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. 1985 Dec;82(23):8153–8157. doi: 10.1073/pnas.82.23.8153

Interleukin 1 can act as a B-cell growth and differentiation factor.

B L Pike, G J Nossal
PMCID: PMC391461  PMID: 3877937

Abstract

Splenic B lymphocytes specifically reactive to the hapten fluorescein (FLU) were prepared from nonimmune adult mice by affinity fractionation on hapten-gelatin. These FLU-specific B cells were cultured as single cells or in small numbers in 10-microliter wells either in the absence of any feeder, filler, or accessory cell or in the presence of 3T3 fibroblasts acting as filler cells. A selected batch of a "T-cell-independent" antigen, FLU-Ficoll, which induces growth and differentiation only in the presence of lymphokines or cytokines acting as B-cell growth and differentiation factors (BGDF), was used as the antigenic stimulus. It was found that murine interleukin 1 prepared by recombinant DNA technology was an effective, although weak, BGDF when acting with antigen on B cells cultured either under filler cell-free conditions or in the presence of 3T3 cells. When the murine interleukin 1 was used in combination with recombinant human interleukin 2, itself a weak but effective BGDF in the system, an additive effect was observed. The results challenge the notion that interleukin 1 is exclusively or even primarily an activating cytokine. This system, in which pure factors are able to act with specific antigen on single hapten-specific B cells, will prove helpful for the further dissection of the respective roles of the various factors that can act on B cells.

