Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1993 Feb;12(2):759–768. doi: 10.1002/j.1460-2075.1993.tb05710.x

Association of p56lck with IL-2 receptor beta chain is critical for the IL-2-induced activation of p56lck.

Y Minami 1, T Kono 1, K Yamada 1, N Kobayashi 1, A Kawahara 1, R M Perlmutter 1, T Taniguchi 1
PMCID: PMC413263  PMID: 8440263

Abstract

Previous studies demonstrate that p56lck, a member of the src-family of protein tyrosine kinases (PTKs), can physically associate with the interleukin-2 (IL-2) receptor beta chain (IL-2R beta) and that IL-2 receptor engagement stimulates p56lck activity. To examine the mechanisms underlying p56lck PTK activation by IL-2, we established a mouse pro-B cell line, BAF-B03, expressing both IL-2R beta (either the wild-type or mutant forms) and mouse p56lck at high levels. BAF-B03 cells expressing a mutant IL-2R beta chain lacking an 'acidic' region of the cytoplasmic domain, previously shown to be essential for association with p56lck, fail to induce p56lck PTK activation upon IL-2 stimulation. This suggests that the association of p56lck with the IL-2R beta chain, despite its low stoichiometry, is required for the activation of cellular p56lck PTK upon IL-2 stimulation. Intriguingly, BAF-B03 cells expressing an IL-2R beta chain which lacks a different cytoplasmic region, the 'serine-rich' region, also fail to activate p56lck in response to IL-2. Hence, physical association of p56lck with the IL-2R beta chain is not by itself sufficient to permit IL-2-mediated regulation of this PTK. Additional experiments suggest that one result of PTK activation is the accumulation of c-fos and c-jun transcripts.

Full text

PDF
759

Images in this article

760Image
on p.760
761Image
on p.761
762Image
on p.762
763Image
on p.763
764Image
on p.764
764Image
on p.764

