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Metabolic-morphologic events in the integument of the Pacific hagfish (Eptatretus stoutii)

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Light- and electron-microscopic autoradiography were used to obtain a coordinated metabolic-morphologic view of some of the events of cellular differentiation that occur across the epidermis of the Pacific hagfish (Eptatretus stoutii) and which enable this animal to secrete copious amounts of mucus. As judged by epidermal incorporation of [3H]-thymidine in vivo, about 98 % of DNA replication is confined to the basal three layers of the total of 6–8 layers of cells. Small mucous cells (SMC), the most numerous of the three major cell types involved in mucigenesis, show in vitro and in vivo radioincorporation profiles of [3H]-L-lysine and [3H]-D-glucosamine which differ markedly from those of [3H]-L-fucose and [3H]-D-galactose. Time-course incorporation profiles (mean silver grains/cell and percentage of cells with at least one cluster of silver grains) of [3H]-L-lysine and [3H]-D-glucosamine not only reflected the metabolic activities of cell renewal and differentiation in basally-located cells but also the high mucigenic activity in cells near the epidermal surface. By contrast, [3H]-L-fucose and [3H]-D-galactose were mainly incorporated by the more mature SMC in juxtanuclear regions near Golgi complexes and newly formed secretory vesicles. The intensity of [3H]-fucose labeling appeared proportional to the intensity of histochemical staining of the apical cytoplasm. The prominent capsule, within SMC in basal and lateral regions, which arises from a tight intermingling of tonofilaments, appears to restrict secretory vesicles to apical regions while the cell progressively differentiates and migrates to the epidermal surface. The other mucigenic cell types, large mucous cells and thread cells, each show distinctive differentiation and radioincorporation patterns.

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References

  • Adler, D.R., Burton, M.P.M.: The pronephron as the site of presumptive interrenal cells in the hagfish Myxine glutinosa L. Comp. Biochem. Physiol. 53, 73–77 (1976)

    Google Scholar 

  • Anderson, W.C., Manion, P.J.: Morphological development of the integument of the sea lamprey, Petromyzon marinus. J. Fish. Res. Board Can. 34, 159–163 (1977)

    Google Scholar 

  • Avtalion, R.R., Weiss, E., Moalen, T.: Regulatory effects of temperature upon immunity in ectothermic vertebrates. In: Comparative immunology (J.J. Marchalonis, ed.), pp. 227–238. New York: John Wiley and Sons 1976

    Google Scholar 

  • Bekesi, J.B., Winzler, R.J.: The metabolism of plasma glycoproteins. Studies on the incorporation of l-fucose-1-14C into tissue and serum in the normal rat. J. Biol. Chem. 242, 3873–3879 (1967)

    Google Scholar 

  • Bennett, G.: Migration of glycoprotein from the Golgi apparatus to cell coat in the columnar cells of the duodenal epithelium. J. Cell Biol. 45, 668–673 (1970)

    Google Scholar 

  • Bennett, G., Leblond, C.P.: Formation of cell coat material for the whole surface of columnar cells in the rat small intestine, as visualized by radioautography with l-fucose3H. J. Cell Biol. 46, 409–416 (1970)

    Google Scholar 

  • Bennett, G., Leblond, C.P.: Passage of fucose-3H label from the Golgi apparatus into dense and multivesicular bodies in the duodenal columnar cells and hepatocytes of the rat. J. Cell Biol. 51, 875–881 (1971)

    Google Scholar 

  • Bernstein, I.A.: Relation of the nucleic acids to protein synthesis in the mammalian epidermis. In: The epidermis (W. Montagna and W.C. Lobitz, eds.), pp. 471–483. New York: Academic Press 1964

    Google Scholar 

  • Blackstad, T.: The skin and its derivatives. In: The biology of Myxine (A. Brodal and R. Fänge, eds.), pp. 195–230. Oslo: Universitetsforlaget 1963

    Google Scholar 

  • Brody, I.: The ultrastructure of the tonofibrils in the keratinization process of normal human epidermis. J. Ultrastruct. Res. 4, 264–297 (1960)

    Google Scholar 

  • Cairnie, A.B., Lala, P.K., Osmond, D.G. (eds.): Stem cells of renewing cell populations. pp. 1–382. New York: Academic Press 1976

    Google Scholar 

  • Cameron, I.L., Greulich, R.C.: Evidence for an essentially constant duration of DNA synthesis in renewing epithelia of the adult mouse. J. Cell Biol. 18, 31–40 (1963)

    Google Scholar 

  • Caro, L.G., Turbergen, R.P. van: High resolution autoradiography. I. Methods. J. Cell Biol. 15, 173–188 (1962)

    Google Scholar 

  • Clamp, J.R.: Mucus in health and disease. Adv. Exp. Med. Biol. 89, 1–15 (1976)

    Google Scholar 

  • Downing, S.W., Novales, R.R.: The fine structure of lamprey epidermis. I. Introduction and mucous cells. J. Ultrastruct. Res. 35, 282–294 (1971a)

    Google Scholar 

  • Downing, S.W., Novales, R.R.: The fine structure of lamprey epidermis. II. Club cells. J. Ultrastruct. Res. 35, 295–303 (1971b)

    Google Scholar 

  • Downing, S.W., Novales, R.R.: The fine structure of lamprey epidermis. III. Granular cells. J. Ultrastruct. Res. 35, 304–313 (1971c)

    Google Scholar 

  • Falkmer, S., Emdin, S.O., Östberg, Y., Matlisson, A., Johansson Sjöbeck, M.-L., Fänge, R.: Tumor pathology of the hagfish, Myxine glutinosa, and the river lamprey, Lampetra fluviatilis. Prog. Exp. Tumor Res. 20, 217–250 (1976)

    Google Scholar 

  • Falkmer, S., Thomas, N.W., Boquist, L.: Endocrinology of the cyclostomata. Chem. Zool. 8, 195–257 (1974)

    Google Scholar 

  • Fletcher, T.C., Grant, P.T.: Immunoglobulins in the serum and mucus of plaice (Pleuronectes platessa L.). Biochem. J. 115, 65 (1969)

    Google Scholar 

  • Greulich, R.C.: Aspects of cell individuality in the renewal of stratified squamous epithelia. In: The epidermis (W. Montagna and W.C. Lobitz, eds.), pp. 117–133. New York: Academic Press 1964

    Google Scholar 

  • Haddad, A., Smith, M.D., Herscovics, A., Nadler, N.J., Leblond, C.P.: Radioautographic study of in vivo and in vitro incorporation of fucose-3H into thyroglobulin by rat thyroid follicular cells. J. Cell Biol. 49, 856–882 (1971)

    Google Scholar 

  • Harris, J.E., Hunt, S.: The fine structure of the epidermis of two species of salmonid fish, the Atlantic salmon (Salmo salar L.) and the brown trout (Salmo trutta L.). I. General organization and filamentcontaining cells. Cell Tissue Res. 157, 553–565 (1975a)

    Google Scholar 

  • Harris, J.E., Hunt, S.: The fine structure of the epidermis of two species of salmonid fish, the Atlantic salmon (Salmo salar L.) and the brown trout (Salmo trutta L.). II. Mucous cells. Cell Tissue Res. 163, 535–543 (1975b)

    Google Scholar 

  • Hawkes, J.W.: The structure of fish skin. I. General organization. Cell Tissue Res. 149, 147–158 (1974a)

    Google Scholar 

  • Hawkes, J.W.: The structure of fish skin. II. The chromatophore unit. Cell Tissue Res. 149, 159–172 (1974b)

    Google Scholar 

  • Henrikson, R.C.: Incorporation of tritiated thymidine by teleost epidermal cells. Experientia 23, 357–358 (1967)

    Google Scholar 

  • Henrikson, R.C., Matoltsy, A.G.: The fine structure of teleost epidermis. I. Introduction and filamentcontaining cells. J. Ultrastruct. Res. 21, 194–212 (1968a)

    Google Scholar 

  • Henrikson, R.C., Matoltsy, A.G.: The fine structure of teleost epidermis. II. Mucous cells. J. Ultrastruct. Res. 21, 213–221 (1968b)

    Google Scholar 

  • Henrikson, R.C., Matoltsy, A.G.: The fine structure of teleost epidermis. III. Club cells and other cell types. J. Ultrastruct. Res. 21, 222–232 (1968c)

    Google Scholar 

  • Herscovics, A.: Biosynthesis of thyroglobulin incorporation of [3H]-fucose into proteins by rat thyroids in vitro. Biochem. J. 117, 411–413 (1970)

    Google Scholar 

  • Humphrey, C.D., Pittman, F.E.: A simple methylene blue-azure II-Basic fuchsin stain for epoxyembedded tissue sections. Stain Technol. 49, 9–14 (1974)

    Google Scholar 

  • Jakowska, J.: Mucus secretion in a fish-a note. Ann. N.Y. Acad. Sci. 106, 458–462 (1963)

    Google Scholar 

  • Jamieson, J.D., Palade, G.E.: Synthesis, intracellular transport and discharge of secretory proteins in stimulated pancreatic exocrine cells. J. Cell Biol. 50, 135–158 (1971)

    Google Scholar 

  • Kaufman, R.L., Ginsburg, V.: The metabolism of L-fucose by HeLa cells. Exp. Cell Res. 50, 127–132 (1968)

    Google Scholar 

  • Lanzing, W.J.R., Wright, R.G.: The ultrastructure of the skin of Tilapia mossambica (Peters). Cell Tissue Res. 154, 251–264 (1974)

    Google Scholar 

  • Leblond, C.P., Meissier, B., Kopriwa, B.: Thymidine-H3 as a tool for the renewal of cell populations. Lab. Invest. 8, 306–308 (1959)

    Google Scholar 

  • Leblond, C.P., Greulich, R.C., Pereira, J.P.M.: Relationship of cell formation and cell migration in the renewal of stratified squamous epithelia. In: Symposium on wound healing (W. Montagna, ed.). New York: Pergamon Press 1964

    Google Scholar 

  • Lehtonen, A., Kärkkäinen, J., Haahti, E.: Carbohydrate components in the epithelial mucin of hagfish, Myxine glutinosa. Acta Chem. Scand. 20, 1456–1462 (1966)

    Google Scholar 

  • Leppi, T.J.: Morphochemical analysis of mucous cells in the skin and slime glands of hagfishes. Histochemie 15, 68–78 (1968)

    Google Scholar 

  • Linthicum, D.S., Hildemann, W.H.: Immunologic responses of Pacific hagfish. III. Serum antibodies to cellular antigens. J. Immunol. 105, 912–918 (1970)

    Google Scholar 

  • Morris, R., Pickering, A.D.: Ultrastructure of the presumed ion-transporting cells in the gills of ammocoete lampreys, Lampetra fluviatilis (L.) and Lampetra planeri (Bloch). Cell Tissue Res. 163, 327–341 (1975)

    Google Scholar 

  • Murray, C.K., Fletcher, T.C.: The immunohistochemical localization of lysozyme in plaice (Pleuronectes platessa L.) tissues. J. Fish Biol. 9, 329–334 (1976)

    Google Scholar 

  • Nelson, D.M., Enders, A.C., King, B.F.: Cytological events involved in protein synthesis in cellular and syncytial trophoblast of human placenta. An electron microscope autoradiographic study of [3H]-leucine incorporation. J. Cell Biol. 76, 400–417 (1978)

    Google Scholar 

  • Neutra, M., Leblond, C.P.: Synthesis of the carbohydrate of mucus in the Golgi complex as shown by electron microscopic radioautography of goblet cells from rats injected with glucose-H3. J. Cell Biol. 30, 119–136 (1966a)

    Google Scholar 

  • Neutra, M., Leblond, C.P.: Radioautographic comparison of the uptake of galactose-H3 and glucose-H3 in the Golgi region of various cells secreting glycoproteins or mucopolysaccharides. J. Cell Biol. 30, 137–150 (1966b)

    Google Scholar 

  • Olson, K.R., Fromm, P.O.: A scanning electron microscopic study of secondary lamellae and chloride cells of rainbow trout (Salmo gairdneri). Z. Zellforsch. 143, 439–449 (1973)

    Google Scholar 

  • Oosten, J. van: The skin and scales. In: The physiology of fishes, Vol. I (E.M. Brown, ed.), pp. 207–244. New York: Academic Press 1957

    Google Scholar 

  • Parakkal, P.F., Matoltsy, A.G.: A study of the fine structure of the epidermis of Ranapipiens. J. Cell Biol. 20, 85–94 (1964)

    Google Scholar 

  • Pelletier, G.: Autoradiographic studies of synthesis and intracellular migration of glycoproteins in the rat anterior pituitary gland. J. Cell Biol. 62, 185–197 (1974)

    Google Scholar 

  • Reutter, K.: Cholinergic innervation of scattered sensory cells in fish epidermis. Cell Tissue Res. 149, 143–146 (1974)

    Google Scholar 

  • Roberts, R.J., Shearer, W.M., Elson, K.G.R., Munro, A.L.S.: Studies on ulcerative dermal necrosis of salmonids. I. The skin of the normal salmon head. J. Fish Biol. 2, 223–229 (1970)

    Google Scholar 

  • Roberts, R.J., Young, H., Milne, J.A.: Studies on the skin of plaice (Pleuronectes platessa L.) I. The structure and ultrastructure of normal skin. J. Fish Biol. 3, 87–98 (1971)

    Google Scholar 

  • Schliwa, M.: Cytoarchitecture of surface layer cells of the teleost epidermis. J. Ultrastruct. Res. 52, 377–386 (1975)

    Google Scholar 

  • Schultze, B., Oehlert, W.: Autoradiographic investigation of incorporation of H3-thymidine into cells of rat and mouse. Science 131, 737–738 (1960)

    Google Scholar 

  • Spitzer, R.H., Downing, S.W., Koch, E.A., Kaplan, M.A.: Hemagglutinins in the mucus of Pacific hagfish, Eptatretus stoutii. Comp. Biochem. Physiol. 54B, 409–411 (1976)

    Google Scholar 

  • Stich, H.F., Acton, A.B.: The possible use of fish tumors in monitoring for carcinogens in the marine environment. Prog. Exp. Tumor Res. 20, 44–54 (1976)

    Google Scholar 

  • Terakado, K., Ogawa, M., Hashimoto, Y., Matsuzaki, H.: Ultrastructure of the thread cells in the slime gland of Japanese hagfishes, Paramyxine atami and Eptatretus burgeri. Cell Tissue Res. 159, 311–323 (1975)

    Google Scholar 

  • Thoenes, G.H., Hildemann, W.H.: Immunological responses of Pacific hagfish. II. Serum antibody production to soluble antigen. In: Developmental aspects of antibody formation and structure (J. Sterzl and I. Riha, eds.), 2nd edn., Vol. II, pp. 711–726. New York: Academic Press 1971

    Google Scholar 

  • Thompson, D.A.: Toxic stress secretions of the boxfish Ostracion meleagris Shaw. Copeia 2, 335–351 (1969)

    Google Scholar 

  • Todd, J.M., Samli, M.H.: The incorporation of [3H]-glucosamine, [3H]-fucose and [3H]-mannose into protein in the rat anterior pituitary incubated in vitro. Biochem. Biophys. Acta 297, 11–21 (1973)

    Google Scholar 

  • Völkyl, A., Bieger, W., Kern, H.F.: Studies on secretory glycoproteins in the rat exocrine pancreas. I. Fine structure of the Golgi complex and release of fucose-labeled proteins after in vivo stimulation with caerulein. Cell Tissue Res. 175, 227–243 (1976)

    Google Scholar 

  • Waechter, C.J., Lennarz, W.J.: The role of polyprenol-linked sugars in glycoprotein synthesis. Ann. Rev. Biochem. (E.E. Snell, ed.), pp. 95–112. Palo Alto, CA, Annual Reviews, Inc. 1976

    Google Scholar 

  • Wellings, S.R., McCain, B.B., Miller, B.S.: Epidermal papillomas in Pleuronectidae of Puget Sound, Washington. Review of the current status of the problem. Prog. Exp. Tumor Res. 20, 55–74 (1976)

    Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry, University of Health Sciences, The Chicago Medical School, 2020 W. Ogden Ave., 60612, Chicago, Illinois, USA

    Robert H. Spitzer & Elizabeth A. Koch

  2. The Department of Biomedical Anatomy, School of Medicine, University of Minnesota, Duluth, Minnesota, USA

    Stephen W. Downing

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  1. Robert H. Spitzer
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  2. Stephen W. Downing
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  3. Elizabeth A. Koch
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This study was supported in part by General Research Support Grant, FR5366 of the NIH, Minnesota Medical Foundation Grants, and the Asthmatic Children's Aid of Chicago, Illinois. The authors wish to thank Karen Brintzenhofe and Doreen Fleetwood for their assistance

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Spitzer, R.H., Downing, S.W. & Koch, E.A. Metabolic-morphologic events in the integument of the Pacific hagfish (Eptatretus stoutii). Cell Tissue Res. 197, 235–255 (1979). https://doi.org/10.1007/BF00233917

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