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The endocrine cell system of the digestive tract

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Ultrastructure of the Digestive Tract

Part of the book series: Electron Microscopy in Biology and Medicine ((EMBM,volume 4))

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Abstract

The sources of gut hormones are basal-granulated cells dispersed in the epithelium of the gastroenteric mucosa. They are clear cells with secretory granules in the basal portion of the cell and were discovered over 100 years ago (1; for early literature see 2). Since the beginning of this century it has been noticed that these granules showed a positive chromaffin reaction, i.e., they tinge yellow after being treated with a fixative containing K2CrO4 (3,4). For this reason the term “enterochromaffin cell” has long been the synonym of the basal-granulated or gut endocrine cell. The chromaffin reaction of the cells, meanwhile, was ascribed to their content of serotonin (5-HT) (5).

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References

  1. Heidenhain R: Untersuchungen über den Bau der Labdrüsen. Arch Mikr Anat 6: 368–406, 1870.

    Article  Google Scholar 

  2. Patzelt V: Der Darm. In: Möllendorff’s Handbuch der Mikroskopischen Anatomie des Menschen, Vol 3. p 1–448, 1936.

    Google Scholar 

  3. Schmidt JE: Beiträge zur normalen und pathologischen Histologie einiger zellarten der Schleimhaut des mems chlichen Darmkanals. Arch Mikr Anat 66: 12–40, 1905.

    Article  Google Scholar 

  4. Ciaccio C: Sur une nouvelle espèce cellulaire dans les glands de Lieberkühn. C R Soc Biol Ses Fil 60; 76–77, 1906.

    Google Scholar 

  5. Erspamer V, Asero B: Identification of enteramine, the specific hormone of the enterochromaffin cell system as 5-hydroxy-tryptamine. Nature (Lond) 169: 800–801, 1952.

    Article  PubMed  CAS  Google Scholar 

  6. Ito S, Winchester RJ: The fine structure of the gastric mucosa in the bat. J Cell Biol 16: 541–577, 1963.

    Article  PubMed  CAS  Google Scholar 

  7. Toner PG: Fine structure of argyrophil and argentaffin cells in the gastrointestinal tract of the fowl. Z Zellforsch 63: 830–839, 1964.

    Article  PubMed  CAS  Google Scholar 

  8. Solcia E, Vassallo G, Sampietro R: Endocrine cells in the antro-pyloric mucosa of the stomach. Z Zellforsch 81: 474–486, 1967.

    Article  PubMed  CAS  Google Scholar 

  9. Orci L, Pictet R, Forssmann WG, Renold AE, Rouiller C: The endocrine cells in the epithelium of the gastrointestinal mucosa of the rat. Diabetologia 4: 56–67, 1968.

    Article  PubMed  CAS  Google Scholar 

  10. Forssmann WG, Orci L, Pictet R, Renold AE, Rouiller C: The endocrine cells in the epithelium of the gastrointestinal mucosa of the rat. An electron microscope study. J Cell Biol 40: 692–715, 1969.

    Article  PubMed  CAS  Google Scholar 

  11. Sasagawa T, Kobayashi S, Fujita T: Electron microscope studies on the endocrine cells of the human gut and pancreas. In: Gastro-entero-pancreatic Endocrine System. A Cell-biological Approach. T Fujita (ed), Tokyo Igaku-Shoin, p 17–38, 1973.

    Google Scholar 

  12. Grube D, Forssmann WG: Morphology and function of the enteroendocrine cells. Horm Metab Res 11: 589–606, 1979.

    Article  PubMed  CAS  Google Scholar 

  13. Solcia A, Creutzfeldt W, Falkmer S, Fujita T, Greider MH, Grossman MI, Grube D, Håkanson R, Larsson LI, Lechago J, Lewin K, Polak JM, Rubin W: Human gastroenteropancreatic endocrineparacrine cells. Santa Monica 1980 classification. In: Cellular Basis of Chemical Messengers in the Digestive System. MI Grossman, MAB Brazier, J Lechago (eds), New York: Academic Press, p 159–165, 1981.

