Negative regulation of gp130 signalling mediated through tyrosine-757 is not dependent on the recruitment of SHP2

Biochemical Journal

Volumn 372, Issue 2, 2003, Pages 495-502

  Fairlie, W Douglas ^a,b   De Souza, David ^a,b   Nicola, Nicos A ^a,b   Baca, Manuel ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b University of Melbourne   (Australia)

Author keywords

Cytokine; Interleukin 6 signalling; Suppressor of cytokine signalling

Indexed keywords

CELLS; CHEMICAL ACTIVATION; CYTOLOGY; GENETIC ENGINEERING;

HOMOLOGY;

AMINO ACIDS;

CHIMERIC PROTEIN; CYTOKINE; GLYCOPROTEIN GP 130; MUTANT PROTEIN; REGULATOR PROTEIN; SHP DOMAIN CONTAINING TYROSINE PHOSPHATASE 2; SUPPRESSOR OF CYTOKINE SIGNALLING 3; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CHIMERA; CONTROLLED STUDY; EMBRYO; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; STIMULATION;

ANIMALS; ANTIGENS, CD; BLOTTING, WESTERN; CELLS, CULTURED; CYTOKINE RECEPTOR GP130; FIBROBLASTS; GENE EXPRESSION; HUMANS; INTERLEUKIN-6; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; LUCIFERASES; MEMBRANE GLYCOPROTEINS; MICE; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHOSPHORYLATION; PLASMIDS; PRECIPITIN TESTS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN-TYROSINE-PHOSPHATASE; PROTEINS; RECEPTORS, ERYTHROPOIETIN; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSCRIPTION FACTORS; TRANSFECTION; TYROSINE;

EID: 0038676954     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20030104     Document Type: Article

References (34)

1. Chow, D., Brevnova, L., He, X., Martick, M. M., Bankovich, A. and Garcia, K. C. (2002) A structural template for gp130-cytokine signaling assemblies. Biechim. Biophys. Acta 1592, 225-235
2. Taga, T. and Kishimoto, T. (1997) Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 15, 797-819
3. Stahl, N., Farruggella, T. J., Boulton, T. G., Zhong, Z., Darnell, Jr, J. E. and Yancopoules, G. D. (1995) Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science 267, 1349-1353
4. Fukada, T., Hibi, M., Yamanaka, Y., Takahashi-Tezuka, M., Fujitani, Y., Yamaguchi, T., Nakajima, K. and Hirano, T. (1996) Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: involvement of STAT3 in anti-apoptosis. Immunity 5, 449-460
5. 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
6. 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
7. Qu, C. K. (2000) The SHP-2 tyrosine phosphatase: signaling mechanisms and biological functions. Cell Res. 10, 279-288
8. Starr, R., Willson, T. A., Viney, E. M., Murray, L. J., Rayner, J. R., Jenkins, B. J., Ganda, T. J., Alexander, W. S., Metcalf, D., Nicola, N. A. et al. (1997) A family of cytokine-inducible inhibitors of signalling. Nature (London) 387, 917-921
9. Suzuki, R., Sakamota, H., Yasukawa, H., Masuhara, M., Wakioka, T., Sasaki, A., Yuge, K., Kamiya, S., Inoue, A. and Yoshimura, A. (1998) CIS3 and JAB have different regulatory roles in interleukin-6 mediated differentiation and STAT3 activation in M1 leukemia cells. Oncogene 17, 2271-2278
10. Nicholson, S. E., Willson, T. A., Farley, A., Starr, R., Zhang, J. G., Baca, M., Alexander, W. S., Metcalf, D., Hilton, D. J. and Nicola, N. A. (1999) Mutational analyses of the SOCS proteins suggest a dual domain requirement but distinct mechanisms for inhibition of LIF and IL-6 signal transduction. EMBO J. 18, 375-385
11. Nakajima, K., Yamanaka, Y., Nakae, K., Kojima, H., Ichiba, M., Kiuchi, N., Kitaoka, T., Fukada, T., Hibi, M. and Hirano, T. (1996) A central role for Stat3 in IL-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO J. 15, 3651-3658
12. Symes, A., Stahl, N., Reeves, S. A., Farruggella, T., Servidei, T., Gearan, T., Yancopoulos, G. and Fink, J. S. (1997) The protein tyrosine phosphatase SHP-2 negatively regulates ciliary neurotrophic factor induction of gene expression. Curr. Biol. 7, 697-700
13. Kim, H., 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
14. Schaper, F., Gendo, C., Eck, M., Schmitz, J., Grimm, C., Anhuf, D., Kerr, I. M. and Heinrich, P. C. (1998) Activabon 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
15. Burdon, T., Stracey, C., Chambers, I., Nichols, J. and Smith, A. (1999) Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev. Biol. 210, 30-43
16. Ohtani, T., Ishihara, K., Atsumi, T., Nishida, K., Kaneko, Y., Miyata, T., Itoh, S., Narimatsu, M., Maeda, H., Fukada, T. et al. (2000) Dissection of signaling cascades through gp130 in vivo: reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity 12, 95-105
17. De Souza, D., Fabri, L. J., Nash, A., Hilton, D. J., Nicola, N. A. and Baca, M. (2002) SH2 domains from suppressor of cytokine signaling-3 and protein tyrosine phosphatase SHP-2 have similar binding specificities. Biochemistry 41, 9229-9236
18. Tauchi, T., Damen, J. E., Toyama, K., Feng, G. S., Broxmeyer, H. E. and Krystal, G. (1995) Tyrosine 425 within the activated erythropoietin receptor binds Syp, reduces the erythropoietin required for Syp tyrosine phosphorylation, and promotes mitogenesis. Blood 87, 4495-4501
19. Carpenter, L. R., Farruggella, T. J., Symes, A., Karow, M. L., Yancopolous, G. D. and Stahl, N. (1998) Enhancing leptin response by preventing SH2-containing phosphatase 2 interaction with Ob receptor. Proc. Natl. Acad. Sci. U.S.A. 95, 6061-6066
20. Sasaki, A., Yasukawa, H., Shouda, T., Kitamura, T., Dikic, I. and Yoshimura, A. (2000) CIS3/SOCS-3 suppresses erythropeietin (EPO) signaling by binding the EPO receptor and JAK2. J. Biol. Chem. 275, 29338-29347
21. Bjorbaek, C., Lavery, H. J., Bates, S. H., Olson, R. K., Davis, S. M, Flier, J. S. and Myers, M. G. (2000) SOCS3 mediates feedback inhibition of the leptin receptor via Tyr(985). J. Biol. Chem. 275, 40649-40657
22. Li, C. and Friedman, J. M. (1999) Leptin receptor activation of SH2 domain containing protein tyrosine phosphatase 2 modulates Ob receptor signal transduction. Proc. Natl. Acad. Sci. U.S.A. 96, 9677-9682
23. Fisher, C. L. and Pei, G. K. (1997) Modification of a PCR-based site-directed mutagenesis method. BioTechniques 23, 570-571
24. Fairlie, W. D., Russell, P. K., Wu, W. M., Moore, A. G., Zhang, H. P., Brown, P. K., Bauskin, A. R. and Breit, S. N. (2001) Epitope mapping of the transforming growth factor-β superfamily protein, macrophage inhibitory cytokine-1 (MIC-1): identification of at least five distinct epitope specificities. Biochemistry 40, 65-73
25. Endo, T. A., Masuhara, M., Yokouchi, M., Suzuki, R., Sakamoto, H., Mitsui, K., Matsumoto, A., Tanimura, S., Ohtsubo, M., Misawa, H. et al. (1997) A new protein containing an SH2 domain that inhibits JAK kinases. Nature (London) 387, 921-924
26. Boulton, T. G., Stahl, N. and Yancopoulos, G. D. (1994) Ciliary neurotrophic factor/leukemia inhibitory factor/interleukin 6/oncostatin M family of cytokines induces tyrosine phosphorylation of a common set of proteins overlapping those induced by other cytokines and growth factors. J. Biol. Chem. 269, 11648-11655
27. 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
28. Marine, J. C., McKay, C., Wang, D., Topham, D. J., Parganas, E., Nakajima, H., Pendeville, H., Yasukawa, H., Sasaki, A., Yoshimura, A. et al. (1999) SOCS3 is essential in the regulation of fetal liver erythropoiesis. Cell (Cambridge, Mass.) 98, 617-627
29. Roberts, A. W., Robb, L., Rakar, S., Hartley, L., Cluse, L., Nicola, N. A., Metcalf, D., Hilton, D. J. and Alexander, W. S. (2001) Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc. Natl. Acad. Sci. U.S.A. 98, 9324-9329
30. Lehmann, U., Schmitz, J., Weissenbach, M., Sobota, R. M., Hortner, M., Friederichs, K., Behrmann, I., Tsiaris, W., Sasaki, A., Schneider-Mergener, J. et al. (2003) SHP2 and SOCS3 contribute to Y759-dependent attenuation of IL-6-signaling through gp130. J. Biol. Chem. 278, 661-671
31. Hof, P., Pluskey, S., Dhe-Paganon, S., Eck, M. J. and Shoelson, S. E. (1998) Crystal structure of the tyrosine phosphatase SHP-2. Cell (Cambridge, Mass.) 92, 441-450
32. Bjorbaek, C., Buchholz, R. M., Davis, S. M., Bates, S. H., Pierroz, D. D., Gu, H., Neel, B. G., Myers, Jr, M. G. and Flier, J. S. (2001) Divergent roles of SHP-2 in ERK activation by leptin receptors. J. Biol. Chem. 276, 4747-4755
33. Bjorbaek, C., Elmquist, J. K., Frantz, J. D., Shoelson, S. E. and Flier, J. S. (1998) Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol. Cell 1, 619-625
34. Tebbutt, N. C., Giraud, A. S., Inglese, M., Jenkins, B., Waring, P., Clay, F. J., Malki, S., Alderman, B. M., Grail, D., Hollande, F. et al. (2002) Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat. Med. 8, 1089-1097