Skip to main content
Log in

An immunohistochemical study on the postnatal development of rat nasal-associated lymphoid tissue (NALT)

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

This study concerns the development of nasal-associated lymphoid tissue in the rat, using immuno- and enzyme-histochemical staining techniques on cryostat sections. Nasal-associated lymphoid tissue is present at birth as a small accumulation of mainly T lymphocytes and non-lymphoid cells; B cells are rare. Distinct areas of T and B cells appear at 10 days after birth; by that time high endothelial venules are also observed. Intra-epithelial lymphocytes are present, most of them being T-helper cells. ED1+ macrophages are seen throughout the tissue. The proportion of ED1+cells does not change during ontogeny. ED2+cells (tissue macrophages) are present predominantly at the border between the lymphoid tissue and the surrounding connective tissue, in all age-groups. ED3+mononuclear cells are scattered throughout the nasal-associated lymphoid tissue of young animals. Later on, the ED3+ cells migrate into the border-area between lymphoid and connective tissue. Ia+ non-lymphoid cells in the nasal lymphoid tissue increase in number during ontogeny. Only a few of them show acid phosphatase activity, indicating that the proportion of classical scavenger macrophages is low. Some of them may be antigen presenting (dendritic) cells. Ia+ dendritic cells also occur between the epithelial cells. Moreover, some epithelial cells express the Ia marker.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barclay AN (1981) The localization of populations of lymphocytes defined by monoclonal antibodies in rat lymphoid tissues. Immunology 42:593–600

    Google Scholar 

  • Barclay AN, Mason DW (1982) Induction of Ia antigen in rat epidermal cells and gut epithelium by immunological stimuli. J Exp Med 156:1665–1676

    Google Scholar 

  • Beelen RHJ, Eestermans IL, Döpp EA, Dijkstra CD (1987) Monoclonal antibodies ED1, ED2, and ED3 against rat macrophages: expression of recognized antigens in different stages of differentiation. Transplant Proc 19:3166–3170

    Google Scholar 

  • Bland P (1988) MHC class II expression by gut epithelium. Immunol Today 9:174–178

    Google Scholar 

  • Breel M, Mebius RE, Kraal G (1987) Dendritic cells of the mouse recognized by two monoclonal antibodies. Eur J Immunol 17:1555–1559

    Google Scholar 

  • Breel M, Van der Ende M, Sminia T, Kraal G (1988) Subpopulations of lymphoid and non-lymphoid cells in bronchus-associated lymphoid tissue (BALT) of the mouse. Immunology 63:657–662

    Google Scholar 

  • Cerf-Bensussan N, Quaroni A, Kurnick JT, Bhan AK (1984) Intraepithelial lymphocytes modulate Ia expression by intestinal epithelial cells. J Immunol 132:2244–2252

    Google Scholar 

  • Dijkstra CD, Döpp EA, Joling P, Kraal G (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2, ED3. Immunology 54:589–599

    Google Scholar 

  • Duijvestijn AM, Schutte R, Köhler YG, Korn C, Hoefsmit ECM (1983) Characterization of the population of phagocytic cells in thymic cell suspensions. A morphological and cytochemical study. Cell Tissue Res 231:313–323

    Google Scholar 

  • Ernst PB, Underdown BJ, Bienenstock J (1987) Immunity in mucosal tissues. In: Stites DP, Stobo JD, Wells JV (eds) Basic and clinical immunology. Appleton and Lange, Norwalk Los Altos, pp 159–166

    Google Scholar 

  • Gregson RL, Davey MJ, Prentice DE (1979) Postnatal development of bronchus-associated lymphoid tissue (BALT) in the rat, Rattus norvegicus. Lab Anim 13:231–238

    Google Scholar 

  • Groenewegen G, Buurman WA (1984) Vascular endothelial cells present alloantigens to unprimed lymphocytes. J Immunol 19:269–273

    Google Scholar 

  • Holt PG, Schon-Hegrad MA (1987) Localization of T cells, macrophages and dendritic cells in rat respiratory tract tissue: implications for immune function studies. Immunology 62:349–356

    Google Scholar 

  • Holt PG, Schon-Hegrad MA, Oliver J (1988) MHC class II antigen-bearing dendritic cells in pulmonary tissues of the rat. Regulation of antigen presentation activity by endogenous macrophage populations. J Exp Med 167:262–274

    Google Scholar 

  • Hume DA, Allan W, Hogan PG, Doe WF (1987) Immunohistochemical characterisation of macrophages in human liver and gastrointestinal tract: Expression of CD4, HLA-Dr, OKM1, and the mature macrophage marker 25F9 in normal and diseased tissue. J Leukocyte Biol 42:474–484

    Google Scholar 

  • Joling P, Vaessen LMB, Tielen FJ, Rozing J (1983) Monoclonal antibodies against cell surface markers of T lymphocyte subpopulations in the rat. In: Weimar W, Marquet RL, Bijnen AB, Ploeg RJ (eds) Modern trends in clinical immunosuppression. Capita Selecta Committee Dijkzigt, Rotterdam, pp 201–207

    Google Scholar 

  • Joling P, Tielen FJ, Vaessen LMB, Hesse CJ, Rozing J (1985) Intrathymic differentiation in the rat. Adv Exp Med Biol 186:235–244

    Google Scholar 

  • Kelemen G (1947) The junction of the nasal cavity and the pharyngeal tube in the rat. Arch Otolaryngol 45:159–168

    Google Scholar 

  • Kelemen G (1962) Histology of the nasal and paranasal cavities of germfree-reared and ex-germfree rats. Acta Anat (Basel) 48:108–113

    Google Scholar 

  • Kroese FGM, Opstelten D, Wubbena AS, Deenen GJ, Aten J, Schwander EH, De Leij L, Nieuwenhuis P (1985) Monoclonal antibodies to rat B lymphocyte (sub-)populations. Adv Exp Med Biol 186:81–89

    Google Scholar 

  • Liebich H-G (1975) Zum Bau der oberen Luftwege der weißen Ratte (Mus rattus norvegicus, var. albinos). Anat Anz 138:170–179

    Google Scholar 

  • Lyscom N, Brueton MJ (1983) The development of intraepithelial and Peyer's patch lymphocyte sub-types in the small intestine of newborn rats. Clin Exp Immunol 54:158–162

    Google Scholar 

  • Mayer L, Shlien R (1987) Evidence for function of Ia molecules on gut epithelial cells in man. J Exp Med 166:1471–1483

    Google Scholar 

  • Mayrhofer G, Pugh CW, Barclay AN (1983) The distribution, ontogeny and origin in the rat of Ia-positive cells with dendritic morphology and of Ia antigen in epithelia, with special reference to the intestine. Eur J Immunol 13:112–122

    Google Scholar 

  • McMaster WR, Williams AF (1979) Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur J Immunol 9:426–433

    Google Scholar 

  • Monteiro-Riviere NA, Popp JA (1984) Ultrastructural characterization of the nasal respiratory epithelium in the rat. Am J Anat 169:31–43

    Google Scholar 

  • Moscicki RA, Amento EP, Krane SM, Kurnick JT, Colvin RB (1983) Modulation of surface antigens of a human monocyte cell line, U937, during incubation with T lymphocyte-conditioned medium: Detection of T4 antigen and its presence on normal blood monocytes. J Immunol 131:743–748

    Google Scholar 

  • Nadler PI, Klingenstein RJ, Hodes RJ (1980) Ontogeny of murine accessory cells: Ia antigen expression and accessory cell function in in vitro primary antibody responses. J Immunol 125:914–920

    Google Scholar 

  • Ohara R, Mitsuyama M, Miyata M, Nomoto K (1985) Ontogeny of macrophage-mediated protection against Listeria monocytogenes. Infec Immun 48:763–768

