Skip to main content
PMC home page
Immunology logoLink to Immunology
. 1989 Jul;67(3):314–320.

Signal delivery by physical interaction and soluble factors from accessory cells in the induction of receptor-mediated T-cell proliferation. Synergistic effect of BSF-2/IL-6 and IL-1.

K Kawakami 1, K Kakimoto 1, T Shinbori 1, K Onoue 1
PMCID: PMC1385346  PMID: 2503436

Abstract

Our recent study revealed that soluble factors derived from accessory cells (AC; monocytes) and physical interaction with T cells of the accessory cells are both required for the induction of the proliferation of human peripheral blood T cells by anti-CD3 antibody coupled on latex beads. The accessory cell-derived soluble factor could be replaced by IL-1 and IL-6, and the role of live macrophages for physical interaction with T cells was found to be replaceable with paraformaldehyde(PFA)-fixed macrophages, provided the macrophages were pretreated with interferon-gamma (IFN-gamma) before fixation. Quantitative analysis in the present study revealed that IL-1 and IL-6 act synergistically to induce T-cell proliferation in the above system but either one of the factors alone reveals only a marginal or weak activity. Furthermore, it was shown that the potentiating activity of the culture supernatants of monocytes was substantially inhibited by anti-IL-6 antibody. Taken together with our previous results that anti-IL-1 serum strongly inhibited the potentiating activity of the culture supernatant, these results indicate that the main responsible molecules in the culture supernatant are IL-1 and IL-6, although a presence of other effective factors is not excluded. The anti-CD3-induced thymidine uptake by T cells in the presence of IL-1 and IL-6 was significantly inhibited by anti-Tac antibody, suggesting that the proliferation of T cells in this system is mostly mediated by a IL-2-dependent pathway. Our study further showed that accessory cells seem to acquire cell surface properties necessary for the effective interaction with T cells during 6-24 hr of culture with IFN-gamma. Presumably, a certain molecule(s) required for the interaction is induced on the cell surface of the AC by IFN-gamma.

Full text

PDF
320

Selected References

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

  1. Aarden L. A., De Groot E. R., Schaap O. L., Lansdorp P. M. Production of hybridoma growth factor by human monocytes. Eur J Immunol. 1987 Oct;17(10):1411–1416. doi: 10.1002/eji.1830171004. [DOI] [PubMed] [Google Scholar]
  2. Bekoff M., Kubo R., Grey H. M. Activation requirements for normal T cells: accessory cell-dependent and -independent stimulation by anti-receptor antibodies. J Immunol. 1986 Sep 1;137(5):1411–1419. [PubMed] [Google Scholar]
  3. Bernabeu C., Carrera A. C., De Landázuri M. O., Sánchez-Madrid F. Interaction between the CD45 antigen and phytohemagglutinin. Inhibitory effect on the lectin-induced T cell proliferation by anti-CD45 monoclonal antibody. Eur J Immunol. 1987 Oct;17(10):1461–1466. doi: 10.1002/eji.1830171012. [DOI] [PubMed] [Google Scholar]
  4. Brakenhoff J. P., de Groot E. R., Evers R. F., Pannekoek H., Aarden L. A. Molecular cloning and expression of hybridoma growth factor in Escherichia coli. J Immunol. 1987 Dec 15;139(12):4116–4121. [PubMed] [Google Scholar]
  5. Fujimoto K., Yamamoto Y., Ohmura T., Kawakami K., Onoue K. Dissection of the role of macrophages in triggering T lymphocytes for interleukin 2 production by monoclonal antibody OKT3. Microbiol Immunol. 1986;30(6):561–572. doi: 10.1111/j.1348-0421.1986.tb02982.x. [DOI] [PubMed] [Google Scholar]
  6. Garman R. D., Jacobs K. A., Clark S. C., Raulet D. H. B-cell-stimulatory factor 2 (beta 2 interferon) functions as a second signal for interleukin 2 production by mature murine T cells. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7629–7633. doi: 10.1073/pnas.84.21.7629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Garman R. D., Raulet D. H. Characterization of a novel murine T cell-activating factor. J Immunol. 1987 Feb 15;138(4):1121–1129. [PubMed] [Google Scholar]
  8. Gauldie J., Richards C., Harnish D., Lansdorp P., Baumann H. Interferon beta 2/B-cell stimulatory factor type 2 shares identity with monocyte-derived hepatocyte-stimulating factor and regulates the major acute phase protein response in liver cells. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7251–7255. doi: 10.1073/pnas.84.20.7251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hirano T., Matsuda T., Hosoi K., Okano A., Matsui H., Kishimoto T. Absence of antiviral activity in recombinant B cell stimulatory factor 2 (BSF-2). Immunol Lett. 1988 Jan;17(1):41–45. doi: 10.1016/0165-2478(88)90099-5. [DOI] [PubMed] [Google Scholar]
  10. Hirano T., Taga T., Nakano N., Yasukawa K., Kashiwamura S., Shimizu K., Nakajima K., Pyun K. H., Kishimoto T. Purification to homogeneity and characterization of human B-cell differentiation factor (BCDF or BSFp-2). Proc Natl Acad Sci U S A. 1985 Aug;82(16):5490–5494. doi: 10.1073/pnas.82.16.5490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Houssiau F. A., Coulie P. G., Olive D., Van Snick J. Synergistic activation of human T cells by interleukin 1 and interleukin 6. Eur J Immunol. 1988 Apr;18(4):653–656. doi: 10.1002/eji.1830180427. [DOI] [PubMed] [Google Scholar]
  12. Kawakami K., Yamamoto Y., Kakimoto K., Onoue K. Requirement for delivery of signals by physical interaction and soluble factors from accessory cells in the induction of receptor-mediated T cell proliferation. Effectiveness of IFN-gamma modulation of accessory cells for physical interaction with T cells. J Immunol. 1989 Mar 15;142(6):1818–1825. [PubMed] [Google Scholar]
  13. Kaye J., Gillis S., Mizel S. B., Shevach E. M., Malek T. R., Dinarello C. A., Lachman L. B., Janeway C. A., Jr Growth of a cloned helper T cell line induced by a monoclonal antibody specific for the antigen receptor: interleukin 1 is required for the expression of receptors for interleukin 2. J Immunol. 1984 Sep;133(3):1339–1345. [PubMed] [Google Scholar]
  14. Koide S. L., Inaba K., Steinman R. M. Interleukin 1 enhances T-dependent immune responses by amplifying the function of dendritic cells. J Exp Med. 1987 Feb 1;165(2):515–530. doi: 10.1084/jem.165.2.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Laing T. J., Weiss A. Evidence for IL-2 independent proliferation in human T cells. J Immunol. 1988 Feb 15;140(4):1056–1062. [PubMed] [Google Scholar]
  16. Lotz M., Jirik F., Kabouridis P., Tsoukas C., Hirano T., Kishimoto T., Carson D. A. B cell stimulating factor 2/interleukin 6 is a costimulant for human thymocytes and T lymphocytes. J Exp Med. 1988 Mar 1;167(3):1253–1258. doi: 10.1084/jem.167.3.1253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Malek T. R., Schmidt J. A., Shevach E. M. The murine IL 2 receptor. III. Cellular requirements for the induction of IL 2 receptor expression on T cell subpopulations. J Immunol. 1985 Apr;134(4):2405–2413. [PubMed] [Google Scholar]
  18. Meuer S. C., Hussey R. E., Cantrell D. A., Hodgdon J. C., Schlossman S. F., Smith K. A., Reinherz E. L. Triggering of the T3-Ti antigen-receptor complex results in clonal T-cell proliferation through an interleukin 2-dependent autocrine pathway. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1509–1513. doi: 10.1073/pnas.81.5.1509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Meuer S. C., Meyer zum Büschenfelde K. H. T cell receptor triggering induces responsiveness to interleukin 1 and interleukin 2 but does not lead to T cell proliferation. J Immunol. 1986 Jun 1;136(11):4106–4112. [PubMed] [Google Scholar]
  20. Moldwin R. L., Lancki D. W., Herold K. C., Fitch F. W. An antigen receptor-driven, interleukin 2-independent pathway for proliferation of murine cytolytic T lymphocyte clones. J Exp Med. 1986 Jun 1;163(6):1566–1582. doi: 10.1084/jem.163.6.1566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. O'Flynn K., Krensky A. M., Beverley P. C., Burakoff S. J., Linch D. C. Phytohaemagglutinin activation of T cells through the sheep red blood cell receptor. Nature. 1985 Feb 21;313(6004):686–687. doi: 10.1038/313686a0. [DOI] [PubMed] [Google Scholar]
  22. Roska A. K., Lipsky P. E. Dissection of the functions of antigen-presenting cells in the induction of T cell activation. J Immunol. 1985 Nov;135(5):2953–2961. [PubMed] [Google Scholar]
  23. Scala G., Oppenheim J. J. Antigen presentation by human monocytes: evidence for stimulant processing and requirement for interleukin 1. J Immunol. 1983 Sep;131(3):1160–1166. [PubMed] [Google Scholar]
  24. Sehgal P. B., May L. T., Tamm I., Vilcek J. Human beta 2 interferon and B-cell differentiation factor BSF-2 are identical. Science. 1987 Feb 13;235(4790):731–732. doi: 10.1126/science.3492764. [DOI] [PubMed] [Google Scholar]
  25. Sitkovsky M. V., Pasternack M. S., Lugo J. P., Klein J. R., Eisen H. N. Isolation and partial characterization of concanavalin A receptors on cloned cytotoxic T lymphocytes. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1519–1523. doi: 10.1073/pnas.81.5.1519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sundström C., Nilsson K. Establishment and characterization of a human histiocytic lymphoma cell line (U-937). Int J Cancer. 1976 May 15;17(5):565–577. doi: 10.1002/ijc.2910170504. [DOI] [PubMed] [Google Scholar]
  27. Teranishi T., Hirano T., Arima N., Onoue K. Human helper T cell factor(s) (ThF). II. Induction of IgG production in B lymphoblastoid cell lines and identification of T cell-replacing factor- (TRF) like factor(s). J Immunol. 1982 Apr;128(4):1903–1908. [PubMed] [Google Scholar]
  28. Thiele D. L., Kurosaka M., Lipsky P. E. Phenotype of the accessory cell necessary for mitogen-stimulated T and B cell responses in human peripheral blood: delineation by its sensitivity to the lysosomotropic agent, L-leucine methyl ester. J Immunol. 1983 Nov;131(5):2282–2290. [PubMed] [Google Scholar]
  29. Thiele D. L., Lipsky P. E. The immunosuppressive activity of L-leucyl-L-leucine methyl ester: selective ablation of cytotoxic lymphocytes and monocytes. J Immunol. 1986 Feb 1;136(3):1038–1048. [PubMed] [Google Scholar]
  30. Tosato G., Pike S. E. Interferon-beta 2/interleukin 6 is a co-stimulant for human T lymphocytes. J Immunol. 1988 Sep 1;141(5):1556–1562. [PubMed] [Google Scholar]
  31. Uchiyama T., Broder S., Waldmann T. A. A monoclonal antibody (anti-Tac) reactive with activated and functionally mature human T cells. I. Production of anti-Tac monoclonal antibody and distribution of Tac (+) cells. J Immunol. 1981 Apr;126(4):1393–1397. [PubMed] [Google Scholar]
  32. Williams J. M., Deloria D., Hansen J. A., Dinarello C. A., Loertscher R., Shapiro H. M., Strom T. B. The events of primary T cell activation can be staged by use of Sepharose-bound anti-T3 (64.1) monoclonal antibody and purified interleukin 1. J Immunol. 1985 Oct;135(4):2249–2255. [PubMed] [Google Scholar]
  33. Wong G. G., Clark S. C. Multiple actions of interleukin 6 within a cytokine network. Immunol Today. 1988 May;9(5):137–139. doi: 10.1016/0167-5699(88)91200-5. [DOI] [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES