SOCS3 binds specific receptor–JAK complexes to control cytokine signaling by direct kinase inhibition (original) (raw)
Wilks, A.F. Two putative protein-tyrosine kinases identified by application of the polymerase chain reaction. Proc. Natl. Acad. Sci. USA86, 1603–1607 (1989). ArticleCAS Google Scholar
Wilks, A.F. & Oates, A.C. The JAK/STAT pathway. Cancer Surv.27, 139–163 (1996). CASPubMed Google Scholar
Shuai, K. et al. Polypeptide signalling to the nucleus through tyrosine phosphorylation of Jak and Stat proteins. Nature366, 580–583 (1993). ArticleCAS Google Scholar
Darnell, J.E. Jr., Kerr, I.M. & Stark, G.R. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science264, 1415–1421 (1994). ArticleCAS Google Scholar
Endo, T.A. et al. A new protein containing an SH2 domain that inhibits JAK kinases. Nature387, 921–924 (1997). ArticleCAS Google Scholar
Hilton, D.J. et al. Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc. Natl. Acad. Sci. USA95, 114–119 (1998). ArticleCAS Google Scholar
Naka, T. et al. Structure and function of a new STAT-induced STAT inhibitor. Nature387, 924–929 (1997). ArticleCAS Google Scholar
Starr, R. et al. A family of cytokine-inducible inhibitors of signalling. Nature387, 917–921 (1997). ArticleCAS Google Scholar
Babon, J.J. et al. The SOCS box domain of SOCS3: Structure and interaction with the elonginBC-cullin5 ubiquitin ligase. J. Mol. Biol.381, 928–940 (2008). ArticleCAS Google Scholar
Babon, J.J., Sabo, J.K., Zhang, J.G., Nicola, N.A. & Norton, R.S. The SOCS box encodes a hierarchy of affinities for cullin5: implications for ubiquitin ligase formation and cytokine signalling suppression. J. Mol. Biol.387, 162–174 (2009). ArticleCAS Google Scholar
Kamizono, S. et al. The SOCS box of SOCS-1 accelerates ubiquitin-dependent proteolysis of TEL-JAK2. J. Biol. Chem.276, 12530–12538 (2001). ArticleCAS Google Scholar
Zhang, J.G. et al. The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc. Natl. Acad. Sci. USA96, 2071–2076 (1999). ArticleCAS Google Scholar
Zhang, J.G. et al. The SOCS box of suppressor of cytokine signaling-1 is important for inhibition of cytokine action in vivo. Proc. Natl. Acad. Sci. USA98, 13261–13265 (2001). ArticleCAS Google Scholar
Sasaki, A. et al. Cytokine-inducible SH2 protein-3 (CIS3/SOCS3) inhibits Janus tyrosine kinase by binding through the N-terminal kinase inhibitory region as well as SH2 domain. Genes Cells4, 339–351 (1999). ArticleCAS Google Scholar
Yasukawa, H. et al. The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J.18, 1309–1320 (1999). ArticleCAS Google Scholar
Boyle, K. et al. Deletion of the SOCS box of suppressor of cytokine signaling 3 (SOCS3) in embryonic stem cells reveals SOCS box-dependent regulation of JAK but not STAT phosphorylation. Cell Signal.21, 394–404 (2009). ArticleCAS Google Scholar
Babon, J.J. et al. Suppression of cytokine signaling by SOCS3: characterization of the mode of inhibition and the basis of its specificity. Immunity36, 239–250 (2012). ArticleCAS Google Scholar
Roberts, A.W. et al. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc. Natl. Acad. Sci. USA98, 9324–9329 (2001). ArticleCAS Google Scholar
Yasukawa, H. et al. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat. Immunol.4, 551–556 (2003). ArticleCAS Google Scholar
Croker, B.A. et al. SOCS3 is a critical physiological negative regulator of G-CSF signaling and emergency granulopoiesis. Immunity20, 153–165 (2004). ArticleCAS Google Scholar
Mori, H. et al. Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity. Nat. Med.10, 739–743 (2004). ArticleCAS Google Scholar
Hörtner, M. et al. Suppressor of cytokine signaling-3 is recruited to the activated granulocyte-colony stimulating factor receptor and modulates its signal transduction. J. Immunol.169, 1219–1227 (2002). Article Google Scholar
De Souza, D. et al. SH2 domains from suppressor of cytokine signaling-3 and protein tyrosine phosphatase SHP-2 have similar binding specificities. Biochemistry41, 9229–9236 (2002). ArticleCAS Google Scholar
Nicholson, S.E. et al. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc. Natl. Acad. Sci. USA97, 6493–6498 (2000). ArticleCAS Google Scholar
Skiniotis, G., Lupardus, P.J., Martick, M., Walz, T. & Garcia, K.C. Structural organization of a full-length gp130/LIF-R cytokine receptor transmembrane complex. Mol. Cell31, 737–748 (2008). ArticleCAS Google Scholar
Bergamin, E., Wu, J. & Hubbard, S.R. Structural basis for phosphotyrosine recognition by suppressor of cytokine signaling-3. Structure14, 1285–1292 (2006). ArticleCAS Google Scholar
Lucet, I.S. et al. The structural basis of Janus kinase 2 inhibition by a potent and specific pan-Janus kinase inhibitor. Blood107, 176–183 (2006). ArticleCAS Google Scholar
Knighton, D.R. et al. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science253, 407–414 (1991). ArticleCAS Google Scholar
Babon, J.J. et al. The structure of SOCS3 reveals the basis of the extended SH2 domain function and identifies an unstructured insertion that regulates stability. Mol. Cell22, 205–216 (2006). ArticleCAS Google Scholar
Babon, J.J. et al. Suppression of cytokine signaling by SOCS3: characterization of the mode of inhibition and the basis of its specificity. Immunity36, 239–250 (2012). ArticleCAS Google Scholar
Hubbard, S.R. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J.16, 5572–5581 (1997). ArticleCAS Google Scholar
Nicholson, S.E. et al. 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 (1999). ArticleCAS Google Scholar
Blat, Y. Non-competitive inhibition by active site binders. Chem. Biol. Drug Des.75, 535–540 (2010). ArticleCAS Google Scholar
Yoshimura, A. The CIS family: negative regulators of JAK-STAT signaling. Cytokine Growth Factor Rev.9, 197–204 (1998). ArticleCAS Google Scholar
Moncoq, K. et al. The PIR domain of Grb14 is an intrinsically unstructured protein: implication in insulin signaling. FEBS Lett.554, 240–246 (2003). ArticleCAS Google Scholar
Depetris, R.S. et al. Structural basis for inhibition of the insulin receptor by the adaptor protein Grb14. Mol. Cell20, 325–333 (2005). ArticleCAS Google Scholar
Béréziat, V. et al. Inhibition of insulin receptor catalytic activity by the molecular adapter Grb14. J. Biol. Chem.277, 4845–4852 (2002). Article Google Scholar
Lei, M. et al. Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell102, 387–397 (2000). ArticleCAS Google Scholar
James, C. et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature434, 1144–1148 (2005). ArticleCAS Google Scholar
Chen, E., Staudt, L.M. & Green, A.R. Janus kinase deregulation in leukemia and lymphoma. Immunity36, 529–541 (2012). ArticleCAS Google Scholar
Tefferi, A. & Pardanani, A. JAK inhibitors in myeloproliferative neoplasms: rationale, current data and perspective. Blood Rev.25, 229–237 (2011). ArticleCAS Google Scholar
Karplus, P.A. & Diederichs, K. Linking crystallographic model and data quality. Science336, 1030–1033 (2012). ArticleCAS Google Scholar
Babon, J.J. et al. Secondary structure assignment of mouse SOCS3 by NMR defines the domain boundaries and identifies an unstructured insertion in the SH2 domain. FEBS J.272, 6120–6130 (2005). ArticleCAS Google Scholar
Kabsch, W. Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D Biol. Crystallogr.66, 133–144 (2010). ArticleCAS Google Scholar
McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr.40, 658–674 (2007). ArticleCAS Google Scholar
Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr.66, 213–221 (2010). ArticleCAS Google Scholar
Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr.66, 486–501 (2010). ArticleCAS Google Scholar
Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol.372, 774–797 (2007). ArticleCAS Google Scholar
Griffin, M.D. et al. Characterisation of the first enzymes committed to lysine biosynthesis in Arabidopsis thaliana. PLoS ONE7, e40318 (2012). ArticleCAS Google Scholar
Petoukhov, M.V., Konarev, P.V., Kikhney, A.G. & Svergun, D.I. ATSAS 2.1—towards automated and web-supported small-angle scattering data analysis. J. Appl. Crystallogr.40, S223–S228 (2007). ArticleCAS Google Scholar
Konarev, P.V., Volkov, V.V., Sokolova, A.V., Koch, M.H.J. & Svergun, D.I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr.36, 1277–1282 (2003). ArticleCAS Google Scholar
Svergun, D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr.25, 495–503 (1992). ArticleCAS Google Scholar
Svergun, D., Barberato, C. & Koch, M.H.J. CRYSOL—a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr.28, 768–773 (1995). ArticleCAS Google Scholar
Franke, D. & Svergun, D.I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr.42, 342–346 (2009). ArticleCAS Google Scholar
Volkov, V.V. & Svergun, D.I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr.36, 860–864 (2003). ArticleCAS Google Scholar
Kozin, M.B. & Svergun, D.I. Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr.34, 33–41 (2001). ArticleCAS Google Scholar