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. 1989 Oct;68(2):227–232.

Lymphocyte migration in the spleen: the effect of macrophage elimination.

G Kraal 1, H Rodrigues 1, K Hoeben 1, N Van Rooijen 1
PMCID: PMC1385422  PMID: 2807380

Abstract

To study the influence of macrophages on the migration and distribution of lymphocytes in the spleen, macrophages were eliminated from the spleen of mice by injection of liposomes in which DMDP was encapsulated. This leads to an elimination of macrophages in both the red pulp and marginal zone of the spleen within 1-2 days. In these animals the distribution of lymphocytes was determined by transfer of either syngeneic fluoresceinated or Ly 5 congeneic cells. It was found that after elimination of the macrophages the number of lymphocytes immigrating into the spleen had decreased, although a comparable mode of compartimentalization was found with an initial localization in the marginal zone and a subsequent distribution into the white pulp. After this elimination spleen macrophage subsets return with different kinetics, and in this way the influence of the red pulp macrophages, the marginal zone macrophages and the marginal metallophilic macrophages on lymphocyte immigration and redistribution could be investigated. A quantitative decrease of immigration was still found when red pulp and marginal metallophilic macrophages had repopulated their compartments, but was only fully restored when the last population to repopulate the spleen after treatment with DMDP-liposomes, the marginal zone macrophages, had returned. Experiments with isolated T and B cells showed that the elimination of macrophages had a profound effect on the localization of B cells in the white pulp, whereas it hardly affected T 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. Brelińska R., Pilgrim C. Macrophages and interdigitating cells; their relationship to migrating lymphocytes in the white pulp of rat spleen. Cell Tissue Res. 1983;233(3):671–688. doi: 10.1007/BF00212234. [DOI] [PubMed] [Google Scholar]
  2. Brelińska R., Pilgrim C., Reisert I. Pathways of lymphocyte migration within the periarterial lymphoid sheath of rat spleen. Cell Tissue Res. 1984;236(3):661–667. doi: 10.1007/BF00217236. [DOI] [PubMed] [Google Scholar]
  3. Classen E., Van Rooijen N. Preparation and characteristics of dichloromethylene diphosphonate-containing liposomes. J Microencapsul. 1986 Apr-Jun;3(2):109–114. doi: 10.3109/02652048609031565. [DOI] [PubMed] [Google Scholar]
  4. Eikelenboom P. Characterization of non-lymphoid cells in the white pulp of the mouse spleen: an in vivo and in vitro study. Cell Tissue Res. 1978 Dec 29;195(3):445–460. doi: 10.1007/BF00233888. [DOI] [PubMed] [Google Scholar]
  5. Ford W. L. The mechanism of lymphopenia produced by chronic irradiation of the rat spleen. Br J Exp Pathol. 1968 Oct;49(5):502–510. [PMC free article] [PubMed] [Google Scholar]
  6. Freitas A. A., de Sousa M. The role of cell interactions in the control of lymphocyte traffic. Cell Immunol. 1976 Mar 15;22(2):345–350. doi: 10.1016/0008-8749(76)90035-6. [DOI] [PubMed] [Google Scholar]
  7. Hammond B. J. A compartmental analysis of circulatory lymphocytes in the spleen. Cell Tissue Kinet. 1975 Mar;8(2):153–169. doi: 10.1111/j.1365-2184.1975.tb01217.x. [DOI] [PubMed] [Google Scholar]
  8. Humphrey J. H., Grennan D. Different macrophage populations distinguished by means of fluorescent polysaccharides. Recognition and properties of marginal-zone macrophages. Eur J Immunol. 1981 Mar;11(3):221–228. doi: 10.1002/eji.1830110311. [DOI] [PubMed] [Google Scholar]
  9. Kraal G., Hardy R. R., Gallatin W. M., Weissman I. L., Butcher E. C. Antigen-induced changes in B cell subsets in lymph nodes: analysis by dual fluorescence flow cytofluorometry. Eur J Immunol. 1986 Jul;16(7):829–834. doi: 10.1002/eji.1830160718. [DOI] [PubMed] [Google Scholar]
  10. Kraal G., Janse M., Claassen E. Marginal metallophilic macrophages in the mouse spleen: effects of neonatal injections of MOMA-1 antibody on the humoral immune response. Immunol Lett. 1988 Feb;17(2):139–144. doi: 10.1016/0165-2478(88)90082-x. [DOI] [PubMed] [Google Scholar]
  11. Kraal G., Janse M. Marginal metallophilic cells of the mouse spleen identified by a monoclonal antibody. Immunology. 1986 Aug;58(4):665–669. [PMC free article] [PubMed] [Google Scholar]
  12. Kraal G., Rep M., Janse M. Macrophages in T and B cell compartments and other tissue macrophages recognized by monoclonal antibody MOMA-2. An immunohistochemical study. Scand J Immunol. 1987 Dec;26(6):653–661. doi: 10.1111/j.1365-3083.1987.tb02301.x. [DOI] [PubMed] [Google Scholar]
  13. Kraal G., Van Hoogstraten I., Klerx J. P., Van Dijk H. The selective localization of B lymphocytes in the spleen and the role of complement receptors. Eur J Immunol. 1985 Jul;15(7):681–686. doi: 10.1002/eji.1830150708. [DOI] [PubMed] [Google Scholar]
  14. Kumararatne D. S., Bazin H., MacLennan I. C. Marginal zones: the major B cell compartment of rat spleens. Eur J Immunol. 1981 Nov;11(11):858–864. doi: 10.1002/eji.1830111103. [DOI] [PubMed] [Google Scholar]
  15. Liu Y. J., Oldfield S., MacLennan I. C. Memory B cells in T cell-dependent antibody responses colonize the splenic marginal zones. Eur J Immunol. 1988 Mar;18(3):355–362. doi: 10.1002/eji.1830180306. [DOI] [PubMed] [Google Scholar]
  16. Nieuwenhuis P., Ford W. L. Comparative migration of B- and T-Lymphocytes in the rat spleen and lymph nodes. Cell Immunol. 1976 May;23(2):254–267. doi: 10.1016/0008-8749(76)90191-x. [DOI] [PubMed] [Google Scholar]
  17. Pabst R., Geisler R. The route of migration of lymphocytes from blood to spleen and mesenteric lymph nodes in the pig. Cell Tissue Res. 1981;221(2):361–370. doi: 10.1007/BF00216740. [DOI] [PubMed] [Google Scholar]
  18. SNOOK T. STUDIES ON THE PERIFOLLICULAR REGION OF THE RAT'S SPLEEN. Anat Rec. 1964 Feb;148:149–159. doi: 10.1002/ar.1091480205. [DOI] [PubMed] [Google Scholar]
  19. Zatz M. M., Lance E. M. The distribution of chromium 51-labelled lymphoid cells in the mouse. A survey of anatomical compartments. Cell Immunol. 1970 May;1(1):3–17. doi: 10.1016/0008-8749(70)90057-2. [DOI] [PubMed] [Google Scholar]
  20. van Ewijk W., Nieuwenhuis P. Compartments, domains and migration pathways of lymphoid cells in the splenic pulp. Experientia. 1985 Feb 15;41(2):199–208. doi: 10.1007/BF02002614. [DOI] [PubMed] [Google Scholar]
  21. van Rooijen N., Kors N., Kraal G. Macrophage subset repopulation in the spleen: differential kinetics after liposome-mediated elimination. J Leukoc Biol. 1989 Feb;45(2):97–104. doi: 10.1002/jlb.45.2.97. [DOI] [PubMed] [Google Scholar]
  22. van Rooijen N., van Nieuwmegen R. Elimination of phagocytic cells in the spleen after intravenous injection of liposome-encapsulated dichloromethylene diphosphonate. An enzyme-histochemical study. Cell Tissue Res. 1984;238(2):355–358. doi: 10.1007/BF00217308. [DOI] [PubMed] [Google Scholar]

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