The ubiquitin-editing enzyme A20 requires RNF11 to downregulate NF-κB signalling

EMBO Journal

Volumn 28, Issue 5, 2009, Pages 513-522

  Shembade, Noula ^a   Parvatiyar, Kislay ^a   Harhaj, Nicole S ^a   Harhaj, Edward W ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

A20; Itch; NF B; RNF11; TAX1BP1

Indexed keywords

ENZYME; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ITCH PROTEIN; LIPOPOLYSACCHARIDE; PROTEIN DERIVATIVE; REGULATOR PROTEIN; RING FINGER PROTEIN; RING FINGER PROTEIN 11; RIP1 PROTEIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TAX1BP1 PROTEIN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN; UBIQUITIN EDITING ENZYME A20; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; STIMULUS; UBIQUITINATION;

CARRIER PROTEINS; CELL LINE; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPOLYSACCHARIDES; MONOCYTES; NEOPLASM PROTEINS; NF-KAPPA B; NUCLEAR PORE COMPLEX PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 61949220270     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2008.285     Document Type: Article

References (41)

1. Anderson LR, Betarbet R, Gearing M, Gulcher J, Hicks AA, Stefansson K, Lah JJ, Levey AI (2007) PARK10 candidate RNF11 is expressed by vulnerable neurons and localizes to Lewy bodies in Parkinson disease brain. J Neuropathol Exp Neurol 66: 955-964
2. Azmi P, Seth A (2005) RNF11 is a multifunctional modulator of growth factor receptor signalling and transcriptional regulation. Eur J Cancer 41: 2549-2560
3. Bohgaki M, Tsukiyama T, Nakajima A, Maruyama S, Watanabe M, Koike T, Hatakeyama S (2008) Involvement of Ymer in suppression of NF-κB activation by regulated interaction with lysine-63-linked polyubiquitin chain. Biochim Biophys Acta 1783: 826-837
4. Boone DL, Turer EE, Lee EG, Ahmad RC, Wheeler MT, Tsui C, Hurley P, Chien M, Chai S, Hitotsumatsu O, McNally E, Pickart C, Ma A (2004) The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 5: 1052-1060
5. Burger A, Li H, Zhang XK, Pienkowska M, Venanzoni M, Vournakis J, Papas T, Seth A (1998) Breast cancer genome anatomy: correlation of morphological changes in breast carcinomas with expression of the novel gene product Di12. Oncogene 16: 327-333
6. Chen ZJ (2005) Ubiquitin signalling in the NF-κB pathway. Nat Cell Biol 7: 758-765
7. Colland F, Jacq X, Trouplin V, Mougin C, Groizeleau C, Hamburger A, Meil A, Wojcik J, Legrain P, Gauthier JM (2004) Functional proteomics mapping of a human signaling pathway. Genome Res 14: 1324-1332
8. Connor MK, Seth A (2004) A central role for the ring finger protein RNF11 in ubiquitin-mediated proteolysis via interactions with E2s and E3s. Oncogene 23: 2089-2095
9. De Valck D, Jin DY, Heyninck K, Van de Craen M, Contreras R, Fiers W, Jeang KT, Beyaert R (1999) The zinc finger protein A20 interacts with a novel anti-apoptotic protein which is cleaved by specific caspases. Oncogene 18: 4182-4190
10. Dhawan P, Richmond A (2002) A novel NF-κB-inducing kinase-MAPK signaling pathway up-regulates NF-κB activity in melanoma cells. J Biol Chem 277: 7920-7928
11. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ (2006) Activation of IKK by TNFα requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 22: 245-257
12. Evans PC, Ovaa H, Hamon M, Kilshaw PJ, Hamm S, Bauer S, Ploegh HL, Smith TS (2004) Zinc-finger protein A20, a regulator of inflammation and cell survival, has de-ubiquitinating activity. Biochem J 378 (Part 3): 727-734
13. Hacker H, Karin M (2006) Regulation and function of IKK and IKK-related kinases. Sci STKE 2006: re13
14. Harhaj NS, Janic B, Ramos JC, Harrington Jr WJ, Harhaj EW (2007a) Deregulated expression of CD40 ligand in HTLV-I infection: distinct mechanisms of downregulation in HTLV-I-transformed cell lines and ATL patients. Virology 362: 99-108
15. Harhaj NS, Sun SC, Harhaj EW (2007b) Activation of NF-κB by the human T cell leukemia virus type I Tax oncoprotein is associated with ubiquitin-dependent relocalization of IκB kinase. J Biol Chem 282: 4185-4192
16. Hayden MS, Ghosh S (2008) Shared principles in NF-κB signaling. Cell 132: 344-362
17. Iha H, Peloponese JM, Verstrepen L, Zapart G, Ikeda F, Smith CD, Starost MF, Yedavalli V, Heyninck K, Dikic I, Beyaert R, Jeang KT (2008) Inflammatory cardiac valvulitis in TAX1BP1-deficient mice through selective NF-κB activation. EMBO J 27: 629-641
18. Jono H, Lim JH, Chen LF, Xu H, Trompouki E, Pan ZK, Mosialos G, Li JD (2004) NF-κB is essential for induction of CLD, the negative regulator of NF-κB: evidence for a novel inducible autoregulatory feedback pathway. J Biol Chem 279: 36171-36174
19. Karin M, Ben-Neriah Y (2000) Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu Rev Immunol 18: 621-663
20. Karin M, Greten FR (2005) NF-κB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5: 749-759
21. Kitching R, Wong MJ, Koehler D, Burger AM, Landberg G, Gish G, Seth A (2003) The RING-H2 protein RNF11 is differentially expressed in breast tumours and interacts with HECT-type E3 ligases. Biochim Biophys Acta 1639: 104-112
22. Krikos A, Laherty CD, Dixit VM (1992) Transcriptional activation of the tumor necrosis factor alpha-inducible zinc finger protein, A20, is mediated by kappa B elements. J Biol Chem 267: 17971-17976
23. Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP, Ma A (2000) Failure to regulate TNF-induced NF-κB and cell death responses in A20-deficient mice. Science 289: 2350-2354
24. Lee TL, Shyu YC, Hsu TY, Shen CK (2008) Itch regulates p45/NF-E2 in vivo by Lys63-linked ubiquitination. Biochem Biophys Res Commun 375: 326-330
25. Li H, Seth A (2004) An RNF11: Smurf2 complex mediates ubiquitination of the AMSH protein. Oncogene 23: 1801-1808
26. Li MO, Flavell RA (2008) Contextual regulation of inflammation: a duet by transforming growth factor-beta and interleukin-10. Immunity 28: 468-476
27. Mauro C, Pacifico F, Lavorgna A, Mellone S, Iannetti A, Acquaviva R, Formisano S, Vito P, Leonardi A (2006) ABIN-1 binds to NEMO/IKKγ and co-operates with A20 in inhibiting NF-κB. J Biol Chem 281: 18482-18488
28. Oliver PM, Cao X, Worthen GS, Shi P, Briones N, Macleod M, White J, Kirby P, Kappler J, Marrack P, Yang B (2006) Ndfip1 protein promotes the function of itch ubiquitin ligase to prevent T cell activation and T helper 2 cell-mediated inflammation. Immunity 25: 929-940
29. Saitoh Y, Yamamoto N, Dewan MZ, Sugimoto H, Martinez BV, Iwasaki Y, Matsubara K, Qi X, Saitoh T, Imoto I, Inazawa J, Utsunomiya A, Watanabe T, Masuda T, Yamamoto N, Yamaoka S (2008) Overexpressed NF-κB inducing kinase contributes to the tumorigenesis of adult T-cell leukemia and Hodgkin Reed-Sternberg cells. Blood 111: 5118-5129
30. Seki N, Hattori A, Hayashi A, Kozuma S, Sasaki M, Suzuki Y, Sugano S, Muramatsu MA, Saito T (1999) Cloning and expression profile of mouse and human genes, Rnf11/RNF11, encoding a novel RING-H2 finger protein. Biochim Biophys Acta 1489: 421-427
31. Shembade N, Harhaj NS, Liebl DJ, Harhaj EW (2007a) Essential role for TAX1BP1 in the termination of TNF-α-, IL-1- and LPS-mediated NF-κB and JNK signaling. EMBO J 26: 3910-3922
32. Shembade N, Harhaj NS, Parvatiyar K, Copeland NG, Jenkins NA, Matesic LE, Harhaj EW (2008) The E3 ligase Itch negatively regulates inflammatory signaling pathways by controlling the function of the ubiquitin-editing enzyme A20. Nat Immunol 9: 254-262
33. Shembade N, Harhaj NS, Yamamoto M, Akira S, Harhaj EW (2007b) The human T-cell leukemia virus type 1 Tax oncoprotein requires the ubiquitin-conjugating enzyme Ubc13 for NF-κB activation. J Virol 81: 13735-13742
34. Subramaniam V, Li H, Wong M, Kitching R, Attisano L, Wrana J, Zubovits J, Burger AM, Seth A (2003) The RING-H2 protein RNF11 is overexpressed in breast cancer and is a target of Smurf2 E3 ligase. Br J Cancer 89: 1538-1544
35. Sudol M, Chen HI, Bougeret C, Einbond A, Bork P (1995) Characterization of a novel protein-binding module - the WW domain. FEBS Lett 369: 67-71
36. Sun SC (2008) Deubiquitylation and regulation of the immune response. Nat Rev Immunol 8: 501-511
37. Sun SC, Ganchi PA, Ballard DW, Greene WC (1993) NF-κB controls expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway. Science 259: 1912-1915
38. Vendrell JA, Ghayad S, Ben-Larbi S, Dumontet C, Mechti N, Cohen PA (2007) A20/TNFAIP3, a new estrogen-regulated gene that confers tamoxifen resistance in breast cancer cells. Oncogene 26: 4656-4667
39. Waterfield MR, Zhang M, Norman LP, Sun SC (2003) NF-κB1/p105 regulates lipopolysaccharide-stimulated MAP kinase signaling by governing the stability and function of the Tpl2 kinase. Mol Cell 11: 685-694
40. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, Wu P, Wiesmann C, Baker R, Boone DL, Ma A, Koonin EV, Dixit VM (2004) De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-κB signalling. Nature 430: 694-699
41. Xiao G, Harhaj EW, Sun SC (2001) NF-κB-inducing kinase regulates the processing of NF-κB2 p100. Mol Cell 7: 401-409