Histochemistry

, Volume 84, Issue 4–6, pp 471–483 | Cite as

Immunocytochemical identification and localization of peptide hormones in the gastro-entero-pancreatic (GEP) endocrine system of the mouse and a stomachless fish, Barbus conchonius

  • I. H. W. M. Rombout
  • C. P. M. van der Grinten
  • F. M. Peeze Binkhorst
  • J. J. Taverne-Thiele
  • H. Schooneveld
Original Articles
Received:
Accepted:

Summary

A large number of antisera mainly raised against mammalian hormones are tested immunocytochemically on the GEP-endocrine system of mouse and fish (Barbus conchonius). The endocrine pancreas of mouse and fish appeared to contain the same four endocrine cell types; insulin-, glucagon-, PP- and somatostatin-immunoreactive cells.

In mouse about 13 GEP endocrine cell types are distinguished 1. insulin-, 2. somatostatin-, 3. glucagon-, 4. PP-, 5. (entero)glucagon-/PP-like, 6. CCK-like, 7. substance P-, 8. neurotensin-, 9. VIP-, 10. gastrin-, 11. secretin-, 12. β-endorphin-, 13. serotonin-immunoreactive cells.

Based on this and a previous study at least 13 GEP endocrine cell types seems to be present in stomachless fish: 1–9 as described for mouse, 10. (entero)glucagon-like, 11. met-enkephalin, 12. VIP-like, 13. unspecific immunoreactive endocrine cells.

Coexistence of glucagon and PP-like peptides is found in the gut and pancreas of mice and in the gut of B. conchonlus. In mouse pancreas and fish gut, endocrine cells showing only PP-or glucagon-like immunoreactivity are found too. In mouse stomach some endocrine cells, showing only PP-immunoreactivity are demonstrated. In the same region coexistence of C-1-gastrin-and FMRF-amide-immunoreactivity is found in endocrine cells. The importance of these phenomena are discussed.

Enteric nerves immunoreactive with antisera raised against substance P and GRP are found in mouse, against somatostatin and met-enkephalin in both mouse and fish and against VIP in fish.

