Skip to main content
SpringerLink
Log in

Precise localization of antigens on follicular dendritic cells

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

Summary

Horse-spleen ferritin or bovine serum albumin conjugated to colloidal gold (BSA-gold) were injected subcutaneously in preimmunized mice. In draining lymph nodes both antigens were located in macrophages or between the cytoplasmic processes of follicular dendritic cells (FDC). Some of the antigens remained trapped on FDC until day 31 after injection. Simultaneous injection of both antigens showed that they were located between the infoldings of the same FDC. These cells are thus able to retain at least two different antigens on their surface. The peculiar arrangement of ferritin between the cytoplasmic infoldings suggests that this antigen is fixed on both cell membranes by specific antibodies. The trapped immune complexes could thus stabilize the FDC membrane system.

The antigen retention requires the presence of specific antibodies since BSA-gold or ferritin injected without preimmunization were not found between FDC processes. Nonantigenic materials, such as colloidal gold or carbon particles, are not trapped by FDC, except when injected in large amounts.

The antigens were trapped on the surface of FDC, however unfrequently in close contact with lymphocytes. FDC might protect lymphocytes against an excess of immune complexes and act as regulators of contacts between lymphocytes and immune complexes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BSA:

bovine serum albumin

BSA-gold:

BSA conjugated to colloidal gold particles

FDC:

follicular dendritic cells

References

  • Baldwin WM, Cohen N (1981) A giant cell with dendritic cell properties in spleens of the anuran amphibian Xenopus laevis. Dev Comp Immunol 5:461–473

    Google Scholar 

  • Balfour BM, Humphrey JM (1966) Localization of gamma-globulin and labelled antigen in germinal centers in relation to the immune response. In: Germinal centers in immune responses, Springer, p 80–85

  • Chen LL, Adams JC, Steinman RM (1978a) Anatomy of germinal centers in mouse spleen, with special reference to “follicular dendritic cells”. J Cell Biol 77:148–164

    Google Scholar 

  • Chen LL, Frank A, Adams J, Steinman R (1978b) Distribution of horseradish peroxidase (HRP) anti-HRP immune complexes in mouse spleen with special reference to follicular dendritic cells. J Cell Biol 79:184–199

    Google Scholar 

  • Cohen S, Vassalli P, Benacerraf B, McCluskey R (1966) The distribution of antigenic and nonantigenic compounds within draining lymph nodes. Lab Invest 15:1143–1155

    Google Scholar 

  • Diener E, Feldmann M (1972) Relationship between antigen and antibody induced suppression of immunity. Transplant Rev 8:76

    Google Scholar 

  • Fossum S (1980) The architecture of rat lymph nodes. III Distribution of ferritin and colloidal carbon in the draining lymph nodes after food-pad injection. Scand J Immunol 12:433–441

    Google Scholar 

  • Gaijl-Peczalska KJ, Fish AJ, Meuwissen HJ, Frommel D, Good RA (1969) Localization of immunological complexes fixing C3 in germinal centers of lymph nodes. J Exp Med 130:1367–1374

    Google Scholar 

  • Groscurth P (1980) Non-lymphatic cells in the lymph node cortex of the mouse. I Morphology and distribution of the interdigitating cells and the dendritic reticular cells in the mesenteric lymph node of adult ICR mouse. Pathol Res Pract 169:211–234

    Google Scholar 

  • Groscurth P (1980) Non-lymphatic cells in the lymph node cortex of the mouse. III Interdigitating cells and dendritic reticular cells in the mesenteric lymph node of the homozygotes “nude” (nu/nu) mouse. Pathol Res Pract 169:255–268

    Google Scholar 

  • Hanna MG, Szakal AK (1968) Localization of 125I-labelled antigen in germinal centers of mouse spleen: histologic and ultrastructural autoradiographic studies of the secondary immune reaction. J Immunol 101:949–962

    Google Scholar 

  • Heinen E, Lilet-Leclercq Ch, Mason DY, Stein H, Boniver J, Radoux D, Kinet-Denoël C and fnSimar LJ (1983a) Isolation of follicular dendritic cells from human tonsils and adenoids. II Immunocytochemical characterization. Eur J Immunol (submitted for publication)

  • Heinen E, Radoux D, Kinet-Denoël C, Simar LJ (1983b) Colloidal gold, a useful marker for antigen localization on follicular dendritic cells. J Immunol Methods 59:361–368

    Google Scholar 

  • Herd ZL, Ada GL (1969) The retention of 125I-immunoglobulin, IgG subunits and antigen-antibody complexes in rat footpads and draining lymph nodes. Aust J Exp Biol Med Sci 47:63–77

    Google Scholar 

  • Heusermann U, Zurborn KH, Schroeder L, Stutte HJ (1980) The origin of the dendritic reticulum cell. An experimental enzymehistochemical and electron microscopic study on the rabbit spleen. Cell Tissue Res 209:279–294

    Google Scholar 

  • Humphrey JG, Frank MM (1967) The localization of non-microbial antigens in the draining lymph nodes of tolerant, normal and primed rabbits. Immunol 13:87–94

    Google Scholar 

  • Kinet-Denoël C, Heinen E, Radoux D, Simar LJ (1982) Follicular dendritic cells in lymph nodes after X-irradiation. Int J Radiat Biol 42:121–130

    Google Scholar 

  • Klaus GGB, Humphrey JH (1977) The generation of memory cells. I. The role of C3 in the generation of B memory cells. Immunol 33:31–40

    Google Scholar 

  • Klaus GGB, Humphrey JH, Kunkl A, Dongworth DW (1980) The follicular dendritic cell: its role in antigen presentation in the generation of immunological memory. Immunol Rev 53:3–28

    Google Scholar 

  • Kunkl A, Klaus GGB (1981) The generation of memory cells. IV Immunization with antigen-antibody complexes accelerates the development of B-memory cells, the formation of germinal centres and the maturation of antibody affinity in the secondary response. Immunology 43:371–378

    Google Scholar 

  • Lilet-Leclercq C, Radoux D, Heinen E, Kinet-Denoël C, Defraigne J-O, Houben-Defresne MP, Simar LJ (1983) Isolation of follicular dendritic cells from human tonsils and adenoids. I. Procedure and morphological characterization. J Immunol Methods (in press)

  • Mandel TE, Phipps RP, Abbot A, Tew JG (1980) The follicular dendritic cell: long term antigen retention during immunity. Immunol Rev 53:29–60

    Google Scholar 

  • Mandel TE, Phipps RP, Abbot AP, Tew JG (1981) Long-term antigen retention by dendritic cells in the popliteal lymph node of immunized mice. Immunology 43:353–362

    Google Scholar 

  • Maruyama K, Masuda T (1965) Electron microscope observation on the germinal center of the lymph node in guinea pigs sensitized with sheep erythrocytes. Ann Rept Inst Virus Res Kyoto Univ 7:149

    Google Scholar 

  • Milanesi S (1965) Sulla presenza di dispositivi di giunzione tra le cellule dendritiche dei follicoli linfactica del linfonodo. Boll Soc Ital Biol Sper 41:1223–1231

    Google Scholar 

  • Morgan EL, Tempelis CH (1977) The role of antigen-antibody complexes in mediating immunologic unresponsiveness in the chicken. J Immunol 119:1293–1298

    Google Scholar 

  • Nossal GJ, Ada GL, Austin CM (1965) Antigens in immunity. VIII Localization of 125I labeled antigens in the secondary response. Immunology 9:349–363

    Google Scholar 

  • Nossal GJ, Abbot A, Mitchell J, Lummus Z (1968) Antigens in immunity. XV Ultrastructural features of antigen capture in primary and secondary lymphoid follicles. J Exp Med 127:277–289

    Google Scholar 

  • Papamichail M, Gutierrez C, Embling P, Johnson P, Holborow E, Pepys M (1975) Complement dependence of localisation of aggregated IgG in germinal centres. Scand J Immunol 4:343–347

    Google Scholar 

  • Romball CG, Ulevith RJ, Weigle WO (1980) Role of C3 in the regulation of a spheric PFC response in rabbits. J Immunol 124:151–155

    Google Scholar 

  • Rooijen van N (1972) Antigen in the spleen. The non-specificity of the follicles in the process of antigen trapping and the role of antibody. Immunology 22:757–765

    Google Scholar 

  • Sakuma H, Asano S, Kojima M (1981) An ultrastructure study of the primary follicle in the lymph node. Acta Pathol Jpn 31:473–493

    Google Scholar 

  • Sordat B, Moser R, Gerber H, Cottier H (1969) Differentiation pathway within germinal centers of human tonsils. In: L FioreDonati, MS Hanna (eds) Lymphatic tissue and germinal centers in immune responses. Plenum Press, New York, pp 73–82

    Google Scholar 

  • Swartzendruber DC (1965) Desmosomes in germinal centers of mouse spleen. Exp Cell Res 40:429–432

    Google Scholar 

  • Szakal AK, Hanna MG (1968) The ultrastructure of antigen localization and virus-like particles in mouse spleen germinal centers. Exp Molec Pathol 8:75–83

    Google Scholar 

  • Tew JG, Mandel T (1978) The maintenance and regulation of serum antibody levels: evidence indicating a role for antigen retained in lymphoid follicles. J Immunol 120:1063–1069

    Google Scholar 

  • Tew JG, Mandel TE, Burgess AW (1979) Retention of intact HSA for prolonged periods in the popliteal lymph nodes of specifically immunized mice. Cell Immunol 45:207–212

    Google Scholar 

  • Tew JG, Mandel TE, Miller GA (1979) Immune retention: immunological requirements for maintaining an easily degradable antigen in vivo. Aust J Exp Biol Med Sc 57:401–414

    Google Scholar 

  • Thorbeke GT, Romano TJ, Lerman SP (1974) Regulatory mechanisms in proliferation and differentiation of lymphoid tissue with particular reference to germinal center development. Prog Immunol Stand II, 3:25–34

    Google Scholar 

  • Tsunoda R, Yaginuma Y, Kojima M (1980) Immunocytological studies on the constituent cells of the secondary nodules in human tonsils. Acta Pathol Jpn 30:33–57

    Google Scholar 

  • Unanue ER (1972) The regulatory role of macrophages in antigenic stimulation. Adv Immunol 15:95–165

    Google Scholar 

  • White RG, French VI, Stark JM (1970) A study of the localization of a protein antigen in the chicken spleen and its relation to the formation of germinal centres. J Med Microbiol 3:65–71

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Human Histology, University of Liège, Liège, Belgium

    Daniel Radoux, Ernst Heinen, Cécile Kinet-Denoël, Elisabeth Tihange & Léon Simar

Authors
  1. Daniel Radoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ernst Heinen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cécile Kinet-Denoël
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elisabeth Tihange
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Léon Simar
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Radoux, D., Heinen, E., Kinet-Denoël, C. et al. Precise localization of antigens on follicular dendritic cells. Cell Tissue Res. 235, 267–274 (1984). https://doi.org/10.1007/BF00217850

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00217850

Key words

Search

Navigation