975) Synaptic potentials from neurons of the submucous plexus of guinea-pig small intestine. J Physiol 249:369–385

    Google Scholar 

  • Keast JR, Furness JB, Costa M (1985) Distribution of certain peptide-containing nerve fibres and endocrine cells in the gastrointestinal mucosa in five mammalian species. J Comp Neurol 236:403–422

    Google Scholar 

  • Kobayashi S, Suzuki M, Uchida T, Yanaihara N (1984) Enkephalin neurons in the guinea pig duodenum: a light and electron microscopic immunocytochemical study using an antiserum to methionine-enkephalin-Arg6-Gly7-Leu8. Biomed Res 5:489–506

    Google Scholar 

  • Kobayashi S, Suzuki M, Yanaihara N (1985) Enkephalin neurons in the guinea pig proximal colon: an immunocytochemical study using an antiserum to methionine-enkephalin-Arg6-Gly7-Leu8. Arch Histol Jpn 48:27–44

    Google Scholar 

  • Li P-L (1940) The intramural nervous system of the small intestine with special reference to the innervation of the inner subdivision of its circular muscle. J Anat 74:348–359

    Google Scholar 

  • Linnoila RI, DiAugustine RP, Miller RJ, Chang KJ, Quatrecasas P (1978) An immunohistochemical and radioimmunological study of the distribution of (met5)- and (leu5)-enkephalin in the gastrointestinal tract. Neuroscience 3:1187–1196

    Google Scholar 

  • Llewellyn-Smith IJ, Costa M, Furness JB (1985) Light and electron microscopic immunocytochemistry of the same nerves from whole mount preparations. J Histochem Cytochem 33:857–866

    Google Scholar 

  • Mannl A, Pospischil A, Dahme E (1986) Der Plexus submucosus (Meissner und Schabadasch) im Darm des Schweines. I. Licht-und elektronenmikroskopische Untersuchung der Normalstruktur. J Vet Med [A] 33:647–659

    Google Scholar 

  • Meissner G (1857) Ueber die Nerven der Darmwand. Z Ration Med N F 8:364–366

    Google Scholar 

  • Melander T, Hökfelt T, Rökaeus Å, Fahrenkrug J, Tatemoto K, Mutt V (1985) Distribution of galanin-like immunoreactivity in the gastro-intestinal tract of several mammalian species. Cell Tissue Res 239:253–270

    Google Scholar 

  • Ohkawa H, Prosser CL (1972) Electrical activity in myenteric and submucous plexuses of cat intestine. Am J Physiol 222:1412–1419

    Google Scholar 

  • Ohkubo K (1936) Studies on the intrinsic nervous system of the digestive tract. I. The submucous plexus of guinea-pig. Jpn J Med Sci Anat 6:1–20

    Google Scholar 

  • Polak JM, Sullivan SN, Bloom SR, Facer P, Pearse AGE (1977) Enkephalin-like immunoreactivity in the human gastrointestinal tract. Lancet 1:972–974

    Google Scholar 

  • Remak R (1858) Ueber peripherische Ganglien an den Nerven des Nahrungsrohrs. Arch Anat Physiol 2:189–192

    Google Scholar 

  • Rintoul JR (1960) The comparative morphology of the enteric nerve plexuses. MD thesis, University of St. Andrews, Scotland

  • Schabadasch A (1930) Intramurale Nervengeflechte des Darmrohrs. Z Zellforsch 10:320–385

    Google Scholar 

  • Scheuermann DW, Stach W (1984) Fluorescence microscopic study of the architecture and structure of an adrenergic network in the plexus myentericus (Auerbach), plexus submucosus externus (Schabadasch) and plexus submucosus internus (Meissner) of the porcine small intestine. Acta Anat (Basel) 119:49–59

    Google Scholar 

  • Scheuermann DW, Stach W, De Groodt-Lasseel MHA, Timmermans J-P (1987a) Calcitonin gene-related peptide in morphologically well-defined type II neurons of the enteric nervous system in the porcine small intestine. Acta Anat (Basel) 129:325–328

    Google Scholar 

  • Scheuermann DW, Stach W, Timmermans J-P (1987b) Topography, architecture and structure of the plexus submucosus internus (Meissner) of the porcine small intestine in scanning electron microscopy. Acta Anat (Basel) 129:96–104

    Google Scholar 

  • Scheuermann DW, Stach W, Timmermans J-P (1987c) Topography, architecture and structure of the plexus submucosus externus (Schabadasch) of the porcine small intestine in scanning electron microscopy. Acta Anat (Basel) 129:105–115

    Google Scholar 

  • Scheuermann DW, Stach W, Timmermans J-P (1988) Morphology and immunocytochemistry of the enteric nervous system in the porcine small intestine. Part II. Acta Gastroenterol Belg 51: A3

  • Scheuermann DW, Stach W, Timmermans J-P (1989a) Three-dimensional visualization of the ganglionated enteric nerve plexuses in the small intestine of the pig. In: Motta PM (ed) Cells and tissues: a three-dimensional approach by modern techniques in microscopy. Alan R. Liss, New York, pp 343–347

    Google Scholar 

  • Scheuermann DW, Stach W, Timmermans J-P, Adriaensen D, De Groodt-Lasseel MHA (1989b) Neuron-specific enolase and S-100 protein immunohistochemistry for defining the structure and topographical relationship of the different enteric nerve plexuses in the small intestine of the pig. Cell Tissue Res 256:65–75

    Google Scholar 

  • Scheuermann DW, Stach W, Timmermans J-P (1989c) Serotonin-immunoreactivity in the wall of the porcine small intestine. Verh Anat Ges 83 (in press)

  • Schofield GC (1968) The enteric plexus of mammals. Int Rev Gen Exp Zool 3:53–116

    Google Scholar 

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

    Google Scholar 

  • Sokolowa ML (1931) Zur Lehre von der Cytoarchitektonik des peripherischen autonomen Nervensystems. II. Die Architektur der intramuralen Ganglien des Verdauungstrakts des Rindes. Z Mikrosk Anat Forsch 23:552–570

    Google Scholar 

  • Stach W (1969) Neurohistologische Untersuchungen an den Nervengeflechten der Dickdarmwand. Ein Beitrag zur Innervation des Magen-Darmkanals. MD thesis, Wilhelm-Pieck University, Rostock, German Democratic Republic

  • Stach W (1977a) Neuronenstruktur und-architektur im Plexus submucosus externus (Schabadasch) des Duodenums. Verh Anat Ges 71:867–871

    Google Scholar 

  • Stach W (1977b) Der Plexus submucosus externus (Schabadasch) in Dünndarm des Schweins. I. Form, Struktur und Verbindungen der Ganglien und Nervenzellen. Z Mikrosk Anat Forsch 91:737–755

    Google Scholar 

  • Stach W (1978) Die Vaskularization des Plexus submucosus externus (Schabadasch) und des Plexus submucosus internus (Meissner) in Dünndarm von Schwein und Katze. Acta Anat (Basel) 101:170–178

    Google Scholar 

  • Stach W (1989) A revised morphological classification of neurons in the enteric nervous system. In: Singer MV, Goebell H (ed) Nerves and the gastrointestinal tract. MTP Press Ltd, Dordrecht, pp 29–45

    Google Scholar 

  • Stach W, Scheuermann DW, Timmermans J-P (1987) Licht- und Rasterelektronenmikroskopie der submukösen Nervengeflechte des Darmwandnervensystems. Verh Anat Ges 81:729–730

    Google Scholar 

  • Stach W, Scheuermann DW, Timmermans J-P (1988) Substanz P in Neuronen und Axonen des Darmwandnervensystems im Schweinedünndarm. Verh Anat Ges 82 (in press)

  • Stöhr P Jr (1952) Zusammenfassende Ergebnisse über die mikroskopische Innervation des Magen-Darmkanals. Ergeb Anat Entwickl 34:250–401

    Google Scholar 

  • Sundler F, Moghimzadeh E, Håkanson R, Ekelund M, Emson P (1983) Nerve fibers in the gut and pancreas of the rat displaying neuropeptide-Y immunoreactivity. Intrinsic and extrinsic origin. Cell Tissue Res 230:487–493

    Google Scholar 

  • Temesrekasi D (1955) Die Synaptologie der Dünndarmgeflechte. Acta Morphol Hung 5:53–69

    Google Scholar 

  • Tramu G, Pillez A, Leonardelli J (1978) An efficient method of antibody elution for the successive or simultaneous localization of two antigens by immunocytochemistry. J Histochem Cytochem 26:322–324

    Google Scholar 

  • Wilson AJ (1981) Ultrastructural and cytochemical studies on the submucous plexus of the guinea-pig small intestine. PhD thesis, Flinders University, Adelaide, Australia

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Authors and Affiliations

  1. Institute of Histology and Microscopic Anatomy, University of Antwerp, Antwerp, Belgium

    Jean-Pierre Timmermans, Dietrich W. Scheuermann, Dirk Adriaensen & Marie H. A. De Groodt-Lasseel

  2. Institute of Anatomy, Wilhelm Pieck University, Rostock, German Democratic Republic

    Werner Stach

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  1. Jean-Pierre Timmermans
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  2. Dietrich W. Scheuermann
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  3. Werner Stach
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  4. Dirk Adriaensen
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  5. Marie H. A. De Groodt-Lasseel
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Timmermans, JP., Scheuermann, D.W., Stach, W. et al. Distinct distribution of CGRP-, enkephalin-, galanin-, neuromedin U-, neuropeptide Y-, somatostatin-, substance P-, VIP- and serotonin-containing neurons in the two submucosal ganglionic neural networks of the porcine small intestine. Cell Tissue Res 260, 367–379 (1990). https://doi.org/10.1007/BF00318639

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