Keywords

Peptide Glucagon Secretin Endocrine Cell Peptide Hormone 
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.
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ali-Rachedi A, Varndell IM, Adrian TE, Gapp DA, Van Noorden S, Bloom SR, Polak JM (1984) Peptide YY (PYY)immunoreactivity is costored with glucagon-related immunoreactants in endocrine cells of the gut and pancreas. Histochemistry 80:487–491Google Scholar
  2. Alumets J, Håkanson R, Sundler F, Chang KJ (1978) Leu-enkephalin-like material in nerves and enterochromaffin cells in the gut. Histochemistry 56:187–196Google Scholar
  3. Baetens D, Malaisse-Lagae F, Perrelet A, Orci L (1979) Endocrine pancreas: three dimensional reconstruction shows two types of islets of Langerhans. Science 206:1323–1325Google Scholar
  4. Bishop CA, O'Shea M, Miller RJ (1981) Neuropeptide, proctolin (H-Arg-Tyr-Leu-Pro-Thr-OH): immunological detection and neuronal localization in insect central nervous system. Proc Natl Acad Sci USA 78:5899–5902Google Scholar
  5. Bonner-Weir S, Bonner GC (1979) The organization of the endocrine pancreas: a hypothetical unifying view of the phylogenetic differences. Gen Comp Endocrinol 38:28–37Google Scholar
  6. Böttcher G, Sjölund K, Ekblad E Håkanson R, Schwartz TW, Sundler F (1984) Coexistence of peptide YY and glicentin immunoreactivity in endocrine cells of the gut. Regul Pept 8:261–266Google Scholar
  7. Buchan AMJ, Polak JM (1980) The classification of the human gastroentero-pancreatic endocrine cells. Invest Cell Pathol 3:51–71Google Scholar
  8. Buchan AMJ, Polak JM, Solcia E, Pearse AGE (1979) Localisation of intestinal gastrin a distinct endocrine cell type. Nature 277:138–140Google Scholar
  9. Buffa R, Solovieva I, Fiocca R, Giorgino S, Rindi G, Solcia E, Mochizuchi T, Yanaihara C, Yanaihara N (1982) Localization of bombesin and GRP (gastrin releasing peptide) sequences in gut nerves or endocrine cells. Histochemistry 76:457–467Google Scholar
  10. Dimaline R, Vaillant C, Dockray GJ (1980) The use of regionspecific antibodies in the characterization and localization of vasoactive intestinal polypeptide-like substances in the rat gastrointestinal tract. Regul Pept 1:1–16Google Scholar
  11. Dubois MP, Billard R, Breton R, Peter RE (1979) Comparative distribution of somatostatin, LH-RH, neurophysin and α-endorphin in the rainbow trout: an immunocytological study. Gen Comp Endocrinol 37:220–232Google Scholar
  12. El-Salhy, M (1984) Immunocytochemical investigation of the gastro-entero-pancreatic (GEP) neurohormonal peptides in the pancreas and gastro-intestinal tract of the dogfish, Squalus acanthias. Histochemistry 80:193–205Google Scholar
  13. El-Salhy M, Grimelius L (1983) Immunocytochemical demonstration of polypeptide YY (PYY) in the gastrointestinal tract of the monkey, Macaca rhesus: a light and electron microscopic study. Biomed Res 4:289–294Google Scholar
  14. El-Salhy M, Wilander E, Abu-Sinna G (1982) The endocrine pancreas of anuran amphibians: a histological and immunocytochemical study. Biomed Res 3:579–589Google Scholar
  15. El-Salhy M, Grimelius L, Wilander E, Ryberg B, Terenius L, Lundberg JM, Tatemoto K (1983a) Immunocytochemical identification of polypeptide YY (PYY) cells in the human gastrointestinal tract. Histochemistry 77:15–23Google Scholar
  16. El-Salhy M, Wilander E, Juntti-Berggren L, Grimelius L (1983b) The distribution of ontogeny of polypeptide, YY (PYY) and pancreatic polypeptide (PP)-immunoreactive cells in the gastrointestinal tract of rat. Histochemistry 78:53–60Google Scholar
  17. Gersel DJ, Gingerich RL, Greider MH (1979) Regional distribution and concentration of pancreatic polypeptide in the human and canine pancreas. Diabetes 28:11–15Google Scholar
