Ubiquitin Binding to A20 ZnF4 Is Required for Modulation of NF-κB Signaling

Molecular Cell

Volumn 40, Issue 4, 2010, Pages 548-557

  Bosanac, Ivan ^a   Wertz, Ingrid E ^a   Pan, Borlan ^a   Yu, Christine ^a   Kusam, Saritha ^a   Lam, Cynthia ^a   Phu, Lilian ^a   Phung, Qui ^a   Maurer, Brigitte ^a   Arnott, David ^a   Kirkpatrick, Donald S ^a   Dixit, Vishva M ^a   Hymowitz, Sarah G ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN; PROTEIN A20; UBIQUITIN; UNCLASSIFIED DRUG; ZINC FINGER 4 PROTEIN; ZINC FINGER PROTEIN;

ARTICLE; HEMATOLOGIC MALIGNANCY; INFLAMMATORY DISEASE; OVARY TUMOR; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; SIGNAL TRANSDUCTION;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; LYSINE; MODELS, MOLECULAR; MUTATION; NF-KAPPA B; NUCLEAR PROTEINS; POLYUBIQUITIN; PROTEIN BINDING; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; ZINC FINGERS;

EID: 78649292467     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.10.009     Document Type: Article

References (51)

1. Blankenship J.W., Varfolomeev E., Goncharov T., Fedorova A.V., Kirkpatrick D.S., Izrael-Tomasevic A., Phu L., Arnott D., Aghajan M., Zobel K., et al. Ubiquitin binding modulates IAP antagonist-stimulated proteasomal degradation of c-IAP1 and c-IAP2(1). Biochem. J. 2009, 417:149-160.
2. Brzovic P.S., Lissounov A., Christensen D.E., Hoyt D.W., Klevit R.E. A UbcH5/ubiquitin noncovalent complex is required for processive BRCA1-directed ubiquitination. Mol. Cell 2006, 21:873-880.
3. Capili A.D., Lima C.D. Structure and analysis of a complex between SUMO and Ubc9 illustrates features of a conserved E2-Ubl interaction. J. Mol. Biol. 2007, 369:608-618.
4. Compagno M., Lim W.K., Grunn A., Nandula S.V., Brahmachary M., Shen Q., Bertoni F., Ponzoni M., Scandurra M., Califano A., et al. Mutations of multiple genes cause deregulation of NF-kappaB in diffuse large B-cell lymphoma. Nature 2009, 459:717-721.
5. Coornaert B., Baens M., Heyninck K., Bekaert T., Haegman M., Staal J., Sun L., Chen Z.J., Marynen P., Beyaert R. T cell antigen receptor stimulation induces MALT1 paracaspase-mediated cleavage of the NF-kappaB inhibitor A20. Nat. Immunol. 2008, 9:263-271.
6. Coornaert B., Carpentier I., Beyaert R. A20: central gatekeeper in inflammation and immunity. J. Biol. Chem. 2009, 284:8217-8221.
7. De Valck D., Jin D.Y., Heyninck K., Van de Craen M., Contreras R., Fiers W., Jeang K.T., Beyaert R. The zinc finger protein A20 interacts with a novel anti-apoptotic protein which is cleaved by specific caspases. Oncogene 1999, 18:4182-4190.
8. Duda D.M., van Waardenburg R.C., Borg L.A., McGarity S., Nourse A., Waddell M.B., Bjornsti M.A., Schulman B.A. Structure of a SUMO-binding-motif mimic bound to Smt3p-Ubc9p: conservation of a non-covalent ubiquitin-like protein-E2 complex as a platform for selective interactions within a SUMO pathway. J. Mol. Biol. 2007, 369:619-630.
9. Eddins M.J., Carlile C.M., Gomez K.M., Pickart C.M., Wolberger C. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat. Struct. Mol. Biol. 2006, 13:915-920.
10. Evans P.C., Ovaa H., Hamon M., Kilshaw P.J., Hamm S., Bauer S., Ploegh H.L., Smith T.S. Zinc-finger protein A20, a regulator of inflammation and cell survival, has de-ubiquitinating activity. Biochem. J. 2004, 378:727-734.
11. Garnett M.J., Mansfeld J., Godwin C., Matsusaka T., Wu J., Russell P., Pines J., Venkitaraman A.R. UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit. Nat. Cell Biol. 2009, 11:1363-1369.
12. Graham R.R., Cotsapas C., Davies L., Hackett R., Lessard C.J., Leon J.M., Burtt N.P., Guiducci C., Parkin M., Gates C., et al. Genetic variants near TNFAIP3 on 6q23 are associated with systemic lupus erythematosus. Nat. Genet. 2008, 40:1059-1061.
13. Harper J.W., Schulman B.A. Structural complexity in ubiquitin recognition. Cell 2006, 124:1133-1136.
14. Hicke L., Schubert H.L., Hill C.P. Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 2005, 6:610-621.
15. Honma K., Tsuzuki S., Nakagawa M., Tagawa H., Nakamura S., Morishima Y., Seto M. TNFAIP3/A20 functions as a novel tumor suppressor gene in several subtypes of non-Hodgkin lymphomas. Blood 2009, 114:2467-2475.
16. Hurley J.H., Lee S., Prag G. Ubiquitin-binding domains. Biochem. J. 2006, 399:361-372.
17. Hymowitz S.G., Wertz I.E. A20: from ubiquitin editing to tumour suppression. Nat. Rev. Cancer 2010, 10:332-341.
18. Iha H., Peloponese J.M., Verstrepen L., Zapart G., Ikeda F., Smith C.D., Starost M.F., Yedavalli V., Heyninck K., Dikic I., et al. Inflammatory cardiac valvulitis in TAX1BP1-deficient mice through selective NF-kappaB activation. EMBO J. 2008, 27:629-641.
19. Iwai K., Tokunaga F. Linear polyubiquitination: a new regulator of NF-kappaB activation. EMBO Rep. 2009, 10:706-713.
20. Jin L., Williamson A., Banerjee S., Philipp I., Rape M. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 2008, 133:653-665.
21. Kato M., Sanada M., Kato I., Sato Y., Takita J., Takeuchi K., Niwa A., Chen Y., Nakazaki K., Nomoto J., et al. Frequent inactivation of A20 in B-cell lymphomas. Nature 2009, 459:712-716.
22. Kirkpatrick D.S., Hathaway N.A., Hanna J., Elsasser S., Rush J., Finley D., King R.W., Gygi S.P. Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nat. Cell Biol. 2006, 8:700-710.
23. Knipscheer P., van Dijk W.J., Olsen J.V., Mann M., Sixma T.K. Noncovalent interaction between Ubc9 and SUMO promotes SUMO chain formation. EMBO J. 2007, 26:2797-2807.
24. Komander D., Barford D. Structure of the A20 OTU domain and mechanistic insights into deubiquitination. Biochem. J. 2008, 409:77-85.
25. Kulathu Y., Akutsu M., Bremm A., Hofmann K., Komander D. Two-sided ubiquitin binding explains specificity of the TAB2 NZF domain. Nat. Struct. Mol. Biol. 2009, 16:1328-1330.
26. Lee E.G., Boone D.L., Chai S., Libby S.L., Chien M., Lodolce J.P., Ma A. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 2000, 289:2350-2354.
27. Lee S., Tsai Y.C., Mattera R., Smith W.J., Kostelansky M.S., Weissman A.M., Bonifacino J.S., Hurley J.H. Structural basis for ubiquitin recognition and autoubiquitination by Rabex-5. Nat. Struct. Mol. Biol. 2006, 13:264-271.
28. Lin S.C., Chung J.Y., Lamothe B., Rajashankar K., Lu M., Lo Y.C., Lam A.Y., Darnay B.G., Wu H. Molecular basis for the unique deubiquitinating activity of the NF-kappaB inhibitor A20. J. Mol. Biol. 2008, 376:526-540.
29. Lo Y.C., Lin S.C., Rospigliosi C.C., Conze D.B., Wu C.J., Ashwell J.D., Eliezer D., Wu H. Structural basis for recognition of diubiquitins by NEMO. Mol. Cell 2009, 33:602-615.
30. Mattera R., Tsai Y.C., Weissman A.M., Bonifacino J.S. The Rab5 guanine nucleotide exchange factor Rabex-5 binds ubiquitin (Ub) and functions as a Ub ligase through an atypical Ub-interacting motif and a zinc finger domain. J. Biol. Chem. 2006, 281:6874-6883.
31. Musone S.L., Taylor K.E., Lu T.T., Nititham J., Ferreira R.C., Ortmann W., Shifrin N., Petri M.A., Kamboh M.I., Manzi S., et al. Multiple polymorphisms in the TNFAIP3 region are independently associated with systemic lupus erythematosus. Nat. Genet. 2008, 40:1062-1064.
32. Newton K., Matsumoto M.L., Wertz I.E., Kirkpatrick D.S., Lill J.R., Tan J., Dugger D., Gordon N., Sidhu S.S., Fellouse F.A., et al. Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 2008, 134:668-678.
33. Novak U., Rinaldi A., Kwee I., Nandula S.V., Rancoita P.M., Compagno M., Cerri M., Rossi D., Murty V.V., Zucca E., et al. The NF-κB negative regulator TNFAIP3 (A20) is inactivated by somatic mutations and genomic deletions in marginal zone lymphomas. Blood 2009, 113:4918-4921.
