Summary
This study was undertaken to determine whether the numerous cytoplasmic tubules (CT) in the apical cytoplasm of goldfish hindgut absorptive cells are directly involved in the endocytotic transport of macromolecules into the cells, or whether they are derived from the intracellular membrane components. The absorptive cells were exposed to horseradish peroxidase (HRP)-containing medium in organ culture and subsequently fixed and prepared for electron microscopy. Analysis revealed that 5 sec after exposure, many vesicular structures, including coated vesicles, were labelled with reaction product whereas almost all CT were negative. After a 1-min exposure, reaction product was detected in about 11 % of the CT, and thereafter, the percentage increased to about 95% after 15 min exposure. As labelled CT increased in number, the number of densely labelled vacuoles with attached CT also increased. CT connected to vacuoles with a peripheral margin of dense reaction product were always HRP-positive, whereas those connected to vacuoles which were not distinctly labelled were themselves also devoid of HRP reaction product. This indicated that the labelling of CT was closely associated with the labelling of the inner surface of the vacuolar membrane. These results indicate that CT are probably formed by a budding off from these vacuoles, rather than being directly involved in endocytosis.
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Block J, Mulder-Staple AA, Ginsel LA, Daems WTh (1981) Endocytosis in absorptive cells of cultured human small-intestinal tissue: horseradish peroxidase, lactoperoxidase, and ferritin as markers. Cell Tissue Res 216:1–13
Christensen EI (1982) Rapid membrane recycling in renal proximal tubular cells. Eur J Cell Biol 29:43–49
Dautry-Varsat A, Lodish HF (1984) How receptors bring proteins and particles into cells. Sci Am 250:48–54
Farquhar MG (1981) Membrane recycling in secretory cells: Implication for traffic of products and specialized membranes within the Golgi complex. Method Cell Biol 23:399–427
Geuze HJ, Slot JW, Strous GJAM, Lodish HF, Schwartz AL (1983) Intracellular site of asialoglycoprotein receptor-ligand uncoupling: Double-label immunoelectron microscopy during receptor-mediated endocytosis. Cell 32:277–287
Gonnella PA, Neutra MR (1984) Membrane-bound and fluidphase macromolecules enter separate prelysosomal compartments in absorptive cells of suckling rat ileum. J Cell Biol 99:909–917
Graham RC, Karnovsky MJ (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14:291–302
Hermo L, Morales C (1984) Endocytosis in nonciliated epithelial cells of the ductuli efferentes in the rat. Am J Anat 171:59–74
Heuser J (1980) Three-dimensional visualization of coated vesicle formation in fibroblasts. J Cell Biol 84:560–583
Hopkins CR (1983) The importance of the endosome in intracellular traffic. Nature 304:684–685
Iida H, Yamamoto T (1984) Morphological studies of the goldfish hindgut mucosa in organ culture. Cell Tissue Res (in press)
Luft JH (1971) Ruthenium red and violet. II. Fine structural localization in animal tissues. Anat Rec 171:369–416
Maunsbach AB (1973) Ultrastructure of the proximal tubule. In: Orloff J, Berliner WR (eds) Handbook of physiology, Sect. 8, pp 71–79, American Physiological Society. Washington
Petersen OW, Van Deurs B (1983) Serial-section analysis of coated pits and vesicles involved in adsorptive pinocytosis in cultured fibroblasts. J Cell Biol 96:277–281
Ryser HJ-P, Drummond I, Shen W-C (1982) The cellular uptake of horseradih peroxidase and its poly(lysine)conjugate by cultured fibroblasts is qualitatively similar despite a 900-fold difference in rate. J Cell Physiol 113:167–178
Van Deurs B (1978) Horseradish peroxidase uptake into the rat choroid plexus epithelium, with special reference to the lysosomal system. J Ulstrastruct Res 62:155–167
Van Deurs B, Christensen EI (1984) Endocytosis in kidney proximal tubule cells and cultured fibroblasts: a review of the structural aspects of membrane recycling between the plasma membrane and endocytic vacuoles. Eur J Cell Biol 33:163–173
Van Deurs B, Nilausen K (1982) Pinocytosis in mouse L-fibroblasts: Ultrastructural evidence for a direct membrane shuttle between the plasma membrane and the lysosomal compartment. J Cell Biol 94:279–286
Van Deurs B, Von Bülow F, Møller M (1981) Vesicular transport of cationized ferritin by the epithelium of the rat choroid plexus. J Cell Biol 89:131–139
Yamamoto T (1966) An electron microscope study of the columnar epithelial cell in the intestine of fresh water teleosts: goldfish (Carassius auratus) and rainbow trout (Salmo irideus). Z Zellforsch 72:66–87
Yamamoto T (1972) Absorption across the plasma membrane of the intestinal absorptive cells. Acta Histochem Cytochem 5:266–268
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Iida, H., Yamamoto, T. Intracellular transport of horseradish peroxidase in the absorptive cells of goldfish hindgut in vitro, with special reference to the cytoplasmic tubules. Cell Tissue Res. 240, 553–560 (1985). https://doi.org/10.1007/BF00216344
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DOI: https://doi.org/10.1007/BF00216344