  18. Grimmelikhuijzen CJP (1983) FMRFamide immunoreactivity is generally occurring in the nervous systems of coelenterates. Histochemistry 78:361–381Google Scholar
  19. Grube D (1982) Die endokrinen Zellen des Verdauungsapparats. Klin Wochenschr 60:361–381Google Scholar
  20. Grube D, Weber E (1979) Corticotropin-lipotropin related peptides in the GEP-endocrine system of rat, dog and man. In: Miyoshi A (ed) Gut peptides, secretion, function and clinical aspects. Elsevier Biomedical Press, Amsterdam, pp 249–257Google Scholar
  21. Grube D, Weber E (1980) Immunoreactivities of gastrin (G-) cells. I. Dilution-dependent staining of G cells by antisera and nonimmune sera. Histochemistry 65:223–237Google Scholar
  22. Grube D, Voigt KH, Weber E (1978) Pancreatic glucagon cells contain endorphin-like, immunoreactivity. Histochemistry 59:75–79Google Scholar
  23. Heitz Ph, Polak JM, Timson CM, Pearse AGE (1976) Enterochromaffin cells as the endocrine source of gastrointestinal substance P. Histochemistry 49:343–347Google Scholar
  24. Heitz Ph, Kasper M, Krey F, Polak JM, Pearse AGE (1978) Immunoelectron cytochemical localization of motilin in human duodenal enterochromaffin cells. Gastroenterology 74:713–717Google Scholar
  25. Helmstaedter V, Taugner Ch, Feurle GE, Forssmann WG (1977) Localization of neurotensin-immunoreactive cells in the small intestine of man and various mammals. Histochemistry 53:35–42Google Scholar
  26. Holmgren S, Vaillant C, Dimaline R (1982) VIP-, substance P-, gastrin/CCK-, bombesin-, somatostatin- and glucagon-like immunoreactivities in the gut of the rainbow trout, Salmo gairdneri. Cell. Tissue Res 223:141–153Google Scholar
  27. Inokuchi H, Azuma T, Kawai K, Takeuchi Y, Sano Y, (1984) Serotonin immunohistochemistry reveals immature EC cells. Histochemistry 80:517–518Google Scholar
  28. Ito S, Takai K, Shibata A, Matsubara Y, Yanaihara N (1979) Met-enkephalin-immunoreactive cells in the human and canine pyloric antrum. Gen Comp Endocrinol 38:238–245Google Scholar
  29. Johnson DE, Torrence JL, Elde RP, Bauer GE, Noe BD, Fletcher DJ (1976) Immunohistochemical localization of somatostatin, insulin and glucagon in principal islets of the anglerfish (Lophilus americanus) and the channel catfish (Ictalurus punctata). Am J Anat 147:119–124Google Scholar
  30. Johnson DE, Noe BD, Bauer GE (1982) Pancreatic polypeptide (PP)-like immunoreactivity in the principal islets of the anglerfish (Lophius americanus) and the channel catfish (Ictalurus punctatus). Anat Rec 204:61–67Google Scholar
  31. Kaung HLC, Elde RP (1980) Distribution and morphometric quantitation of pancreatic endocrine cells in the frog Rana pipiens. Anat Rec 196:173–181Google Scholar
  32. Klein C, Noorden S van (1978) Use of immunocytochemical staining of somatostatin for correlative light and electron microscopic investigation of D cells in the pancreatic islet of Xiphophorus helleri (Teleostei). Cell Tissue Res 194:399–404Google Scholar
  33. Klein C, Noorden S van (1980) Pancreatic polypeptide (PP)- and glucagon cells in the pancreatic islet of Xiphophorus helleri H. (Teoleostei). Cell Tissue Res 205:187–198Google Scholar
  34. Lance V, Hamilton JW, Rouse JB, Kimmel JR, Pollock HG (1984) Isolation and characterization of reptilian insulin, glucagon and pancreatic polypeptide complete amino acid sequence of alligator (Alligator mississippiensis) insulin and pancreatic polypeptide. Gen Comp Endocrinol 55:112–124Google Scholar
  35. Langer M, Noorden S van, Polak JM, Pearse AGE (1979) Peptide hormone-like immunoreactivity in the gastrointestinal tract and endocrine pancreas of eleven teleost species. Cell Tissue Res 199:493–508Google Scholar
