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. 1987 Aug 1;105(2):983–990. doi: 10.1083/jcb.105.2.983

Lymphocyte recognition of high endothelium: antibodies to distinct epitopes of an 85-95-kD glycoprotein antigen differentially inhibit lymphocyte binding to lymph node, mucosal, or synovial endothelial cells

PMCID: PMC2114763  PMID: 2442176

Abstract

The tissue-specific homing of lymphocytes is directed by specialized high endothelial venules (HEV). At least three functionally independent lymphocyte/HEV recognition systems exist, controlling the extravasation of circulating lymphocytes into peripheral lymph nodes, mucosal lymphoid tissues (Peyer's patches or appendix), and the synovium of inflamed joints. We report here that antibodies capable of inhibiting human lymphocyte binding to one or more HEV types recognize a common 85- 95-kD lymphocyte surface glycoprotein antigen, defined by the non- blocking monoclonal antibody, Hermes-1. We demonstrate that MEL-14, a monoclonal antibody against putative lymph node "homing receptors" in the mouse, functionally inhibits human lymphocyte binding to lymph node HEV but not to mucosal or synovial HEV, and cross-reacts with the 85-95- kD Hermes-1 antigen. Furthermore, we show that Hermes-3, a novel antibody produced by immunization with Hermes-1 antigen isolated from a mucosal HEV-specific cell line, selectively blocks lymphocyte binding to mucosal HEV. Such tissue specificity of inhibition suggests that MEL- 14 and Hermes-3 block the function of specific lymphocyte recognition elements for lymph node and mucosal HEV, respectively. Recognition of synovial HEV also involves the 85-95-kD Hermes-1 antigen, in that a polyclonal antiserum produced against the isolated antigen blocks all three classes of lymphocyte-HEV interaction. From these studies, it is likely that the Hermes-1-defined 85-95-kD glycoprotein class either comprises a family of related but functionally independent receptors for HEV, or associates both physically and functionally with such receptors. The findings imply that related molecular mechanisms are involved in several functionally independent cell-cell recognition events that direct lymphocyte traffic.

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Selected References

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  1. Bourne H. R. GTP-binding proteins. One molecular machine can transduce diverse signals. 1986 Jun 26-Jul 2Nature. 321(6073):814–816. doi: 10.1038/321814a0. [DOI] [PubMed] [Google Scholar]
  2. Butcher E. C., Scollay R. G., Weissman I. L. Lymphocyte adherence to high endothelial venules: characterization of a modified in vitro assay, and examination of the binding of syngeneic and allogeneic lymphocyte populations. J Immunol. 1979 Nov;123(5):1996–2003. [PubMed] [Google Scholar]
  3. Butcher E. C. The regulation of lymphocyte traffic. Curr Top Microbiol Immunol. 1986;128:85–122. doi: 10.1007/978-3-642-71272-2_3. [DOI] [PubMed] [Google Scholar]
  4. Carpenter D., Jackson T., Hanley M. R. Protein kinase Cs. Coping with a growing family. Nature. 1987 Jan 8;325(7000):107–108. doi: 10.1038/325107a0. [DOI] [PubMed] [Google Scholar]
  5. Chin Y. H., Rasmussen R. A., Woodruff J. J., Easton T. G. A monoclonal anti-HEBFPP antibody with specificity for lymphocyte surface molecules mediating adhesion to Peyer's patch high endothelium of the rat. J Immunol. 1986 Apr 1;136(7):2556–2561. [PubMed] [Google Scholar]
  6. Chin Y. H., Rasmussen R., Cakiroglu A. G., Woodruff J. J. Lymphocyte recognition of lymph node high endothelium. VI. Evidence of distinct structures mediating binding to high endothelial cells of lymph nodes and Peyer's patches. J Immunol. 1984 Dec;133(6):2961–2965. [PubMed] [Google Scholar]
  7. Damsky C. H., Richa J., Solter D., Knudsen K., Buck C. A. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell. 1983 Sep;34(2):455–466. doi: 10.1016/0092-8674(83)90379-3. [DOI] [PubMed] [Google Scholar]
  8. Edelman G. M. Cell adhesion molecules. Science. 1983 Feb 4;219(4584):450–457. doi: 10.1126/science.6823544. [DOI] [PubMed] [Google Scholar]
  9. Faissner A., Kruse J., Goridis C., Bock E., Schachner M. The neural cell adhesion molecule L1 is distinct from the N-CAM related group of surface antigens BSP-2 and D2. EMBO J. 1984 Apr;3(4):733–737. doi: 10.1002/j.1460-2075.1984.tb01876.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gallatin M., St John T. P., Siegelman M., Reichert R., Butcher E. C., Weissman I. L. Lymphocyte homing receptors. Cell. 1986 Mar 14;44(5):673–680. doi: 10.1016/0092-8674(86)90832-9. [DOI] [PubMed] [Google Scholar]
  11. Gallatin W. M., Weissman I. L., Butcher E. C. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature. 1983 Jul 7;304(5921):30–34. doi: 10.1038/304030a0. [DOI] [PubMed] [Google Scholar]
  12. Grumet M., Edelman G. M. Heterotypic binding between neuronal membrane vesicles and glial cells is mediated by a specific cell adhesion molecule. J Cell Biol. 1984 May;98(5):1746–1756. doi: 10.1083/jcb.98.5.1746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hershko A. Ubiquitin: roles in protein modification and breakdown. Cell. 1983 Aug;34(1):11–12. doi: 10.1016/0092-8674(83)90131-9. [DOI] [PubMed] [Google Scholar]
  14. Jalkanen M., Nguyen H., Rapraeger A., Kurn N., Bernfield M. Heparan sulfate proteoglycans from mouse mammary epithelial cells: localization on the cell surface with a monoclonal antibody. J Cell Biol. 1985 Sep;101(3):976–984. doi: 10.1083/jcb.101.3.976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jalkanen S. T., Bargatze R. F., Herron L. R., Butcher E. C. A lymphoid cell surface glycoprotein involved in endothelial cell recognition and lymphocyte homing in man. Eur J Immunol. 1986 Oct;16(10):1195–1202. doi: 10.1002/eji.1830161003. [DOI] [PubMed] [Google Scholar]
  16. Jalkanen S. T., Butcher E. C. In vitro analysis of the homing properties of human lymphocytes: developmental regulation of functional receptors for high endothelial venules. Blood. 1985 Sep;66(3):577–582. [PubMed] [Google Scholar]
  17. Jalkanen S., Reichert R. A., Gallatin W. M., Bargatze R. F., Weissman I. L., Butcher E. C. Homing receptors and the control of lymphocyte migration. Immunol Rev. 1986 Jun;91:39–60. doi: 10.1111/j.1600-065x.1986.tb01483.x. [DOI] [PubMed] [Google Scholar]
  18. Jalkanen S., Steere A. C., Fox R. I., Butcher E. C. A distinct endothelial cell recognition system that controls lymphocyte traffic into inflamed synovium. Science. 1986 Aug 1;233(4763):556–558. doi: 10.1126/science.3726548. [DOI] [PubMed] [Google Scholar]
  19. Köhler G., Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature. 1975 Aug 7;256(5517):495–497. doi: 10.1038/256495a0. [DOI] [PubMed] [Google Scholar]
  20. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  21. Ledbetter J. A., Herzenberg L. A. Xenogeneic monoclonal antibodies to mouse lymphoid differentiation antigens. Immunol Rev. 1979;47:63–90. doi: 10.1111/j.1600-065x.1979.tb00289.x. [DOI] [PubMed] [Google Scholar]
  22. Rasmussen R. A., Chin Y. H., Woodruff J. J., Easton T. G. Lymphocyte recognition of lymph node high endothelium. VII. Cell surface proteins involved in adhesion defined by monoclonal anti-HEBFLN (A.11) antibody. J Immunol. 1985 Jul;135(1):19–24. [PubMed] [Google Scholar]
  23. Rogers G. N., Paulson J. C., Daniels R. S., Skehel J. J., Wilson I. A., Wiley D. C. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature. 1983 Jul 7;304(5921):76–78. doi: 10.1038/304076a0. [DOI] [PubMed] [Google Scholar]
  24. Rutishauser U. Developmental biology of a neural cell adhesion molecule. Nature. 1984 Aug 16;310(5978):549–554. doi: 10.1038/310549a0. [DOI] [PubMed] [Google Scholar]
  25. Shulman M., Wilde C. D., Köhler G. A better cell line for making hybridomas secreting specific antibodies. Nature. 1978 Nov 16;276(5685):269–270. doi: 10.1038/276269a0. [DOI] [PubMed] [Google Scholar]
  26. Siegelman M., Bond M. W., Gallatin W. M., St John T., Smith H. T., Fried V. A., Weissman I. L. Cell surface molecule associated with lymphocyte homing is a ubiquitinated branched-chain glycoprotein. Science. 1986 Feb 21;231(4740):823–829. doi: 10.1126/science.3003913. [DOI] [PubMed] [Google Scholar]
  27. St John T., Gallatin W. M., Siegelman M., Smith H. T., Fried V. A., Weissman I. L. Expression cloning of a lymphocyte homing receptor cDNA: ubiquitin is the reactive species. Science. 1986 Feb 21;231(4740):845–850. doi: 10.1126/science.3003914. [DOI] [PubMed] [Google Scholar]
  28. Stamper H. B., Jr, Woodruff J. J. Lymphocyte homing into lymph nodes: in vitro demonstration of the selective affinity of recirculating lymphocytes for high-endothelial venules. J Exp Med. 1976 Sep 1;144(3):828–833. doi: 10.1084/jem.144.3.828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stevens S. K., Weissman I. L., Butcher E. C. Differences in the migration of B and T lymphocytes: organ-selective localization in vivo and the role of lymphocyte-endothelial cell recognition. J Immunol. 1982 Feb;128(2):844–851. [PubMed] [Google Scholar]
  30. Stoolman L. M., Tenforde T. S., Rosen S. D. Phosphomannosyl receptors may participate in the adhesive interaction between lymphocytes and high endothelial venules. J Cell Biol. 1984 Oct;99(4 Pt 1):1535–1540. doi: 10.1083/jcb.99.4.1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wood G. S., Link M., Warnke R. A., Dilley J., Levy R. Pan-leukocyte monoclonal antibody L3B12. Characterization and application to research and diagnostic problems. Am J Clin Pathol. 1984 Feb;81(2):176–183. doi: 10.1093/ajcp/81.2.176. [DOI] [PubMed] [Google Scholar]
  32. Yednock T. A., Butcher E. C., Stoolman L. M., Rosen S. D. Receptors involved in lymphocyte homing: relationship between a carbohydrate-binding receptor and the MEL-14 antigen. J Cell Biol. 1987 Mar;104(3):725–731. doi: 10.1083/jcb.104.3.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Yoshida C., Takeichi M. Teratocarcinoma cell adhesion: identification of a cell-surface protein involved in calcium-dependent cell aggregation. Cell. 1982 Feb;28(2):217–224. doi: 10.1016/0092-8674(82)90339-7. [DOI] [PubMed] [Google Scholar]

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