Skip to main content
Log in

Histochemical analysis of glycoproteins in the unicellular glands in the epidermis of an Indian freshwater fish Mastacembelus pancalus (Hamilton)

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

Summary

The unicellular glands in the epidermis of the Indian freshwater fish Mastacembelus pancalus consist of three types of mucous cells and sacciform cells. The histochemical properties of their secretory glycoproteins have been analysed by means of a battery of histochemical methods. These included methods for the identification and simultaneous visualization of oxidizable vicinal diols, O-acyl sugars, O-sulphate esters and sialic acid residues with or without side-chain O-acyl variants. Four general classes of glycoproteins (GPs) were identified. These included (i) GPs with O-sulphate esters and oxidizable vicinal diols, (ii) GPs with oxidizable vicinal diols and sialic acid residues with or without O-acyl substitution at C7, (iii) GPs mainly with O-sulphate esters, low moieties of GPs with oxidizable vicinal diols, O-acyl sugars and sialic acid residues with side-chain O-acyl variant predominantly at C8 (or which are di- or tri-substituted) or C9 and in traces of sialic acid residues without O-acyl substitution or with O-acyl substitution at C7, and (iv) GPs with traces of oxidizable vicinal diols, O-acyl sugars and sialic acid residues with O-acyl substitution at C8 (or which are di- or tri-substituted) or C9. The physiological significances of these GP classes and their release on the surface of the epidermis are discussed with special reference to their role in lubrication, protection and inhibition of the invasion and proliferation of pathogenic microorganisms in the epidermis, as adapted to the peculiar mode of life of the fish.

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

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

    Google Scholar 

  • AL-SUHAIL, A. A., REID, P. E., CULLING, C. F. A., DUNN, W. L. & CLAY, M. G. (1984b) Studies of the degraded carrageenan-induced colitis of rabbits. II. Changes in the epithelial glycoprotein O-acylated sialic acids associated with the induction and healing phases. Histochem. J. 16, 555–64.

    Google Scholar 

  • BULLOCK, A. M. (1980) A comparative study of the epidermal morphology of fishes of order Anacanthini with reference to their ecology and distribution. Oceanogr. Mar. Biol. Ann. Rev. 18, 251–315.

    Google Scholar 

  • CULLING, C. F. A., REID, P. E., CLAY, M. G. &DUNN, W. L. (1974) The histochemical demonstration of O-acylated sialic acid in gastrointestinal mucins. Their association with the potassium hydroxideperiodic acid-Schiff effect. J. Histochem. Cytochem. 22, 826–31.

    Google Scholar 

  • CULLING, C. F. A., REID, P. E. & DUNN, W. L. (1976) A new histochemical method for the identification and visualisation of both side chain acylated and non-acylated sialic acids. J. Histochem. Cytochem. 24, 1225–30.

    Google Scholar 

  • DRZENICK, R. (1973) Substrate specificity of neuraminidase. Histochem. J. 5, 271–90.

    Google Scholar 

  • FASULO, S., TAGLIAFIERRO, G., CONTINI, A., AINIS, L., RICCA, M. B., YANAIHARA, N. &ZACCONE, G. (1993) Ectopic expression of bioactive peptides and serotonin in the sacciform gland cells of teleost skin. Arch. Histol. Cytol. 56, 117–25.

    Google Scholar 

  • FOX, R. A. (1979) Membrane glycoproteins shed in defence of the cells of the gastrointestinal tract. Med. Hypoth. 5, 669–82.

    Google Scholar 

  • GILL, G. W., FROST, J. K. & MILLER, K. A. (1974) A new formula for a half-oxidized hematoxylin solution that neither over stains nor requires differentiation. Acta Cytol. 18, 300–11.

    Google Scholar 

  • GREENWOOD, P. H., ROSEN, D. E., WEITZMAN, S. H. & MYERS, G. S. (1966) Phyletic studies of teleostean fishes, with a provisional classification of living forms. Bull. Amer. Mus. Nat. Hist. 131, 339–456.

    Google Scholar 

  • HAFEZ, E. S. E. (1977) Functional anatomy of mucus secreting cells. Adv. Exp. Med. Biol. 89, 19–38.

    Google Scholar 

  • HERRLER, G., ROTT, R., KLENK, H.-D., MULLER, H.-P., SHUKLA, A. K. & SCHAUER, R. (1985) The receptor destroying enzyme of influenza C virus is neuraminate-O-acetyl-esterase. EMBO J. 4, 1503–6.

    Google Scholar 

  • HILDEMANN, W. H. (1962) Immunogenetic studies of poikilothermic animals. Am. Naturalist, 96, 195–204.

