Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 Aug;84(15):5399–5403. doi: 10.1073/pnas.84.15.5399

T-cell-replacing factor (interleukin 5) induces expression of interleukin 2 receptors on murine splenic B cells.

M S Loughnan, K Takatsu, N Harada, G J Nossal
PMCID: PMC298863  PMID: 3110787

Abstract

Small, resting B lymphocytes express few, if any, interleukin 2 (IL-2) receptors, but activated B cells may express such receptors. This paper examines the requirements for receptor expression. Normal murine splenocyte populations were enriched for B cells and cultured at relatively low density. IL-2 receptor expression was studied by measuring the binding of the anti-IL-2 receptor monoclonal antibody PC61. Lymphoblasts arising through stimulation by Escherichia coli lipopolysaccharide failed to express IL-2 receptors. B cells cultured with conditioned medium from concanavalin A-stimulated EL4 thymoma cells, with or without LPS, displayed IL-2 receptors. This bioactivity of EL4 conditioned medium could not be replaced by any concentration of B-cell-stimulatory factor 1 (IL-4), IL-1, IL-2, or IL-3 tested. However, the recently cloned lymphokine T-cell-replacing factor (IL-5) was a potent inducer of IL-2 receptor expression, as was the probably identical material known as eosinophil differentiation factor. The receptors so induced appeared to be functional, as receptor-expressing (but not control) lymphoblasts, responded to IL-2 by proliferation, indicative of high-affinity-receptor expression.

Full text

PDF
5399

Images in this article

Selected References

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

  1. Armitage R. J., Cawley J. C. Normal and certain leukaemic B cells express IL-2 receptors without in vitro activation. Clin Exp Immunol. 1986 Feb;63(2):298–302. [PMC free article] [PubMed] [Google Scholar]
  2. Azuma C., Tanabe T., Konishi M., Kinashi T., Noma T., Matsuda F., Yaoita Y., Takatsu K., Hammarström L., Smith C. I. Cloning of cDNA for human T-cell replacing factor (interleukin-5) and comparison with the murine homologue. Nucleic Acids Res. 1986 Nov 25;14(22):9149–9158. doi: 10.1093/nar/14.22.9149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Birchenall-Sparks M. C., Farrar W. L., Rennick D., Kilian P. L., Ruscetti F. W. Regulation of expression of the interleukin-2 receptor on hematopoietic cells by interleukin-3. Science. 1986 Jul 25;233(4762):455–458. doi: 10.1126/science.3088729. [DOI] [PubMed] [Google Scholar]
  4. Burgess A. W., Camakaris J., Metcalf D. Purification and properties of colony-stimulating factor from mouse lung-conditioned medium. J Biol Chem. 1977 Mar 25;252(6):1998–2003. [PubMed] [Google Scholar]
  5. Ceredig R., Lowenthal J. W., Nabholz M., MacDonald H. R. Expression of interleukin-2 receptors as a differentiation marker on intrathymic stem cells. Nature. 1985 Mar 7;314(6006):98–100. doi: 10.1038/314098a0. [DOI] [PubMed] [Google Scholar]
  6. Clark-Lewis I., Kent S. B., Schrader J. W. Purification to apparent homogeneity of a factor stimulating the growth of multiple lineages of hemopoietic cells. J Biol Chem. 1984 Jun 25;259(12):7488–7494. [PubMed] [Google Scholar]
  7. Gillis S., Ferm M. M., Ou W., Smith K. A. T cell growth factor: parameters of production and a quantitative microassay for activity. J Immunol. 1978 Jun;120(6):2027–2032. [PubMed] [Google Scholar]
  8. Howard M., Farrar J., Hilfiker M., Johnson B., Takatsu K., Hamaoka T., Paul W. E. Identification of a T cell-derived b cell growth factor distinct from interleukin 2. J Exp Med. 1982 Mar 1;155(3):914–923. doi: 10.1084/jem.155.3.914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kinashi T., Harada N., Severinson E., Tanabe T., Sideras P., Konishi M., Azuma C., Tominaga A., Bergstedt-Lindqvist S., Takahashi M. Cloning of complementary DNA encoding T-cell replacing factor and identity with B-cell growth factor II. Nature. 1986 Nov 6;324(6092):70–73. doi: 10.1038/324070a0. [DOI] [PubMed] [Google Scholar]
  10. Korsmeyer S. J., Greene W. C., Cossman J., Hsu S. M., Jensen J. P., Neckers L. M., Marshall S. L., Bakhshi A., Depper J. M., Leonard W. J. Rearrangement and expression of immunoglobulin genes and expression of Tac antigen in hairy cell leukemia. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4522–4526. doi: 10.1073/pnas.80.14.4522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Leanderson T., Julius M. H. Mouse B cells do not proliferate in human interleukin 2. Eur J Immunol. 1986 Feb;16(2):182–187. doi: 10.1002/eji.1830160213. [DOI] [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. Lowenthal J. W., Zubler R. H., Nabholz M., MacDonald H. R. Similarities between interleukin-2 receptor number and affinity on activated B and T lymphocytes. Nature. 1985 Jun 20;315(6021):669–672. doi: 10.1038/315669a0. [DOI] [PubMed] [Google Scholar]
  14. Nakanishi K., Hashimoto T., Hiroishi K., Matsui K., Yoshimoto T., Morse H. C., 3rd, Furuyama J., Hamaoka T., Higashino K., Paul W. E. Demonstration of up-regulated IL 2 receptor expression on an in vitro cloned BCL1 subline. J Immunol. 1987 Mar 15;138(6):1817–1825. [PubMed] [Google Scholar]
  15. Nakanishi K., Malek T. R., Smith K. A., Hamaoka T., Shevach E. M., Paul W. E. Both interleukin 2 and a second T cell-derived factor in EL-4 supernatant have activity as differentiation factors in IgM synthesis. J Exp Med. 1984 Dec 1;160(6):1605–1621. doi: 10.1084/jem.160.6.1605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ohara J., Paul W. E. Production of a monoclonal antibody to and molecular characterization of B-cell stimulatory factor-1. Nature. 1985 May 23;315(6017):333–336. doi: 10.1038/315333a0. [DOI] [PubMed] [Google Scholar]
  17. Ohara J., Paul W. E. Receptors for B-cell stimulatory factor-1 expressed on cells of haematopoietic lineage. Nature. 1987 Feb 5;325(6104):537–540. doi: 10.1038/325537a0. [DOI] [PubMed] [Google Scholar]
  18. Ono S., Hayashi S., Takahama Y., Dobashi K., Katoh Y., Nakanishi K., Paul W. E., Hamaoka T. Identification of two distinct factors, B151-TRF1 and B151-TRF2, inducing differentiation of activated B cells and small resting B cells into antibody-producing cells. J Immunol. 1986 Jul 1;137(1):187–196. [PubMed] [Google Scholar]
  19. 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]
  20. Pike B. L., Nossal G. J. Interleukin 1 can act as a B-cell growth and differentiation factor. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8153–8157. doi: 10.1073/pnas.82.23.8153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Rambaldi A., Young D. C., Herrmann F., Cannistra S. A., Griffin J. D. Interferon-gamma induces expression of the interleukin 2 receptor gene in human monocytes. Eur J Immunol. 1987 Jan;17(1):153–156. doi: 10.1002/eji.1830170127. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Sanderson C. J., O'Garra A., Warren D. J., Klaus G. G. Eosinophil differentiation factor also has B-cell growth factor activity: proposed name interleukin 4. Proc Natl Acad Sci U S A. 1986 Jan;83(2):437–440. doi: 10.1073/pnas.83.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shortman K., Linthicum D. S., Battye F. L., Goldschneider I., Liabeuf A., Golstein P., Clark E. A., Lake P. Cytotoxic and fluorescent assays for thymocyte subpopulations differing in surface thy-1 level. Cell Biophys. 1979 Sep;1(3):255–270. doi: 10.1007/BF02783667. [DOI] [PubMed] [Google Scholar]
  27. Smith K. A. Interleukin 2. Annu Rev Immunol. 1984;2:319–333. doi: 10.1146/annurev.iy.02.040184.001535. [DOI] [PubMed] [Google Scholar]
  28. Smith K. A. T-cell growth factor. Immunol Rev. 1980;51:337–357. doi: 10.1111/j.1600-065x.1980.tb00327.x. [DOI] [PubMed] [Google Scholar]
  29. Takatsu K., Harada N., Hara Y., Takahama Y., Yamada G., Dobashi K., Hamaoka T. Purification and physicochemical characterization of murine T cell replacing factor (TRF). J Immunol. 1985 Jan;134(1):382–389. [PubMed] [Google Scholar]
  30. Tsudo M., Uchiyama T., Uchino H. Expression of Tac antigen on activated normal human B cells. J Exp Med. 1984 Aug 1;160(2):612–617. doi: 10.1084/jem.160.2.612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Walker F., Nicola N. A., Metcalf D., Burgess A. W. Hierarchical down-modulation of hemopoietic growth factor receptors. Cell. 1985 Nov;43(1):269–276. doi: 10.1016/0092-8674(85)90032-7. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Zubler R. H., Lowenthal J. W., Erard F., Hashimoto N., Devos R., MacDonald H. R. Activated B cells express receptors for, and proliferate in response to, pure interleukin 2. J Exp Med. 1984 Oct 1;160(4):1170–1183. doi: 10.1084/jem.160.4.1170. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES