Syk-mediated tyrosine phosphorylation of mule promotes TNF-induced JNK activation and cell death

Oncogene

Volumn 35, Issue 15, 2016, Pages 1988-1995

  Lee, C K ^a   Yang, Y ^b   Chen, C ^a   Liu, J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LIGASE; PROTEIN KINASE SYK; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MIZ1; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG; CDKN2A PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; HUWE1 PROTEIN, HUMAN; HUWE1 PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; MIZ1 PROTEIN, MOUSE; NUCLEAR PROTEIN; PROTEASOME; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN TYROSINE KINASE; SIGNAL PEPTIDE; SMALL INTERFERING RNA; SYK PROTEIN, HUMAN; SYK PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE; ZBTB17 PROTEIN, HUMAN;

ARTICLE; CELL DEATH; CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; MULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; APOPTOSIS; CELL LINE; ENZYME ACTIVATION; FIBROBLAST; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; APOPTOSIS; CELL LINE; CYCLIN-DEPENDENT KINASE INHIBITOR P16; ENZYME ACTIVATION; FIBROBLASTS; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MAP KINASE SIGNALING SYSTEM; MICE; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-TYROSINE KINASES; PROTEOLYSIS; RNA, SMALL INTERFERING; SYK KINASE; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84937928120     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.275     Document Type: Article

References (57)

1. Tartaglia LA, Goeddel DV. Two TNF receptors. Immunol Today 1992; 13: 151-153
2. Tracey KJ, Cerami A. Tumor necrosis factor: a pleiotropic cytokine and therapeutic target. Annu Rev Med 1994; 45: 491-503
3. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998; 281: 1305-1308
4. Hibi M, Lin A, Smeal T, Minden A, Karin M. Identification of an oncoprotein-and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 1993; 7: 2135-2148
5. Kyriakis JM, Banerjee P, Nikolakaki E, Dai T, Rubie EA, Ahmad MF, et al. The stressactivated protein kinase subfamily of c-Jun kinases. Nature 1994; 369: 156-160
6. Liu Y, Guyton KZ, Gorospe M, Xu Q, Lee JC, Holbrook NJ. Differential activation of ERK, JNK/SAPK and P38/CSBP/RK map kinase family members during the cellular response to arsenite. Free Radic Biol Med 1996; 21: 771-781
7. Tada K, Okazaki T, Sakon S, Kobarai T, Kurosawa K, Yamaoka S, et al. Critical roles of TRAF2 and TRAF5 in tumor necrosis factor-induced NF-kappa B activation and protection from cell death. J Biol Chem 2001; 276: 36530-36534
8. Yeh KW, Chen JC, Lin MI, Chen YM, Lin CY. Functional activity of sporamin from sweet potato (Ipomoea batatas Lam.): a tuber storage protein with trypsin inhibitory activity. Plant Mol Biol 1997; 33: 565-570
9. Liu ZG, Hsu H, Goeddel DV, Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 1996; 87: 565-576
10. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003; 114: 181-190
11. Yeh WC, Shahinian A, Speiser D, Kraunus J, Billia F, Wakeham A, et al. Early lethality, functional NF-kappaB activation, and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice. Immunity 1997; 7: 715-725
12. Takada Y, Aggarwal BB. TNF activates Syk protein tyrosine kinase leading to TNFinduced MAPK activation, NF-kappaB activation, and apoptosis. J Immunol 2004; 173: 1066-1077
13. Mocsai A, Abram CL, Jakus Z, Hu Y, Lanier LL, Lowell CA. Integrin signaling in neutrophils and macrophages uses adaptors containing immunoreceptor tyrosine-based activation motifs. Nat Immunol 2006; 7: 1326-1333
14. Mocsai A, Humphrey MB, Van Ziffle JA, Hu Y, Burghardt A, Spusta SC, et al. The immunomodulatory adapter proteins DAP12 and Fc receptor gamma-chain (FcRgamma) regulate development of functional osteoclasts through the Syk tyrosine kinase. Proc Natl Acad Sci USA 2004; 101: 6158-6163
15. Mocsai A, Zhou M, Meng F, Tybulewicz VL, Lowell CA. Syk is required for integrin signaling in neutrophils. Immunity 2002; 16: 547-558
16. Obergfell A, Eto K, Mocsai A, Buensuceso C, Moores SL, Brugge JS, et al. Coordinate interactions of Csk, Src, and Syk kinases with [alpha]IIb[beta]3 initiate integrin signaling to the cytoskeleton. J Cell Biol 2002; 157: 265-275
17. Poole A, Gibbins JM, Turner M, van Vugt MJ, van de Winkel JG, Saito T, et al. The Fc receptor gamma-chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. EMBO J 1997; 16: 2333-2341
18. Vines CM, Potter JW, Xu Y, Geahlen RL, Costello PS, Tybulewicz VL, et al. Inhibition of beta 2 integrin receptor and Syk kinase signaling in monocytes by the Src family kinase Fgr. Immunity 2001; 15: 507-519
19. Chen D, Kon N, Li M, Zhang W, Qin J, Gu W. ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell 2005; 121: 1071-1083
20. Adhikary S, Marinoni F, Hock A, Hulleman E, Popov N, Beier R, et al. The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 2005; 123: 409-421
21. Hall JR, Kow E, Nevis KR, Lu CK, Luce KS, Zhong Q, et al. Cdc6 stability is regulated by the Huwe1 ubiquitin ligase after DNA damage. Mol Biol Cell 2007; 18: 3340-3350
22. Herold S, Hock A, Herkert B, Berns K, Mullenders J, Beijersbergen R, et al. Miz1 and HectH9 regulate the stability of the checkpoint protein, TopBP1. EMBO J 2008; 27: 2851-2861
23. Liu Z, Oughtred R, Wing SS. Characterization of E3Histone, a novel testis ubiquitin protein ligase which ubiquitinates histones. Mol Cell Biol 2005; 25: 2819-2831
24. Noy T, Suad O, Taglicht D, Ciechanover A. HUWE1 ubiquitinates MyoD and targets it for proteasomal degradation. Biochem Biophys Res Commun 2012; 418: 408-413
25. Parsons JL, Tait PS, Finch D, Dianova II, Edelmann MJ, Khoronenkova SV, et al. Ubiquitin ligase ARF-BP1/Mule modulates base excision repair. EMBO J 2009; 28: 3207-3215
26. Yang Y, Do H, Tian X, Zhang C, Liu X, Dada LA, et al. E3 ubiquitin ligase Mule ubiquitinates Miz1 and is required for TNFalpha-induced JNK activation. Proc Natl Acad Sci USA 2010; 107: 13444-13449
27. Zhong Q, Gao W, Du F, Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 2005; 121: 1085-1095
28. Kosan C, Saba I, Godmann M, Herold S, Herkert B, Eilers M, et al. Transcription factor miz-1 is required to regulate interleukin-7 receptor signaling at early commitment stages of B cell differentiation. Immunity 2010; 33: 917-928
29. Peukert K, Staller P, Schneider A, Carmichael G, Hanel F, Eilers M. An alternative pathway for gene regulation by Myc. EMBO J 1997; 16: 5672-5686
30. Wanzel M, Kleine-Kohlbrecher D, Herold S, Hock A, Berns K, Park J, et al. Akt and 14-3-3eta regulate Miz1 to control cell-cycle arrest after DNA damage. Nat Cell Biol 2005; 7: 30-41
31. Do-Umehara HC, Chen C, Urich D, Zhou L, Qiu J, Jang S, et al. Suppression of inflammation and acute lung injury by Miz1 via repression of C/EBP-delta. Nat Immunol 2013; 14: 461-469
32. Liu J, Zhao Y, Eilers M, Lin A, Herold S, Hock A, et al. Miz1 is a signal-and pathwayspecific modulator or regulator (SMOR) that suppresses TNF-alpha-induced JNK1 activation. Proc Natl Acad Sci USA 2009; 106: 18279-18284
33. Itahana K, Bhat KP, Jin A, Itahana Y, Hawke D, Kobayashi R, et al. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol Cell 2003; 12: 1151-1164
34. Bertwistle D, Sugimoto M, Sherr CJ. Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23. Mol Cell Biol 2004; 24: 985-996
35. de Stanchina E, McCurrach ME, Zindy F, Shieh SY, Ferbeyre G, Samuelson AV, et al. E1A signaling to p53 involves the p19(ARF) tumor suppressor. Genes Dev 1998; 12: 2434-2442
36. Khan SH, Moritsugu J, Wahl GM. Differential requirement for p19ARF in the p53-dependent arrest induced by DNA damage, microtubule disruption, and ribonucleotide depletion. Proc Natl Acad Sci USA 2000; 97: 3266-3271
37. Abida WM, Gu W. p53-Dependent and p53-independent activation of autophagy by ARF. Cancer Res 2008; 68: 352-357
38. Reef S, Zalckvar E, Shifman O, Bialik S, Sabanay H, Oren M, et al. A short mitochondrial form of p19ARF induces autophagy and caspase-independent cell death. Mol Cell 2006; 22: 463-475
39. Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M, et al. Inhibition of JNK activation through NF-kappaB target genes. Nature 2001; 414: 313-317
40. Cheng PL, Lu H, Shelly M, Gao H, Poo MM. Phosphorylation of E3 ligase Smurf1 switches its substrate preference in support of axon development. Neuron 2011; 69: 231-243
41. Gallagher E, Gao M, Liu YC, Karin M. Activation of the E3 ubiquitin ligase Itch through a phosphorylation-induced conformational change. Proc Natl Acad Sci USA 2006; 103: 1717-1722
42. Gao M, Labuda T, Xia Y, Gallagher E, Fang D, Liu YC, et al. Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science 2004; 306: 271-275
43. Rotin D, Kumar S. Physiological functions of the HECT family of ubiquitin ligases. Nat Rev Mol Cell Biol 2009; 10: 398-409
44. Gu J, Dubner R, Fornace AJ Jr, Iadarola MJ. UREB1, a tyrosine phosphorylated nuclear protein, inhibits p53 transactivation. Oncogene 1995; 11: 2175-2178
45. Gu J, Ren K, Dubner R, Iadarola MJ. Cloning of a DNA binding protein that is a tyrosine kinase substrate and recognizes an upstream initiator-like sequence in the promoter of the preprodynorphin gene. Brain Res Mol Brain Res 1994; 24: 77-88
46. Hsu H, Shu HB, Pan MG, Goeddel DV. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 1996; 84: 299-308
47. Takeuchi M, Rothe M, Goeddel DV. Anatomy of TRAF2. Distinct domains for nuclear factor-kappaB activation and association with tumor necrosis factor signaling proteins. J Biol Chem 1996; 271: 19935-19942
48. Honda R, Yasuda H. Association of p19(ARF) with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53. EMBO J 1999; 18: 22-27
49. Rocha S, Campbell KJ, Perkins ND. p53-and Mdm2-independent repression of NF-kappa B transactivation by the ARF tumor suppressor. Mol Cell 2003; 12: 15-25
50. Inoue S, Hao Z, Elia AJ, Cescon D, Zhou L, Silvester J, et al. Mule/Huwe1/Arf-BP1 suppresses Ras-driven tumorigenesis by preventing c-Myc/Miz1-mediated downregulation of p21 and p15. Genes Dev 2013; 27: 1101-1114
51. Sherr CJ. Divorcing ARF and p53: an unsettled case. Nat Rev Cancer 2006; 6: 663-673
52. Gu J, Ren K, Dubner R, Iadarola MJ. Cloning of a DNA binding protein that is a tyrosine kinase substrate and recognizes an upstream initiator-like sequence in the promoter of the preprodyorphin gene. Mol Brain Res 1994; 24: 77-88
53. Gu J, Dubner R, Fornace AJ Jr, Iadarola MJ. UREB1, a tyrosine phosphorylated nuclear protein, inhibits p53 transactivation. Oncogene 1995; 11: 2175-2178
54. Liu J, Yan J, Jiang S, Wen J, Chen L, Zhao Y, et al. Site-specific ubiquitination is required for relieving the transcription factor Miz1-mediated suppression on TNF-alpha-induced JNK activation and inflammation. Proc Natl Acad Sci USA 2012; 109: 191-196
55. Liu J, Minemoto Y, Lin A. c-Jun N-terminal protein kinase 1 (JNK1), but not JNK2, is essential for tumor necrosis factor alpha-induced c-Jun kinase activation and apoptosis. Mol Cell Biol 2004; 24: 10844-10856
56. Lin A, Minden A, Martinetto H, Claret FX, Lange-Carter C, Mercurio F, et al. Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science 1995; 268: 286-290
57. Liu J, Yang D, Minemoto Y, Leitges M, Rosner MR, Lin A. NF-kappaB is required for UV-induced JNK activation via induction of PKCdelta. Mol Cell 2006; 21: 467-480