    Google Scholar 

  • Owen RL, Jones AL (1974) Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66:189–203

    Google Scholar 

  • Pearse AGE (1968) Histochemistry: theoretical and applied. Vol 1, 3rd ed. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Plesch BEC (1982) Histology and immunohistochemistry of bronchus associated lymphoid tissue (BALT) in the rat. Adv Exp Med Biol 149:491–497

    Google Scholar 

  • Plesch BEC, Gamelkoorn GJ, Van de Ende M (1983) Development of bronchus associated lymphoid tissue (BALT) in the rat, with special reference to T- and B-cells. Dev Comp Immunol 7:179–188

    Google Scholar 

  • Pober JS, Gimbrone MA, Cotran RS, Reiss CS, Burakoff SJ, Fiers W, Ault KA (1983) Ia expression by vascular endothelium is inducible by activated T cells and by human γ interferon. J Exp Med 157:1339–1353

    Google Scholar 

  • Popp JA, Martin JT (1984) Surface topography and distribution of cell types in the rat nasal respiratory epithelium: scanning electron microscopic observations. Am J Anat 169:425–436

    Google Scholar 

  • Selby WS, Janossy G, Goldstein G, Jewell DP (1981) T lymphocyte subsets in human intestinal mucosa: the distribution and relationship to MHC-derived antigens. Clin Exp Immunol 44:453–458

    Google Scholar 

  • Sertl K, Takemura T, Tschachler E, Ferrans VJ, Kaliner MA, Shevach EM (1986) Dendritic cells with antigen-presenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. J Exp Med 163:436–451

    Google Scholar 

  • Smart CJ, Trejdosiewicz LK, Badr-El-Din S, Heatley RV (1988) T lymphocytes of the human colonic mucosa: functional and phenotypic analysis. Clin Exp Immunol 73:63–69

    Google Scholar 

  • Sminia T, Janse EM, Plesch BEC (1983) Ontogeny of Peyer's patches of the rat. Anat Rec 207:309–316

    Google Scholar 

  • Spencer J, Macdonald TT, Finn T, Isaacson PG (1986) The development of gut associated lymphoid tissue in the terminal ileum of fetal human intestine. Clin Exp Immunol 64:536–543

    Google Scholar 

  • Spit BJ, Hendriksen EGJ, Bruijntjes JP, Kuper CF (1989) Nasal lymphoid tissue in the rat. Cell Tissue Res 255:193–198

    Google Scholar 

  • Van der Brugge-Gamelkoorn GJ, Dijkstra CD, Sminia T (1985a) Characterization of pulmonary macrophages and bronchus associated lymphoid tissue (BALT) macrophages of the rat. An enzyme-cytochemical and immunocytochemical study. Immunobiology 169:553–562

    Google Scholar 

  • Van der Brugge-Gamelkoorn GJ, Van de Ende M, Sminia T (1985b) Uptake of antigens and inert particles by bronchus associated lymphoid tissue (BALT) epithelium in the rat. Cell Biol Int Rep 9:524

    Google Scholar 

  • Van der Heijden FL (1986) Mucosal lymphocytes in the rat small intestine: phenotypical characterization in situ. Immunology 59:397–399

    Google Scholar 

  • Van Rees EP, Dijkstra CD, Van Rooijen N (1987) The early postnatal development of the primary immune response in rat popliteal lymph node, stimulated with thymus-independent type-1 and type-2 antigens. Cell Tissue Res 250:695–699

    Google Scholar 

  • Wilders MM, Sminia T, Janse EM (1983) Ontogeny of non-lymphoid and lymphoid cells in the rat gut with special reference to large mononuclear Ia-positive dendritic cells. Immunology 50:303–314

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hameleers, D.M.H., van der Ende, M., Biewenga, J. et al. An immunohistochemical study on the postnatal development of rat nasal-associated lymphoid tissue (NALT). Cell Tissue Res. 256, 431–438 (1989). https://doi.org/10.1007/BF00218901

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00218901

Key words

Navigation