The ultrastructure of the human circumvallate papilla. I. Cilia of the papillary cryptкод для вставкиСкачать
The Ultrastructure of the Human Circumvallate Papilla I. CILIA OF THE PAPILLARY CRYPT CARL F. T. MATTERN, WENDELL A. DANIEL AND ROBERT I. HENKIN1 U.S. Department of Health, Education and Welfare, Public Health Service, National Institutes of Health, National Institute of Allergy and Infectious Diseases, Lnboratoiy of Viral Diseases and 1 National Heart Institute, Experimental Therapeutics Branch, Bethseda, Wlnryland 20014 ABSTRACT Cilia-bearing cells have been observed near the bottom of the crypt of the human circumvallate papilla, between the lower taste buds and the duct of van Ebner's gland. It is likely that they serve one or more of the following functions: cleansing the papillary crypt, circulation of tastants, and bathing the pores of the taste bud in the various fluid secretions of the oral cavity. The kinetosomes of these cells were observed to possess typical transitional fibers and rootlets with periodic structure. In addition, a single, lateral, satellite-like projection from the midregion of the kinetosome was connected to microtubules which coursed deeply with the mitochondria-rich cytoplasm as did fine fibrils and some rootlets. Human circumvallate papillae are tion of cilia in this location will be preslightly raised, verrucous structures which sented. are located on the posterior third of the MATERIALS AND METHODS tongue, mainly in or near the sulcus terminalis. A trench or crypt surrounds each Several circumvallate papillae were surpapilla as a circular invagination of the gically excised in toto from a 42 year old, epithelium. On the lateral aspect of the Caucasian female who subsequently unpapilla as many as 100 taste buds may be derwent surgery for a malignant process found opening into the crypt (fig. 1 ) . Von involving the maxillary sinus. Prior to opEbner's glands are serous glands which lie eration, detection and recognition threshamong lingual muscle fibers beneath the olds for four .qualities of taste (salt, sweet, epithelium of the floor of the crypt. Their sour and bitter) were measured in the oral branching ducts converge to empty into cavity by techniques previously described the bottom of the papillary trench (Bloom in detail (Henkin et al., '63; Henkin and and Fawcett, '68). Christiansen, '67). These thresholds were Motile cilia are found extensively within within normal limits for each quality. the respiratory tract. Other cilia, apparThe excised papillae were immediately ently serving some function in sensory re- immersed in 2.5% glutaraldehyde i n phosception, are found in the olfactory epi- phate buffer (pH 7.4). After fixation for thelium and in other sensory organs of at least 24 hours (4°C) the papillae were man and other animals. However, they sectioned radially into six portions, posthave not been demonstrated in the oral fixed i n 1 % osmium tetroxide (phosphate cavity i n higher animals. This communica- buffered to pH 7.4), and embedded in tion will demonstrate the presence of cilia- epon-araldite. Sections were cut with a diabearing cells near the floor of the crypt of mond knife, stained successively with uracircumvallate papillae i n the vicinity of nyl acetate and lead citrate, and examined both the taste buds and the ducts of von in RCA EMU 3E or 3H electron microEbner's glands. Some ultrastructural de- scopes. tails of these ciliated cells will also be described. Hypotheses concerning the funcReceived Oct. 27, '69. Accepted Jan. 14. '70. ANAT. REC., 167: 175-182 175 176 C . F. T. MATTERN, W. A. DANIEL A N D R. I. H E N K I N RESULTS of this row is virtuallv imaossible to determine by electron microscopy, and we have been unable to identify these cells by light microscopy. We have observed as many as seven consecutive cilia-bearing cells in one section. Cilia-bearing cells have been observed in three of six portions into which a single papilla had been divided. They are located approximately 0.25 to 0.50 m m beneath the lowest taste buds. The cytoplasm of the cilia-bearing cells stains less densely and their mitochondria are more numerous and more elongated than the adjacent epithelial cells. About 280 cilia and kinetosomes are seen in the large cluster (fig. 3 ) which represents the cilia of a single cell. Numerous microvilli are interspersed with the cilia. I n figures 4 and 5 some details of the kinetosome are seen. In addition to the rootlet with its typical periodic structure each kinetosome has a single lateral projec, A typical circumvallate papilla is shown schematically in figure 1. The lingual surface consists solely of epithelium which extends into the crypt. Over a substantial portion of the lateral surface of the papilla numerous taste buds open into the crypt through pores. Internally the buds are continuous with unmyelinated nerves which are present within the lamina propria along with blood vessels, lymphatics, other unmyelinated nerve fibers and collagenous stroma. The ultrastructure of the human circumvallate taste bud will be the subject of a subsequent communication. A section nearly perpendicular to the epithelial surface of the crypt is presented in figure 2, and one tangent to the surface in figure 3 . Cilia bearing cells are seen surrounded by epithelial cells and they appear to be arranged in a double row. The extent A Fig. 1 Schematic drawing of a circumvallate papilla. L, lingual surface; E, epithelium; B, taste buds; P, taste pores; C, cilia; D, duct of von Ebner’s gland, G ; L. P. lamina propria containing nerves, N. Blood vessels, lymphatics, unmyelinated nerve fibers not related to the taste buds and the collagenous stroma are not shown for purposes of ciarity. CILIA OF THE CIRCUMVALLATE PAPILLA 177 Fig. 2 A section nearly perpendicular to the epithelial surface showing two cilia-bearing cells. C, cilia; K, kinetosomes; MV, microvilli; M, mitochondria. x 6,500. tion which i s reminiscent of satellite structures frequently seen around centrioles (Fawcett, '66). In addition, near the cell membrane the kinetcisomes demonstrate transitional fibers which appear as nine radiating spokes and which presumably attach to the inner surface of the cell. A number of microtubules are also seen in figure 4 apparently coursing from the kinetosome to a n unknown region deeper within the cytoplasm. As may be seen in figure 6 one or possibly more microtubules appear to arise from or attach to the lateral satellite. In several sections we have observed large rootlet structures deep in the cytoplasm of cilia-bearing cells. Such a rootlet is seen near the nucleus in figure 7. 178 C. F. T. M A T T E R N , W. A. D A N I E L AND R. I. HENKIN Fig. 3 A section nearly tangent to the epithelial surface of cilia-bearing cells. Legends a s in figure 2. >: 7,000. In other cilia-bearing cells both microtubules and fine fibrils are interspersed with mitochondria and in some instances the fine fibrils are closely applied to mitochondria. DISCUSSION To our knowledge this is the first demonstration of the presence of locomotor cilia on the tongue of vertebrates. In the human circumvallate papilla these cilia-bearing Fig. 4 Higher magnification of a section similar to figure 2. C, cilia; MV, microvilli; K, kinetosomes; R, rootlets; S, satellite-like, lateral projection; MT, microtubules; M. mitochondria. x 26,200. Fig. 5 Higher magnification of a portion of figure 3. In addition to numerous cilia, microvilli, and kinetosomes, in cross section, satellite-like lateral projections ( S ) and superficial transitional fibers ( T ) are apparent. x 15,000. 180 C . F. T. MATTERN, W . A. DANIEL AND R. I. HENKIN Fig. 6 Three views of kinetosomes ( K ) and lateral satellites ( S ) with attached microtubules (arrows), left x 26,100, center and right X 46,500. Fig. 7 Kinetosomal rootlets (R) deep in the cytoplasm are seen near the nucleus ( N ) of a ciliabearing cell. x 28,000. CILIA OF THE CIRCUMVALLATE PAPILLA cells probably serve one or more of three functions : ( 1) removal of detritus and general cleansing of the crypt of the papilla; (2) assistance in the process of taste by circulation of tastants; and (3) circulation of the serous secretion of von Ebner's gland and other oral fluids which bathe the pores of these taste buds. Taste buds must be continually bathed in order for normal taste acuity to be maintained. This suggests an important relationship between cilia-bearing cells and oral secretions. This is supported by observations made in patients with Sjoegren's syndrome (rheumatoid arthritis with xerostomia and xerophthalmia) which indicate both a decreased taste acuity and absence of oral fluids (Henkin unpublished observations). As yet it is not possible to deduce the specifk function of the complex structures associated with the kinetosomes. These include the periodic rootlets, the lateral, satellite-like projections with attached microtubules passing into the mitochondriarich cytoplasm, and the fine filaments seen in proximity to the mitochondria. Similar periodic rootlets are commonly associated with kinetosomes throughout the animal kingdom and microtubules are often associated with centrioles and kinetosomes, 181 either directly or through satellites. The presence of mitochondria in proximity to these complexes suggests a role in supplying ATP as the energy source of cilia and flagella (Sleigh, '62). In a wide variety of systems these various structures have been implicated in a number of roles: support, coordination of cilia, ciliary bending, contraction or flexion and other specialized functions. However their speciflc structural-functional relationships are not completely understood (Sleigh, '62). LITERATURE CITED Bloom, W., and D. W. Fawcett 1968 A textbook of histology. W. B. Saunders Co., Ninth edition, Philadelphia. Fawcett, D. W. 1966 An atlas of fine structure. W. B. Saunders Co., Philadelphia. Henkin, R. I., and R. L. Christiansen 1967 Taste localization on the tongue, palate and pharynx of normal man. J. Appl. Physiol.. 22: 316. Henkin, R. I., J. R. Gill, Jr., and F. C. Bartter 1963 Studies in taste thresholds in normal man and in patients with adrenal cortical insufficiency: The role of adrenal cortical steroids and of serum sodium concentration. J. Clin. Invest., 42: 727. Sleigh, M. A. 1962 The biology of cilia and flagella. Permagon Press Ltd., Oxford.