Cullin 5-RING E3 ubiquitin ligases, new therapeutic targets?

Biochimie

Volumn 122, Issue , 2016, Pages 339-347

  Lamsoul, Isabelle ^a,b   Uttenweiler Joseph, Sandrine ^a,b   Moog Lutz, Christel ^a,b   Lutz, Pierre G ^a,b  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

Cullin RING ligase; E3 ubiquitin ligase; Therapeutic targets; Ubiquitin proteasome system

Indexed keywords

ANKYRIN REPEAT CONTAINING PROTEIN WITH A SOCS BOX 11; ANKYRIN REPEAT CONTAINING PROTEIN WITH A SOCS BOX 2ALPHA; ANKYRIN REPEAT CONTAINING PROTEIN WITH A SOCS BOX 2BETA; ANKYRIN REPEAT CONTAINING PROTEIN WITH A SOCS BOX 3; ANKYRIN REPEAT CONTAINING PROTEIN WITH A SOCS BOX 4; ANKYRIN REPEAT CONTAINING PROTEIN WITH A SOCS BOX 9; CISPLATIN; CULLIN; CULLIN 5; ELONGIN; ELONGIN A; NEDD8 PROTEIN; PEVONEDISTAT; PROTEASOME; PROTEIN BLZF1; PROTEIN GAM1; PROTEIN LANA; RING FINGER PROTEIN; SH2 DOMAIN CONTAINING PROTEIN WITH A SOCS BOX 1; SH2 DOMAIN CONTAINING PROTEIN WITH A SOCS BOX 3; SH2 DOMAIN CONTAINING PROTEIN WITH A SOCS BOX 6; SPRY DOMAIN CONTAINING PROTEIN WITH A SOCS BOX 1; SPRY DOMAIN CONTAINING PROTEIN WITH A SOCS BOX 2; SPRY DOMAIN CONTAINING PROTEIN WITH A SOCS BOX 4; SUPPRESSOR OF CYTOKINE SIGNALING; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VIF PROTEIN; VIRUS PROTEIN; WD40 REPEAT CONTAINING PROTEIN WITH A SOCS BOX 1; ANTINEOPLASTIC AGENT; CUL5 PROTEIN, HUMAN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

DRUG TARGETING; ENZYME DEGRADATION; HUMAN; NONHUMAN; PROTEIN FAMILY; REVIEW; UBIQUITINATION; BIOLOGICAL MODEL; DRUG EFFECTS; METABOLISM; NEOPLASMS; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; CULLIN PROTEINS; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84957851716     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2015.08.003     Document Type: Review

References (124)

1. A. Hershko, and A. Ciechanover The ubiquitin system Annu. Rev. Biochem. 67 1998 425 479
2. M.B. Metzger, V.A. Hristova, and A.M. Weissman HECT and RING finger families of E3 ubiquitin ligases at a glance J. Cell Sci. 125 2012 531 537
3. D. Komander, and M. Rape The ubiquitin code Annu. Rev. Biochem. 81 2012 203 229
4. T.A. Soucy, P.G. Smith, M.A. Milhollen, A.J. Berger, J.M. Gavin, S. Adhikari, J.E. Brownell, K.E. Burke, D.P. Cardin, S. Critchley, C.A. Cullis, A. Doucette, J.J. Garnsey, J.L. Gaulin, R.E. Gershman, A.R. Lublinsky, A. McDonald, H. Mizutani, U. Narayanan, E.J. Olhava, S. Peluso, M. Rezaei, M.D. Sintchak, T. Talreja, M.P. Thomas, T. Traore, S. Vyskocil, G.S. Weatherhead, J. Yu, J. Zhang, L.R. Dick, C.F. Claiborne, M. Rolfe, J.B. Bolen, and S.P. Langston An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer Nature 458 2009 732 736
5. J. Jin, T. Cardozo, R.C. Lovering, S.J. Elledge, M. Pagano, and J.W. Harper Systematic analysis and nomenclature of mammalian F-box proteins Genes Dev. 18 2004 2573 2580
6. E.M. Linossi, and S.E. Nicholson The SOCS box-adapting proteins for ubiquitination and proteasomal degradation IUBMB Life 64 2012 316 323
7. P.J. Stogios, G.S. Downs, J.J. Jauhal, S.K. Nandra, and G.G. Prive Sequence and structural analysis of BTB domain proteins Genome Biol. 6 2005 R82
8. Y.J. He, C.M. McCall, J. Hu, Y. Zeng, and Y. Xiong DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases Genes Dev. 20 2006 2949 2954
9. A. Kibel, O. Iliopoulos, J.A. DeCaprio, and W.G. Kaelin Jr. Binding of the von Hippel-Lindau tumor suppressor protein to Elongin B and C Science 269 1995 1444 1446
10. T. Kishida, T.M. Stackhouse, F. Chen, M.I. Lerman, and B. Zbar Cellular proteins that bind the von Hippel-Lindau disease gene product: mapping of binding domains and the effect of missense mutations Cancer Res. 55 1995 4544 4548
11. T. Kamura, S. Sato, D. Haque, L. Liu, W.G. Kaelin Jr., R.C. Conaway, and J.W. Conaway The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families Genes Dev. 12 1998 3872 3881
12. N. Mahrour, W.B. Redwine, L. Florens, S.K. Swanson, S. Martin-Brown, W.D. Bradford, K. Staehling-Hampton, M.P. Washburn, R.C. Conaway, and J.W. Conaway Characterization of cullin-box sequences that direct recruitment of CUL2-RBX1 and CUL5-RBX2 modules to Elongin BC-based ubiquitin ligases J. Biol. Chem. 283 2008 8005 8013
13. A. Sarikas, T. Hartmann, and Z.Q. Pan The cullin protein family Genome Biol. 12 2011 220
14. M.A. Read, J.E. Brownell, T.B. Gladysheva, M. Hottelet, L.A. Parent, M.B. Coggins, J.W. Pierce, V.N. Podust, R.S. Luo, V. Chau, and V.J. Palombella NEDD8 modification of cul-1 activates SCF(β-TrCP)-dependent ubiquitination of IκBα Mol. Cell Biol. 20 2000 2326 2333
15. J.R. Lydeard, B.A. Schulman, and J.W. Harper Building and remodelling Cullin-RING E3 ubiquitin ligases EMBO Rep. 14 2013 1050 1061
16. S. Lyapina, G. Cope, A. Shevchenko, G. Serino, T. Tsuge, C. Zhou, D.A. Wolf, N. Wei, and R.J. Deshaies Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome Science 292 2001 1382 1385
17. G.A. Cope, G.S. Suh, L. Aravind, S.E. Schwarz, S.L. Zipursky, E.V. Koonin, and R.J. Deshaies Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of NEDD8 from Cul1 Science 298 2002 608 611
18. T. Kamura, M.N. Conrad, Q. Yan, R.C. Conaway, and J.W. Conaway The Rbx1 subunit of SCF and VHL E3 ubiquitin ligase activates Rub1 modification of cullins Cdc53 and CUL2 Genes Dev. 13 1999 2928 2933
19. D.T. Huang, O. Ayrault, H.W. Hunt, A.M. Taherbhoy, D.M. Duda, D.C. Scott, L.A. Borg, G. Neale, P.J. Murray, M.F. Roussel, and B.A. Schulman E2-RING expansion of the NEDD8 cascade confers specificity to cullin modification Mol. Cell 33 2009 483 495
20. D.M. Duda, L.A. Borg, D.C. Scott, H.W. Hunt, M. Hammel, and B.A. Schulman Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation Cell 134 2008 995 1006
21. B.K. Boh, P.G. Smith, and T. Hagen Neddylation-induced conformational control regulates cullin RING ligase activity in vivo J. Mol. Biol. 409 2011 136 145
22. N.W. Pierce, G. Kleiger, S.O. Shan, and R.J. Deshaies Detection of sequential polyubiquitylation on a millisecond timescale Nature 462 2009 615 619
23. J.K. Monda, D.C. Scott, D.J. Miller, J. Lydeard, D. King, J.W. Harper, E.J. Bennett, and B.A. Schulman Structural conservation of distinctive N-terminal acetylation-dependent interactions across a family of mammalian NEDD8 ligation enzymes Structure 21 2013 42 53
24. T. Kurz, Y.C. Chou, A.R. Willems, N. Meyer-Schaller, M.L. Hecht, M. Tyers, M. Peter, and F. Sicheri DCN1 functions as a scaffold-type E3 ligase for cullin neddylation Mol. Cell 29 2008 23 35
25. D.C. Scott, J.K. Monda, E.J. Bennett, J.W. Harper, and B.A. Schulman N-terminal acetylation acts as an avidity enhancer within an interconnected multiprotein complex Science 334 2011 674 678
26. D.C. Scott, V.O. Sviderskiy, J.K. Monda, J.R. Lydeard, S.E. Cho, J.W. Harper, and B.A. Schulman Structure of a RING E3 trapped in action reveals ligation mechanism for the ubiquitin-like protein NEDD8 Cell 157 2014 1671 1684
27. L. Pintard, T. Kurz, S. Glaser, J.H. Willis, M. Peter, and B. Bowerman Neddylation and deneddylation of CUL3 is required to target MEI-1/Katanin for degradation at the meiosis-to-mitosis transition in C. elegans Curr. Biol. 13 2003 911 921
28. M. Sharon, H. Mao, E. Boeri Erba, E. Stephens, N. Zheng, and C.V. Robinson Symmetrical modularity of the COP9 signalosome complex suggests its multifunctionality Structure 17 2009 31 40
29. A. Echalier, Y. Pan, M. Birol, N. Tavernier, L. Pintard, F. Hoh, C. Ebel, N. Galophe, F.X. Claret, and C. Dumas Insights into the regulation of the human COP9 signalosome catalytic subunit, CSN5/Jab1 Proc. Natl. Acad. Sci. U. S. A. 110 2013 1273 1278
30. E.J. Bennett, J. Rush, S.P. Gygi, and J.W. Harper Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics Cell 143 2010 951 965
31. L.K. Teixeira, and S.I. Reed Ubiquitin ligases and cell cycle control Annu. Rev. Biochem. 82 2013 387 414
32. F.C. Guibal, C. Moog-Lutz, P. Smolewski, Y. Di Gioia, Z. Darzynkiewicz, P.G. Lutz, and Y.E. Cayre ASB2 inhibits growth and promotes commitment in myeloid leukemia cells J. Biol. Chem. 277 2002 218 224
33. N.F. Bello, I. Lamsoul, M.L. Heuze, A. Metais, G. Moreaux, D.A. Calderwood, D. Duprez, C. Moog-Lutz, and P.G. Lutz The E3 ubiquitin ligase specificity subunit ASB2β is a novel regulator of muscle differentiation that targets filamin B to proteasomal degradation Cell Death Differ. 16 2009 921 932
34. I. Lamsoul, A. Metais, E. Gouot, M.L. Heuze, A.M. Lennon-Dumenil, C. Moog-Lutz, and P.G. Lutz ASB2α regulates migration of immature dendritic cells Blood 122 2013 533 541
35. M.W. Schmidt, P.R. McQuary, S. Wee, K. Hofmann, and D.A. Wolf F-box-directed CRL complex assembly and regulation by the CSN and CAND1 Mol. Cell 35 2009 586 597
36. N.W. Pierce, J.E. Lee, X. Liu, M.J. Sweredoski, R.L. Graham, E.A. Larimore, M. Rome, N. Zheng, B.E. Clurman, S. Hess, S.O. Shan, and R.J. Deshaies Cand1 promotes assembly of new SCF complexes through dynamic exchange of F box proteins Cell 153 2013 206 215
37. S. Wu, W. Zhu, T. Nhan, J.I. Toth, M.D. Petroski, and D.A. Wolf CAND1 controls in vivo dynamics of the cullin 1-RING ubiquitin ligase repertoire Nat. Commun. 4 2013 1642
38. D.J. Hilton, R.T. Richardson, W.S. Alexander, E.M. Viney, T.A. Willson, N.S. Sprigg, R. Starr, S.E. Nicholson, D. Metcalf, and N.A. Nicola Twenty proteins containing a C-terminal SOCS box form five structural classes Proc. Natl. Acad. Sci. U. S. A. 95 1998 114 119
39. X. Yu, Y. Yu, B. Liu, K. Luo, W. Kong, P. Mao, and X.F. Yu Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-CUL5-SCF complex Science 302 2003 1056 1060
40. E. Querido, P. Blanchette, Q. Yan, T. Kamura, M. Morrison, D. Boivin, W.G. Kaelin, R.C. Conaway, J.W. Conaway, and P.E. Branton Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a cullin-containing complex Genes Dev. 15 2001 3104 3117
41. Q.L. Cai, J.S. Knight, S.C. Verma, P. Zald, and E.S. Robertson EC5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumor suppressors PLoS Pathog. 2 2006 e116
42. J. Jin, X.L. Ang, T. Shirogane, and J. Wade Harper Identification of substrates for F-box proteins Methods Enzymol. 399 2005 287 309
43. F. Verdier, S. Chretien, O. Muller, P. Varlet, A. Yoshimura, S. Gisselbrecht, C. Lacombe, and P. Mayeux Proteasomes regulate erythropoietin receptor and signal transducer and activator of transcription 5 (STAT5) activation. Possible involvement of the ubiquitinated Cis protein J. Biol. Chem. 273 1998 28185 28190
44. P. De Sepulveda, S. Ilangumaran, and R. Rottapel Suppressor of cytokine signaling-1 inhibits VAV function through protein degradation J. Biol. Chem. 275 2000 14005 14008
45. A. Ryo, F. Suizu, Y. Yoshida, K. Perrem, Y.C. Liou, G. Wulf, R. Rottapel, S. Yamaoka, and K.P. Lu Regulation of NF-κB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA Mol. Cell 12 2003 1413 1426
46. E. Liu, J.F. Cote, and K. Vuori Negative regulation of FAK signaling by SOCS proteins Embo J. 22 2003 5036 5046
47. A. Mansell, R. Smith, S.L. Doyle, P. Gray, J.E. Fenner, P.J. Crack, S.E. Nicholson, D.J. Hilton, L.A. O'Neill, and P.J. Hertzog Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation Nat. Immunol. 7 2006 148 155
48. S. Kamizono, T. Hanada, H. Yasukawa, S. Minoguchi, R. Kato, M. Minoguchi, K. Hattori, S. Hatakeyama, M. Yada, S. Morita, T. Kitamura, H. Kato, K. Nakayama, and A. Yoshimura The SOCS box of SOCS1 accelerates ubiquitin-dependent proteolysis of TEL-JAK2 J. Biol. Chem. 276 2001 12530 12538
49. J. Frantsve, J. Schwaller, D.W. Sternberg, J. Kutok, and D.G. Gilliland Socs-1 inhibits TEL-JAK2-mediated transformation of hematopoietic cells through inhibition of JAK2 kinase activity and induction of proteasome-mediated degradation Mol. Cell Biol. 21 2001 3547 3557
50. D. Ungureanu, P. Saharinen, I. Junttila, D.J. Hilton, and O. Silvennoinen Regulation of Jak2 through the ubiquitin-proteasome pathway involves phosphorylation of JAK2 on Y1007 and interaction with SOCS1 Mol. Cell Biol. 22 2002 3316 3326
51. L. Rui, M. Yuan, D. Frantz, S. Shoelson, and M.F. White SOCS1 and SOCS3 block insulin signaling by ubiquitin-mediated degradation of IRS1 and IRS2 J. Biol. Chem. 277 2002 42394 42398
52. S.J. Orr, N.M. Morgan, J. Elliott, J.F. Burrows, C.J. Scott, D.W. McVicar, and J.A. Johnston CD33 responses are blocked by SOCS3 through accelerated proteasomal-mediated turnover Blood 109 2007 1061 1068
53. F. Zadjali, A.C. Pike, M. Vesterlund, J. Sun, C. Wu, S.S. Li, L. Ronnstrand, S. Knapp, A.N. Bullock, and A. Flores-Morales Structural basis for c-KIT inhibition by the suppressor of cytokine signaling 6 (SOCS6) ubiquitin ligase J. Biol. Chem. 286 2011 480 490
54. Y.B. Choi, M. Son, M. Park, J. Shin, and Y. Yun SOCS-6 negatively regulates T cell activation through targeting p56lck to proteasomal degradation J. Biol. Chem. 285 2010 7271 7280
55. M.L. Heuze, F.C. Guibal, C.A. Banks, J.W. Conaway, R.C. Conaway, Y.E. Cayre, A. Benecke, and P.G. Lutz ASB2 is an elongin BC-interacting protein that can assemble with cullin 5 and RBX1 to reconstitute an E3 ubiquitin ligase complex J. Biol. Chem. 280 2005 5468 5474
56. M.L. Heuze, I. Lamsoul, M. Baldassarre, Y. Lad, S. Leveque, Z. Razinia, C. Moog-Lutz, D.A. Calderwood, and P.G. Lutz ASB2 targets filamins A and B to proteasomal degradation Blood 112 2008 5130 5140
57. C.F. Burande, M.L. Heuze, I. Lamsoul, B. Monsarrat, S. Uttenweiler-Joseph, and P.G. Lutz A label-free quantitative proteomics strategy to identify E3 ubiquitin ligase substrates targeted to proteasome degradation Mol. Cell Proteomics 8 2009 1719 1727
58. M. Baldassarre, Z. Razinia, C.F. Burande, I. Lamsoul, P.G. Lutz, and D.A. Calderwood Filamins regulate cell spreading and initiation of cell migration PLoS One 4 2009 e7830
59. I. Lamsoul, C.F. Burande, Z. Razinia, T.C. Houles, D. Menoret, M. Baldassarre, M. Erard, C. Moog-Lutz, D.A. Calderwood, and P.G. Lutz Functional and structural insights into ASB2α, a novel regulator of integrin-dependent adhesion of hematopoietic cells J. Biol. Chem. 286 2011 30571 30581
60. L. Nie, Y. Zhao, W. Wu, Y.Z. Yang, H.C. Wang, and X.H. Sun Notch-induced ASB2 expression promotes protein ubiquitination by forming non-canonical E3 ligase complexes Cell Res. 21 2011 754 769
61. W. Wu, and X.H. Sun A mechanism underlying NOTCH-induced and ubiquitin-mediated JAK3 degradation J. Biol. Chem. 286 2011 41153 41162
62. I. Lamsoul, M. Erard, P.F. van der Ven, and P.G. Lutz Filamins but not janus kinases are substrates of the ASB2α cullin-ring E3 ubiquitin ligase in hematopoietic cells PLoS One 7 2012 e43798
63. J. Wang, A.G. Muntean, and J.L. Hess ECSASB2 mediates MLL degradation during hematopoietic differentiation Blood 119 2012 1151 1161
64. J.H. Martens, A.B. Brinkman, F. Simmer, K.J. Francoijs, A. Nebbioso, F. Ferrara, L. Altucci, and H.G. Stunnenberg PML-RARα/RXR alters the epigenetic landscape in acute promyelocytic leukemia Cancer Cell 17 2010 173 185
65. J.H. Martens, A. Mandoli, F. Simmer, B.J. Wierenga, S. Saeed, A.A. Singh, L. Altucci, E. Vellenga, and H.G. Stunnenberg ERG and FLI1 binding sites demarcate targets for aberrant epigenetic regulation by AML1-ETO in acute myeloid leukemia Blood 120 2012 4038 4048
66. S. Spicuglia, C. Vincent-Fabert, T. Benoukraf, G. Tiberi, A.J. Saurin, J. Zacarias-Cabeza, D. Grimwade, K. Mills, B. Calmels, F. Bertucci, M. Sieweke, P. Ferrier, and E. Duprez Characterisation of Genome-Wide PLZF/RARA Target Genes PLoS One 6 2011 e24176
67. A.S. Chung, Y.J. Guan, Z.L. Yuan, J.E. Albina, and Y.E. Chin Ankyrin repeat and SOCS box 3 (ASB3) mediates ubiquitination and degradation of tumor necrosis factor receptor II Mol. Cell Biol. 25 2005 4716 4726
68. J.Y. Li, B. Chai, W. Zhang, X. Wu, C. Zhang, D. Fritze, Z. Xia, C. Patterson, and M.W. Mulholland Ankyrin repeat and SOCS box containing protein 4 (ASB4) colocalizes with insulin receptor substrate 4 (IRS4) in the hypothalamic neurons and mediates IRS4 degradation BMC Neurosci. 12 2011 95
69. W.H. Townley-Tilson, Y. Wu, J.E. Ferguson 3rd, and C. Patterson The ubiquitin ligase ASB4 promotes trophoblast differentiation through the degradation of ID2 PLoS One 9 2014 e89451
70. M.A. Debrincat, J.G. Zhang, T.A. Willson, J. Silke, L.M. Connolly, R.J. Simpson, W.S. Alexander, N.A. Nicola, B.T. Kile, and D.J. Hilton Ankyrin repeat and suppressors of cytokine signaling box protein ASB9 targets creatine kinase B for degradation J. Biol. Chem. 282 2007 4728 4737
71. S.H. Diks, M.A. Sartori da Silva, J.L. Hillebrands, R.J. Bink, H.H. Versteeg, C. van Rooijen, A. Brouwers, A.B. Chitnis, M.P. Peppelenbosch, and D. Zivkovic d-ASB11 is an essential mediator of canonical Delta-Notch signalling Nat. Cell Biol. 10 2008 1190 1198
72. M.A. Sartori da Silva, J.M. Tee, J. Paridaen, A. Brouwers, V. Runtuwene, D. Zivkovic, S.H. Diks, D. Guardavaccaro, and M.P. Peppelenbosch Essential role for the d-ASB11 CUL5 Box domain for proper notch signaling and neural cell fate decisions in vivo PLoS One 5 2010 e14023
73. S. Liu, T. Nheu, R. Luwor, S.E. Nicholson, and H.J. Zhu SPSB1, a novel negative regulator of the TGF-β signaling pathway targeting the Type II receptor J. Biol. Chem. 290 2015 17894 17908
74. Z. Kuang, R.S. Lewis, J.M. Curtis, Y. Zhan, B.M. Saunders, J.J. Babon, T.B. Kolesnik, A. Low, S.L. Masters, T.A. Willson, L. Kedzierski, S. Yao, E. Handman, R.S. Norton, and S.E. Nicholson The SPRY domain-containing SOCS box protein SPSB2 targets iNOS for proteasomal degradation J. Cell Biol. 190 2010 129 141
75. T. Nishiya, K. Matsumoto, S. Maekawa, E. Kajita, T. Horinouchi, M. Fujimuro, K. Ogasawara, T. Uehara, and S. Miwa Regulation of inducible nitric-oxide synthase by the SPRY domain- and SOCS box-containing proteins J. Biol. Chem. 286 2011 9009 9019
76. Y. Feng, T.C. Pan, D.K. Pant, K.R. Chakrabarti, J.V. Alvarez, J.R. Ruth, and L.A. Chodosh SPSB1 promotes breast cancer recurrence by potentiating c-MET signaling Cancer Discov. 4 2014 790 803
77. D.W. Choi, Y.M. Seo, E.A. Kim, K.S. Sung, J.W. Ahn, S.J. Park, S.R. Lee, and C.Y. Choi Ubiquitination and degradation of homeodomain-interacting protein kinase 2 by WD40 repeat/SOCS box protein WSB-1 J. Biol. Chem. 283 2008 4682 4689
78. M. Dentice, A. Bandyopadhyay, B. Gereben, I. Callebaut, M.A. Christoffolete, B.W. Kim, S. Nissim, J.P. Mornon, A.M. Zavacki, A. Zeold, L.P. Capelo, C. Curcio-Morelli, R. Ribeiro, J.W. Harney, C.J. Tabin, and A.C. Bianco The Hedgehog-inducible ubiquitin ligase subunit WSB-1 modulates thyroid hormone activation and PTHrP secretion in the developing growth plate Nat. Cell Biol. 7 2005 698 705
79. T. Yasukawa, T. Kamura, S. Kitajima, R.C. Conaway, J.W. Conaway, and T. Aso Mammalian Elongin A complex mediates DNA-damage-induced ubiquitylation and degradation of Rpb1 EMBO J. 27 2008 3256 3266
