Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1988 Nov 1;107(5):1845–1851. doi: 10.1083/jcb.107.5.1845

Evolutionary conservation of tissue-specific lymphocyte-endothelial cell recognition mechanisms involved in lymphocyte homing

PMCID: PMC2115327  PMID: 3182939

Abstract

Tissue-specific interactions with specialized high endothelial venules (HEV) direct the homing of lymphocytes from the blood into peripheral lymph nodes, mucosal lymphoid organs, and tissue sites of chronic inflammation. These interactions have been demonstrated in all mammalian species examined and thus appear highly conserved. To assess the degree of evolutionary divergence in lymphocyte-HEV recognition mechanisms, we have studied the ability of lymphocytes to interact with HEV across species barriers. By using an in vitro assay of lymphocyte binding to HEV in frozen sections of lymphoid tissues, we confirm that mouse, guinea pig, and human lymphocytes bind to xenogeneic as well as homologous HEV. In addition, we show that mouse and human lymphoid cell lines that bind selectively to either peripheral lymph node or mucosal vessels (Peyer's patches, appendix) in homologous lymphoid tissues exhibit the same organ specificity in binding to xenogeneic HEV. Furthermore, monoclonal antibodies that recognize lymphocyte "homing receptors" and block homologous lymphocyte binding to peripheral lymph node or to mucosal HEV, also inhibit lymphocyte interactions with xenogeneic HEV in a tissue-specific fashion. Similarly, anti-HEV antibodies against organ-specific mouse high endothelial cell "addressins" involved in lymphocyte homing to peripheral lymph node or mucosal lymphoid organs, not only block the adhesion of mouse lymphocytes but also of human lymphocytes to target mouse HEV. The results illustrate a remarkable degree of functional conservation of elements mediating these cell-cell recognition events involved in organ- specific lymphocyte homing.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. Barbas J. A., Chaix J. C., Steinmetz M., Goridis C. Differential splicing and alternative polyadenylation generates distinct NCAM transcripts and proteins in the mouse. EMBO J. 1988 Mar;7(3):625–632. doi: 10.1002/j.1460-2075.1988.tb02856.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bargatze R. F., Wu N. W., Weissman I. L., Butcher E. C. High endothelial venule binding as a predictor of the dissemination of passaged murine lymphomas. J Exp Med. 1987 Oct 1;166(4):1125–1131. doi: 10.1084/jem.166.4.1125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bergman Y., Haimovich J. Characterization of a carcinogen-induced murine B lymphocyte cell line of C3H/eB origin. Eur J Immunol. 1977 Jul;7(7):413–417. doi: 10.1002/eji.1830070702. [DOI] [PubMed] [Google Scholar]
  4. Braaten B. A., Spangrude G. J., Daynes R. A. Molecular mechanisms of lymphocyte extravasation. II. Studies of in vitro lymphocyte adherence to high endothelial venules. J Immunol. 1984 Jul;133(1):117–122. [PubMed] [Google Scholar]
  5. Butcher E. C., Scollay R. G., Weissman I. L. Direct fluorescent labeling of cells with fluorescein or rhodamine isothiocyanate. II. Potential application to studies of lymphocyte migration and maturation. J Immunol Methods. 1980;37(2):109–121. doi: 10.1016/0022-1759(80)90196-9. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. Butcher E., Scollay R., Weissman I. Evidence of continuous evolutionary change in structures mediating adherence of lymphocytes to specialised venules. Nature. 1979 Aug 9;280(5722):496–498. doi: 10.1038/280496a0. [DOI] [PubMed] [Google Scholar]
