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

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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.

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References

  • 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 80:487–491

    Google Scholar 

  • Alumets J, Håkanson R, Sundler F, Chang KJ (1978) Leu-enkephalin-like material in nerves and enterochromaffin cells in the gut. Histochemistry 56:187–196

    Google Scholar 

  • Baetens D, Malaisse-Lagae F, Perrelet A, Orci L (1979) Endocrine pancreas: three dimensional reconstruction shows two types of islets of Langerhans. Science 206:1323–1325

    Google Scholar 

  • 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 78:5899–5902

    Google Scholar 

  • Bonner-Weir S, Bonner GC (1979) The organization of the endocrine pancreas: a hypothetical unifying view of the phylogenetic differences. Gen Comp Endocrinol 38:28–37

    Google Scholar 

  • 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 8:261–266

    Google Scholar 

  • Buchan AMJ, Polak JM (1980) The classification of the human gastroentero-pancreatic endocrine cells. Invest Cell Pathol 3:51–71

    Google Scholar 

  • Buchan AMJ, Polak JM, Solcia E, Pearse AGE (1979) Localisation of intestinal gastrin a distinct endocrine cell type. Nature 277:138–140

    Google Scholar 

  • 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 76:457–467

    Google Scholar 

  • 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 1:1–16

    Google Scholar 

  • 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 37:220–232

    Google Scholar 

  • 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 80:193–205

    Google Scholar 

  • 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 4:289–294

    Google Scholar 

  • El-Salhy M, Wilander E, Abu-Sinna G (1982) The endocrine pancreas of anuran amphibians: a histological and immunocytochemical study. Biomed Res 3:579–589

    Google Scholar 

  • 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 77:15–23

    Google Scholar 

  • 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 78:53–60

    Google Scholar 

  • Gersel DJ, Gingerich RL, Greider MH (1979) Regional distribution and concentration of pancreatic polypeptide in the human and canine pancreas. Diabetes 28:11–15

    Google Scholar 

  • Grimmelikhuijzen CJP (1983) FMRFamide immunoreactivity is generally occurring in the nervous systems of coelenterates. Histochemistry 78:361–381

    Google Scholar 

  • Grube D (1982) Die endokrinen Zellen des Verdauungsapparats. Klin Wochenschr 60:361–381

    Google Scholar 

  • 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 249–257

    Google Scholar 

  • Grube D, Weber E (1980) Immunoreactivities of gastrin (G-) cells. I. Dilution-dependent staining of G cells by antisera and nonimmune sera. Histochemistry 65:223–237

    Google Scholar 

  • Grube D, Voigt KH, Weber E (1978) Pancreatic glucagon cells contain endorphin-like, immunoreactivity. Histochemistry 59:75–79

    Google Scholar 

  • Heitz Ph, Polak JM, Timson CM, Pearse AGE (1976) Enterochromaffin cells as the endocrine source of gastrointestinal substance P. Histochemistry 49:343–347

    Google Scholar 

  • Heitz Ph, Kasper M, Krey F, Polak JM, Pearse AGE (1978) Immunoelectron cytochemical localization of motilin in human duodenal enterochromaffin cells. Gastroenterology 74:713–717

    Google Scholar 

  • Helmstaedter V, Taugner Ch, Feurle GE, Forssmann WG (1977) Localization of neurotensin-immunoreactive cells in the small intestine of man and various mammals. Histochemistry 53:35–42

    Google Scholar 

  • 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 223:141–153

    Google Scholar 

  • Inokuchi H, Azuma T, Kawai K, Takeuchi Y, Sano Y, (1984) Serotonin immunohistochemistry reveals immature EC cells. Histochemistry 80:517–518

    Google Scholar 

  • 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 38:238–245

    Google Scholar 

  • 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 147:119–124

    Google Scholar 

  • 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 204:61–67

    Google Scholar 

  • Kaung HLC, Elde RP (1980) Distribution and morphometric quantitation of pancreatic endocrine cells in the frog Rana pipiens. Anat Rec 196:173–181

