Extracellular signal-regulated kinase mitogen-activated protein kinase-dependent SOCS-3 gene induction requires c-Jun, signal transducer and activator of transcription 3,and specificity protein 3 transcription factors

Molecular Pharmacology

Volumn 81, Issue 5, 2012, Pages 657-668

  Wiejak, Jolanta ^a   Dunlop, Julia ^a   Gao, Shan ^a   Borland, Gillian ^a   Yarwood, Stephen J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN C JUN; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRANSCRIPTION FACTOR SP3;

ARTICLE; BINDING SITE; GENE INDUCTION; HUMAN; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; BINDING SITES; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELLS, CULTURED; ENDOTHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; EXTRACELLULAR SPACE; HUMANS; MICE; PROMOTER REGIONS, GENETIC; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-JUN; SIGNAL TRANSDUCTION; SP3 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84859952395     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.111.076976     Document Type: Article

References (46)

1. Ammanamanchi S, Freeman JW, and Brattain MG (2003) Acetylated sp3 is a transcriptional activator. J Biol Chem 278:35775-35780. (Pubitemid 37102354)
2. Auernhammer CJ, Bousquet C, and Melmed S (1999) Autoregulation of pituitary corticotroph SOCS-3 expression: characterization of the murine SOCS-3 promoter. Proc Natl Acad Sci USA 96:6964-6969. (Pubitemid 29274993)
3. Bain J, McLauchlan H, Elliott M, and Cohen P (2003) The specificities of protein kinase inhibitors: an update. Biochem J 371:199-204. (Pubitemid 36458094)
4. Baker BJ, Qin H, and Benveniste EN (2008) Molecular basis of oncostatin M-induced SOCS-3 expression in astrocytes. Glia 56:1250-1262.
5. Barclay JL, Anderson ST, Waters MJ, and Curlewis JD (2007) Characterization of the SOCS3 promoter response to prostaglandin E2 in T47D cells. Mol Endocrinol 21:2516-2528. (Pubitemid 47529362)
6. Barclay JL, Anderson ST, Waters MJ, and Curlewis JD (2009) SOCS3 as a tumor suppressor in breast cancer cells, and its regulation by PRL. Int J Cancer 124: 1756-1766.
7. Borland G, Bird RJ, Palmer TM, and Yarwood SJ (2009) Activation of protein kinase Calpha by EPAC1 is required for the ERK- and CCAAT/enhancer- binding protein beta-dependent induction of the SOCS-3 gene by cyclic AMP in COS1 cells. J Biol Chem 284:17391-17403.
8. Bousquet C, Chesnokova V, Kariagina A, Ferrand A, and Melmed S (2001) cAMP neuropeptide agonists induce pituitary suppressor of cytokine signaling-3: novel negative feedback mechanism for corticotroph cytokine action. Mol Endocrinol 15:1880-1890. (Pubitemid 33022529)
9. Croker BA, Kiu H, and Nicholson SE (2008) SOCS regulation of the JAK/STAT signalling pathway. Semin Cell Dev Biol 19:414-422.
10. Croker BA, Kiu H, Pellegrini M, Toe J, Preston S, Metcalf D, O'Donnell JA, Cengia LH, McArthur K, Nicola NA, et al. (2012) IL-6 promotes acute and chronic inflammatory disease in the absence of SOCS3. Immunol Cell Biol 90:124-129.
11. Dalpke A, Heeg K, Bartz H, and Baetz A (2008) Regulation of innate immunity by suppressor of cytokine signaling (SOCS) proteins. Immunobiology 213:225-235. (Pubitemid 351479858)
12. Darnell JE Jr, Kerr IM, and Stark GR (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415-1421. (Pubitemid 24217131)
13. Davies SP, Reddy H, Caivano M, and Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105.
14. Dimitriou ID, Clemenza L, Scotter AJ, Chen G, Guerra FM, and Rottapel R (2008) Putting out the fire: coordinated suppression of the innate and adaptive immune systems by SOCS1 and SOCS3 proteins. Immunol Rev 224:265-283.
15. Ehlting C, Häussinger D, and Bode JG (2005) Sp3 is involved in the regulation of SOCS3 gene expression. Biochem J 387:737-745. (Pubitemid 40685708)
16. Emanuelli B, Peraldi P, Filloux C, Sawka-Verhelle D, Hilton D, and Van Obberghen E (2000) SOCS-3 is an insulin-induced negative regulator of insulin signaling. J Biol Chem 275:15985-15991. (Pubitemid 30366903)
17. He B, You L, Uematsu K, Matsangou M, Xu Z, He M, McCormick F, and Jablons DM (2003a) Cloning and characterization of a functional promoter of the human SOCS-3 gene. Biochem Biophys Res Commun 301:386-391. (Pubitemid 36279250)
18. He B, You L, Uematsu K, Zang K, Xu Z, Lee AY, Costello JF, McCormick F, and Jablons DM (2003b) SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc Natl Acad Sci USA 100:14133-14138. (Pubitemid 37499203)
19. Hiwatashi K, Tamiya T, Hasegawa E, Fukaya T, Hashimoto M, Kakoi K, Kashiwagi I, Kimura A, Inoue N, Morita R, et al. (2011) Suppression of SOCS3 in macrophages prevents cancer metastasis by modifying macrophage phase and MCP2/ CCL8 induction. Cancer Lett 308:172-180.
20. Jo D, Liu D, Yao S, Collins RD, and Hawiger J (2005) Intracellular protein therapy with SOCS3 inhibits inflammation and apoptosis. Nat Med 11:892-898. (Pubitemid 41161123)
21. Kamura T, Sato S, Haque D, Liu L, Kaelin WG Jr, Conaway RC, and Conaway JW (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 12:3872-3881. (Pubitemid 29024849)
22. Krebs DL and Hilton DJ (2001) SOCS proteins: negative regulators of cytokine signaling. Stem Cells 19:378-387. (Pubitemid 32900080)
23. Kubo M, Hanada T, and Yoshimura A (2003) Suppressors of cytokine signaling and immunity. Nat Immunol 4:1169-1176. (Pubitemid 37540685)
24. Kuroki M and O'Flaherty JT (1999) Extracellular signal-regulated protein kinase (ERK)-dependent and ERK-independent pathways target STAT3 on serine-727 in human neutrophils stimulated by chemotactic factors and cytokines. Biochem J 341:691-696.
25. Martini M, Pallini R, Luongo G, Cenci T, Lucantoni C, and Larocca LM (2008) Prognostic relevance of SOCS3 hypermethylation in patients with glioblastoma multiforme. Int J Cancer 123:2955-2960.
26. Mellor H and Parker PJ (1998) The extended protein kinase C superfamily. Biochem J 332:281-292. (Pubitemid 28271856)
27. Pagès G (2007) Sp3-mediated VEGF regulation is dependent on phosphorylation by extra-cellular signals regulated kinases (Erk). J Cell Physiol 213:454-463.
28. Parnell E, Smith BO, Palmer TM, Terrin A, Zaccolo M and Yarwood SJ (2011) Regulation of the inflammatory response of vascular endothelial cells by EPAC1. Br J Pharmacol http://dx.doi.org/10.1111/j.1476-5381.2011.01808.x.
29. Pulverer BJ, Kyriakis JM, Avruch J, Nikolakaki E, and Woodgett JR (1991) Phosphorylation of c-jun mediated by MAP kinases. Nature 353:670-674. (Pubitemid 21912588)
30. Qin H, Roberts KL, Niyongere SA, Cong Y, Elson CO, and Benveniste EN (2007) Molecular mechanism of lipopolysaccharide-induced SOCS-3 gene expression in macrophages and microglia. J Immunol 179:5966-5976.
31. Sands WA and Palmer TM (2005) Adenosine receptors and the control of endothelial cell function in inflammatory disease. Immunol Lett 101:1-11. (Pubitemid 41297492)
32. Sands WA, Woolson HD, Milne GR, Rutherford C, and Palmer TM (2006) Exchange protein activated by cyclic AMP (Epac)-mediated induction of suppressor of cytokine signaling 3 (SOCS-3) in vascular endothelial cells. Mol Cell Biol 26:6333-6346. (Pubitemid 44277875)
33. Sasaki A, Yasukawa H, Suzuki A, Kamizono S, Syoda T, Kinjyo I, Sasaki M, Johnston JA, and Yoshimura A (1999) 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 Cells 4:339-351. (Pubitemid 29359449)
34. Silver JS and Hunter CA (2010) gp130 at the nexus of inflammation, autoimmunity, and cancer. J Leukoc Biol 88:1145-1156.
35. Tischoff I, Hengge UR, Vieth M, Ell C, Stolte M, Weber A, Schmidt WE, and Tannapfel A (2007) Methylation of SOCS-3 and SOCS-1 in the carcinogenesis of Barrett's adenocarcinoma. Gut 56:1047-1053. (Pubitemid 47123231)
36. Tokita T, Maesawa C, Kimura T, Kotani K, Takahashi K, Akasaka T, and Masuda T (2007) Methylation status of the SOCS3 gene in human malignant melanomas. Int J Oncol 30:689-694.
37. Vries RG, Prudenziati M, Zwartjes C, Verlaan M, Kalkhoven E, and Zantema A (2001) A specific lysine in c-Jun is required for transcriptional repression by E1A and is acetylated by p300. EMBO J 20:6095-6103. (Pubitemid 33049284)
38. Weber A, Hengge UR, Bardenheuer W, Tischoff I, Sommerer F, Markwarth A, Dietz A, Wittekind C, and Tannapfel A (2005) SOCS-3 is frequently methylated in head and neck squamous cell carcinoma and its precursor lesions and causes growth inhibition. Oncogene 24:6699-6708. (Pubitemid 41486800)
39. Wen Z, Zhong Z, and Darnell JE Jr (1995) Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82:241-250.
40. White GE, Cotterill A, Addley MR, Soilleux EJ, and Greaves DR (2011) Suppressor of cytokine signalling protein SOCS3 expression is increased at sites of acute and chronic inflammation. J Mol Histol 42:137-151.
41. Woolson HD, Thomson VS, Rutherford C, Yarwood SJ, and Palmer TM (2009) Selective inhibition of cytokine-activated extracellular signal-regulated kinase by cyclic AMP via Epac1-dependent induction of suppressor of cytokine signalling-3. Cell Signal 21:1706-1715.
42. Yang J, Huang J, Dasgupta M, Sears N, Miyagi M, Wang B, Chance MR, Chen X, Du Y, Wang Y, et al. (2010) Reversible methylation of promoter-bound STAT3 by histone-modifying enzymes. Proc Natl Acad Sci USA 107:21499-21504.
43. Yarwood SJ, Borland G, Sands WA, and Palmer TM (2008) Identification of CCAAT/ enhancer-binding proteins as exchange protein activated by cAMP-activated transcription factors that mediate the induction of the SOCS-3 gene. J Biol Chem 283:6843-6853.
44. Yuan ZL, Guan YJ, Chatterjee D, and Chin YE (2005) Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 307:269-273. (Pubitemid 40116244)
45. Zagariya A, Mungre S, Lovis R, Birrer M, Ness S, Thimmapaya B, and Pope R (1998) Tumor necrosis factor alpha gene regulation: enhancement of C/EBPbeta-induced activation by c-Jun. Mol Cell Biol 18:2815-2824. (Pubitemid 28183450)
46. Zhang JG, Farley A, Nicholson SE, Willson TA, Zugaro LM, Simpson RJ, Moritz RL, Cary D, Richardson R, Hausmann G, et al. (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 USA 96:2071-2076.