  10. Butcher E., Scollay R., Weissman I. Lymphocyte-high endothelial venule interactions: examination of species specificity. Adv Exp Med Biol. 1979;114:65–72. doi: 10.1007/978-1-4615-9101-6_11. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Cunningham B. A., Hemperly J. J., Murray B. A., Prediger E. A., Brackenbury R., Edelman G. M. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 1987 May 15;236(4803):799–806. doi: 10.1126/science.3576199. [DOI] [PubMed] [Google Scholar]
  14. Dickerson R. E. The structures of cytochrome c and the rates of molecular evolution. J Mol Evol. 1971;1(1):26–45. doi: 10.1007/BF01659392. [DOI] [PubMed] [Google Scholar]
  15. Duijvestijn A. M., Kerkhove M., Bargatze R. F., Butcher E. C. Lymphoid tissue- and inflammation-specific endothelial cell differentiation defined by monoclonal antibodies. J Immunol. 1987 Feb 1;138(3):713–719. [PubMed] [Google Scholar]
  16. Edelman G. M. CAMs and Igs: cell adhesion and the evolutionary origins of immunity. Immunol Rev. 1987 Dec;100:11–45. doi: 10.1111/j.1600-065x.1987.tb00526.x. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Haran-Chera N., Peled A. Thymus and bone marrow derived lymphatic leukaemia in mice. Nature. 1973 Feb 9;241(5389):396–398. doi: 10.1038/241396a0. [DOI] [PubMed] [Google Scholar]
  19. Hynes R. O. Integrins: a family of cell surface receptors. Cell. 1987 Feb 27;48(4):549–554. doi: 10.1016/0092-8674(87)90233-9. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Jalkanen S., Bargatze R. F., de los Toyos J., Butcher E. C. 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. J Cell Biol. 1987 Aug;105(2):983–990. doi: 10.1083/jcb.105.2.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. Littman D. R., Gettner S. N. Unusual intron in the immunoglobulin domain of the newly isolated murine CD4 (L3T4) gene. 1987 Jan 29-Feb 4Nature. 325(6103):453–455. doi: 10.1038/325453a0. [DOI] [PubMed] [Google Scholar]
  26. Nakauchi H., Nolan G. P., Hsu C., Huang H. S., Kavathas P., Herzenberg L. A. Molecular cloning of Lyt-2, a membrane glycoprotein marking a subset of mouse T lymphocytes: molecular homology to its human counterpart, Leu-2/T8, and to immunoglobulin variable regions. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5126–5130. doi: 10.1073/pnas.82.15.5126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ralph P., Nakoinz I., Raschke W. C. Lymphosarcoma cell growth is selectively inhibited by B lymphocyte mitogens: LPS, dextran sulfate and PPD. Biochem Biophys Res Commun. 1974 Dec 23;61(4):1268–1275. doi: 10.1016/s0006-291x(74)80421-3. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Ruoslahti E., Pierschbacher M. D. New perspectives in cell adhesion: RGD and integrins. Science. 1987 Oct 23;238(4826):491–497. doi: 10.1126/science.2821619. [DOI] [PubMed] [Google Scholar]
  30. SIMPSON G. G. The nature and origin of supraspecific taxa. Cold Spring Harb Symp Quant Biol. 1959;24:255–271. doi: 10.1101/sqb.1959.024.01.025. [DOI] [PubMed] [Google Scholar]
  31. Springer T. A., Dustin M. L., Kishimoto T. K., Marlin S. D. The lymphocyte function-associated LFA-1, CD2, and LFA-3 molecules: cell adhesion receptors of the immune system. Annu Rev Immunol. 1987;5:223–252. doi: 10.1146/annurev.iy.05.040187.001255. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Stoolman L. M., Yednock T. A., Rosen S. D. Homing receptors on human and rodent lymphocytes--evidence for a conserved carbohydrate-binding specificity. Blood. 1987 Dec;70(6):1842–1850. [PubMed] [Google Scholar]
  35. Streeter P. R., Berg E. L., Rouse B. T., Bargatze R. F., Butcher E. C. A tissue-specific endothelial cell molecule involved in lymphocyte homing. Nature. 1988 Jan 7;331(6151):41–46. doi: 10.1038/331041a0. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Zamoyska R., Vollmer A. C., Sizer K. C., Liaw C. W., Parnes J. R. Two Lyt-2 polypeptides arise from a single gene by alternative splicing patterns of mRNA. Cell. 1985 Nov;43(1):153–163. doi: 10.1016/0092-8674(85)90020-0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES