TNF-α induces tyrosine phosphorylation and recruitment of the Src homology protein-tyrosine phosphatase 2 to the gp130 signal-transducing subunit of the IL-6 receptor complex

Journal of Immunology

Volumn 171, Issue 1, 2003, Pages 257-266

  Bode, Johannes G ^a   Schweigart, Jens ^a   Kehrmann, Jan ^a   Ehlting, Christian ^a   Schaper, Fred ^b   Heinrich, Peter C ^b   Häussinger, Dieter ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 130; PROTEIN TYROSINE PHOSPHATASE; RECEPTOR SUBUNIT; STAT PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COMPLEX FORMATION; EFFECTOR CELL; ENZYME INDUCTION; EXON; IMMUNE RESPONSE; INFLAMMATORY CELL; MACROPHAGE ACTIVATION; MEDIATOR RELEASE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STIMULUS RESPONSE;

EID: 0037530607     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.1.257     Document Type: Article

References (55)

1. Bode, J. G., and P. C. Heinrich. 2001. Interleukin-6 signaling during the acute phase response of the liver. In The Liver: Biology and Pathobiology, 4th Ed. I. M. Arias, J. L. Boyer, N. Fausto, F. V. Chisari, H. Schachter, and D. A. Shafritz, eds. Lippincott Williams & Wilkins, Philadelphia, p. 565.
2. Heinrich, P. C., I. Behrmann, G. Müller-Newen, F. Schaper, and L. Graeve. 1998. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 334:297.
3. Gabay, C., and I. Kushner. 1999. Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 340:448.
4. Ramadori, G., and B. Christ. 1999. Cytokines and the hepatic acute-phase response. Semin. Liv. Dis. 19:141.
5. Barton, B. E. 1996. The biological effects of interleukin-6. Med. Res. Rev. 16:87.
6. Romano, M., M. Sironi, C. Toniatti, N. Polentarutti, P. Fruscella, P. Ghezzi, R. Faggioni, W. Luini, V. van Hinsbergh, S. Sozzani, et al. 1997. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 6:315.
7. Riedy, M. C., and C. C. Stewart. 1992. Inhibitory role of interleukin-6 in macrophage proliferation. J. Leukocyte Biol. 52:125.
8. Ulich, T. R., K. Z. Guo, D. Remick, J. del Castillo, and S. M. Yin. 1991. Endotoxin-induced cytokine gene expression in vivo. III. IL-6 mRNA and serum protein expression and the in vivo hematologic effects of IL-6. J. Immunol. 146:2316.
9. Oh, J. W., N. J. Van Wagoner, S. Rose-John, and E. N. Benveniste. 1998. Role of IL-6 and the soluble IL-6 receptor receptor in inhibition of VCAM-1 gene expression. J. Immunol. 161:4992.
10. Gatsios, P., H. D. Haubeck, E. Van de Leur, W. Frisch, S. S. Apte, H. Greiling, P. C. Heinrich, and L. Graeve. 1996. Oncostatin M differentially regulates tissue inhibitors of metalloproteinases TIMP-1 and TIMP-3 gene expression in human synovial lining cells. Eur. J. Biochem. 241:56.
11. Tilg, H., E. Trehu, M. B. Atkins, C. A. Dinarello, and J. W. Mier. 1994. Interleuki-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 83:113.
12. Tilg, H., E. Vannier, G. Vachino, C. A. Dinarello, and J. W. Mier. 1993. Anti-inflammatory properties of hepatic acute phase proteins: preferential induction of interleukin 1 IL-1 receptor antagonist over IL-1β synthesis by human peripheral blood mononuclear cells. J. Exp. Med. 178:1629.
13. Lütticken, C., U. M. Wegenka, J. Yuan, J. Buschmann, C. Schindler, A. Ziemiecki, A. G. Harpur, A. F. Wilks, K. Yasukawa, T. Taga, et al. 1994. Association of transcription factor APRF and protein kinase Jak 1 with the Interleukin-6 signal transducer gp 130. Science 263:89.
14. Stahl, N., T. G. Boulton, T. Farruggella, N. Y. Ip, S. Davis, B. A. Witthuhn, F. W. Quelle, O. Silvennoinen, G. Barbieri, S. Pellegrini, et al. 1994. Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 β receptor components. Science 263:92.
15. Stahl, N., T. J. Faruggella, T. G. Boulton, Z. Zhong, J. E. Darnell, Jr., and G. D. Yancopoulos. 1995. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 267:1349.
16. Heim, M. H., I. M. Kerr, G. R. Stark, and J. E. Darnell, Jr. 1995. Contribution of STAT SH2 groups to specific interferon signaling by the Jak-STAT pathway. Science 267:1347.
17. Hemmann, U., C. Gerhartz, B. Hessel, J. Sasse, G. Kurapkat, J. Grötzinger, Wollmer A., Z. Zhong, J. E. Darnell, Jr., L. Graeve, et al. 1996. Differential activation of acute phase response factor/Stat3 and Stat1 via the cytoplasmic domain of the interleukin 6 signal transducer gp130. II. Src homology SH2 domains define the specificity of Stat factor activation. J. Biol. Chem. 271:12999.
18. Zhong, Z., Z. Wen, and J. E. Damell, Jr. 1994. Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264:95.
19. Wegenka, U. M., J. Buschmann, C. Lütticken, P. C. Heinrich, and F. Horn. 1993. Acute-phase response factor, a nuclear factor binding to acute-phase response elements, is rapidly activated by interleukin-6 at the posttranslational level. Mol. Cell. Biol. 13:276.
20. Haspel, R. L., M. Salditt-Georgieff, and J. E. Darnell, Jr. 1996. The rapid inactivation of nuclear tyrosine phosphorylated Stat1 depends upon a protein tyrosine phosphatase. EMBO J. 15:6262.
21. Kim, T. K., and T. Maniatis. 1996. Regulation of interferon-γ-activated STAT1 by the ubiquitin-proteasome pathway. Science 273:1717.
22. Chung, C. D., J. Y. Liao, B. Liu, X. P. Rao, P. Jay, P. Berta, and K. Shuai. 1997. Specific inhibition of Stat3 signal transduction by PIAS3. Science 278:1803.
23. Liu, B., J. Y. Liao, X. P. Rao, S. A. Kushner, C. D. Chung, D. D. Chang, and K. Shuai. 1998. Inhibition of Stat1-mediated gene activation by PIAS1. Proc. Natl. Acad. Sci. USA 95:10626.
24. Starr, R., T. A. Willson, E. M. Viney, L. J. Murray, J. R. Rayner, B. J. Jenkins, T. J. Gonda, W. S. Alexander, D. Metcalf, N. A. Nicola, et al. 1997. A family of cytokine-inducible inhibitors of signalling. Nature 387:917.
25. Endo, T. A., M. Masuhara, M. Yokouchi, R. Suzuki, H. Sakamoto, K. Mitsui, A. Matsumoto, S. Tanimura, M. Ohtsubo, H. Misawa, et al. 1997. A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387:921.
26. Naka, T., M. Narazaki, M. Hirata, T. Matsumoto, S. Minamoto, A. Aono, N. Nishimoto, T. Kajita, T. Taga, K. Yoshizaki, et al. 1997. Structure and function of a new STAT-induced STAT inhibitor. Nature 387:924.
27. Fukada, T., M. Hibi, Y. Yamanaka, M. Takahashitezuka, Y. Fujitani, T. Yamaguchi, K. Nakajima, and T. Hirano. 1996. Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: involvement of STAT3 in anti-apoptosis. Immunity 5:449.
28. Kim, H. K., T. S. Hawley, R. G. Hawley, and H. Baumann. 1998. Protein tyrosine phosphatase 2 (SHP2) moderates signaling by gp130 but is not required for the induction of acute-phase plasma protein genes in hepatic cell. Mol. Cell. Biol. 18:1525.
29. Symes, A., N. Stahl, S. A. Reeves, T. Farruggella, T. Servidei, T. Gearan, G. Yancopoulos, and J. S. Fink. 1997. The protein tyrosine phosphatase SHP-2 negatively regulates ciliary neurotrophic factor induction of gene expression. Curr. Biol. 7:697.
30. Schaper, F., C. Gendo, M. Eck, J. Schmitz, C. Grimm, D. Anhuf, I. M. Kerr, and P. C. Heinrich. 1998. Activation of SHP2 via the IL-6 signal transducing receptor protein gp130 requires JAK1 and limits acute-phase protein expression. Biochem. J. 335:557.
31. Bode, J. G., A. Nimmesgem, J. Schmitz, F. Schaper, M. Schmitt, W. Frisch, D. Häussinger, P. C. Heinrich, and L. Graeve. 1999. LPS and TNFα induce SOCS3 mRNA and inhibit IL-6-induced activation of STAT3 in macrophages. FEBS Lett. 463:365.
32. Stoiber, D., P. Kovarik, S. Cohney, J. A. Johnston, P. Steinlein, and T. Decker. 1999. Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-γ. J. Immunol. 163:2640.
33. Lehmann, U., J. Schmitz, M. Weissenbach, R. M. Sobota, M. Hortner, K. Friederichs, I. Behrmann, W. Tsiaris, A. Sasaki, J. Schneider-Mergener, et al. 2003. SHP2 and SOCS3 contribute to Y759-dependent attenuation of IL-6-signaling through gp130. J. Biol. Chem. 278:661.
34. Weiergräber, O., U. Hemmann, A. Küster, G. Müller-Newen, J. Schneider, S. Rose-John, P. Kurschat, J. P. J. Brakenhoff, M. H. L. Hart, S. Stabel, et al. 1995. Soluble human interleukin-6 receptor: expression in insect cells, purification and characterization. Eur. J. Biochem. 234:661.
35. Oh, E. S., H. Gu, T. M. Saxton, J. F. Timms, S. Hausdorff, E. U. Frevert, B. B. Kahn, T. Pawson, B. G. Neel, and S. M. Thomas. 1999. Regulation of early events in integrin signaling by protein tyrosine phosphatase SHP-2. Mol. Cell. Biol. 19:3205.
36. Andrews, N. C., and D. V. Faller. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19:2499.
37. Ludwig, S., A. Hoffmeyer, M. Goebler, K. Kilian, H. Häfner, B. Neufeld, H. Jiahuai, and U. R. Rapp. 1998. The stress inducer arsenite activates mitogen-activated protein kinases extracellular signal-regulated kinases 1 and 2 via a MAPK kinase 6/p38-dependent pathway. J. Biol. Chem. 273:1917.
38. Flory, E., A. Hoffmeyer, U. Smola, U. R. Rapp, and J. T. Bruder. 1996. Raf-1 kinase targets GA-binding protein in transcriptional regulation of the human immunodeficiency virus type 1 promoter. J. Virol. 70:2260.
39. Schmitz, J., M. Weissenbach, S. Haan, P. C. Heinrich, and F. Schaper. 2000. SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J. Biol. Chem. 275:12848.
40. Wagner, B. J., T. E. Hayes, C. J. Hoban, and B. H. Cochran. 1990. The SIF binding element confers sis/PDGF inducibility onto the c-fos promoter. EMBO J. 9:4477.
41. Nicholson, S. E., D. De Souza, L. J. Fabri, J. Corbin, T. A. Willson, J. G. Zhang, A. Silva, M. Asimakis, A. Farley, A. D. Nash, et al. 2000. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc. Natl. Acad. Sci. USA 97:6493.
42. Ahmed, S. T., and L. B. Ivashkiv. 2000. Inhibition of IL-6 and IL-10 signaling and STAT activation by inflammatory and stress pathways. J. Immunol. 165:5227.
43. Ahmed, S. T., A. Mayer, J. D. Ji, and L. B. Ivashkiv. 2002. Inhibition of IL-6 signaling by a p38-dependent pathway occurs in the absence of new protein synthesis. J. Leukocyte Biol. 72:154.
44. Pearson, G., F. Robinson, T. B. Gibson, B. E. Xu, M. Karandikar, K. Berman, and M. H. Cobb. 2001. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22:153.
45. Li, J., M. Gorospe, D. Hutter, J. Barnes, S. M. Keyse, and Y. Liu. 2001. Transcriptional induction of MKP-1 in response to stress is associated with histone H3 phosphorylation-acetylation. Mol. Cell. Biol. 21:8213.
46. Bokemeyer, D., A. Sorokin, M. Yan, N. G. Ahn, D. J. Templeton, and M. J. Dunn. 1996. Induction of mitogen-activated protein kinase phosphatase 1 by the stress-activated protein kinase signaling pathway but not by extracellular signal-regulated kinase in fibroblasts. J. Biol. Chem. 271:639.
47. Schliess, F., S. Heinrich, and D. Haussinger. 1998. Hyperosmotic induction of the mitogen-activated protein kinase phosphatase MKP-1 in H411E rat hepatoma cells Arch. Biochem. Biophys. 351:35.
48. Deon, D., S. Ahmed, K. Tai, N. Scaletta, C. Herrero, I. H. Lee, A. Krause, and L. B. Ivashkiv. 2001. Cross-talk between IL-1 and IL-6 signaling pathways in rheumatoid arthritis synovial fibroblasts. J. Immunol. 167:5395.
49. Andus, T., T. Geiger, T. Hirano, T. Kishimoto, and P. C. Heinrich. 1988. Action of recombinant human interleukin 6, interleukin 1β and tumor necrosis factor α on the mRNA induction of acute-phase proteins. Eur. J. Immunol. 18:739.
50. Zhang, Z., and G. M. Fuller. 2001. Interleukin 1β inhibits interleukin 6-mediated rat γ fibrinogen gene expression. Blood 96:3466.
51. 2-macroglobulin expression is due to activation of NF-κB. J. Immunol. 167:1469.
52. Bode, J. G., S. Ludwig, C. A. Correia Freitas, F. Schaper, M. Ruhl, S. Melmed, P. C. Heinrich, and D. Häussinger. 2001. The MKK6/p38 mitogen activated protein kinase pathway is capable to induce SOCS3 gene expression and inhibits IL-6-induced gene induction. Biol. Chem. 382:1447.
53. Han, J., J. D. Lee, L. Bibbs, and R. J. Ulevitch. 1994. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265:808.
54. Takahashi-Tezuka, M., Y. Yoshida, T. Fukada, T. Ohtani, Y. Yamanaka, K. Nishida, K. Nakajima, M. Hibi, and T. Hirano. 1998. Gab1 acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase. Mol. Cell. Biol. 18:4109.
55. Ernst, M., M. Inglese, P. Waring, I. K. Campbell, S. Bao, F. J. Clay, W. S. Alexander, I. P. Wicks, D. M. Tarlinton, U. Novak, et al. 2001. Defective gp130-mediated signal transducer and activator of transcription (STAT) signaling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J. Exp. Med. 194:189.