    Google Scholar 

  • HUGHES, R. C. (1975) The complex carbohydrates of mammalian cell surfaces and their biological roles. Essays Biochem. 11, 1–36.

    Google Scholar 

  • IMAKI, H. & CHAVIN, W. (1984) Ultrastructure of mucous cells in the sarcopterygian integument. Scan. Electron Microsc. 1, 409–22.

    Google Scholar 

  • JEANLOZ, R. W. & CODINGTON, J. F. (1976) The biological role of sialic acid at the surface of the cell. In Biological Roles of Sialic Acid (edited by ROSENBERG, A. & SCHENGRUND, C. L.), pp. 201–38. New York: Plenum Press.

    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 

  • LEWIS, R. W. (1970) Fish cutaneous mucus: a new source of skin surface lipids. Lipids 5, 947–9.

    Google Scholar 

  • LIEM, K. F. (1967) Functional morphology of the integumentary, respiratory and digestive systems of the synbranchoid fish Monopterus albus. Copeia. 1967, 375–88.

    Google Scholar 

  • LIGUORI, V. R., RUGGIERI, G. D., BASLOW, S. J. M. H., STEMPIEN, M. F. & NIGRELLI, R. F. (1963) Antibiotic and toxic activity of the mucus of the pacific golden striped bass Grammistes sexlineatus. Am. Zoologist 3, 546.

    Google Scholar 

  • LILLIE, R. D. & FULLMER, H. M. (1976) Histopathologic Technic and Practical Histochemistry, 4th edn. New York: McGraw-Hill.

    Google Scholar 

  • MCMANUS, J. F. A. (1948) Histological and histochemical uses of periodic acid. Stain Technol. 23, 99–108.

    Google Scholar 

  • MITTAL, A. K. & AGARWAL, S. K. (1977) Histochemistry of the unicellular glands in relation to their physiological significance in the epidermis of Monopterus cuchia (Synbranchiformes, Pisces). J. Zool. 182, 429–39.

    Google Scholar 

  • MITTAL, A. K. & BANERJEE, T. K. (1980) Keratinization versus mucus secretion in fish epidermis. In The Skin of Vertebrates (edited by SPEARMAN, R. I. C. & RILEY, P. A.), Linnean Society Symposium Series No. 9, pp. 1–12. London: Academic Press.

    Google Scholar 

  • MITTAL, A. K. & MUNSHI, J. S. D. (1971) A comparative study of the structure of the skin of certain air-breathing freshwater teleosts. J. Zool. (Lond.) 163, 515–32.

    Google Scholar 

  • MITTAL, A. K. & WHITEAR, M. (1978) A note on cold anaesthesia of poikilotherms. J. Fish Biol. 13, 519–20.

    Google Scholar 

  • MITTAL, A. K., WHITEAR, M. & BULLOCK, A. M. (1981) Sacciform cells in the skin of teleost fish. Z. mikrosk. -anat. Forsch. (Leipzig) 95, 559–85.

    Google Scholar 

  • MOWRY, R. W. (1956) Alcian blue techniques for the histochemical study of acidic carbohydrates. J. Histochem. Cytochem. 4, 407–8.

    Google Scholar 

  • MOWRY, R. W. (1963) The special value of methods that color 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. NY Acad. Sci. 106, 402–23.

    Google Scholar 

  • NAKAMURA, M., KITAMURA, H. & YAMADA, K. (1985) A sensitive method for the histochemical demonstration of vicinal diols of carbohydrates. Histochem. J. 17, 477–85.

    Google Scholar 

  • NIGRELLI, R. F. (1937) Further studies on the susceptibility and acquired immunity of marine fishes to Epibdella melleni, a monogenetic trematode. Zoologica (New York) 22, 185–92.

    Google Scholar 

  • NIGRELLI, R. F., JAKOWSKA, S. & PADNOS, M. (1955) Pathogenicity of epibionts in fishes. J. Protozool. 2 (suppl.), 7.

    Google Scholar 

  • PAINTER, R. G. & WHITE, A. (1976) Effect of concanavalin A on expression of cell surface sialyltransferase activity of mouse thymocytes. Proc. Natl Acad. Sci. USA 73, 837–41.

    Google Scholar 

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

    Google Scholar 

  • PARK, C. M., REID, P. E., OWEN, D. A., VOLZ, D. & DUNN, W. L. (1987b) Histochemical studies of epithelial cell glycoproteins in normal rat colon. Histochem. J. 19, 546–54.

    Google Scholar 

  • REID, P. E. & PARK, C. M. (1990) Carbohydrate histochemistry of epithelial glycoproteins. Progr. Histochem. Cytochem. 21, 1–170.

    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.

    Google Scholar 

  • REID, P. E., DUNN, W. L., RAMEY, C. W., CORET, E., TRUEMAN, L. & CLAY, M. G. (1984) 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.

    Google Scholar 

  • REID, P. E., OWEN, D. A., RAMEY, C. W., DUNN, W. L., CLAY, M. G. & JONES, E. A. (1985a) Histochemical procedures for simultaneous visualization of sialic acid, its side chain O-acyl variants and O-sulphate esters. Histochem. J. 17, 113–7.

    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.

    Google Scholar 

  • ROSEN, M. W. & CORNFORD, N. E. (1971) Fluid friction of fish slimes. Nature 234, 49–51.

    Google Scholar 

  • ROSENBERG, A. & SCHENGRUND, C. L. (1976) Biological Roles of Sialic Acid. New York: Plenum Press.

    Google Scholar 

  • SCHENGRUND, C. L., DUFF, R. & ROSENBERG, A. (1974) Sialidase activity of oncogenic cells transformed by herpes simplex virus. Virology 58, 595–9.

    Google Scholar 

  • SCHRÖDER, B. (1903) Uber den schleim und seine biologische Bedeutung. Biologische Zentralblatt 23, 457–68.

    Google Scholar 

  • SHINOHARA, H. (1977) On glycoproteins. Biochemistry 49, 1219–37.

    Google Scholar 

  • SINGH, S. K. & MITTEL, A. K. (1990) A comparative study of epidermis of the common carp and the three Indian major carps. J. Fish Biol. 36, 9–19.

    Google Scholar 

  • SPECKART, S. F., BOLDT, D. H. & RYERSON, K. L. (1978) Different effects of concanavalin A and E-phytohemagglutinin upon lymphocyte glycosyltranferase activities. Cancer Res. 38, 4554–61.

    Google Scholar 

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

    Google Scholar 

  • SPICER, S. S., HORN, R. G. & LEPPI, T. J. (1967) Histochemistry of connective tissue mucopolysaccharides. In The Connective Tissue (edited by WAGNER, B. M. & SMITH, D. E.), pp. 251–303. Baltimore: Williams & Wilkins.

    Google Scholar 

  • SPICER, S. S. & SCHULTE, B. A. (1992) Diversity of cell glycoconjugates shown histochemically: a perspective. J. Histochem. Cytochem. 40, 1–38.

    Google Scholar 

  • SPICER, S. S. & WARREN, L. (1960) The histochemistry of sialic acid containing mucoproteins. J. Histochem. Cytochem. 8, 135–7.

    Google Scholar 

  • STOKLOSOWA, S. (1966) Sexual dimorphism in the skin of the seatrout Salmo trutta. Copeia 1966, 613–4.

    Google Scholar 

  • SUPRASERT, A., FUJIOKA, T. & YAMADA, K. (1986) Glycoconjugates in the secretory epithelium of the chicken mandibular gland. Histochem. J. 18, 115–21.

    Google Scholar 

  • SUPRASERT, A., FUJIOKA, T. & YAMADA, K. (1987) The histochemistry of glycoconjugates in the colonic epithelium of the chicken. Histochemistry 86, 491–7.

    Google Scholar 

  • TADANO, Y. & YAMADA, K. (1978) The histochemistry of complex carbohydrates in the ovarian follicles of adult mice. Histochemistry 57, 203–15.

    Google Scholar 

  • TAO, T.-W. & BURGER, M. M. (1977) Non-metastasising variants selected from metastasising melanoma cells. Nature 270, 437–8.

    Google Scholar 

  • TSUJI, S., YAMASHITA, T., TANAKA, M. & NAGAI, Y. (1988) Synthetic sialyl compounds as well as neutral gangliosides induce neuritogenesis in a mouse neuroblastoma cell line (Neuro 2a). J. Neurochem. 50, 414–23.

    Google Scholar 

  • TSUKISE, A. & YAMADA, K. (1981) The histochemistry of complex carbohydrates in the secrotum of the boar. Histochemistry 72, 511–21.

    Google Scholar 

  • UCHIDA, Y., TSUKADA, Y. & SUGIMORI, T. (1979) Enzymatic properties of neuraminidase from Arthrobacter ureafaciens. J. Biochem. 86, 1573–85.

    Google Scholar 

  • USUKI, S., LYU, S.-C. & SWEELEY, C. C. (1988) Sialidase activities of cultured human fibroblasts and the metabolism of GM3 ganglioside. J. Biol. Chem. 263, 6847–53.

    Google Scholar 

  • USUKI, S., HOOPS, P. & SWEELEY, C. C. (1988) Growth control of human foreskin fibroblasts and inhibition of extracellular sialidase activity by 2-deoxy-2,3-dehydro-N-acetyl neuraminic acid. J. Biol. Chem. 263, 10595–9.