    Google Scholar 

  14. Kobayashi S, Segi M: Gut paraneurons and Segi’s cap. In: Ultrastructure of Endocrine Cells and Tissues. PM Motta (ed), Boston: Martinus Nijhoff Publishers, p 127–135, 1984.

    Google Scholar 

  15. Fujita T, Kobayashi S: The cells and hormones of the GEP endocrine system - the current of studies. In: Gastro-entero-pancreatic Endocrine System. A Cell-biological Approach. T Fujita (ed), Tokyo: Igaku-shoin, p 1–16, 1973.

    Google Scholar 

  16. Fujita T, Kobayashi S: Structure and function of gut endocrine cells. Int Rev Cytol Suppl 6: 187–233, 1977.

    PubMed  CAS  Google Scholar 

  17. Iwanaga T, Yamada J: Endocrinelike cells of peculiar shape in the proventriculus of the chicken - possible mechanoreceptors? Biomed Res 1 (suppl): 28–32, 1980.

    Google Scholar 

  18. Kobayashi S, Fujita T, Sasagawa T: Electron microscope studies on the endocrine cells of the human gastric fundus. Arch Histol Jap 32: 429–444, 1971.

    PubMed  CAS  Google Scholar 

  19. Böck P, Gorgas K: Enterochromaffin cells and enterochromaffinlike cells in the cat pancreas. In: Endocrine Gut and Pancreas. T Fujita (ed), Amsterdam: Elsevier Scientific Publishing Company, p 13–24, 1976.

    Google Scholar 

  20. Nihei K, Iwanaga T, Yanaihara N, Mochizuki T, Fujita T: Preproenkephalin A occurs in the enterochromaffin (EC) cells of the procine intestine: An immunocytochemical study using antisera to met-enkephalin-Arg6-Gly7-Leos and to serotonin. Biomed Res 4: 393–398, 1983.

    CAS  Google Scholar 

  21. Håkanson R, Owman CH, Sjoberg NO, Sporrong B: Amine mechanisms in enterochromaffin and enterochromaffinlike cells of gastric mucosa in various mammals. Histochemie 21: 189–220, 1970.

    Article  PubMed  Google Scholar 

  22. Håkanson R, Lindstrand K, Nordgren L, Owman CH: Histamine-containing epithelial cells in rat stomach: A possible storage site for the intrinsic factor. Eur J Pharmacol 8: 315–325, 1969.

    Article  PubMed  Google Scholar 

  23. Polak JM, Bloom SE, Kuzio M, Brown JC, Pearse AGE: Cellular localization of gastric inhibitory polypeptide in the duodenum and jejunum. Gut 14: 284, 1973.

    Article  PubMed  CAS  Google Scholar 

  24. Polak JM, Buchan AMJ: Heterogeneity of the D1 cell. In: Cellular Basis of Chemical Messengers in the Digestive System. MI Grossman, MAB Brazier, J Lechago (eds), New York: Academic Press, p 121–131, 1981.

    Google Scholar 

  25. Fujita T, Kobayashi S: Experimentally induced granule release in the endocrine cells of dog pyloric antrum. Z Zellforsch 116: 52–60, 1971.

    Article  PubMed  CAS  Google Scholar 

  26. Kobayashi S, Fujita T: Emiocytotic granule release in the basal-granulated cells of the dog induced by intraluminal application of adequate stimuli. In: Gastro-enteropancreatic Endocrine System. A Cell-biological Approach. T Fujita (ed), Tokyo, Igaku-Shoin, p 49–58, 1973.

    Google Scholar 

  27. Osaka M, Sasagawa T, Fujita T: Emiocytotic granule release in the human antral endocrine cells. In: Gastroentero-pancreatic Endocrine System. A Cell-biological Approach. T Fujita (ed), Tokyo: Igaku-Shoin, p 59–63, 1973.

