The role of the inhibitors of interleukin-6 signal transduction SHP2 and SOCS3 for desensitization of interleukin-6 signalling

Biochemical Journal

Volumn 378, Issue 2, 2004, Pages 449-460

  Fischer, Patrick ^a   Lehmann, Ute ^a   Sobota, Radoslaw M ^a   Schmitz, Jochen ^a   Niemand, Claudia ^a   Linnemann, Sonja ^a   Haan, Serge ^a   Behrmann, Iris ^a   Yoshimura, Akihiko ^b   Johnston, James A ^c   Müller Newen, Gerhard ^a   Heinrich, Peter C ^a   Schaper, Fred ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b KYUSHU UNIVERSITY   (Japan)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Inflammation; Interleukin 6; Signal transducer and activator of transcription 3 (STAT3); Signal transduction; Src homology domain 2 containing protein tyrosine phosphatase (SHP2); Suppressor of cytokine signalling 3 (SOCS3)

Indexed keywords

BIODEGRADATION; CELLS; ENZYME INHIBITION;

GLYCOPROTEINS; SIGNAL TRANSDUCTION;

ENZYMES;

INTERLEUKIN 6; PROTEIN TYROSINE PHOSPHATASE SHP 2; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DESENSITIZATION; EMBRYO; EXPERIMENTAL DESIGN; FIBROBLAST; HEPATOMA CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD; CARRIER PROTEINS; CELL LINE; CYTOKINE RECEPTOR GP130; DNA-BINDING PROTEINS; DOWN-REGULATION; HUMANS; INTERLEUKIN-6; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JANUS KINASE 1; KINETICS; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; PROTEIN-TYROSINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; RECEPTORS, INTERLEUKIN-6; REPRESSOR PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TYROSINE;

ANIMALIA;

EID: 12144290834     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20030893     Document Type: Article

References (47)