    Google Scholar 

  • WERNER, R., ECKART, K., CHRISTIAN, B. & WOLFGANG, G. (1982) Biological significance of sialic acid. In Sialic Acid: Chemistry, Metabolism and Function (edited by SCHAUER, R.) Cell biology monographs. Vol. 10, pp. 263–305. Vienna: Springer.

    Google Scholar 

  • WHARTON, S. A., WEIS, W., SKEHEL, J. J. & WILEY, D. C. (1989) Structure, function, and antigenicity of the hemagglutinin of influenza virus. In The Influenza Viruses (edited by KRUG, R., M.), pp. 153–73. New York: Plenum Press.

    Google Scholar 

  • WHITEAR, M. (1986) The skin of fishes including cyclostomes: epidermis. In Biology of the Integument, Vol. 2. Vertebrates (edited by BEREITER-HAHN, J., et al.) pp. 8–38, Berlin: Springer-Verlag.

    Google Scholar 

  • WINZLER, R. J. (1970) Carbohydrates in cell surfaces. In International Review of Cytology (edited by BOURNE, G. H. & DANIELLI, J. F.), Vol. 29, pp. 77–125. New York: Academic Press.

    Google Scholar 

  • WOODRUFF, J. J. & GESNER, B. M. (1969) The effect of neuraminidase on the fate of transfused lymphocytes. J. Exp. Med. 129, 551–67.

    Google Scholar 

  • YAMADA, K. (1993) Histochemistry of carbohydrates as performed by physical development procedures. Histochem. J. 25, 95–106.

    Google Scholar 

  • YOGEESWARAN, G., STEIN, B. S. & SEBASTIAN, H. (1978) Altered cell surface organization of gangliosides and sialylglycoproteins of mouse metastatic melanoma variant lines selected in vivo for enhanced lung implantation. Cancer Res. 38, 1336–44.

    Google Scholar 

  • ZACCONE, G. (1981) Studies on the structure and histochemistry of the epidermis in the airbreathing teleost Mastacembelus armatus (Mastacembelidae, Pisces). Z. mikrosk. -anat. Forsch. (Leipzig) 95, 809–26.

    Google Scholar 

  • ZACCONE, G. (1982a) Histochemical studies of the epithelial mucosubstances, respiratory and pentose shunt enzymes in the skin epidermis of the airbreathing teleost Mastacembelus erythrotaenia (Mastacembelidae, Pisces). Gegenbaurs morph. Jahrb. (Leipzig) 128, 918–21.

    Google Scholar 

  • ZACCONE, G. (1982b) Histochemical studies of some hydrolytic and oxidative enzymes in the skin epidermis of the clingfish Lepadogaster candollei Risso (Gobiesociformes, Pisces). Bas. Appl. Histochem. 26, 199–207.

    Google Scholar 

  • ZACCONE, G. & LICATA, A. (1983) Histochemistry and fine structure of the secretory epidermis and sucking disc in the clingfish Lepadogaster candollei Risso (Gobiesociformes, Pisces). Zool. Jb. Anat. 109, 319–34.

    Google Scholar 

  • ZACCONE, G., FASULO, S., LO CASCIO, P. & LICATA, A. (1986) 5-Hydroxytryptamine immunoreactivity in the epidermal sacciform gland cells of the clingfish Lepadogaster candollei Risso. Cell Tissue Res. 246, 679–82.

    Google Scholar 

  • ZACCONE, G., FASULO, S., LO CASCIO, P., LICATA, A. &AINIS, L. (1987) Occurrence of gastrin-releasing peptide-like and bombesin-like immunoreactivities in the epidermal sacciform gland cells of the clingfish Lepadogaster candollei. Bas. Appl. Histochem. 31, 455–64.

    Google Scholar 

  • ZACCONE, G., FASULO, S., LICATA, A., AINIS, L. & LO CASCIO, P. (1988) GRP/bombesin-immunoreactive sacciform gland cells in the epidermis of the clingfish, Lepadogaster candollei. Ann. N.Y. Acad. Sci. 547, 464–5.

    Google Scholar 

  • ZACCONE, G., FASULO, S., AINIS, L. & CONTINI, A. (1989) Localization of calmodulin positive immunoreactivity in the surface epidermis of the brown trout, Salmo trutta. Histochemistry 91, 13–6.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mittal, A.K., Ueda, T., Fujimori, O. et al. Histochemical analysis of glycoproteins in the unicellular glands in the epidermis of an Indian freshwater fish Mastacembelus pancalus (Hamilton). Histochem J 26, 666–677 (1994). https://doi.org/10.1007/BF00158292

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00158292

Keywords

Navigation