Regulation of cellular responses by deubiquitinating enzymes: An update

Frontiers in Bioscience

Volumn 17, Issue 3, 2012, Pages 1184-1200

  Burrows, James F ^a   Johnston, James A ^b  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Cell cycle; Cell migration; Deubiquitinating; Disease; Intracellular signaling; Receptor trafficking; Review; Transcription

Indexed keywords

ENZYME;

METABOLISM; REVIEW; UBIQUITINATION;

ENZYMES; UBIQUITINATION;

EID: 84859256752     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3980     Document Type: Article

References (128)

1. A. Adhikari and Z.J. Chen: Diversity of polyubiquitin chains. Dev Cell 16, 485-486 (2009).
2. A.M. Weissman: Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol 2, 169-178 (2001). (Pubitemid 33675741)
3. H.C. Ardley and P.A. Robinson: E3 ubiquitin ligases. Essays Biochem 41, 15-30 (2005). (Pubitemid 41500968)
4. S.M. Nijman, M. Luna-Vargas, A. Velds, T.R. Brummelkamp, A.M. Dirac, T.K. Sixma and R. Bernards: A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786 (2005). (Pubitemid 41721026)
5. M.E. Sowa, E.J. Bennet, S.P. Gygi and J.W. Harper: Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403 (2009).
6. D. Komander, M.J. Clague and S. Urbe: Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10, 550-563 (2009).
7. A.Y. Amerik and M. Hochstrasser: Mechanism and function of deubiquitinating enzymes. Biochim Biophys Acta 1695, 189-207 (2004). (Pubitemid 39574973)
8. K.S. Makarova, L. Aravind and E.V. Koonin: A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem Sci 25, 50-52 (2000). (Pubitemid 30100365)
9. M.Y. Balakirev, S.O. Tcherniuk, M. Jaquinod and J. Chroboczek: Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep 4, 517-522 (2003). (Pubitemid 36789851)
10. A. Kovalenko, C. Chable-Bessia, G. Cantarella, A. Israel, D. Wallach and G. Courtois: The tumour suppressor CYLD negatively regulates NF-kappaB signaling by deubiquitination. Nature 424, 801-805 (2003). (Pubitemid 37021712)
11. P.C. Evans, T.S. Smith, M.J. Lai, M.G. Williams, D.F. Burke, K. Heyninck, M.M. Kreike, R. Beyaert, T.L. Blundell and P.J. Kilshaw: A novel type of deubiquitinating enzyme. J Biol Chem 278, 23180-23186 (2003). (Pubitemid 36830384)
12. B. Burnett, F. Li and R.N. Pittman: The polyglutamine neurodegenerative protein ataxin-3 binds polyubiquitylated proteins and has ubiquitin protease activity. Hum Mol Genet 12, 3195-3205 (2003). (Pubitemid 37508890)
13. H. Scheel, S. Tomiuk and K. Hofmann: Elucidation of ataxin-3 and ataxin-7 function by integrative bioinformatics. Hum Mol Genet 12, 2845-2852 (2003). (Pubitemid 37407121)
14. B-H. Lee, M.J. Lee, S. Park, D-C. Oh, S. Elsasser, P-C. Chen, C. Gartner, N. Dimova, J. Hanna, S.P. Gygi, S.M. Wilson, R.W. King and D. Finley: Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 467, 179-184 (2010).
15. M.J. Clague and S. Urbe: Endocytosis: the DUB version. Trends in Cell biology 16, 551-559 (2006). (Pubitemid 44636216)
16. G. Levkowitz, H. Waterman, E. Zamir, Z. Kam, S. Oved, W.Y. Langdon, L. Beguinot, B. Geiger and Y. Yarden: c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev 12, 3663-3674 (1998). (Pubitemid 29019647)
17. S. Urbe, M. Sachse, P.E. Row, C. Preisinger, F.A. Barr, G. Strous, J. Klumperman and M.J. Clague: The UIM domain of Hrs couples receptor sorting to vesicle formation. J. Cell Sci. 116, 4169-4179 (2003). (Pubitemid 37337090)
18. R.L. Williams and S. Urbe: The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368 (2007). (Pubitemid 46643239)
19. P.E. Row, I.A. Prior, J. McCullough, M.J. Clague and S. Urbé: The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J. Biol. Chem. 281, 12618-12624 (2006). (Pubitemid 43855351)
20. K. Bowers, S.C. Piper, M.A. Edeling, S.R. Gray, D.J. Owen, P.J. Lehner and J.P. Luzio: Degradation of endocytosed epidermal growth factor and virally ubiquitinated major histocompatibility complex class I is independent of mammalian ESCRTII. J. Biol. Chem. 281, 5094-5105 (2006). (Pubitemid 43847775)
21. E. Mizuno, K. Kobayashi, A. Yamamoto, N. Kitamura and M. Komada: A deubiquitinating enzyme UBPY regulates the level of protein ubiquitination on endosomes. Traffic 7, 1017-1031 (2006).
22. S. Niendorf, A. Oksche, A. Kisser, J. Löhler, M. Prinz, H. Schorle, S. Feller, M. Lewitzky, I. Horak and K.P. Knobeloch: Essential role of ubiquitin-specific protease 8 for receptor tyrosine kinase stability and endocytic trafficking in vivo. Mol. Cell Biol. 27, 5029-5039 (2007). (Pubitemid 47016150)
23. I. M.J. Meijer and J.E.M. van Leeuwen: ERBB2 is a target for USP8-mediated deubiquitination. Cellular Signalling 23, 458-467 (2011).
24. B. Hasdemir, J.E. Murphy, G.S. Cottrell and N.W. Bunnett: Endosomal deubiquitinating enzymes control ubiquitination and down-regulation of protease-activated receptor 2. J Biol Chem 284, 28453-28466 (2009).
25. J.N. Hislop, A.G. Henry, A. Marchese and M. von Zastrow: Ubiquitination regulates proteolytic processing of G protein-coupled receptors after their sorting to lysosomes. J. Biol. Chem. 284, 19361-19370 (2009).
26. I. Berlin, K.M. Higginbotham, R.S. Dise, M.I. Sierra and P.D. Nash: The deubiquitinating enzyme USP8 promotes trafficking and degradation of the chemokine receptor 4 at the sorting endosome. J Biol Chem 285, 37895-37908 (2010).
27. M. Berthouze, V. Venkataramanan, Y. Li and S.K. Shenoy: The deubiquitinases USP33 and USP20 coordinate beta2 adrenergic receptor recycling and resensitization. EMBO J 28, 1684-1696 (2009).
28. J.M. Bomberger, R.L. Barnaby and B.A. Stanton: The deubiquitinating enzyme USP10 regulates the endocytic recycling of CFTR in airway epithelial cells. Channels 4, 150-154 (2010).
29. M.B. Butterworth, R.S. Edinger, H. Ovaa, D. Burg, J.P. Johnson, R.A. Frizzell: The deubiquitinating enzyme UCHL3 regulates the apical membrane recycling of the epithelial sodium channel. J Biol Chem 282, 37885-37893 (2007).
30. L. Song and M. Rape: Reverse the curse-the role of deubiquitination in cell cycle control. Curr Opin Cell Biol 20, 156-63 (2008).
31. D. Zhang, K. Zaugg, T.W. Mak and S.J. Elledge: A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell 126, 529-542 (2006). (Pubitemid 44163600)
32. N. Popov, M. Wanzel, M. Madiredjo, D. Zhang, R. Beijersbergen, R. Bernards, R. Moll, S.J. Elledge and M. Eilers: The ubiquitin-specific protease USP28 is required for MYC stability. Nat Cell Biol 9, 765-774 (2007). (Pubitemid 47019463)
33. N. Popov, S. Herold, M. Llamazares, C. Schülein and M. Eilers: Fbw7 and Usp28 regulate myc protein stability in response to DNA damage. Cell Cycle 6, 2327-2331 (2007). (Pubitemid 350058681)
34. G.R. Bignell, W. Warren, S. Seal, M. Takahashi, E. Rapley, R. Barfoot, H. Green, C. Brown, P.J. Biggs, S.R. Lakhani, C. Jones, J. Hansen, E. Blair, B. Hofmann, R. Siebert, G. Turner, D.G. Evans, C. Schrander-Stumpel, F.A. Beemer, A. van Den Ouweland, D. Halley, B. Delpech, M.G. Cleveland, I. Leigh, J. Leisti and S. Rasmussen: Identification of the familial cylindromatosis tumour-suppressor gene. Nat Genet. 25, 160-165 (2005).
35. R. Massoumi, K. Chmielarska, K. Hennecke, A. Pfeifer and R. Fässler: Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-kappaB signaling. Cell 125, 665-677 (2006).
36. S.A. Wickström, K.C. Masoumi, S. Khochbin, R. Fässler and R. Massoumi: CYLD negatively regulates cellcycle progression by inactivating HDAC6 and increasing the levels of acetylated tubulin. EMBO J 29, 131-144 (2010).
37. C. McFarlane, A.A. Kelvin, M.A. de la Vega, U. Govender, C.J. Scott, J.F. Burrows and J.A. Johnston: The deubiquitinating enzyme USP17 is cell cycle regulated and mediates G1-S transition. Cancer Res 70, 3329-3339 (2010).
38. J.F. Burrows, A.A. Kelvin, C. McFarlane, R.E. Burden, M.J. McGrattan, M.A. de la Vega, U. Govender, D.J. Quinn, K. Dib, M. Gadina, C.J. Scott and J.A. Johnston: USP17 regulates Ras activation and cell proliferation by blocking RCE1 activity. J Biol Chem 284, 9587-9595 (2009).
39. F. Stegmeier, M. Rape, V.M. Draviam, G. Nalepa, M.E. Sowa, X.L. Ang, E.R. McDonald 3rd, M.Z. Li, G.J. Hannon, P.K. Sorger, M.W. Kirschner, J.W. Harper and S.J. Elledge: Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature 446, 876-881 (2007).
40. J.R. van Leuken, M.P. Luna-Vargas, T.K. Sixma, R.M.F. Wolthuis and R.H. Medema: Usp39 is essential for mitotic spindle checkpoint integrity and controls mRNAlevels of Aurora B. Cell Cycle 7, 2710-2719 (2008).
41. A. Bheda, A. Gullapalli, M. Caplow, J.S. Pagano and J. Shackelford: Ubiquitin editing enzyme UCH L1 and microtubule dynamics: implication in mitosis. Cell Cycle 9, 980-994 (2010).
42. D.E. Jensen, M. Proctor, S.T. Marquis, H.P. Gardner, S.I. Ha, L.A. Chodosh, A.M. Ishov, N. Tommerup, H. Vissing, Y. Sekido, J. Minna, A. Borodovsky, D.C. Schultz, K.D. Wilkinson, G.G. Maul, N. Barlev, S.L. Berger, G.C. Prendergast and F.J. Rauscher 3rd: BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene 16, 1097-1112 (1998). (Pubitemid 28127509)
43. K.H. Ventii, N.S. Devi, K.L. Friedrich, T.A. Chernova, M. Tighiouart, E.G. Van Meir and K.D. Wilkinson: BRCA1-associated protein-1 is a tumor suppressor that requires deubiquitinating activity and nuclear localization. Cancer Res 68, 6953-6962 (2008).
44. Y.J. Machida, Y. Machida, A.A. Vashisht, J.A. Wohlschlegel and A. Dutta: The deubiquitinating enzyme BAP1 regulates cell growth via interaction with HCF-1. J Biol Chem 284, 34179-34188 (2009).
45. B. Aressy, D. Jullien, M. Cazales, M. Marcellin, B. Bugler, O. Burlet-Schiltz and B. Ducommun: A screen for deubiquitinating enzymes involved in the G2/M checkpoint identifies USP50 as a regulator of HSP90-dependent Wee1 stability. Cell Cycle 9, 3815-3822 (2010).
46. A.D. D'Andrea: The Fanconi road to cancer. Genes Dev 17, 1933-1936 (2003).
47. I. Garcia-Higuera, T. Taniguchi, S. Ganesan, M.S. Meyn, C. Timmers, J. Hejna, M. Grompe and A.D. D'Andrea: Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7, 249-262 (2001). (Pubitemid 32206493)
48. N.G. Howlett, T. Taniguchi, S. Olson, B. Cox, Q. Waisfisz, C. De Die-Smulders, N. Persky, M. Grompe, H. Joenje, G. Pals, H. Ikeda, E.A. Fox and A.D. D'Andrea: Biallelic inactivation of BRCA2 in Fanconi anemia. Science 297, 606-609 (2002). (Pubitemid 34815345)
49. S.M. Nijman, T.T. Huang, A.M. Dirac, T.R. Brummelkamp, R.M. Kerkhoven, A.D. D'Andrea and R. Bernards: The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell 17, 331-339 (2005). (Pubitemid 40193305)
50. P.L. Kannouche, J. Wing and A.R. Lehmann: Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol Cell 14, 491-500 (2004). (Pubitemid 38648802)
51. T.T Huang, S.M. Nijman, K.D. Mirchandani, P.J. Galardy, M.A. Cohn, W. Haas, S.P. Gygi, H.L. Ploegh, R. Bernards and A.D. D'Andrea: Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat Cell Biol 8, 339-347 (2006).
52. C.L. Brooks and W. Gu: p53 ubiquitination: Mdm2 and beyond. Mol Cell 21, 307-315 (2006). (Pubitemid 43163526)
53. J. Gu, H. Kawai, L. Nie, H. Kitao, D. Wiederschain, A.G. Jochemsen, J. Parant, G. Lozano and Z.M. Yuan: Mutual dependence of MDM2 and MDMX in their functional inactivation of p53. J Biol Chem 277, 19251- 19254 (2002). (Pubitemid 34967428)
54. K. Okamoto, K. Kashima, Y. Pereg, M. Ishida, S. Yamazaki, A. Nota, A. Teunisse, D. Migliorini, I. Kitabayashi, J.C. Marine, C. Prives, Y. Shiloh, A.G. Jochemsen and Y. Taya: DNA damage-induced phosphorylation of MdmX at serine 367 activates p53 by targeting MdmX for Mdm2-dependent degradation. Mol Cell Biol 25, 9608-9620 (2005). (Pubitemid 41507859)
55. M. Li, D. Chen, A. Shiloh, J. Luo, A.Y. Nikolaev, J. Qin and W. Gu: Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416, 648- 653 (2002). (Pubitemid 34406767)
56. E. Meulmeester, M.M. Maurice, C. Boutell, A.F.A.S. Teunisse, H. Ovaa, T.E. Abraham, R.W. Dirks and A.G. Jochemsen: Loss of HAUSP-mediated deubiquitination contributes to DNA damage-induced destabilization of Hdmx and Hdm2. Mol Cell 18, 565-576 (2005). (Pubitemid 40726233)
57. J. Yuan, K. Luo, L. Zhang, J.C. Cheville and Z. Lou: USP10 regulates p53 localization and stability by deubiquitinating p53. Cell 140, 384-396 (2010).
58. S. Nakada, I. Tai, S. Panier, A. Al-Hakim, S. Iemura, Y.C. Juang, L. O'Donnell, A. Kumakubo, M. Munro, F. Sicheri, A.C. Gingras, T. Natsume, T. Suda and D. Durocher: Non-canonical inhibition of DNA damagedependent ubiquitination by OTUB1. Nature 466, 941-946 (2010).
59. G. Shao, D.R. Lilli, J. Patterson-Fortin, K.A. Coleman, D.E. Morrissey and R.A. Greenberg: The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8- Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc Natl Acad Sci USA 106, 3166-3171 (2009).
60. F. Nicassio, N. Corrado, J.H. Vissers, L.B. Areces, S. Bergink, J.A. Marteijn, B. Geverts, A.B. Houtsmuller, W. Vermeulen, P.P. Di Fiore and E. Citterio: Human USP3 is a chromatin modifier required for S phase progression and genome stability. Curr Biol 17, 1972-1977 (2007). (Pubitemid 350088491)
61. N.M. Shanbhag, I.U. Rafalska-Metcalf, C. Balane- Bolivar, S.M. Janicki and R.A. Greenberg: ATMdependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141, 970-981 (2010).
62. H.Y. Joo, L. Zhai, C. Yang, S. Nie, H. Erdjument- Bromage, P. Tempst, C. Chang and H. Wang: Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature 449, 1068-1072 (2007). (Pubitemid 350014605)
63. M.A. Mines, J.S. Goodwin, L.E. Limbird, F.F. Cui and G.H. Fan: Deubiquitination of CXCR4 by USP14 is critical for both CXCL12-induced CXCR4 degradation and chemotaxis but not ERK activation. J Biol Chem 284, 5742-5752 (2009).
64. M. de la Vega, A.A. Kelvin, D.J. Dunican, C. McFarlane, J.F. Burrows, J. Jaworski, N.J. Stevenson, K. Dib, J.Z. Rappoport, C.J. Scott, A. Long and J.A. Johnston: The deubiquitinating enzyme USP17 is essential for GTPase subcellular localization and cell motility. Nat Comms, In Press (2011).
65. R. Buus, M. Faronato, D.E. Hammond, S. Urbé and M.J. Clague: Deubiquitinase activities required for hepatocyte growth factor-induced scattering of epithelial cells. Curr Biol 19, 1463-1466 (2009).
66. B. Skaug, X. Jiang and Z.J. Chen: The Role of Ubiquitin in NF-κB Regulatory Pathways. Annu Rev Biochem 78, 769-796 (2009).
67. L. Deng, C. Wang, E. Spencer, L. Yang, A. Braun, J. You, C. Slaughter, C. Pickart and Z.J. Chen: Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103, 351-361 (2000).
68. C. Wang, L. Deng, M. Hong, G.R. Akkaraju, J. Inoue and Z.J. Chen: TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412, 346-351 (2001). (Pubitemid 32694385)
69. A. Kanayama, R.B. Seth, L. Sun, C.K. Ea, M. Hong, A. Shaito, Y.H. Chiu, L. Deng and Z.J. Chen: TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol Cell 15, 535-548 (2004). (Pubitemid 39141781)
70. C.S. Shi and J.H. Kehrl: Tumor necrosis factor (TNF)- induced germinal center kinase-related (GCKR) and stressactivated protein kinase (SAPK) activation depends upon the E2/E3 complex Ubc13-Uev1A/TNF receptor-associated factor 2 (TRAF2). J Biol Chem 278, 15429-15434 (2003). (Pubitemid 36799883)
71. I.E. Wertz, K.M. O'Rourke, H. Zhou, M. Eby, L. Aravind, S. Seshagiri, P. Wu, C. Wiesmann, R. Baker, D.L. Boone, A. Ma, E.V. Koonin and V.M. Dixit: Deubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430, 694- 699 (2004). (Pubitemid 39061687)
72. H. Zhou, J. Wertz, K. O'Rourke, M. Ultsch, S. Seshagiri, M. Eby, W. Xiao and V.M. Dixit: Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature 427, 167-171 (2004). (Pubitemid 38094958)
73. Y. Yang, C. Yin, A. Pandey, D. Abbott, C. Sassetti and M.A. Kelliher: NOD2 pathway activation by MDP or Mycobacterium tuberculosis infection involves the stable polyubiquitination of Rip2. J Biol Chem 282, 36223-36229 (2007).
74. H. Oshiumi, M. Matsumoto, S. Hatakeyama and T. Seya: Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection. J Biol Chem 284, 807-817 (2009).
75. M.S. Hayden and S. Ghosh: Signaling to NFkappaB. Genes Dev 18, 2195-2224 (2004).
76. E. Trompouki, E. Hatzivassiliou, T. Tsichritzis, H. Farmer, A. Ashworth and G. Mosialos: CYLD is a deubiquitinating enzyme that negatively regulates NFkappaB activation by TNFR family members. Nature 424, 793-796 (2003). (Pubitemid 37021710)
77. T.R. Brummelkamp, S.M. Nijman, A.M. Dirac and R. Bernards, R: Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature 424, 797-801 (2003). (Pubitemid 37021711)
78. H. Jono, J.H. Lim, L.F. Chen, H. Xu, E. Trompouki, Z.K. Pan, G. Mosialos and J.D. Li: NF-kappaB is essential for induction of CYLD, the negative regulator of NF-kappaB: evidence for a novel inducible autoregulatory feedback pathway. J Biol Chem 279, 36171-36174 (2004). (Pubitemid 39128950)
79. W. Reiley, M. Zhang and S.C. Sun: Negative regulation of JNK signaling by the tumor suppressor CYLD. J Biol Chem 279, 55161-55167 (2004). (Pubitemid 40066510)
80. W.W. Reiley, M. Zhang, W. Jin, M. Losiewicz, K.B. Donohue, C.C. Norbury and S.C. Sun: Regulation of T cell development by the deubiquitinating enzyme CYLD. Nat Immunol 7, 411-417 (2006).
81. W.W. Reiley, W. Jin, A.J. Lee, A. Wright, X. Wu, E.F. Tewalt, T.O. Leonard, C.C. Norbury, L. Fitzpatrick, M. Zhang and S.C. Sun: Deubiquitinating enzyme CYLD negatively regulates the ubiquitin-dependent kinase Tak1 and prevents abnormal T cell responses. J Exp Med 204, 1475-1485 (2007). (Pubitemid 46919884)
82. R. Massoumi, K. Chmielarska, K. Hennecke, A. Pfeifer and R. Fassler: Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-kappaB signaling. Cell 125, 665-677 (2006).
83. D.V. Tauriello, A. Haegebarth, I. Kuper, M.J. Edelmann, M. Henraat, M.R. Canninga-van Dijk, B.M. Kessler, H. Clevers and M.M. Maurice: Loss of the tumor suppressor CYLD enhances Wnt/beta-catenin signaling through K63-linked ubiquitination of Dvl. Mol Cell 37, 607-619 (2010).
84. E.G. Lee, D.L. Boone, S. Chai, S.L. Libby, M. Chien, J.P. Lodolce and A. Ma: Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 289, 2350-2354 (2000).
85. D.L. Boone, E.E. Turer, E.G. Lee, R.C. Ahmad, M.T. Wheeler, C. Tsui, P. Hurley, M. Chien, S. Chai, O. Hitotsumatsu, E. McNally, C. Pickart and A. Ma: The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 5, 1052-1060 (2004). (Pubitemid 41057725)
86. C. Mauro, F. Pacifico, A. Lavorgna, S. Mellone, A. Iannetti, R. Acquaviva, S. Formisano, P. Vito and A. Leonardi: ABIN-1 binds to NEMO/IKKgamma and cooperates with A20 in inhibiting NF-kappaB. J Biol Chem 281, 18482-18488 (2006). (Pubitemid 44035507)
87. K. Enesa, M. Zakkar, H. Chaudhury, A. Luong le, L. Rawlinson, J.C. Mason, D.O. Haskard, J.L. Dean and P.C. Evans: NF-kappaB suppression by the deubiquitinating enzyme Cezanne: a novel negative feedback loop in proinflammatory signaling. J Biol Chem 283, 7036-7045 (2008).
88. A. Bremm, S.M. Freund and D. Komander: Lys11- linked ubiquitin chains adopt compact conformations and are preferentially hydrolyzed by the deubiquitinase Cezanne. Nat Struct Mol Biol 17, 939-947 (2010).
89. C. Tzimas, G. Michailidou, M. Arsenakis, E. Kieff, G. Mosialos and E.G. Hatzivassiliou: Human ubiquitin specific protease 31 is a deubiquitinating enzymeimplicated in activation of nuclear factor-kappaB. Cell Signal 18, 83-92 (2006). (Pubitemid 41415717)
90. N. Kayagaki, Q. Phung, S. Chan, R. Chaudhari, C. Quan, K.M. O'Rourke, M. Eby, E. Pietras, G. Cheng, J.F. Bazan, Z. Zhang, D. Arnott and V.M. Dixit: DUBA: a deubiquitinase that regulates type I interferon production. Science 318, 1628-1632 (2007). (Pubitemid 350233662)
91. Y. Takami, H. Nakagami, R. Morishita, T. Katsuya, T.X. Cui, T. Ichikawa, Y. Saito, H. Hayashi, Y. Kikuchi, T. Nishikawa, Y. Baba, O. Yasuda, H. Rakugi, T. Ogihara and Y. Kaneda: Ubiquitin carboxyl-terminal hydrolase L1, a novel deubiquitinating enzyme in the vasculature, attenuates NFkappaB activation. Arterioscler Thromb Vasc Biol 27, 2184- 2190 (2007). (Pubitemid 350287248)
92. T. Yamaguchi, J. Kimura, Y. Miki and K. Yoshida: The deubiquitinating enzyme USP11 controls an IkappaB kinase alpha (IKKalpha)-p53 signaling pathway in response to tumor necrosis factor alpha (TNFalpha). J Biol Chem 282, 33943- 33948 (2007). (Pubitemid 350159476)
93. H. Zhou, D.M. Monack, N. Kayagaki, I. Wertz, J. Yin, B. Wolf and V.M. Dixit : Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation. J Exp Med 202, 1327-1332 (2005). (Pubitemid 41668735)
94. Z. Sun, Z. Chen, S.R. Lawson and Y. Fang: The cysteine protease domain of porcine reproductive and respiratory syndrome virus nonstructural protein 2 possesses deubiquitinating and interferon antagonism functions. J Virol 84, 7832-7846 (2010).
95. Y. Zhu, K. Lambert, C. Corless, N.G. Copeland, D.J. Gilbert, N.A. Jenkins and A.D. D'Andrea: DUB-2 is a member of a novel family of cytokine-inducible deubiquitinating enzymes. J Biol Chem 272, 51-57 (1997). (Pubitemid 27021529)
96. J.F. Burrows, M.J. McGrattan, A. Rascle, M. Humbert, K.H. Baek and J.A. Johnston: DUB-3, a cytokine-inducible deubiquitinating enzyme that blocks proliferation. J Biol Chem 279, 13993-14000 (2004). (Pubitemid 38468933)
97. M.A. de la Vega, J.F. Burrows, C. McFarlane, U. Govender, C.J. Scott and J.A. Johnston: The deubiquitinating enzyme USP17 blocks N-Ras membrane trafficking and activation, but leaves K-Ras unaffected. J Biol Chem 285, 12028-12036 (2010).
98. S. Dupont, A. Mamidi, M. Cordenonsi, M. Montagner, L. Zacchigna, M. Adorno, G. Martello, M.J. Stinchfield, S. Soligo, L. Morsut, M. Inui, S. Moro, N. Modena, F. Argenton, S.J. Newfeld and S. Piccolo: FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell 136, 123-135 (2009).
99. S.J. Wicks, T. Grocott, K. Haros, M. Maillard, P. ten Dijke and A. Chantry: Reversible ubiquitination regulates the Smad/TGF-beta signalling pathway. Biochem Soc Trans 34 (Pt 5), 761-763 (2006). (Pubitemid 44796415)
100. W.K. Tse, B. Eisenhaber, S.H. Ho, Q. Ng, F. Eisenhaber and Y.J. Jiang: Genome-wide loss-of-function analysis of deubiquitylating enzymes for zebrafish development. BMC Genomics 10, 637 (2009).
101. B.S. Atanassov, E. Koutelou and S.Y. Dent: The role of deubiquitinating enzymes in chromatin regulation. FEBS Lett [Epub ahead of print] (2010).
102. K.S. Makarova, L. Aravind and E.V. Koonin: A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem Sci 25, 50-52 (2000). (Pubitemid 30100365)
103. M.Y. Balakirev, S.O. Tcherniuk, M. Jaquinod and J. Chroboczek: Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep 4, 517-522 (2003). (Pubitemid 36789851)
104. L. Lv, X.Y. Xiao, Z.H. Gu, F.Q. Zeng, L.Q. Huang and G.S. Jiang: Silencing USP22 by asymmetric structure of interfering RNA inhibits proliferation and induces cell cycle arrest in bladder cancer cells. Mol Cell Biochem 346, 11-21 (2010).
105. Y.L. Liu, Y.M. Yang, H. Xu and X.S. Dong: Increased expression of ubiquitin-specific protease 22 can promote cancer progression and predict therapy failure in human colorectal cancer. J Gastroenterol Hepatol 25, 1800-1805 (2010).
106. P. Zhu, W. Zhou, J. Wang, J. Puc, K.A. Ohgi, H. Erdjument-Bromage, P. Tempst, C.K. Glass and M.G. Rosenfeld: A Histone H2A Deubiquitinase Complex Coordinating Histone Acetylation and H1 Dissociation in Transcriptional Regulation. Mol Cell 27, 609-621 (2007). (Pubitemid 47238636)
107. X.Y. Zhang, H.K. Pfeiffer, A.W. Thorne and S.B. McMahon: USP22, an hSAGA subunit and potential cancer stem cell marker, reverses the polycomb-catalyzed ubiquitylation of histone H2A. Cell Cycle 7, 1522-1524 (2008). (Pubitemid 351881314)
108. T. Nakagawa, T. Kajitani, S. Togo, N. Masuko, H. Ohdan, Y. Hishikawa, T. Koji, T. Matsuyama, T. Ikura, M. Muramatsu and T. Ito: Deubiquitylation of histone H2A activates transcriptional initiation via trans-histone crosstalk with H3K4 di- and trimethylation. Genes Dev 22, 37- 49 (2008).
109. G.N. Maertens, S. El Messaoudi-Aubert, S. Elderkin, K. Hiom and G. Peters: Ubiquitin-specific proteases 7 and 11 modulate Polycomb regulation of the INK4a tumour suppressor. EMBO J 29, 2553-2565 (2010).
110. S. Bowen, M. Gill, D.A. Lee, G. Fisher, R.G. Geronemus, M.E. Vazquez and J.T. Celebi: Mutations in the CYLD gene in Brooke-Spiegler syndrome, familial cylindromatosis, and multiple familial trichoepithelioma: lack of genotype-phenotype correlation. J Invest Dermatol 124, 919-920 (2005). (Pubitemid 40629091)
111. K. Honma, S. Tsuzuki, M. Nakagawa, H. Tagawa, S. Nakamura, Y. Morishima and M. Seto: TNFAIP3/A20functions as a novel tumor suppressor gene in several subtypes of non-Hodgkin lymphomas. Blood 114, 2467- 2475 (2009).
112. M. Kato, M. Sanada, I. Kato, Y. Sato, J. Takita, K. Takeuchi, A. Niwa, Y. Chen, K. Nakazaki, J. Nomoto, Y. Asakura, S. Muto, A. Tamura, M. Iio, Y. Akatsuka, Y. Hayashi, H. Mori, T. Igarashi, M. Kurokawa, S. Chiba, S. Mori, Y. Ishikawa, K. Okamoto, K. Tobinai, H. Nakagama, T. Nakahata, T. Yoshino, Y. Kobayashi and S. Ogawa: Frequent inactivation of A20 in B-cell lymphomas. Nature 459, 712-716 (2009).
113. U. Novak, A. Rinaldi, I. Kwee, S.V. Nandula, P.M. Rancoita, M. Compagno, M. Cerri, D. Rossi, V.V. Murty, E. Zucca, G. Gaidano, R. Dalla-Favera, L. Pasqualucci, G Bhagat and F. Bertoni: The NF-{kappa}B negative regulator TNFAIP3 (A20) is inactivated by somatic mutations and genomic deletions in marginal zone lymphomas. Blood 113, 4918-4921 (2009).
114. D. Masuya, D. Huang, D. Liu, T. Nakashima, H. Yokomise, M. Ueno, N. Nakashima and S. Sumitomo: The HAUSP gene plays an important role in non-small cell lung carcinogenesis through p53-dependent pathways. J Pathol 208, 724-732 (2006).
115. D.A. Gray, J. Inazawa, K. Gupta, A. Wong, R. Ueda and T. Takahashi: Elevated expression of Unph, a protooncogene at 3p21.3, in human lung tumors. Oncogene 10, 2179-2183 (1995).
116. D. Velazquez-Fernandez, C. Laurell, J. Geli, A. Hoog, J. Odeberg, M. Kjellman, J. Lundeberg, B. Hamberger, P. Nilsson and M. Backdahl: Expression profiling of adrenocortical neoplasms suggests a molecular signature of malignancy. Surgery 138, 1087-1094 (2005). (Pubitemid 41797349)
117. K. Gupta, M. Chevrette and D.A. Gray: The Unp proto-oncogene encodes a nuclear protein. Oncogene 9, 1729-1731 (1994). (Pubitemid 24163401)
118. J.W. Janssen, J. Braunger, K. Ballas, M. Faust, U. Siebers, A.C. Steenvoorden and C.R. Bartram: Spectrum of transforming sequences detected by tumorigenicity assay in a large series of human neoplasms. Int J Cancer 80, 857- 862 (1999). (Pubitemid 29108860)
119. A.M. Oliveira, A.R. Perez-Atayde, P. Dal Cin, M.C. Gebhardt, C.J. Chen, J.R. Neff, G.D. Demetri, A.E. Rosenberg, J.A. Bridge and J.A. Fletcher: Aneurysmal bone cyst variant translocations upregulate USP6 transcription by promoter swapping with the ZNF9, COL1A1, TRAP150, and OMD genes. Oncogene 24, 3419- 3426 (2005). (Pubitemid 40756243)
120. Y. Pereg, B.Y. Liu, K.M. O'Rourke, M. Sagolla, A. Dey, L. Komuves, D.M. French and V.M. Dixit: Ubiquitin hydrolase Dub3 promotes oncogenic transformation by stabilizing Cdc25A. Nat Cell Biol 12, 400-406 (2010).
121. S. Lincoln, J. Vaughan, N. Wood, M. Baker, J. Adamson, K. Gwinn-Hardy, T. Lynch, J. Hardy and M. Farrer: Low frequency of pathogenic mutations in the ubiquitin carboxy-terminal hydrolase gene in familial Parkinson's disease. Neuroreport 10, 427-429 (1999). (Pubitemid 29104826)
122. J. Zhang, N. Hattori, E. Leroy, H.R. Morris, S. Kubo, T. Kobayashi, N.W. Wood, M.H. Polymeropoulos and Y. Mizuno: Association between a polymorphism of ubiquitin carboxy-terminal hydrolase L1 (UCH-L1) gene and sporadic Parkinson's disease. Parkinsonism Relat Disord 6, 195-197 (2000). (Pubitemid 30438775)
123. K. Saigoh, Y.L. Wang, J.G. Suh, T. Yamanishi, Y. Sakai, H. Kiyosawa, T. Harada, N. Ichihara, S. Wakana, T. Kikuchi and K. Wada: Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat Genet 23, 47-51 (1999). (Pubitemid 29418786)
124. H.L. Paulson, S.S. Das, P.B. Crino, M.K. Perez, S.C. Patel, D. Gotsdiner, K.H. Fischbeck and R.N. Pittman: Machado-Joseph disease gene product is a cytoplasmic protein widely expressed in brain. Ann Neurol 41, 453-462 (1997). (Pubitemid 27169184)
125. Q. Wang, L. Li and Y. Ye: Regulation of retrotranslocation by p97-associated deubiquitinating enzyme ataxin-3. J Cell Biol 174, 963-971 (2006). (Pubitemid 44455185)
126. L. Vereecke, R. Beyaert and G. van Loo: The ubiquitin-editing enzyme A20 (TNFAIP3) is a central regulator of immunopathology. Trends Immunol 30, 383- 391 (2009).
127. F. Colland: The therapeutic potential of deubiquitinating enzyme inhibitors. Biochem Soc Trans 38, 137-143 (2010).
128. B. Nicholson, J.G. Marblestone, T.R. Butt and M.R. Mattern: Deubiquitinating enzymes as novel anticancer targets. Future Oncol 3, 191-199 (2007). (Pubitemid 46592727)