Tachykinin and Calcitonin Gene-Related Peptide Immunoreactivities and Mrnas in the Mammalian Enteric Nervous System and Sensory Ganglia

  • Catia Sternini
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 298)

Abstract

The enteric nervous system, which extends with continuity from the esophagus to the anal canal, including the hepatobiliary pathway and pancreas, comprises a large number of intrinsic (enteric) neurons embedded within the alimentary tract itself and the processes of extrinsic (efferent and afferent) neurons (Furness and Costa, 1987). It contains a heterogeneous population of neurochemically distinct types of neurons, which are characterized by different morphologies, projection patterns, pharmacological and electrophysiological properties and functions (Costa et al., 1987; Furness and Costa, 1987). During the past decade, a variety of chemical messengers, including bioactive peptides, or different combinations of them, have been recognized in enteric neurons and their terminals, and in extrinsic nerves supplying the enteric nervous system as well (Costa et al., 1986; Furness et al., 1988; Llewellyn-Smith, 1989; Sternini, 1988). The same chemical messengers can occur also in other neuronal structures, including primary sensory neurons and terminals (Gibbins et al., 1987; Ju et al., 1987).

Keywords

Dorsal Root Ganglion Enteric Nervous System Primary Sensory Neuron Enteric Neuron Sensory Ganglion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Amara, S.G., Jones, V., Rosenfeld, M.G., Ong, E.S., and Evans, R.M., 1982, Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products, Nature, 298: 240.PubMedCrossRefGoogle Scholar
  2. Amara, S.G., Arriza, J.L., Leff, S.E., Swanson, L.W., Evans, R.M., Rosenfeld, M.G., 1985, Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide, Science, 229: 1094.PubMedCrossRefGoogle Scholar
  3. Barthó, L., Holzer, P., 1985, Search for a physiological role of substance P in gastrointestinal motility, Neuroscience, 16: 1.PubMedCrossRefGoogle Scholar
  4. Brecha, N.C, Sternini, C., Anderson, K., Krause, J.E., 1989, Expression and cellular localization of substance P/neuro-kinin A and neurokinin B mRNAs in the rat retina, Visual Neurosci., 3: 527.CrossRefGoogle Scholar
  5. Clague, J.R., Sternini, C., Brecha, N.C, 1985, Localization of calcitonin gene-related peptide-like immunoreactivity in neurons of the rat gastrointestinal tract, Neurosci. Lett., 56: 63.PubMedCrossRefGoogle Scholar
  6. Costa, M., Furness, J.B., Llewellyn-Smith, I.J., Murphy, R., Bornstein, J.C., Keast, J.R., 1985, Functional roles for substance P-containing neurons in the gastrointestinal tract, in: “Substance P. Metabolism and Biological Actions,” C.C. Jordan, P. Oehme, eds., Taylor and Francis, London.Google Scholar
  7. Costa, M., Furness, J.B., Gibbins, I.L., 1986, Chemical coding of enteric neurons, Prog. Brain Res., Volume 68, “Coexistence of Neuronal Messengers: a New Principle of Chemical Transmission,” T. Hökfelt, K. Fuxe, B. Pernow, eds., Elsevier, New York.Google Scholar
  8. Costa, M., Furness, J.B., Llewellyn-Smith, I.J., 1987, Histochemistry of the enteric nervous system, in: “Physiology of the Gastrointestinal Tract,” L.R. Johnson, ed., Raven, New York.Google Scholar
  9. Dockray, G.J., 1987, Physiology of enteric neuropeptides in: “Physiology of the Gastrointestinal Tract,” L.R. Johnson, ed., Raven, New York.Google Scholar
  10. Dockray, G.J., Sharkey, K.A., 1986, Neurochemistry of visceral afferent neurons, Prog. Brain Res., Volume 67, “Visceral Sensation,” F. Cervero, J.F.B. Morrison, eds., Elsevier, New York.Google Scholar
  11. Erspamer, V., 1981, The tachykinin peptide family, Trends Neurosci., 4: 267.CrossRefGoogle Scholar
  12. Eysselein, V.E., Khan, H., Davis, M., Sternini, C., Brecha, N., Cominelli, F., Williams, R., Snape, W., 1990, Neurokinin B is an abundant tachykinin form in bovine but not in human, rabbit and rat intestine: species differences in the expression of the preprotachykinin-II precursor, Gastroenterology, 98: A493.Google Scholar
  13. Fisher, J.A., Born, W., 1985, Novel peptides from the calcitonin gene: Expression, receptors and biological function, Peptides, 6: 265.CrossRefGoogle Scholar
  14. Furness, J.B., Costa, M., 1987, “The Enteric Nervous System,” Churchill Livingstone, London.Google Scholar
