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The Specialised Structure of Crypt Epithelium in the Human Palatine Tonsil and Its Functional Significance

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The Specialised Structure of Crypt Epithelium in the Human Palatine Tonsil and Its Functional Significance J. Anat. (1994) 185, pp. 111-127, with 21 figures Printed in Great Britain III The specialised structure of crypt epithelium in the human palatine tonsil and its functional significance MARTA E. PERRY Division of Anatomy and Cell Biology, United Medical and Dental Schools, Guy's Campus, London, U.K. (Accepted 18 January 1994) ABSTRACT Material from 25 human palatine tonsils was studied by light microscopy, immunocytochemistry, scanning and transmission electron microscopy. Special attention was focused on the structure of the epithelium lining the tonsillar crypts in the context of its ascribed immunological functions. This epithelium was not uniform and contained patches of stratified squamous nonkeratinising epithelium and patches of reticulated sponge-like epithelium. The degree of reticulation of the epithelial cells and the infiltration of nonepithelial cells varied. Reticulated patches were associated with disruptions in the continuity of basement membrane, and often also with desquamation of the upper cell layers, and contained numerous small blood vessels. The epithelial cells showed considerable variation in their morphology when surrounded by infiltrating cells. The rearrangement of their cytoskeleton and redistribution of desmosomal contacts indicate the responsiveness and dynamic nature of such epithelium. Cytoplasmic glycogen granules, located in the upper strata, suggest the possibility of energy-demanding functions such as absorption and secretion. The numerous membrane-coating granules may have contributed to cell membrane thickening and possibly also to tonsillar mucosal protection. Some areas contained a few keratohyalin granules but there was little evidence of keratinisation. The presence, and sometimes the predominance, of nonepithelial cells was characteristic of the reticulated epithelium. T and B cells often infiltrated the whole epithelial thickness, and many plasma cells were located around intraepithelial vessels, while macrophages and interdigitating cells showed a patchy distribution. It is proposed that the major functions of the reticulated epithelium are: (1) to provide a favourable environment for the intimate contact between the effector cells of immune responses; (2) to facilitate direct transport of antigens; (3) to synthesise the secretory component continually; and (4) to contain a pool of immunoglobulins. Thus the reticulated epithelium lining the tonsillar crypts represents a specialised compartment, important in the immunological functions of the tonsil as a whole. Key words: Lymphoid tissue; reticulated cells; mucosal protection. form ofthe stratified squamous epithelium that covers INTRODUCTION the oropharyngeal surface of the tonsil. As early as The epithelium of the human palatine tonsil is a site of 1884, St6hr recognised that crypt epithelium was interest because it overlies a mass of lymphoid tissue usually infiltrated by lymphocytes. This observation that forms a first line of defence in protecting the was later confirmed by Barnes (1923) and Kahler oropharyngeal isthmus, and as such is constantly (1933), the latter proposing that the function of the exposed both to airborne and alimentary antigens. palatine tonsil was 'protection and defence'. The surface area of the tonsillar epithelium available Fioretti (1957) termed the mixing of lymphoid and for this defensive role is maximised by the 10-30 epithelial cells in the crypt epithelium 'si'biosi blind-ending crypts and their rami (Kassay & Sandor, linfoepitheliale' tthe lymphoepithelial symbiosis). 1962; Olah, 1978), extending through the full thick- Hellman (1932) and Koburg (1967) likened the ness of the tonsil almost to reach its hemicapsule network ofepithelial cells to a sponge 'der epithelialer (Kassay, 1938; Fioretti, 1957). Schwammk6rper', which holds the lymphoid cells in The epithelium lining the crypts is a highly modified its interstices. In 1978 Olah termed this specialised Correspondence to Dr M. E. Perry, Division of Anatomy & Cell Biology, UMDS (Guy's Campus), London Bridge, London SEI 9RT, U.K. 112 Marta E. Perry dF. ,OW.- Nlv; Q.;a V it Of Aft,U-Au. v 4p Z o E reoi 4w -7N 47 4 s L d,--, 41 It ao .,w416 4 v. 4th 4NO I 4Q tvwo MtRy Z :R f n' 4W Ot"W'W A ; ,. C'm it as,' 4 J 6 40 0 '(4. 4L -4 i. WP-, 'ot. ". 4 o otj 46 v "P V'4 0-b "Nk ..4*A1. 41111illillimlo ;g. Vw, N. low .,ks 4P q 4j 106 4W 4*1 4D dp N 4F W & 4 Al 0 .41V 100'* Ow oP .11,10. *% 4.4 Wm* 4 N A& 419' *W' -.1AOV*l _0 di - -, l-- AF 'w OCI S M'. .114 ..w .T a Figs 1-4. For legend see opposite. Tonsillar crypt epithelium 113 crypt epithelium 'reticular epithelium' and found that were fixed in 10 % formol saline and processed for it lined most, though not all, of the cryptal surfaces. paraffin wax embedding. Subsequently, 2-4 gm sec- The nonepithelial elements identified in the reticulated tions were obtained, which were stained with haema- epithelium include lymphoid cells, numerous antigen toxylin and eosin, Heidenhain's azan and Gordon and presenting cells (Yamamoto et al. 1988; Perry & Sweet's stain for reticulin (Bancroft & Cook, 1984). Mustafa, 1992) and a network of small blood vessels The latter two were used to demonstrate the connec- (Fujihara et al. 1988, 1989; Perry et al. 1992a, b). tive tissue components of basement membranes of The significance of this specialised epithelium has both epithelia and blood vessels. been highlighted by Korsrud & Brandtzaeg (1981 a, b), Cellular inclusions. Sections were also stained using Brandtzaeg (1988) and Brandtzaeg & Halstensen the periodic acid-Schifftechnique (PAS) for examining (1992) following their comprehensive immunological glycogen distribution; performic acid-methylene blue studies on human palatine and nasopharyngeal (PAMB) for keratin, with human skin as a control; tonsils. They were the first to propose that in addition Gram's stain for keratohyalin; Alcian blue (range of to the germinal centre, mantle zone and interfollicular pH between 1 and 2) and Csaba's stain (acetate buffer regions, the tonsillar crypt epithelium functions as an pH 1.42) for mast cells; and Giemsa's stain for aiding additional lymphoid compartment by contributing to identification ofplasma cells. All methods were carried the production of immunocytes and to the protection out according to Bancroft & Cook (1984). of the mucosal surface (Korsrud & Brandtzaeg, Immunocytochemistry. Small pieces (- 5 mm3) of 1981 b; Cortesina et al. 1992; Kataura et al. 1992). fresh tissue were oriented using the binocular micro- The aim of the present study was to investigate the scope to ensure the presence of crypt epithelium in specialised structure ofthe crypt epithelium in relation subsequent sectioning. They were then embedded in to its ascribed immunological function, using light Tissue Tek and frozen in melting isopentane precooled microscopy, and scanning and transmission electron in liquid nitrogen. Frozen sections (4 gm) were microscopy. obtained, which together with the 2 jim paraffin sections, were used for immunocytochemistry. The antibodies applied were CD3 (anti-LEU-4) (Becton MATERIALS AND METHODS Dickinson Immunocytometry Systems) for T cells; Human palatine tonsils were obtained randomly from MB2 (Euro-Diagnostic BV, Holland) for B cells; and 26 children (17 boys and 9 girls) undergoing tonsil- S-100, Cow S-100 (Dakopatts, Denmark) for lectomy. The youngest child was aged 23 months, and macrophage/dendritic cells. The direct and indirect the oldest was 14 y 4 months at the time of the routine peroxidase-antiperoxidase (PAP) technique operation. Preoperative diagnoses ranged from was used to visualise the reactions. Incubation with recurrent tonsillitis and upper respiratory tract primary antibodies was carried out for 1 h in a wet infection, with or without otitis media, to the non- chamber at room temperature. Anti-LEU-4 and MB2 inflammatory condition of nasal obstruction with antibodies were used in 1/10 dilution and S-100 in nocturnal apnoea. None of the patients suffered from 1/75 dilution. Secondary antibodies used were 1/20 acute tonsillitis or had received a course of antibiotics dilution ofeither rabbit antimouse or swine antirabbit in the immediate preoperative period. conjugated antiserum, applied to the sections for 1 h or 30 min respectively, in a wet chamber at room temperature. Positive labelling was identified as Light microscopy distinctive brown reaction products visible with a light Architecture of the epithelia. Tonsillar samples, microscope. The PAP method was applied to control containing both oropharyngeal and crypt epithelia, sections with the omission of primary antibodies or Fig. 1. The oropharyngeal surface of the palatine tonsil (top) is covered with stratified squamous nonkeratinising epithelium, underlined by a connective tissue band (short arrows). Transected tonsillar crypt (long arrows). F, lymphoid follicles. Haematoxylin and eosin. Bar, 100 gm. Fig. 2. A patch ofreticulated epithelium (upper half) covered with a thin layer ofsquamous cells. Note distorted epithelial cells with attenuated cytoplasmic processes (arrowheads) and an indistinct boundary between the epithelium and the underlying lymphoid tissue (arrows). P, intraepithelial plasma cells. Haematoxylin and eosin. Bar, 25 gm. Fig. 3. Reticulated crypt epithelium containing many infiltrating nonepithelial cells and transected capillaries (arrows). The epithelial surface (right) shows a 'fountain-like' disruption. Haematoxylin and eosin. Bar, 25 gm. Fig. 4. Heavily reticulated patch of crypt epithelium containing a longitudinally
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