Summary
Pancreatic polypeptide-like immunoreactivity (PPLI) has been localized in nerves of the guinea-pig stomach and intestine with the use of antibodies raised against avian, bovine and human pancreatic polypeptide (PP), the C-terminal hexapeptide of mammalian PP, and against the related peptide, NPY. Each of the antibodies revealed the same population of neurones. Reactive cell bodies were found in both myenteric (5% of all neurones) and submucous ganglia (26% of all neurones) of the small intestine, and varicose processes were observed in the myenteric plexus, circular muscle, mucosa and around arterioles. The nerves were unaffected by bilateral subdiaphragmatic truncal vagotomy, but the staining of the periarterial nerves disappeared after treatment of animals with reserpine or 6-hydroxydopamine and was also absent after mesenteric nerves had been cut and allowed to degenerate. Vascular nerves showing immunoreactivity for dopamine it-hydroxylase and PPLI had the same distribution. It is concluded that PPLI is located in periarterial noradrenergic nerves. However, other noradrenergic nerves in the intestine do not show PPLI, and PPLI also occurs in nerves that are not noradrenergic. Analysis of changes in the distribution of terminals after microsurgical lesions of pathways in the small intestine showed that processes of myenteric PP-nerve cells provide terminals in the underlying circular muscle and in myenteric ganglia up to about 2 mm more anal. Submucous PP-cell bodies provide terminals to the mucosa.
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Costa M, Furness JB (1971) Storage uptake and synthesis of catecholamines in the intrinsic adrenergic neurones in the proximal colon of the guinea-pig. Z Zellforsch 120:364–385
Costa M, Furness JB (1982) Neuronal peptides in the intestine. Brit Med Bull 38:247–252
Costa M, Furness JB (1983a) The origins, pathways and terminations of neurones with VIP-like immunoreactivity in the guinea-pig small intestine. Neuroscience 8:665–676
Costa M, Gabella G (1971) Adrenergic innervation of the alimentary canal. Z Zellforsch 122:357–377
Costa M, Buffa R, Furness JB, Solcia EL (1980) Immunohistochemical localization of polypeptides in peripheral autonomic nerves using whole mount preparations. Histochemistry 65:157–165
Costa M, Furness JB, Llewellyn-Smith IJ, Davies B, Oliver J (1980) An immunohistochemical study of the projections of somatostatin-containing neurones in the guinea-pig intestine. Neuroscience 5:841–852
Costa M, Furness JB, Llewellyn-Smith IJ, Cuello AC (1981) Projections of substance P neurones within the guinea-pig small intestine. Neuroscience 6:411–424
Costa M, Furness JB, Cuello AC, Verhofstad AAJ, Steinbusch HWJ, Elde RP (1982) Neurones with 5-hydroxytryptamine-like immunoreactivity in the enteric nervous system: Their visualization and reactions to drug treatment. Neuroscience 7:351–363
Costa M, Buffa R, Furness JB, Solcia EL (1980) Immunohistochemical localization of polypeptides in peripheral autonomic nerves using whole mount preparations. Histochemistry 65:157–165
Dogiel AS (1899) Über den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Säugetiere. Archiv für Anat und Entwickl 130–138
Furness JB (1971) The adrenergic innervation of the vessels supplying and draining the gastrointestinal tract. Z Zellforsch 113:67–82
Furness JB, Costa M (1974) The adrenergic innervation of the gastrointestinal tract. Ergeb Physiol 69:1–54
Furness JB, Costa M (1975) The use of glyoxylic acid for the fluorescence histochemical demonstration of peripheral stores of noradrenaline and 5-hydroxytryptamine in whole mounts. Histochemistry 41:335–352
Furness JB, Costa M (1982) Neurones with 5-hydroxytryptamine-like immunoreactivity in the enteric nervous system: Their projections in the guinea-pig small intestine. Neuroscience 7:341–349
Furness JB, Elliot JM, Murphy R, Costa M, Chalmers JP (1982) Baroreceptor reflexes in conscious guinea-pigs are unaffected by depletion of cardiovascular substance P nerves. Neurosci Lett 32:285–290
Furness JB, Costa M, Miller RJ (1983) Distribution and projections of nerves with enkephalinlike immunoreactivity in the guinea-pig small intestine. Neuroscience 8:653–664
Jacobowitz DM (1965) Histochemical studies of the autonomic innervation of the gut. J Pharmacol Exp Ther 149:358–364
Jacobowitz DM, Olschowka JA (1982) Bovine pancreatic polypeptide-like immunoreactivity in brain and peripheral nervous system: Coexistence with catecholaminergic nerves. Peptides 3:569–590
Jurio AV, Gabella G (1974) Noradrenaline in the guinea-pig alimentary canal: Regional distribution and sensitivity to denervation and reserpine. J Neurochem 22:851–858
Kimmel JR, Hayden LJ, Pollock HG (1975) Isolation and characterization of a new pancreatic polypeptide hormone. J Biol Chem 250:9369–9376
Kimmel JR, Pollock HG, Hazelwood RL (1968) Isolation and characterization of chicken insulin. Diabetologia 12:211–226
Lin TM (1980) Pancreatic polypeptide isolation, chemistry and biological function. In: Glass GBJ (ed) Gastrointestinal hormones. Raven Press, New York, pp 275–306
Lin TM, Chance RE (1974) Gastrointestinal actions of a new bovine pancreatic polypeptide (BPP) In: Chey WY, Brooks FP (eds) Endocrinology of the gut. CR Slack, New Jersey pp 143–145
Lorén I, Alumets J, Håkanson R, Sundler F (1979) Immunoreactive pancreatic polypeptide (PP) occurs in the central and peripheral nervous system: Preliminary immunocytochemical observations. Cell Tissue Res 200:179–186
Lundberg JM, Hökfelt T, Änggard A, Kimmel J, Goldstein M, Markey K (1980) Coexistence of an avian pancreatic polypeptide (APP) immunoreactive substance and catecholamines in some peripheral and central neurones. Acta Physiol Scand 110:107–109
Norberg K-A (1964) Adrenergic innervation of the intestinal wall studied by fluorescence microscopy. Int J Neuropharmacol 3:379–382
Schultzberg M, Hökfelt T, Nilsson G, Terenius L, Rehfeld JM, Brown M, Elde R, Goldstein M, Said SI (1980) Distribution of peptide and catecholamine neurones in the gastrointestinal tract of rat and guinea-pig: Immunohistochemical studies with antisera to substance P, VIP, enkepahalins, somatostatin, gastrin, neurotensin and dopamine β-hydroxylase. Neuroscience 5:689–744
Sundler F, Moghimzadeh E, Häkanson R, Ekelund M, Emson PC (1983) Nerve fibers in the gut and pancreas of the rat displaying neuropeptide Y immunoreactivity. Cell Tissue Res (in press)
Tatemoto K (1982) New peptides, their structures and functions. In: Bloom SR, Polak JM, Lindenlaub E (eds) Systemic role of regulatory peptides. FK Schattauer, Stuttgart New York, pp 507–531
Tatemoto K, Mutt V (1980) Isolation of two novel candidate hormones using a chemical method for finding naturally occurring polypeptides. Nature 285:417–418
Tatemoto K, Carlquist M, Mutt V (1982) Neuropeptide Y — a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296:659–660
Tramu G, Pillez A, Leonardelli J (1978) A efficient method of antibody elution for successive or simultaneous location of two antigens by immunocytochemistry. J Histochem Cytochem 26:322–324
Vaillant C, Taylor IL (1981) Demonstration of carboxyl-terminal PP-like peptides in endocrine cells and nerves. Peptides 2:31–35
Wilson AJ, Furness JB, Costa M (1981) The fine structure of the submucous plexus of the guinea-pig ileum. I. The ganglia, neurones, Schwann cells and neuropil. J Neurocytol 10:759–784
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Furness, J.B., Costa, M., Emson, P.C. et al. 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 (1983). https://doi.org/10.1007/BF00217403
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DOI: https://doi.org/10.1007/BF00217403