  15. Furness, J. B., Llewellyn-Smith, I.J., Bornstein, J. C., Costa, M., 1988, Chemical neuroanatomy and the analysis of neuronal circuitry in the enteric nervous system, in: “Handbook of Chemical Neuroanatomy,” Volume 6: The Peripheral Nervous System, A. Björklund, T. Hökfelt, C. Owman, eds., Elsevier, New York.Google Scholar
  16. Galligan, J.J., Tokimasa, T., North, R.A., 1987, Effects of three mammalian tachykinins on single enteric neurons, Neu-rosci. Lett., 82: 167.CrossRefGoogle Scholar
  17. Gibbins, I.L., Furness, J.B., Costa, M., Maclntyre, I., Hillyard, C.J. Girgis, S., 1985, Colocalization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of the guinea pig, Neurosci. Lett., 57: 125.PubMedCrossRefGoogle Scholar
  18. Gibbins, I.L. Furness, J.B., Costa, M., 1987, Pathway-specific patterns of the co-existence of substance P, calcitonin gene-related peptide, cholecystokinin and dynorphin in neurons of the dorsal root ganglia of the guinea-pig, Cell Tissue Res., 248: 417.PubMedCrossRefGoogle Scholar
  19. Goehler, E.L., Sternini, C., Brecha, N., 1988a, Calcitonin generelated peptide immunoreactivity in the biliary pathway and liver of the guinea-pig: distribution and colocalization with substance P, Cell Tissue Res., 253: 145.PubMedCrossRefGoogle Scholar
  20. Goehler, E.L. Sternini, C., 1988b, Effect of extrinsic denervation on calcitonin gene-related peptide immunoreactivity (CGRP-IR) in the rat hepatobiliary system, Soc. Neurosci. Abs., 14: 984.Google Scholar
  21. Goodman, E.C., Iversen, L.L., 1986, Calcitonin gene-related peptide: novel neuropeptide, Life Sci., 38: 2169.PubMedCrossRefGoogle Scholar
  22. Green, T., Dockray, G.J., 1987, Calcitonin gene-related peptide and substance P in afferents to the upper gastrointestinal tract in the rat, Neurosci. Lett., 76: 151.PubMedCrossRefGoogle Scholar
  23. Green, T., Dockray, G.J., 1988, Characterization of the peptidergic afferent innervation of the stomach in the rat, mouse and guinea-pig, Neuroscience, 25: 181.PubMedCrossRefGoogle Scholar
  24. Gulbenkian, S., Merighi, A., Wharton, J., Varndell, I.M., Polak, J.M., 1986, Ultrastructural evidence for the coexistence of calcitonin gene-related peptide and substance P in secretory vesicles of peripheral nerves in the guinea pig, J. Neurocytol., 15: 535.PubMedCrossRefGoogle Scholar
  25. Helke, C.J., Hill, K.M., 1988, Immunohistochemical studies of neuropeptides in vagal and glossopharyngeal afferent neurons in the rat, Neuroscience, 26: 539.PubMedCrossRefGoogle Scholar
  26. Holzer, P., 1988, Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides, Neuroscience, 24: 739.PubMedCrossRefGoogle Scholar
  27. Holzer, P., Barthó, L., Matusaki, O., Bauer, V., 1989, Calcitonin gene-related peptide action on intestinal circular muscle, Am. J. Physiol., 256: G546.Google Scholar
  28. Jessell, T.M., 1983, Substance P in the nervous system, in: “Handbook of Psychopharmacology” Volume 16, L.L. Iversen, S.D. Iversen, S.H. Snyder, eds., Plenum, New York.Google Scholar
  29. Ju, G., Hökfelt, T., Brodin, E., Fahrenkrug, J., Fisher, J.A., Frey, P., Elde, R.P., Brown, J.C., 1987, Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, vasoactive intestinal polypeptide- and cholecysto-kinin-immunoreactive ganglion cells, Cell Tissue Res., 247: 417.PubMedCrossRefGoogle Scholar
  30. Kage, R., McGregor, G.P., Thim, L., Conlon, J.M., 1988, Neuro-peptide-gamma: a peptide isolated from rabbit intestine that is derived from gamma-preprotachykinin, J. Neurochem., 50: 1412.PubMedCrossRefGoogle Scholar
  31. Krause, J.E., Chirgwin, J.M., Carter, M.S., Xu, Z.S., Hershey, A.D., 1987, Three rat preprotachykinin mRNAs encode the neuropeptide substance P and neurokinin A, Proc. Natl. Acad. Sci. USA, 84: 881.PubMedCrossRefGoogle Scholar
  32. Kruger, L., Silverman, J.D., Mantyh, P.W., Sternini, C., Brecha, N., 1989, Peripheral patterns of calcitonin gene-related peptide general somatic sensory innervation: cutaneous and deep terminations, J. Comp. Neurol., 280: 291.PubMedCrossRefGoogle Scholar
  33. Llewellyn-Smith, I.J., 1989, Neuropeptides and the microcircuitry of the enteric nervous system, in: “Regulatory Peptides,” J.M. Polak, ed., Verlag.Google Scholar
  34. Maggio, J.E., 1988, Tachykinins, Ann. Rev. Neurosci., 11: 13.PubMedCrossRefGoogle Scholar
