Structural features of the apical and tubulovesicular membranes of rodent small intestinal tuft cells
Jerry S. Trier
Department of Medicine, Brigham and Women's Hospital and Harvard Medical School and the Harvard Digestive Diseases Center, Boston, MA 02115
Search for more papers by this authorCarol H. Allan
Department of Medicine, Brigham and Women's Hospital and Harvard Medical School and the Harvard Digestive Diseases Center, Boston, MA 02115
Search for more papers by this authorManuel A. Marcial
Department of Pathology, Brigham and Women's Hospital and Harvard Medical School and the Harvard Digestive Diseases Center, Boston, MA 02115
Search for more papers by this authorJames L. Madara
Department of Pathology, Brigham and Women's Hospital and Harvard Medical School and the Harvard Digestive Diseases Center, Boston, MA 02115
Search for more papers by this authorJerry S. Trier
Department of Medicine, Brigham and Women's Hospital and Harvard Medical School and the Harvard Digestive Diseases Center, Boston, MA 02115
Search for more papers by this authorCarol H. Allan
Department of Medicine, Brigham and Women's Hospital and Harvard Medical School and the Harvard Digestive Diseases Center, Boston, MA 02115
Search for more papers by this authorManuel A. Marcial
Department of Pathology, Brigham and Women's Hospital and Harvard Medical School and the Harvard Digestive Diseases Center, Boston, MA 02115
Search for more papers by this authorJames L. Madara
Department of Pathology, Brigham and Women's Hospital and Harvard Medical School and the Harvard Digestive Diseases Center, Boston, MA 02115
Search for more papers by this authorAbstract
Tuft cells are present in most columnar epithelia derived from endoderm including the small intestine. They are characterized by long, wide apical microvilli and an extensively developed cytoplasmic tubulovesicular system. We examined in detail the structural features of the apical plasma membrane of small intestinal tuft cells from adult guinea pigs, rats, and adult and suckling mice with freeze-fracture and conventional transmission electron microscopy methods and utilized cationized ferritin and horseradish peroxidase as tracers to determine whether tuft cells endocytose macromolecules. The microvillus membrane of intestinal tuft cells has few P-face intramembrane particles, displays little alkaline phosphatase activity, and is highly enriched in cholesterol. Tuft cell tight junctions resemble those of absorptive cells in strand count and strand-to-strand crosslinks but, unlike those of absorptive cells, they display many abluminal free-ending strands. Tuft cells of adult and suckling mouse intestine show no evidence of internalization of cationized ferritin or, in suckling mice, uptake of horseradish peroxidase. We conclude that the microvillus membrane of small intestinal tuft cells is protein poor but cholesterol-rich and that small intestinal tuft cells do not endocytose macromolecules in bulk from the intestinal lumen.
Literature Cited
- Allan, E. M. (1978) The ultrastructure of the brush cell in bovine lung. Res. Vet. Sci., 25: 314–317.
- Ferguson, D. J. (1969) Structure of antral gastric mucosa Surgery, 65: 280–291.
- Forstner, G. G., K., Tanaka, and K. J. Isselbacher (1968) Lipid composition of the isolated rat intestinal microvillus membrane. Biochem. J., 109: 51–59.
- Forte, T. M., T. E., Machen, and J. G. Forte (1977) Ultrastructural changes in oxyntic cells associated with secretory function: A membrane recycling nypothesis. Gastroenterology, 73: 941–955.
- Friend, D. S., and E. L. Bearer (1981) Beta-hydroxysterol distribution as determined by freeze-fracture cytochemistry. Histochem. J., 13: 536–546.
- Fujimoto, T., and K. Ogawa (1983) Uneven formation of filipinsterol complexes in frog urinary bladder epithelium. Acta Histochem. Cytochem., 16: 513–521.
- Gonnella, P. A., and M. R. Neutra (1984) Membrane-bound and fluidphase macromolecules enter separate prelysosomal compartments in absorptive cells of suckling rat ileum. J. Cell Biol., 99: 909–917.
- Graham, R. C., and M. J. Karnovsky (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.
- Hauser, H., K., However, R. M. C. Dawson, and D. E. Bowyer (1980) 1 Rabbit small intestinal brush border membrane preparation and lipid composition. Biochim. Biophys. Acta, 602: 567–577.
- Hugon, J., and M. Borgers (1966) Ultrastructural localization of alkaline phosphatase activity in the absorbing cells of the duodenum of mouse. J. Histochem. Cytochem., 14: 629–640.
- Isomäki, A. M. (1973) A new cell type (tuft cell) in the gastrointestinal mucosa of the rat. Acta Pathol. Microbiol. Scand A [Suppl.], 240: 1–35.
- Jarvi, O. H., and O. Keyrilainen (1955) On the cellular structures of the epithelial invasions in the glandular stomach of mice caused by intramural application of 20-methylcholanthrene. Acta. Pathol. Microbiol. Scand. A [Suppl.], 111: 72.
- Karnovsky, M. J. (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol., 27: 137 (Abstract).
- Luciano, L., E., Reale, and H. Ruska (1968) Uber eine glykogenheltige Burztenzelle in Rectum der Ratte. Z. Zellforsch., 91: 153–158.
- Luciano, L., and E. Reale (1969) A new cell type (“brush cell”) in the gallbladder epithelium of the mouse. J. Submicrosc. Cytol., 1: 43–52.
- Luciano, L., E., Reale, and H. Ruska (1969) Burstenzellen in Alveolarepithel der Rattenlunge. Z. Zellforsch., 95: 198–201.
- Luciano, L., and E. Reale (1979) A new morphological aspect of the brush cells of the mouse gallbladder epithelium. Cell Tissue Res., 201: 37–44.
- Luciano, L., M., Castellucci, and E. Reale (1981) The brush cells of the common bile duct of the rat. Thin section, freeze-fracture and scanning electron microscopy. Cell Tissue Res., 218: 403–420.
- Luciano, L., and E. Reale (1985) Filipin-cholesterol complexes (FCC) in the goblet cell granule membrane of the distal colon are arranged in a rhombic pattern. J. Histochem. Cytochem., 33: 360–366.
- Madara, J. L., and J. S. Trier (1982) Structure and permeability of goblet cell tight junctions in rat small intestine. J. Membr. Biol., 66: 145–157.
- Madara, J. L. (1983) Increases in guinea pig small intestinal transepithelial resistance induced by osmotic loads are accompanied by rapid alterations in absorptive-cell tight-junction structure. J. Cell Biol., 97: 125–136.
- Madara, J. L., W. A., Bye, and J. S. Trier (1984) Structural features of and cholesterol distribution in M-cell membranes in guinea pig, rat, and mouse Peyer's patches. Gastroenterology, 87: 1091–1103.
- Meyrick, B., and L. Reid (1968) The alveolar brush cell in rat lung–A third pneumocyte. J. Ultrastruct. Res., 23: 71–80.
- Nabeyama, A., and C. P. Leblond (1974) “Caveolated cells” characterized by deep surface invaginations and abundant filaments in mouse gastro-intestinal epithelia. Am. J. Anat., 140: 147–166.
- Owen, R. L. (1977) Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in the normal unobstructed mouse intestine: An ultrastructural study. Gastroenterology, 72: 440–451.
- Rhodin, J. A. G., and T. Dalhamn (1956) Electron microscopy of the tracheal ciliated mucosa in rat. Z. Zellforsch., 44: 345–412.
- Schliwa, M. (1984) Mechanisms of intracellular organelle transport. In: Cell and Muscle Motility. J. W. Shay, ed. Plenum Publishing Corp., New York, Vol. 5, pp. 1–82.
- Schofield, G. C., S. Ito, and R. P., Bolender (1979) Changes in membrane surface areas in mouse parietal cells in relation to high levels of acid secretion. J. Anat., 128: 669–692.
- Severs, N. J., and H. Robenek (1983) Detection of microdomains in biomembranes: An appraisal of recent developments in freeze-fracture cytochemistry. Biochim. Biophys. Acta 737: 373–408.
- Silva, D. G. (1966) The fine structure of multivesicular cells with large microvilli in the epithelium of mouse colon. J. Ultrastruct. Res., 16: 693–705.
- Steer, C. J., M., Bisher, R. Blumenthal, A. C. Steven (1984) Detection of membrane cholesterol by filipin in isolated rat liver coated vesicles is dependent upon removal of the clathrin coat. J. Cell Biol., 99: 315–319.
- Sugimoto, K., Y., Ichikawa, and I. Nakamura (1983) Endogenous peroxidase activity in brush cell-like cells in the large intestine of the bullfrog tadpole, Rana catesbeiana. Cell Tissue Res., 230: 451–461.
- Tilluck, T. W., R. E., Scott, and V. T. Marchesi (1972) The structure of erythrocyte membranes studied by freeze etching. II. Localization of receptors for phytohemagglutinin and influenza virus to the intramembranous particles. J. Exp. Med., 135: 1209–1227.
- Trier, J. S., and J. L. Madara (1984) Distribution of filipin-sterol complexes in villus goblet cell membranes of rat small intestine. Lab. Invest., 50: 673–682.
- Tsubouchi, S., and C. P. Leblond (1979) Micration and turnover of entero-endocrine and caveolated cells in the epithelium of the descending colon, as shown by radioautography after continuous infusion of 3H-thymidine into mice. Am. J. Anat., 156: 431–452.
- Vail, W. J., D., Papahadjopoulos, and M. A. Moscarello (1974) Interaction of a hydrophobic protein with liposomes. Evidence for particles seen in freeze-fracture as being proteins. Biochim. Biophys. Acta, 345: 463–467.
- Wattel, W., and J. J. Geuze (1978) The cells of the rat gastric groove and cardia. An ultrastructural and carbohydrate histochemical study, with special reference to the fibrillovesicular cells. Cell Tissue Res., 186: 375–391.
- Weyrauch, K. D., and D. Schnorr (1976) Die Feinstruktur des Epithels des Ductus pancreaticus major des Schafes. Acta Anat. (Basel), 96: 232–247.