Skip to main content
Log in

Histochemical studies of epithelial cell glycoproteins in normal rat colon

  • Papers
  • Published:
The Histochemical Journal Aims and scope Submit manuscript

Summary

Two general classes of glycoproteins have been identified in the colonic epithelial cells of the Sprague Dawley rat. Glycoproteins belonging to the first of these classes contain sialic acids both with and without side chaino-acyl substituents, abundanto-sulphate ester and ‘neutral sugars’ (hexose, 6-deoxyhexose or N-acetyl hexosamine residues) with oxidisablevicinal diols and are located in the goblet cells of the descending colon and in goblet cells populating the upper halves of the crypts of the ascending colon. In the descending colon, the sulphosialoglycoproteins in the goblet cells in the base of the crypts contain sialic acids without side chaino-acyl substituents. It appears that as these cells migrate up the crypts, there iso-acylation of the side chains of the sialic acids of the glycoproteins and an increase in the quantity of ‘neutral sugars’ without a corresponding increase in sialic acid. Glycoproteins with similar properties to those of the goblet cells of the upper halves of the crypts of the descending colon, but containing less sulphate, are found in the goblet cells of the upper half of the crypts of the ascending colon. The second general class of glycoproteins contain sialic acids all, or almost all of which, are substituted at position C8 and only relatively small quantities of sulphate. They are located in the mucous cells of the descending colon, the deep crypt secretory cells of the ascending colon and the columnar absorptive cell brush border. Glycoproteins of all three types contain neutral sugars but the periodate oxidation of those in the mucous cells is apparently prevented by the presence of ano-acyl ester substituent(s) located on theirvicinal diol(s). Such sugars have not previously been identified in mammalian epithelial glycoproteins; their presence, together with that of 8-o-acyl sialic acids, would account for the observed lack of PAS reactivity of the mucous cell glycoproteins.

We propose that (i) there are two general biosynthetic sequences for colonic epithelial cell glycoproteins and (ii) the primary function of 8-o-acyl sialoglycoproteins is protective while that of the sulphated species is lubrication.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • ALTMANN, G. G. (1983) Morphological observations on mucus-secreting nongoblet cells in the deep crypts of rat ascending colon.Amer. J. Anat. 167 95–117.

    PubMed  Google Scholar 

  • AL-SUHAIL, A. A., REID, P.E., CULLING, C. F. A., DUNN, W. L. & CLAY, M.G. (1984) Studies of the degraded carrageen-induced colitis of rabbits I. Changes in the epithelial glycoproteino-acylated sialic acids associated with ulceration.Histochem. J. 16 543–53.

    PubMed  Google Scholar 

  • BARGER, J. D. & DELAMATER E. D. (1948) The use of thionyl chloride in the preparation of Schiff reagent.Science 108 121–2.

    Google Scholar 

  • CHANG, W. W. L. & LEBLOND C. P. (1971) Renewal of the epithelium in the descending colon of the mouse I. Presence of three cell populations: vacuolated — columnar, mucous and argentaffin.Amer. J. Anat. 131 73–100.

    PubMed  Google Scholar 

  • CULLING, C. F. A. (1974)Handbook of Histopathological and Histochemical Technique, 3rd ed. pp. 211–20 London, Butterworth.

    Google Scholar 

  • CULLING, C. F. A., REID, P. E. & DUNN, W. L. (1971) The effect of saponification upon certain histochemical reactions of the epithelial mucins of the G.I. tract.J. Histochem. Cytochem. 19 654–62.

    PubMed  Google Scholar 

  • CULLING, C. F. A., REID, P. E., DUNN, W. L. & CLAY, M. G. (1974) The histochemical demonstration ofo-acylated sialic acids in gastrointestinal mucins: their association with the potassium hydroxide-periodic acid — Schiff effect.J. Histochem. 22 826–31.

    PubMed  Google Scholar 

  • DECAENS, C., BARA, J., ROSA, B., DAHER, N. & BURTIN, P. (1983) Early oncofetal antigenic modifications during rat colonic carcinogenesis.Cancer Res. 43 355–62.

    PubMed  Google Scholar 

  • ESSNER, E., SHREIBER, J. & GRIEUSKI, R. A. (1978) Localization of carbohydrate components in rat colon with fluoresceinated lectins.J. Histochem. Cytochem. 26 452–8.

    PubMed  Google Scholar 

  • FAILLARD, H. & SCHAUER, R. (1972) Glycoproteins as lubricants, protective agents, carriers, structural proteins and as participants in other functions. In: Glycoproteins. Their composition, structure and function (edited by GOTTESCHALK, A.) Vol. 5 pp. 1256–67. Amsterdam, London, New York: Elsevier.

    Google Scholar 

  • FILIPE, M. I. (1975) Mucous secretion in rat colonic mucosa during carcinogenous induced by DMH. A morphological and histochemical study.Br. J. Cancer 32 60–77.

    PubMed  Google Scholar 

  • FLOREY, H. (1955) Mucin and protection in the body.Proc. R. Soc. Lond. Biol. Series B143 147–59.

    Google Scholar 

  • FORSTNER, J. F. (1978) Intestinal mucus in health and disease.Digestion 17 234–63.

    PubMed  Google Scholar 

  • FREEMAN, H. J., LOTAN, H. & KIM, Y. S. (1980) Application of lectins for detection of goblet cell glycoconjugate differences in proximal and distal colon of the rat.Lab. Invest. 42 405–12.

    PubMed  Google Scholar 

  • HOSKINS, L. C. (1978) Degradation of mucus glycoproteins in the gastrointestinal tract. In:The Glycoconjugates (edited by HOROVITZ, M. I. & PIGMAN, W.) Vol. II pp. 235–53. New York, San Francisco, London: Academic Press.

    Google Scholar 

  • KENT, P. W. (1962) The chemistry of mucoproteins: an introduction to gastrointestinal mucus.Gastroent. 43 292–302.

    Google Scholar 

  • LILLIE, R. D. & PIZZOLATO, P. (1972) Histochemical use of borohydrides as aldehyde blocking reagents.Stain Technol. 43 13–6.

    Google Scholar 

  • MOWRY, R. W. (1963) Special value of methods that colour both acidic and vicinal hydroxyl groups in the histochemical study of mucins. With revised directions for the colloidal iron stain, the use of Alcian Blue 8GX and their combination with the periodic acid-Schiff reaction.Ann. N. Y. Acad. Sci. 106 402–23.

    Google Scholar 

  • PARK, C. M., REID, P. E., WALKER, D. C. & MACPHERSON, B. R. (1987a) A simple practical ‘swiss’ roll method of preparing tissues for paraffin and methacrylate embedding.J. Microsc. 145 115–20.

    PubMed  Google Scholar 

  • PARK, C. M., REID, P. E., OWEN, D. A., DUNN, W. L. & VOLZ, D. (1987b) Histochemical procedures for the simultaneous visualization of neutral sugars and either sialic acid and itso-acyl variants oro-sulphates ester II. Methods based upon the periodic acid-phenylhydrazine method.Histochem. J. 19 257–63.

    PubMed  Google Scholar 

  • POON, H., REID, P. E., RAMEY, C. W. & DUNN, W. L. (1983) Removal ofo-acylated sialic acids from rat colonic epithelial glycoproteins by cell-free extracts of rat faeces.Can. J. Biochem. 61 868–74.

    Google Scholar 

  • REID, P. E., CULLING, C. F. A. & DUNN, W. L. (1973). Saponification—induced increase in the periodic acid-Schiff reaction in the gastrointestinal tract: mechanism and distribution of the reactive substance.J. Histochem. Cytochem. 21 473–82.

    PubMed  Google Scholar 

  • REID, P. E., CULLING, C. F. A. & DUNN, W. L. (1974) The histochemical interpretation of the complex results of methylation upon gastrointestinal tract mucins with special reference to the periodic acid-Schiff reactivity.J. Histochem. Cytochem. 22 986–91.

    PubMed  Google Scholar 

  • REID, P. E., CULLING, C. F. A., DUNN, W. L., RAMEY, C. W. & CLAY, M. G. (1985) Differences in chemical composition between the epithelial glycoproteins of the upper and lower halves of rat colon.Can. J. Biochem. 53 1328–32.

    Google Scholar 

  • REID, P. E., CULLING, C. F. A., RAMEY, C. W., DUNN, W. L. & CLAY, M. G. (1977) A simple method for the determination of theo-acetyl substitution pattern of the sialic acids of colonic epithelial glycoprotein.Can. J. Biochem. 55 493–503.

    PubMed  Google Scholar 

  • REID, P. E., CULLING, C. F. A., DUNN, W. L., RAMEY, C. W., MAGIL, A. B. & CLAY, M. G. (1980) Differences between theo-acetylated sialic acids of the epithelial mucins of human colonic tumours and normal controls.J. Histochem. Cytochem. 27 217–22.

    Google Scholar 

  • REID, P. E., DUNN, W. L., RAMEY, C. W., CORET, E., TRUEMAN, L. & CLAY, M. G. (1984a) Histochemical identification of side chain substituted O-acylated sialic acids: The PAT-KOH-Bh-PAS and the PAPT-KOH-Bh-PAS procedures.Histochem. J. 16 623–39.

    PubMed  Google Scholar 

  • REID, P. E., CULLING, C. F. A., DUNN, W. L., RAMEY, C. W. & CLAY, M. G. (1984b) Chemical and histochemical studies of normal and diseased human gastrointestinal tract I. A comparison between histologically normal colon, colonic tumours, ulcerative colitis and diverticular disease of the colon.Histochem. J. 16 235–51.

    PubMed  Google Scholar 

  • REID, P. E., OWEN, D. A., RAMEY, C. W., DUNN, W.L., CLAY, M. G. & JONES E. A. (1985a) Histochemical procedures for the simultaneous visualization of sialic acid, its side chaino-acyl variants ando-sulphate ester.Histochem. J. 17 113–17.

    PubMed  Google Scholar 

  • REID, P. E., OWEN, D. A., RAMEY, C. W., DUNN, W. L., JONES, E. A., LAZOSKY, D. A., ALLEN, E., PARK, C. M. & CLAY, M. G. (1985b) Chemical and histochemical studies of normal and diseased human gastrointestinal tract V. A differential diagnostic method for the histochemical classification of glycoproteins.Histochem. J. 17 891–903.

    PubMed  Google Scholar 

  • SHAMSUDDIN, A. K. M. & TRUMP, B. F. (1981) Colon epithelium I. Light microscopic, histochemical and ultrastructural features of normal colon epithelium of male Fischer 344 rats.J. Natl. Cancer Inst. 66 375–88.

    PubMed  Google Scholar 

  • SHEAHAN, D. G. & JERVIS, H. R. (1976) Comparative histochemistry of gastrointestinal mucosubstances.Am. J. Anat. 146 103–32.

    PubMed  Google Scholar 

  • SLOMIANY, B. L., MURTY, V. L. N. & SLOMIANY, A. (1980) Isolation and characterization of oligosaccharides from rat colonic mucus glycoprotein.J. Biol. Chem. 255 9719–23.

    PubMed  Google Scholar 

  • SPICER, S. S. (1960) A correlative study of the histochemical properties of rodent acid mucopolysaccharides.J. Histochem. Cytochem. 8 18–33.

    PubMed  Google Scholar 

  • SPICER, S. S. (1965) Diamine methods for differentiating mucosubstances histochemically.J. Histochem. 13 211–34.

    PubMed  Google Scholar 

  • THOMOPOULOS, G. N., SCHULTE, B. A. & SPICER, S. S. (1983). Light and electron microscopic cytochemistry of glycoconjugates in the rectosigmoid colonic epithelium of the mouse and rat.Amer. J. Anat. 168 239–56.

    PubMed  Google Scholar 

  • TSUYAMA, S., SUZUKI, S. & MURATA, F. (1983) The histochemical differences of intestinal gland epithelial in the rat colon with special reference to their glycoconjugates.Acta Histochem. Cytochem. 16 456–71.

    Google Scholar 

  • VAN DUIN (1956) A histochemical specific thionine-SO3 reagent and its use in a bi-colour method for deoxyribonucleic acid and periodic acid Schiff positive substance.J. Histochem. Cytochem. 4 55–63.

    PubMed  Google Scholar 

  • VOLZ, D., REID, P. E., PARK, C. M., OWEN, D. A. & DUNN, W. L. (1987a) A new method for the selective periodate oxidation of total tissue sialic acids.Histochem. J. 19 311–18.

    PubMed  Google Scholar 

  • VOLZ, D., REID, P. E., PARK, C. M., OWEN, D. A. & DUNN, W. L. (1987b) Histochemical procedures for the simultaneous visualisation of neutral sugars and either sialic acid and its side chaino-acyl variants oro-sulphate ester I. Methods based upon the selective periodate oxidation of sialic acids.Histochem. J. 19 249–56.

    PubMed  Google Scholar 

  • WETZEL, M. G., WETZEL, B. K. & SPICER, S. S. (1966) Ultrastructural localization of acid mucosubstances in the mouse colon with iron-containing stains.J. Cell. Biol. 30 299–315.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Park, C.M., Reid, P.E., Owen, D.A. et al. Histochemical studies of epithelial cell glycoproteins in normal rat colon. Histochem J 19, 546–554 (1987). https://doi.org/10.1007/BF01687362

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01687362

Keywords

Navigation