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Endocytosis of native and cationized ferritin by intralobular duct cells of the rat parotid gland

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The ability of the intralobular ducts of the rat parotid gland to take up protein from the lumen was examined after retrograde infusion of native and cationized ferritin. At high concentrations (3–10 mg/ml), cells of both intercalated- and striated ducts avidly internalized the tracers. No differences were noted in the mode of uptake or fate of native or cationized ferritin. Large, apical ferritin-containing vacuoles up to 5 μm in size were present in cells of the intercalated ducts after infusion for 15 min. Small, smooth-surfaced spherical or flattened vesicles and tubules containing ferritin were also observed, often in association with the large vacuoles. Ferritin uptake increased with increasing infusion time, up to 1 h. Uptake by the striated ducts was less consistent than by the intercalated ducts, and occurred mainly in small vesicles and tubules. Secondary lysosomes became labeled with ferritin in both cell types. Ferritin was not observed in the Golgi saccules, nor was it discharged from the cells at the basolateral surfaces. At low concentrations (0.3–1 mg/ml), uptake was reduced, especially by cells of intercalated ducts, and differences were noted in the behavior of the two tracers. Cationized ferritin was internalized mainly into vesicles and tubules of cells of striated ducts; little uptake of native ferritin occurred at low concentrations. These results demonstrate that the ductal cells of the salivary glands are capable of luminal endocytosis of foreign proteins. They also suggest that in addition to modifying the primary saliva by electrolyte reabsorption and secretion, and secretion of various glycoproteins, the ductal cells are able to reabsorb proteins secreted by the acinar cells.

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References

  • Alvares EP, Sesso A (1975) Cell proliferation and transformation in the rat submandibular gland during early postnatal growth A quantitative and morphological study. Arch Histol Jpn 38:177–208

    Google Scholar 

  • Ball WD, Hand AR, Johnson AO (1986) Secretory proteins in the perinatal submandibular gland of the rat. J Dent Res 65:325

    Google Scholar 

  • Chang WWL (1974) Cell population changes during acinus formation in the postnatal rat submandibular gland. Anat Rec 178:187–202

    Google Scholar 

  • Christensen EI, Carone FA, Rennke HG (1981) Effect of molecular charge on endocytic uptake of ferritin in renal proximal tubule cells. Lab Invest 44:351–358

    Google Scholar 

  • Coleman R, Mazariegos MR, and AR (1984) Endocytosis of periodate-oxidized horseradish peroxidase (HRP) by duct cells of the rat parotid gland. J Cell Biol 99:379a

  • Danon D, Goldstein L, Marikovsky Y, Skutelsky E (1972) Use of cationized ferritin as a label of negative charges on cell surfaces. J Ultrastrucl Res 38:500–510

    Google Scholar 

  • Farrant JL (1954) An electron microscopic study of ferritin. Biochim Biophys Acta 13:569–576

    Google Scholar 

  • Farquhar MG (1978) Recovery of surface membrane in anterior pituitary cells. Variations in traffic detected with anionic and cationic ferritin. J Cell Biol 77:R35-R42

    Google Scholar 

  • Farquhar MG (1981) Membrane recycling in secretory cells: Implications for traffic of products and specialized membranes within the Golgi complex. Methods Cell Biol 23:399–427

    Google Scholar 

  • Hand AR (1979) Synthesis of secretory and plasma membrane glycoproteins by striated duct cells of rat salivary glands as visualized by radioautography after 3H-fucose injection. Anat Rec 195:317–340

    Google Scholar 

  • Hand AR, Ball WD (1986) Organ specificity and subcellular localization of perinatal submandibular gland (SMG) proteins. J Dent Res 65:325

    Google Scholar 

  • Hand AR, Coleman R, Mazariegos MR, Lustmann J, Lotti LV (1987) Endocytosis of proteins by salivary gland duct cells. J Dent Res (in press)

  • Hand AR, Weiss RE (1984) Effects of streptozotocin-induced diabetes on the rat parotid gland. Lab Invest 51:429–440

    Google Scholar 

  • Hanks CT, Chaudhry AP (1971) Regeneration of rat submandibular gland following partial extirpation. A light and electron microscopic study. Am J Anat 130:195–208

    Google Scholar 

  • Herzog V, Miller F (1979) Membrane retrieval in epithelial cells of isolated thyroid follicles. Eur J Cell Biol 19:203–215

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137a-138a

    Google Scholar 

  • Korsrud FR, Brandtzaeg P (1982) Characterization of epithelial elements in human major salivary glands: localization of amylase, lactoferrin, lysozyme, secretory component, and secretory immunoglobulins by paired immunofluorescence staining. J Histochem Cytochem 30:657–666

    Google Scholar 

  • Lima TG, Haddad A, Fava-de-Moraes F (1977) Glycoprotein secretion in the mouse submandibular gland as revealed by radioautography after l-3H-fucose injection. Cell Tissue Res 183:519–530

    Google Scholar 

  • Maunsbach AB (1966) Absorption of ferritin by rat kidney proximal tubule cells. Electron microscopic observations of the initial uptake phase in cells of microperfused single proximal tubules. J Ultrastruct Res 16:1–12

    Google Scholar 

  • Mazariegos MR, Tice LW, Hand AR (1984) Alteration of tight junctional permeability in the rat parotid gland after isoproterenol stimulation. J Cell Biol 98:1865–1877

    Google Scholar 

  • Nichols BA (1982) Uptake and digestion of horseradish peroxidase in rabbit alveolar macrophages. Formation of a pathway connecting lysosomes to the cell surface. Lab Invest 47:235–246

    Google Scholar 

  • Nustad K, Ørstavik TB, Gautvik KM, Pierce JV (1978) Glandular kallikreins. Gen Pharmacol 9:1–9

    Google Scholar 

  • Oliver C, Hand AR (1978) Uptake and fate of luminally administered horseradish peroxidase in resting and stimulated rat parotid acinar cells. J Cell Biol 76:207–220

    Google Scholar 

  • Ørstavik TB (1980) The kallikrein-kinin system in exocrine organs. J Histochem Cytochem 28:881–889

    Google Scholar 

  • Ottosen PD, Courtoy PJ, Farquhar MG (1980) Pathways followed by membrane recovered from the surface of plasma cells and myeloma cells. J Exp Med 152:1–19

    Google Scholar 

  • Parks HF (1961) On the fine structure of the parotid gland of mouse and rat. Am J Anat 108:303–329

    Google Scholar 

  • Qwarnström EE, Hand AR (1982) A light and electron microscopic study of the distribution and effects of water-soluble radiographic contrast medium after retrograde infusion into the rat submandibular gland. Arch Oral Biol 27:117–127

    Google Scholar 

  • Riva A, Testa-Riva F, Del Fiacco M, Lantini MS (1976) Fine structure and cytochemistry of the intralobular ducts of the human parotid gland. J Anat 122:627–640

    Google Scholar 

  • Rutberg U (1961) Ultrastructure and secretory mechanism of the parotid gland. Acta Odont Scand [Suppl] 19:30

    Google Scholar 

  • Schneyer LH, Young JA, Schneyer CA (1972) Salivary secretion of electrolytes. Physiol Rev 52:720–777

    Google Scholar 

  • Scott BL (1969) Colloidal tracer studies on the striated ducts in rat submaxillary glands. J Cell Biol 43:126a

    Google Scholar 

  • Scott BL, Pease DC (1959) Electron microscopy of the salivary and lacrimal glands of the rat. Am J Anat 104:115–140

    Google Scholar 

  • Shackleford JM, Wilborn WH (1970) Ultrastructural aspects of cat submandibular glands. J Morphol 131:253–276

    Google Scholar 

  • Smith PH, Patel DG (1984) Immunochemical studies of the insulinlike material in the parotid gland of rats. Diabetes 33:661–666

    Google Scholar 

  • Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    CAS  PubMed  Google Scholar 

  • Storrie B, Pool RR Jr, Sachdeva M, Maurey KM, Oliver C (1984) Evidence for both prelysosomal and lysosomal intermediates in endocytic pathways. J Cell Biol 98:108–115

    Google Scholar 

  • Tamarin A, Sreebny LM (1965) The rat submaxillary gland. A correlative study by light and electron microscopy. J Morphol 117:295–352

    Google Scholar 

  • Tandler B, MacCallum DK (1974) Ultrastructure and histochemistry of the submandibular gland of the European hedgehog, Erinaceus europaeus L. II. Intercalated ducts and granular striated ducts. J Anat 117:117–131

    Google Scholar 

  • Testa-Riva F (1977) Ultrastructure of human submandibular gland. J Submicrosc Cytol 9:251–266

    Google Scholar 

  • Thyberg J (1980) Internalization of cationized ferritin into the Golgi complex of cultured mouse peritoneal macrophages. Effects of colchicine and cytochalasin B. Eur J Cell Biol 23:95–103

    Google Scholar 

  • Thyberg J, Nilsson J, Hellgren D (1980) Recirculation of cationized ferritin in cultured mouse peritoneal macrophages. Electron microscopic and cytochemical studies with double-labeling technique. Eur J Cell Biol 23:85–94

    Google Scholar 

  • van Deurs B, Christensen El (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

    Google Scholar 

  • 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

    Google Scholar 

  • Yagil C, Michaeli Y, Zajicek G (1985) Compensatory proliferative response of the rat submandibular salivary gland to unilateral extirpation. Virchows Arch (Cell Pathol) 49:83–92

    Google Scholar 

  • Young JA, Schneyer CA (1981) Composition of saliva in mammalia. Aust J Exp Biol Med Sci 59:1–53

    Google Scholar 

  • Young JA, van Lennep EW (1978) The morphology of salivary glands. Academic Press, London

    Google Scholar 

  • Young JA, van Lennep EW (1979) Transport in salivary and salt glands. In: Giebisch G, Tosteson DC, Ussing HH (eds) Membrane transport in biology, vol 4B. Springer, Berlin, pp 563–674

    Google Scholar 

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Coleman, R., Hand, A.R. Endocytosis of native and cationized ferritin by intralobular duct cells of the rat parotid gland. Cell Tissue Res. 249, 577–586 (1987). https://doi.org/10.1007/BF00217329

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