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Distribution and origin of calcitonin gene-related peptide in the rat stomach and duodenum: An immunocytochemical analysis

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Summary

We studied the three-dimensional distribution of structures with calcitonin gene-related peptide-like immunoreactivity (CGRPI) in the rat stomach and duodenum, including the origins of these structures, using indirect immunofluorescence in both muscle strips and frozen sections. There was a very dense meshwork of CGRPI fibers in the circular and longitudinal muscle layers, and also in the myenteric and submucous plexuses of the stomach and duodenum. No CGRPI neurons were seen in the stomach, even in rats treated with colchicine; in the duodenum, there was a group of CGRPI cells in the myenteric and submucous ganglia. No regional differences were seen in the stomach and duodenum.

We found by experimental manipulations that CGRPI fibers in the stomach were exclusively extrinsic in origin; some of such fibers in the duodenum were intrinsic in origin, though most were supplied by CGRPI cells outside the duodenum.

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References

  • Amara SG, Jonas V, Rosenfeld MG, Ong ES, Evans RM (1982) Alternative RNA processing in calcitonin gene expression generate mRNAs encoding different polypeptide products. Nature 298: 240–244

    PubMed  Google Scholar 

  • Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre I (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature 313: 54–56

    PubMed  Google Scholar 

  • Coons AH (1958) Fluorescent antibody method. In: Danielli JF (ed) General cytochemical methods. Academic Press, New York, pp 1–90

    Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Costa M, Furness JB, Llewellyn-Smith IJ, Cuello AC (1981) Projection of substance P neurons within the guinea-pig small intestine. Neuroscience 6: 411–428

    PubMed  Google Scholar 

  • Dahlström A (1968) Effects of colchicine on transport of amine storage granules in sympathetic nerve of the rat. Eur J Pharmacol 5: 111–112

    PubMed  Google Scholar 

  • Fisher JA, Kikkawa DO, Rivier JE, Amara SG, Evans RM, Rosenfeld M, Vale WW, Brown MR (1983) Stimulation of noradrenergic sympathetic out-flow by calcitonin gene-related peptide. Nature 305: 534–536

    PubMed  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

    PubMed  Google Scholar 

  • Gibson SJ, Polak JM, Bloom SR, Sabate IM, Mulderry PM, Ghatei MA, McGregor GP, Morrison JFB, Kelley JS, Evans RM, Rosenfeld MG (1984) Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J Neurosci 4: 3101–3111

    PubMed  Google Scholar 

  • Inagaki S, Kito S, Kubota Y, Girgis S, Hillyard CJ, MacIntyre I (1986) Autoradiographic localization of calcitonin gene-related peptide bindings sites in human and rat brains. Brain Res (in press)

  • Kawai Y, Takami K, Shiosaka S, Emson PC, Hillyard CJ, Girgis S, MacIntyre I, Tohyama M (1985) Topographic localization of calcitonin gene-related peptide in the rat brain: an immunohistochemical analysis. Neuroscience 15: 747–763

    PubMed  Google Scholar 

  • Kiyama H, Katayama Y, Hillyard CJ, Girgis S, MacIntyre I, Emson PC, Tohyama M (1985) Occurrence of calcitonin gene-related peptide in the chicken amacrine cells. Brain Res 327: 367–369

    PubMed  Google Scholar 

  • Kreutzberg G (1969) Neuronal dynamics and flow-IV. Blockage of intraaxonal enzyme transport by colchicine. Proc Natl Acad Sci USA. 62: 722–728

    PubMed  Google Scholar 

  • Lee Y, Kawai Y, Shiosaka S, Takami K, Kiyama H, Hillyard CJ, MacIntyre I, Emson PC, Tohyama M (1985 a) Coexistence of calcitonin gene-related peptide (CGRP)- and substance P-like peptide in a single cells of the trigeminal ganglion of the rat. Brain Res 330: 194–196

    PubMed  Google Scholar 

  • Lee Y, Takami K, Kawai Y, Girgis S, Hillyard CJ, MacIntyre I, Emson PC, Tohyama M (1985 b) Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistence with substance P. Neuroscience 15: 1227–1237

    Google Scholar 

  • Minagawa H, Shiosaka S, Inoue H, Hayashi N, Kasahara A, Kamada T, Tohyama M, Shiotani Y (1984) Three-dimensional distribution of substance P-containing structures in the rat stomach and their origins using whole-mount tissue. Gastroenterology 86: 51–59

    PubMed  Google Scholar 

  • Morris HR, Panico M, Etine T, Tippins J, Girgis SI, MacIntyre I (1984) Isolation and characterization of human calcitonin gene-related peptide. Nature 308: 746–748

    PubMed  Google Scholar 

  • Mulderry PK, Ghatei MA, Rodrigo J, Allen JM, Rosenfeld MG, Polak JM, Bloom SR (1985) Calcitonin gene-related peptide in cardiovascular tissues of the rat. Neuroscience 14: 947–954

    PubMed  Google Scholar 

  • Rosenfeld MG, Mermod JJ, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of novel neuropeptide encoded by the calcitonin gene via tissue specific RNA processing. Nature 304: 129–135

    PubMed  Google Scholar 

  • Sakanaka M, Magari S, Emson PC, Hillyard CJ, Girgis S, MacIntyre I, Tohyama M (1985) The calcitonin gene-related peptide-containing fiber projection from the hypothalamus to the septal area including its fine structures. Brain Res 344: 196–199

