Requirement for distinct Janus kinases and STAT proteins in T cell proliferation versus IFN-γ, production following IL-12 stimulation

Journal of Immunology

Volumn 161, Issue 11, 1998, Pages 5893-5900

  Ahn, Hyun Jong ^a   Tomura, Michio ^a   Yu, Wen Gong ^a   Iwasaki, Masayuki ^a   Park, Woong Ryeon ^a   Hamaoka, Toshiyuki ^a   Fujiwara, Hiromi ^a  

^a OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 2; MESSENGER RNA; PROTEIN; PROTEIN TYROSINE KINASE; STAT4 PROTEIN; STAT5 PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE;

ANIMALS; CELL LINE; CLONE CELLS; DNA-BINDING PROTEINS; INTERFERON TYPE II; INTERLEUKIN-12; INTERLEUKIN-2; JANUS KINASE 2; LYMPHOCYTE ACTIVATION; MICE; MILK PROTEINS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTEINS; PROTO-ONCOGENE PROTEINS; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-12; RECOMBINANT PROTEINS; STAT3 TRANSCRIPTION FACTOR; STAT4 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, HELPER-INDUCER; TRANS-ACTIVATORS; TYK2 KINASE; TYROSINE;

EID: 0032400981     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (46)

1. Trinchieri, G. 1994. Interleukin-12: a cytokine produced by antigen-presenting cells with immunoregulatory functions in the generation of T-helper cells type 1 and cytotoxic lymphocytes. Blood 84:4008.
2. Brunda, M. J. 1994. Interleukin-12. J. Leukocyte Biol. 55:280.
3. Kobayashi, M., L. Fitz, M. Ryan, R. M. Hewick, S. C. Clark, S. Chan, R. Loudon, F. Sherman, B. Perussia, and G. Trinchieri. 1989. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J. Exp. Med. 170:827.
4. Chan, S. H., B. Perussia, J. W. Gupta, M. Kobayashi, M. Pospisil, H. A. Young, S. F. Wolf, D. Young, S. C. Clark, and G. Trinchieri. 1991. Induction of interferon γ production by natural killer cell stimulatory factor: characterization of the responder cells and synergy with other inducers. J. Exp. Med. 173:869.
5. Robertson, M. J., R. J. Soiffer, S. F. Wolf, T. J. Manley, C. Donahue, D. Young, S. H. Herrmann, and J. Ritz. 1992. Response of human natural killer (NK) cells to NK cell stimulatory factor (NKSF): cytolytic activity and proliferation of NK cells are differentially regulated by NKSF. J. Exp. Med. 175:779.
6. Gately, M. K., B. B. Desai, A. G. Wolitzky, P. M. Quinn, C. M. Dwyer, F. J. Podlaski, P. C. Familletti, F. Sinigaglia, R. Chizonnite, U. Gubler, and A. S. Stern. 1991. Regulation of human lymphocyte proliferation by a heterodimeric cytokine, IL-12 (cytotoxic lymphocyte maturation factor). J. Immunol. 147:874.
7. Stern, A. S., F. J. Podlaski, J. D. Hulmes, Y. C. Pan, P. M. Quinn, A. G. Wolitzky, P. C. Familletti, D. L. Stremlo, T. Truitt, R. Chizzonite, and M. K. Gately. 1990. Purification to homogeneity and partial characterization of cytotoxic lymphocyte maturation factor from human B-lymphoblastoid cells. Proc. Natl. Acad. Sci. USA 87:6808.
8. Manetti, R., P. Parronchi, M. G. Giudizi, M. P. Piccinni, E. Maggi, G. Trinchieri, and S. Romagnani. 1993. Natural killer cell stimulatory factor (interleukin 12 (IL-12)) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. J. Exp. Med. 177:1199.
9. Guler, M. L., J. D. Gorham, C. S. Hsieh, A. J. Mackey, R. G. Steen, W. F. Dietrich, and K. M. Murphy. 1996. Genetic susceptibility to Leishmania: IL-12 responsiveness in TH1 cell development. Science 271:984.
10. Presky, D. H., H. Yang, L. J. Minetti, A. O. Chua, N. Nabavi, C. Y. Wu, M. K. Gately, and U. Gubler. 1996. A functional interleukin 12 receptor complex is composed of two β-type cytokine receptor subunits. Proc. Natl. Acad. Sci. USA 93:14002.
11. Ihle, J. N. 1995. The Janus protein tyrosine kinases in hematopoietic cytokine signaling. Semin. Immunol. 7:247.
12. Johnston, J. A., C. M. Bacon, M. C. Riedy, and J. J. O'Shea. 1996. Signaling by IL-2 and related cytokines: JAKs, STATs, and relationship to immunodeficiency. J. Leukoc. Biol. 60:441.
13. Bacon, C. M., D. W. McVicar, J. R. Ortaldo, R. C. Rees, J. J. O'Shea, and J. A. Johnston. 1995. Interleukin 12 (IL-12) induces tyrosine phosphorylation of JAK2 and TYK2: differential use of Janus family tyrosine kinases by IL-2 and IL-12. J. Exp. Med. 181:399.
14. Schindler, C., and J. Darnell Jr. 1995. Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 64:621.
15. Ihle, J. N., B. A. Witthuhn, F. W. Quelle, K. Yamamoto, and O. Silvennoinen. 1995. Signaling through the hematopoietic cytokine receptors. Annu. Rev. Immunol. 13:369.
16. Bacon, C. M., E. F. Petricoin III, J. R. Ortaldo, R. C. Rees, A. C. Larner, J. A. Johnston, and J. J. O'Shea. 1995. Interleukin 12 induces tyrosine phosphorylation and activation of STAT4 in human lymphocytes. Proc. Natl. Acad. Sci. USA 92:7307.
17. Jacobson, N. G., S. J. Szabo, R. M. Weber-Nordt, Z. Zhong, R. D. Schreiber, J. Darnell Jr., and K. M. Murphy. 1995. Interleukin 12 signaling in T helper type 1 (Th1) cells involves tyrosine phosphorylation of signal transducer and activator of transcription (Stat)3 and Stat4. J. Exp. Med. 181:1755.
18. Velazquez, L., M. Fellous, G. R. Stark, and S. Pellegrini. 1992. A protein tyrosine kinase in the interferon α/β signaling pathway. Cell 70:313.
19. Watling, D., D. Guschin, M. Muller, O. Silvennoinen, B. A. Witthuhn, F. W. Quelle, N. C. Rogers, C. Schindler, G. R. Stark, J. N. Ihle, and I. M. Kerr. 1993. Complementation by the protein tyrosine kinase JAK2 of a mutant cell line defective in the interferon-γ signal transduction pathway. Nature 366:166.
20. Stahl, N., T. G. Boulton, T. Farruggella, N. Y. Ip, S. Davis, B. A. Witthuhn, F. W. Quelle, O. Silvennoinen, G. Barbieri, S. Pellegrini, J. N. Ihle, and G. D. Yancopoulos. 1994. Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 β receptor components. Science 263:92.
21. Silvennoinen, O., B. A. Witthuhn, F. W. Quelle, J. L. Cleveland, T. Yi, and J. N. Ihle. 1993. Structure of the murine Jak2 protein-tyrosine kinase and its role in interleukin 3 signal transduction. Proc. Natl. Acad. Sci. USA 90:8429.
22. Quelle, F. W., N. Sato, B. A. Witthuhn, R. C. Inhorn, M. Eder, A. Miyajima, J. D. Griffin, and J. N. Ihle. 1994. JAK2 associates with the βc chain of the receptor for granulocyte-macrophage colony-stimulating factor, and its activation requires the membrane-proximal region. Mol. Cell. Biol. 14:4335.
23. Maruo, S., H. J. Ahn, W. G. Yu, M. Tomura, M. Wysocka, N. Yamamoto, M. Kobayashi, T. Hamaoka, G. Trinchieri, and H. Fuijiwara. 1997. Establishment of an IL-12-responsive T cell clone: its characterization and utilization in the quantitation of IL-12 activity. J. Leukocyte Biol. 61:346.
24. Chua, A. O., V. L. Wilkinson, D. H. Presky, and U. Gubler. 1995. Cloning and characterization of a mouse IL-12 receptor-β component. J. Immunol. 155:4286.
25. Marchuk, D., M. Drumm, A. Saulino, and F. S. Collins. 1991. Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Res. 19:1154.
26. Wilson, K. C., and D. S. Finbloom. 1992. Interferon γ rapidly induces in human monocytes a DNA-binding factor that recognizes the γ response region within the promoter of the gene for the high-affinity Fc γ receptor. Proc. Natl. Acad. Sci. USA 89:11964.
27. Masuda, E. S., H. Tokumitsu, A. Tsuboi, J. Shlomai, P. Hung, K. Arai, and N. Arai. 1993. The granulocyte-macrophage colony-stimulating factor promoter cis-acting element CLEO mediates induction signals in T cells and is recognized by factors related to AP1 and NFAT. Mol. Cell. Biol. 13:7399.
28. Mui, A. L., H. Wakao, A. M. O'Farrell, N. Harada, and A. Miyajima. 1995. Interleukin-3, granulocyte-macrophage colony stimulating factor and interleukin-5 transduce signals through two STAT5 homologs. EMBO J. 14:1166.
29. Yamamoto, K., F. W. Quelle, W. E. Thierfelder, B. L. Kreider, D. J. Gilbert, N. A. Jenkins, N. G. Copeland, O. Silvennoinen, and J. N. Ihle. 1994. Stat4, a novel γ interferon activation site-binding protein expressed in early myeloid differentiation. Mol. Cell. Biol. 14:4342.
30. 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 Jak-3 Janus kinase in response to interleukin-2. Nature 370:151.
31. Ahn, H. J., S. Maruo, M. Tomura, J. Mu, T. Hamaoka, K. Nakanishi, S. Clark, M. Kurimoto, H. Okamura, and H. Fujiwara. 1997. A mechanism underlying synergy between IL-12 and IFN-γ-inducing factor in enhanced production of IFN-γ. J. Immunol. 159:2125.
32. Cho, S. S., C. M. Bacon, C. Sudarshan, R. C. Rees, D. Finbloom, R. Pine, and J. J. O'Shea. 1996. Activation of STAT4 by IL-12 and IFN-α: evidence for the involvement of ligand-induced tyrosine and serine phosphorylation. J. Immunol. 157:4781.
33. 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.
34. Hou, J., U. Schindler, W. J. Henzel, S. C. Wong, and S. L. McKnight. 1995. Identification and purification of human Stat proteins activated in response to interleukin-2. Immunity 2:321.
35. Mui, A. L., H. Wakao, T. Kinoshita, T. Kitamura, and A. Miyajima. 1996. Suppression of interleukin-3-induced gene expression by a C-terminal truncated Stat5: role of Stat5 in proliferation. EMBO J. 15:2425.
36. Szabo, S. J., N. G. Jacobson, A. S. Dighe, U. Gubler, and K. M. Murphy. 1995. Developmental commitment to the Th2 lineage by extinction of IL-12 signaling. Immunity 2:665.
37. Gollob, J. A., H. Kawasaki, and J. Ritz. 1997. Interferon-γ and interleukin-4 regulate T cell interleukin-12 responsiveness through the differential modulation of high-affinity interleukin-12 receptor expression. Eur. J. Immunol. 27:647.
38. Szabo, S. J., A. S. Dighe, U. Gubler, and K. M. Murphy. 1997. Regulation of the interleukin (IL)-12R 02 subunit expression in developing T helper 1 (Th1) and Th2 cells. J. Exp. Med. 185:817.
39. Rogge, L., L. Barberis-Maino, M. Biffi, N. Passini, D. H. Presky, U. Gubler, and F. Sinigaglia. 1997. Selective expression of an interleukin-12 receptor component by human T helper 1 cells. J. Exp. Med. 185:825.
40. Galbiati, F., L. Rogge, J. C. Guery, S. Smiroldo, and L. Adorini. 1998. Regulation of the IL-12 receptor β2 subunit by soluble antigen and IL-12 in vivo. Eur. J. Immunol. 28:209.
41. Kaplan, M. H., Y. L. Sun, T. Hoey, and M. J. Grusby. 1996. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382:174.
42. Thierfelder, W. E., J. M. van-Deursen, K. Yamamoto, R. A. Tripp, S. R. Sarawar, R. T. Carson, M. Y. Sangster, D. A. Vignali, P. C. Doherty, G. C. Grosveld, and J. N. Ihle. 1996. Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature 382:171.
43. Desai, B. B., P. M. Quinn, A. G. Wolitzky, P. K. Mongini, R. Chizzonite, and M. K. Gately. 1992. IL-12 receptor. II. Distribution and regulation of receptor expression. J. Immunol. 148:3125.
44. Wakao, H., N. Harada, T. Kitamura, A. L. Mui, and A. Miyajima. 1995. Interleukin 2 and erythropoietin activate STAT5/MGF via distinct pathways. EMBO J. 14:2527.
45. Azam, M., H. Erdjument-Bromage, B. L. Kreider, M. Xia, F. Quelle, R. Basu, C. Saris, P. Tempst, J. N. Ihle, and C. Schindler. 1995. Interleukin-3 signals through multiple isoforms of Stat5. EMBO J. 14:1402.
46. Friedmann, M. C., T. S. Migone, S. M. Russell, and W. J. Leonard. 1996. Different interleukin 2 receptor β-chain tyrosines couple to at least two signaling pathways and synergistically mediate interleukin 2-induced proliferation. Proc. Natl. Acad. Sci. USA 93:2077. 1