  35. Mantyh, P.W., Gates, T., Mantyh, C.R., Maggio, J.E., 1989, Autoradiographic localization and characterization of tachykinin receptor binding sites in the rat brain and peripheral tissues, J. Neurosci., 9: 258.PubMedGoogle Scholar
  36. Mantyh, P.W., Mantyh, C.R., Gates, T., Vigna, S.R., Maggio, J.E., 1988, Receptor binding sites for substance P and substance K in the canine gastrointestinal tract and their possible role in inflammatory bowel disease, Neuroscience, 25: 817.PubMedCrossRefGoogle Scholar
  37. Mulderry, P.K., Ghatei, M.A., Bishop, A.E., Allen, Y.S., Polak, J.M., Bloom, S.R., 1985, Distribution and chromatographic characterization of CGRP-like immunoreactivity in the brain and gut of the rat, Reg. Pept., 12: 133.CrossRefGoogle Scholar
  38. Mulderry, P.K., Ghatei, M.A., Spokes, R.A., Jones, P.M., Pierson, A.M., Hamid, Q.A., Kanse, S., Amara, S.G., Burrin, J.M., Legon, S., Polak, J.M., Bloom, S.R., 1988, Differential expression of α-CGRP and β-CGRP by primary sensory neurons and enteric autonomic neurons of the rat, Neuroscience, 25: 195.PubMedCrossRefGoogle Scholar
  39. Palmer, J.M., Schemann, M., Tamura, K., Wood, J.D., 1986, Calcitonin gene-related peptide excites myenteric neurons, Eur. J. Pharmacol., 132: 163.PubMedCrossRefGoogle Scholar
  40. Pernow, B., 1983, Substance P, Pharmacol. Rev., 35: 85.PubMedGoogle Scholar
  41. Rosenfeld, M., Mermod, J.-J., Amara, S.G., Sawcenko, P.E., Rivier, J., Vale, W.W., Evans, R.M., 1983, Production of a novel neuropeptide encoded by the calcitonin gene via tissue specific RNA processing, Nature, 304: 129.PubMedCrossRefGoogle Scholar
  42. Rosenfeld, M.G., Amara, S.G., Evans, R.M., 1984, Alternative RNA processing: determining neuronal phenotype, Science, 225: 1315.PubMedCrossRefGoogle Scholar
  43. Steenbergh, P.H., Höppener, J.W.M., Zandberg, J., Lips, C.J.M., Jansz, H.S., 1985, A second human calcitonin/CGRP gene, FEBS Lett., 183: 402.CrossRefGoogle Scholar
  44. Sternini, C., 1988, Structural and chemical organization of the myenteric plexus, Ann. Rev. Physiol., 50: 81.CrossRefGoogle Scholar
  45. Sternini, C., 1990, Neurochemistry of spinal afferents supplying the upper gastrointestinal tract and pancreas, in: “Brain and Gut Interactions,” Y. Taché, D. Wingate, eds., CRC Press, in press.Google Scholar
  46. Sternini, C., Anderson, K., 1990, Differential distribution of α- and β-calcitonin gene-related peptide (CGRP) mRNAs in enteric and sensory neurons, Gastroenterology, 98: A526.Google Scholar
  47. Sternini, C., Anderson, K., Frantz, G., Krause, J.E., 1989, Expression of substance P/neurokinin A-encoding preprotachykinin messenger ribonucleic acids in the rat enteric nervous system, Gastroenterology, 97: 348.PubMedGoogle Scholar
  48. Sternini, C., Brecha, N., 1986, Immunocytochemical identification of islet cells and nerve fibers containing calcitonin gene-related peptide-like immunoreactivity in the rat pancreas, Gastroenterology, 90: 1155.PubMedGoogle Scholar
  49. Sternini, C., Reeve, J.R., Jr., Brecha, N., 1987, Distribution and characterization of calcitonin gene-related peptide immunoreactivity in the digestive system of normal and capsaicin-treated rats, Gastroenterology, 93: 852.PubMedGoogle Scholar
  50. Su, H.C., Bishop, A.E., Power, R.F., Hamada, Y., Polak, J.M., 1987, Dual intrinsic and extrinsic origins of CGRP- and NPY-immunoreactive nerves of rat gut and pancreas, J. Neurosci., 7: 2674.PubMedGoogle Scholar
  51. Takaki, M., Jin, J.-G., Nakayama, S., 1989, Possible involvement of calcitonin gene-related peptide (CGRP) in non-cholinergic, non-adrenergic relaxation induced by mesenteric nerve stimulation in guinea pig ileum, Brain Res., 478: 199.PubMedCrossRefGoogle Scholar
  52. Tatemoto, K., Lundberg, J.M., Jornvall, H., Mutt, V., 1985, Neuropeptide K: isolation, structure and biological activities of a novel brain tachykinin, Biochem. Biophys. Res. Commun., 128: 947.PubMedCrossRefGoogle Scholar
  53. Warden, M.K., Young, W.S., III, 1988, Distribution of cells containing mRNAs encoding substance P and neurokinin B in the rat central nervous system, J. Comp. Neurol., 272: 90.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • Catia Sternini
    • 1
  1. 1.Department of Medicine and Brain Research Institute UCLA School of Medicine and Center for Ulcer Research and EducationVeterans’ Administration Medical CenterLos AngelesUSA

Personalised recommendations