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Ontogeny of sulphated glycoconjugate-producing cells in the rat fundic gland

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The ontogeny of sulphated glycoconjugate-producing cells in the rat fundic gland has been studied using high iron diamine (HID), Alcian Blue (AB) at pH 1.0, high iron diamine in combination with Alcian Blue at pH 2.5 (HID-AB), cationic colloidal gold (CCG) at pH 1.0 under light microscopy and CCG (1.0), HID-thiocarbohydrazide (TCH)-silver proteinate (SP)-physical development (PD) under electron microscopy. From day 19.5 of gestation, sulphated glycoconjugate-producing cells were discernible under both light and electron microscopy. The development of such cells can be classified into four stages: (1) a prenatal period from day 19.5 of gestation extending to 0.5 days after birth; (2) 1 day to 2 weeks after birth; (3) 2 to 4 weeks after birth; and (4) the final period from 4 to 8 weeks after birth. Glycoconjugate-producing cells reached maturity by 4 weeks after birth. Our results indicated that glycoconjugate-producing cells were cells along the wall of foveolar lumen, but not those covering the gastric mucosa surface. Our results also suggested that thetrans totransmost Golgi apparatus lamellae were the sites of sulphation in the developing rat stomach.

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References

  • Albedi, F.M., Cassano, A.M., Ciaralli, F., Taruscio, D. &Donelli, G. (1989) Ultrastructural identification of sulphated glycoconjugates in the Golgi apparatus in human colonic absorptive cells.Histochemistry 92, 73–9.

    Article  CAS  Google Scholar 

  • Carlemalm, E., Garavito, R.M. &Villiger, W. (1982) Resin development for electron microscopy and an analysis of embedding at low temperature.J. Microscopy 126, 123–43.

    CAS  Google Scholar 

  • Danon, D., Goldstein, L., Marikovsky, Y. &Skutelsky, E. (1972) Use of cationized ferritin as a label of negative charges on cell surface.J. Ultrastruct. Res. 38, 500–10.

    Article  CAS  PubMed  Google Scholar 

  • Falk, P., Roth, K. A. &Gordon, J. I. (1994) Lectins are sensitive tools for defining the differentiation programs of mouse gut epithelial cell lineages.Am. J. Physiol. 266 G987-G1003.

    CAS  PubMed  Google Scholar 

  • Fischer, J., Klein, P. J., Vierbuchen, M., Skutta, B., Uhlenbruck, G. &Fischer, R. (1984a) Characterization of glycoconjugates of human gastrointestinal mucosa by lectins. I. Histochemical distribution of lectin binding sites in normal alimentary tract as well as in benign and malignant gastric neoplasms.J. Histochem. Cytochem. 32, 681–9.

    CAS  PubMed  Google Scholar 

  • Fischer, J., Vierbuchen, M., Klein, P. J., Uhlenbruck, G. &Fischer, R. (1984b) Characterization of glycoconjugates of human gastrointestinal mucosa by lectins. II Lectin binding to the isolated glycoproteins of normal and malignant gastric mucosa.J. Histochem. Cytochem. 32, 690–6.

    CAS  PubMed  Google Scholar 

  • Häkkinen, I., Järvi, O. &Grönroos, J. (1968) Sulphoglycoprotein antigens in the human alimentary canal and gastric cancer. An immunohistological study.Int. J. Cancer,3, 572–81.

    PubMed  Google Scholar 

  • Helander, H. F. (1969) Ultrastructure and function of gastric mucoid and zymogen cells in the rat during development.Gastroenterology,56, 53–70.

    CAS  PubMed  Google Scholar 

  • Helander, H. F. (1981) The cells of the gastric mucosa.Int. Rev. Cytol. 70, 217–89.

    CAS  PubMed  Google Scholar 

  • Ihida, K., Suganuma, T., Tsuyama, S. &Murata, F. (1988) Glycoconjugate histochemistry of the rat fundic gland usingGriffonia simplicifolia agglutinin II during development.Am. J. Anat. 182, 250–6.

    Article  CAS  PubMed  Google Scholar 

  • Ihida, K., Tsuyama, S., Kashio, N. &Murata, F. (1991) Subcompartment sugar residues of gastric surface mucous cells studied with labelled lectins.Histochemistry 95, 329–35.

    Article  CAS  PubMed  Google Scholar 

  • Irimura, T., Wynn, D. M., Hager, L. G., Cleary, K. R. &Ota, D. M. (1991) Human colonic sulfomucin identified by a specific monoclonal antibody.Cancer Res. 51, 5728–35.

    CAS  PubMed  Google Scholar 

  • Ito, M., Takata, K., Saito, S., Aoyagi, T. &Hirano, H. (1985) Lectin-binding pattern in normal human gastric mucosa. A light and electron microscopic study.Histochemistry 83, 189–93.

    Article  CAS  PubMed  Google Scholar 

  • Ito, S. &Winchester, R. J. (1963) The fine structure of the gastric mucosa in the bat.J. Cell Biol. 16, 541–77.

    Article  CAS  PubMed  Google Scholar 

  • Kantani-Matsumoto, A. &Kataoka, K. (1989) A carbohydrate histochemical study on surface mucous cells, mucous neck cells and chief cells in the gastric mucosa of developing mice.Arch. Histol. Cytol. 52, 37–50.

    CAS  PubMed  Google Scholar 

  • Karam, S. M. &Leblond, C. P. (1992) Identifying and counting epithelial cell types in the ‘corpus’ of the mouse stomach.Anat. Rec. 232, 231–46.

    Article  CAS  PubMed  Google Scholar 

  • Karam, S. M. &Leblond, C. P. (1993) Dynamics of epithelial cells in the corpus of the mouse stomach, II Outward migration of pit cells.Anat. Rec. 236, 280–96.

    CAS  PubMed  Google Scholar 

  • Kashio, N., Tsuyama, S., Ihida, K. &Murata, F. (1992) Cationic colloidal gold-a probe for light- and electron-microscopic characterization of acidic glycoconjugates using poly-l-lysing gold complex.Histochem. J. 24, 419–30.

    Article  CAS  PubMed  Google Scholar 

  • Kataoka, K., Sakano, Y. &Miura, J. (1984) Histogenesis of the mouse gastric mucosa, with special reference to type and distribution of proliferative cells.Arch. Histol. Jpn 47, 459–74.

    CAS  PubMed  Google Scholar 

  • Kaufman, M. H. (1992)The Atlas of Mouse Development, p. 8. London: Academic Press.

    Google Scholar 

  • Kitamura, H. (1990) Diamine-thiocarbohydrazide-silver proteinate development methods for the histochemical detection of acidic glycoconjugates in electron microscopy.Acta. Histochem. Cytochem. 23, 281–94.

    Google Scholar 

  • Kogaya, Y. &Nanci, A. (1992) Post-embedding staining with high-iron diamine-thiocarbohydrazide-silver proteinate and its application to visualizing sulfated glycoconjugates in cryofixed kidney and cartilage.J. Histochem. Cytochem. 40, 1257–67.

    CAS  PubMed  Google Scholar 

  • Kramer, M. F., Geuze, J. J. &Strous, G. J. A. M. (1978) Site of synthesis, intracellular transport and secretion of glycoprotein in exocrine cells.Ciba Found. Symp. 57, 25–51.

    Google Scholar 

  • Lane, N., Caro, L., Otero-Vilardebó, L. R. &Godman, G. C. (1964) On the site of sulfation in colonic goblet cells.J. Cell Biol. 21, 339–51.

    Article  CAS  PubMed  Google Scholar 

  • Murata, F., Yoshida, K., Ohno, S. &Nagata, T. (1979) Mucosubstances of rabbit granulocytes studied by means of electron-microscopic radioautography and X-ray microanalysis.Histochemistry 61, 139–50.

    Article  CAS  PubMed  Google Scholar 

  • Murata, F., Suganuma, T., Tsuyama, S., Suzuki, S. &Enokizono, N. (1984) A simplified embedding method of Lowicryl K4M and lectin colloidal gold staining (in Japanese).Igaku no ayumi 131, 669–71.

    Google Scholar 

  • Murata, F., Tsuyama, S., Ihida, K., Kashio, N., Kawano, M. &Zeng, Z. L. (1992) Sulfated glycoconjugates demonstrated in combination with high iron diamine thiocarbohydrazide-silver proteinate and silver acetate physical development.J. Electron Microsc. 41, 14–20.

    CAS  Google Scholar 

  • Ohe, Y., Hinoda, Y., Irimura, T., Imai, K. &Yachi, A. (1994) Expression of sulfated carbohydrate chains detected by monoclonal antibody 91.9H in human gastric cancer tissues.Cancer Res. 85, 400–8.

    CAS  Google Scholar 

  • Parmley, R. T., Eguchi, M., Spicer, S. S., Alvarez, C. J. &Austin, R. L. (1980) Ultrastructural cytochemistry and radioautography of complex carbohydrates in heterophil granulocytes from rabbit bone marrow.J. Histochem Cytochem. 28, 1067–80.

    CAS  PubMed  Google Scholar 

  • Rademacher, T. W., Parekh, R. B. &Dwek, R. A. (1988) Glycobiology.Ann. Rev. Biochem. 57, 785–838.

    CAS  PubMed  Google Scholar 

  • Rios-Martin, J. J., Diaz-Cano, S. J. &Rivera-Hueto, F. (1993) Ultrastructural distribution of lectin-binding sites on gastric superficial mucous-secreting epithelial cells. The role of Golgi apparatus in the initial glycosylation.Histochemistry 99, 181–9.

    CAS  PubMed  Google Scholar 

  • Sannes, P. L., Spicer, S. S. &Katsuyama, T. (1979) Ultrastructural localization of sulfated complex carbohydrates with a modified iron diamine procedure.J. Histochem. Cytochem. 27, 1108–11.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Skutelsky, E. &Roth, J. (1986) Cationic colloidal gold — a new probe for the detection of anionic cell surface sites by electron microscopy.J. Histochem. Cytochem. 34, 693–6.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Spicer, S. S., Horn, R. G. &Leppi, T. J. (1967) Histochemistry of connective tissue mucopolysaccharides. InThe Connective Tissue (edited byWagner, B. M. &Smith, D. E.) pp. 251–303. Baltimore: Williams and Wilkins.

    Google Scholar 

  • Spicer, S. S., Hardin, J. H. &Setser, M. E. (1978a) Ultrastructural visualization of sulfated complex carbohydrates in blood and epithelial cells with the high iron diamine procedure.Histochem J. 10, 435–52.

    CAS  PubMed  Google Scholar 

  • Spicer, S. S., Katsuyama, T. &Sannes, P. L. (1978b) Ultrastructural carbohydrate cytochemistry of gastric epithelium.Histochem J. 10, 309–31.

    CAS  PubMed  Google Scholar 

  • Suganuma, T., Katsuyama, T., Tsukahara, M., Sakakura, M. &Murata, F. (1981a) Comparative histochemical study of alimentary tracts with special reference to the mucous neck cells of the stomach.Am. J. Anat. 161, 219–38.

    Article  CAS  PubMed  Google Scholar 

  • Suganuma, T., Suzuki, S., Tsuyama, S. &Murata, F. (1981b) Mucosubstances of the rat gastric mucosa studied by means of several histochemical methods.Acta. Histochem. Cytochem. 14, 534–48.

    Google Scholar 

  • Suganuma, T., Tsuyama, S., Suzuki, S. &Murata, F. (1984) Lectinperoxidase reactivity in rat gastric mucosa.Arch. Histol. Jpn 47, 197–207.

    CAS  PubMed  Google Scholar 

  • Suganuma, T., Tsuyama, S. &Murata, F. (1985) Glycoconjugate cytochemistry of rat fundic gland using lectin/colloidal gold conjugates and Lowicryl K4M.Helix pomatia lectin is a specific marker for mucous neck cells in fundic gland of the rat gastric mucosa.Histochemistry 83, 489–95.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, S., Tsuyama, S. &Murata, F. (1982) Post-embedding staining of rat gastric mucous cells with lectins.Histochemistry 73, 563–75.

    Article  CAS  PubMed  Google Scholar 

  • Thiéry, J. P. &Ovtracht, L. (1979) Differential characterization of carboxyl and sulphate groups in thin sections for electron microscopy.Biol. Cell 36, 281–8.

    Google Scholar 

  • Thomopoulos, G. N., Schulte, B. A. &Spicer, S. S. (1983) The influence of embedding media and fixation on the postembedment ultrastructural demonstration of complex carbohydrates.J. Histochem. Cytochem. 31, 871–8.

    CAS  PubMed  Google Scholar 

  • Vorbrodt, A. W. (1987) Demonstration of anionic sites on the luminal and abluminal fronts of endothelial cells with poly-l-lysine-gold complexes.J. Histochem. Cytochem. 35, 1261–6.

    CAS  PubMed  Google Scholar 

  • Wattel, W., Geuze, J. J. &Rooij, D. G. (1977) Ultrastructural and carbohydrate histochemical studies on the differentiation and renewal of mucous cells in the rat gastric fundus.Cell Tiss. Res. 176, 445–62.

    Article  CAS  Google Scholar 

  • Wattel, W., Van Huis, G. A., Kramer, M. F. &Geuze, J. J. (1979) Glycoptein synthesis in the mucous cells of the vascular perfused rat stomach. II. Differentiating mucous cells.Am. J. Anat. 156, 313–20.

    Article  CAS  PubMed  Google Scholar 

  • Yamori, T., Ota, D. M., Cleary, K. R., Hoff, S., Hager, L. C. &Irimura, T. (1989) Monoclonal antibody against human colonic sulfomucin: immunochemical detection of its binding sites in colonic mucosa, colorectal primary carcinoma, and metastases.Cancer Res. 49, 887–94.

    CAS  PubMed  Google Scholar 

  • Yeomans, N. D., &Trier, J. S. (1976) Epithelial cell proliferation and migration in the developing rat gastric mucosa.Dev. Biol. 53, 206–16.

    Article  CAS  PubMed  Google Scholar 

  • Young, R. W. (1973) The role of the Golgi complex in sulfate metabolism.J. Cell Biol. 57, 175–89.

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Anatomy, Faculty of Medicine, Kagoshima University, 890, Kagoshima, Japan

    Dong-Hua Yang, Hiroshi Kasamo, Munenori Miyauchi, Shinichiro Tsuyama & Fusayoshi Murata

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  1. Dong-Hua Yang
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  2. Hiroshi Kasamo
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  3. Munenori Miyauchi
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  4. Shinichiro Tsuyama
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  5. Fusayoshi Murata
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Yang, DH., Kasamo, H., Miyauchi, M. et al. Ontogeny of sulphated glycoconjugate-producing cells in the rat fundic gland. Histochem J 28, 33–43 (1996). https://doi.org/10.1007/BF02331425

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