Hierarchy of protein tyrosine kinases in interleukin-2 (IL-2) signaling: Activation of Syk depends on Jak3; however, neither Syk nor Lck is required for IL-2-mediated STAT activation

Molecular and Cellular Biology

Volumn 20, Issue 12, 2000, Pages 4371-4380

  Zhou, Yong Jie ^a   Magnuson, Kelly S ^b   Cheng, Tammy P ^c   Gadina, Massimo ^a   Frucht, David M ^a   Galon, Jerome ^a   Candotti, Fabio ^d   Geahlen, Robert L ^e   Changelian, Paul S ^b   O'Shea, John J ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b PFIZER INC   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^e PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 2; PHOSPHOTRANSFERASE; PROTEIN TYROSINE KINASE; STAT PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; ENZYME PRECURSORS; HUMANS; INTERLEUKIN-2; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JANUS KINASE 3; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MILK PROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RECEPTORS, INTERLEUKIN-2; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS;

ANIMALIA;

EID: 0034088346     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.12.4371-4380.2000     Document Type: Article

References (55)

1. Beadling, C., D. Guschin, B. A. Witthuhn, A. Ziemiecki, J. N. Ihle, I. M. Kerr, and D. A. Cantrell. 1944. Activation of JAK kinases and STAT proteins by interleukin-2 and interferon alpha, but not the T cell antigen receptor, in human T lymphocytes. EMBO J. 13:5605-5615.
2. Chaturvedi, P., M. V. Reddy, and E. P. Reddy. 1998. Src kinases and not JAKs activate STATs during IL-3 induced myeloid cell proliferation. Oncogene 16:1749-1758.
3. Chen, M., A. Cheng, Y. Q. Chen, A. Hymel, E. P. Hanson, L. Kimmel, Y. Minami, T. Taniguchi, P. S. Changelian, and J. J. O'Shea. 1997. The amino terminus of JAK3 is necessary and sufficient for binding to the common gamma chain and confers the ability to transmit interleukin 2-mediated signals. Proc. Natl. Acad. Sci. USA 94:6910-6915.
4. Darnell, J. E., Jr., I. M. Kerr, and G. R. Stark. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415-1421.
5. Darnell, J. E., Jr. 1997. STATs and gene regulation. Science 277:1630-1635.
6. Evans, G. A., M. A. Goldsmith, J. A. Johnston, W. Xu, S. R. Weiler, R. Erwin, O. M. Howard, R. T. Abraham, J. J. O'Shea, W. C. Greene, et al. 1995. Analysis of interleukin-2-dependent signal transduction through the Shc/ Grb2 adapter pathway. Interleukin-2-dependent mitogenesis does not require Shc phosphorylation or receptor association. J. Biol. Chem. 270:28858-28863.
7. Friedmann, M. C., T. S. Migone, S. M. Russell, and W. J. Leonard. 1996. Different interleukin 2 receptor beta-chain tyrosines couple to at least two signaling pathways and synergistically mediate interleukin 2-induced proliferation. Proc. Natl. Acad. Sci. USA 93:2077-2082.
8. Fujii, H., K. Ogasawara, H. Otsuka, M. Suzuki, K. Yamamura, T. Yokochi, T. Miyazaki, H. Suzuki, T. W. Mak, S. Taki, and T. Taniguchi. 1998. Functional dissection of the cytoplasmic subregions of the IL-2 receptor beta chain in primary lymphocyte populations. EMBO J. 17:6551-6557.
9. Gonzalez-Garcia, A., I. Merida, C. Martinez-A, and A. C. Carrera. 1997. Intermediate affinity interleukin-2 receptor mediates survival via a phosphatidylinositol 3-kinase-dependent pathway. J. Biol. Chem. 272:10220-10226.
10. Hanke, J. H., J. P. Gardner, R. L. Dow, P. S. Changelian, W. H. Brissette, E. J. Weringer, B. A. Pollok, and P. A. Connelly. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and Fyn T-dependent T cell activation. J. Biol. Chem. 271:695-701.
11. Hatakeyama, M., T. Kono, N. Kobayashi, A. Kawahara, S. D. Levin, R. M. Perlmutter, and T. Taniguchi. 1991. Interaction of the IL-2 receptor with the src-family kinase p56lck: identification of novel intermolecular association. Science 252:1523-1528.
12. Hatakeyama, M., A. Kawahara, H. Mori, H. Shibuya, and T. Taniguchi. 1992. C-fos gene induction by interleukin 2: identification of the critical cytoplasmic regions within the interleukin 2 receptor beta chain. Proc. Natl. Acad. Sci. USA 89:2022-2026.
13. Horak, I. D., R. E. Gress, P. J. Lucas, E. M. Horak, T. A. Waldmann, and J. B. Bolen. 1991. T-lymphocyte interleukin 2-dependent tyrosine protein kinase signal transduction involves the activation of p56lck. Proc. Natl. Acad. Sci. USA 88:1996-2000.
14. Ihle, J. N. 1995. Cytokine receptor signalling. Nature 377:591-594.
15. Ihle, J. N. 1996. STATs: signal transducers and activators of transcription. Cell 84:331-334.
16. Johnston, J. A., M. Kawamura, R. A. Kirken, Y. Q. Chen, T. H. Blake, K. Shibuya, J. R. Ortaldo, D. W. McVicar, and J. J. O'Shea. 1994. Phosphorylation and activation of the Jak-3 Janus kinase in response to interleukin-2. Nature 370:151-153.
17. Johnston, J. A., L. M. Wang, E. P. Hanson, X. J. Sun, M. F. White, S. A. Oakes, J. H. Pierce, and J. J. O'Shea. 1995. Interleukins 2, 4, 7, and 15 stimulate tyrosine phosphorylation of insulin receptor substrates 1 and 2 in T cells. Potential role of JAK kinases. J. Biol. Chem. 270:28527-28530.
18. Johnston, J. A., C. M. Bacon, D. S. Finbloom, R. C. Rees, D. Kaplan, K. Shibuya, J. R. Ortaldo, S. Gupta, Y. Q. Chen, J. D. Giri, et al. 1995. Tyrosine phosphorylation and activation of STAT5, STAT3, and Janus kinases by interleukins 2 and 15. Proc. Natl. Acad. Sci. USA 92:8705-8709.
19. lck deficiency on the growth and cytolytic effector function of an interleukin-2-dependent cytotoxic T-cell line. Mol. Cell. Biol. 12:4521-4530.
20. Kawahara, A., Y. Minami, T. Miyazaki, J. N. Ihle, and T. Taniguchi. 1995. Critical role of the inlerteukin 2 (IL-2) receptor gamma-chain-associated Jak3 in the IL-2-induced c-fos and c-myc, but not bcl-2, gene induction. Proc. Natl. Acad. Sci. USA 92:8724-8728.
21. Kawamura, M., D. W. McVicar, J. A. Johnston, T. B. Blake, Y. Q. Chen, B. K. Lal, A. R. Lloyd, D. J. Kelvin, J. E. Staples, J. R. Ortaldo, et al. 1994. Molecular cloning of L-JAK, a Janus family protein-tyrosine kinase expressed in natural killer cells and activated leukocytes. Proc. Natl. Acad. Sci. USA 91:6374-6378.
22. Leonard, W. J. 1999. Type I cytokines, interferons and their receptors, p. 741-774. In W. E. Paul (ed.), Fundamental immunology, 4th ed. Lippincott-Raven Publisher, Philadelphia, Pa.
23. Leonard, W. J., and J. J. O'Shea. 1998. Jaks and STATs: biological implications. Annu. Rev. Immunol. 16:293-322.
24. Liu, K. D., S. L. Gaffen, M. A. Goldsmith, and W. C. Greene. 1997. Janus kinases in interleukin-2-mediated signaling: JAK1 and JAK3 are differentially regulated by tyrosine phosphorylation. Curr. Biol. 7:817-826.
25. Lord, J. D., B. C. McIntosh, P. D. Greenberg, and B. H. Nelson. 1998. The IL-2 receptor promotes proliferation, bcl-2 and bcl-x induction, but not cell viability through the adapter molecule Shc. J. Immunol. 161:4627-4633.
26. lck. J. Virol. 71:6677-6682.
27. Macchi, P., A. Villa, S. Gillani, M. G. Sacco, A. Frattini, F. Porta, A. G. Ugazio, J. A. Johnston, F. Candotti, J. J. O'Shea, et al. 1995. Mutations of Jak-3 gene in patients with autosomal severe combined immune deficiency (SCID). Nature 377:65-68.
28. Minami, Y., T. Kono, K. Yamada, N. Kobayashi, A. Kawahara, R. M. Perlmutter, and T. Taniguchi. 1993. Association of p56lck with IL-2 receptor beta chain is critical for the IL-2-induced activation of p56lck. EMBO J. 12:759-768.
29. Minami, Y., I. Oishi, Z. J. Liu, S. Nakagawa, T. Miyazaki, and T. Taniguchi. 1994. Signal transduction mediated by the reconstituted IL-2 receptor. Evidence for a cell type-specific function of IL-2 receptor beta-chain. J. Immunol. 152:5680-5690.
30. Minami, Y., Y. Nakagawa, A. Kawahara, T. Miyazaki, K. Sada, H. Yamamura, and T. Taniguchi. 1995. Protein tyrosine kinase Syk is associated with and activated by the IL-2 receptor: possible link with the c-myc induction pathway. Immunity 2:89-100.
31. Miyazaki, T., A. Kawahara, H. Fujii, Y. Nakagawa, Y. Minami, Z. J. Liu, I. Oishi, O. Silvennoinen, B. A. Witthuhn, J. N. Ihle, et al. 1994. Functional activation of Jak1 and Jak3 by selective association with IL-2 receptor subunits. Science 266:1045-1047.
32. Miyazaki, T., Z. J. Liu, A. Kawahara, Y. Minami, K. Yamada, Y. Tsujimoto, E. L. Barsoumian, R. M. Permutter, and T. Taniguchi. 1995. Three distinct IL-2 signaling pathways mediated by bcl-2, c-myc, and lck cooperate in hematopoietic cell proliferation. Cell 81:223-231.
33. Molina, T. J., K. Kishihara, D. P. Siderovski, W. van Ewijt, A. Narendran, E. Timms, A. Wakeham, C. J. Paige, K. U. Hartmann, and A. Veillette, et al. 1992. Profound block in thymocyte development in mice lacking p56lck. Nature 357:161-164.
34. Nelson, B. H., B. C. McIntosh, L. L. Rosencrans, and P. D. Greenberg. 1997. Requirement for an initial signal from the membrane-proximal region of the interleukin 2 receptor gamma(c) chain for Janus kinase activation leading to T cell proliferation. Proc. Natl. Acad. Sci. USA 94:1878-1883.
35. Noguchi, M., H. Yi, H. M. Rosenblatt A. H. Filipovich, S. Adelstein, W. S. Modi, O. W. McBride, and W. J. Leonard. 1993. Interleukin-2 receptor gamma chain mutation results in X-linked severe combined immunodeficiency in humans. Cell 73:147-157.
36. Nosaka, T., J. M. Van Deursen, R. A. Tripp, W. E. Thieifelder, B. A. Witthuhn, A. P. McMickle, P. C. Doherty, G. C. Grosveld, and J. N. Ihle. 1995. Defective lymphoid development in mice lacking Jak3. Science 270: 800-802.
37. Oakes, S. A., F. Candotti, J. A. Johnston, Y. Q. Chen, J. J. Ryan, N. Taylor, X. Liu, L. Hennighausen, L. D. Notarangelo, W. E. Paul, R. M. Blaese, and J. J. O'Shea. 1996. Signaling via IL-2 and IL-4 in JAK3-deficient severe combined immunodeficiency lymphocytes: JAK3-dependent and independent pathways. Immunity 5:605-615.
38. O'Shea, J. J. 1997. Jaks, STATs, cytokine signal transduction, and immunoregulation: are we there yet? Immunity 7:1-11.
39. Qin, S., T. Inazu, C. Yang, K. Sada, T. Taniguchi, and H. Yamamura. 1994. Interleukin 2 mediates p72syk activation in peripheral blood lymphocytes. FEBS Lett. 345:233-236.
40. Ravichandran, K. S., V. Igras, S. E. Shoelson, S. W. Fesik, and S. J. Burakoff. 1996. Evidence for a role for the phosphotyrosine-binding domain of Shc in interleukin 2 signaling. Proc. Natl. Acad. Sci. USA 93:5275-5280.
41. Rodig, S. J., M. A. Meraz, J. M. White, P. A. Lampe, J. K. Riley, C. D. Arthur, K. L. King, K. C. Sheehan, L. Yin, D. Pennica, E. M. J. Johnson, and R. D. Schreiber. 1998. Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses. Cell 93:373-383.
42. Russell, S. M., J. A. Johnston, M. Noguchi, M. Kawamura, C. M. Bacon, M. Friedmann, M. Berg, D. W. McVicar, B. A. Witthuhn, O. Silvennoinen, et al. 1994. Interaction of IL-2R beta and gamma c chains with Jak1 and Jak3: implications for XSCID and XCID. Science 266:1042-1045.
43. Russell, S. M., N. Tayebi, H. Nakajima, M. C. Riedy, J. L. Roberts, M. J. Aman, T. S. Migone, M. Noguchi, M. L. Markert, R. H. Buckley, et al. 1995. Mutation of Jak3 in a patient with SCID: essential role of Jak3 in lymphoid development. Science 270:797-800.
44. Satoh, T., Y. Minami, T. Kono, K. Yamada, A. Kawahara, T. Taniguchi, and Y. Kaziro. 1992. Interleukin 2-induced activation of Ras requires two domains of interleukin 2 receptor beta subunit, the essential region for growth stimulation and Lck-binding domain. J. Biol. Chem. 267:25423-25427.
45. Shibuya, H., M. Yoneyama, J. Ninomiya-Tsuji, K. Matsumoto, and T. Taniguchi. 1992. IL-2 and EGF receptors stimulate the hematopoietic cell cycle via different signaling pathways: demonstration of a novel role for c-myc. Cell 70:57-67.
46. Taniguchi, T. 1995. Cytokine signaling through nonreceptor protein tyrosine kinases. Science 268:251-255.
47. Thomis, D. C., C. B. Gurniak, E. Tivol, A. H. Sharpe, and L. J. Berg. 1995. Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3. Science 270:794-797.
48. Turner, M., P. J. Mee, P. S. Costello, O. Williams, A. A. Price, L. P. Duddy, M. T. Furlong, R. L. Geahlen, and V. L. Tybulewicz. 1995. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 378:298-302.
49. Van Oers, N. S., and A. Weiss. 1995. The Syk/ZAP-70 protein tyrosine kinase connection to antigen receptor signalling processes. Semin. Immunol, 7:227-236
50. Weite, T., D. Leitenberg, B. N. Dittel, B. K. al-Ramadi, B. Xie, Y. E. Chin, C. A. J. Janeway, A. L. M. Bothwell, K. Bottomly, and X. Y. Fu. 1999. STAT5 interaction with the T cell receptor complex and stimulation of T cell proliferation. Science 283:222-225.
51. Witthuhn, B. A., O. Silvennoinen, O. Miura, K. S. Lai, C. Cwik, E. T. Liu, and J. N. Ihle. 1994. Involvement of the Jak-3 Janus kinase in signalling by interleukins 2 and 4 in lymphoid and myeloid cells. Nature 370:153-157.
52. Witthuhn, B. A., M. D. Williams, H. Kerawalla, and F. M. Uckun. 1999. Differential substrate recognition capabilities of Janus family protein tyrosine kinases within the interleukin 2 receptor (IL2R) system: Jak3 as a potential molecular target for treatment of leukemias with a hyperactive Jak-Stat signaling machinery. Leuk. Lymphoma 32:289-297.
53. Yu, C. L., R. Jove, and S. J. Burakoff. 1997. Constitutive activation of the Janus kinase-STAT pathway in T lymphoma overexpressing the Lck protein tyrosine kinase. J. Immunol. 159:5206-5210.
54. Zhou, Y. J., E. P. Hanson, Y. Q. Chen, K. Magnuson, M. Chen, P. G. Swann, R. L. Wange, P. S. Changelian, and J. J. O'Shea. 1997. Distinct tyrosine phosphorylation sites in JAK3 kinase domain positively and negatively regulate its enzymatic activity. Proc. Natl. Acad. Sci. USA 94:13850-13855.
55. Zhu, M. H., J. A. Berry, S. M. Russell, and W. J. Leonard. 1998. Delineation of the regions of interleukin-2 (IL-2) receptor beta chain important for association of Jak1 and Jak3. Jak1-independent functional recruitment of Jak3 to II-2Rbeta. J. Biol. Chem. 273:10719-10725.