    Google Scholar 

  • 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 194:399–404

    Google Scholar 

  • Klein C, Noorden S van (1980) Pancreatic polypeptide (PP)- and glucagon cells in the pancreatic islet of Xiphophorus helleri H. (Teoleostei). Cell Tissue Res 205:187–198

    Google Scholar 

  • 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 55:112–124

    Google Scholar 

  • 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 199:493–508

    Google Scholar 

  • Larsson LI, Stengaard-Pedersen K (1981) Enkephalin-Endorphin-related peptides in antropyloric gastrin cells. J Histochem 29:1088–1098

    Google Scholar 

  • Larsson LI, Polak JM, Buffa R, Sundler F, Solcia E (1979) On the immunocytochemical localization of the vasoactive intestinal polypeptide. J Histochem Cytochem 27:936–938

    Google Scholar 

  • 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 6:219–230

    Google Scholar 

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

    Google Scholar 

  • 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 71:67–80

    Google Scholar 

  • Marks V, Morgan LM (1982) Gastrointestinal hormones. Mol Aspects Med 5:225–292

    Google Scholar 

  • McNeill DL, Brinn JE, Fletcher DJ (1984) An immunocytochemical study of the pancreatic islet system of the channel catfish. Anat Rec 209:381–384

    Google Scholar 

  • 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 216:193–203

    Google Scholar 

  • Noorden S van, Falkmer S (1980) Gut-islet endocrinology — some evolutionary aspects. Invest Cell Pathol 3:21–35

    Google Scholar 

  • Noorden S van, Patent GJ (1978) Localization of pancreatic polypeptide (PP)-like immunoreactivity in the pancreatic islets of some teleost fishes. Cell Tissue Res 188:521–525

    Google Scholar 

  • 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 212:139–146

    Google Scholar 

  • Noorden S van, Polak JM (1980) Hormones of the alimentary tract. In: Barrington EJW (ed) Hormones and evolution. Academic Press, New York, pp 791–828

    Google Scholar 

  • Orci L, Baetens D, Ravazolla M, Stefan Y, Malaisse Lagae F (1976) Pancreatic polypeptide and glucagon: non-random distribution in pancreatic islets. Life Sci 19:1811–1816

    Google Scholar 

  • Orci L, Malaisse-Lagae F, Baetens D, Perrelet A (1978) Pancreatic polypeptide-rich regions in human pancreas. Lancet 2:1200–1201

    Google Scholar 

  • Pearse AGE (1972) Histochemistry. Theoretical and applied. Churchill Livingstone, Edinburgh London, p 1439

    Google Scholar 

  • Polak JM, Buchan AMJ (1979) Motilin immunocytochemical localisation indicates molecular heterogeneity or the existence of a motilin family. Gastroenterology 76:1065–1066

    Google Scholar 

  • Polak JM, Sullivan SM, Bloom SR, Facer P, Pearse AGE (1977) Enkephalin-like immunoreactivity in the human gastrointestinal tract. Lancet 1:972–974

    Google Scholar 

  • Price DA (1983) FMRFamide: assays and artifacts. In: Lever J, Boer HH (eds) Molluscan neuroendocrinology. North Holland, Amsterdam, pp 184–190

    Google Scholar 

  • Ravazolla M, Orci L (1980) A pancreatic polypeptide (PP)-like immunoreactant is present in the glicentin-containing cell of cat intestine. Histochemistry 67:221–224

    Google Scholar 

  • Read JB, Burnstock G (1968) Fluorescent histochemical studies on the mucosa of the vertebrate gastrointestinal tract. Histochemic 16:324–332

    Google Scholar 

  • Reifel CW, Marin-Sorensen M, Samlof IM (1983) Gastrin immunoreactive cells in the gastrointestinal tracts from four species of fish. Can J Zool 61:1464–1468

    Google Scholar 

  • 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 205:383–395

    Google Scholar 

  • 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 212:173–183

    Google Scholar 

  • 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):149–156

    Google Scholar 

  • Rombout JHWM (1977) Enteroendocrine cells in the digestive tract of Barbus conchonius (Teleostei, Cyprinidae). Cell Tissue Res 185:435–450

