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. 1992 Sep 1;176(3):647–655. doi: 10.1084/jem.176.3.647

Sialoadhesin on macrophages: its identification as a lymphocyte adhesion molecule

PMCID: PMC2119373  PMID: 1512534

Abstract

In this study we present evidence that the mouse and rat sialoadhesin (originally named sheep erythrocyte receptor) on macrophages can function as a lymphocyte adhesion molecule. Lymphocytes were shown to bind to the splenic marginal zone, and lymph node subcapsular sinus and medulla in a frozen section assay. Selective depletion experiments showed that binding was mediated by macrophages. Adhesion was blocked by preincubation of the sections with monoclonal antibodies against mouse or rat sialoadhesin. Binding was temperature dependent, divalent cation independent, and involved sialic acid residues on the lymphocyte, as it could be inhibited by prior neuraminidase treatment or addition of the ganglioside GD1a. Binding to sialoadhesin was confirmed using the purified receptor and was observed among T cells, T blasts, B cells, and B blasts. Isolated macrophages or dendritic cells showed little binding. Sialoadhesin provides the first example of a macrophage-restricted lymphocyte adhesion molecule.

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Selected References

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  1. Breel M., Mebius R. E., Kraal G. Dendritic cells of the mouse recognized by two monoclonal antibodies. Eur J Immunol. 1987 Nov;17(11):1555–1559. doi: 10.1002/eji.1830171105. [DOI] [PubMed] [Google Scholar]
  2. Butcher E. C., Scollay R. G., Weissman I. L. Organ specificity of lymphocyte migration: mediation by highly selective lymphocyte interaction with organ-specific determinants on high endothelial venules. Eur J Immunol. 1980 Jul;10(7):556–561. doi: 10.1002/eji.1830100713. [DOI] [PubMed] [Google Scholar]
  3. Chao D., MacPherson G. G. Lymph node macrophage heterogeneity: the phenotypic and functional characterization of two distinct populations of macrophages from rat lymph node. Eur J Immunol. 1989 Jul;19(7):1273–1281. doi: 10.1002/eji.1830190719. [DOI] [PubMed] [Google Scholar]
  4. Crocker P. R., Gordon S. Mouse macrophage hemagglutinin (sheep erythrocyte receptor) with specificity for sialylated glycoconjugates characterized by a monoclonal antibody. J Exp Med. 1989 Apr 1;169(4):1333–1346. doi: 10.1084/jem.169.4.1333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Crocker P. R., Gordon S. Properties and distribution of a lectin-like hemagglutinin differentially expressed by murine stromal tissue macrophages. J Exp Med. 1986 Dec 1;164(6):1862–1875. doi: 10.1084/jem.164.6.1862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crocker P. R., Hill M., Gordon S. Regulation of a murine macrophage haemagglutinin (sheep erythrocyte receptor) by a species-restricted serum factor. Immunology. 1988 Dec;65(4):515–522. [PMC free article] [PubMed] [Google Scholar]
  7. Crocker P. R., Kelm S., Dubois C., Martin B., McWilliam A. S., Shotton D. M., Paulson J. C., Gordon S. Purification and properties of sialoadhesin, a sialic acid-binding receptor of murine tissue macrophages. EMBO J. 1991 Jul;10(7):1661–1669. doi: 10.1002/j.1460-2075.1991.tb07689.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crocker P. R., Morris L., Gordon S. Novel cell surface adhesion receptors involved in interactions between stromal macrophages and haematopoietic cells. J Cell Sci Suppl. 1988;9:185–206. doi: 10.1242/jcs.1988.supplement_9.10. [DOI] [PubMed] [Google Scholar]
  9. Crocker P. R., Werb Z., Gordon S., Bainton D. F. Ultrastructural localization of a macrophage-restricted sialic acid binding hemagglutinin, SER, in macrophage-hematopoietic cell clusters. Blood. 1990 Sep 15;76(6):1131–1138. [PubMed] [Google Scholar]
  10. Dallman M. J., Thomas M. L., Green J. R. MRC OX-19: a monoclonal antibody that labels rat T lymphocytes and augments in vitro proliferative responses. Eur J Immunol. 1984 Mar;14(3):260–267. doi: 10.1002/eji.1830140311. [DOI] [PubMed] [Google Scholar]
  11. Damoiseaux J. G., Döpp E. A., Beelen R. H., Dijkstra C. D. Rat bone marrow and monocyte cultures: influence of culture time and lymphokines on the expression of macrophage differentiation antigens. J Leukoc Biol. 1989 Sep;46(3):246–253. doi: 10.1002/jlb.46.3.246. [DOI] [PubMed] [Google Scholar]
  12. Damoiseaux J. G., Döpp E. A., Dijkstra C. D. Cellular binding mechanism on rat macrophages for sialylated glycoconjugates, inhibited by the monoclonal antibody ED3. J Leukoc Biol. 1991 May;49(5):434–441. doi: 10.1002/jlb.49.5.434. [DOI] [PubMed] [Google Scholar]
  13. Damoiseaux J. G., Döpp E. A., Neefjes J. J., Beelen R. H., Dijkstra C. D. Heterogeneity of macrophages in the rat evidenced by variability in determinants: two new anti-rat macrophage antibodies against a heterodimer of 160 and 95 kd (CD11/CD18). J Leukoc Biol. 1989 Dec;46(6):556–564. doi: 10.1002/jlb.46.6.556. [DOI] [PubMed] [Google Scholar]
  14. Damoiseaux J. G., Huitinga I., Döpp E. A., Dijkstra C. D. Expression of the ED3 antigen on rat macrophages in relation to experimental autoimmune diseases. Immunobiology. 1992 Apr;184(4-5):311–320. doi: 10.1016/S0171-2985(11)80589-9. [DOI] [PubMed] [Google Scholar]
  15. Delemarre F. G., Kors N., Kraal G., van Rooijen N. Repopulation of macrophages in popliteal lymph nodes of mice after liposome-mediated depletion. J Leukoc Biol. 1990 Mar;47(3):251–257. doi: 10.1002/jlb.47.3.251. [DOI] [PubMed] [Google Scholar]
  16. Dijkstra C. D., Döpp E. A., Joling P., Kraal G. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology. 1985 Mar;54(3):589–599. [PMC free article] [PubMed] [Google Scholar]
  17. Freedman A. S., Munro J. M., Rice G. E., Bevilacqua M. P., Morimoto C., McIntyre B. W., Rhynhart K., Pober J. S., Nadler L. M. Adhesion of human B cells to germinal centers in vitro involves VLA-4 and INCAM-110. Science. 1990 Aug 31;249(4972):1030–1033. doi: 10.1126/science.1697696. [DOI] [PubMed] [Google Scholar]
  18. Hamann A., Jablonski-Westrich D., Duijvestijn A., Butcher E. C., Baisch H., Harder R., Thiele H. G. Evidence for an accessory role of LFA-1 in lymphocyte-high endothelium interaction during homing. J Immunol. 1988 Feb 1;140(3):693–699. [PubMed] [Google Scholar]
  19. Holzmann B., McIntyre B. W., Weissman I. L. Identification of a murine Peyer's patch--specific lymphocyte homing receptor as an integrin molecule with an alpha chain homologous to human VLA-4 alpha. Cell. 1989 Jan 13;56(1):37–46. doi: 10.1016/0092-8674(89)90981-1. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Picker L. J., Kishimoto T. K., Smith C. W., Warnock R. A., Butcher E. C. ELAM-1 is an adhesion molecule for skin-homing T cells. Nature. 1991 Feb 28;349(6312):796–799. doi: 10.1038/349796a0. [DOI] [PubMed] [Google Scholar]
  23. Shaw S., Luce G. E., Quinones R., Gress R. E., Springer T. A., Sanders M. E. Two antigen-independent adhesion pathways used by human cytotoxic T-cell clones. Nature. 1986 Sep 18;323(6085):262–264. doi: 10.1038/323262a0. [DOI] [PubMed] [Google Scholar]
  24. Shimizu Y., Shaw S., Graber N., Gopal T. V., Horgan K. J., Van Seventer G. A., Newman W. Activation-independent binding of human memory T cells to adhesion molecule ELAM-1. Nature. 1991 Feb 28;349(6312):799–802. doi: 10.1038/349799a0. [DOI] [PubMed] [Google Scholar]
  25. Springer T. A. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. doi: 10.1038/346425a0. [DOI] [PubMed] [Google Scholar]
  26. Streeter P. R., Rouse B. T., Butcher E. C. Immunohistologic and functional characterization of a vascular addressin involved in lymphocyte homing into peripheral lymph nodes. J Cell Biol. 1988 Nov;107(5):1853–1862. doi: 10.1083/jcb.107.5.1853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Van Rooijen N. The liposome-mediated macrophage 'suicide' technique. J Immunol Methods. 1989 Nov 13;124(1):1–6. doi: 10.1016/0022-1759(89)90178-6. [DOI] [PubMed] [Google Scholar]
  28. Van den Berg T. K., Döpp E. A., Brevé J. J., Kraal G., Dijkstra C. D. The heterogeneity of the reticulum of rat peripheral lymphoid organs identified by monoclonal antibodies. Eur J Immunol. 1989 Sep;19(9):1747–1756. doi: 10.1002/eji.1830190933. [DOI] [PubMed] [Google Scholar]
  29. van Vliet E., Melis M., van Ewijk W. Marginal zone macrophages in the mouse spleen identified by a monoclonal antibody. Anatomical correlation with a B cell subpopulation. J Histochem Cytochem. 1985 Jan;33(1):40–44. doi: 10.1177/33.1.3880783. [DOI] [PubMed] [Google Scholar]

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