1. Andus, T., Geiger, T., Hirano, T., Northoff, H., Ganter, U., Bauer, J., Kishimoto, T. and Heinrich, P. C. (1987) Recombinant human B cell stimulatory factor 2 (BSF-2/IFN-beta 2) regulates beta-fibrinogen and albumin mRNA levels in Fao-9 cells. FEBS Lett. 221, 18-22
2. Gauldie, J., Richards, C., Harnish, D., Lansdorp, P. and Baumann, H. (1987) Interferon beta 2/B-cell stimulatory factor type 2 shares identity with monocyte-derived hepatocyte-stimulating factor and regulates the major acute phase protein response in liver cells. Proc. Natl. Acad. Sci. U.S.A. 84, 7251-7255
3. Andus, T., Geiger, T., Hirano, T., Kishimoto, T. and Heinrich, P. C. (1988) Action of recombinant human interleukin 6, interleukin 1 beta and tumor necrosis factor alpha on the mRNA induction of acute-phase proteins. Eur. J. Immunol. 18, 739-746
4. Kopf, M., Baumann, H., Freer, G., Freudenberg, M., Lamers, M., Kishimoto, T., Zinkernagel, R., Bluethmann, H. and Köhler, G. (1994) Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature (London) 368, 339-342
5. Heinrich, P. C., Behrmann, I., Müller-Newen, G., Schaper, F. and Graeve, L. (1998) Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 334, 297-314
6. Murakami, M., Hibi, M., Nakagawa, N., Nakagawa, T., Yasukawa, K., Yamanishi, K., Taga, T. and Kishimoto, T. (1993) IL-6-induced homodimerization of gp130 and associated activation of a tyrosine kinase. Science 260, 1808-1810
7. Yamasaki, K., Taga, T., Hirata, Y., Yawata, H., Kawanishi, Y., Seed, B., Taniguchi, T., Hilano, T. and Kishimoto, T. (1988) Cloning and expression of the human interleukin-6 (BSF-2/IFN beta 2) receptor. Science 241, 825-828
8. Boulanger, M. J., Chow, D. C., Ḃrevnova, E. E. and Garcia, K. C. (2003) Hexameric structure and assembly of the interleukin-6/IL-6 alpha-receptor/gp130 complex. Science 300, 2101-2104
9. Lütticken, C., Wegenka, U. M., Yuan, J., Buschmann, J., Schindler, C., Ziemiecki, A., Haipur, A. G., Wilks, A. F., Yasukawa, K., Taga, T. et al. (1994) Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science 263, 89-92
10. Stahl, N., Boulton, T. G., Farruggella, T., Ip, N. Y., Davis, S., Witthuhn, B. A., Quelle, F. W., Silvennoinen, O., Barbieri, G., Pellegrini, S. et al. (1994) Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 beta receptor components. Science 263, 92-95
11. Stahl, N., Farruggella, T. J., Boulton, T. G., Zhong, Z., Darnell, J. E. and Yancopoulos, G. D. (1995) Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 267, 1349-1353
12. Gerhartz, C., Heesel, B., Sasse, J., Hemmann, U., Landgraf, C., Schneider-Mergener, J., Horn, F., Heinrich, P. C. and Graeve, L. (1996) Differential activation of acute phase response factor/STAT3 and STAT1 via the cytoplasmic domain of the interleukin 6 signal transducer gp130.1. Definition of a novel phosphotyrosine motif mediating STAT1 activation. J. Biol. Chem. 271, 12991-12998
13. Wegenka, U. M., Buschmann, J., Lütticken, C., Heinrich, P. C. and Horn, F. (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, 276-288
14. Zhong, Z., Wen, Z. and Darnell, Jr, J. E. (1994) Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264, 95-98
15. Heinrich, P. C., Behrmann, I., Haan, S., Hermanns, H. M., Müller-Newen, G. and Schaper, F. (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 374, 1-20
16. Inagaki-Ohara, K., Hanada, T. and Yoshimura, A. (2003) Negative regulation of cytokine signaling and inflammatory diseases. Curr. Opin. Pharmacol. 3, 435-442
17. Gerhartz, C., Dittrich, E., Stoyan, T., Rose-John, S., Yasukawa, K., Heinrich, P. C. and Graeve, L. (1994) Biosynthesis and half-life of the interleukin-6 receptor and its signal transducer gp130. Eur. J. Biochem. 223, 265-274
18. Graeve, L., Korolenko, T. A., Hemmann, U., Weiergraber, O., Dittrich, E. and Heinrich, P. C. (1996) A complex of the soluble interleukin-6 receptor and interleukin-6 is internalized via the signal transducer gp130. FEBS Lett. 399, 131-134
19. Thiel, S., Behrmann, I., Dittrich, E., Muys, L., Tavernier, J., Wijdenes, J., Heinrich, P. C. and Graeve, L. (1998) Internalization of the interleukin 6 signal transducer gp130 does not require activation of the Jak/STAT pathway. Biochem. J. 330, 47-54
20. Schaper, F., Gendo, C., Eck, M., Schmitz, J., Grimm, C., Anhuf, D., Kerr, I. M. and Heinrich, P. C. (1998) Activation of the protein tyrosine phosphatase SHP2 via the interleukin-6 signal transducing receptor protein gp130 requires tyrosine kinase Jak1 and limits acute-phase protein expression. Biochem. J. 335, 557-565
21. Kim, H. K., Hawley, T. S., Hawley, R. G. and Baumann, H. (1998) Protein tyrosine phosphatase 2 (SHP-2) moderates signaling by gp130 but is not required for the induction of acute-phase plasma protein genes in hepatic cells. Mol. Cell. Biol. 18, 1525-1533
22. Lehmann, U., Schmitz, J., Weissenbach, M., Sobota, R. M., Hörtner, M., Friederichs, K., Behrmann, I., Tsiaris, W., Sasaki, A., Schneider-Mergener, J. et al. (2003) SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J. Biol. Chem. 278, 661-671
23. Schmitz, J., Weissenbach, M., Haan, S., Heinrich, P. C. and Schaper, F. (2000) SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J. Biol. Chem. 275, 12848-12856
24. Nicholson, S. E., De Souza, D., Fabri, L. J., Corbin, J., Willson, T. A., Zhang, J. G., Silva, A., Asimakis, M., Farley, A., Nash, A. D. 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. U.S.A. 97, 6493-6498
25. Yasukawa, H., Ohishi, M., Mori, H., Murakami, M., Chinen, T., Aki, D., Hanada, T., Takeda, K., Akira, S., Hoshijima, M. et al. (2003) IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat. Immunol. 4, 551-556
26. Lang, R., Pauleau, A. L., Parganas, E., Takahashi, Y., Mages, J., Ihle, J. N., Rutschman, R. and Murray, P. J. (2003) SOCS3 regulates the plasticity of gp130 signaling. Nat. Immunol. 4, 546-550
27. Croker, B. A., Krebs, D. L., Zhang, J. G., Wormald, S., Willson, T. A., Stanley E. G., Robb, L., Greenhalgh, C. J., Forster, I., Clausen, B. E. et al. (2003) SOCS3 negatively regulates IL-6 signaling in vivo. Nat. Immunol. 4, 540-545
28. Chung, C. D., Liao, J. Y., Liu, B., Rao, X. P., Jay, P., Berta, P. and Shuai, K. (1997) Specific inhibition of Stat3 signal transduction by PIAS3. Science 278, 1803-1805
29. Liu, B., Liao, J. Y., Rao, X. P., Kushner, S. A., Chung, C. D., Chang, D. D. and Shuai, K. (1998) Inhibition of Stat1-mediated gene activation by PIAS1. Proc. Natl. Acad. Sci. U.S.A. 95, 10626-10631
30. Kim, T. K. and Maniatis, T. (1996) Regulation of interferon-gamma- activated STAT1 by the ubiquitin-proteasome pathway. Science 273, 1717-1719
31. Haspel, R. L., Salditt-Georgieff, M. and Darnell, J. J. E. (1996) The rapid inactivation of nuclear tyrosine phosphorylated Stat1 depends upon a protein tyrosine phosphatase. EMBO J. 15, 6262-6268
32. ten Hoeve, J., de Jesus Ibarra-Sanchez, M., Fu, Y., Zhu, W., Tremblay, M., David, M. and Shuai, K. (2002) Identification of a nuclear Stat1 protein tyrosine phosphatase. Mol. Cell. Biol. 22, 5662-5668
33. Yamamoto, T., Sekine, Y., Kashima, K., Kubota, A., Sato, N., Aoki, N. and Matsuda, T. (2002) The nuclear isoform of protein-tyrosine phosphatase TC-PTP regulates interleukin-6-mediated signaling pathway through STAT3 dephosphorylation. Biochem. Biophys. Res. Commun. 297, 811-817
34. Köster, M. and Hauser, H. (1999) Dynamic redistribution of STAT1 protein in IFN signaling visualized by GFP fusion proteins. Eur. J. Biochem. 260, 137-144
35. McBride, K. M., McDonald, C. and Reich, N. C. (2000) Nuclear export signal located within the DNA-binding domain of the STAT1 transcription factor. EMBO J. 19, 6196-6206
36. Begitt, A., Meyer, T., van Rossum, M. and Vinkemeier, U. (2000) Nucleocytoplasmic translocation of Stat1 is regulated by a leucine-rich export signal in the coiled-coil domain. Proc. Natl. Acad. Sci. U.S.A. 97, 10418-10423
37. Anhuf, D., Weissenbach, M., Schmitz, J., Sobota, R., Hermanns, H. M., Radtke, S., Linnemann, S., Behrmann, I., Heinrich, P. C. and Schaper, F. (2000) Signal transduction of IL-6, leukemia-inhibitory factor, and oncostatin M: structural receptor requirements for signal attenuation. J. Immunol. 165, 2535-2543
38. Weiergräber, O., Hemmann, U., Küster, A., Müller-Newen, G., Schneider, J., Rose-John, S., Kurschat, P., Brakenhoff, J. P. J., Hart, M. H. L., Stabel, S. and Heinrich, P. C. (1995) Soluble human interleukin-6 receptor - Expression in insect cells, purification and characterization. Eur. J. Biochem. 234, 661-669
39. Horsten, U., Müller-Newen, G., Gerhartz, C., Wollmer, A., Wijdenes, J., Heinrich, P. C. and Grötzinger, J. (1997) Molecular modeling-guided mutagenesis of the extracellular part of gp130 leads to the identification of contact sites in the interleukin-6 (IL-6).IL-6 receptor.gp130 complex. J. Biol. Chem. 272, 23748-23757
40. Wagner, B. J., Hayes, T. E., Hoban, C. J. and Cochran, B. H. (1990) The SIF binding element confers sis/PDGF inducibility onto the c-fos promoter. EMBO J. 9, 4477-4484
41. Sambrook, J. and Russell, D. (2000) Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Press, Cold Spring Harbor, NY
42. Schmitz, J., Dahmen, H., Grimm, C., Gendo, C., Müller-Newen, G., Heinrich, P. C. and Schaper, F. (2000) The cytoplasmic tyrosine motifs in full-length glycoprotein 130 have different roles in IL-6 signal transduction. J. Immunol. 164, 848-854
43. Oumard, A., Hennecke, M., Hauser, H. and Nourbakhsh, M. (2000) Translation of NRF mRNA is mediated by highly efficient internal ribosome entry. Mol. Cell. Biol. 20, 2755-2759
44. Starr, R., Willson, T. A., Viney, E. M., Murray, L. J., Rayner, J. R., Jenkins, B. J., Gonda, T. J., Alexander, W. S., Metcalf, D., Nicola, N. A. and Hilton, D. J. (1997) A family of cytokine-inducible inhibitors of signalling. Nature (London) 387, 917-921
45. Saxton, T. M., Henkemeyer, M., Gasca, S., Shen, R., Rossi, D. J., Shalaby, F., Feng, G. S. and Pawson, T. (1997) Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2. EMBO J. 16, 2352-2364
46. Thiel, S., Sommer, U., Kortylewski, M., Haan, C., Behrmann, I., Heinrich, P. C. and Graeve, L. (2000) Termination of IL-6-induced STAT activation is independent of receptor internalization but requires de nova protein synthesis. FEBS Lett. 470, 15-19
47. Mahboubi, K., Kirkiles-Smith, N. C., Karras, J. and Pober, J. S. (2003) Desensitization of signaling by oncostatin M in human vascular cells involves cytoplasmic Tyr residue 759 in gp130 but is not mediated by either Src homology 2 domain-containing tyrosine phosphatase 2 or suppressor of cytokine signaling 3. J. Biol. Chem. 278, 25014-25023