    Google Scholar 

  • 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 237:57–65

    Google Scholar 

  • 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 227:577–593

    Google Scholar 

  • 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 203:9–23

    Google Scholar 

  • 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 230:67–76

    Google Scholar 

  • 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 243:9–14

    Google Scholar 

  • Seino Y, Porte D, Smith PH (1979) Immunohistochemical localization of somatostatin-containing cells in the intestinal tract: a comparative study. Gen Comp Endocrinol 38:229–233

    Google Scholar 

  • 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 31:811–817

    Google Scholar 

  • Sjölund K, Sandén G, Håkanson R, Sundler F (1983b) Endocrine cells in human intestine: an immunocytochemical study. Gastroenterology 85:1120–1130

    Google Scholar 

  • Sokolski KN, Lechago J (1984) Human colonic substance P-producing cells and a separate population from the serotonin-producing enterochromaffin cells. J Histochem Cytochem 32:1066–1074

    Google Scholar 

  • 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 303–309

    Google Scholar 

  • 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 39–58

    Google Scholar 

  • 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 5:777–782

    Google Scholar 

  • 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 42:171–178

    Google Scholar 

  • 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 286:1073–1075

    Google Scholar 

  • Sternberger LA (1979) Immunohistochemistry. John Wiley and Sons, New York

    Google Scholar 

  • Sundler F, Alumets J, Håkanson R (1977) 5-Hydroxytryptamine-containing enterochromaffin cells: storage site of substance P. Acta Physiol Scand (Suppl) 452:121

    Google Scholar 

  • Sundler F, Sjölund K, Håkanson R (1983) Gut endocrine cells-an overview. Upsala J Med Sci 39:17–32

    Google Scholar 

  • 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 8:217–224

    Google Scholar 

  • Tobe T, Yamahiro A, Manabe T, Noguchi M, Akaji K, Yajima H (1982) Gastrin releasing peptide (GRP) in the human stomach. Acta Histochem Cytochem 15:102–107

    Google Scholar 

  • Tsutsumi Y (1984) Immunohistochemical studies on glucagon, glicentin and pancreatic polypeptide in human stomach: normal and pathological conditions. Histochem J 16:869–883

    Google Scholar 

  • Triepel J, Grimmelikhuijzen CJP (1984a) A critical examination of the occurrence of FMRFamide immunoreactivity in the brain of guinea pig and rat. Histochemistry 80:63–71

    Google Scholar 

  • 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 237:575–586

    Google Scholar 

  • Usellini L (1982) Ultrastructural localization of pancreatic polypeptide (PP)-like-immunoreactivity in the glicentin-containing (L cell) of human large intestine. Caryologia 35:110

    Google Scholar 

  • 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 81:363–368

    Google Scholar 

  • Vaillant C, Taylor IL (1984) Demonstration of carboxylterminal PP-like peptides in endocrine cells and nerves. Peptides 2:31–35

    Google Scholar 

  • 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 48:185–190

    Google Scholar 

  • 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 235:303–308

    Google Scholar 

  • Wagner GF, McKeown BA (1981) Immunocytochemical localisation of hormone producing cells within the pancreatic islets of the rainbow trout (Salmo gairdneri). Cell Tissue Res 221:181–192

    Google Scholar 

  • Yoshida K, Iwanaga T, Fujita T (1983) Gastro-Entero-Pancreatic (GEP) endocrine system of the flatfish, Paralichtys olivaceus: an immunocytochemical study. Arch Histol Jpn 46:259–266

    Google Scholar 

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In honour of Prof. P. van Duijn

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Rombout, I.H.W.M., van der Grinten, C.P.M., Peeze Binkhorst, F.M. et al. Immunocytochemical identification and localization of peptide hormones in the gastro-entero-pancreatic (GEP) endocrine system of the mouse and a stomachless fish, Barbus conchonius . Histochemistry 84, 471–483 (1986). https://doi.org/10.1007/BF00482980

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