  36. Larsson LI, Stengaard-Pedersen K (1981) Enkephalin-Endorphin-related peptides in antropyloric gastrin cells. J Histochem 29:1088–1098Google Scholar
  37. Larsson LI, Polak JM, Buffa R, Sundler F, Solcia E (1979) On the immunocytochemical localization of the vasoactive intestinal polypeptide. J Histochem Cytochem 27:936–938Google Scholar
  38. Leduque P, Pacelin C, Dubois PM (1983) Immunocytochemical evidence for a substance related to the bovine pancreatic polypeptide-peptide YY group of peptides in the human fetal gastrointestinal tract. Reg Peptides 6:219–230Google Scholar
  39. Lehy T, Willems G (1976) Population kinetics of antral gastrin cells in the mouse. Gastroenterology 71:614–619Google Scholar
  40. Lehy T, Peranzi G, Cristina ML (1981) Correlative immunocytochemical and electron microscopic studies: identification of (entero)glucagon-, somatostatin- and pancreatic polypeptide-like-containing cells in human colon. Histochemistry 71:67–80Google Scholar
  41. Marks V, Morgan LM (1982) Gastrointestinal hormones. Mol Aspects Med 5:225–292Google Scholar
  42. McNeill DL, Brinn JE, Fletcher DJ (1984) An immunocytochemical study of the pancreatic islet system of the channel catfish. Anat Rec 209:381–384Google Scholar
  43. Noaillac-Depeyre J, Hollande E (1981) Evidence of somatostatin, gastrin and pancreatic polypeptide-like substances in the mucosa cells of the gut in fishes with and without stomach. Cell Tissue Res 216:193–203Google Scholar
  44. Noorden S van, Falkmer S (1980) Gut-islet endocrinology — some evolutionary aspects. Invest Cell Pathol 3:21–35Google Scholar
  45. Noorden S van, Patent GJ (1978) Localization of pancreatic polypeptide (PP)-like immunoreactivity in the pancreatic islets of some teleost fishes. Cell Tissue Res 188:521–525Google Scholar
  46. Noorden S van, Patent GJ (1978) Vasoactive intestinal polypeptide-like immunoreactivity in nerves of the pancreatic islet of the teleost fish, Gillichthys mirabilis. Cell Tissue Res 212:139–146Google Scholar
  47. Noorden S van, Polak JM (1980) Hormones of the alimentary tract. In: Barrington EJW (ed) Hormones and evolution. Academic Press, New York, pp 791–828Google Scholar
  48. Orci L, Baetens D, Ravazolla M, Stefan Y, Malaisse Lagae F (1976) Pancreatic polypeptide and glucagon: non-random distribution in pancreatic islets. Life Sci 19:1811–1816Google Scholar
  49. Orci L, Malaisse-Lagae F, Baetens D, Perrelet A (1978) Pancreatic polypeptide-rich regions in human pancreas. Lancet 2:1200–1201Google Scholar
  50. Pearse AGE (1972) Histochemistry. Theoretical and applied. Churchill Livingstone, Edinburgh London, p 1439Google Scholar
  51. Polak JM, Buchan AMJ (1979) Motilin immunocytochemical localisation indicates molecular heterogeneity or the existence of a motilin family. Gastroenterology 76:1065–1066Google Scholar
  52. Polak JM, Sullivan SM, Bloom SR, Facer P, Pearse AGE (1977) Enkephalin-like immunoreactivity in the human gastrointestinal tract. Lancet 1:972–974Google Scholar
  53. Price DA (1983) FMRFamide: assays and artifacts. In: Lever J, Boer HH (eds) Molluscan neuroendocrinology. North Holland, Amsterdam, pp 184–190Google Scholar
  54. Ravazolla M, Orci L (1980) A pancreatic polypeptide (PP)-like immunoreactant is present in the glicentin-containing cell of cat intestine. Histochemistry 67:221–224Google Scholar
  55. Read JB, Burnstock G (1968) Fluorescent histochemical studies on the mucosa of the vertebrate gastrointestinal tract. Histochemic 16:324–332Google Scholar
  56. Reifel CW, Marin-Sorensen M, Samlof IM (1983) Gastrin immunoreactive cells in the gastrointestinal tracts from four species of fish. Can J Zool 61:1464–1468Google Scholar