    PubMed  Google Scholar 

  • Skofitsch G, Jacobowitz DM (1985) Calcitonin gene-related peptide: Detailed immunohistochemical distribution in the central nervous system. Peptides 6: 721–745

    PubMed  Google Scholar 

  • Skofitsch G, Jacobowitz DM (1985) Autoradiographic distribution of125I calcitonin gene-related peptide binding sites in the rat central nervous system. Peptides 4: 975–986

    Google Scholar 

  • Schwartz CJ, Hökfelt T, Nilsson G, Terenius L, Rehfeld J, Brown M, Elde RP, Goldstein M, Said SI (1986) Distribution of peptide and catecholamine neurons in the gastrointestinal tract of rat and guinea-pig. Neuroscience 5: 689–697

    Google Scholar 

  • Shimada S, Shiosaka S, Emson PC, Hillyard CJ, Girgis S, MacIntyre I, Tohyama M (1985) Calcition gene-related peptidergic projection from the parabrachial area to the forebrain and diencephalon in the rat: an immunohistochemical analysis. Neuroscience 16: 607–616

    PubMed  Google Scholar 

  • Shimada S, Shiosaka S, Hillyard CJ, Girgis S, MacIntyre I, Emson PC, Tohyama M (1985) Calcition gene-related peptide projection from ventromedial nucleus to the insular cortex: a combined retrograde transport and immunocytochemical study. Brain Res 344: 200–203

    PubMed  Google Scholar 

  • Tache Y, Pappas T, Lauffenburger M, Goto Y, Walsh JH, Debas H (1984) Calcitonin gene-related peptide: Potent peripheral inhibitor of gastric acid secretion in rats and dogs. Gastroenterology 87: 344–349

    PubMed  Google Scholar 

  • Takami K, Kawai Y, Shiosaka S, Lee Y, Girgis S, MacIntyre I, Emson PC, Tohyama M (1985) Immunohistochemical evidence for the coexistence of calcitonine gene-related peptide- and choline acetyltransferase-like immunoreactivity in the neurons of the rat hypoglossal, facial and ambigous nucleus. Brain Res 328: 386–389

    PubMed  Google Scholar 

  • Takami K, Kawai Y, Uchida S, Tohyama M, Shiotani Y, Yoshida H, Emson PC, Girgis S, Hillyard CJ, MacIntyre I (1985) Effect of calcitonin generelated peptide on contraction of striated muscle in the mouse. Neurosci Lett 60: 227–231

    PubMed  Google Scholar 

  • Terenghi G, Polak JM, Ghatei MA, Mulderry PK, Butler JM, Unger WG, Bloom SR (1985) Distribution and origin of calcitonin gene-related peptide (CGRP) immunoreactivity in the sensory innervation of the mammalian eye. J Comp Neurol 233: 506–516

    PubMed  Google Scholar 

  • Tipins JR, Morris HR, Panico M, Etienne T, Bevis P, Girgis S, MacIntyre I, Azria M, Attinger M (1986) The myotropic and plasma-calcium modulating effects of calcitonin gene-related peptide (CGRP). Brain Res (in press)

  • Tom RT, Peterfreund RA, Sawchenko PE, Corrigan AZ, Rivier JE, Vale WW (1984) Release of the predicted calcitonin gene-related peptide from cultured rat trigeminal ganglion cells. Nature 308: 653–655

    PubMed  Google Scholar 

  • Tschopp FA, Henke H, Petermann JB, Tobler PH, Janzer R, Hökfelt T, Lundberg JM, Cuello C, Fsaicher JA (1985) Calcitonin gene-related peptide and its binding sites in the human central nervous system and pituitary. Proc Natl Acad Sci USA. 82: 248–252

    PubMed  Google Scholar 

  • Wanaka A, Matsuyama T, Yoneda S, Kimura K, Kamada T, Hillyard CJ, MacIntyre I, Emson PC, Tohyama M (1986) Origins and distribution of calcitonin gene-related peptide-containing nerves in the wall of the cerebral arteries of the guinea pig with special reference to the co-existence with substance P. Brain Res 369: 185–192

    PubMed  Google Scholar 

  • Zamboni L, De Martini C (1967) Buffered picric acid formaldehyde: a new rapid fixative for electron microscopy. J Cell Biol 35: 148A

    Google Scholar 

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Author notes

  1. Y. Lee

    Present address: Department of Neuroanatomy, Institute of Higher Nervous Activity, Japan

Authors and Affiliations

  1. First Department of Internal Medicine, Osaka University Medical School, Fukushimaku, Osaka, Japan

    N. Hayashi & T. Kamada

  2. Department of Chemical Pathology, University of London, Royal Postgraduate Medical School, Hammersmith Hospital, London, UK

    C. J. Hillyard, S. I. Girgis & I. MacIntyre

  3. Second-Department of Anatomy, Osaka University Medical School, Kitaku, Osaka, Japan

    M. Tohyama

  4. Department of Neuroanatomy, Institute of Higher Nervous Activity, Japan

    Y. Shiotani, N. Hayashi, T. Kamada, C. J. Hillyard, S. I. Girgis, I. MacIntyre & M. Tohyama

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  1. Y. Lee
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  2. Y. Shiotani
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  8. M. Tohyama
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Lee, Y., Shiotani, Y., Hayashi, N. et al. Distribution and origin of calcitonin gene-related peptide in the rat stomach and duodenum: An immunocytochemical analysis. J. Neural Transmission 68, 1–14 (1987). https://doi.org/10.1007/BF01244635

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  • DOI: https://doi.org/10.1007/BF01244635

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