The IL-4 Receptor α-Chain Cytoplasmic Domain Is Sufficient for Activation of JAK-1 and STAT6 and the Induction of IL-4-Specific Gene Expression

Journal of Immunology

Volumn 158, Issue 12, 1997, Pages 5860-5867

  Reichel, Martin ^a   Nelson, Brad H ^b,c,d   Greenberg, Philip D ^b,c   Rothman, Paul B ^a,e  

^a The New York Presbyterian Hospital   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d BENAROYA RESEARCH INSTITUTE   (United States)

^e Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; INTERLEUKIN RECEPTOR; JAK1 PROTEIN, HUMAN; JAK3 PROTEIN, HUMAN; JANUS KINASE 1; JANUS KINASE 3; LEUKOCYTE ANTIGEN; PROTEIN TYROSINE KINASE; STAT6 PROTEIN; STAT6 PROTEIN, HUMAN; STEM CELL FACTOR RECEPTOR; TRANSACTIVATOR PROTEIN; TYROSINE;

ARTICLE; CELL CULTURE; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANTIGENS, CD; BASE SEQUENCE; CELLS, CULTURED; ENZYME ACTIVATION; GENE EXPRESSION; HUMANS; INTERLEUKIN-4; JANUS KINASE 1; JANUS KINASE 3; LYMPHOCYTE ACTIVATION; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-4; SIGNAL TRANSDUCTION; STAT6 TRANSCRIPTION FACTOR; T-LYMPHOCYTES; TRANS-ACTIVATORS; TYROSINE;

EID: 0031570471     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (49)

1. de Vos, A., M. Ultsch, and A. A. Kossiakoff. 1992. Human growth hormone and extracellular domain of its receptor: crystal structure of the complex. Science 255:306.
2. Davis, S., T. H. Aldrich, N. Stahl, L. Pan, T. Taga, T. Kishimoto, N. Y. Ip, and G. D. Yancopoulos. 1993. LIFRβ and gp130 as heterodimerizing signal transducers of the tripartite CNTF receptor. Science 260:1805.
3. Bach, E. A., J. W. Tanner, S. Marsters, A. Ashkenazi, M. Aguet, A. S. Shaw, and R. D. Schreiber. 1996. Ligand-induced assembly and activation of the gamma interferon receptor in intact cells. Mol. Cell. Biol. 16:3214.
4. Lowenthal, J. W., B. E. Castle, J. Christiansen, J. Schreurs, D. Rennick, N. Arai, Y. Takebe, and M. Howard. 1988. Expression of high affinity receptors for murine interleukin 4 (BSF-1) on hemopoietic and nonhemopoietic cells. J. Immunol. 140:456.
5. Russell, S. M., A. D. Keegan, N. Harada, Y. Nakamura, M. Noguchi, P. Leland, M. C. Friedmann, A. Maiyajima, R. K. Puri, W. E. Paul, and W. J. Leonard. 1993. Interleukin-2 receptor γ chain: a functional component of the interleukin-4 receptor. Science 262:1880.
6. Hou, J., U. Schindler, W. Henzel, T. C. Ho, M. Brasseur, and S. L. McKnight. 1994. An interleukin-4 induced transcription factor: IL-4 Stat. Science 265: 1701.
7. Quelle, F., K. Shimoda, W. Thierfelder, C. Fisher, A. Kim, S. Ruben, J. Cleveland, J. Pierce, A. Keegan, K. Nelms, W. Paul, and J. Ihle. 1995. Cloning of murine Stat6 and human Stat6, Stat proteins that are tyrosine phosphorylated in response to IL-4 and IL-3 but are not required for mitogenesis. Mol. Cell. Biol. 15:3336.
8. Schindler, C., H. Kashleva, A. Pernis, R. Pine, and P. Rothman. 1994. STF-IL-4: a novel IL-4-induced signal transducing factor. EMBO J. 13:1350.
9. Schindler, U., P. Wu, M. Rothe, M. Brasseur, and S. L. McKnight. 1995. Components of a Stat recognition code: evidence for two layers of molecular selectivity. Immunity 2:689.
10. Kondo, M., T. Takeshita, N. Ishii, M. Nakamura, S. Watanabe, K.-I. Arai, and K. Sugamura. 1993. Sharing of the interleukin-2 (IL-2) receptor γ chain between receptors for IL-2 and IL-4. Science 262:1874.
11. c chains with Jak1 and Jak3: implications for XSCID and XCID. Science 266:1042.
12. Miyazaki, T., A. Kawahara, H. Fujii, Y. Nakagawa, Y. Minami, Z.-J. Liu, I. Oishi, O. Silvennoinen, B. A. Witthuhn, J. N. Ihle, and T. Taniguchi. 1994. Functional activation of Jak1 and Jak3 by selective association with IL-2 receptor subunits. Science 266:1045.
13. Johnston, J. A., M. Kawamura, R. A. Kirken, Y.-Q. Chen, T. B. Blake, K. Shibuya, J. R. Ortaldo, D. W. McVicar, and J. J. O'Shea. 1994. Phosphorylation and activation of the JAK3 Janus kinase in response to IL-2. Nature 370: 151.
14. 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.
15. Yin, T., M. L. Tsang, and T. C. Yang. 1994. JAK1 kinase forms complexes with interleukin-4 receptor and 4PS/insulin receptor substrate-1-like protein and is activated by interleukin-4 and interleukin-9 in T lymphocytes. J. Biol. Chem. 269:26614.
16. Schindler, C., and J. E. Darnell. 1995. Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 64:621.
17. Izuhara, K., R. A. Feldman, P. Greer, and N. Harada. 1994. Interaction of the c-fes proto-oncogene product with the interleukin-4 receptor. J. Biol. Chem. 269: 18623.
18. Miyazaki, T., Z. J. Liu, A. Kawahara, Y. Minami, K. Yamada, Y. Tsujimoto, E. L. Barsoumian, R. M. Perlmutter, 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.
19. Xu, M. Z., and J. Stavnezer. 1992. Regulation of transcription of immunoglobulin germ-line gamma 1 RNA: analysis of the promoter/enhancer. EMBO J. 11:145.
20. Kotanides, H., and N. C. Reich. 1993. Requirement of tyrosine phosphorylation for rapid activation of a DNA binding factor by IL-4. Science 262:1265.
21. Delphin, S., and J. Stavnezer. 1995. Characterization of an interleukin 4 (IL-4) responsive region in the immunoglobulin heavy chain germline ∈ promoter: regulation by NF-IL4, a C/EBP family member and NF-kB/p50. J. Exp. Med. 181: 181.
22. Kohler, I., and E. Rieber. 1993. Allergy-associated I∈ AND Fc∈ receptor II (CD23b) genes activated via binding of an interleukin-4-induced transcription factor to a novel responsive element. Eur. J. Immunol. 23:3066.
23. Kaplan, M. H., U. Schindler, S. T. Smiley, and M. J. Grusby. 1996. Stat6 is required for mediating responses to IL-4 and for the development of Th2 cells. Immunity 4:313.
24. Takeda, K., T. Tanaka, W. Shi, M. Matsumoto, M. Minami, S.-I. Kashiwamura, K. Nakanishi, N. Yoshida, T. Kishimoto, and S. Akira. 1996. Essential role of Stat6 in IL-4 signalling. Nature 380:627.
25. Shimoda, K., J. van Deursen, M. Y. Sangster, S. R. Sarawar, R. T. Carson, R. A. Tripp, C. Chu, F. W. Quelle, T. Nosaka, D. A. A. Vignali, P. C. Doherty, G. Grosveld, W. E. Paul, and J. N. Ihle. 1996. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380:630.
26. Wang, H. Y., W. E. Paul, and A. D. Keegan. 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.
27. Ryan, J. J., L. J. McReynolds, A. Keegan, L.-H. Wang, E. Garfein, P. Rothman, K. Nelms, and W. E. Paul. 1996. Growth and gene expression are predominantly controlled by distinct regions of the human IL-4 receptor. Immunity 4:123.
28. Lin, J.-X., T.-S. Migone, M. Tsang, M. Friedmann, J. A. Weatherbee, L. Zhou, A. Yamauchi, E. T. Bloom, J. Mietz, S. John, and W. J. Leonard. 1995. The role of shared receptor motifs and common Stat proteins in the generation of cytokine pleiotropy and redundancy by IL-2, IL-4, IL-7, IL-13, and IL-15. Immunity 2:331.
29. Takeshita, T., H. Asao, K. Ohtani, N. Ishii, S. Kumaki, N. Tanaka, H. Munakata, M. Nakamura, and K. Sugamura. 1992. Cloning of the γ chain of the human IL-2 receptor. Science 257:379.
30. de Wit, H., D. W. Hendriks, M. R. Halie, and E. Bellenga. 1994. Interleukin-4 receptor regulation in human monocytic cell lines. Blood 84:608.
31. c chain does not function as a subunit shared by the IL-4 and IL-13 receptors. J. Immunol. 155:9.
32. Matthews, D. J., P. A. Clark, J. Herbert, G. Morgan, R. J. Armitage, C. Kinnon, A. Minty, K. H. Grabstein, D. Caput, P. Ferrara, and R. Callard. 1995. Function of the interleukin-2 (IL-2) receptor γ-chain in biologic responses of X-linked severe combined immunodeficient B cells to IL-2, IL-4, IL-13, and IL-15. Blood 85:38.
33. Glimcher, L. H., T. Hamano, R. Asofsky, E. Heber-Katz, R. H. Schwartz, and W. E. Paul. 1982. I region-restricted antigen presentation by B cell-B lymphoma hybridomas. Nature 298:283.
34. Nelson, B. H., J. D. Lord, and P. D. Greenberg. 1994. Cytoplasmic domains of the interleukin-2 receptor β and γ chains mediate the signal for T-cell proliferation. Nature 369:333.
35. Loh, J. E., C. Schindler, A. Ziemiecki, A. G. Harpur, A. F. Wilks, and R. A. Flavell. 1994. Mutants cell lines unresponsive to alpha/beta and gamma interferon are defective in tyrosine phosphorylation of ISGF-3α components. Mol. Cell. Biol. 14:2170.
36. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51.
37. Schindler, C., K. Shuai, V. R. Prezioso, and J. E. Darnell. Jr. 1992. Interferon dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257:809.
38. Danial, N. N., A. Penis, and P. B. Rothman. 1995. Jak-Stat signaling induced by the v-abl oncogene. Science 269:1875.
39. Xu, L., and P. Rothman. 1994. IFN-γ represses ∈ germline transcription and subsequently down-regulates switch recombination to ∈. Int. Immunol. 6:515.
40. Lev, S., Y. Yarden, and D. Givol. 1992. Dimerization and activation of the kit receptor by monovalent and bivalent binding of the stem cell factor. J. Biol. Chem. 267:15970.
41. Nakamura, Y., S. M. Russell, S. A. Mess, M. Friedmann, M. Erdos, C. Francois, Y. Jacques, S. Adelstein, and W. J. Leonard. 1994. Heterodimerization of the IL-2 receptor β-and γ-chain cytoplasmic domains is required for signalling. Nature 369:330.
42. Keegan, A. D., K. Nelms, M. White, L. M. Wang, J. H. Pierce, and W. E. Paul. 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.
43. Kuhn, R., K. Rajewsky, and W. Muller. 1991. Generation and analysis of interleukin 4 deficient mice. Science 254:707.
44. Coffman, R. L., D. A. Lebman, and P. Rothman. 1993. Mechanism and regulation of immunoglobulin isotype switching. Adv. Immunol. 54:229.
45. Kawahara, A., Y. Minami, and T. Taniguchi. 1994. Evidence for a critical role for the cytoplasmic region of the interleukin 2 (IL-2) receptor γ chain in IL-2, IL-4, and IL-7 signalling. Mol. Cell. Biol. 14:5433.
46. Nosaka, T., J. M. A. van Deursen, R. A. Tripp, W. E. Thierfelder, 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.
47. Hilton, D. J., J.-G. Zhang, D. Metcalf, W. S. Alexander, N. A. Nicola, and T. A. Willson. 1996. Cloning and characterization of a binding subunit of the interleukin 13 receptor that is also a component of the interleukin 4 receptor. Proc. Natl. Acad. Sci. USA 93:497.
48. Kammer, W., A. Lischke, R. Moriggl, B. Groner, A. Ziemiecki, C. B. Gurniak, L. J. Berg, and K. Friedrich. 1996. Homodimerization of interleukin-4 receptor α chain can induce intracellular signaling. J. Biol. Chem. 271:23634.
49. Lai, S. Y., J. Molden, K. D. Liu, J. M. Puck, M. D. White, and M. A. Goldsmith. 1996. Interleukin-4-specific signal transduction events are driven by homotypic interactions of the interleukin-4 receptor α subunit. EMBO J. 15:4506.