    Google Scholar 

  28. Osaka M, Sasagawa T, Fujita T: Granule release from endocrine cells in acidified human duodenal bulb. An electron microscope study of biopsy materials. Arch Histol Jpn 37: 73–94, 1974.

    PubMed  CAS  Google Scholar 

  29. Miyagami H, Watanabe Y, Sawada Y, Kato K, Shiono K, Kondo K, Kidokoro T: Ultrastructures of G cells and the mechanism of gastrin release before and after selective vagotomy with pyloroplasty. Arch Histol Jpn 40: 51–62, 1977.

    PubMed  CAS  Google Scholar 

  30. Kobayashi S, Sasagawa T: Morphological aspects of the secretion of gastro-enteric hormones. In: Endocrine, Gut and Pancreas. T Fujita (ed), Amsterdam: Elsevier Scientific Publishing Company, p 255–271, 1976.

    Google Scholar 

  31. Fujita T, Osaka M, Yanatori Y: Granule release of enterochromaffin (EC) cells by cholera enterotoxin in the rabbit. Arch Histol Jpn 36: 367–378, 1974.

    PubMed  CAS  Google Scholar 

  32. Osaka M, Fujita T, Yanatori Y: On the possible role of intestinal hormones as the diarrhoeagenic messenger in cholera. Virchows Arch B (Cell Pathol) 18: 287–296, 1975.

    CAS  Google Scholar 

  33. Grossman MI: Integration of neural and hormonal control of gastric secretion. Physiologist 6: 349–357, 1963.

    Google Scholar 

  34. Fujita T, Muraki S, Sato K, Noguchi R, Shimoji K: Effects of atropine and tetrodotoxin upon pancreozymin release from canine duodenum in response to luminal stimuli. Biomed Res 1: 59–65, 1980.

    CAS  Google Scholar 

  35. Fujita T, Matsunai Y, Muraki S, Sato K, Shimoji K: Effect of intraluminally administered lidocaine upon the pancreozymin-producing endocrine cells of the canine duodenum. In: Integrative Control Functions of the Brain, vol 1. M Ito (ed), Tokyo: Kodansha Scientific, p 296–297, 1978.

    Google Scholar 

  36. Fujita T, Kobayashi S, Muraki S, Sato K, Shimoji K: Gut endocrine cells as chemoreceptors. In: Gut Peptides. Secretion, Function and Clinical Aspects. A Miyoshi (ed), Tokyo: Kodansha, p 47–52, 1979.

    Google Scholar 

  37. Fujita T: Messenger substances of neurons and paraneurons: Their chemical nature and the routes and ranges of their transport to targets. Biomed Res 4: 239–256, 1983.

    CAS  Google Scholar 

  38. Pearse AGE, Polak JM: Neural crest origin of the endocrine polypeptide (APUD) cells of the gastrointestinal tract and pancreas. Gut 12: 783–788, 1971.

    Article  PubMed  CAS  Google Scholar 

  39. Fujita T: The gastro-enteric endocrine cell and its paraneuronic nature. In: Chromaffin, Enterochromaffin and Related Cells. RE Coupland, T Fujita (eds), Amsterdam: Elsevier, p 191–208, 1976.

    Google Scholar 

  40. Fujita T, Kobayashi S: Current views on the paraneurone concept. TINS 2: 27–30, 1979.

    Google Scholar 

  41. O’Conner DT, Burton D, Deftos LJ: Chromogranin A: Immunohistology reveals its universal occurrence in normal polypeptide hormone producing endocrine glands. Life Sci 33: 1657–1663, 1983.

    Article  Google Scholar 

  42. Nolan JA, Trojanowski JQ, Hogue-Angeletti R: Neurons and neuroendocrine cells contain chromogranin: Detection of the molecule in normal bovine tissues by immunochemical and immunohistochemical methods. J Histochem Cytochem 33: 791–798, 1985.

    Article  PubMed  CAS  Google Scholar 

  43. Fischer-Colbrie R, Lassmann H, Hagn C, Winkler H: Immunological studies on the distribution of chromogranin A and B in endocrine and nervous tissues. Neurosci 16: 547–555, 1985.

    Article  CAS  Google Scholar 

  44. Kobayashi S: Cellular background in gut hormone secretion. In: Gut Peptides. Secretion, Function and Clinical Aspects. A Miyoshi (ed), Tokyo: Kodansha, p 53–58, 1979.

    Google Scholar 

  45. Kanno T, Saito A, Yonezawa H: Unidirectional cellular processes of stimulus-secretion coupling in a cell secreting cholecystokininpancreozymin. In: Histochemistry and Cell Biology of Autonomic Neurons, SIF Cells and Para-neurons. O Eränko et al. (eds), New York: Raven Press, p 327–332, 1980.

    Google Scholar 

  46. Osaka M, Kobayashi S: Duodenal basal-granulated cells in the human fetus with special reference to their relationship to nervous elements. In: Endocrine Gut and Pancreas. T Fujita (ed), Amsterdam: Elsevier Scientific Publishing Company, p 145–158, 1976.

    Google Scholar 

  47. Kusumoto Y, Iwanaga T, Ito S, Fujita T: Juxtaposition of somatostatin cell and parietal cell in the dog stomach. Arch Histol Jpn 42: 459–465, 1979.

    PubMed  CAS  Google Scholar 

  48. Larsson LI, Goltermann N, de Magistris L, Rehfeld JF, Schwartz TW: Somatostatin cell processes as pathways for paracrine secretion. Science 205: 1393–1395, 1979.

    Article  PubMed  CAS  Google Scholar 

  49. Schmechel D, Marangos PJ, Brightman M: Neurone-specific enolase is a molecular marker for peripheral and central neuroendocrine cells. Nature 276: 834–836, 1978.

    Article  PubMed  CAS  Google Scholar 

  50. Wharton J, Polak JM, Cole GA, Marangos PJ, Pearse AGE: Neuron-specific enolase as an immunocytochemical marker for the diffuse neuroendocrine system in human foetal lung. J Histochem Cytochem 29: 1359–1364, 1981.

    Article  PubMed  CAS  Google Scholar 

  51. Fujita T, Iwanaga T, Nakajima T: Immunohistochemical detection of nervous system-specific proteins in normal and neoplastic paraneurons in the gut and pancreas. In: Gut Peptides and Ulcer. A Miyoshi (ed), Tokyo: Biomedical Research Foundation, p 81–88, 1983.

    Google Scholar 

  52. Iwanaga T, Fujita T, Ito S: Immunohistochemical staining of enteroendocrine paraneurons with anti-brain tubulin antiserum. Biomed Res 3: 99–101, 1982.

    Google Scholar 

  53. Iwanaga T, Hozumi I, Yamakuni T, Takahashi Y, Fujita T: A cerebellar Purkinje cell-specific protein (spot 35 protein) showing wide distribution in the endocrine system of some mammals: An immunohistochemical study. Cell Tissue Res (in press).

    Google Scholar 

  54. Iwanaga T, Takahashi-Iwanaga H, Fujita T, Yamakuni T, Takahashi Y: Immunohistochemical demonstration of a cerebellar protein (spot 35 protein) in some sensory cells of guinea pig. Biomed Res 6: 329–334, 1985.

    CAS  Google Scholar 

  55. Dias-Amads L: Sur la signification des cellules de Nicolas. C R Soc Biol (Paris) 93: 1550–1551, 1925.

    Google Scholar 

  56. Danisch F: Zur Histogenese der sogenannten Appendixkarzinoide. Beitr Pathol Anat Allgem Pathol 72: 687–709, 1924.

    Google Scholar 

  57. Andrew A: APUD cells and paraneurons: Embryonic origin. Adv Cell Neurobiol 2: 3–32, 1981.

    CAS  Google Scholar 

  58. Le Douarin NM, Teillet MA: The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryo! Morphol 30: 31–48, 1973.

    Google Scholar 

  59. Andrew A: APUD cells in the endocrine pancreas and intestine of chick embryos. Gen Comp Endocrinol 26: 485–495, 1975.

    Article  PubMed  CAS  Google Scholar 

  60. Osaka M, Kobayashi S: Duodenal basal-granulated cells in the human fetus with special reference to their relationship to nervous elements. In: Endocrine Gut and Pancreas. T Fujita (ed), Amsterdam: Elsevier Scientific Publishing Company, p 145–158, 1976.

    Google Scholar 

  61. Fujii S: Development of pancreatic endocrine cells in the rat fetus. Arch Histol Jpn 42: 467–479, 1979.

    PubMed  CAS  Google Scholar 

  62. Larsson LI: Ontogeny of peptide-producing nerves and endocrine cells of the gastro-duodeno-pancreatic region. Histochemistry 54: 133–142, 1977.

    Article  PubMed  CAS  Google Scholar 

  63. Inokuchi H, Fujimoto S, Kawai K: Cellular kinetics of gastrointestinal mucosa, with special reference to gut endocrine cells. Arch Histol Jpn 46: 137–157, 1983.

    Article  PubMed  CAS  Google Scholar 

  64. Deschner EE, Lipkin M: An autoradiographic study of the renewal of argentaffin cells in human rectal mucosa. Exp Cell Res 43: 661–665, 1966.

    Article  PubMed  CAS  Google Scholar 

  65. Lehy T, Willems G: Population kinetics of antral gastrin cells in the mouse. Gastroenterology 71: 614–619, 1976.

    PubMed  CAS  Google Scholar 

  66. Kobayashi S, Iwanaga T, Fujita T: Segi’s cap: Huge aggregation of basal-granulated cells discovered by Segi (1935) on the intestinal villi of the human fetus. Arch Histol Jpn 43: 79–83, 1980.

    PubMed  CAS  Google Scholar 

  67. Tsubouchi S, Leblond CP: Migration and turnover of enteroendocrine and caveolated cells in the epithelium of the descending colon, as shown by radioautography after continuous infusion of 3H-thymidine into mice. Am J Anat 156: 431–452, 1979.

    Article  PubMed  CAS  Google Scholar 

  68. Odartchenko N, Hedinger C, Ruzicka J, Weber E: Cytokinetics of argentaffin cells in mouse intestinal mucosa. Virchows Arch Abt B Zellpathol 6: 132–136, 1970.

    Google Scholar 

  69. Ferreira MN, Leblond CP: Argentaffin and other “endocrine” cells of the small intestine in the adult mouse. 2. Renewal. Am J Anat 131: 331–352, 1971.

    Article  PubMed  CAS  Google Scholar 

  70. Cheng H, Leblond CP: Origin and differentiation and renewal of the four main epithelial cell types in the mouse small intestine. 3. Entero-endocrine cells. Am J Anat 141: 503–520, 1974.

    Article  PubMed  CAS  Google Scholar 

  71. Fujita T, Kobayashi S, Yui R, Iwanaga T: Evolution of neurons and paraneurons. In: Hormones, Adaptation and Evolution. S Ishii et al. (eds), Tokyo: Japan Scientific Society Press/Berlin: Springer-Verlag, p 35–43, 1980.

    Google Scholar 

  72. Westfall JA, Kinnamon JC: A second sensory-motorinterneuron with neurosecretory granules in Hydra. J Neurocytol 7: 365–379, 1978.

    Article  PubMed  CAS  Google Scholar 

  73. Grimmelikhuijzen CJP, Carraway RE, Rökaeus Å, Sundler F: Neurotensinlike immunoreactivity in the nervous system of hydra. Histochemistry 72: 199–209, 1981.

