Skip to main content
PMC home page
Cell Regulation logoLink to Cell Regulation
. 1989 Nov;1(1):27–35. doi: 10.1091/mbc.1.1.27

B lymphocytes express and lose syndecan at specific stages of differentiation.

R D Sanderson 1, P Lalor 1, M Bernfield 1
PMCID: PMC361422  PMID: 2519615

Abstract

Lymphopoietic cells require interactions with bone marrow stroma for normal maturation and show changes in adhesion to matrix during their differentiation. Syndecan, a heparan sulfate-rich integral membrane proteoglycan, functions as a matrix receptor by binding cells to interstitial collagens, fibronectin, and thrombospondin. Therefore, we asked whether syndecan was present on the surface of lymphopoietic cells. In bone marrow, we find syndecan only on precursor B cells. Expression changes with pre-B cell maturation in the marrow and with B-lymphocyte differentiation to plasma cells in interstitial matrices. Syndecan on B cell precursors is more heterogeneous and slightly larger than on plasma cells. Syndecan 1) is lost immediately before maturation and release of B lymphocytes into the circulation, 2) is absent on circulating and peripheral B lymphocytes, and 3) is reexpressed upon their differentiation into immobilized plasma cells. Thus, syndecan is expressed only when and where B lymphocytes associate with extracellular matrix. These results indicate that B cells differentiating in vivo alter their matrix receptor expression and suggest a role for syndecan in B cell stage-specific adhesion.

Full text

PDF
27

Images in this article

30Image
on p.30
31Image
on p.31

Selected References

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

  1. Bentley S. A. Close range cell:cell interaction required for stem cell maintenance in continuous bone marrow culture. Exp Hematol. 1981 Mar;9(3):308–312. [PubMed] [Google Scholar]
  2. Bentley S. A., Foidart J. M. Some properties of marrow derived adherent cells in tissue culture. Blood. 1980 Dec;56(6):1006–1012. [PubMed] [Google Scholar]
  3. Bernardi P., Patel V. P., Lodish H. F. Lymphoid precursor cells adhere to two different sites on fibronectin. J Cell Biol. 1987 Jul;105(1):489–498. doi: 10.1083/jcb.105.1.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Campbell A., Wicha M. S., Long M. Extracellular matrix promotes the growth and differentiation of murine hematopoietic cells in vitro. J Clin Invest. 1985 Jun;75(6):2085–2090. doi: 10.1172/JCI111928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carter W. G., Wayner E. A. Characterization of the class III collagen receptor, a phosphorylated, transmembrane glycoprotein expressed in nucleated human cells. J Biol Chem. 1988 Mar 25;263(9):4193–4201. [PubMed] [Google Scholar]
  6. Chiarugi V. P., Vannucchi S. Surface heparan sulphate as a control element in eukariotic cells: a working model. J Theor Biol. 1976 Sep 21;61(2):459–475. doi: 10.1016/0022-5193(76)90030-8. [DOI] [PubMed] [Google Scholar]
  7. Chiquet-Ehrismann R., Mackie E. J., Pearson C. A., Sakakura T. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell. 1986 Oct 10;47(1):131–139. doi: 10.1016/0092-8674(86)90374-0. [DOI] [PubMed] [Google Scholar]
  8. Coffman R. L. Surface antigen expression and immunoglobulin gene rearrangement during mouse pre-B cell development. Immunol Rev. 1982;69:5–23. doi: 10.1111/j.1600-065x.1983.tb00446.x. [DOI] [PubMed] [Google Scholar]
  9. Coffman R. L., Weissman I. L. B220: a B cell-specific member of th T200 glycoprotein family. Nature. 1981 Feb 19;289(5799):681–683. doi: 10.1038/289681a0. [DOI] [PubMed] [Google Scholar]
  10. Dexter T. M., Spooncer E., Schofield R., Lord B. I., Simmons P. Haemopoietic stem cells and the problem of self-renewal. Blood Cells. 1984;10(2-3):315–339. [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. Gordon M. Y., Riley G. P., Watt S. M., Greaves M. F. Compartmentalization of a haematopoietic growth factor (GM-CSF) by glycosaminoglycans in the bone marrow microenvironment. 1987 Mar 26-Apr 1Nature. 326(6111):403–405. doi: 10.1038/326403a0. [DOI] [PubMed] [Google Scholar]
  14. Hayashi K., Hayashi M., Jalkanen M., Firestone J. H., Trelstad R. L., Bernfield M. Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissues. A light and electron microscopic study. J Histochem Cytochem. 1987 Oct;35(10):1079–1088. doi: 10.1177/35.10.2957423. [DOI] [PubMed] [Google Scholar]
  15. Herzenberg L. A., Stall A. M., Braun J., Weaver D., Baltimore D., Herzenberg L. A., Grosschedl R. Depletion of the predominant B-cell population in immunoglobulin mu heavy-chain transgenic mice. Nature. 1987 Sep 3;329(6134):71–73. doi: 10.1038/329071a0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Jalkanen S., Jalkanen M., Bargatze R., Tammi M., Butcher E. C. Biochemical properties of glycoproteins involved in lymphocyte recognition of high endothelial venules in man. J Immunol. 1988 Sep 1;141(5):1615–1623. [PubMed] [Google Scholar]
  18. Kincade P. W., Lee G., Sun L., Watanabe T. Monoclonal rat antibodies to murine IgM determinants. J Immunol Methods. 1981;42(1):17–26. doi: 10.1016/0022-1759(81)90220-9. [DOI] [PubMed] [Google Scholar]
  19. Klebe R. J., Mock P. J. Effect of glycosaminoglycans on fibronectin-mediated cell attachment. J Cell Physiol. 1982 Jul;112(1):5–9. doi: 10.1002/jcp.1041120103. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Lee G., Namen A. E., Gillis S., Ellingsworth L. R., Kincade P. W. Normal B cell precursors responsive to recombinant murine IL-7 and inhibition of IL-7 activity by transforming growth factor-beta. J Immunol. 1989 Jun 1;142(11):3875–3883. [PubMed] [Google Scholar]
  22. Liao N. S., St John J., Du Z. J., Cheung H. T. Adhesion of lymphoid cell lines to fibronectin-coated substratum: biochemical and physiological characterization and the identification of a 140-kDa fibronectin receptor. Exp Cell Res. 1987 Aug;171(2):306–320. doi: 10.1016/0014-4827(87)90164-9. [DOI] [PubMed] [Google Scholar]
  23. Patel V. P., Lodish H. F. The fibronectin receptor on mammalian erythroid precursor cells: characterization and developmental regulation. J Cell Biol. 1986 Feb;102(2):449–456. doi: 10.1083/jcb.102.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rapraeger A., Jalkanen M., Bernfield M. Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J Cell Biol. 1986 Dec;103(6 Pt 2):2683–2696. doi: 10.1083/jcb.103.6.2683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Roberts R., Gallagher J., Spooncer E., Allen T. D., Bloomfield F., Dexter T. M. Heparan sulphate bound growth factors: a mechanism for stromal cell mediated haemopoiesis. Nature. 1988 Mar 24;332(6162):376–378. doi: 10.1038/332376a0. [DOI] [PubMed] [Google Scholar]
  26. Sanderson R. D., Bernfield M. Molecular polymorphism of a cell surface proteoglycan: distinct structures on simple and stratified epithelia. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9562–9566. doi: 10.1073/pnas.85.24.9562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Saunders S., Bernfield M. Cell surface proteoglycan binds mouse mammary epithelial cells to fibronectin and behaves as a receptor for interstitial matrix. J Cell Biol. 1988 Feb;106(2):423–430. doi: 10.1083/jcb.106.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Saunders S., Jalkanen M., O'Farrell S., Bernfield M. Molecular cloning of syndecan, an integral membrane proteoglycan. J Cell Biol. 1989 Apr;108(4):1547–1556. doi: 10.1083/jcb.108.4.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Spangrude G. J., Heimfeld S., Weissman I. L. Purification and characterization of mouse hematopoietic stem cells. Science. 1988 Jul 1;241(4861):58–62. doi: 10.1126/science.2898810. [DOI] [PubMed] [Google Scholar]
  30. Spooncer E., Gallagher J. T., Krizsa F., Dexter T. M. Regulation of haemopoiesis in long-term bone marrow cultures. IV. Glycosaminoglycan synthesis and the stimulation of haemopoiesis by beta-D-xylosides. J Cell Biol. 1983 Feb;96(2):510–514. doi: 10.1083/jcb.96.2.510. [DOI] [PMC free article] [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. Springer T., Galfré G., Secher D. S., Milstein C. Mac-1: a macrophage differentiation antigen identified by monoclonal antibody. Eur J Immunol. 1979 Apr;9(4):301–306. doi: 10.1002/eji.1830090410. [DOI] [PubMed] [Google Scholar]
  33. Stall A. M., Loken M. R. Allotypic specificities of murine IgD and IgM recognized by monoclonal antibodies. J Immunol. 1984 Feb;132(2):787–795. [PubMed] [Google Scholar]
  34. Stamatoglou S. C., Keller J. M. Correlation between cell substrate attachment in vitro and cell surface heparan sulfate affinity for fibronectin and collagen. J Cell Biol. 1983 Jun;96(6):1820–1823. doi: 10.1083/jcb.96.6.1820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stoolman L. M. Adhesion molecules controlling lymphocyte migration. Cell. 1989 Mar 24;56(6):907–910. doi: 10.1016/0092-8674(89)90620-x. [DOI] [PubMed] [Google Scholar]
  36. Strasser A. PB76: a novel surface glycoprotein preferentially expressed on mouse pre-B cells and plasma cells detected by the monoclonal antibody G-5-2. Eur J Immunol. 1988 Nov;18(11):1803–1810. doi: 10.1002/eji.1830181123. [DOI] [PubMed] [Google Scholar]
  37. Sun X., Mosher D. F., Rapraeger A. Heparan sulfate-mediated binding of epithelial cell surface proteoglycan to thrombospondin. J Biol Chem. 1989 Feb 15;264(5):2885–2889. [PubMed] [Google Scholar]
  38. Thesleff I., Jalkanen M., Vainio S., Bernfield M. Cell surface proteoglycan expression correlates with epithelial-mesenchymal interaction during tooth morphogenesis. Dev Biol. 1988 Oct;129(2):565–572. doi: 10.1016/0012-1606(88)90401-0. [DOI] [PubMed] [Google Scholar]
  39. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Vainio S., Lehtonen E., Jalkanen M., Bernfield M., Saxén L. Epithelial-mesenchymal interactions regulate the stage-specific expression of a cell surface proteoglycan, syndecan, in the developing kidney. Dev Biol. 1989 Aug;134(2):382–391. doi: 10.1016/0012-1606(89)90110-3. [DOI] [PubMed] [Google Scholar]
  41. Zuckerman K. S., Rhodes R. K., Goodrum D. D., Patel V. R., Sparks B., Wells J., Wicha M. S., Mayo L. A. Inhibition of collagen deposition in the extracellular matrix prevents the establishment of a stroma supportive of hematopoiesis in long-term murine bone marrow cultures. J Clin Invest. 1985 Mar;75(3):970–975. doi: 10.1172/JCI111798. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Cell Regulation are provided here courtesy of American Society for Cell Biology

RESOURCES