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Distribution of T-Cell Subsets and Immunoglobulin-Containing Cells in Nasal-Associated Lymphoid Tissue (NALT) of Chickens

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Distribution of T-Cell Subsets and Immunoglobulin-Containing Cells in Nasal-Associated Lymphoid Tissue (NALT) of Chickens Histol Histopathol (2000) 15: 713-720 Histology and 001: 10.14670/HH-15.713 Histopathology http://www.hh.um.es Cellular and Molecular Biology Distribution of T-cell subsets and immunoglobulin-containing cells in nasal-associated lymphoid tissue (NALT) of chickens K. Ohshima and K. Hiramatsu Laboratoryof Functional Anatomy, Faculty of Agriculture, Shinshu University, Ina, Japan Summary. The present study demonstrated the and to denote it as nasal-associated lymphoid tissue localization of the T-cell subsets (CD4+ and CD8+) and (NALT) in analogy with the gut- and bronchus­ immunoglobulin (Ig)-containing cells (IgA, IgM, and associated lymphoid tissue (GALT and BALT, IgG) in the nasal mucosa and its accessory structures. respectively). However, the nature of local immune These lymphoid structures may be compared with nasal­ responses, and the role of NALT in these responses have associated lymphoid tissue (NALT) of rats and mice. In rarely been studied, due to the absence of a suitable the chicken NALT, T-cell subsets were more widely model (Kuper et aI. , 1992). distributed than Ig-containing cells, especially in large Recently, the structure and development of NALT in lymphoid accumulations restricted to the respiratory the rat (Hameleers et aI., 1989; Spit et aI. , 1989; Kuper mucosa in the nasal cavity and the nasolacrimal duct. et aI. , 1990; van Poppel et aI., 1993) and mouse (van der These lymphoid accumulations in the mucosa of the Yen and Sminia, 1993; Heritage et aI., 1997) have been nasal cavity and nasolacrimal duct consisted of widely investigated by immunohistochemical or electron distributed CD8+ cells and deeply aggregated CD4+ microscopic methods. Consequently, since it has been cells adjacent to large germinal centers. In these demonstrated that GALT, BALT and NALT differ in lymphoid accumulations, IgG-containing cells were T/B-cell ratios (Kuper et aI., 1990, 1992; Heritage et aI., more frequently observed than IgM- and 19A-containing 1997), their function may differ in the defense cells. T-cell subsets, predominantly CD8+ cells were mechanism of the mucosal sites; Peyer's patches (PP) more widely distributed in the duct epithelium of the may be the central tissue in the induction of secretory lateral nasal glands than Ig-containing cells. Moreover, immunoglobulin (Ig) synthesis, while BALT and NALT numerous CD8+ cells and a few Ig-containing cells were appear to be more involved in cellular responses. found in the chicken salivary glands, especially around Moreover, Kuper et aI. (1992) reported that even within the orifice of their ducts into the oral cavity. Therefore, it the respiratory tract there are some differences in the seems likely that the chicken NALT plays an important state of activation and in the number of B-cells between part in the upper respiratory tract, with a close BALT and NALT of conventionally housed, untreated relationship to the paraocular immune system. rats. They suggested that the more activated appearance and earlier development in NALT than BALT were Key words: Nasal-associated lymphoid tissue (NALT), probably due to its strategic position with respect to Immunoglobulin-containing cells, T-cell subsets , incoming air containing aeroantigens. Ichikawa et aI. Immunohistochemistry, Chicken (1991) suggested that immunocompetent cells distributed in normal nasal mucosa of mice might locally develop or mobilize from systemic circulation according Introduction to antigenic stimuli. In contrast to mammals, most avian species The nasal mucosa lining the upper respiratory tract is including chickens entirely lack lymph nodes, but have a the first site of contact with inhaled aeroantigens. system of lymphoid nodules normally associated with According to Spit et aI. (1989), it seems justified to lymph vessels (King and McLelland, 1975). consider the nasal lymphoid tissue as a general part of Accumulation of lymphoid tissue has been demonstrated the mucosa-associated lymphoid tissue (MALT) system, in the oculo-nasal region in many avian species (Bang and Bang, 1968; Hodges, 1974; Aitken and Survasche, Offprint requests to: Dr. Koji Ohshima, Laboratory of Functional 1977; Rose, 1981). Plasma cells and lymphoid foci were Anatomy, Faculty of Agriculture, Shinshu University, Ina, Nagano·ken, common in paranasal tissues of chickens, but rare in 399·4598 Japan. Fax: 81-265-72-5259. e-mail: ohshima@ those of other birds (Aitken and Survashe, 1977). gipmc.shinshu-u.ac.jp Invasive lymphocyte populations consistently found in 714 Immunocompetent cells in chicken NALT the paraocular (Harderian glands and their ducts) and immunohistochemical analysis, they were incubated paranasal organs (nasolacrimal ducts, lateral nasal glands overnight at room temperature with one of the following and their ducts) of healthy commercial stock chickens primary antibodies, after pre-incubation with normal suggested that these tissue systems may be capable of rabbit serum (1:20, Cedarlane Laboratories, USA) for 10 local immune response to environmental stimuli (Bang min. Cryostat sections; mouse anti-chicken monoclonal and Bang, 1968). antibodies directed to CD4, and CDS (1 :500, Southern The distributions of T- and B-Iymphocytes in the Biotechnology Associates, USA). Paraffin sections; goat chicken BALT (Fagerland and Arp, 1993a) are generally anti-chicken polyclonal antibodies respectively directed similar to those in mammalian BALT (Plesch et aI., to IgA, IgM or IgG (1:1000, Bethyl Laboratories, USA). 1983). These observations suggested that the chicken Following incubation with these antibodies, the BALT may also be mainly involved in cellular immune cryostat sections were incubated with biotinylated rabbit responses, but the functional nature of the T-cells in the anti-mouse Ig G 1 (1 :500, Zymed Laboratories, USA) respiratory mucosa is not yet clear. and the paraffin sections were incubated with Respiratory diseases in poultry are of major biotinylated rabbit anti-goat IgG (1 :1000, EY economic importance, and vaccination via an aerosol Laboratories, USA) for 20 min. Then, they were route would be a practical and economical method of incubated with peroxidase-conjugated streptavidin protecting large flocks of chickens and turkeys (1 :100, Zymed Laboratories) for 20 min. The normal (Fagerland and Arp, 1993a,b). However, immunohisto­ serum, primary and secondary antibodies were diluted chemical studies with respect to nasal lymphoid tissues with O.OIM phosphate-buffered saline (PBS). The have not yet been performed in chickens or other avian sections were washed with PBS three times for 5 min species. each time after each incubation step. Staining for The aim of the present study was to determine the peroxidase was performed using 0 .05M Tris-HCI structure and organization of the immunocompetent buffered (pH7.6) containing 0.05% 3,3 ' -diamino­ elements in the chicken NALT, especially with respect to benzidine (DAB) and 0.006% H20 2. After immuno­ T-cell subsets and Ig-containing cells, using histochemical staining, the sections were slightly immunohistochemical methods. counterstained with hematoxylin, dehydrated, cleared and mounted. Materials and methods Controls stained with normal serum instead of each respective primary antibody all gave negative results. Chickens and tissue processing Also, some adjacent serial sections were stained using the periodic acid-Schiff (PAS) technique and Eighteen adult male White Leghorn chickens from counterstained with hematoxylin. 25 weeks to 1-2 years of age were used in this study. They received food and water ad libitum and were Results clinically healthy. Twelve birds anesthetized with thiopental sodium, The nasal cavity was covered with three different were perfused with saline followed by periodate-Iysine­ types of epithelium, i.e. the vestibular, respiratory and paraformaldehyde (PLP) solution. The Nasal tissues olfactory epithelium (Figs. la-c, 2). The nasolacrimal were dissected out with the surrounding tissues and ducts and the infra-orbital sinuses were situated in the immersed in the same fixative for at least 4 h at 4 QC. ventro-Iateral wall of the nasal cavity and covered with They were rinsed and dialyzed using O.lM cacodylate the respiratory epithelium (Fig. la,d). Also, lateral nasal buffer (pH 7.4) containing 10% to 20% sucrose for 24 h glands were found in the ventro-Iateral wall, opening at 4 QC, embedded in Tissue-Tek ocr compound (Miles, into the nasal cavity (Fig. 1 a,d), and medial and lateral USA) and frozen after decalcification for 3-5 weeks with palatine salivary glands were in close proximity to the 5% ethylendiaminetetra-acetic acid (EDTA) solution nasal cavity, opening into the oral cavity (pharynx) (Fig. except for two tissue samples which were embedded and 1a,e). Lymphoid tissues were observed in the mucosa frozen without decalcification. lining the nasal cavity and in its accessory structures in The other six birds were killed by decapitation, and various amounts and with various distribution patterns as the nasal tissues were removed with the surrounding follows (summarized in Table 1). tissues. They were immediately fixed with Bouin's fluid for 1S-24 h at 4 QC, dehydrated through a graded ethanol Vestibular epithelium series and embedded in paraffin after decalcification for v;; weeks with 5% EDTA solution. The vestibular region was situated at the entrance of the nasal cavity, which was lined with keratinized II nmunohistochemistry stratified squamous epithelium (Fig. 2). Within and under the vestibular epithelium, scarcely any cells
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