The Histochemical Journal

, Volume 27, Issue 3, pp 231–239 | Cite as

A comparison of membrane enzymes of human and pig oesophagus; the pig oesophagus is a good model for studies of the gullet in man

  • K. N. Christie
  • C. Thomson
  • D. Hopwood


The distribution and relative catalytic activities of five plasma membrane enzymes (alkaline phosphatase, dipeptidyl peptidase IV, γ-glutamyl transpeptidase, microsomal alanyl aminopeptidase and glutamyl aminopeptidase) were examined in human and pig oesophagus. In both species, alkaline phosphatase activity occurred in basal and suprabasal cells of the epithelium and in capillaries. Stromal cells in the human submucosa were particularly reactive. Dipeptidyl peptidase IV was present in blood vessels and capillaries in man and pig and in submucous glands in the pig. The enzyme was also present in both species in the lamina propria cells immediately adjacent to the epithelial basal lamina. In the human, γ-glutamyl transpeptidase occurred in the epithelial basal cells and in isolated basal and lower prickle cells in the pig. Stromal cells in the human submucosa were strongly reactive and capillaries in the muscularis propria in both species moderately active. Microsomal alanyl aminopeptidase was detected in lamina propria cells adjacent to the epithelial basal cell layer in man and pig and at the apices of mucous cells in pig submucous glands. Weak glutamyl aminopeptidase activity was confined to capillaries in both species. The findings of this study, along with the ready availability of pig oesophagus, suggest that the pig may be a suitable model for studies of the gullet in man.


Alkaline Phosphatase Activity Muscularis Propria Mucous Cell Dipeptidyl Peptidase Membrane Enzyme 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ahmad,S.,Linhong,W. &Ward,P. E. (1992) Dipeptidyl (amino) peptidase IV and aminopeptidase M metabolize circulating substance Pin vivo. J. Pharmacol. Exp. Ther.260, 1257–61.PubMedGoogle Scholar
  2. Boyce,S. T. (1994) Epidermis as a secretory tissue.J. Invest. Dermatol. 102, 8–10.CrossRefPubMedGoogle Scholar
  3. Braverman,I. M. &Yen,A. (1977) Ultrastructure of the human dermal circulation. II. The capillary loops of the dermal papillae.J. Invest. Dermatol. 68, 44–52.PubMedGoogle Scholar
  4. Brown,C. M.,Snowdon,C. F.,Slee,B.,Sandle,L. N. &Rees,W. D. W. (1993) Measurement of bicarbonate output from the intact human oesophagus.Gut 34, 872–80.PubMedGoogle Scholar
  5. Clemente,G.,Manni,R.,Vecchio,F. M.,Rizzo,S.,Furgiuele,S.,Perrotti,P. &Crucitti,F. (1990) Effect of different fractions of alkaline reflux on the gastric stump and the oesophagus: an experimental research on pigs.J. Surg. Res. 48, 121–6.PubMedGoogle Scholar
  6. Dobson, H., Pignatelli, M., Hopwood, D. &D'Arrigo, C. (1994) Cell adhesion molecules in oesophageal epithelium.Gut 34, (in press).Google Scholar
  7. Frey,A.,Meckelein,B.,Weiler-Guettler,H.,Moeckel,B.,Flach,R. &Gassen,H. G. (1991) Pericytes of brain microvasculature express γ-glutamyl transpeptidase.Eur. J. Biochem. 202, 421–9.CrossRefPubMedGoogle Scholar
  8. Fukasawa,K. M.,Fukasawa,K.,Sahara,N.,Harada,M.,Kondo,Y. &Nagatsu,I. (1981) Immunohisto-chemical localization of dipeptidyl aminopeptidase IV in rat kidney, liver and salivary glands.J. Histochem. Cytochem. 29, 337–43.PubMedGoogle Scholar
  9. Gossrau,R. (1979) Peptidasen II. Zur Lokalisation der dipeptidyl peptidase IV (DPPIV). Histochemische und biochemische untersuchung.Histochemistry 60, 231–48.CrossRefPubMedGoogle Scholar
  10. Gossrau,R. (1981) Investigation of proteinases in the digestive tract using 4-methoxy-2-naphthylamide (MNA) substrates.J. Histochem. Cytochem. 29, 464–80.PubMedGoogle Scholar
  11. Griffith,O. W.,Bridges,R. J. &Meister,A. (1979) Transport of γ-glutamyl amino acids: role of glutathione and γ-glutamyl transpeptidase.Proc. Natl Acad. Sci. USA 76, 6319–22.PubMedGoogle Scholar
  12. Hamilton,B. H. &Orlando,R. C. (1989) In vivo alkaline secretion by mammalian esophagus.Gastroenterology 97, 640–8.PubMedGoogle Scholar
  13. Hamilton,S. R. &Smith,R. L. (1987) The relationship between columnar lined epithelial dysplasia and invasive adenocarcinoma arising in Barrett's esophagus.Am. J. Clin. Pathol. 87, 301–12.PubMedGoogle Scholar
  14. Hatier,R.,Malprade,D.,Sabolovic,N. &Grignon,C. (1991) Gamma glutamyl transpeptidase activity in the epididymis during fetal and postnatal development in rats.Arch. Androl. 27, 185–95.PubMedGoogle Scholar
  15. Heymann,E.,Erlanson-Albertsson,C.,Mentlein,R.,Nausch,J.,Scholz,W.,Struckhoff,G. &Yoshimoto,T. (1990) Dipeptidyl peptidase IV (DPPIV, EC as an enzyme of the plasma membrane.Beitr. Wirkstofforschung 38, 22–37.Google Scholar
  16. Hopwood,D.,Milne,G.,Jankowski,J.,Howat,K.,Johnston,D. &Wormsley,K. G. (1994) Secretory and absorptive activity of oesophageal epithelium: evidence of circulating mucosubstances.Histochem. J. 26, 41–9.CrossRefPubMedGoogle Scholar
  17. Hopwood,D.,Ross,P. E. &Bouchier,I. A. D. (1981) Reflux oesophagitis.Clin. Gastroenterol. 10, 505–20.PubMedGoogle Scholar
  18. Ismail-Beigi,F.,Horton,P. F. &Pope,C. E. (1970) Histological consequences of gastroesophageal reflux in man.Gastroenterology 58, 163–74.PubMedGoogle Scholar
  19. Jaeger,L. A. &Lamar,C. H. (1992) Immunolocalization of epidermal growth factor (EGF) and EFG receptors in the porcine upper gastrointestinal tract.Am. J. Vet. Res. 53, 1685–92.PubMedGoogle Scholar
  20. Jankowski,J. (1993) Gene expression in Barrett's mucosa: acute and chronic adaptive responses in the oesophagus.Gut 34, 1649–50.PubMedGoogle Scholar
  21. Jankowski,J.,Hopwood,D. &Wormsley,K. G. (1993) Expression of epidermal growth factor, transforming growth factor alpha and their receptors in gastroesophageal disease.Dig. Dis. 11, 1–11.PubMedGoogle Scholar
  22. Jubb,K. V. F.,Kennedy,P. C.,Palmer,N. (eds) (1991)Pathology of Domestic Animals, Vol 2, London: Academic Press.Google Scholar
  23. Lojda,Z., (1979) Studies on dipeptidyl(amino)peptidase IV (glycl-proline naphthylamidase). II Blood vessels.Histochemistry 59, 153–66.CrossRefPubMedGoogle Scholar
  24. Lojda,Z. &Frič,P. (1992) Brush border enzymes in colorectal adenomas and carcinomas.Histochem. J. 24, 292–3.Google Scholar
  25. Lojda,Z.,Gossrau,R. &Schiebler,T. H. (eds) (1979)Enzyme Histochemistry. Berlin:. Springer-Verlag.Google Scholar
  26. Mcdonald,J. K. &Barrett,A. J. (1986)Mammalian Proteases: a Glossary and Bibliography, Vol 2,Exopeptidases. London: Academic Press.Google Scholar
  27. Meister,A., (1973) Enzymology of amino acid transport.Science 180, 33–9.PubMedGoogle Scholar
  28. Millán,J. L. (1990) Oncodevelopmental alkaline phosphatases: in search for a function.Prog. Clin. Biol. Res. 344, 453–75.PubMedGoogle Scholar
  29. Orlando,R. C.,Powell,D. W. &Carney,C. N. (1981) Pathophysiology of acute acid injury in rabbit esophageal epithelium.J. Clin. Invest. 68, 286–93.PubMedGoogle Scholar
  30. Rabito,C. A.,Kreisberg,J. I. &Wight,D. (1984) Alkaline phosphatase and γ-glutamyl transpeptidase as polarization markers during the organization of LLC-PK1 cells into an epithelial cell membrane.J. Cell. Biol. 259, 574–82.Google Scholar
  31. Ryrfeldt,A.,Norbeck,K.,Reiland,S. &Moldeus,P. (1990) Drug induced esophageal lesions studiedin vitro.Acta Physiol. Scand. (suppl.) 592, 73–82.Google Scholar
  32. Sarosiek,J.,Hetzel,D. P.,Yu,Z.,Piascik,R.,Li,L.,Rourk,R. M. &Mccallum,R. W. (1993) Evidence on secretion of epidermal growth factor by the esophageal mucosa in humans.Am. J. Gastroenterol. 88, 1081–7.PubMedGoogle Scholar
  33. Schwint,A. E.,Collet,A. M.,Mendez,A. E.,Cabrini,R. L. &Itoiz,M. E. (1992) The first normal oral mucosa epithelium in which γ-glutamyl transpeptidase activity has been detected.Histochem. J. 24, 964–8.CrossRefPubMedGoogle Scholar
  34. Stefanovic,V.,Vlahovic,P.,Ardaillon,N. &Ardaillon,R. (1991) Receptor-mediated induction of aminopeptidase A (APA) of human glomeular epithelial cells.Febs Lett. 294, 171–4.CrossRefPubMedGoogle Scholar
  35. Stoward,P. J. &Pearse,A. G. E. (eds) (1991)Histochemistry Theoretical and Applied, Vol 3, Edinburgh: Churchill Livingstone.Google Scholar
  36. Tobey,N. A. &Orlando,R. C. (1991) Mechanisms of acid injury to rabbit esophageal epithelium.Gastroenterology 101, 1220–8.PubMedGoogle Scholar
  37. Tobey,N. A.,Powell,D. W.,Scheiner,V. J. &Orlando,R. C. (1989) Serosal bicarbonate protects against acid injury to rabbit esophagus.Gastroenterology 96, 1466–77.PubMedGoogle Scholar
  38. Vina,J. R.,Blay,P.,Ramirez,A.,Castells,A. &Vina,J. (1990) Inhibition of γ-glutamyl transpeptidase decreases amino acid uptake in human keratinocyctes in culture.Febs Lett. 269, 86–8.PubMedGoogle Scholar
  39. Wang,L.,Ahmad,S.,Benter,I.,Ibrahim,F.,Chow,A.,Mizutani,S. &Ward,P. E. (1991) Differential processing of substance P and neurokinin A by plasma dipeptidyl (amino) peptidase IV, aminopeptidase M and angiotensin converting enzyme.Peptides (Lafayette, N.Y.) 12, 1357–64.Google Scholar
  40. Winters,C.,Spurling,T. J.,Chobanian,S. J.,Curtis,D. J. &Esposito,R. L. (1987). Barrett's esophagus: a prevalent occult complication of gastro-esophageal reflux disease.Gastroenterology 92, 118–24.PubMedGoogle Scholar
  41. Wright,J. W.,Amir,H. Z.,Murray,C. E.,Roberts,K. A.,Harding,J. W.,Mizutani,S. &Ward,P. E. (1991) Use of aminopeptidase M as a hypotensive agent in spontaneously hypertensive rats.Brain Res. Bull. 27, 545–51.CrossRefPubMedGoogle Scholar
  42. Xu,Y. H.,Campbell,H. A.,Sattler,G. L.,Hendrick,S.,Maronpot,R.,Sato,K. &Pitot,H. C. (1990) Quantitative stereological analysis of the effects of age and sex on multistage hepatocarcinogenesis in the rat by use of four cytochemical markers.Cancer Res.,50, 472–9.PubMedGoogle Scholar

Copyright information

© Chapman & Hall 1995

Authors and Affiliations

  • K. N. Christie
    • 1
  • C. Thomson
    • 1
  • D. Hopwood
    • 2
  1. 1.Department of Anatomy & PhysiologyUniversity of DundeeDundeeUK
  2. 2.Department of PathologyUniversity of DundeeDundeeUK

Personalised recommendations