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Selected References

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

  1. Booth R. J., Watson J. D. Interleukin 1 induces proliferation in two distinct B cell subpopulations responsive to two different murine B cell growth factors. J Immunol. 1984 Sep;133(3):1346–1349. [PubMed] [Google Scholar]
  2. Corbel C., Melchers F. The synergism of accessory cells and of soluble alpha-factors derived from them in the activation of B cells to proliferation. Immunol Rev. 1984 Apr;78:51–74. doi: 10.1111/j.1600-065x.1984.tb00476.x. [DOI] [PubMed] [Google Scholar]
  3. Gery I., Gershon R. K., Waksman B. H. Potentiation of the T-lymphocyte response to mitogens. I. The responding cell. J Exp Med. 1972 Jul 1;136(1):128–142. doi: 10.1084/jem.136.1.128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Good M. F., Boyd A. W., Nossal G. J. Analysis of true anti-hapten cytotoxic clones in limit dilution microcultures after correction for "anti-self" activity: precursor frequencies, Ly-2 and Thy-1 phenotype, specificity, and statistical methods. J Immunol. 1983 May;130(5):2046–2055. [PubMed] [Google Scholar]
  5. Harada N., Kikuchi Y., Tominaga A., Takaki S., Takatsu K. BCGFII activity on activated B cells of a purified murine T cell-replacing factor (TRF) from a T cell hybridoma (B151K12). J Immunol. 1985 Jun;134(6):3944–3951. [PubMed] [Google Scholar]
  6. Howard M., Nakanishi K., Paul W. E. B cell growth and differentiation factors. Immunol Rev. 1984 Apr;78:185–210. doi: 10.1111/j.1600-065x.1984.tb00482.x. [DOI] [PubMed] [Google Scholar]
  7. Howard M., Paul W. E. Regulation of B-cell growth and differentiation by soluble factors. Annu Rev Immunol. 1983;1:307–333. doi: 10.1146/annurev.iy.01.040183.001515. [DOI] [PubMed] [Google Scholar]
  8. Kishimoto T. Factors affecting B-cell growth and differentiation. Annu Rev Immunol. 1985;3:133–157. doi: 10.1146/annurev.iy.03.040185.001025. [DOI] [PubMed] [Google Scholar]
  9. Kishimoto T., Yoshizaki K., Kimoto M., Okada M., Kuritani T., Kikutani H., Shimizu K., Nakagawa T., Nakagawa N., Miki Y. B cell growth and differentiation factors and mechanism of B cell activation. Immunol Rev. 1984 Apr;78:97–118. doi: 10.1111/j.1600-065x.1984.tb00478.x. [DOI] [PubMed] [Google Scholar]
  10. Larsson E. L., Iscove N. N., Coutinho A. Two distinct factors are required for induction of T-cell growth. Nature. 1980 Feb 14;283(5748):664–666. doi: 10.1038/283664a0. [DOI] [PubMed] [Google Scholar]
  11. Liebson H. J., Marrack P., Kappler J. B cell helper factors. II. Synergy among three helper factors in the response of T cell- and macrophage-depleted B cells. J Immunol. 1982 Oct;129(4):1398–1402. [PubMed] [Google Scholar]
  12. Lomedico P. T., Gubler U., Hellmann C. P., Dukovich M., Giri J. G., Pan Y. C., Collier K., Semionow R., Chua A. O., Mizel S. B. Cloning and expression of murine interleukin-1 cDNA in Escherichia coli. 1984 Nov 29-Dec 5Nature. 312(5993):458–462. doi: 10.1038/312458a0. [DOI] [PubMed] [Google Scholar]
  13. Melchers F., Andersson J. B cell activation: three steps and their variations. Cell. 1984 Jul;37(3):713–720. doi: 10.1016/0092-8674(84)90407-0. [DOI] [PubMed] [Google Scholar]
  14. Mizel S. B., Dukovich M., Rothstein J. Preparation of goat antibodies against interleukin 1: use of an immunoadsorbent to purify interleukin 1. J Immunol. 1983 Oct;131(4):1834–1837. [PubMed] [Google Scholar]
  15. Mizel S. B., Mizel D. Purification to apparent homogeneity of murine interleukin 1. J Immunol. 1981 Mar;126(3):834–837. [PubMed] [Google Scholar]
  16. 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]
  17. Monroe J. G., Cambier J. C. Level of mIa expression on mitogen-stimulated murine B lymphocytes is dependent on position in cell cycle. J Immunol. 1983 Feb;130(2):626–631. [PubMed] [Google Scholar]
  18. Noelle R., Krammer P. H., Ohara J., Uhr J. W., Vitetta E. S. Increased expression of Ia antigens on resting B cells: an additional role for B-cell growth factor. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6149–6153. doi: 10.1073/pnas.81.19.6149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nossal G. J., Pike B. L., Battye F. L. Sequential use of hapten-gelatin fractionation and fluorescence-activated cell sorting in the enrichment of hapten-specific B llymphocytes. Eur J Immunol. 1978 Mar;8(3):151–157. doi: 10.1002/eji.1830080302. [DOI] [PubMed] [Google Scholar]
  20. Nossal G. J., Pike B. L. Single cell studies on the antibody-forming potential of fractionated, hapten-specific B lymphocytes. Immunology. 1976 Feb;30(2):189–202. [PMC free article] [PubMed] [Google Scholar]
  21. Oliver K., Noelle R. J., Uhr J. W., Krammer P. H., Vitetta E. S. B-cell growth factor (B-cell growth factor I or B-cell-stimulating factor, provisional 1) is a differentiation factor for resting B cells and may not induce cell growth. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2465–2467. doi: 10.1073/pnas.82.8.2465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pike B. L., Nossal G. J. A high-efficiency cloning system for single hapten-specific B lymphocytes that is suitable for assay of putative growth and differentiation factors. Proc Natl Acad Sci U S A. 1985 May;82(10):3395–3399. doi: 10.1073/pnas.82.10.3395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pike B. L., Nossal G. J. A reappraisal of "T-independent" antigens. I. Effect of lymphokines on the response of single adult hapten-specific B lymphocytes. J Immunol. 1984 Apr;132(4):1687–1695. [PubMed] [Google Scholar]
  24. Pike B. L., Raubitschek A., Nossal G. J. Human interleukin 2 can promote the growth and differentiation of single hapten-specific B cells in the presence of specific antigen. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7917–7921. doi: 10.1073/pnas.81.24.7917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pike B. L., Vaux D. L., Clark-Lewis I., Schrader J. W., Nossal G. J. Proliferation and differentiation of single hapten-specific B lymphocytes is promoted by T-cell factor(s) distinct from T-cell growth factor. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6350–6354. doi: 10.1073/pnas.79.20.6350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pike B. L., Vaux D. L., Nossal G. J. Single cell studies on hapten-specific B lymphocytes: differential cloning efficiency of cells of various sizes. J Immunol. 1983 Aug;131(2):554–560. [PubMed] [Google Scholar]
  27. Rabin E. M., Ohara J., Paul W. E. B-cell stimulatory factor 1 activates resting B cells. Proc Natl Acad Sci U S A. 1985 May;82(9):2935–2939. doi: 10.1073/pnas.82.9.2935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Roehm N. W., Leibson H. J., Zlotnik A., Kappler J., Marrack P., Cambier J. C. Interleukin-induced increase in Ia expression by normal mouse B cells. J Exp Med. 1984 Sep 1;160(3):679–694. doi: 10.1084/jem.160.3.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rosenberg S. A., Grimm E. A., McGrogan M., Doyle M., Kawasaki E., Koths K., Mark D. F. Biological activity of recombinant human interleukin-2 produced in Escherichia coli. Science. 1984 Mar 30;223(4643):1412–1414. doi: 10.1126/science.6367046. [DOI] [PubMed] [Google Scholar]
  30. Swain S. L., Howard M., Kappler J., Marrack P., Watson J., Booth R., Wetzel G. D., Dutton R. W. Evidence for two distinct classes of murine B cell growth factors with activities in different functional assays. J Exp Med. 1983 Sep 1;158(3):822–835. doi: 10.1084/jem.158.3.822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Swain S. L. Role of BCGFII in the differentiation to antibody secretion normal and tumor B cells. J Immunol. 1985 Jun;134(6):3934–3943. [PubMed] [Google Scholar]
  32. Takatsu K., Tanaka K., Tominaga A., Kumahara Y., Hamaoka T. Antigen-induced T cell-replacing factor (TRF). III. Establishment of T cell hybrid clone continuously producing TRF and functional analysis of released TRF. J Immunol. 1980 Dec;125(6):2646–2653. [PubMed] [Google Scholar]
  33. Vaux D. L., Pike B. L., Nossal G. J. Antibody production by single, hapten-specific B lymphocytes: an antigen-driven cloning system free of filler or accessory cells. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7702–7706. doi: 10.1073/pnas.78.12.7702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wetzel G. D., Swain S. L., Dutton R. W., Kettman J. R. Evidence for two distinct activation states available to B lymphocytes. J Immunol. 1984 Nov;133(5):2327–2332. [PubMed] [Google Scholar]

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