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Localization and characterization of T-cell subpopulations and natural killer cells (HNK 1+ cells) in the human tonsilla palatina

An ultrastructural-immunocytochemical study

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Summary

In the present study attention was focussed on several lymphoid subpopulations and specific stationary cells of the human tonsilla palatina. They were labeled at the light- and electron-microscopic levels by means of monoclonal antibodies to cell surface antigens. Cells resembling interdigitating cells (IDC-like cells) within the crypt epithelium and the interdigitating cells in the parafollicular T-cell region express the HLA-DR antigen. This fact suggests a relationship between these two populations of cells. Both cell types were frequently found in close contact to T-helper cells labeled with Anti-Leu 3a. This fact is discussed as a confirmation of earlier suggestions that the tonsillar crypt epithelium serves as T-cell region. Cytotoxic/ suppressor-T cells (OKT 8 +) and Leu 7-positive cells do not appear to contact interdigitating cells. Anti-Leu 7 is a monoclonal antibody, that defines a differentiation antigen shown to be selectively expressed on human natural killer cells (NK-cells). With the use of the immuno-electron-microscopic labeling method it was possible to analyze the ultrastructure of this lymphoid subpopulation. Two morphologically distinguishable subtypes of Leu 7-positive cells populate different microenvironments: The Leu 7-positive large-granular lymphocyte was predominantly found in the crypt epithelium, while numerous Leu 7-positive cells located in the germinal centers had the appearance of small lymphocytes. This finding is discussed in favour of distinct phenotypes representing different stages in a differentiation pathway of the maturing NK-cell: Small Leu 7-positive lymphocytes in the germinal centers are supposed to be functionally inactive precursors, and only the Leu 7-positive large granulated lymphocytes in the crypt epithelium may represent differentiated active NK-cells. This interpretation is in agreement with the observation that the tonsilla palatina, in spite of containing numerous Leu 7-positive cells, shows only low NK-activity against tumor cells.

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Abbreviations

DAB:

diamino-benzidine

DMSO:

dimethyl sulfoxide

HLA:

human leucocyte antigen

HLA-DR:

human leucocyte antigen, D-region related

Ia-antigen:

immune-associated antigen of the MHC

IDC:

interdigitating cell

IDC-like cell:

cell that resembles an interdigitating cell

LGL:

large granular lymphocyte

MHC:

major histocompatibility gene complex

NK-cell:

natural killer cell

PBS:

phosphate-buffered saline

References

  • Abo T, Balch CM (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK 1). J Immunol 127:1024–1029

    Google Scholar 

  • Abo T, Cooper MD, Balch CM (1982a) Characterization of human NK cells identified by the monoclonal HNK-1 (leu-7) antibody. In: Herberman RB (ed) NK-cells and other natural effector cells. Academic Press New York London, pp 31–38

    Google Scholar 

  • Abo T, Cooper MD, Balch CM (1982b) Postnatal expansion of the natural killer and killer cell population in humans identified by the monoclonal HNK-1 antibody. J Exp Med 155:321–326

    Google Scholar 

  • Banerjee D, Thibert RF (1983) Natural killer-like cells found in B-cell compartments of human lymphoid tissues. Nature 304:270–272

    Google Scholar 

  • Carpen O, Virtanen I, Saksela E (1982) Ultrastructure of human natural killer cells. Nature of the cytolytic contacts in relation to cellular secretion. J Immunol 128:2691–2697

    Google Scholar 

  • Evans RL, Wall DW, Platsoucas CD, Siegal FP, Fikrig SM, Testa CM, Good RA (1981) Thymus-dependent membrane antigens in man: Inhibition of cell-mediated lympholysis by monoclonal antibodies to the TH2 antigen. PNAS 78:544–548

    Google Scholar 

  • Ewijk W van, Rouse RV, Weissman IL (1980) Distribution of H-2 microenvironments in the mouse thymus. Immunoelectronmicroscopic identification of I-A and H-2K bearing cells. J Histochem Cytochem 28:1089–1099

    Google Scholar 

  • Gaudecker B von (1978) Ultrastructure of the age-involuted human thymus. Cell Tissue Res 186:507–525

    Google Scholar 

  • Gaudecker B von, Müller-Hermelink HK (1980) Ontogeny and organization of the stationary non-lymphoid cells in the human thymus. Cell Tissue Res 207:287–306

    Google Scholar 

  • Gaudecker B von, Müller-Hermelink HK (1982) The development of the human tonsilla palatina. Cell Tissue Res 224:579–600

    Google Scholar 

  • Gerdes J, Naiem M, Mason DJ, Stein H (1982) Human complement (C3b) receptors defined by a mouse monoclonal antibody. Immunology 45:645–653

    Google Scholar 

  • Gerdes J, Stein H, Mason DY, Ziegler A (1983) Human dendritic reticulum cells of lymphoid follicles: Their antigenic profile and their identification as multinucleated giant cells. Virchows Arch [Cell Pathol] 42:161–172

    Google Scholar 

  • Glauert AM, Glauert RH (1958) Araldite as an embedding medium for electron microscopy. J Biophys Biochem 4:191–194

    Google Scholar 

  • Grossi CE, Webb SR, Zicca A, Lydyard PM, Moretta L, Mingari MC, Cooper MD (1978) Morphological and histochemical analysis of two human T-cell subpopulations bearing receptors for IgM or IgG. J Exp Med 147:1405–1417

    Google Scholar 

  • Herberman RB, Ortaldo JR (1981) Natural killer cells: Their role in defenses against disease. Science 214:24–30

    Google Scholar 

  • Hoffmann-Fezer G, Löhrs U, Rodt HV, Thierfelder S (1981) Immunohistochemical identification of T- and B-lymphocytes delineated by the unlabelled antibody enzyme method. III. Topographical and quantitative distribution of T- and B-cells in human palatine tonsils. Cell Tissue Res 216:361–375

    Google Scholar 

  • Huhn D, Huber C, Gastl G (1982) Large granular lymphocytes: Morphological studies. Eur J Immunol 12:985–988

    Google Scholar 

  • Janossy G, Tidman N, Selby WS, Thomas JA, Granger S, Kung PC, Goldstein G (1980) Human T-lymphocytes of inducer and supressor type occupy different microenvironments. Nature 288:81–84

    Google Scholar 

  • Janossy G, Tidman N, Papageorgiou ES, Kung PC, Goldstein G (1981a) Distribution of T-lymphocyte subsets in the human bone marrow and thymus: an analysis with monoclonal antibodies. J Immunol 126:1608–1613

    Google Scholar 

  • Janossy G, Thomas JA, Pizzolo G (1981b) The analysis of lymphoid subpopulations in normal and malignant tissues by immuno fluorescence technique. J Cancer Res Clin Oncol 101:13–22

    Google Scholar 

  • Kung PC, Talle MA, DeMaria M, Butler M, Lifter M, Goldstein G (1980) Strategies for generating monoclonal antibodies defining human T-lymphocyte differentiation antigens. Transplant Proc 12:141–146

    Google Scholar 

  • Ledbetter JA, Evans RL, Lipinski M, Cunningham-Rundles C, Good RA, Herzenberg LA (1981) Evolutionary conservation of surface molecules that distinguish T-lymphocyte helper/inducer and T-cytotoxic/supressor subpopulation in mouse and man. J Exp Med 153:310–323

    Google Scholar 

  • Lennert K, Stein H (1982) The germinal center: Morphology, histochemistry and immunohistology. In: Goos M, Christophers E (eds) Lymphoproliferative diseases of the skin. Springer-Verlag Berlin Heidelberg New York, pp 3–15

    Google Scholar 

  • Mason DY, Bell JI, Christenson B, Biberfeld P (1980) An immunohistochemical study of human lymphoma. Clin Exp Immunol 40:235–248

    Google Scholar 

  • Mason DY, Stein H, Naiem M, Abdulaziz Z (1981) Immunohistological analysis of human lymphoid tissue by double immunoenzymatic labelling. J Cancer Res Clin Oncol 101:13–22

    Google Scholar 

  • McMillan EM, Wasik R, Everett MA (1981) Identification of T- lymphocytes and T-subsets in human tonsil using monoclonal antibodies and the immunoperoxidase technic. Am J Clin Pathol 76:737–744

    Google Scholar 

  • Poppema S, Bhan AK, Reinherz EL, McCluskey RT, Schlossman SF (1981) Distribution of T-cell subsets in human lymph node. J Exp Med 153:30–41

    Google Scholar 

  • Reinherz EL, Kung PC, Goldstein G, Levey RH, Schlossman SE (1980a) Discrete stages of human intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of T-cell lineage. Proc Natl Acad Sci USA 77:1588–1592

    Google Scholar 

  • Reinherz EL, Kung PC, Goldstein G, Schlossman SF (1980b) A monoclonal antibody reactive with the human cytotoxic/supressor T-cell subset previously defined by a heteroantiserum termed TH2. J Immunol 124:1301–1307

    Google Scholar 

  • Rouse RV, Ledbetter JA, Weissman IL (1982) Mouse lymph node germinal centers contain a selected subset of T-cells — the helper phenotype. J Immunol 128:2243–2246

    Google Scholar 

  • Seymour GJ, Greaves MF, Janossy G (1981) Identification of cells expressing T and p 28 (Ia-like) antigens in sections of human lymphoid tissue. Clin Exp Immunol 36:66–75

    Google Scholar 

  • Si L, Whiteside TL (1983) Tissue distribution of human NK cells studied with anti-Leu 7 monoclonal antibody. J Immunol 130:2149–2155

    Google Scholar 

  • Si L, Roscoe G, Whiteside TL (1983) Selective distribution and quantitation of T-lymphocyte subsets in germinal centers of human tonsils. Definition by use of monoclonal antibodies. Arch Pathol Lab Med 107:228–231

    Google Scholar 

  • Stein H, Bonk A, Tolksdorf G, Lennert K, Rodt H, Gerdes J (1980) Immunohistologic analysis of the organization of normal lymphoid tissue and non-Hodgkin's lymphomas. J Histochem Cytochem 28:746–760

    Google Scholar 

  • Stutte HJ, Müller-Hermelink HK (1976) Lysosomen in Blutzellen als diagnostischer Parameter. Verh Dtsch Ges Pathol 50:155–175

    Google Scholar 

  • Timonen T, Saksela E, Ranki A, Häyry P (1979) Fractionation, morphological and functional characterization of effector cells responsible for human natural killer activity against cell-line targets. Cell Immunol 48:133–148

    Google Scholar 

  • Timonen T, Ortaldo JR, Herberman RB (1981) Characteristics of human large granular lymphocytes and relationship to natural killer and K-cells. J Exp Med 153:569–582

    Google Scholar 

  • Wilson MB, Nakane PK (1978) Recent developments in the periodate method of conjugating horseradish peroxidase (HRPO) to antibodies, immunofluorescence and related staining techniques. Knopp E, Holubar K, Wicks G (eds) Amsterdam Elsevier/North Holland Biomedical Press, pp 215

    Google Scholar 

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von Gaudecker, B., Pfingsten, U. & Müller-Hermelink, HK. Localization and characterization of T-cell subpopulations and natural killer cells (HNK 1+ cells) in the human tonsilla palatina. Cell Tissue Res. 238, 135–143 (1984). https://doi.org/10.1007/BF00215154

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