The SOCS box: a tale of destruction and degradation

Ihle, 1994, Signaling by the cytokine receptor superfamily: JAKs and STATs, Trends Biochem. Sci., 19, 222, 10.1016/0968-0004(94)90026-4 Neel, 1997, The role of phosphatases in lymphocyte activation, Curr. Opin. Immunol., 9, 405, 10.1016/S0952-7915(97)80088-X Irie-Sasaki, 2001, CD45 is a JAK phosphatase and negatively regulates cytokine receptor signalling, Nature, 409, 349, 10.1038/35053086 Chung, 1997, Specific inhibition of Stat3 signal transduction by PIAS3, Science, 278, 1803, 10.1126/science.278.5344.1803 Hilton, 1999, Negative regulators of cytokine signal transduction, Cell. Mol. Life Sci., 55, 1568, 10.1007/s000180050396 Yoshimura, 1995, A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors, EMBO J., 14, 2816, 10.1002/j.1460-2075.1995.tb07281.x Alexander, 1999, SOCS1 is a critical inhibitor of interferon γ signaling and prevents the potentially fatal neonatal actions of this cytokine, Cell, 98, 597, 10.1016/S0092-8674(00)80047-1 Marine, 1999, SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality, Cell, 98, 609, 10.1016/S0092-8674(00)80048-3 Naka, 1998, Accelerated apoptosis of lymphocytes by augmented induction of Bax in SSI-1 (STAT-induced STAT inhibitor-1) deficient mice, Proc. Natl. Acad. Sci. U. S. A., 95, 15577, 10.1073/pnas.95.26.15577 Naka, 2001, SOCS-1/SSI-1-deficient NKT cells participate in severe hepatitis through dysregulated cross-talk inhibition of IFN-γ and IL-4 signaling in vivo, Immunity, 14, 535, 10.1016/S1074-7613(01)00132-7 Starr, 1998, Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1, Proc. Natl. Acad. Sci. U. S. A., 95, 14395, 10.1073/pnas.95.24.14395 Horvat, 2001, Lack of Socs2 expression causes the high-growth phenotype in mice, Genomics, 72, 209, 10.1006/geno.2000.6441 Metcalf, 2000, Gigantism in mice lacking suppressor of cytokine signalling-2, Nature, 405, 1069, 10.1038/35016611 Marine, 1999, SOCS3 is essential in the regulation of fetal liver erythropoiesis, Cell, 98, 617, 10.1016/S0092-8674(00)80049-5 Roberts, 2001, Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3, Proc. Natl. Acad. Sci. U. S. A., 98, 9324, 10.1073/pnas.161271798 Dearolf, 1999, JAKs and STATs in invertebrate model organisms, Cell. Mol. Life Sci., 55, 1578, 10.1007/s000180050397 Brown, 2001, Identification of the first invertebrate interleukin JAK/STAT receptor, the Drosophila gene domeless, Curr. Biol., 11, 1700, 10.1016/S0960-9822(01)00524-3 Mooney, 2001, Suppressors of cytokine signaling-1 and -6 associate with and inhibit the insulin receptor. A potential mechanism for cytokine-mediated insulin resistance, J. Biol. Chem., 276, 25889, 10.1074/jbc.M010579200 Kile, 2001, Functional analysis of Asb-1 using genetic modification in mice, Mol. Cell. Biol., 21, 6189, 10.1128/MCB.21.18.6189-6197.2001 Vasiliauskas, 1999, SWiP-1: novel SOCS box containing WD-protein regulated by signalling centres and by Shh during development, Mech. Dev., 82, 79, 10.1016/S0925-4773(99)00014-3 Zhang, 1999, 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. U. S. A., 96, 2071, 10.1073/pnas.96.5.2071 Kamura, 1998, The elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, Ras, WD-40 repeat, and ankyrin repeat families, Genes Dev., 12, 3872, 10.1101/gad.12.24.3872 Bradsher, 1993, RNA polymerase II transcription factor SIII. I. Identification, purification, and properties, J. Biol. Chem., 268, 25587, 10.1016/S0021-9258(19)74431-7 Aso, 1995, Elongin (SIII): a multisubunit regulator of elongation by RNA polymerase II, Science, 269, 1439, 10.1126/science.7660129 Kibel, 1995, Binding of the von Hippel—Lindau tumor suppressor protein to elongin B and C, Science, 269, 1444, 10.1126/science.7660130 Linehan, 1995, Identification of the von Hippel—Lindau (VHL) gene. Its role in renal cancer, J. Am. Med. Assoc., 273, 564, 10.1001/jama.1995.03520310062031 Gnarra, 1996, Post-transcriptional regulation of vascular endothelial growth factor mRNA by the product of the VHL tumor suppressor gene, Proc. Natl. Acad. Sci. U. S. A., 93, 10589, 10.1073/pnas.93.20.10589 Iliopoulos, 1996, Negative regulation of hypoxia-inducible genes by the von Hippel—Lindau protein, Proc. Natl. Acad. Sci. U. S. A., 93, 10595, 10.1073/pnas.93.20.10595 Maxwell, 1999, The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis, Nature, 399, 271, 10.1038/20459 Iwai, 1999, Identification of the von Hippel—Lindau tumor-suppressor protein as part of an active E3 ubiquitin ligase complex, Proc. Natl. Acad. Sci. U. S. A., 96, 12436, 10.1073/pnas.96.22.12436 Pause, 1997, The von Hippel—Lindau tumor-suppressor gene product forms a stable complex with human CUL-2, a member of the Cdc53 family of proteins, Proc. Natl. Acad. Sci. U. S. A., 94, 2156, 10.1073/pnas.94.6.2156 Lisztwan, 1999, The von Hippel—Lindau tumor suppressor protein is a component of an E3 ubiquitin-protein ligase activity, Genes Dev., 13, 1822, 10.1101/gad.13.14.1822 Ohh, 2000, Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel—Lindau protein, Nat. Cell Biol., 2, 423, 10.1038/35017054 Ivan, 2001, HIF- targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing, Science, 292, 464, 10.1126/science.1059817 Stebbins, 1999, Structure of the VHL—elongin C—elongin B complex: implications for VHL tumor suppressor function, Science, 284, 455, 10.1126/science.284.5413.455 De Sepulveda, 1999, Socs1 binds to multiple signalling proteins and suppresses steel factor-dependent proliferation, EMBO J., 18, 904, 10.1093/emboj/18.4.904 Yasukawa, 1999, The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop, EMBO J., 18, 1309, 10.1093/emboj/18.5.1309 Nicholson, 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, 10.1093/emboj/18.2.375 Nicholson, 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, 10.1073/pnas.100135197 Schmitz, 2000, SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130, J. Biol. Chem., 275, 12848, 10.1074/jbc.275.17.12848 Bjorbaek, 2000, SOCS3 mediates feedback inhibition of the leptin receptor via Tyr985, J. Biol. Chem., 275, 40649, 10.1074/jbc.M007577200 Hansen, 1999, Mechanism of inhibition of growth hormone receptor signaling by suppressor of cytokine signaling proteins, Mol. Endocrinol., 13, 1832, 10.1210/mend.13.11.0368 De Sepulveda, 2000, Suppressor of cytokine signaling-1 inhibits VAV function through protein degradation, J. Biol. Chem., 275, 14005, 10.1074/jbc.C000106200 Monni, 2001, The TEL—Jak2 oncoprotein induces Socs1 expression and altered cytokine response in Ba/F3 cells, Oncogene, 20, 849, 10.1038/sj.onc.1204201 Frantsve, 2001, Socs-1 inhibits TEK-JAK2-mediated transformation of hematopoietic cells through inhibition of JAK2 kinase activity and induction of proteasome-mediated degradation, Mol. Cell. Biol., 21, 3547, 10.1128/MCB.21.10.3547-3557.2001 Ungureanu, D. et al. Regulation of Jak2 through the ubiquitin-proteasome pathway involves phosphorylation of Jak2 on Y1007 and interaction with SOCS-1, Mol. Cell. Biol. (in press) Callus, 1998, Interleukin-3-induced activation of the JAK/STAT pathway is prolonged by proteasome inhibitors, Blood, 91, 3182, 10.1182/blood.V91.9.3182 Verdier, 1998, Proteasomes regulate erythropoietin receptor and signal transducer and activator of transcription 5 (STAT5) activation, J. Biol. Chem., 273, 28185, 10.1074/jbc.273.43.28185 Kishida, 1995, Cellular proteins that bind the von Hippel—Lindau disease gene product: mapping of binding domains and the effect of missense mutations, Cancer Res., 55, 4544 Narazaki, 1998, Three distinct domains of SSI-1/SOCS-1/JAB protein are required for its suppression of interleukin 6 signalling, Proc. Natl. Acad. Sci. U. S. A., 95, 13130, 10.1073/pnas.95.22.13130 Zhang, 2001, The SOCS box of suppressor of cytokine signaling-1 is important for inhibition of cytokine action in vivo, Proc. Natl. Acad. Sci. U. S. A., 98, 13261, 10.1073/pnas.231486498 Ellgaard, 1999, Setting the standards: quality control in the secretory pathway, Science, 286, 1882, 10.1126/science.286.5446.1882 Lai, 2001, Drosophila Neuralized is a ubiquitin ligase that promotes the internalization and degradation of Delta, Dev. Cell, 1, 783, 10.1016/S1534-5807(01)00092-2 Deblandre, 2001, Xenopus Neuralized is a ubiquitin ligase that interacts with XDelta1 and regulates Notch signaling, Dev. Cell, 1, 795, 10.1016/S1534-5807(01)00091-0 Nakamura, 1998, Identification of a human homolog of the Drosophila Neuralized gene within the 10q25.1 malignant astrocytoma deletion region, Oncogene, 16, 1009, 10.1038/sj.onc.1201618 Ivan, 2001, The von Hippel—Lindau tumor suppressor protein, Curr. Opin. Genet. Dev., 11, 27, 10.1016/S0959-437X(00)00152-0 Patton, 1998, Combinatorial control in ubiquitin-dependent proteolysis: don't Skp the F-box hypothesis, Trends Genet., 14, 236, 10.1016/S0168-9525(98)01473-5 Carrano, 1999, SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27, Nat. Cell Biol., 1, 193, 10.1038/12013 Schulman, 2000, Insights into SCF ubiquitin ligases from the structure of the Skp1—Skp2 complex, Nature, 408, 381, 10.1038/35042620 Hershko, 1998, The ubiquitin system, Annu. Rev. Biochem., 67, 425, 10.1146/annurev.biochem.67.1.425