Skip to main content
Immunology logoLink to Immunology
. 1984 Aug;52(4):711–719.

Primary in vitro plaque-forming cell response to DAGG-Ficoll: LPS-induced enhancement mediated by interleukin-1.

J L Curtis, A A Nordin
PMCID: PMC1454635  PMID: 6378771

Abstract

The specific primary in vitro plaque-forming cell (PFC) response of C57B1/6 nu/nu spleen cells to the Type 2 T-independent (TI-2) antigen DAGG-Ficoll was analysed in the absence of T cell help in a serum-free medium. Lipopolysaccharide (LPS) enhancement of the antigen-specific response was shown to be mediated by soluble factors contained in the supernatants of LPS-induced bone marrow-derived macrophages. The activity of these supernatants was not associated with residual LPS, since the antigen-specific response of B cells from mice genetically deficient in LPS receptors was equally well enhanced. The activity of these supernatants was associated with interleukin-1 (IL-1) and partially purified IL-1 prepared from P388D1 cells also enhanced the primary in vitro response to DAGG-Ficoll. Limiting dilution analysis experiments showed that only in the presence of exogenously added IL-1 could a single cell type, presumably the B cells, be shown to be limiting.

Full text

PDF
711

Selected References

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

  1. Beattie G. M., Baird S. M., Lipsick J. S., Lannom R. A., Kaplan N. O. Induction of T- and B-lymphocyte responses in antigenically stimulated athymic mice. Cancer Res. 1981 Jun;41(6):2322–2327. [PubMed] [Google Scholar]
  2. Beattie G., Baird S., Lannom R., Slimmer S., Jensen F. C., Kaplan N. O. Induction of lymphoma in athymic mice: a model for study of the human disease. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4971–4974. doi: 10.1073/pnas.77.8.4971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boswell H. S., Ahmed A., Scher I., Singer A. Role of accessory cells in B cell activation. II. The interaction of B cells with accessory cells results in the exclusive activation of an Lyb5+ B cell subpopulation. J Immunol. 1980 Sep;125(3):1340–1348. [PubMed] [Google Scholar]
  4. Cosenza H., Quintáns J., Lefkovits I. Antibody response to phosphorylcholine in vitro. I. Studies on the frequency of precursor cells, average clone size and cellular cooperation. Eur J Immunol. 1975 May;5(5):343–349. doi: 10.1002/eji.1830050510. [DOI] [PubMed] [Google Scholar]
  5. Coutinho A., Möller G. Mitogenic properties of the thymus-independent antigen pneumococcal polysaccharide S3. Eur J Immunol. 1973 Oct;3(10):608–613. doi: 10.1002/eji.1830031003. [DOI] [PubMed] [Google Scholar]
  6. Dutton R. W. Separate signals for the initiation of proliferation and differentiation in the b cell response to antigen. Transplant Rev. 1975;23:66–77. doi: 10.1111/j.1600-065x.1975.tb00149.x. [DOI] [PubMed] [Google Scholar]
  7. Farrar J. J., Hilfiker M. L. Antigen-nonspecific helper factors in the antibody response. Fed Proc. 1982 Feb;41(2):263–268. [PubMed] [Google Scholar]
  8. Goding J. W. The chromic chloride method of coupling antigens to erythrocytes: definition of some important parameters. J Immunol Methods. 1976;10(1):61–66. doi: 10.1016/0022-1759(76)90007-7. [DOI] [PubMed] [Google Scholar]
  9. Hammerling U., Chin A. F., Abbott J., Scheid M. P. The ontogeny of murine B lymphocytes. I. Induction of phenotypic conversion of Ia-to Ia+ lymphocytes. J Immunol. 1975 Nov;115(5):1425–1431. [PubMed] [Google Scholar]
  10. Havell E. A., Spitalny G. L. The induction and characterization of interferon from pure cultures of murine macrophages. Ann N Y Acad Sci. 1980;350:413–421. doi: 10.1111/j.1749-6632.1980.tb20643.x. [DOI] [PubMed] [Google Scholar]
  11. Hoffmann M. K., Koenig S., Mittler R. S., Oettgen H. F., Ralph P., Galanos C., Hammerling U. Macrophage factor controlling differentiation of B cells. J Immunol. 1979 Feb;122(2):497–502. [PubMed] [Google Scholar]
  12. Hoffmann M. K. Macrophages and T cells control distinct phases of B cell differentiation in the humoral immune response in vitro. J Immunol. 1980 Nov;125(5):2076–2081. [PubMed] [Google Scholar]
  13. Howard M., Mizel S. B., Lachman L., Ansel J., Johnson B., Paul W. E. Role of interleukin 1 in anti-immunoglobulin-induced B cell proliferation. J Exp Med. 1983 May 1;157(5):1529–1543. doi: 10.1084/jem.157.5.1529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hämmerling U., Chin A. F., Abbott J. Ontogeny of murine B lymphocytes: sequence of B-cell differentiation from surface-immunoglobulin-negative precursors to plasma cells. Proc Natl Acad Sci U S A. 1976 Jun;73(6):2008–2012. doi: 10.1073/pnas.73.6.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Inman J. K., Merchant B., Claflin L., Tacey S. E. Coupling of large haptens to proteins and cell surfaces: preparation of stable, optimally sensitized erythrocytes for hapten-specific, hemolytic plaque assays. Immunochemistry. 1973 Mar;10(3):165–174. doi: 10.1016/0019-2791(73)90005-0. [DOI] [PubMed] [Google Scholar]
  16. Inman J. K. Thymus-independent antigens: the preparation of covalent, hapten-ficoll conjugates. J Immunol. 1975 Feb;114(2 Pt 1):704–709. [PubMed] [Google Scholar]
  17. Iscove N. N., Melchers F. Complete replacement of serum by albumin, transferrin, and soybean lipid in cultures of lipopolysaccharide-reactive B lymphocytes. J Exp Med. 1978 Mar 1;147(3):923–933. doi: 10.1084/jem.147.3.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jerne N. K., Nordin A. A. Plaque Formation in Agar by Single Antibody-Producing Cells. Science. 1963 Apr 26;140(3565):405–405. doi: 10.1126/science.140.3565.405. [DOI] [PubMed] [Google Scholar]
  19. Kearney J. F., Cooper M. D., Klein J., Abney E. R., Parkhouse R. M., Lawton A. R. Ontogeny of Ia and IgD on IgM-bearing B lymphocytes in mice. J Exp Med. 1977 Jul 1;146(1):297–301. doi: 10.1084/jem.146.1.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kettman J., Soederberg A., Lefkovits I. Heterogeneity of B cell clones: immunoglobulin-secreting subsets. Cell Immunol. 1982 Jan 1;66(1):70–77. doi: 10.1016/0008-8749(82)90158-7. [DOI] [PubMed] [Google Scholar]
  21. Kettman J., Wetzel M. Antibody synthesis in vitro, a marker of B cell differentiation. J Immunol Methods. 1980;39(3):203–222. doi: 10.1016/0022-1759(80)90056-3. [DOI] [PubMed] [Google Scholar]
  22. Kirkland T. N., Sieckmann D. G., Longo D. L., Mosier D. E. Cellular requirements for antigen presentation in the induction of a thymus-independent antibody response in vitro. J Immunol. 1980 Apr;124(4):1721–1726. [PubMed] [Google Scholar]
  23. Lefkovits I. Induction of antibody-forming cell clones in microcultures. Eur J Immunol. 1972 Aug;2(4):360–366. doi: 10.1002/eji.1830020412. [DOI] [PubMed] [Google Scholar]
  24. McGhee J. R., Farrar J. J., Michalek S. M., Mergenhagen S. E., Rosenstreich D. L. Cellular requirements for lipopolysaccharide adjuvanticity. A role for both T lymphocytes and macrophages for in vitro responses to particulate antigens. J Exp Med. 1979 Apr 1;149(4):793–807. doi: 10.1084/jem.149.4.793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Melchers F., Andersson J., Lernhardt W., Schreier M. H. Roles of surface-bound immunoglobulin molecules in regulating the replication and maturation to immunoglobulin secretion of B lymphocytes. Immunol Rev. 1980;52:89–114. doi: 10.1111/j.1600-065x.1980.tb00332.x. [DOI] [PubMed] [Google Scholar]
  26. Mizel S. B., Mizel D. Purification to apparent homogeneity of murine interleukin 1. J Immunol. 1981 Mar;126(3):834–837. [PubMed] [Google Scholar]
  27. Mizel S. B., Oppenheim J. J., Rosenstreich D. L. Characterization of lymphocyte-activating factor (LAF) produced by the macrophage cell line, P388D1. I. Enhancement of LAF production by activated T lymphocytes. J Immunol. 1978 May;120(5):1497–1503. [PubMed] [Google Scholar]
  28. Mizel S. B., Rosenstreich D. L., Oppenheim J. J. Phorbol myristic acetate stimulates LAF production by the macrophage cell line, P388D. Cell Immunol. 1978 Sep 15;40(1):230–235. doi: 10.1016/0008-8749(78)90330-1. [DOI] [PubMed] [Google Scholar]
  29. Mizel S. B. Studies on the purification and structure-functional relationships of murine lymphocyte activating factor (Interleukin 1). Mol Immunol. 1980 May;17(5):571–577. doi: 10.1016/0161-5890(80)90155-8. [DOI] [PubMed] [Google Scholar]
