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. 1986 Jan;57(1):99–104.

Germinal centre formation and follicular antigen trapping in the spleen of lethally X-irradiated and reconstituted rats.

F G Kroese, A S Wubbena, P Nieuwenhuis
PMCID: PMC1453887  PMID: 3510969

Abstract

In this study, the relationship between germinal centre formation and the follicular trapping of immune complexes in the rat spleen was investigated. Lethally (9 Gy) X-irradiated rats were reconstituted with thoracic duct lymphocytes and subsequently challenged with sheep red blood cells to induce germinal centre formation. Rats were killed at daily intervals from 1 to 8 days after reconstitution and antigenic stimulation. Antigen trapping capacity during this interval was assessed by intravenous injection of HRP-anti-HRP immune complexes, 24 hr before killing of the animals. Germinal centre formation could be observed from Day 4 onwards. The follicular trapping capacity, which had been abolished by the X-irradiation, however, returned 2 days later (i.e. by Day 6). Apparently, in these experiments, early germinal centre formation could occur without an intact follicular trapping mechanism. It was, therefore, concluded that in this transfer system follicular immune complex trapping is not a prerequisite for the induction of de novo germinal centre formation. Previous studies have shown that both follicular dendritic cells and marginal zone B cells may play a role in the follicular antigen trapping mechanism. FDCs, as detectable with mAB MRC OX 2 in immunoperoxidase-stained frozen sections, were present in spleens at any time after irradiation and reconstitution; the impaired follicular trapping of HRP-anti-HRP immune complexes was therefore not due to an absence of FDCs. Marginal zone B cells, however, were almost absent until 5 days after reconstitution, as observed by immunohistochemical staining with anti-B cell mABs (HIS 14 and HIS 22) and a polyclonal anti-IgD antiserum. Our data suggest that regeneration of follicular antigen trapping capacity is dependent on the presence of marginal zone B cells.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barclay A. N. Different reticular elements in rat lymphoid tissue identified by localization of Ia, Thy-1 and MRC OX 2 antigens. Immunology. 1981 Dec;44(4):727–736. [PMC free article] [PubMed] [Google Scholar]
  2. Brown J. C., Harris G., Papamichail M., Sljivić V. S., Holborow E. J. The localization of aggregated human -globulin in the spleens of normal mice. Immunology. 1973 Jun;24(6):955–968. [PMC free article] [PubMed] [Google Scholar]
  3. Chen L. L., Frank A. M., Adams J. C., Steinman R. M. Distribution of horseradish peroxidase (HRP)-anti-HRP immune complexes in mouse spleen with special reference to follicular dendritic cells. J Cell Biol. 1978 Oct;79(1):184–199. doi: 10.1083/jcb.79.1.184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Coico R. F., Bhogal B. S., Thorbecke G. J. Relationship of germinal centers in lymphoid tissue to immunologic memory. VI. Transfer of B cell memory with lymph node cells fractionated according to their receptors for peanut agglutinin. J Immunol. 1983 Nov;131(5):2254–2257. [PubMed] [Google Scholar]
  5. Dijkstra C. D., van Tilburg N. J., Döpp E. A. Ontogenetic aspects of immune-complex trapping in the spleen and popliteal lymph nodes of the rat. Cell Tissue Res. 1982;223(3):545–552. doi: 10.1007/BF00218475. [DOI] [PubMed] [Google Scholar]
  6. Enriquez-Rincon F., Klaus G. G. Follicular trapping of hapten-erythrocyte-antibody complexes in mouse spleen. Immunology. 1984 May;52(1):107–116. [PMC free article] [PubMed] [Google Scholar]
  7. Gastkemper N. A., Wubbena A. S., Gimbrère F. J., de Graaff A., Nieuwenhuis P. Germinal centres and the B-cell system. V. Presence of germinal centre-precursor cells among lymphocytes of the thoracic duct in the rat. Cell Tissue Res. 1981;219(2):281–289. doi: 10.1007/BF00210148. [DOI] [PubMed] [Google Scholar]
  8. Gray D., MacLennan I. C., Bazin H., Khan M. Migrant mu+ delta+ and static mu+ delta- B lymphocyte subsets. Eur J Immunol. 1982 Jul;12(7):564–569. doi: 10.1002/eji.1830120707. [DOI] [PubMed] [Google Scholar]
  9. Gray D., McConnell I., Kumararatne D. S., MacLennan I. C., Humphrey J. H., Bazin H. Marginal zone B cells express CR1 and CR2 receptors. Eur J Immunol. 1984 Jan;14(1):47–52. doi: 10.1002/eji.1830140109. [DOI] [PubMed] [Google Scholar]
  10. Kinet-Denoël C., Heinen E., Radoux D., Simar L. J. Follicular dendritic cells in lymph nodes after x-irradiation. Int J Radiat Biol Relat Stud Phys Chem Med. 1982 Aug;42(2):121–130. doi: 10.1080/09553008214550991. [DOI] [PubMed] [Google Scholar]
  11. Klaus G. G., Humphrey J. H., Kunkl A., Dongworth D. W. The follicular dendritic cell: its role in antigen presentation in the generation of immunological memory. Immunol Rev. 1980;53:3–28. doi: 10.1111/j.1600-065x.1980.tb01038.x. [DOI] [PubMed] [Google Scholar]
  12. Kroese F. G., Opstelten D., Wubbena A. S., Deenen G. J., Aten J., Schwander E. H., de Leij L., Nieuwenhuis P. Monoclonal antibodies to rat B lymphocyte (sub-)populations. Adv Exp Med Biol. 1985;186:81–89. doi: 10.1007/978-1-4613-2463-8_10. [DOI] [PubMed] [Google Scholar]
  13. Kunkl A., Klaus G. G. 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. 1981 Jun;43(2):371–378. [PMC free article] [PubMed] [Google Scholar]
  14. Laissue J., Cottier H., Hess M. W., Stoner R. D. Early and enhanced germinal center formation and antibody responses in mice after primary stimulation with antigen-isologous antibody complexes as compared with antigen alone. J Immunol. 1971 Sep;107(3):822–831. [PubMed] [Google Scholar]
  15. Marcinkiewicz J., Bereta M., Malinowski J., Ptak W. The induction of oxazolone-specific T suppressor afferent cells in mice by hapten-modified isologous IgG. Eur J Immunol. 1984 Aug;14(8):759–762. doi: 10.1002/eji.1830140818. [DOI] [PubMed] [Google Scholar]
  16. Nettesheim P., Hammons A. S. Recovery of the antigen retention mechanism after sublethal x-irradiation in mice receiving cells from various sources. J Immunol. 1971 Aug;107(2):518–525. [PubMed] [Google Scholar]
  17. Nieuwenhuis P., Opstelten D. Functional anatomy of germinal centers. Am J Anat. 1984 Jul;170(3):421–435. doi: 10.1002/aja.1001700315. [DOI] [PubMed] [Google Scholar]
  18. Opstelten D., Stikker R., Deenen G. J., Nieuwenhuis P. Germinal centers and the B-cell system. VII. Complement receptors, antigen receptors, immunoglobulin and alkaline phosphatase in germinal centers of the rabbit appendix and popliteal lymph nodes. Cell Tissue Res. 1982;224(3):505–516. doi: 10.1007/BF00213748. [DOI] [PubMed] [Google Scholar]
  19. Sordat B., Sordat M., Hess M. W., Stoner R. D., Cottier H. Specific antibody within lymphoid germinal center cells of mice after primary immunization with horseradish peroxidase: a light and electron microscopic study. J Exp Med. 1970 Jan 1;131(1):77–91. doi: 10.1084/jem.131.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Terashima K., Imai Y., Kasajima T., Tsunoda R., Takahashi K., Kojima M. An ultrastructure study on antibody production of the lymph nodes of rats with special reference to the role of germinal centers. Acta Pathol Jpn. 1977 Jan;27(1):1–24. doi: 10.1111/j.1440-1827.1977.tb01856.x. [DOI] [PubMed] [Google Scholar]
  21. Veerman A. J., van Rooijen N. Lymphocyte capping and lymphocyte migration as associated events in the in vivo antigen trapping process. An electron-microscopic autoradiographic study in the spleen of mice. Cell Tissue Res. 1975 Aug 18;161(2):211–217. doi: 10.1007/BF00220369. [DOI] [PubMed] [Google Scholar]
  22. van Rooijen N. Antigens in the spleen. The non-specificity of the follicles in the process of antigen trapping and the role of antibody. Immunology. 1972 May;22(5):757–765. [PMC free article] [PubMed] [Google Scholar]
  23. van Rooijen N. Immune complexes in the spleen. The difference between competitive inhibition of immune complex trapping in spleen follicles and inhibition by paratyphoid vaccine. Immunology. 1975 Jun;28(6):1155–1163. [PMC free article] [PubMed] [Google Scholar]
  24. van Rooijen N. Mechanism of follicular antigen trapping. Migration of antigen-antibody complexes from marginal zone towards follicle centres. Immunology. 1973 Nov;25(5):847–852. [PMC free article] [PubMed] [Google Scholar]
  25. van Rooijen N., Streefkerk J. G. Autoradiography and immunohistoperoxidase techniques applied to the same tissue section. J Immunol Methods. 1976;10(4):379–383. doi: 10.1016/0022-1759(76)90032-6. [DOI] [PubMed] [Google Scholar]

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