34. Opipari A.W., Boguski M.S., Dixit V.M. The A20 cDNA induced by tumor necrosis factor alpha encodes a novel type of zinc finger protein. J. Biol. Chem. 1990, 265:14705-14708.
35. Penengo L., Mapelli M., Murachelli A.G., Confalonieri S., Magri L., Musacchio A., Di Fiore P.P., Polo S., Schneider T.R. Crystal structure of the ubiquitin binding domains of rabex-5 reveals two modes of interaction with ubiquitin. Cell 2006, 124:1183-1195.
36. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70:503-533.
37. Plenge R.M., Cotsapas C., Davies L., Price A.L., de Bakker P.I., Maller J., Pe'er I., Burtt N.P., Blumenstiel B., DeFelice M., et al. Two independent alleles at 6q23 associated with risk of rheumatoid arthritis. Nat. Genet. 2007, 39:1477-1482.
38. Rahighi S., Ikeda F., Kawasaki M., Akutsu M., Suzuki N., Kato R., Kensche T., Uejima T., Bloor S., Komander D., et al. Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell 2009, 136:1098-1109.
39. Sakata E., Satoh T., Yamamoto S., Yamaguchi Y., Yagi-Utsumi M., Kurimoto E., Tanaka K., Wakatsuki S., Kato K. Crystal structure of UbcH5b∼ubiquitin intermediate: insight into the formation of the self-assembled E2∼Ub conjugates. Structure 2010, 18:138-147.
40. Sato Y., Yoshikawa A., Yamashita M., Yamagata A., Fukai S. Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by NZF domains of TAB2 and TAB3. EMBO J. 2009, 28:3903-3909.
41. Schmitz R., Hansmann M.L., Bohle V., Martin-Subero J.I., Hartmann S., Mechtersheimer G., Klapper W., Vater I., Giefing M., Gesk S., et al. TNFAIP3 (A20) is a tumor suppressor gene in Hodgkin lymphoma and primary mediastinal B cell lymphoma. J. Exp. Med. 2009, 206:981-989.
42. Shembade N., Harhaj N.S., Liebl D.J., Harhaj E.W. Essential role for TAX1BP1 in the termination of TNF-alpha-, IL-1- and LPS-mediated NF-kappaB and JNK signaling. EMBO J. 2007, 26:3910-3922.
43. Shembade N., Harhaj N.S., Parvatiyar K., Copeland N.G., Jenkins N.A., Matesic L.E., Harhaj E.W. The E3 ligase Itch negatively regulates inflammatory signaling pathways by controlling the function of the ubiquitin-editing enzyme A20. Nat. Immunol. 2008, 9:254-262.
44. Shembade N., Parvatiyar K., Harhaj N.S., Harhaj E.W. The ubiquitin-editing enzyme A20 requires RNF11 to downregulate NF-kappaB signalling. EMBO J. 2009, 28:513-522.
45. Shembade N., Ma A., Harhaj E.W. Inhibition of NF-kappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 2010, 327:1135-1139.
46. Thomson W., Barton A., Ke X., Eyre S., Hinks A., Bowes J., Donn R., Symmons D., Hider S., Bruce I.N., et al. Rheumatoid arthritis association at 6q23. Nat. Genet. 2007, 39:1431-1433. Wellcome Trust Case Control Consortium, YEAR ConsortiumYEAR Consortium.
47. Van Huffel S., Delaei F., Heyninck K., De Valck D., Beyaert R. Identification of a novel A20-binding inhibitor of nuclear factor-κ B activation termed ABIN-2. J. Biol. Chem. 2001, 276:30216-30223.
48. Vijay-Kumar S., Bugg C.E., Cook W.J. Structure of ubiquitin refined at 1.8 A resolution. J. Mol. Biol. 1987, 194:531-544.
49. Wertz I.E., O'Rourke K.M., Zhou H., Eby M., Aravind L., Seshagiri S., Wu P., Wiesmann C., Baker R., Boone D.L., et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004, 430:694-699.
50. Williamson A., Wickliffe K.E., Mellone B.G., Song L., Karpen G.H., Rape M. Identification of a physiological E2 module for the human anaphase-promoting complex. Proc. Natl. Acad. Sci. USA 2009, 106:18213-18218.
51. Xu P., Duong D.M., Seyfried N.T., Cheng D., Xie Y., Robert J., Rush J., Hochstrasser M., Finley D., Peng J. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009, 137:133-145.