  57. Reinecke M, Almasan K, Carraway RE, Helmstaedter V, Forssmann WB (1980a) Distribution patterns of neurotensin-like immunoreactive cells in the gastrointestinal tract of higher vertebrates. Cell Tissue Res 205:383–395Google Scholar
  58. Reinecke M, Carraway RE, Falkmer S, Feurle GE, Forssmann WG (1980b) Occurrence of neurotensin-immunoreactive cells in the digestive tract of lower vertebrates and deuterostomian invertebrates. A correlated immunohistochemical and radioimmunochemical study. Cell Tissue Res 212:173–183Google Scholar
  59. Reinecke M, Schlüter P, Yanaihara N, Forssmann WG (1981) VIP-immunoreactivity in enteric nerves and endocrine cells of the vertebrate gut. Peptides 2: (Suppl 2):149–156Google Scholar
  60. Rombout JHWM (1977) Enteroendocrine cells in the digestive tract of Barbus conchonius (Teleostei, Cyprinidae). Cell Tissue Res 185:435–450Google Scholar
  61. Rombout JHWM, Reinecke M (1984) Immunohistochemical localization of (neuro-)peptide hormones in endocrine cells and nerves of the gut of a stomachless teleost fish, Barbus conchonius (Cyprinidae). Cell Tissue Res 237:57–65Google Scholar
  62. Rombout JHWM, Taverne-Thiele JJ (1982) An immunocytochemical and electronmicroscopical study of endocrine cells in the gut and pancreas of a stomachless teleost fish, Barbus conchonius (Cyprinidae). Cell Tissue Res 227:577–593Google Scholar
  63. Rombout JHWM, Rademakers LHPM, Hees JP van (1979) Pancreatic endocrine cells of Barbus conchonius (Teleostei, Cyprinidae) and their relation to the enteroendocrine cells. Cell Tissue Res 203:9–23Google Scholar
  64. Schooneveld H, Tesser GI, Veenstra JA, Romberg-Privee HM (1983) Adipokinetic hormone and AKH-like peptide demonstrated in the corpora cardiaca and nervous system of Locusta migratoria by immunocytochemistry. Cell Tissue Res 230:67–76Google Scholar
  65. Schooneveld H, Romberg-Privee HM, Veenstra JA (1986) Immunocytochemical differentiation between adipokinetic hormone (AKH)-like peptides in neurons and glandular cells in the corpus cardiacum of Locusta migratoria and Periplaneta americana with C-terminal and N-terminal specific antisera to AKH. Cell Tissue Res 243:9–14Google Scholar
  66. Seino Y, Porte D, Smith PH (1979) Immunohistochemical localization of somatostatin-containing cells in the intestinal tract: a comparative study. Gen Comp Endocrinol 38:229–233Google Scholar
  67. Sjölund K, Ekelund M, Hakanson R, Moody AJ, Sundler F (1983a) Gastric inhibitory peptide-like immunoreactivity in glucagon and glicentin cells: properties and orgin. An immunocytochemical study using several antisera. J Histochem Cytochem 31:811–817Google Scholar
  68. Sjölund K, Sandén G, Håkanson R, Sundler F (1983b) Endocrine cells in human intestine: an immunocytochemical study. Gastroenterology 85:1120–1130Google Scholar
  69. Sokolski KN, Lechago J (1984) Human colonic substance P-producing cells and a separate population from the serotonin-producing enterochromaffin cells. J Histochem Cytochem 32:1066–1074Google Scholar
  70. Solcia E, Buffa R, Capella C, Fiocca R, Fontana P, Crivelii O (1979) Immunohistochemical characterization of gastroenteropancreatic endocrine cells and related multihormonal cells problems, pitfalls and facts. In: Miyoshi A (ed) Gut peptides, secretion, function and clinical aspects. Elsevier Biomedical Press, Amsterdam, pp 303–309Google Scholar
  71. Solcia E, Capella C, Buffa R, Usellini L, Fiocca R, Sessa F (1981) Endocrine cells of the digestive system. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven Press, New York, pp 39–58Google Scholar
  72. Sorenson RL, Sasek CA, Elde RP (1984) Phe-Met-Arg-Phe-amide (FMRF-NH2) inhibits insulin and somatostatin secretion and anti-FMRF-NH2 sera dectects pancreatic polypeptide cells in the rat islets. Peptides 5:777–782Google Scholar
