Skip to main content
NCBI home page
Immunology logoLink to Immunology
. 1993 Jul;79(3):471–478.

Characterization of the ovine interleukin-2 receptor-alpha chain: differential induction on precultured alpha beta and gamma delta T cells.

A M Verhagen 1, M R Brandon 1, A D Nash 1
PMCID: PMC1421989  PMID: 8406574

Abstract

A combination of concanavalin A (Con A)-stimulated ovine lymph node (LN) cells and Chinese hamster ovarian (CHO) cells stably transfected with the ovine interleukin-2 receptor-alpha (IL-2R alpha) chain cDNA (CHO IL-2R cells) were used in a differential immunization strategy to generate several monoclonal antibodies (mAb) against the ovine IL-2R alpha chain. The specificity of one of the mAb, designated mAb 9-14, for the ovine IL-2R alpha chain was demonstrated by its reactivity with Con A-stimulated LN cells and CHO IL-2R cells, immunoprecipitation of a 47,000 MW protein from CHO IL-2R cells and inhibition of IL-2-dependent proliferation of Con A-stimulated ovine LN cells. Examination of IL-2R alpha chain expression on resting lamb peripheral blood lymphocyte populations showed a high frequency of IL-2R alpha chain expression on CD4 T cells but not on CD8 T cells, CD45RA+ cells or gamma delta T cells, which comprise up to 60% of lamb peripheral blood T cells. The kinetics of IL-2R alpha chain induction on Con A-stimulated peripheral blood alpha beta and gamma delta T cells was compared. A rapid induction of IL-2R alpha chain expression on precultured gamma delta T cells but not alpha beta T cells was observed within 6 hr of Con A stimulation. A preculturing period was required to 'prime' gamma delta T cells for rapid responsiveness to Con A. Using appropriate inhibitors, we demonstrated that both transcription and translation events were required for rapid IL-2R expression on precultured gamma delta T cells and therefore the 'priming' of gamma delta T cells by in vitro culture did not involve an accumulation of IL-2R alpha chain mRNA or preformed receptors within these cells.

Full text

PDF
471

Images in this article

473Figure 2
on p.473

Selected References

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

  1. Born W., Hall L., Dallas A., Boymel J., Shinnick T., Young D., Brennan P., O'Brien R. Recognition of a peptide antigen by heat shock--reactive gamma delta T lymphocytes. Science. 1990 Jul 6;249(4964):67–69. doi: 10.1126/science.1695022. [DOI] [PubMed] [Google Scholar]
  2. Boyle W. An extension of the 51Cr-release assay for the estimation of mouse cytotoxins. Transplantation. 1968 Sep;6(6):761–764. doi: 10.1097/00007890-196809000-00002. [DOI] [PubMed] [Google Scholar]
  3. Böhnlein E., Ballard D. W., Bogerd H., Peffer N. J., Lowenthal J. W., Greene W. C. Induction of interleukin-2 receptor-alpha gene expression is regulated by post-translational activation of kappa B specific DNA binding proteins. J Biol Chem. 1989 May 25;264(15):8475–8478. [PubMed] [Google Scholar]
  4. Böhnlein E., Lowenthal J. W., Siekevitz M., Ballard D. W., Franza B. R., Greene W. C. The same inducible nuclear proteins regulates mitogen activation of both the interleukin-2 receptor-alpha gene and type 1 HIV. Cell. 1988 Jun 3;53(5):827–836. doi: 10.1016/0092-8674(88)90099-2. [DOI] [PubMed] [Google Scholar]
  5. Caligiuri M. A., Zmuidzinas A., Manley T. J., Levine H., Smith K. A., Ritz J. Functional consequences of interleukin 2 receptor expression on resting human lymphocytes. Identification of a novel natural killer cell subset with high affinity receptors. J Exp Med. 1990 May 1;171(5):1509–1526. doi: 10.1084/jem.171.5.1509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cole S. R., Ashman L. K., Ey P. L. Biotinylation: an alternative to radioiodination for the identification of cell surface antigens in immunoprecipitates. Mol Immunol. 1987 Jul;24(7):699–705. doi: 10.1016/0161-5890(87)90051-4. [DOI] [PubMed] [Google Scholar]
  7. Cross S. L., Halden N. F., Lenardo M. J., Leonard W. J. Functionally distinct NF-kappa B binding sites in the immunoglobulin kappa and IL-2 receptor alpha chain genes. Science. 1989 Apr 28;244(4903):466–469. doi: 10.1126/science.2497520. [DOI] [PubMed] [Google Scholar]
  8. Damle N. K., Klussman K., Aruffo A. Intercellular adhesion molecule-2, a second counter-receptor for CD11a/CD18 (leukocyte function-associated antigen-1), provides a costimulatory signal for T-cell receptor-initiated activation of human T cells. J Immunol. 1992 Feb 1;148(3):665–671. [PubMed] [Google Scholar]
  9. Goddeeris B. M., Morrison W. I., Naessens J., Magondu J. G. The bovine autologous mixed leukocyte reaction: a proliferative response of non-T cells under the control of monocytes. Immunobiology. 1987 Dec;176(1-2):47–62. doi: 10.1016/S0171-2985(87)80099-2. [DOI] [PubMed] [Google Scholar]
  10. Harding F. A., McArthur J. G., Gross J. A., Raulet D. H., Allison J. P. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature. 1992 Apr 16;356(6370):607–609. doi: 10.1038/356607a0. [DOI] [PubMed] [Google Scholar]
  11. Havran W. L., Poenie M., Tigelaar R. E., Tsien R. Y., Allison J. P. Phenotypic and functional analysis of gamma delta T cell receptor-positive murine dendritic epidermal clones. J Immunol. 1989 Mar 1;142(5):1422–1428. [PubMed] [Google Scholar]
  12. Hein W. R., Dudler L., Morris B. Differential peripheral expansion and in vivo antigen reactivity of alpha/beta and gamma/delta T cells emigrating from the early fetal lamb thymus. Eur J Immunol. 1990 Aug;20(8):1805–1813. doi: 10.1002/eji.1830200827. [DOI] [PubMed] [Google Scholar]
  13. Hémar A., Cereghini S., Cornet V., Blank V., Israël A., Greene W. C., Dautry-Varsat A. Kappa B binding proteins are constitutively expressed in an IL-2 autocrine human T cell line. J Immunol. 1991 Apr 1;146(7):2409–2416. [PubMed] [Google Scholar]
  14. Jankovic D. L., Rebollo A., Kumar A., Gibert M., Thèze J. IL-2-dependent proliferation of murine T cells requires expression of both the p55 and p70 subunits of the IL-2 receptor. J Immunol. 1990 Dec 15;145(12):4136–4144. [PubMed] [Google Scholar]
  15. Kabelitz D., Bender A., Schondelmaier S., da Silva Lobo M. L., Janssen O. Human cytotoxic lymphocytes. V. Frequency and specificity of gamma delta+ cytotoxic lymphocyte precursors activated by allogeneic or autologous stimulator cells. J Immunol. 1990 Nov 1;145(9):2827–2832. [PubMed] [Google Scholar]
  16. Kanegane H., Miyawaki T., Kato K., Yokoi T., Uehara T., Yachie A., Taniguchi N. A novel subpopulation of CD45RA+ CD4+ T cells expressing IL-2 receptor alpha-chain (CD25) and having a functionally transitional nature into memory cells. Int Immunol. 1991 Dec;3(12):1349–1356. doi: 10.1093/intimm/3.12.1349. [DOI] [PubMed] [Google Scholar]
  17. Leonard W. J., Depper J. M., Kanehisa M., Krönke M., Peffer N. J., Svetlik P. B., Sullivan M., Greene W. C. Structure of the human interleukin-2 receptor gene. Science. 1985 Nov 8;230(4726):633–639. doi: 10.1126/science.2996141. [DOI] [PubMed] [Google Scholar]
  18. Lowenthal J. W., Ballard D. W., Bogerd H., Böhnlein E., Greene W. C. Tumor necrosis factor-alpha activation of the IL-2 receptor-alpha gene involves the induction of kappa B-specific DNA binding proteins. J Immunol. 1989 May 1;142(9):3121–3128. [PubMed] [Google Scholar]
  19. Lowenthal J. W., Ballard D. W., Böhnlein E., Greene W. C. Tumor necrosis factor alpha induces proteins that bind specifically to kappa B-like enhancer elements and regulate interleukin 2 receptor alpha-chain gene expression in primary human T lymphocytes. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2331–2335. doi: 10.1073/pnas.86.7.2331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lowenthal J. W., Greene W. C. Contrasting interleukin 2 binding properties of the alpha (p55) and beta (p70) protein subunits of the human high-affinity interleukin 2 receptor. J Exp Med. 1987 Oct 1;166(4):1156–1161. doi: 10.1084/jem.166.4.1156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mackay C. R., Beya M. F., Matzinger P. Gamma/delta T cells express a unique surface molecule appearing late during thymic development. Eur J Immunol. 1989 Aug;19(8):1477–1483. doi: 10.1002/eji.1830190820. [DOI] [PubMed] [Google Scholar]
  22. Mackay C. R., Hein W. R. A large proportion of bovine T cells express the gamma delta T cell receptor and show a distinct tissue distribution and surface phenotype. Int Immunol. 1989;1(5):540–545. doi: 10.1093/intimm/1.5.540. [DOI] [PubMed] [Google Scholar]
  23. Mackay C. R., Maddox J. F., Brandon M. R. A monoclonal antibody to the p220 component of sheep LCA identifies B cells and a unique lymphocyte subset. Cell Immunol. 1987 Nov;110(1):46–55. doi: 10.1016/0008-8749(87)90100-6. [DOI] [PubMed] [Google Scholar]
  24. Mackay C. R., Maddox J. F., Brandon M. R. Three distinct subpopulations of sheep T lymphocytes. Eur J Immunol. 1986 Jan;16(1):19–25. doi: 10.1002/eji.1830160105. [DOI] [PubMed] [Google Scholar]
  25. Mackay C. R., Marston W. L., Dudler L. Naive and memory T cells show distinct pathways of lymphocyte recirculation. J Exp Med. 1990 Mar 1;171(3):801–817. doi: 10.1084/jem.171.3.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Matis L. A., Fry A. M., Cron R. Q., Cotterman M. M., Dick R. F., Bluestone J. A. Structure and specificity of a class II MHC alloreactive gamma delta T cell receptor heterodimer. Science. 1989 Aug 18;245(4919):746–749. doi: 10.1126/science.2528206. [DOI] [PubMed] [Google Scholar]
  27. Moebius U., Kober G., Griscelli A. L., Hercend T., Meuer S. C. Expression of different CD8 isoforms on distinct human lymphocyte subpopulations. Eur J Immunol. 1991 Aug;21(8):1793–1800. doi: 10.1002/eji.1830210803. [DOI] [PubMed] [Google Scholar]
  28. Pomerantz J. L., Mauxion F., Yoshida M., Greene W. C., Sen R. A second sequence element located 3' to the NF-kappa B-binding site regulates IL-2 receptor-alpha gene induction. J Immunol. 1989 Dec 15;143(12):4275–4281. [PubMed] [Google Scholar]
  29. Robb R. J., Greene W. C., Rusk C. M. Low and high affinity cellular receptors for interleukin 2. Implications for the level of Tac antigen. J Exp Med. 1984 Oct 1;160(4):1126–1146. doi: 10.1084/jem.160.4.1126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Roberts K., Yokoyama W. M., Kehn P. J., Shevach E. M. The vitronectin receptor serves as an accessory molecule for the activation of a subset of gamma/delta T cells. J Exp Med. 1991 Jan 1;173(1):231–240. doi: 10.1084/jem.173.1.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rubin L. A., Kurman C. C., Fritz M. E., Biddison W. E., Boutin B., Yarchoan R., Nelson D. L. Soluble interleukin 2 receptors are released from activated human lymphoid cells in vitro. J Immunol. 1985 Nov;135(5):3172–3177. [PubMed] [Google Scholar]
  32. Smith M. R., Greene W. C. The same 50-kDa cellular protein binds to the negative regulatory elements of the interleukin 2 receptor alpha-chain gene and the human immunodeficiency virus type 1 long terminal repeat. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8526–8530. doi: 10.1073/pnas.86.21.8526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Taga K., Kasahara Y., Yachie A., Miyawaki T., Taniguchi N. Preferential expression of IL-2 receptor subunits on memory populations within CD4+ and CD8+ T cells. Immunology. 1991 Jan;72(1):15–19. [PMC free article] [PubMed] [Google Scholar]
  34. Takeshita T., Asao H., Ohtani K., Ishii N., Kumaki S., Tanaka N., Munakata H., Nakamura M., Sugamura K. Cloning of the gamma chain of the human IL-2 receptor. Science. 1992 Jul 17;257(5068):379–382. doi: 10.1126/science.1631559. [DOI] [PubMed] [Google Scholar]
  35. Verhagen A. M., Andrews A. E., Brandon M. R., Nash A. D. Molecular cloning, expression and characterization of the ovine IL-2R alpha chain. Immunology. 1992 May;76(1):1–9. [PMC free article] [PubMed] [Google Scholar]
  36. Wano Y., Uchiyama T., Fukui K., Maeda M., Uchino H., Yodoi J. Characterization of human interleukin 2 receptor (Tac antigen) in normal and leukemic T cells: co-expression of normal and aberrant receptors on Hut-102 cells. J Immunol. 1984 Jun;132(6):3005–3010. [PubMed] [Google Scholar]
  37. Wilde D. B., Roberts K., Sturmhöfel K., Kikuchi G., Coligan J. E., Shevach E. M. Mouse autoreactive gamma/delta T cells. I. Functional properties of autoreactive T cell hybridomas. Eur J Immunol. 1992 Feb;22(2):483–489. doi: 10.1002/eji.1830220229. [DOI] [PubMed] [Google Scholar]
  38. Zachowski A., Henry J. P., Devaux P. F. Control of transmembrane lipid asymmetry in chromaffin granules by an ATP-dependent protein. Nature. 1989 Jul 6;340(6228):75–76. doi: 10.1038/340075a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES