Abstract
Tuft cells, also known as brush cells, are widespread in the hollow organs of the digestive tract including the duct system of the salivary gland and in the respiratory tract, from simple vertebrates to humans. The shape of tuft cells varies from pear-shaped, to barrel-shaped and goblet-shaped, apparently depending on the plane of section. The most characteristic morphological features of tuft cells are their long and blunt microvilli, which have prominent rootlets, and a well developed tubulovesicular system in the supranuclear cytoplasm. Both the microvilli and tubulovesicular system can be labeled with lectin and periodic acid-thiocarbohydrazide-silver proteinate-physical development (PA-TCH-SP-PD), suggesting a relationship between them. Many spheres observed among the microvilli seem to originate from the head of a polyp-like structure protruding into the vesicles, suggesting some type of apocrine secretion. During mammalian development, tuft cells increase around the time of weaning as neonates gradually become accustomed to solid food. Tuft cells in the rat gallbladder and stomach possess intermediate filaments, that is, neurofilaments and cytokeratin-18 filaments. Despite numerous morphological studies, the functions of tuft cells are still obscure. The discovery of the presence of α-gustducin has provided a clue to the long-sought function of tuft cells, which appear to possess the cellular and molecular basis for chemoreception. The present review discusses the three currently proposed functions of tuft cells — secretory, absorptive and receptive — on the basis of morphological, histochemical and cytochemical evidence.
Similar content being viewed by others
References
Afzelius BA (1984) Glycocalyx and glycocalyceal bodies in the respiratory epithelium of nose and bronchi. Ultrastruct Pathol 7, 1–8.
Allan EM (1978) The ultrastructure of the brush cell in bovine lung. Res Vet Sci 25, 314–17.
Chang LY, Merceer RR, Crapo JD (1986) Differential distribution of brush cells in the rat lung. Anat Rec 216, 49–54.
Christensen TG, Breuer R, Hornstra LJ, Lucey EC, Snider GL (1987) The ultrastructure of hamster bronchial epithelium. Exp Lung Res 13, 253–77.
Cutz E (1987) Cytomorphology and differentiation of airway epithelium in developing human lung. In: Lung Carcinomas (McDowell EM, ed.). Churchill Livingstone, New York, 1-41.
DiMaio MF, Dische R, Gordon RE, Kattan M (1988) Alveolar brush cells in an infant with desquamative interstitial pneumonitis. Pediatr Pulmonol 4, 185–91.
DiMaio MF, Kattan M, Ciurea D, Gil J, Dische R (1990) Brush cells in the human fetal trachea. Pediatr Pulmonol 8, 40–44.
Ellingr A, Gruber K, Stockinger L (1994) Glycocalyceal bodies: A marker for different epithelial cell types in human airways. J Submicrosc Cytol 19, 311–20.
Ferguson DJ (1969) Structure of antral mucosa. Surgery 65, 280–91.
Filippenko LN (1978) Light and electron microscopic study of rat lung brush alveolocytes in rats. Biull Eksp Biol Med 92, 616–20.
Foliguet B, Grignon G (1980) Type III pneumocyte. The alveolar brush-border cell in rat lung. Study by transmission electron microscopy. Poumon Coeur 36, 149–53.
Gebhard A, Gebert A (1999) Brush cells of the mouse intestine possess a specialized glycocalyx as revealed by quantitative lectin histochemistry: Further evidence for a sensory function. J Histochem Cytochem 47, 799–808.
Ghadially FN (1985) Filamentous core rootlets and glycocalyceal bodies. In: Diagnostic Electron Microscopy of Tumor (Ghadially FN, ed.). Butterworths, London, 334-42.
Gomi T, Kimura A, Kikuch Y et al. (1991) Electron-microscopic observations of the alveolar brush cell of the rat. Acta Anat 141, 294–301.
Gomi T, Kimura A, Tsuchiya H, Hashimoto T, Higashi K, Sasa S (1987) Electron microscopic observations of the alveolar brush cell of the Bullfrog. Zool Sci 4, 613–20.
Hammond JB, LaDeur L (1968) Fibrillovesicular cells in the fundic glands of the canine stomach: Evidence for a new cell type. Anat Rec 161, 394–412.
Hand AR (1981) Ultrastructure of the main excretory ducts of the rat parotid and submandibular gland. J Dent Res 60A, 395.
Higashi K, Gomi T, Soeda M, Sasa S, Kimura A, Kikuchi Y (1989) New morphological aspects of the brush cells in the main excretory ducts of the rat submandibular gland. Zool Sci 6, 675–80.
Hijiya K (1978) Electron microscope study of the alveolar brush cell. J Electron Microsc 27, 223–7.
Hijiya K, Okada Y, Tankawa H (1977) Ultrastructural study of the alveolar brush cell. J Electron Microsc 26, 321–9.
Höfer D, Drenckhahn D (1992) Identification of brush cells in the alimentary and respiratory system by antibodies to villin and fimbrin. Histochemistry 98, 237–42.
Höfer D, Drenckhahn D (1996) Cytoskeletal markers allowing discrimination between brush cells and other epithelial cells of the gut including enteroendocrine cells. Histochem Cell Biol 105, 405–12.
Höfer D, Drenckhahn D (1998) Identification of the taste cell G-protein, α-gustducin, in brush cells of the rat pancreatic duct system. Histochem Cell Biol 110, 303–9.
Höfer D, Puschel B, Drenckhahn D (1996) Taste receptor-like cells in the gut identified by expression of α-gustducin. Proc Natl Acad Sci USA 93, 6631–4.
Höfer D, Shin DW, Drenckhahn D (2000) Identification of cytoskeletal markers for the different microvilli and cell types of the rat vomeronasal sensory epithelium. J Neurocytol 29, 147–56.
Iseki S (1991) Postnatal development of the brush cells in the common bile duct of the rat. Cell Tissue Res 266, 507–10.
Iseki S, Kanda T, Hitomi M, Ono T (1991) Ontogenic appearance of three fatty acid binding proteins in the rat stomach. Anat Rec 229, 51–60.
Iseki S, Kondo H (1990) An immunocytochemical study on the occurrence of liver fatty-acid-binding protein in the digestive organs of rats: Specific localization in the D cells and brush cells. Acta Anat 138, 15–23.
Ishida H (1977) Fine structural study on the postnatal development of the rat tracheal mucosa with special reference to the brush cells. Yokohama Med Bull 28, 123–47.
Isomäki AM (1973) A new cell type (tuft cell) in the gastrointestinal mucosa of the rat. Acta Pathol Microbiol Scand Sect A 240 (Suppl), 1–35.
Ito T, Kitamura H, Inayama Y, Nozawa A, Kanisawa M (1992) Uptake and intracellular transport of cationic ferritin in the bronchiolar and alveolar epithelia of the rat. Cell. Tissue Cell Res 268, 335–40.
Järvi O (1961) A review of the part played by gastrointestinal heterotopias in neoplasmogenesis. Proc Finn Acad Sci (letters), 151–87.
Järvi O, Keyrilainen O (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 111 (Suppl), 72–3.
Jeffery PK, Reid L (1975) New observations of rat airway epithelium: A quantitative and electron microscopic study. J Anat 120, 295–320.
Johnson FR, Young BA (1968) Undifferentiated cells in gastric mucosa. J Anat 102, 541–51.
Kasper M, Höfer D, Woodcock-Mitchell L et al. (1994) Colocalization of cytokeratin 18 and villin in type III alveolar cells (brush cells) of the rat lung. Histochemistry 101, 57–62.
Kugler P, Höfer D, Mayer B, Drenckhahn D (1994) Nitric oxide synthase and NADP-linked glucose-6-phosphate dehydrogenase are co-localized in brush cells of rat stomach and pancreas. J Histochem Cytochem 42, 1317–21.
Leeson TS (1961) The development of the trachea in the rabbit, with particular reference to its fine structure. Anat Anz 110, 214–23.
Luciano L, Armbruckner L, Sewing KF, Real E (1993) Isolated brush cells of the rat stomach retain their structural polarity. Cell Tissue Res 271, 47–57.
Luciano L, Castellucci M, Real E (1981) The brush cells of the common bile duct of the rat. This section, freeze-fracture and scanning electron microscopy. Cell Tissue Res 218, 403–20.
Luciano L, Groos S, Reale E (2003) Brush cells of rodent gallbladder and stomach epithelia express neurofilaments. J Histochem Cytochem 51, 187–98.
Luciano L, Real E (1969) A new cell type (‘brush cell’) in the gallbladder epithelium of the mouse. J Submicrosc Cytol 1, 153–8.
Luciano L, Real E (1979) A new morphological aspect of the brush cells of the mouse gallbladder epithelium. Cell Tissue Res 201, 37–44.
Luciano L, Real E (1990) Brush cells of the mouse gallbladder. Cell Tissue Res 262, 339–49.
Luciano L, Real E (1992) The ‘limiting ridge’ of the rat stomach. Arch Histol Cytol 55, 131–8.
Luciano L, Real E (1997) Presence of brush cells in the mouse gallbladder. Microsc Res Techn 38, 598–608.
Luciano L, Real E, Ruska H (1968) Über eine ‘chemorezeptive’ Sinneszelle in der Trachea der Ratte. Z Zellforsch 85, 350–75.
Luciano L, Real E, Ruska H (1969) Burstenzellen im Alveolarepithel der Rattenlunge. Z Zellforsch 95, 198–201.
Luciano L, Real E, Von Engelhardt W (1980) The fine structure of the stomach mucosa of the Llama (Llama guanacoe). II. The fundic region of the hind stomach. Cell Tissue Res 208, 207–28.
Margolskee RF (2002) Molecular mechanisms of bitter and sweet taste transduction. J Biol Chem 277, 1–4.
McDowell EM, Barett LA, Glavin F, Harris CC, Trump BF (1978) The respiratory epithelium. I. Human bronchus. J Natl Cancer Inst 61, 539–45.
McLaughlin SK, McKinnon PJ, Margolskee RF (1992) Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature 357, 563–9.
Meyrick B, Reid L (1968) The alveolar brush cell in rat lung: A third pneumonocyte. J Ultrastruct Res 23, 71–80.
Monterio-Riviere NA, Popp JA (1984) Ultrastructural characterization of the nasal respiratory epithelium in the rat. Am J Anat 169, 31–43.
Moxey PC, Trier JS (1978) Specialized cell types in the human fetal small intestine. Anat Rec 191, 269–86.
Murayama T, Kataoka H, Koiata H, Nabeshima K, Koono M (1991) Glycocalyceal bodies in a human rectal carcinoma cell line and their intestinal collagenolytic activities. Virchows Arch B Cell Pathol 60, 263–70.
Nabeyama A, Leblond CP (1974) ‘Caveolated cells’ characterized by deep surface invaginations and abundant filaments in mouse gastro-intestinal epithelia. Am J Anat 140, 147–66.
Nevalainen TJ (1977) Ultrastructural characteristics of tuft cells in mouse gallbladder epithelium. Acta Anat 98, 210–20.
Ogata T (2000) Mammalian tuft (brush) cells and chloride cells of other vertebrates share a similar structure and cytochemical reactivities. Acta Histochem Cytochem 33, 439–49.
Ohiwa K, Harada T, Morikawa TS, Nakamura T (1994) Immuno-electron microscopic localization of carcinoembryonic antigen in gastric adenocarcinoma cell lines. Pathol Int 44, 635–44.
Ozzello L, Savary M, Roethlisberger B (1977) Columnar mucosa of the distal esophagus in patients with gastroesophageal reflux. Pathol Annu 12, 41–86.
Podokowa D, Goniakowska-Witalinska L (2002) Adaptations to the air breathing in the posterior intestine of the catfish (Corydoras aeneus: Callichthyidae). A histological and ultrastructural study. Folia Biol (Krakow) 50, 69–82.
Raeder MG (1992) The origin of and subcellular mechanisms causing pancreatic bicarbonate secretion. Gastroenterology 103, 1674–84.
Reid L, Meyrick B, Antony VB, Chang LY, Crapo JD, Reynolds HY (2005) The mysterious pulmonary brush cells: A cell in search of a function. Am J Respir Crit Care Med 172, 136–9.
Rhodin JAG (1959) Ultrastructure of the tracheal ciliated mucosa in rat and man. Ann Otol Rhinol Laryngol 68, 964–74.
Rhodin JAG (1966) Ultrastructure and function of the human tracheal mucosa. The ciliated cell. Am Rev Respir Dis 93, 1–15.
Rhodin JAG, Dalhamn D (1956) Electron microscopy of the trachea ciliated mucosa in rat. Z Zellforsch 44, 345–412.
Riches DJ (1972) Ultrastructural observations on the common bile duct epithelium of the rat. J Anat 111, 157–70.
Sato A (1980) Fine structure of the main excretory duct of rat submandibular gland. Biol Cell 39, 237–40.
Sato A (1982) Scanning and transmission electron microscopical study of the main excretory duct of rat major salivary glands. J Kyushu Dent Soc 36, 610–31.
Sato A, Hamano M, Miyoshi S (1998) Increasing frequency of occurrence of tuft cells in the main excretory duct during postnatal development of the rat submandibular gland. Anat Rec 252, 276–80.
Sato A, Hisanaga Y, Inoue Y, Nagato T, Toh H (2002) Three-dimensional structure of apical vesicles of tuft cells in the main excretory duct of the rat submandibular gland. Eur J Morphol 40, 235–9.
Sato A, Kodama J, Inoue Y, Nagato T (2004) Analysis of the tubulovesicular system of tuft cells in the main excretory duct of the rat submandibular gland by EFTEM-TEM tomography. 16th International congress of the IFAA proceedings. Anat Sci Int 79, 125.
Sato A, Miyoshi S (1988) Ultrastructure of the main excretory duct epithelia of the rat parotid and submandibular glands with a review of the literature. Anat Rec 220, 239–51.
Sato A, Miyoshi S (1996) Tuft cells in the main excretory duct epithelium of the three major rat salivary glands. Eur J Morphol 34, 225–8.
Sato A, Miyoshi S (1997) Fine structure of tuft cells of the main excretory duct epithelium in the rat submandibular gland. Anat Rec 248, 325–31.
Sato A, Miyoshi S (1998a) Topographical distribution of cells in the rat submandibular gland duct system with special reference to dark cells and tuft cells. Anat Rec 252, 159–64.
Sato A, Miyoshi S (1998b) Cells in the duct system of the rat submandibular gland. Eur J Morphol 36, 61–6.
Sato A, Suganuma T, Ide S, Kawano J, Nagato T (2000) Tuft cells in the main excretory duct of the rat submandibular gland. Eur J Morphol 38, 227–31.
Sbarbati A, Merigo F, Benati D et al. (2004) Identification and characterization of a specific sensory epithelium in the rat larynx. J Comp Neurol 475, 188–201.
Sbarbati A, Osculati F (2005) A new fate for old cells: Brush cells and related elements. J Anat 206, 349–58.
Schmidt H, Lohmann S, Walter U (1993) The nitric oxide and cGMP signal-transduction pathway. Biochim Biophys Acta 1178, 153–75.
Schofield GC (1970) Columnar cells with secretory granules in the large intestine of the macaque (Cynamolgus irus). J Anat 106, 1–14.
Shackleford JM, Schneyer LH (1971) Ultrastructural aspects of the main excretory of rat submandibular gland. Anat Rec 169, 693–705.
Silva DG (1966) The structure of multivesicular cells with large microvilli in the epithelium of the mouse colon. J Ultrastruct Res 16, 639–705.
Sugimoto K, Ichikawa Y, Nakamura I (1983) Endogenous peroxidase activity in brush cell-like cells in the large intestine of the bullfrog tadpole, Rana catesbeiana. Cell Tissue Res 230, 451–61.
Sweetser DA, Heuckeroth RO, Gordon JI (1987) The metabolic significance of mammalian fatty-acid-binding proteins: Abundant proteins in search of a function. Annu Rev Nutr 7, 337–57.
Taira K, Shibasaki S (1978) A fine structure study of the nonciliated cells in the mouse tracheal epithelium with special reference to the relation of ‘brush cells’ and ‘endocrine cells’. Arch Histol Jpn 41, 351–66.
Thurbeck WM (1990) A rose is a rose is a rose, but what is a brush cell? Pediatr Pulmonol 8, 3.
Trier JS (1963) Studies on small intestinal crypt epithelium. I. The fine structure of the crypt epithelium of the proximal small intestine of fasting humans. J Cell Biol 18, 599–620.
Trier JS, Allan CH, Marcial MA, Madara JL (1987) Structural features of the apical and tubulovesicular membranes of rodent small intestinal tuft cells. Anat Rec 219, 69–77.
Tsubouchi S, Leblond CP (1979) Migration 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, 431–51.
Watson JH, Brinkman GL (1964) Electron microscopy of the epithelial cells of normal and bronchitic human bronchus. Am Rev Respir Dis 90, 851–66.
Wattel W, Geuze JJ (1978) The cells of the rat gastric groove and cardia. Cell Tissue Res 186, 375–91.
Weyrauch KD, Schnorr B (1976) Ultrastructure of the epithelium of the major pancreatic duct in sheep. Acta Anat 96, 232–47.
Wille KH (2001) The functional morphology of the large intestinal mucosa of the ox (Bos promigenius f. taurus), sheep (Ovis ammon f. aries) and goat (Capra aegagrus f. hircus). Anat Histol Embryol 30, 65–76.
Wong GT, Gannon KS, Margolskee RF (1996) Transduction of bitter and sweet taste by gustducin. Nature 381, 796–800.
Yang R, Tabata S, Crowley HH, Margolskee RF, Kinnamon JC (2000) Ultrastructural localization of gustducin immuno-reactivity in microvilli of type II cells in the rat. J Comp Neurol 425, 139–51.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sato, A. Tuft cells. Anato Sci Int 82, 187–199 (2007). https://doi.org/10.1111/j.1447-073X.2007.00188.x
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1111/j.1447-073X.2007.00188.x