  73. Stefan Y, Falkmer S (1980) Identification of four endocrine cell types in the pancreas of Cottus scorpius (Teleostei) by immunofluorescence and electron microscopy. Gen Comp Endocrinol 42:171–178Google Scholar
  74. Stefan Y, Dufour C, Falkmer S (1978) Mise en evidence par immunofluorescence de cellules a polypeptide pancreatique (PP) dans le pancreas et le tube digestif de poissons osseux et cartilagineux. CR Acad Sci D 286:1073–1075Google Scholar
  75. Sternberger LA (1979) Immunohistochemistry. John Wiley and Sons, New YorkGoogle Scholar
  76. Sundler F, Alumets J, Håkanson R (1977) 5-Hydroxytryptamine-containing enterochromaffin cells: storage site of substance P. Acta Physiol Scand (Suppl) 452:121Google Scholar
  77. Sundler F, Sjölund K, Håkanson R (1983) Gut endocrine cells-an overview. Upsala J Med Sci 39:17–32Google Scholar
  78. Sundler F, Böttcher G, Håkanson R, Schwartz TW (1984) Immunocytochemical localisation of the icosapeptide fragment of the PP precursor: a marker for ‘true’ PP cells? Regul Pep 8:217–224Google Scholar
  79. Tobe T, Yamahiro A, Manabe T, Noguchi M, Akaji K, Yajima H (1982) Gastrin releasing peptide (GRP) in the human stomach. Acta Histochem Cytochem 15:102–107Google Scholar
  80. Tsutsumi Y (1984) Immunohistochemical studies on glucagon, glicentin and pancreatic polypeptide in human stomach: normal and pathological conditions. Histochem J 16:869–883Google Scholar
  81. Triepel J, Grimmelikhuijzen CJP (1984a) A critical examination of the occurrence of FMRFamide immunoreactivity in the brain of guinea pig and rat. Histochemistry 80:63–71Google Scholar
  82. Triepel J, Grimmelikhuijzen CJP (1984b) Mapping of neurons in the central nervous system of the guinea pig by use of antisera specific to the molluscan neuropeptide FMRFamide. Cell Tissue Res 237:575–586Google Scholar
  83. Usellini L (1982) Ultrastructural localization of pancreatic polypeptide (PP)-like-immunoreactivity in the glicentin-containing (L cell) of human large intestine. Caryologia 35:110Google Scholar
  84. Usellini L, Buchan AMJ, Polak JM, Capella C, Cornaggia M, Solcia E (1984) Ultrastructural localization of motilin in endocrine cells of human and dog intestine by immunogold technique. Histochemistry 81:363–368Google Scholar
  85. Vaillant C, Taylor IL (1984) Demonstration of carboxylterminal PP-like peptides in endocrine cells and nerves. Peptides 2:31–35Google Scholar
  86. Veenstra JA (1984) Immunocytochemical demonstration of a homology in peptidergic neurosecretory cells in the suboesophageal ganglion of a beetle and a locust with antisera to bovine pancreatic polypeptide, FMRFamide, vasopressin and α-MSH. Neurosci Lett 48:185–190Google Scholar
  87. Veenstra JA, Schooneveld H (1984) Immunocytochemical localization of neurons in the nervous system of the Colorado potato beetle with antisera against FMRFamide and bovine polypeptide. Cell Tissue Res 235:303–308Google Scholar
  88. Wagner GF, McKeown BA (1981) Immunocytochemical localisation of hormone producing cells within the pancreatic islets of the rainbow trout (Salmo gairdneri). Cell Tissue Res 221:181–192Google Scholar
  89. Yoshida K, Iwanaga T, Fujita T (1983) Gastro-Entero-Pancreatic (GEP) endocrine system of the flatfish, Paralichtys olivaceus: an immunocytochemical study. Arch Histol Jpn 46:259–266Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • I. H. W. M. Rombout
    • 1
  • C. P. M. van der Grinten
    • 1
  • F. M. Peeze Binkhorst
    • 1
  • J. J. Taverne-Thiele
    • 1
  • H. Schooneveld
    • 2
  1. 1.Department of Experimental Animal Morphology and Cell BiologyAgricultural UniversityWageningenThe Netherlands
  2. 2.Department of EntomologyAgricultural UniversityWageningenThe Netherlands

Personalised recommendations