80. Y. Yu, Z. Xiao, E.S. Ehrlich, X. Yu, and X.F. Yu Selective assembly of HIV-1 Vif-Cul5-ElonginB-ElonginC E3 ubiquitin ligase complex through a novel SOCS box and upstream cysteines Genes Dev. 18 2004 2867 2872
81. B. Liu, P.T. Sarkis, K. Luo, Y. Yu, and X.F. Yu Regulation of Apobec3F and human immunodeficiency virus type 1 Vif by Vif-CUL5-ElonB/C E3 ubiquitin ligase J. Virol. 79 2005 9579 9587
82. J.N. Harada, A. Shevchenko, D.C. Pallas, and A.J. Berk Analysis of the adenovirus E1B-55K-anchored proteome reveals its link to ubiquitination machinery J. Virol. 76 2002 9194 9206
83. P. Blanchette, C.Y. Cheng, Q. Yan, G. Ketner, D.A. Ornelles, T. Dobner, R.C. Conaway, J.W. Conaway, and P.E. Branton Both BC-box motifs of adenovirus protein E4orf6 are required to efficiently assemble an E3 ligase complex that degrades p53 Mol. Cell Biol. 24 2004 9619 9629
84. K. Luo, E. Ehrlich, Z. Xiao, W. Zhang, G. Ketner, and X.F. Yu Adenovirus E4orf6 assembles with Cullin5-ElonginB-ElonginC E3 ubiquitin ligase through an HIV/SIV Vif-like BC-box to regulate p53 FASEB J. 21 2007 1742 1750
85. T.H. Stracker, C.T. Carson, and M.D. Weitzman Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex Nature 418 2002 348 352
86. A. Baker, K.J. Rohleder, L.A. Hanakahi, and G. Ketner Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation J. Virol. 81 2007 7034 7040
87. F. Dallaire, P. Blanchette, P. Groitl, T. Dobner, and P.E. Branton Identification of integrin α3 as a new substrate of the adenovirus E4orf6/E1B 55-kilodalton E3 ubiquitin ligase complex J. Virol. 83 2009 5329 5338
88. R. Nayak, and D.J. Pintel Positive and negative effects of adenovirus type 5 helper functions on adeno-associated virus type 5 (AAV5) protein accumulation govern AAV5 virus production J. Virol. 81 2007 2205 2212
89. R. Boggio, A. Passafaro, and S. Chiocca Targeting SUMO E1 to ubiquitin ligases: a viral strategy to counteract sumoylation J. Biol. Chem. 282 2007 15376 15382
90. Y. Sato, T. Kamura, N. Shirata, T. Murata, A. Kudoh, S. Iwahori, S. Nakayama, H. Isomura, Y. Nishiyama, and T. Tsurumi Degradation of phosphorylated p53 by viral protein-ECS E3 ligase complex PLoS Pathog. 5 2009 e1000530
91. Y. Sato, N. Shirata, A. Kudoh, S. Iwahori, S. Nakayama, T. Murata, H. Isomura, Y. Nishiyama, and T. Tsurumi Expression of Epstein-Barr virus BZLF1 immediate-early protein induces p53 degradation independent of MDM2, leading to repression of p53-mediated transcription Virology 388 2009 204 211
92. L. Rodrigues, J. Filipe, M.P. Seldon, L. Fonseca, J. Anrather, M.P. Soares, and J.P. Simas Termination of NF-κB activity through a gammaherpesvirus protein that assembles an EC5S ubiquitin-ligase EMBO J. 28 2009 1283 1295
93. L.R. Dick, and P.E. Fleming Building on bortezomib: second-generation proteasome inhibitors as anti-cancer therapy Drug Discov. Today 15 2010 243 249
94. D.F. Ceccarelli, X. Tang, B. Pelletier, S. Orlicky, W. Xie, V. Plantevin, D. Neculai, Y.C. Chou, A. Ogunjimi, A. Al-Hakim, X. Varelas, J. Koszela, G.A. Wasney, M. Vedadi, S. Dhe-Paganon, S. Cox, S. Xu, A. Lopez-Girona, F. Mercurio, J. Wrana, D. Durocher, S. Meloche, D.R. Webb, M. Tyers, and F. Sicheri An allosteric inhibitor of the human Cdc34 ubiquitin-conjugating enzyme Cell 145 2011 1075 1087
95. H. Huang, D.F. Ceccarelli, S. Orlicky, D.J. St-Cyr, A. Ziemba, P. Garg, S. Plamondon, M. Auer, S. Sidhu, A. Marinier, G. Kleiger, M. Tyers, and F. Sicheri E2 enzyme inhibition by stabilization of a low-affinity interface with ubiquitin Nat. Chem. Biol. 10 2014 156 163
96. J.E. Brownell, M.D. Sintchak, J.M. Gavin, H. Liao, F.J. Bruzzese, N.J. Bump, T.A. Soucy, M.A. Milhollen, X. Yang, A.L. Burkhardt, J. Ma, H.K. Loke, T. Lingaraj, D. Wu, K.B. Hamman, J.J. Spelman, C.A. Cullis, S.P. Langston, S. Vyskocil, T.B. Sells, W.D. Mallender, I. Visiers, P. Li, C.F. Claiborne, M. Rolfe, J.B. Bolen, and L.R. Dick Substrate-assisted inhibition of ubiquitin-like protein-activating enzymes: the NEDD8 E1 inhibitor MLN4924 forms a NEDD8-AMP mimetic in situ Mol. Cell 37 2010 102 111
97. M.A. Milhollen, T. Traore, J. Adams-Duffy, M.P. Thomas, A.J. Berger, L. Dang, L.R. Dick, J.J. Garnsey, E. Koenig, S.P. Langston, M. Manfredi, U. Narayanan, M. Rolfe, L.M. Staudt, T.A. Soucy, J. Yu, J. Zhang, J.B. Bolen, and P.G. Smith MLN4924, a NEDD8-activating enzyme inhibitor, is active in diffuse large B-cell lymphoma models: rationale for treatment of NF-{kappa}B-dependent lymphoma Blood 116 2010 1515 1523
98. J.C. Godbersen, L.A. Humphries, O.V. Danilova, P.E. Kebbekus, J.R. Brown, A. Eastman, and A.V. Danilov The NEDD8-activating enzyme inhibitor MLN4924 thwarts microenvironment-driven NF-kappaB activation and induces apoptosis in chronic lymphocytic leukemia B cells Clin. Cancer Res. 20 2014 1576 1589
99. R.T. Swords, K.R. Kelly, P.G. Smith, J.J. Garnsey, D. Mahalingam, E. Medina, K. Oberheu, S. Padmanabhan, M. O'Dwyer, S.T. Nawrocki, F.J. Giles, and J.S. Carew Inhibition of NEDD8-activating enzyme: a novel approach for the treatment of acute myeloid leukemia Blood 115 2010 3796 3800
100. D.W. McMillin, H.M. Jacobs, J.E. Delmore, L. Buon, Z.R. Hunter, V. Monrose, J. Yu, P.G. Smith, P.G. Richardson, K.C. Anderson, S.P. Treon, A.L. Kung, and C.S. Mitsiades Molecular and cellular effects of NEDD8-activating enzyme inhibition in myeloma Mol. Cancer Ther. 11 2012 942 951
101. C. Mackintosh, D.J. Garcia-Dominguez, J.L. Ordonez, A. Ginel-Picardo, P.G. Smith, M.P. Sacristan, and E. de Alava WEE1 accumulation and deregulation of S-phase proteins mediate MLN4924 potent inhibitory effect on Ewing sarcoma cells Oncogene 32 2013 1441 1451
102. L. Jia, H. Li, and Y. Sun Induction of p21-dependent senescence by an NAE inhibitor, MLN4924, as a mechanism of growth suppression Neoplasia 13 2011 561 569
103. D.J. Hughes, J.J. Wood, B.R. Jackson, B. Baquero-Perez, and A. Whitehouse NEDDylation is essential for Kaposi's sarcoma-associated herpesvirus latency and lytic reactivation and represents a novel anti-KSHV target PLoS Pathog. 11 2015 e1004771
104. Z. Luo, G. Yu, H.W. Lee, L. Li, L. Wang, D. Yang, Y. Pan, C. Ding, J. Qian, L. Wu, Y. Chu, J. Yi, X. Wang, Y. Sun, L.S. Jeong, J. Liu, and L. Jia The NEDD8-activating enzyme inhibitor MLN4924 induces autophagy and apoptosis to suppress liver cancer cell growth Cancer Res. 72 2012 3360 3371
105. Y. Zhao, X. Xiong, L. Jia, and Y. Sun Targeting Cullin-RING ligases by MLN4924 induces autophagy via modulating the HIF1-REDD1-TSC1-mTORC1-DEPTOR axis Cell Death Dis. 3 2012 e386
106. D. Yang, M. Tan, G. Wang, and Y. Sun The p21-dependent radiosensitization of human breast cancer cells by MLN4924, an investigational inhibitor of NEDD8 activating enzyme PLoS One 7 2012 e34079
107. D. Wei, H. Li, J. Yu, J.T. Sebolt, L. Zhao, T.S. Lawrence, P.G. Smith, M.A. Morgan, and Y. Sun Radiosensitization of human pancreatic cancer cells by MLN4924, an investigational NEDD8-activating enzyme inhibitor Cancer Res. 72 2012 282 293
108. A.A. Jazaeri, E. Shibata, J. Park, J.L. Bryant, M.R. Conaway, S.C. Modesitt, P.G. Smith, M.A. Milhollen, A.J. Berger, and A. Dutta Overcoming platinum resistance in preclinical models of ovarian cancer using the neddylation inhibitor MLN4924 Mol. Cancer Ther. 12 2013 1958 1967
109. S.T. Nawrocki, K.R. Kelly, P.G. Smith, C.M. Espitia, A. Possemato, S.A. Beausoleil, M. Milhollen, S. Blakemore, M. Thomas, A. Berger, and J.S. Carew Disrupting protein NEDDylation with MLN4924 is a novel strategy to target cisplatin resistance in ovarian cancer Clin. Cancer Res. 19 2013 3577 3590
110. K. Garcia, J.L. Blank, D.C. Bouck, X.J. Liu, D.S. Sappal, G. Hather, K. Cosmopoulos, M.P. Thomas, M. Kuranda, M.D. Pickard, R. Liu, S. Bandi, P.G. Smith, and E.S. Lightcap NEDD8-activating enzyme inhibitor MLN4924 provides synergy with mitomycin C through interactions with ATR, BRCA1/BRCA2, and chromatin dynamics pathways Mol. Cancer Ther. 13 2014 1625 1635
111. S.T. Nawrocki, K.R. Kelly, P.G. Smith, M. Keaton, H. Carraway, M.A. Sekeres, J.P. Maciejewski, and J.S. Carew The NEDD8-activating enzyme inhibitor MLN4924 disrupts nucleotide metabolism and augments the efficacy of cytarabine Clin. Cancer Res. 21 2015 439 447
112. M.A. Milhollen, M.P. Thomas, U. Narayanan, T. Traore, J. Riceberg, B.S. Amidon, N.F. Bence, J.B. Bolen, J. Brownell, L.R. Dick, H.K. Loke, A.A. McDonald, J. Ma, M.G. Manfredi, T.B. Sells, M.D. Sintchak, X. Yang, Q. Xu, E.M. Koenig, J.M. Gavin, and P.G. Smith Treatment-emergent mutations in NAEβ confer resistance to the NEDD8-activating enzyme inhibitor MLN4924 Cancer Cell 21 2012 388 401
113. G.W. Xu, J.I. Toth, S.R. da Silva, S.L. Paiva, J.L. Lukkarila, R. Hurren, N. Maclean, M.A. Sukhai, R.N. Bhattacharjee, C.A. Goard, B. Medeiros, P.T. Gunning, S. Dhe-Paganon, M.D. Petroski, and A.D. Schimmer Mutations in UBA3 confer resistance to the NEDD8-activating enzyme inhibitor MLN4924 in human leukemic cells PLoS One 9 2014 e93530
114. Z. Wang, P. Liu, H. Inuzuka, and W. Wei Roles of F-box proteins in cancer Nat. Rev. Cancer 14 2014 233 247
115. J.R. Skaar, J.K. Pagan, and M. Pagano SCF ubiquitin ligase-targeted therapies Nat. Rev. Drug Discov. 13 2014 889 903
116. A.N. Bullock, J.E. Debreczeni, A.M. Edwards, M. Sundstrom, and S. Knapp Crystal structure of the SOCS2-elongin C-elongin B complex defines a prototypical SOCS box ubiquitin ligase Proc. Natl. Acad. Sci. U. S. A. 103 2006 7637 7642
117. A.N. Bullock, M.C. Rodriguez, J.E. Debreczeni, Z. Songyang, and S. Knapp Structure of the SOCS4-ElonginB/C complex reveals a distinct SOCS box interface and the molecular basis for SOCS-dependent EGFR degradation Structure 15 2007 1493 1504
118. Y.K. Kim, M.J. Kwak, B. Ku, H.Y. Suh, K. Joo, J. Lee, J.U. Jung, and B.H. Oh Structural basis of intersubunit recognition in elongin BC-cullin 5-SOCS box ubiquitin-protein ligase complexes Acta Crystallogr. D Biol. Crystallogr. 69 2013 1587 1597
119. J.R. Muniz, K. Guo, N.J. Kershaw, V. Ayinampudi, F. von Delft, J.J. Babon, and A.N. Bullock Molecular architecture of the ankyrin SOCS box family of Cul5-dependent E3 ubiquitin ligases J. Mol. Biol. 425 2013 3166 3177
120. J.C. Thomas, D. Matak-Vinkovic, I. Van Molle, and A. Ciulli Multimeric complexes among ankyrin-repeat and SOCS-box protein 9 (ASB9), ElonginBC, and Cullin 5: insights into the structure and assembly of ECS-type Cullin-RING E3 ubiquitin ligases Biochemistry 52 2013 5236 5246
121. Y. Guo, L. Dong, X. Qiu, Y. Wang, B. Zhang, H. Liu, Y. Yu, Y. Zang, M. Yang, and Z. Huang Structural basis for hijacking CBF-beta and CUL5 E3 ligase complex by HIV-1 Vif Nature 505 2014 229 233
122. N. Zheng, B.A. Schulman, L. Song, J.J. Miller, P.D. Jeffrey, P. Wang, C. Chu, D.M. Koepp, S.J. Elledge, M. Pagano, R.C. Conaway, J.W. Conaway, J.W. Harper, and N.P. Pavletich Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex Nature 416 2002 703 709
123. R. Nathans, H. Cao, N. Sharova, A. Ali, M. Sharkey, R. Stranska, M. Stevenson, and T.M. Rana Small-molecule inhibition of HIV-1 Vif Nat. Biotechnol. 26 2008 1187 1192
124. T. Zuo, D. Liu, W. Lv, X. Wang, J. Wang, M. Lv, W. Huang, J. Wu, H. Zhang, H. Jin, L. Zhang, W. Kong, and X. Yu Small-molecule inhibition of human immunodeficiency virus type 1 replication by targeting the interaction between Vif and ElonginC J. Virol. 86 2012 5497 5507