OTUB1 modulates c-IAP1 stability to regulate signalling pathways

EMBO Journal

Volumn 32, Issue 8, 2013, Pages 1103-1114

  Goncharov, Tatiana ^a   Niessen, Kyle ^a   De Almagro, Maria Cristina ^a   Izrael Tomasevic, Anita ^a   Fedorova, Anna V ^a   Varfolomeev, Eugene ^a   Arnott, David ^a   Deshayes, Kurt ^a   Kirkpatrick, Donald S ^a   Vucic, Domagoj ^a  

^a GENENTECH INC   (United States)

Author keywords

c IAP1; DUB; OTUB1; TWEAK; ubiquitin

Indexed keywords

BIRC2 PROTEIN; CASPASE; CELLULAR INHIBITOR OF APOPTOSIS 1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; OTUB1 PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL VIABILITY; DOWN REGULATION; ENZYME DEGRADATION; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UBIQUITINATION; ZEBRA FISH;

ANIMALS; BLOOD VESSELS; CELL LINE; CYSTEINE ENDOPEPTIDASES; HUMANS; HYDROLYSIS; INHIBITOR OF APOPTOSIS PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NF-KAPPA B; SIGNAL TRANSDUCTION; UBIQUITIN; ZEBRAFISH;

DANIO RERIO;

EID: 84876412379     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.62     Document Type: Article

References (44)

1. Annunziata CM, Davis RE, Demchenko Y, Bellamy W, Gabrea A, Zhan F, Lenz G, Hanamura I, Wright G, Xiao W, Dave S, Hurt EM, Tan B, Zhao H, Stephens O, Santra M, Williams DR, Dang L, Barlogie B, Shaughnessy Jr. JD et al (2007) Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 12: 115-130
2. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J, Gillard JW, Jaquith JB, Morris SJ, Barker PA (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 30: 689-700
3. Blankenship JW, Varfolomeev E, Goncharov T, Fedorova AV, Kirkpatrick DS, Izrael-Tomasevic A, Phu L, Arnott D, Aghajan M, Zobel K, Bazan JF, Fairbrother WJ, Deshayes K, Vucic D (2009) Ubiquitin binding modulates IAP antagonist-stimulated proteasomal degradation of c-IAP1 and c-IAP2. Biochem J 417: 149-160
4. Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78: 399-434
5. Dynek JN, Goncharov T, Dueber EC, Fedorova AV, Izrael-Tomasevic A, Phu L, Helgason E, Fairbrother WJ, Deshayes K, Kirkpatrick DS, Vucic D (2010) c-IAP1 and UbcH5 promote K11-linked poly-ubiquitination of RIP1 in TNF signalling. EMBO J 29: 4198-4209
6. Edelmann MJ, Iphofer A, Akutsu M, Altun M, di Gleria K, Kramer HB, Fiebiger E, Dhe-Paganon S, Kessler BM (2009) Structural basis and specificity of human otubain 1-mediated deubiquitina-tion. Biochem J 418: 379-390
7. Emmerich CH, Schmukle AC, Walczak H (2011) The emerging role of linear ubiquitination in cell signaling. Sci Signal 4: re5
8. Flygare JA, Beresini M, Budha N, Chan H, Chan IT, Cheeti S, Cohen F, Deshayes K, Doerner K, Eckhardt SG, Elliott LO, Feng B, Franklin MC, Reisner SF, Gazzard L, Halladay J, Hymowitz SG, La H, LoRusso P, Maurer B et al (2012) Discovery of a potent small-molecule antagonist of inhibitor of apoptosis (IAP) proteins and clinical candidate for the treatment of cancer (GDC-0152). J Med Chem 55: 4101-4113
9. Fulda S, Vucic D (2012) Targeting IAP proteins for therapeutic intervention in cancer. Nat Rev Drug Discov 11 : 109-124
10. Haas TL, Emmerich CH, Gerlach B, Schmukle AC, Cordier SM, Rieser E, Feltham R, Vince J, Warnken U, Wenger T, Koschny R, Komander D, Silke J, Walczak H (2009) Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol Cell 36: 831-844
11. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67: 425-479
12. Husnjak K, Dikic I (2012) Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu Rev Biochem 81: 291-322
13. Ikeda F, Dikic I (2008) Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: Beyond the Usual Suspects' review series. EMBO Rep 9: 536-542
14. Iwai K, Tokunaga F (2009) Linear polyubiquitination: a new regulator of NF-kappaB activation. EMBO Rep 10 : 706-713
15. Juang YC, Landry MC, Sanches M, Vittal V, Leung CC, Ceccarelli DF, Mateo AR, Pruneda JN, Mao DY, Szilard RK, Orlicky S, Munro M, Brzovic PS, Klevit RE, Sicheri F, Durocher D (2012) OTUB1 co-opts Lys48-linked ubiquitin recognition to suppress E2 enzyme function. Mol Cell 45: 384-397
16. Keats JJ, Fonseca R, Chesi M, Schop R, Baker A, Chng WJ, Van Wier S, Tiedemann R, Shi CX, Sebag M, Braggio E, Henry T, Zhu YX, Fogle H, Price-Troska T, Ahmann G, Mancini C, Brents LA, Kumar S, Greipp P et al (2007) Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma. Cancer Cell 12: 131-144
17. Li S, Zheng H, Mao AP, Zhong B, Li Y, Liu Y, Gao Y, Ran Y, Tien P, Shu HB (2010) Regulation of virus-triggered signaling by OTUB1-and OTUB2-mediated deubiquitination of TRAF3 and TRAF6. J Biol Chem 285: 4291-4297
18. Lobov IB, Cheung E, Wudali R, Cao J, Halasz G, Wei Y, Economides A, Lin HC, Papadopoulos N, Yancopoulos GD, Wiegand SJ (2011) The Dll4/Notch pathway controls postangiogenic blood vessel remodeling and regression by modulating vasoconstriction and blood flow. Blood 117: 6728-6737
19. Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104: 487-501
20. Matsumoto ML, Wickliffe KE, Dong KC, Yu C, Bosanac I, Bustos D, Phu L, Kirkpatrick DS, Hymowitz SG, Rape M, Kelley RF, Dixit VM (2010) K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol Cell 39: 477-484
21. Moulin M, Anderton H, Voss AK, Thomas T, Wong WW, Bankovacki A, Feltham R, Chau D, Cook WD, Silke J, Vaux DL (2012) IAPs limit activation of RIP kinases by TNF receptor 1 during development. EMBO J 31: 1679-1691
22. Nakada S, Tai I, Panier S, Al-Hakim A, Iemura S, Juang YC, O'Donnell L, Kumakubo A, Munro M, Sicheri F, Gingras AC, Natsume T, Suda T, Durocher D (2010) Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466: 941-946
23. Newton K, Matsumoto ML, Wertz IE, Kirkpatrick DS, Lill JR, Tan J, Dugger D, Gordon N, Sidhu SS, Fellouse FA, Komuves L, French DM, Ferrando RE, Lam C, Compaan D, Yu C, Bosanac I, Hymowitz SG, Kelley RF, Dixit VM (2008) Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134: 668-678
24. Pereg Y, Liu BY, O'Rourke KM, Sagolla M, Dey A, Komuves L, French DM, Dixit VM (2010) Ubiquitin hydrolase Dub3 promotes oncogenic transformation by stabilizing Cdc25A. Nat Cell Biol 12: 400-406
25. Phu L, Izrael-Tomasevic A, Matsumoto ML, Bustos D, Dynek JN, Fedorova AV, Bakalarski CE, Arnott D, Deshayes K, Dixit VM, Kelley RF, Vucic D, Kirkpatrick DS (2011) Improved quantitative mass spectrometry methods for characterizing complex ubiquitin signals. Mol Cell Proteomics 10: M110.003756
26. Pickart CM, Fushman D (2004) Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol 8: 610-616
27. Reyes-Turcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78: 363-397
28. Rothe M, Pan MG, Henzel WJ, Ayres TM, Goeddel DV (1995) The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 83: 1243-1252
29. Santoro MM, Samuel T, Mitchell T, Reed JC, Stainier DY (2007) Birc2 (cIap1) regulates endothelial cell integrity and blood vessel homeostasis. Nat Genet 39: 1397-1402
30. Sato Y, Yamagata A, Goto-Ito S, Kubota K, Miyamoto R, Nakada S, Fukai S (2012) Molecular basis of K63-linked polyubiquitination inhibition by the interaction between human deubiquitinating enzyme OTUB1 and ubiquitin- conjugating enzyme UBC13. J Biol Chem 287: 25860-25868
31. Schulman BA, Harper JW (2009) Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat Rev Mol Cell Biol 10: 319-331
32. Silke J, Brink R (2010) Regulation of TNFRSF and innate immune signalling complexes by TRAFs and cIAPs. Cell Death Differ 17: 35-45
33. Sun XX, Challagundla KB, Dai MS (2012) Positive regulation of p53 stability and activity by the deubiquitinating enzyme Otubain 1. EMBO J 31: 576-592
34. Tse WK, Eisenhaber B, Ho SH, Ng Q, Eisenhaber F, Jiang YJ (2009) Genome-wide loss-of-function analysis of deubiquitylating enzymes for zebrafish development. BMC Genomics 10: 637
35. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, Wang H, Vignali DA, Bergsagel PL, Karin M (2008) Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiqui-tination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol 9: 1364-1370
36. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, Zobel K, Dynek JN, Elliott LO, Wallweber HJ, Flygare JA, Fairbrother WJ, Deshayes K, Dixit VM, Vucic D (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-kB activation, and TNFa-dependent apoptosis. Cell 131: 669-681
37. Varfolomeev E, Goncharov T, Fedorova AV, Dynek JN, Zobel K, Deshayes K, Fairbrother WJ, Vucic D (2008) c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFa)-induced NF-kB activation. J Biol Chem 283: 24295-24299
38. Varfolomeev E, Goncharov T, Maecker H, Zobel K, Komuves LG, Deshayes K, Vucic D (2012) Cellular inhibitors of apoptosis are global regulators of NF-kappaB and MAPK activation by members of the TNF family of receptors. Sci Signal 5: ra22
39. Vince JE, Chau D, Callus B, Wong WW, Hawkins CJ, Schneider P, McKinlay M, Benetatos CA, Condon SM, Chunduru SK, Yeoh G, Brink R, Vaux DL, Silke J (2008) TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. J Cell Biol 182: 171-184
40. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, Benetatos CA, Chunduru SK, Condon SM, McKinlay M, Brink R, Leverkus M, Tergaonkar V, Schneider P, Callus BA, Koentgen F, Vaux DL, Silke J (2007) IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 131: 682-693
41. Vucic D, Dixit VM, Wertz IE (2011) Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 12: 439-452
42. Wacker A, Gerhardt H (2011) Endothelial development taking shape. Curr Opin Cell Biology 23: 676-685
43. Wiener R, Zhang X, Wang T, Wolberger C (2012) The mechanism of OTUB1-mediated inhibition of ubiquitination. Nature 483: 618-622
44. Zarnegar BJ, Wang Y, Mahoney DJ, Dempsey PW, Cheung HH, He J, Shiba T, Yang X, Yeh WC, Mak TW, Korneluk RG, Cheng G (2008) Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol 9: 1371-1378