Skip to main content
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1974 Oct 1;140(4):877–894. doi: 10.1084/jem.140.4.877

BINDING OF SOLUBLE IMMUNE COMPLEXES TO HUMAN LYMPHOBLASTOID CELLS

I. Characterization of Receptors for IgG Fc and Complement and Description of the Binding Mechanism

Argyrios N Theofilopoulos 1, Frank J Dixon 1, Viktor A Bokisch 1
PMCID: PMC2139634  PMID: 4139225

Abstract

In the present work we studied the expression of membrane-bound Ig (MBIg) as well as receptors for IgG Fc and complement on nine human lymphoblastoid cell lines. When MBIg and receptors for IgG Fc were compared, four categories of cell lines could be distinguished: (a) cell lines having both MBIg and receptors for IgG Fc, (b) cell lines having MBIg but lacking receptors for IgG Fc, (c) cell lines lacking MBIg but having receptors for IgG Fc, and (d) cell lines lacking both MBIg and receptors for IgG Fc. Two types of receptors for complement could be detected on the cell lines studied, one for C3-C3b and one for C3d. When sensitized red cells carrying C3b or C3d were used for rosette tests, three categories of cell lines could be distinguished: (a) cell lines having receptors for C3b and C3d, (b) cell lines having receptors only for C3d and (c) cell lines lacking both receptors. However, when a more sensitive immunofluorescent method was used instead of the rosette technique, it was found that cell lines unable to form rosettes with EAC1423bhu were able to bind soluble C3 or C3b which indicated the presence of these receptors on the cell surface. Inhibition experiments showed that receptors for C3-C3b and receptors for C3d are distinct and that receptors for C3-C3b and C3d are different from receptors for IgG Fc. A cell line (Raji) without MBIg but with receptors for IgG Fc, C3-C3b, and C3d was selected for use in studying the binding mechanism of soluble immune complexes to cell surface membrane. Aggregated human gamma globulin was used in place of immune complexes. Immune complexes containing complement bind to Raji cells only via receptors for complement, namely receptors for C3-C3b and C3d. Binding of immune complexes containing complement to cells is much greater than that of complexes without complement. Immune complexes bound to cells via receptors for complement can be partially released from the cell surface by addition of normal human serum as well as isolated human C3 or C3b. We postulate that such release is due to competition of immune complex bound C3b and free C3 or C3b for the receptors on Raji cells.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Bentwich Z., Douglas S. D., Siegal F. P., Kunkel H. G. Human lymphocyte-sheep erythrocyte rosette formation: some characteristics of the interaction. Clin Immunol Immunopathol. 1973 Jul;1(4):511–522. doi: 10.1016/0090-1229(73)90007-x. [DOI] [PubMed] [Google Scholar]
  2. Bokisch V. A., Müller-Eberhard H. J., Cochrane C. G. Isolation of a fragment (C3a) of the third component of human complement containing anaphylatoxin and chemotactic activity and description of an anaphylatoxin inactivator of human serum. J Exp Med. 1969 May 1;129(5):1109–1130. doi: 10.1084/jem.129.5.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. CHRISTIAN C. L. Studies of aggregated gamma-globulin. I. Sedimentation, electrophoretic and anticomplementary properties. J Immunol. 1960 Jan;84:112–116. [PubMed] [Google Scholar]
  4. CLARK H. F., SHEPARD C. C. A DIALYSIS TECHNIQUE FOR PREPARING FLUORESCENT ANTIBODY. Virology. 1963 Aug;20:642–644. doi: 10.1016/0042-6822(63)90292-7. [DOI] [PubMed] [Google Scholar]
  5. Dickler H. B., Kunkel H. G. Interaction of aggregated -globulin with B lymphocytes. J Exp Med. 1972 Jul 1;136(1):191–196. doi: 10.1084/jem.136.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dickler H. B., Siegal F. P., Bentwich Z. H., Kunkel H. G. Lymphocyte binding of aggregated IgG and surface Ig staining in chronic lymphocytic leukaemia. Clin Exp Immunol. 1973 May;14(1):97–106. [PMC free article] [PubMed] [Google Scholar]
  7. Eden A., Bianco C., Nussenzweig Mechanism of binding of soluble immune complexes to lymphocytes. Cell Immunol. 1973 Jun;7(3):459–473. doi: 10.1016/0008-8749(73)90210-4. [DOI] [PubMed] [Google Scholar]
  8. Eden A., Miller G. W., Nussenzweig V. Human lymphocytes bear membrane receptors for C3b and C3d. J Clin Invest. 1973 Dec;52(12):3239–3242. doi: 10.1172/JCI107525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Finegold I., Fahey J. L., Granger H. Synthesis of immunoglobulins by human cell lines in tissue culture. J Immunol. 1967 Nov;99(5):839–848. [PubMed] [Google Scholar]
  10. Glade P. R., Hirschhorn K. Products of lymphoid cells in continuous culture. Am J Pathol. 1970 Sep;60(3):483–494. [PMC free article] [PubMed] [Google Scholar]
  11. Huber H., Polley M. J., Linscott W. D., Fudenberg H. H., Müller-Eberhard H. J. Human monocytes: distinct receptor sites for the third component of complement and for immunoglobulin G. Science. 1968 Dec 13;162(3859):1281–1283. doi: 10.1126/science.162.3859.1281. [DOI] [PubMed] [Google Scholar]
  12. ISHIZAKA K. Gamma globulin and molecular mechanisms in hypersensitivity reactions. Prog Allergy. 1963;7:32–106. [PubMed] [Google Scholar]
  13. Jondal M., Holm G., Wigzell H. Surface markers on human T and B lymphocytes. I. A large population of lymphocytes forming nonimmune rosettes with sheep red blood cells. J Exp Med. 1972 Aug 1;136(2):207–215. doi: 10.1084/jem.136.2.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Klein E., Klein G., Nadkarni J. S., Nadkarni J. J., Wigzell H., Clifford P. Surface IgM-kappa specificity on a Burkitt lymphoma cell in vivo and in derived culture lines. Cancer Res. 1968 Jul;28(7):1300–1310. [PubMed] [Google Scholar]
  15. Lay W. H., Nussenzweig V. Receptors for complement of leukocytes. J Exp Med. 1968 Nov 1;128(5):991–1009. doi: 10.1084/jem.128.5.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lerner R. A., Hodge L. D. Gene expression in synchronized lymphocytes: studies on the control of synthesis of immunoglobulin polypeptides. J Cell Physiol. 1971 Apr;77(2):265–276. doi: 10.1002/jcp.1040770215. [DOI] [PubMed] [Google Scholar]
  17. Levy J. A., Virolainen M., Defendi V. Human lymphoblastoid lines from lymph node and spleen. Cancer. 1968 Sep;22(3):517–524. doi: 10.1002/1097-0142(196809)22:3<517::aid-cncr2820220305>3.0.co;2-a. [DOI] [PubMed] [Google Scholar]
  18. MARDINEY M. R., Jr, MUELLER-EBERHARD H. J. MOUSE BETA-1C-GLOBULIN: PRODUCTION OF ANTISERUM AND CHARACTERIZATION IN THE COMPLEMENT REACTION. J Immunol. 1965 Jun;94:877–882. [PubMed] [Google Scholar]
  19. McConahey P. J., Dixon F. J. A method of trace iodination of proteins for immunologic studies. Int Arch Allergy Appl Immunol. 1966;29(2):185–189. doi: 10.1159/000229699. [DOI] [PubMed] [Google Scholar]
  20. Miller G. W., Saluk P. H., Nussenzweig V. Complement-dependent release of immune complexes from the lymphocyte membrane. J Exp Med. 1973 Sep 1;138(3):495–507. doi: 10.1084/jem.138.3.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. NILSSON U. R., MUELLER-EBERHARD H. J. ISOLATION OF BETA IF-GLOBULIN FROM HUMAN SERUM AND ITS CHARACTERIZATION AS THE FIFTH COMPONENT OF COMPLEMENT. J Exp Med. 1965 Aug 1;122:277–298. doi: 10.1084/jem.122.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nilsson U. R., Müller-Eberhard H. J. Deficiency of the fifth component of complement in mice with an inherited complement defect. J Exp Med. 1967 Jan 1;125(1):1–16. doi: 10.1084/jem.125.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. PULVERTAFT J. V. A STUDY OF MALIGNANT TUMOURS IN NIGERIA BY SHORT-TERM TISSUE CULTURE. J Clin Pathol. 1965 May;18:261–273. doi: 10.1136/jcp.18.3.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pincus S., Bianco C., Nussenzweig V. Increased proportion of complement-receptor lymphocytes in the peripheral blood of patients with chronic lymphocytic leukemia. Blood. 1972 Sep;40(3):303–310. [PubMed] [Google Scholar]
  25. Ross G. D., Polley M. J., Rabellino E. M., Grey H. M. Two different complement receptors on human lymphocytes. One specific for C3b and one specific for C3b inactivator-cleaved C3b. J Exp Med. 1973 Oct 1;138(4):798–811. doi: 10.1084/jem.138.4.798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ross G. D., Rabellino E. M., Polley M. J., Grey H. M. Combined studies of complement receptor and surface immunoglobulin-bearing cells and sheep erythrocyte rosette-forming cells in normal and leukemic human lymphocytes. J Clin Invest. 1973 Feb;52(2):377–385. doi: 10.1172/JCI107194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rother K., Rother U., Müller-Eberhard H. J., Nilsson J. R. Deficiency of the sixth component of complement in rabbits with an inherited complement defect. J Exp Med. 1966 Oct 1;124(4):773–785. doi: 10.1084/jem.124.4.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ruddy S., Austen K. F. C3b inactivator of man. II. Fragments produced by C3b inactivator cleavage of cell-bound or fluid phase C3b. J Immunol. 1971 Sep;107(3):742–750. [PubMed] [Google Scholar]
  29. Schiff R. I., Buckley R. H., Gilbertsen R. B., Metzgar R. S. Membrane receptors and in vitro responsiveness of lymphocytes in human immunodeficiency. J Immunol. 1974 Jan;112(1):376–386. [PubMed] [Google Scholar]
  30. Shevach E. M., Herberman R., Frank M. M., Green I. Receptors for complement and immunoglobulin on human leukemic cells and human lymphoblastoid cell lines. J Clin Invest. 1972 Aug;51(8):1933–1938. doi: 10.1172/JCI106999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Theofilopoulos A. N., Bokisch V. A., Dixon F. J. Receptor for soluble C3 and C3b on human lymphoblastoid (RAJI) cells. Properties and biologocal significance. J Exp Med. 1974 Mar 1;139(3):696–711. doi: 10.1084/jem.139.3.696. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES