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. 1987 Jul 1;105(1):489–498. doi: 10.1083/jcb.105.1.489

Lymphoid precursor cells adhere to two different sites on fibronectin

PMCID: PMC2114903  PMID: 2956270

Abstract

Several precursor lymphoid cell lines, blocked at specific stages of differentiation, adhere specifically to fibronectin in vitro. Whereas the Ba F3 cell line, which has both immunoglobulin heavy- and light- chain genes in germline configuration, interacts with the arg-gly-asp- containing cell-binding domain of fibronectin, the B-committed line PD 31, which is undergoing rearrangement of immunoglobulin light-chain genes, does not. Accordingly the Ba F3, but not the putative PD 31 surface fibronectin receptor, binds to an affinity matrix containing the 115-kD cell-binding domain of fibronectin. PD 31 cells recognize a different domain of the fibronectin molecule, which is contained within the carboxy terminal segment possessing a high-affinity binding site for heparin. A polyclonal antibody raised against the fibronectin receptor of mouse erythroleukemic cells inhibits adhesion of these lymphoid lines to fibronectin. It precipitates two major species of 140 and 70 kD from surface-radioiodinated Ba F3 cells and species of 140 and 120 kD from PD 31 cells. We propose that the two types of cells express different fibronectin receptors mediating substrate adhesion, and suggest that receptor(s) with different specificity might be expressed in the course of B cell maturation. Because we show that these adhesion properties are shared by normal bone marrow lymphoid precursors, we infer that these receptors may play a role in normal lymphopoiesis.

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Selected References

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  1. Akiyama S. K., Yamada S. S., Yamada K. M. Characterization of a 140-kD avian cell surface antigen as a fibronectin-binding molecule. J Cell Biol. 1986 Feb;102(2):442–448. doi: 10.1083/jcb.102.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alt F. W., Enea V., Bothwell A. L., Baltimore D. Activity of multiple light chain genes in murine myeloma cells producing a single, functional light chain. Cell. 1980 Aug;21(1):1–12. doi: 10.1016/0092-8674(80)90109-9. [DOI] [PubMed] [Google Scholar]
  3. Bennett J. S., Vilaire G., Cines D. B. Identification of the fibrinogen receptor on human platelets by photoaffinity labeling. J Biol Chem. 1982 Jul 25;257(14):8049–8054. [PubMed] [Google Scholar]
  4. Burns G. F., Cosgrove L., Triglia T., Beall J. A., López A. F., Werkmeister J. A., Begley C. G., Haddad A. P., d'Apice A. J., Vadas M. A. The IIb-IIIa glycoprotein complex that mediates platelet aggregation is directly implicated in leukocyte adhesion. Cell. 1986 Apr 25;45(2):269–280. doi: 10.1016/0092-8674(86)90391-0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Cosgrove L. J., Sandrin M. S., Rajasekariah P., McKenzie I. F. A genomic clone encoding the alpha chain of the OKM1, LFA-1, and platelet glycoprotein IIb-IIIa molecules. Proc Natl Acad Sci U S A. 1986 Feb;83(3):752–756. doi: 10.1073/pnas.83.3.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davignon D., Martz E., Reynolds T., Kürzinger K., Springer T. A. Lymphocyte function-associated antigen 1 (LFA-1): a surface antigen distinct from Lyt-2,3 that participates in T lymphocyte-mediated killing. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4535–4539. doi: 10.1073/pnas.78.7.4535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dexter T. M., Heyworth C., Spooncer E. Studies on the self-renewal and differentiation of stem cells in long term marrow cultures. Prog Clin Biol Res. 1985;184:235–246. [PubMed] [Google Scholar]
  9. Fitzgerald L. A., Charo I. F., Phillips D. R. Human and bovine endothelial cells synthesize membrane proteins similar to human platelet glycoproteins IIb and IIIa. J Biol Chem. 1985 Sep 15;260(20):10893–10896. [PubMed] [Google Scholar]
  10. GOWANS J. L., KNIGHT E. J. THE ROUTE OF RE-CIRCULATION OF LYMPHOCYTES IN THE RAT. Proc R Soc Lond B Biol Sci. 1964 Jan 14;159:257–282. doi: 10.1098/rspb.1964.0001. [DOI] [PubMed] [Google Scholar]
  11. Gardner J. M., Hynes R. O. Interaction of fibronectin with its receptor on platelets. Cell. 1985 Sep;42(2):439–448. doi: 10.1016/0092-8674(85)90101-1. [DOI] [PubMed] [Google Scholar]
  12. Giancotti F. G., Comoglio P. M., Tarone G. Fibronectin-plasma membrane interaction in the adhesion of hemopoietic cells. J Cell Biol. 1986 Aug;103(2):429–437. doi: 10.1083/jcb.103.2.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Giancotti F. G., Tarone G., Knudsen K., Damsky C., Comoglio P. M. Cleavage of a 135 kD cell surface glycoprotein correlates with loss of fibroblast adhesion to fibronectin. Exp Cell Res. 1985 Jan;156(1):182–190. doi: 10.1016/0014-4827(85)90272-1. [DOI] [PubMed] [Google Scholar]
  14. Ginsberg M., Pierschbacher M. D., Ruoslahti E., Marguerie G., Plow E. Inhibition of fibronectin binding to platelets by proteolytic fragments and synthetic peptides which support fibroblast adhesion. J Biol Chem. 1985 Apr 10;260(7):3931–3936. [PubMed] [Google Scholar]
  15. Gowans J. L. The origin and development of lymphocytes. J Reticuloendothel Soc. 1975 Feb;17(2):97–98. [PubMed] [Google Scholar]
  16. Horwitz A., Duggan K., Greggs R., Decker C., Buck C. The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J Cell Biol. 1985 Dec;101(6):2134–2144. doi: 10.1083/jcb.101.6.2134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kuehl W. M., Scharff M. D. Synthesis of a carboxyl-terminal (constant region) fragment of the immunoglobulin light chain by a mouse myeloma cell line. J Mol Biol. 1974 Nov 5;89(3):409–421. doi: 10.1016/0022-2836(74)90472-0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Lewis S., Rosenberg N., Alt F., Baltimore D. Continuing kappa-gene rearrangement in a cell line transformed by Abelson murine leukemia virus. Cell. 1982 Oct;30(3):807–816. doi: 10.1016/0092-8674(82)90285-9. [DOI] [PubMed] [Google Scholar]
  20. McCarthy J. B., Hagen S. T., Furcht L. T. Human fibronectin contains distinct adhesion- and motility-promoting domains for metastatic melanoma cells. J Cell Biol. 1986 Jan;102(1):179–188. doi: 10.1083/jcb.102.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Oliver J. P., Goldstein A. L. Rapid method for preparing bone marrow cells from small laboratory animals. J Immunol Methods. 1978;19(2-3):289–292. doi: 10.1016/0022-1759(78)90188-6. [DOI] [PubMed] [Google Scholar]
  22. Osmond D. G., Nossal G. J. Differentiation of lymphocytes in mouse bone marrow. II. Kinetics of maturation and renewal of antiglobulin-binding cells studied by double labeling. Cell Immunol. 1974 Jul;13(1):132–145. doi: 10.1016/0008-8749(74)90233-0. [DOI] [PubMed] [Google Scholar]
  23. Paige C. J., Kincade P. W., Ralph P. Murine B cell leukemia line with inducible surface immunoglobulin expression. J Immunol. 1978 Aug;121(2):641–647. [PubMed] [Google Scholar]
  24. Palacios R., Steinmetz M. Il-3-dependent mouse clones that express B-220 surface antigen, contain Ig genes in germ-line configuration, and generate B lymphocytes in vivo. Cell. 1985 Jul;41(3):727–734. doi: 10.1016/s0092-8674(85)80053-2. [DOI] [PubMed] [Google Scholar]
  25. Patel V. P., Ciechanover A., Platt O., Lodish H. F. Mammalian reticulocytes lose adhesion to fibronectin during maturation to erythrocytes. Proc Natl Acad Sci U S A. 1985 Jan;82(2):440–444. doi: 10.1073/pnas.82.2.440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Patel V. P., Lodish H. F. Loss of adhesion of murine erythroleukemia cells to fibronectin during erythroid differentiation. Science. 1984 Jun 1;224(4652):996–998. doi: 10.1126/science.6585955. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Pierschbacher M. D., Ruoslahti E., Sundelin J., Lind P., Peterson P. A. The cell attachment domain of fibronectin. Determination of the primary structure. J Biol Chem. 1982 Aug 25;257(16):9593–9597. [PubMed] [Google Scholar]
  29. Pytela R., Pierschbacher M. D., Ginsberg M. H., Plow E. F., Ruoslahti E. Platelet membrane glycoprotein IIb/IIIa: member of a family of Arg-Gly-Asp--specific adhesion receptors. Science. 1986 Mar 28;231(4745):1559–1562. doi: 10.1126/science.2420006. [DOI] [PubMed] [Google Scholar]
  30. Pytela R., Pierschbacher M. D., Ruoslahti E. Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell. 1985 Jan;40(1):191–198. doi: 10.1016/0092-8674(85)90322-8. [DOI] [PubMed] [Google Scholar]
  31. Ralph P. Functional subsets of murine and human B lymphocyte cell lines. Immunol Rev. 1979;48:107–121. doi: 10.1111/j.1600-065x.1979.tb00300.x. [DOI] [PubMed] [Google Scholar]
  32. Ruggeri Z. M., Bader R., de Marco L. Glanzmann thrombasthenia: deficient binding of von Willebrand factor to thrombin-stimulated platelets. Proc Natl Acad Sci U S A. 1982 Oct;79(19):6038–6041. doi: 10.1073/pnas.79.19.6038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ruoslahti E., Hayman E. G., Engvall E., Cothran W. C., Butler W. T. Alignment of biologically active domains in the fibronectin molecule. J Biol Chem. 1981 Jul 25;256(14):7277–7281. [PubMed] [Google Scholar]
  34. Ruoslahti E., Hayman E. G., Pierschbacher M., Engvall E. Fibronectin: purification, immunochemical properties, and biological activities. Methods Enzymol. 1982;82(Pt A):803–831. doi: 10.1016/0076-6879(82)82103-4. [DOI] [PubMed] [Google Scholar]
  35. Ruoslahti E., Pierschbacher M. D. Arg-Gly-Asp: a versatile cell recognition signal. Cell. 1986 Feb 28;44(4):517–518. doi: 10.1016/0092-8674(86)90259-x. [DOI] [PubMed] [Google Scholar]
  36. Sefton B. M., Wickus G. G., Burge B. W. Enzymatic iodination of Sindbis virus proteins. J Virol. 1973 May;11(5):730–735. doi: 10.1128/jvi.11.5.730-735.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Tamkun J. W., DeSimone D. W., Fonda D., Patel R. S., Buck C., Horwitz A. F., Hynes R. O. Structure of integrin, a glycoprotein involved in the transmembrane linkage between fibronectin and actin. Cell. 1986 Jul 18;46(2):271–282. doi: 10.1016/0092-8674(86)90744-0. [DOI] [PubMed] [Google Scholar]
  39. Thiagarajan P., Shapiro S. S., Levine E., DeMarco L., Yalcin A. A monoclonal antibody to human platelet glycoprotein IIIa detects a related protein in cultured human endothelial cells. J Clin Invest. 1985 Mar;75(3):896–901. doi: 10.1172/JCI111789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tonegawa S. Somatic generation of antibody diversity. Nature. 1983 Apr 14;302(5909):575–581. doi: 10.1038/302575a0. [DOI] [PubMed] [Google Scholar]
  41. Woods A., Couchman J. R., Johansson S., Hök M. Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. EMBO J. 1986 Apr;5(4):665–670. doi: 10.1002/j.1460-2075.1986.tb04265.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yamada K. M., Kennedy D. W. Dualistic nature of adhesive protein function: fibronectin and its biologically active peptide fragments can autoinhibit fibronectin function. J Cell Biol. 1984 Jul;99(1 Pt 1):29–36. doi: 10.1083/jcb.99.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zuckerman K. S., Rhodes R. K. The hematopoietic extracellular matrix. Prog Clin Biol Res. 1985;184:257–266. [PubMed] [Google Scholar]

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