Selected References

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

  1. Asao H., Takeshita T., Nakamura M., Nagata K., Sugamura K. Interleukin 2 (IL-2)-induced tyrosine phosphorylation of IL-2 receptor p75. J Exp Med. 1990 Mar 1;171(3):637–644. doi: 10.1084/jem.171.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Augustine J. A., Sutor S. L., Abraham R. T. Interleukin 2- and polyomavirus middle T antigen-induced modification of phosphatidylinositol 3-kinase activity in activated T lymphocytes. Mol Cell Biol. 1991 Sep;11(9):4431–4440. doi: 10.1128/mcb.11.9.4431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bazan J. F. Structural design and molecular evolution of a cytokine receptor superfamily. Proc Natl Acad Sci U S A. 1990 Sep;87(18):6934–6938. doi: 10.1073/pnas.87.18.6934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cantley L. C., Auger K. R., Carpenter C., Duckworth B., Graziani A., Kapeller R., Soltoff S. Oncogenes and signal transduction. Cell. 1991 Jan 25;64(2):281–302. doi: 10.1016/0092-8674(91)90639-g. [DOI] [PubMed] [Google Scholar]
  5. Cosman D., Lyman S. D., Idzerda R. L., Beckmann M. P., Park L. S., Goodwin R. G., March C. J. A new cytokine receptor superfamily. Trends Biochem Sci. 1990 Jul;15(7):265–270. doi: 10.1016/0968-0004(90)90051-c. [DOI] [PubMed] [Google Scholar]
  6. D'Andrea A. D., Fasman G. D., Lodish H. F. Erythropoietin receptor and interleukin-2 receptor beta chain: a new receptor family. Cell. 1989 Sep 22;58(6):1023–1024. doi: 10.1016/0092-8674(89)90499-6. [DOI] [PubMed] [Google Scholar]
  7. Doi T., Hatakeyama M., Minamoto S., Kono T., Mori H., Taniguchi T. Human interleukin 2 (IL 2) receptor beta chain allows transduction of IL 2-induced proliferation signal(s) in a murine cell line. Eur J Immunol. 1989 Dec;19(12):2375–2378. doi: 10.1002/eji.1830191229. [DOI] [PubMed] [Google Scholar]
  8. Farrar W. L., Ferris D. K. Two-dimensional analysis of interleukin 2-regulated tyrosine kinase activation mediated by the p70-75 beta subunit of the interleukin 2 receptor. J Biol Chem. 1989 Jul 25;264(21):12562–12567. [PubMed] [Google Scholar]
  9. Ferris D. K., Willette-Brown J., Ortaldo J. R., Farrar W. L. IL-2 regulation of tyrosine kinase activity is mediated through the p70-75 beta-subunit of the IL-2 receptor. J Immunol. 1989 Aug 1;143(3):870–876. [PubMed] [Google Scholar]
  10. Fukunaga R., Ishizaka-Ikeda E., Pan C. X., Seto Y., Nagata S. Functional domains of the granulocyte colony-stimulating factor receptor. EMBO J. 1991 Oct;10(10):2855–2865. doi: 10.1002/j.1460-2075.1991.tb07835.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harada H., Willison K., Sakakibara J., Miyamoto M., Fujita T., Taniguchi T. Absence of the type I IFN system in EC cells: transcriptional activator (IRF-1) and repressor (IRF-2) genes are developmentally regulated. Cell. 1990 Oct 19;63(2):303–312. doi: 10.1016/0092-8674(90)90163-9. [DOI] [PubMed] [Google Scholar]
  12. Hatakeyama M., Kawahara A., Mori H., Shibuya H., Taniguchi T. c-fos gene induction by interleukin 2: identification of the critical cytoplasmic regions within the interleukin 2 receptor beta chain. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2022–2026. doi: 10.1073/pnas.89.6.2022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hatakeyama M., Kono T., Kobayashi N., Kawahara A., Levin S. D., Perlmutter R. M., Taniguchi T. Interaction of the IL-2 receptor with the src-family kinase p56lck: identification of novel intermolecular association. Science. 1991 Jun 14;252(5012):1523–1528. doi: 10.1126/science.2047859. [DOI] [PubMed] [Google Scholar]
  14. Hatakeyama M., Mori H., Doi T., Taniguchi T. A restricted cytoplasmic region of IL-2 receptor beta chain is essential for growth signal transduction but not for ligand binding and internalization. Cell. 1989 Dec 1;59(5):837–845. doi: 10.1016/0092-8674(89)90607-7. [DOI] [PubMed] [Google Scholar]
  15. Hatakeyama M., Tsudo M., Minamoto S., Kono T., Doi T., Miyata T., Miyasaka M., Taniguchi T. Interleukin-2 receptor beta chain gene: generation of three receptor forms by cloned human alpha and beta chain cDNA's. Science. 1989 May 5;244(4904):551–556. doi: 10.1126/science.2785715. [DOI] [PubMed] [Google Scholar]
  16. Hibi M., Murakami M., Saito M., Hirano T., Taga T., Kishimoto T. Molecular cloning and expression of an IL-6 signal transducer, gp130. Cell. 1990 Dec 21;63(6):1149–1157. doi: 10.1016/0092-8674(90)90411-7. [DOI] [PubMed] [Google Scholar]
  17. Horak I. D., Gress R. E., Lucas P. J., Horak E. M., Waldmann T. A., Bolen J. B. T-lymphocyte interleukin 2-dependent tyrosine protein kinase signal transduction involves the activation of p56lck. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1996–2000. doi: 10.1073/pnas.88.5.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hsi E. D., Siegel J. N., Minami Y., Luong E. T., Klausner R. D., Samelson L. E. T cell activation induces rapid tyrosine phosphorylation of a limited number of cellular substrates. J Biol Chem. 1989 Jun 25;264(18):10836–10842. [PubMed] [Google Scholar]
  19. Hunter T., Cooper J. A. Protein-tyrosine kinases. Annu Rev Biochem. 1985;54:897–930. doi: 10.1146/annurev.bi.54.070185.004341. [DOI] [PubMed] [Google Scholar]
  20. Idzerda R. L., March C. J., Mosley B., Lyman S. D., Vanden Bos T., Gimpel S. D., Din W. S., Grabstein K. H., Widmer M. B., Park L. S. Human interleukin 4 receptor confers biological responsiveness and defines a novel receptor superfamily. J Exp Med. 1990 Mar 1;171(3):861–873. doi: 10.1084/jem.171.3.861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Isfort R. J., Stevens D., May W. S., Ihle J. N. Interleukin 3 binds to a 140-kDa phosphotyrosine-containing cell surface protein. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7982–7986. doi: 10.1073/pnas.85.21.7982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Itoh N., Yonehara S., Schreurs J., Gorman D. M., Maruyama K., Ishii A., Yahara I., Arai K., Miyajima A. Cloning of an interleukin-3 receptor gene: a member of a distinct receptor gene family. Science. 1990 Jan 19;247(4940):324–327. doi: 10.1126/science.2404337. [DOI] [PubMed] [Google Scholar]
  23. Kawakami T., Kawakami Y., Aaronson S. A., Robbins K. C. Acquisition of transforming properties by FYN, a normal SRC-related human gene. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3870–3874. doi: 10.1073/pnas.85.11.3870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kono T., Doi T., Yamada G., Hatakeyama M., Minamoto S., Tsudo M., Miyasaka M., Miyata T., Taniguchi T. Murine interleukin 2 receptor beta chain: dysregulated gene expression in lymphoma line EL-4 caused by a promoter insertion. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1806–1810. doi: 10.1073/pnas.87.5.1806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Koyasu S., Tojo A., Miyajima A., Akiyama T., Kasuga M., Urabe A., Schreurs J., Arai K., Takaku F., Yahara I. Interleukin 3-specific tyrosine phosphorylation of a membrane glycoprotein of Mr 150,000 in multi-factor-dependent myeloid cell lines. EMBO J. 1987 Dec 20;6(13):3979–3984. doi: 10.1002/j.1460-2075.1987.tb02740.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kupfer A., Singer S. J., Janeway C. A., Jr, Swain S. L. Coclustering of CD4 (L3T4) molecule with the T-cell receptor is induced by specific direct interaction of helper T cells and antigen-presenting cells. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5888–5892. doi: 10.1073/pnas.84.16.5888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lord K. A., Abdollahi A., Thomas S. M., DeMarco M., Brugge J. S., Hoffman-Liebermann B., Liebermann D. A. Leukemia inhibitory factor and interleukin-6 trigger the same immediate early response, including tyrosine phosphorylation, upon induction of myeloid leukemia differentiation. Mol Cell Biol. 1991 Sep;11(9):4371–4379. doi: 10.1128/mcb.11.9.4371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Louie R. R., King C. S., MacAuley A., Marth J. D., Perlmutter R. M., Eckhart W., Cooper J. A. p56lck protein-tyrosine kinase is cytoskeletal and does not bind to polyomavirus middle T antigen. J Virol. 1988 Dec;62(12):4673–4679. doi: 10.1128/jvi.62.12.4673-4679.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Luo K. X., Sefton B. M. Cross-linking of T-cell surface molecules CD4 and CD8 stimulates phosphorylation of the lck tyrosine protein kinase at the autophosphorylation site. Mol Cell Biol. 1990 Oct;10(10):5305–5313. doi: 10.1128/mcb.10.10.5305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Marth J. D., Cooper J. A., King C. S., Ziegler S. F., Tinker D. A., Overell R. W., Krebs E. G., Perlmutter R. M. Neoplastic transformation induced by an activated lymphocyte-specific protein tyrosine kinase (pp56lck). Mol Cell Biol. 1988 Feb;8(2):540–550. doi: 10.1128/mcb.8.2.540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Marth J. D., Lewis D. B., Cooke M. P., Mellins E. D., Gearn M. E., Samelson L. E., Wilson C. B., Miller A. D., Perlmutter R. M. Lymphocyte activation provokes modification of a lymphocyte-specific protein tyrosine kinase (p56lck). J Immunol. 1989 Apr 1;142(7):2430–2437. [PubMed] [Google Scholar]
  32. Merida I., Diez E., Gaulton G. N. IL-2 binding activates a tyrosine-phosphorylated phosphatidylinositol-3-kinase. J Immunol. 1991 Oct 1;147(7):2202–2207. [PubMed] [Google Scholar]
  33. Merida I., Gaulton G. N. Protein tyrosine phosphorylation associated with activation of the interleukin 2 receptor. J Biol Chem. 1990 Apr 5;265(10):5690–5694. [PubMed] [Google Scholar]
  34. Mills G. B., May C., McGill M., Fung M., Baker M., Sutherland R., Greene W. C. Interleukin 2-induced tyrosine phosphorylation. Interleukin 2 receptor beta is tyrosine phosphorylated. J Biol Chem. 1990 Feb 25;265(6):3561–3567. [PubMed] [Google Scholar]
  35. Morgan D. A., Ruscetti F. W., Gallo R. Selective in vitro growth of T lymphocytes from normal human bone marrows. Science. 1976 Sep 10;193(4257):1007–1008. doi: 10.1126/science.181845. [DOI] [PubMed] [Google Scholar]
  36. Mori H., Barsoumian E. L., Hatakeyama M., Taniguchi T. Signal transduction by interleukin 2 receptor beta chain: importance of the structural integrity as revealed by site-directed mutagenesis and generation of chimeric receptors. Int Immunol. 1991 Feb;3(2):149–156. doi: 10.1093/intimm/3.2.149. [DOI] [PubMed] [Google Scholar]
  37. Morla A. O., Schreurs J., Miyajima A., Wang J. Y. Hematopoietic growth factors activate the tyrosine phosphorylation of distinct sets of proteins in interleukin-3-dependent murine cell lines. Mol Cell Biol. 1988 May;8(5):2214–2218. doi: 10.1128/mcb.8.5.2214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Murakami M., Narazaki M., Hibi M., Yawata H., Yasukawa K., Hamaguchi M., Taga T., Kishimoto T. Critical cytoplasmic region of the interleukin 6 signal transducer gp130 is conserved in the cytokine receptor family. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11349–11353. doi: 10.1073/pnas.88.24.11349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Nakajima K., Wall R. Interleukin-6 signals activating junB and TIS11 gene transcription in a B-cell hybridoma. Mol Cell Biol. 1991 Mar;11(3):1409–1418. doi: 10.1128/mcb.11.3.1409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Okamoto Y., Minamoto S., Shimizu K., Mogami H., Taniguchi T. Interleukin 2 receptor beta chain expressed in an oligodendroglioma line binds interleukin 2 and delivers growth signal. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6584–6588. doi: 10.1073/pnas.87.17.6584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Palacios R., Steinmetz M. Il-3-dependent mouse clones that express B-220 surface antigen, contain Ig genes in germ-line configuration, and generate B lymphocytes in vivo. Cell. 1985 Jul;41(3):727–734. doi: 10.1016/s0092-8674(85)80053-2. [DOI] [PubMed] [Google Scholar]
  42. Rauscher F. J., 3rd, Voulalas P. J., Franza B. R., Jr, Curran T. Fos and Jun bind cooperatively to the AP-1 site: reconstitution in vitro. Genes Dev. 1988 Dec;2(12B):1687–1699. doi: 10.1101/gad.2.12b.1687. [DOI] [PubMed] [Google Scholar]
  43. Remillard B., Petrillo R., Maslinski W., Tsudo M., Strom T. B., Cantley L., Varticovski L. Interleukin-2 receptor regulates activation of phosphatidylinositol 3-kinase. J Biol Chem. 1991 Aug 5;266(22):14167–14170. [PubMed] [Google Scholar]
  44. 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]
  45. Rudd C. E. CD4, CD8 and the TCR-CD3 complex: a novel class of protein-tyrosine kinase receptor. Immunol Today. 1990 Nov;11(11):400–406. doi: 10.1016/0167-5699(90)90159-7. [DOI] [PubMed] [Google Scholar]
  46. Rudd C. E., Trevillyan J. M., Dasgupta J. D., Wong L. L., Schlossman S. F. The CD4 receptor is complexed in detergent lysates to a protein-tyrosine kinase (pp58) from human T lymphocytes. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5190–5194. doi: 10.1073/pnas.85.14.5190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Saltzman E. M., Thom R. R., Casnellie J. E. Activation of a tyrosine protein kinase is an early event in the stimulation of T lymphocytes by interleukin-2. J Biol Chem. 1988 May 25;263(15):6956–6959. [PubMed] [Google Scholar]
  48. Saltzman E. M., White K., Casnellie J. E. Stimulation of the antigen and interleukin-2 receptors on T lymphocytes activates distinct tyrosine protein kinases. J Biol Chem. 1990 Jun 15;265(17):10138–10142. [PubMed] [Google Scholar]
  49. Samelson L. E., Phillips A. F., Luong E. T., Klausner R. D. Association of the fyn protein-tyrosine kinase with the T-cell antigen receptor. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4358–4362. doi: 10.1073/pnas.87.11.4358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Sefton B. M. The lck tyrosine protein kinase. Oncogene. 1991 May;6(5):683–686. [PubMed] [Google Scholar]
  51. Shaw A. S., Amrein K. E., Hammond C., Stern D. F., Sefton B. M., Rose J. K. The lck tyrosine protein kinase interacts with the cytoplasmic tail of the CD4 glycoprotein through its unique amino-terminal domain. Cell. 1989 Nov 17;59(4):627–636. doi: 10.1016/0092-8674(89)90008-1. [DOI] [PubMed] [Google Scholar]
  52. Shaw A. S., Chalupny J., Whitney J. A., Hammond C., Amrein K. E., Kavathas P., Sefton B. M., Rose J. K. Short related sequences in the cytoplasmic domains of CD4 and CD8 mediate binding to the amino-terminal domain of the p56lck tyrosine protein kinase. Mol Cell Biol. 1990 May;10(5):1853–1862. doi: 10.1128/mcb.10.5.1853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Shibuya H., Yoneyama M., Nakamura Y., Harada H., Hatakeyama M., Minamoto S., Kono T., Doi T., White R., Taniguchi T. The human interleukin-2 receptor beta-chain gene: genomic organization, promoter analysis and chromosomal assignment. Nucleic Acids Res. 1990 Jul 11;18(13):3697–3703. doi: 10.1093/nar/18.13.3697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Shibuya H., Yoneyama M., Ninomiya-Tsuji J., Matsumoto K., Taniguchi T. IL-2 and EGF receptors stimulate the hematopoietic cell cycle via different signaling pathways: demonstration of a novel role for c-myc. Cell. 1992 Jul 10;70(1):57–67. doi: 10.1016/0092-8674(92)90533-i. [DOI] [PubMed] [Google Scholar]
  55. Siegel J. P., Sharon M., Smith P. L., Leonard W. J. The IL-2 receptor beta chain (p70): role in mediating signals for LAK, NK, and proliferative activities. Science. 1987 Oct 2;238(4823):75–78. doi: 10.1126/science.3116668. [DOI] [PubMed] [Google Scholar]
  56. Smith K. A. Interleukin-2: inception, impact, and implications. Science. 1988 May 27;240(4856):1169–1176. doi: 10.1126/science.3131876. [DOI] [PubMed] [Google Scholar]
  57. Springer T., Galfrè G., Secher D. S., Milstein C. Monoclonal xenogeneic antibodies to murine cell surface antigens: identification of novel leukocyte differentiation antigens. Eur J Immunol. 1978 Aug;8(8):539–551. doi: 10.1002/eji.1830080802. [DOI] [PubMed] [Google Scholar]
  58. Stefanová I., Horejsí V., Ansotegui I. J., Knapp W., Stockinger H. GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science. 1991 Nov 15;254(5034):1016–1019. doi: 10.1126/science.1719635. [DOI] [PubMed] [Google Scholar]
  59. 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]
  60. Takeshita T., Asao H., Suzuki J., Sugamura K. An associated molecule, p64, with high-affinity interleukin 2 receptor. Int Immunol. 1990;2(5):477–480. doi: 10.1093/intimm/2.5.477. [DOI] [PubMed] [Google Scholar]
  61. Taniguchi T., Matsui H., Fujita T., Hatakeyama M., Kashima N., Fuse A., Hamuro J., Nishi-Takaoka C., Yamada G. Molecular analysis of the interleukin-2 system. Immunol Rev. 1986 Aug;92:121–133. doi: 10.1111/j.1600-065x.1986.tb01497.x. [DOI] [PubMed] [Google Scholar]
  62. Tsudo M., Goldman C. K., Bongiovanni K. F., Chan W. C., Winton E. F., Yagita M., Grimm E. A., Waldmann T. A. The p75 peptide is the receptor for interleukin 2 expressed on large granular lymphocytes and is responsible for the interleukin 2 activation of these cells. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5394–5398. doi: 10.1073/pnas.84.15.5394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Tsudo M., Kitamura F., Miyasaka M. Characterization of the interleukin 2 receptor beta chain using three distinct monoclonal antibodies. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1982–1986. doi: 10.1073/pnas.86.6.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Turner J. M., Brodsky M. H., Irving B. A., Levin S. D., Perlmutter R. M., Littman D. R. Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell. 1990 Mar 9;60(5):755–765. doi: 10.1016/0092-8674(90)90090-2. [DOI] [PubMed] [Google Scholar]
  65. Uetsuki T., Naito A., Nagata S., Kaziro Y. Isolation and characterization of the human chromosomal gene for polypeptide chain elongation factor-1 alpha. J Biol Chem. 1989 Apr 5;264(10):5791–5798. [PubMed] [Google Scholar]
  66. Ullrich A., Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell. 1990 Apr 20;61(2):203–212. doi: 10.1016/0092-8674(90)90801-k. [DOI] [PubMed] [Google Scholar]
  67. Veillette A., Bolen J. B., Bookman M. A. Alterations in tyrosine protein phosphorylation induced by antibody-mediated cross-linking of the CD4 receptor of T lymphocytes. Mol Cell Biol. 1989 Oct;9(10):4441–4446. doi: 10.1128/mcb.9.10.4441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Veillette A., Bookman M. A., Horak E. M., Bolen J. B. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell. 1988 Oct 21;55(2):301–308. doi: 10.1016/0092-8674(88)90053-0. [DOI] [PubMed] [Google Scholar]
  69. Veillette A., Fournel M. The CD4 associated tyrosine protein kinase p56lck is positively regulated through its site of autophosphorylation. Oncogene. 1990 Oct;5(10):1455–1462. [PubMed] [Google Scholar]
  70. Veillette A., Horak I. D., Horak E. M., Bookman M. A., Bolen J. B. Alterations of the lymphocyte-specific protein tyrosine kinase (p56lck) during T-cell activation. Mol Cell Biol. 1988 Oct;8(10):4353–4361. doi: 10.1128/mcb.8.10.4353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Waldmann T. A. The multi-subunit interleukin-2 receptor. Annu Rev Biochem. 1989;58:875–911. doi: 10.1146/annurev.bi.58.070189.004303. [DOI] [PubMed] [Google Scholar]
  72. Wang J. Y. Isolation of antibodies for phosphotyrosine by immunization with a v-abl oncogene-encoded protein. Mol Cell Biol. 1985 Dec;5(12):3640–3643. doi: 10.1128/mcb.5.12.3640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Weissman A. M., Harford J. B., Svetlik P. B., Leonard W. L., Depper J. M., Waldmann T. A., Greene W. C., Klausner R. D. Only high-affinity receptors for interleukin 2 mediate internalization of ligand. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1463–1466. doi: 10.1073/pnas.83.5.1463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Yamanashi Y., Kakiuchi T., Mizuguchi J., Yamamoto T., Toyoshima K. Association of B cell antigen receptor with protein tyrosine kinase Lyn. Science. 1991 Jan 11;251(4990):192–194. doi: 10.1126/science.1702903. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES