Activation of STAT6 is not dependent on phosphotyrosine-mediated docking to the interleukin-4 receptor and can be blocked by dominant-negative mutants of both receptor subunits

European Journal of Biochemistry

Volumn 251, Issue 1-2, 1998, Pages 25-35

  Moriggl, Richard ^a   Erhardt, Ingrid ^b   Kammer, Winfried ^b   Berchtold, Susanne ^a   Schnarr, Bernd ^b   Lischke, Antje ^b   Groner, Bernd ^a   Friedrich, Karlheinz ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Cytokine receptor; Janus kinase signal transducer and activator of the transcription (JAK STAT) pathway; Signal transduction; Transcription factor; Tyrosine phosphorylation

Indexed keywords

CYTOKINE RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; PHOSPHOTYROSINE; TRANSCRIPTION FACTOR;

ARTICLE; CELL NUCLEUS; GENE CONTROL; GENETIC TRANSCRIPTION; HUMAN CELL; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

EID: 0032518431     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1998.2510025.x     Document Type: Article

References (60)

1. Paul, W. E. (1991) Interleukin-4: a prototypic immunoregulatory cytokine, Blood 77, 1859-1870.
2. Idzerda, R. L., March, C. J., Mosley, B., Lyman, S. D., Bos, T. V., Gimpel, S. D., Din, W. S., Grabstein, K. H., Widmer, M. B., Park, L. S., Cosman, D. & Beckman, M. P. (1990) Human interleukin 4 receptor confers biological responsiveness and defines a novel receptor superfamily, J. Exp. Med. 171, 861-973.
3. Russell, S. M., Keegan, A. D., Harada, N., Nakamura, Y., Noguchi, M., Leland, P., Friedman, M. C., Miyajima, A., Puri, R. K., Paul, W. E. & Leonard, W. J. (1993) Interleukin-2 receptor γ chain: A functional component of the interleukin-4 receptor, Science 262, 1880-1883.
4. Kondo, M., Takeshita, T., Ishii, N., Nakamura, M., Watanabe, S., Arai, K. & Sugamura, K. (1993) Sharing of the interleukin-2 (IL-2) receptor γ chain between receptors for IL-2 and IL-4, Science 262, 1874-1877.
5. Bazan, J. F. (1990) Haemopoietic receptors and helical cytokines, Immunol. Today 11, 350-354.
6. Duschl, A. & Sebald, W. (1996) Transmembrane and intracellular signalling by interleukin-4: Receptor dimerization and beyond, Eur. Cytokine Netw. 7, 37-49.
7. Russell, S. M., Johnston, J. A., Noguchi, M., Kawamura, M., Bacon, C. M., Friedmann, M., Berg, M., McVicar, D. W., Witthuhn, B. A., Silvennoinen, O., Goldman, A. S., Schmalstieg, F. C., Ihle, I. N., O'Shea, J. J. & Leonard, W. J. (1994) Interactions of IL-2Rβ and γc chain with jak1 and jak3: Implications for XSCID and XCID, Science 266, 1042-1045.
8. Miyazaki, T., Kawahara, A., Fujii, H., Nakagawa, Y., Minami, Y., Liu, Z.-J., Oishi, I., Silvennoinen, O., Witthuhn, B. A., Ihle, J. N. & Taniguchi, T. (1994) Functional activation of jak1 and jak3 by selective association with IL-2 receptor subunits, Science 266, 1045-1047.
9. Wang, L.-M., Keegan, A. D., Paul, W. E., Heidaran, M. A., Gutkind, S. & Pierce, J. H. (1992) IL-4 activates a distinct signal transduction cascade from factor-dependent myeloid cells, EMBO J. 11, 4899-4908.
10. Sun, X. J., Wang, L.-M., Zhang, Y., Yenush, L., Myers, M. G. Jr, Glasheen, L., Lane, W. S., Pierce, J. H. & White, M. F. (1995) Role of IRS-2 in insulin and cytokine signalling, Nature 377, 173-177.
11. Ihle, J. N. & Kerr, I. M. (1995) Jaks and Stats in signalling by the cytokine receptor superfamily, Trends Genet. 11, 69-74.
12. Schindler, C., Shuai, K., Prezioso, V. R. & Darnell, J. E. (1992) Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor, Science 257, 4215-4218.
13. Fu, X.-Y. (1992) A transcription factor with SH2 and SH3 domains is directly activated by an interferon α-induced cytoplasmic protein tyrosine kinase(s), Cell 70, 323-335.
14. Velazquez, L., Fellous, M., Stark, G. R. & Pellegrini, S. (1992) A protein tyrosine kinase in the interferon α/β signaling pathway, Cell 70, 313-322.
15. Schindler, C. & Darnell, J. E. (1995) Transcriptional responses to polypeptide ligands: The Jak-Stat pathway, Annu. Rev. Biochem. 64, 621-651.
16. Köhler, I. & Rieber, E. P. (1993) Allergy-associated Iε and Fcε receptor II (CD23b) genes activated via binding of an interleukin-4-induced transcription factor to a novel responsive element, Eur. J. Immunol. 23, 3066-3071.
17. Kotanides, H. & Reich, N. C. (1993) Requirement of tyrosine phosphorylation for rapid activation of a DNA binding factor by IL-4, Science 262, 1265-1267.
18. Schindler, C., Kashleva, H., Pernis, A., Pine, R. & Rothman, P. (1994) STF-IL-4: a novel IL-4-induced signal transducing factor, EMBO J. 13, 1350-1356.
19. Köhler, I., Alliger, P., Minty, A., Caput, D., Ferrara, P., Hoell-Neugebauer, B., Rank, G. & Rieber, P. (1994) Human interleukin-13 activates the interleukin-4-dependent transcription factor NF-IL-4 sharing a DNA binding motif with an interferon-γ-induced nuclear binding factor, FEBS Lett. 345, 187-192.
20. Ryan, J. J., McReynolds, L. J., Keegan, A., Wang, L.-H., Garfein, E., Rothman, P., Nelms, K. & Paul, W. E. (1996) Growth and gene expression are predominantly controlled by distinct regions of the human IL-4 receptor, Immunity 4, 123-132.
21. Hou, J., Schindler, U., Henzel, W. J., Ho, T. C., Brasseur, M. & McKnight, S. L. (1994) An interleukin-4-induced transcription factor: IL-4 Stat, Science 265, 1701-1706.
22. Quelle, F. W., Shimoda, K., Thierfelder, W., Fischer, C., Kim, A., Ruben, S. M., Cleveland, J. L., Pierce, J. H., Keegan, A. D., Nelms, K., Paul, W. E. & Ihle, J. N. (1995) Cloning of murine Stat6 and human Stat6, Stat proteins that are tyrosine phosphorylated in responses to IL-4 and IL-3 but are not required for mitogenesis, Mol. Cell. Biol. 15, 3336-3343.
23. Takeda, K., Tanaka, T., Shi, W., Matsamuto, M., Minami, M., Kashiwamura, S.-I., Nakanishi, K., Yoshida, N., Kishimoto, T. & Akira, S. (1996) Essential role of Stat6 in IL-4 signalling, Nature 380, 627-630.
24. Kaplan, M. H., Schindler, U., Smiley, S. T. & Grusby, M. J. (1996) Stat6 is required for mediating responses to IL-4 and for the development of Th2 cells, Immunity 4, 313-319.
25. Shimoda, K., Deursen, J., Sangster, M. Y., Sarawar, S. R., Carson, R. T., Tripp, R. A., Chu, C., Quelle, F. W., Nosaka, T., Vignali, D. A. A., Doherty, P. C., Grosveld, G., Paul, W. E. & Ihle, J. N. (1996) Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene, Nature 380, 630-633.
26. Kopf, M., LeGros, G., Bachmann, M., Lamers, M. C., Bluethmann, H. & Koehler, G. (1993) Disruption of the murine IL-4 gene blocks Th2 cytokine responses, Nature 362, 245-248.
27. Seidel, H. M., Milocco, L. H., Lamb, P., Darnell, J. E., Stein, R. B., & Rosen, J. (1995) Spacing of palindromic half sites as a determinant of selective Stat (signal transducers and activators of transcription) DNA binding and transcriptional activity, Proc. Natl Acad. Sci. USA 92, 3041-3045.
28. Ivashkiv, L. B. (1995) Cytokines and STATs: How can signals achieve specificity? Immunity 3, 1-4.
29. Mikita, T., Campbell, D., Wu, P., Williamson, K., & Schindler, U. (1996) Requirements for interleukin-4-induced gene expression and functional characterization of Stat6, Mol. Cell. Biol. 16, 5811-5820.
30. Stahl, N., Farruggella, T. J., Boulton, T. G., Zhong, Z., Darnell, J. E. & Yancopoulos, G. D. (1995) Choice of Stats and other substrates specified by modular tyrosine-based motifs in cytokine receptors, Science 267, 1349-1353.
31. Heim, M. H., Kerr, I. M., Stark, G. R. & Darnell, J. E. (1995) Contribution of Stat SH2 groups to specific interferon signaling by the Jak-Stat pathway, Science 267, 1347-1349.
32. Schindler, U., Wu, P., Rothe, M., Brasseur, M. & McKnight, S. L. (1995) Components of a Stat recognition code: Evidence for two layers of molecular selectivity, Immunity 2, 689-697.
33. Mui, A. L.-F., Wakao, H., O'Farrell, A.-M., Harada, N. & Miyajima, A. (1995) Interleukin-3, granulocyte-macrophage colony stimulating factor and interleukin-5 transduce signals through two Stat5 homologs, EMBO J. 14, 1116-1175.
34. Sotiropoulos, A., Moutoussamy, S., Binart, N., Kelly, P. A. & Finidori, J. (1995) The membrane proximal region of the cytoplasmic domain of the growth hormone receptor is involved in the activation of Stat3, FEBS Lett. 369, 169-172.
35. Pernis, A., Witthuhn, B., Keegan, A. D., Nelms, K., Garfein, E., Ihle, J. N., Paul, W. E., Pierce, J. H. & Rothman, P. (1995) Interleukin 4 signals through two related pathways, Proc. Natl Acad. Sci. USA 92, 7971-7975.
36. Fujitani, Y., Hibi, M., Fukada, T., Takahashi-Tezuka, M., Yoshida, H., Yamaguchi, T., Sugiyama, K., Yamanaka, Y., Nakajima, K. & Hirano, T. (1997) An alternative pathway for STAT activation that is mediated by the direct interaction between JAK and STAT, Oncogene 14, 751-761.
37. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn, Cold Spring Harbor Laboratory, Cold Spring Harbor NY.
38. Kreis, T. E. & Lodish, H. F. (1986) Oligomerization is essential for transport of Vesicular Stomatitis viral glycoprotein to the cell surface, Cell 46, 929-937.
39. Lischke, A., Kammer, W. & Friedrich, K. (1995) Different human interleukin-4 mutants preferentially activate human or murine common receptor γ chain, Eur. J. Biochem. 234, 100-107.
40. Kammer, W., Lischke, A., Moriggl, R., Groner, B., Ziemiecki, A., Gurniak, C. B., Berg, L. J. & Friedrich, K. (1996) Homodimerization of interleukin-4 receptor α chain can induce intracellular signaling, J. Biol. Chem. 271, 23634-23637.
41. Moriggl, R., Berchtold, S., Friedrich, K., Standke, G. J. R., Kammer, W., Heim, M., Wissler, M., Stöcklin, E., Gouilleux, F. & Groner, B. (1997) Comparison of the transactivation domains of Stat5 and Stat6 in lymphoid cells and mammary epithelial cells, Mol. Cell. Biol. 17, 3663-3678.
42. Wakao, H., Gouilleux, F. & Groner, B. (1994) Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the PRL response, EMBO J. 13, 2182-2191.
43. Bönsch, D., Kammer, W., Lischke, A. & Friedrich, K. (1995) Species-specific agonist/antagonist activities of human interleukin-4 variants suggest distinct ligand binding properties of human and murine common receptor γ chain, J. Biol. Chem. 270, 8452-8457.
44. Moriggl, R., Gouilleux-Gruart, V., Jähne, R., Gartmann, C., Liu, X., Hennighausen, L., Sotiropoulos, A., Groner, B. & Gouilleux, F. (1996) Deletion of the carboxyl-terminal transactivation domain of MGF-Stat5 results in sustained DNA binding and a dominant negative phenotype, Mol. Cell. Biol. 16, 5691-5700.
45. Wakao, H., Schmidt-Ney, M. & Groner, B. (1992) Mammary gland-specific nuclear factor is present in lactating rodent and bovine mammary tissue and composed of a single polypeptide of 89 kDa, J. Biol. Chem. 267, 16 365-16 370.
46. Delphin, S. & Stavnezer, J. (1995) Characterization of an interleukin 4 (IL-4) responsive region in the immunoglobulin heavy chain germline ε promoter: Regulation by NF-IL-4, a C/EBP family member and NF-κB/p50, J. Exp. Med 181, 181-192.
47. Harada, N., Yang, G., Miyajima, A. & Howard, M. (1992) Identification of an essential region for growth signal transduction in the cytoplasmic domain of the human interleukin-4 receptor, J. Biol. Chem. 267, 22752-22758.
48. Vita, N., Lefort, S., Laurent, P., Caput, D. & Ferrara, P. (1995) Characterization and comparison of the interleukin-13 receptor with the interleukin-4 receptor on several cell types, J. Biol. Chem. 270, 3512-3517.
49. DaSilva, L., Zack Howard, O. M., Rui, H., Kirken, R. A. & Farrar, W. L. (1994) Growth signaling and JAK2 association mediated by membrane-proximal cytoplasmic regions of prolactin receptors, J. Biol. Chem. 269, 18 267-18 270.
50. Lai, S. Y., Molden, J., Liu, K. D., Puck, J. M., White, M. D. & Goldsmith, M. A. (1996) Interleukin-4 specific signal transduction events are driven by homotyptc interactions of the interleukin-4 receptor α subunit, EMBO J. 15, 4506-4514.
51. Izuhara, K., Heike, T., Otsuka, T., Yamaoka, K., Mayumi, M., Imamura, T., Niho, Y. & Harada, N. (1996) Signal transduction pathway of interleukin-4 and interleukin-13 in human B cells derived from X-linked severe combined immunodeficiency patients, J. Biol. Chem. 271, 619-622.
52. Russell, S. M., Tayebi, N., Nikajima, H., Riedy, M. C., Roberts, J. L., Aman, M. J., Migone, T.-S., Noguchi, M., Marken, M. L., Buckley, R. H., O'Shea, J. J. & Leonard, W. J. (1995) Mutation of jak3 in a patient with SCID: Essential role of jak3 in lymphoid development, Science 270, 297-800.
53. Greenlund, A. C., Morales, M. O., Viviano, B. L., Yan, H., Krolewski, J. & Schreiber, R. D. (1995) Stat recruitment by tyrosine-phosphorylated cytokine receptors: An ordered reversible affinity-driven process, Immunity 2, 677-687.
54. Keegan, A. D., Nelms, K., White, M., Wang, L.-M., Pierce, J. H. & Paul, W. E. (1994) An IL-4 receptor region containing an insulin receptor motif is important for IL-4-mediated IRS-1 phosphorylation and cell growth, Cell 76, 811-820.
55. Wang, H. Y., Paul, W. E. & Keogan, A. D. (1996) IL-4 function can be transferred to the IL-2 receptor by tyrosine containing sequences found in the IL-4 receptor α chain, Immunity 4, 113-121.
56. Greenlund, A. C., Farrar, M. A., Viviano, B. L. & Schreiber, R. (1994) Ligand-induced IFN γ receptor tyrosine phosphorylation couples the receptor to its signal transduction system (p91), EMBO J. 13, 1591-1600.
57. Farrar, M. A., Campbell, J. D. & Schreiber, R. D. (1992) Identification of a functionally important sequence in the C terminus of the interferon-γ receptor, Proc. Natl Acad. Sci. USA 89, 11 706-11 710.
58. Ruff-Jamison, S., Chen, K. & Cohen, S. (1995) Epidermal growth factor induces the tyrosine phosphorylation and nuclear translocation of Stat5 in mouse liver, Proc. Natl Acad. Sci. USA 92, 4215-4218.
59. Chen, J., Sadowski, H. B., Kohanski, R. A. & Wang, L.-H. (1997) Stat5 is a physiological substrate of the insulin receptor, Proc. Natl Acad. Sci. USA 94, 2295-2300.
60. Patel, B. K. R., Wang, L.-M., Lee, C.-C., Taylor, W. G., Pierce, J. H. & LaRochelle, W. J. (1996) Stat6 and jak1 are common elements in platelet-derived growth factor and interleukin-4 signal transduction pathways in NIH 3T3 fibroblasts, J. Biol. Chem. 271, 22 175-22 182.