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Structure and histochemistry of the normal intestine of the fowl. I. The mature absorptive cell

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The fine structure and cytochemistry of the intestinal epithelial cell of the fowl have been investigated. The fine structure of the mature absorptive cell of the fowl duodenum was very similar to that described for man and other mammals. Minor differences were the thinner microvillous glycocalyx, the unusual length of the cells and their microvilli, and the wide distribution of lysosomal bodies. The membrane-associated enzymes alkaline phosphatase, ATPase (pH 7.2) and leucine naphthylamidase were mainly associated with the brush border; this organelle also gave positive reactions for mucopolysaccharides and phospholipids. No enzyme activities were found in the terminal web.

The distribution of lysosomes between the terminal web and the Golgi apparatus was correlated with the granular localization of the lysosomal enzymes acid phosphatase, β-glucuronidase and non-specific esterase. The mitochondrial enzyme succinate dehydrogenase was seen to be localized in rod-like dots which marked the distribution of mitochondria in the absorptive cell. The localization of mitochondrial ATPase (pH 9.4) was not clearly demonstrated because of diffusion artifacts. The region of the Golgi apparatus gave a strong reaction for thiamine pyrophosphatase, together with weak reactions for acid and alkaline phosphatases after extensive overincubation.

The endoplasmic reticulum-associated enzymes glucose-6-phosphatase and nonspecific esterase were distributed throughout the absorptive cell, with a maximum activity apical to the Golgi apparatus. Additionally, the jejunal absorptive cells showed endoplasmic reticulum-as well as lysosomal-associated β-glucuronidase.

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References

  • Allen, J. M. &Slater, J. J. (1961). A cytochemical study of Golgi-associated thiamine pyrophosphatase in the epididymis of the mouse.J. Histochem. Cytochem. 9, 418–23.

    Google Scholar 

  • Ashworth, C. T., Luibel, F. J. &Stewart, S. G. (1963). The fine structural localization of adenosine triphosphatase in the small intestine, kidney and liver of the rat.J. Cell Biol. 17, 1–18.

    Google Scholar 

  • Baker, J. R. (1946). The histochemical recognition of lipine.Q. Jl. microsc. Sci. 87, 441–70.

    Google Scholar 

  • Bancroft, J. D. (1967).An Introduction to Histochemical Technique. London: Butterworths.

    Google Scholar 

  • Barka, T. (1960). A simple azo-dye method for histochemical demonstration of acid phosphatase.Nature (Lond.) 187, 248–9.

    Google Scholar 

  • Barka, T. (1964). Electron histochemical localization of acid phosphatase activity in the small intestine of mouse.J. Histochem. Cytochem. 12, 229–38.

    Google Scholar 

  • Barka, T. &Anderson, P. J. (1963).Histochemistry. Theory, Practice and Bibliography. New York, London: Harper & Row.

    Google Scholar 

  • Barrett, A. J. (1969). Properties of lysosomal enzymes, in:Lysosomes in Biology and Pathology, Vol. 2 (eds. J. T. Dingle & H. B. Fell), pp. 245–312. Amsterdam: North-Holland.

    Google Scholar 

  • Barrnett, R. J. &Seligman, A. M. (1952). Histochemical demonstration of protein-bound sulfhydryl groups.Science 116, 323–7.

    Google Scholar 

  • Barrnett, R. J. &Seligman, A. M. (1954) Histochemical demonstration of sulfhydryl and disulfide groups of protein.J. natn. Cancer Inst. 14, 769–804.

    Google Scholar 

  • Baxter-Grillo, D. L. (1969). Enzyme histochemistry and hormones of the developing gastrointestinal tract of the chick embryo. I. A histochemical and quantitative study of glycogen, uridine diphosphate glucose-glycogen transglucosylase, glucose-6-phosphatase and phosphorylase.Histochemie 19, 31–43.

    Google Scholar 

  • Baxter-Grillo, D. L. (1970). Enzyme histochemistry and hormones of the developing gastro-intestinal tract of the chick embryo. IV. The enzyme activity during functional differentiation.Histochemie 21, 268–76.

    Google Scholar 

  • Berg, G. G. &Chapman, B. (1965). The sodium and potassium activated ATPase of intestinal epithelium. I. Location and enzymatic activity in the cell.J. Cell comp. Physiol. 65, 361–72.

    Google Scholar 

  • Burstone, M. S. (1957a). Polyvinyl pyrrolidone as a mounting medium for fat stains and azo-dye procedures.Am. J. clin. Path. 28, 429–39.

    Google Scholar 

  • Burstone, M. S. (1957b). Polyvinyl acetate as a mounting medium for azo-dye procedures.J. Histochem. Cytochem. 5, 196.

    Google Scholar 

  • Burstone, M. S. (1958). Histochemical comparison of naphthol AS-phosphates for the demonstration of phosphatases.J. natn. Cancer Inst. 20, 601–13.

    Google Scholar 

  • Chiquoine, A. D. (1955). Further studies on the histochemistry of glucose-6-phosphatase.J. Histochem. Cytochem. 3, 471–8.

    Google Scholar 

  • Davies, B. J. &Ornstein, L. (1959). High resolution enzyme localization with a new diazo reagent ‘Hexazonium Pararosanilin’.J. Histochem. Cytochem. 7, 297–8.

    Google Scholar 

  • Deane, H. W. &Dempsey, E. W. (1945). The localisation of phosphatases in the Golgi region of intestinal and other cells.Anat. Rec. 93, 401–17.

    Google Scholar 

  • Einarson, L. (1951). On the theory of gallocyanin-Chromalum staining and its application for quantitative estimation of basophilia. A selective staining of exquisite progressivity.Acta path. microbiol. scand 28, 82–102.

    Google Scholar 

  • Feulgen, R. &Rossenbeck, H. (1924). Microskopisch-Chemischen Nachweis einer Nukleinsäure von Typus der Thymonucleinsaure und die darauf beruhende elektive Färbung von Zellkernen in microskopischen Präparaten.Z. physiol. Chem. 135, 203–48.

    Google Scholar 

  • Fishman, W. H., Goldman, S. S. &De, Lellis, R. (1967). Dual localisation of β-glucuronidase in endoplasmic reticulum and in lysosomes.Nature (Lond.) 213, 457–60.

    Google Scholar 

  • Floch, M. H., van Noorden, S. &Spiro, H. M. (1967). Histochemical localisation of gastric and small bowel mucosal enzymes of man, monkey and chimpanzee.Gastroenterology 52, 230–8.

    Google Scholar 

  • Forstner, G. G. (1969). Surface sugar in the intestine.Am. J. med. Sci. 258, 172–80.

    Google Scholar 

  • Fredricsson, B. (1956). Alkaline phosphatase in the Golgi substance of intestinal epithelium.Expl. Cell Res. 10, 63–5.

    Google Scholar 

  • Goldfischer, S., Essner, E. &Novikoff, A. B. (1964). The localisation of phosphatase activities at the level of ultrastructure.J. Histochem. Cytochem. 12, 72–95.

    Google Scholar 

  • Gomori, G. (1950). Sources of error in enzymatic histochemistry.J. lab. clin. Med. 35, 802–9.

    Google Scholar 

  • Grey, R. D. &Le Count, T. S. (1970). Distribution of leucine naphthylamidase and alkaline phosphatase on the villi of the chick duodenum.J. Histochem. Cytochem. 18, 416–23.

    Google Scholar 

  • Hayashi, M., Nakajima, Y. &Fishman, W. H. (1964). The cytologic demonstration of β-glucuronidase employing naphthol AS-BI glucuronide and hexazonium pararosanilin; a preliminary report.J. Histochem. Cytochem. 12, 293–7.

    Google Scholar 

  • Himes, M. &Moriber, L. (1956). A triple stain for Deoxyribonucleic acid, polysaccharides and proteins.Stain Technol. 31, 67–70.

    Google Scholar 

  • Holt, S. J. (1954). A new approach to the cytochemical localisation of enzymes.Proc. Roy. Soc. B. 142, 160–9.

    Google Scholar 

  • Holt, S. J. (1963). Some observations on the occurrence and nature of esterases in lysosomes in:Lysosomes, Ciba Foundation Symposium (eds. A. V. S. De Reuck & M. P. Cameron), pp. 114–25. London: Churchill.

    Google Scholar 

  • Holt, J. H. &Miller, D. (1962). The localisation of phosphomonoesterase and aminopeptidase in brush borders isolated from intestinal epithelial cells.Biochem. biophys. Acta 58, 239–43.

    Google Scholar 

  • Hugon, J. S. &Borgers, M. (1966). Ultrastructural localisation of alkaline phosphatase activity in the absorbing cells of the duodenum of the mouse.J. Histochem. Cytochem. 14, 629–40.

    Google Scholar 

  • Hugon, J. S. &Borgers, M. (1968). Fine structural localisation of acid and alkaline phosphatase activities in the absorbing cells of the duodenum of rodents.Histochemie 12, 42–66.

    Google Scholar 

  • Hugon, J. S. &Borgers, M. (1969). Localisation of acid and alkaline phosphatase activities in the duodenum of the chick.Acta histochem. 34 349–59.

    Google Scholar 

  • Hugon, J. S., Borgers, M. &Maestracci, D (1970). Glucose-6-phosphatase and thiamine pyrophosphatase activities in the jejunal epithelium of the mouse.J. Histochem. Cytochem. 18, 361–4.

    Google Scholar 

  • Ito, S. & Revel, J. P. (1966). Autoradiography of intestinal epithelial cells.Proc. 6th Internat. Congr. Electron Microscopy, p. 585.

  • Jervis, H. R. (1963). Enzymes in the mucosa of the small intestine of the rat, the guinea-pig and the rabbit.J. Histochem. Cytochem. II, 692–9.

    Google Scholar 

  • Karnovsky, M. J. (1965). A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy.J. Cell Biol. 27, 137A-38A.

    Google Scholar 

  • Kurnick, N. B. (1955). Histochemistry of nucleic acids.Int. Rev. Cytol. 4, 221–86.

    Google Scholar 

  • Lev, R. &Spicer, S. S. (1964). Specific staining of sulphate groups with Alcian Blue at low pH.J. Histochem. Cytochem. 12, 309.

    Google Scholar 

  • Lillie, R. D. &Ashburn, L. L. (1943). Supersaturated solutions of fat stains in dilute isopropanol for demonstration of acute fatty degeneration not shown by Herzheimer technique.Arch. Path. 36, 432–5.

    Google Scholar 

  • Lison, L. & Dagnelie, J. (1935). Quoted by Bancroft (1967).

  • Maestracci, D. & Hugon, J. S. (1970). Mouse intestinal glucose-6-phosphatase (G-6-Pase): localisation, adaptation.Proc. Can. Fed. Biol. Soc. June 1970, 631.

  • Mcgadey, J. (1970). A tetrazolium method for non-specific alkaline phosphatase.Histochemie 23, 180–4.

    Google Scholar 

  • McManus, J. F. A. (1946). Histological demonstration of mucin after periodic acid.Nature (Lond.) 158, 202.

    Google Scholar 

  • Michael, E. (1972). Histochemical studies on intestinal coccidiosis of the fowl.Ph.D. thesis, University of London.

  • Moog, F. (1944). Localisation of alkaline and acid phosphatase in the early embryogenesis of the chick.Biol. Bull. 86, 51–80.

    Google Scholar 

  • Moog, F. (1950). The functional differentiation of the small intestine. I. The accumulation of alkaline phosphomonoesterase in the duodenum of the chick.J. exp. Zool. 115, 109–26.

    Google Scholar 

  • Moog, F. (1961). The functional differentiation of the small intestine. IX. The influence of thyroid function on cellular differentiation and accumulation of alkaline phosphatase in the duodenum of the chick embryo.Gen. comp. Endocr. I, 416–32.

    Google Scholar 

  • Mowry, R. W. (1963). The 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 combinations with the periodic acid-Schiff reaction.Ann. N.Y. Acad. Sci. 106, 402–23.

    Google Scholar 

  • Nachlas, M. M., Crawford, D. T., &Seligman, A. M. (1957). The histochemical demonstration of leucine aminopeptidase.J. Histochem. Cytochem. 5, 264–78.

    Google Scholar 

  • Nachlas, M. M., Monis, B., Rosenblatt, D. &Seligman, A. M. (1960). Improvement in the histochemical localisation of leucine aminopeptidase with a new substrate, L-leucyl-4-methoxy-2-naphthylamide.J. biophys. biochem. Cytol. 7, 261–4.

    Google Scholar 

  • Nordstrom, C., Dhalquist, A. &Josefsson, L. (1968). Quantitative determination of enzymes in different parts of the villi and crypts of rat small intestine. Comparison of alkaline phosphatase, disaccharidases and dipeptidases.J. Histochem. Cytochem. 15, 713–21.

    Google Scholar 

  • Novikoff, A. B., Essner, E., Goldfischer, S. &Heus, M. (1962). Nucleoside phosphatase activities of cyto-membranes. In:The Interpretation of Ultrastructure (ed., R. J. C. Harris),Symp. Intl. Soc. Cell Biol., Vol. 1, pp. 149–92. New York: Academic Press.

    Google Scholar 

  • Overton, J. &Shoup, J. (1964). Fine structure of cell surface specialiations in the maturing duodenal mucosa of the chick.J. Cell Biol. 21, 75–85.

    Google Scholar 

  • Padykula, H. A. &Herman, E. (1955a) Factors affecting the activity of adenosine triphosphatase and other phosphatases as measured by histochemical techniques.J. Histochem. Cytochem. 3, 161–9.

    Google Scholar 

  • Padykula, H. A. &Herman, E. (1955b). The specificity of the histochemical method for adenosine triphosphatase.J. Histochem. Cytochem. 3 170–95.

    Google Scholar 

  • Padykula, H. A., Strauss, E. W., Ladman, A. J. &Gardner, F. H. (1961). A morphologic and histochemical analysis of the human jejunal epithelium in non-tropic sprue.Gastroenterology 40, 735–65.

    Google Scholar 

  • Pearse, A. G. E. (1960).Histochemistry, Theoretical and Applied, 2nd Edn. London: Churchill.

    Google Scholar 

  • Pearse, A. G. E. (1968).Histochemistry, Theoretical and Applied, 3rd Edn. Vol. I. London: Churchill.

    Google Scholar 

  • Pearse, A. G. E. &Riecken, E. O. (1967). Histology and cytochemistry of the cells of the small intestine in relation to absorption.Br. med. Bull. 23, 217–22.

    Google Scholar 

  • Persijn, J. P., Daems, W. T., Derman, J. C. H. &Merjer, A. E. F. H. (1961). The demonstration of adenosine triphosphatase activity with the electron microscope.Histochemie 2, 372–82.

    Google Scholar 

  • Reynolds, F. S. (1963). The use of lead citrate at high pH as an electron opaque stain in electron microscopy.J. Cell Biol. 17, 208–13.

    Google Scholar 

  • Rhodes, J. B., Eichholz, A. &Crane, R. K. (1967). Studies on the organisation of the brush border in intestinal epithelial cells. IV. Aminopeptidase activity in microvillous membranes of hamster intestinal brush borders.Biochim. biophys. Acta 135, 959–65.

    Google Scholar 

  • Riecken, E. O. (1970). Histochemistry of the small intestine in various malabsorption states. In:Modern Trends in Gastroenterology Vol. 4 (eds. W. I. Card & B. Creamer), pp. 20–41. London: Butterworths.

    Google Scholar 

  • Riecken, E. O., Stewart, J. S., Booth C. C. &Pearse, A. G. E. (1966). A histochemical study on the role of lysosomal enzymes in idiopathic steatorrhoea before and during a gluten-free diet.Gut 7, 317–32.

    Google Scholar 

  • Shnitka, T. K. (1960). Enzymatic histochemistry of gastrointestinal mucous membrane.Fedn. Proc. 19, 897–904.

    Google Scholar 

  • Siekewitz, P., Low, H., Ernster, L. &Lindberg, O. (1958). On a possible mechanism of the adenosine triphosphatase of liver mitochondria.Biochim. biophys. Acta 29, 378–91.

    Google Scholar 

  • Spicer, S. S. (1960). A correlative study of the histochemical properties of rodent acid mucopolysaccharides.J. Histochem. Cytochem. 8, 18–35.

    Google Scholar 

  • Taylor, C. B. (1962). Cation-stimulation of an ATPase system from the intestinal mucosa of the guinea pig.Biochem. biophys. Acta 60, 437–40.

    Google Scholar 

  • Thompson, S. W. (1966).Selected Histochemical and Histopathological Methods. Springfield, Illinois: Thomas.

    Google Scholar 

  • Toner, P. G. (1968). Cytology of intestinal epithelial cells.Int. Rev. Cytol. 24, 233–343.

    Google Scholar 

  • Vanha-Perttula, T., Hopsu, V. K., Sonninen, V. &Glenner, G. G. (1965). Cathepsin C activity as related to some histochemical substrates.Histochemie 5, 170–81.

    Google Scholar 

  • Van Lanker, J. L. &Lentz, P. L. (1970). Study on the site of biosynthesis of β-glucuronidase and its appearance in lysosomes in normal and hypoxic rats.J. Histochem. Cytochem. 18, 529–41.

    Google Scholar 

  • Wachstein, M. &Meisel, E. (1956). On the histochemical demonstration of glucose-6-phosphatase.J. Histochem. Cytochem. 4, 592.

    Google Scholar 

  • Wachstein, M., Meisel, E. &Niedzwiedz, A. (1960). Histochemical demonstration of mitochondrial adenosine triphosphatase with the lead adenosine triphosphate technique.J. Histochem. Cytochem. 8, 387–8.

    Google Scholar 

  • Warren, L. &Spicer, S. S. (1961). Biochemical and histochemical identification of sialic acid containing mucins of rodent vagina and salivary glands.J. Histochem. Cytochem. 9, 400–8.

    Google Scholar 

  • Webster, H. L. &Harrison, D. D. (1969). Enzymatic activities during the transformation of crypts to columnar intestinal cells.Expl. Cell Res. 56, 245–53.

    Google Scholar 

  • Yasuma, A. &Itchikawa, T. (1953). Ninhydrin-Schiff and Alloxan-Schiff staining.Lab. clin. Med. 41, 296–9.

    Google Scholar 

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  1. Wye College, University of London, Wye, Ashford, Kent

    E. Michael & R. D. Hodges

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Michael, E., Hodges, R.D. Structure and histochemistry of the normal intestine of the fowl. I. The mature absorptive cell. Histochem J 5, 313–333 (1973). https://doi.org/10.1007/BF01004800

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