    Article  PubMed  CAS  Google Scholar 

  74. Grimmelikhuijzen CJP, Dierickx K, Boer GJ: Oxytocin/ vasopressinlike immunoreactivity is present in the nervous system of hydra. Neuroscience 7: 3191–3199, 1982.

    Article  PubMed  CAS  Google Scholar 

  75. Reuter M, Karhi T, Schot LPC: Immunocytochemical demonstration of peptidergic neurons in the central and peripheral nervous systems of the flatworm Microstomum lineare with antiserum to FMRF-amide. Cell Tiss Res 238: 431–436, 1984.

    Article  CAS  Google Scholar 

  76. Nishiitsutsuji-Uwo J, Endo Y: Gut endocrine cells in insects: The ultrastructure of the endocrine cells in the cockroach midgut. Biomed Res 2: 30–44, 1981.

    Google Scholar 

  77. Iwanaga T, Fujita T, Nishiitsutsuji-Uwo J, Endo Y: Immunohistochemical demonstration of PP-, somatostatin-, enteroglucagon- and VIP-like immunoreactivities in the cockroach midgut. Biomed Res 2: 202–207, 1981.

    CAS  Google Scholar 

  78. Fujita T, Yui R, Iwanaga T, Nishiitsutsuji-Uwo J, Endo Y, Yanaihara N: Evolutionary aspects of “brain-gut peptides”: An immunohistochemical study. Peptides 2 (suppl 2): 123–131, 1981.

    Article  PubMed  CAS  Google Scholar 

  79. Fujita T, Yui R, Iwanaga T: Immunohistochemical studies of neuropeptides in invertebrates. Adv Neurolog Sci 27: 468–478, 1983.

    CAS  Google Scholar 

  80. Yui R, Iwanaga T, Kuramoto H, Fujita T: Neuropeptide immunocytochemistry in protostomian invertebrates, with special reference to insects and molluscs. Peptides 6(suppl 3): 411–415, 1985.

    Article  PubMed  CAS  Google Scholar 

  81. Endo Y, Nishiitsutsuji-Uwo J: Exocytotic release of secretory granules from endocrine cells in the midgut of insects. Cell Tiss Res 222: 515–522, 1982.

    Article  CAS  Google Scholar 

  82. Bevis PJR, Thorndyke MC: A cytochemical and immunofluorescence study of endocrine cells in the gut of the ascidian Styela clava. Cell Tiss Res 199: 139–144, 1979.

    Article  CAS  Google Scholar 

  83. Pestarino M: Occurrence of different secretinlike cells in the digestive tract of the ascidian Styela plicata (Urochordata, Ascidiacea). Cell Tiss Res 226: 231–235, 1982.

    Article  CAS  Google Scholar 

  84. Fritsch HAR, Van Noorden S, Pearse AGE: Gastrointestinal and neurohormonal peptides in the alimentary tract and cerebral complex of Ciona intestinalis (Ascidiaceae). Their relevance to the evolution of the diffuse neuroendocrine system. Cell Tiss Res 223: 369–402, 1982.

    Article  CAS  Google Scholar 

  85. Kataoka K, Fujita H: The occurrence of endocrine cells in the intestine of the lancelet, Branchiostoma japonicum. An electron microscope study. Arch Histol Jpn 36: 401406, 1974.

    Google Scholar 

  86. Van Noorden S, Pearse AGE: The localization of immunoreactivity to insulin, glucagon and gastrin in the gut of Amphioxus (Branchiostoma) lanceolatus. In: The Evolution of the Pancreatic Islets. TAI Grillo, L Liebson, A Epple (eds), Oxford: Pergamon Press, p 163–178, 1976.

    Google Scholar 

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Fujita, T. (1988). The endocrine cell system of the digestive tract. In: Motta, P.M., Fujita, H., Correr, S. (eds) Ultrastructure of the Digestive Tract. Electron Microscopy in Biology and Medicine, vol 4. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2071-5_13

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