  30. Mizuguchi J., Kakiuchi T., Nariuchi H., Matuhasi T. Different effect of LPS-induced macrophage factor on antibody responses to TI-1 and TI-2 antigens. Immunology. 1982 Sep;47(1):183–192. [PMC free article] [PubMed] [Google Scholar]
  31. Mond J. J., Mongini P. K., Sieckmann D., Paul W. E. Role of T lymphocytes in the response to TNP-AECM-Ficoll. J Immunol. 1980 Sep;125(3):1066–1070. [PubMed] [Google Scholar]
  32. Mond J. J., Sehgal E., Sachs D. H., Paul W. E. Expression of Ia antigen on adult and neonatal B lymphocytes responsive to thymus-independent antigens. J Immunol. 1979 Oct;123(4):1619–1623. [PubMed] [Google Scholar]
  33. Morrison D. C., Betz S. J., Jacobs D. M. Isolation of a lipid A bound polypeptide responsible for "LPS-initiated" mitogenesis of C3H/HeJ spleen cells. J Exp Med. 1976 Sep 1;144(3):840–846. doi: 10.1084/jem.144.3.840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Möller G., Coutinho A., Persson U. Mechanism of b-lymphocyte activation: failure to obtain evidence of a direct role of the Ig receptors in the triggering process. Scand J Immunol. 1975;4(1):37–52. doi: 10.1111/j.1365-3083.1975.tb02598.x. [DOI] [PubMed] [Google Scholar]
  35. Möller G. One non-specific signal triggers b lymphocytes. Transplant Rev. 1975;23:126–137. [PubMed] [Google Scholar]
  36. Nariuchi H., Kakiuchi T. Antibody responses to various T-independent antigens of B cells with or without C3 receptors and adherent cell requirement for these responses. J Immunol. 1982 Jan;128(1):161–167. [PubMed] [Google Scholar]
  37. Nathan C. F., Murray H. W., Cohn Z. A. The macrophage as an effector cell. N Engl J Med. 1980 Sep 11;303(11):622–626. doi: 10.1056/NEJM198009113031106. [DOI] [PubMed] [Google Scholar]
  38. Nordin A. A., Schreier M. H. T cell control of the antibody response to the T-independent antigen, DAGG-Ficoll. J Immunol. 1982 Aug;129(2):557–562. [PubMed] [Google Scholar]
  39. Nordin A. A. The in vitro immune response to a T-independent antigen. I. The effect of macrophages and 2-mercaptoethanol. Eur J Immunol. 1978 Nov;8(11):776–781. doi: 10.1002/eji.1830081105. [DOI] [PubMed] [Google Scholar]
  40. Press J. L., Klinman N. R., McDevitt H. O. Expression of Ia antigens on hapten-specific B cells. I. Delineation of B-cell subpopulations. J Exp Med. 1976 Aug 1;144(2):414–427. doi: 10.1084/jem.144.2.414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Schrader J. W. Mechanism of activation of the bone marrow-derived lymphocyte. 3. A distinction between a macrophage-produced triggering signal and the amplifying effect on triggered B lymphocytes of allogeneic interactions. J Exp Med. 1973 Dec 1;138(6):1466–1480. doi: 10.1084/jem.138.6.1466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schreier M. H. B-cell precursors specific to sheep erythrocytes. Estimation of frequency in a specific helper assay. J Exp Med. 1978 Dec 1;148(6):1612–1619. doi: 10.1084/jem.148.6.1612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sultzer B. M., Goodman G. W. Endotoxin protein: a B-cell mitogen and polyclonal activator of C3H/HeJ lymphocytes. J Exp Med. 1976 Sep 1;144(3):821–827. doi: 10.1084/jem.144.3.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Watson J., Riblet R. Genetic control of responses to bacterial lipopolysaccharides in mice. I. Evidence for a single gene that influences mitogenic and immunogenic respones to lipopolysaccharides. J Exp Med. 1974 Nov 1;140(5):1147–1161. doi: 10.1084/jem.140.5.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wetzel G. D., Kettman J. R. Activation of murine B lymphocytes. III. Stimulation of B lymphocyte clonal growth with lipopolysaccharide and dextran sulfate. J Immunol. 1981 Feb;126(2):723–728. [PubMed] [Google Scholar]
  46. Wood D. D., Cameron P. M., Poe M. T., Morris C. A. Resolution of a factor that enhances the antibody response of T cell-depleted murine splenocytes from several other monocyte products. Cell Immunol. 1976 Jan;21(1):88–96. doi: 10.1016/0008-8749(76)90330-0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES