Inhibition of NEDD8-conjugation pathway by novel molecules: Potential approaches to anticancer therapy

Molecular Oncology

Volumn 6, Issue 3, 2012, Pages 267-275

  Tanaka, Tomoaki ^a   Nakatani, Tatsuya ^a   Kamitani, Tetsu ^b  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

MLN4924; NEDD8; NUB1; SCF complex; Ubc12; Ubiquitination

Indexed keywords

COP9 SIGNALOSOME; CULLIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NEDD8 PROTEIN; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE E3; [4 [4 [(2,3 DIHYDRO 1H INDEN 1 YL)AMINO] 7H PYRROLO[2,3 D]PYRIMIDIN 7 YL] 2 HYDROXYCYCLOPENTYLMETHYL] SULFAMATE;

APOPTOSIS; CANCER THERAPY; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONJUGATION; DNA REPLICATION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; HUMAN; IN VITRO STUDY; NEDDYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; UBIQUITINATION;

EID: 84862786350     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2012.01.003     Document Type: Review

References (113)

1. Abida W.M., Nikolaev A., Zhao W., Zhang W., Gu W. FBXO11 promotes the neddylation of p53 and inhibits its transcriptional activity. J. Biol. Chem. 2007, 282:1797-1804.
2. Adler A.S., Lin M., Horlings H., Nuyten D.S., van de Vijver M.J., Chang H.Y. Genetic regulators of large-scale transcriptional signatures in cancer. Nat. Genet. 2006, 38:421-430.
3. Amir R.E., Iwai K., Ciechanover A. The NEDD8 pathway is essential for SCF(beta -TrCP)-mediated ubiquitination and processing of the NF-kappa B precursor p105. J. Biol. Chem. 2002, 277:23253-23259.
4. Andrews P., He Y.J., Xiong Y. Cytoplasmic localized ubiquitin ligase cullin 7 binds to p53 and promotes cell growth by antagonizing p53 function. Oncogene 2006, 25:4534-4548.
5. Angers S., Thorpe C.J., Biechele T.L., Goldenberg S.J., Zheng N., MacCoss M.J., Moon R.T. The KLHL12-Cullin-3 ubiquitin ligase negatively regulates the Wnt-beta-catenin pathway by targeting Dishevelled for degradation. Nat. Cell Biol. 2006, 8:348-357.
6. Bawa-Khalfe T., Yeh E.T. SUMO losing balance: SUMO proteases disrupt SUMO homeostasis to facilitate cancer development and progression. Genes Cancer 2010, 1:748-752.
7. Belaidouni N., Peuchmaur M., Perret C., Florentin A., Benarous R., Besnard-Guerin C. Overexpression of human beta TrCP1 deleted of its F box induces tumorigenesis in transgenic mice. Oncogene 2005, 24:2271-2276.
8. Berg J.P., Zhou Q., Breuhahn K., Schirmacher P., Patil M.A., Chen X., Schafer N., Holler T.T., Fischer H.P., Buttner R., Gutgemann I. Inverse expression of Jun activation domain binding protein 1 and cell cycle inhibitor p27Kip1: influence on proliferation in hepatocellular carcinoma. Hum. Pathol. 2007, 38:1621-1627.
9. Bosu D.R., Kipreos E.T. Cullin-RING ubiquitin ligases: global regulation and activation cycles. Cell Div. 2008, 3:7.
10. Burnatowska-Hledin M.A., Kossoris J.B., Van Dort C.J., Shearer R.L., Zhao P., Murrey D.A., Abbott J.L., Kan C.E., Barney C.C. T47D breast cancer cell growth is inhibited by expression of VACM-1, a cul-5 gene. Biochem. Biophys. Res. Commun. 2004, 319:817-825.
11. Chairatvit K., Ngamkitidechakul C. Control of cell proliferation via elevated NEDD8 conjugation in oral squamous cell carcinoma. Mol. Cell Biochem. 2007, 306:163-169.
12. Chan Y., Yoon J., Wu J.T., Kim H.J., Pan K.T., Yim J., Chien C.T. DEN1 deneddylates non-cullin proteins in vivo. J. Cell Sci. 2008, 121:3218-3223.
13. Chen L.C., Manjeshwar S., Lu Y., Moore D., Ljung B.M., Kuo W.L., Dairkee S.H., Wernick M., Collins C., Smith H.S. The human homologue for the Caenorhabditis elegans cul-4 gene is amplified and overexpressed in primary breast cancers. Cancer Res. 1998, 58:3677-3683.
14. Ciechanover A. The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J. 1998, 17:7151-7160.
15. Ciechanover A., Schwartz A.L. The ubiquitin-proteasome pathway: the complexity and myriad functions of proteins death. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:2727-2730.
16. Cope G.A., Suh G.S., Aravind L., Schwarz S.E., Zipursky S.L., Koonin E.V., Deshaies R.J. Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 2002, 298:608-611.
17. Deng X.W., Dubiel W., Wei N., Hofmann K., Mundt K., Colicelli J., Kato J., Naumann M., Segal D., Seeger M., Carr A., Glickman M., Chamovitz D.A. Unified nomenclature for the COP9 signalosome and its subunits: an essential regulator of development. Trends Genet. 2000, 16:202-203.
18. Dubiel W. Resolving the CSN and CAND1 paradoxes. Mol. Cell 2009, 35:547-549.
19. Furukawa M., He Y.J., Borchers C., Xiong Y. Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases. Nat. Cell Biol. 2003, 5:1001-1007.
20. Furukawa M., Xiong Y. BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the Cullin 3-Roc1 ligase. Mol. Cell Biol. 2005, 25:162-171.
21. Gao F., Cheng J., Shi T., Yeh E.T. Neddylation of a breast cancer-associated protein recruits a class III histone deacetylase that represses NFkappaB-dependent transcription. Nat. Cell Biol. 2006, 8:1171-1177.
22. Goldenberg S.J., Cascio T.C., Shumway S.D., Garbutt K.C., Liu J., Xiong Y., Zheng N. Structure of the Cand1-Cul1-Roc1 complex reveals regulatory mechanisms for the assembly of the multisubunit cullin-dependent ubiquitin ligases. Cell 2004, 119:517-528.
23. Gong L., Yeh E.T. Identification of the activating and conjugating enzymes of the NEDD8 conjugation pathway. J. Biol. Chem. 1999, 274:12036-12042.
24. Gong L., Kamitani T., Millas S., Yeh E.T. Identification of a novel isopeptidase with dual specificity for ubiquitin- and NEDD8-conjugated proteins. J. Biol. Chem. 2000, 275:14212-14216.
25. Groisman R., Polanowska J., Kuraoka I., Sawada J., Saijo M., Drapkin R., Kisselev A.F., Tanaka K., Nakatani Y. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 2003, 113:357-367.
26. Grossberger R., Gieffers C., Zachariae W., Podtelejnikov A.V., Schleiffer A., Nasmyth K., Mann M., Peters J.M. Characterization of the DOC1/APC10 subunit of the yeast and the human anaphase-promoting complex. J. Biol. Chem. 1999, 274:14500-14507.
27. Guardavaccaro D., Pagano M. Oncogenic aberrations of cullin-dependent ubiquitin ligases. Oncogene 2004, 23:2037-2049.
28. Haas A.L., Ahrens P., Bright P.M., Ankel H. Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J. Biol. Chem. 1987, 262:11315-11323.
29. Harper J.W. Neddylating the guardian; Mdm2 catalyzed conjugation of Nedd8 to p53. Cell 2004, 118:2-4.
30. Hershko A. The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle. Cell Death Differ. 2005, 12:1191-1197.
31. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
32. Hilton D.J. Negative regulators of cytokine signal transduction. Cell Mol. Life Sci. 1999, 55:1568-1577.
33. Hori T., Osaka F., Chiba T., Miyamoto C., Okabayashi K., Shimbara N., Kato S., Tanaka K. Covalent modification of all members of human cullin family proteins by NEDD8. Oncogene 1999, 18:6829-6834.
34. Hosono T., Tanaka T., Tanji K., Nakatani T., Kamitani T. NUB1, an interferon-inducible protein, mediates anti-proliferative actions and apoptosis in renal cell carcinoma cells through cell-cycle regulation. Br. J. Cancer 2010, 102:873-882.
35. Hu J., McCall C.M., Ohta T., Xiong Y. Targeted ubiquitination of CDT1 by the DDB1-CUL4A-ROC1 ligase in response to DNA damage. Nat. Cell Biol. 2004, 6:1003-1009.
36. Hu J., Zacharek S., He Y.J., Lee H., Shumway S., Duronio R.J., Xiong Y. WD40 protein FBW5 promotes ubiquitination of tumor suppressor TSC2 by DDB1-CUL4-ROC1 ligase. Genes Dev. 2008, 22:866-871.
37. Huang D.T., Paydar A., Zhuang M., Waddell M.B., Holton J.M., Schulman B.A. Structural basis for recruitment of Ubc12 by an E2 binding domain in NEDD8's E1. Mol. Cell 2005, 17:341-350.
38. Ichimura Y., Kirisako T., Takao T., Satomi Y., Shimonishi Y., Ishihara N., Mizushima N., Tanida I., Kominami E., Ohsumi M., Noda T., Ohsumi Y. A ubiquitin-like system mediates protein lipidation. Nature 2000, 408:488-492.
39. Jackson S., Xiong Y. CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem. Sci. 2009, 34:562-570.
40. Jagannath S., Barlogie B., Berenson J.R., Singhal S., Alexanian R., Srkalovic G., Orlowski R.Z., Richardson P.G., Anderson J., Nix D., Esseltine D.L., Anderson K.C. Bortezomib in recurrent and/or refractory multiple myeloma. Initial clinical experience in patients with impaired renal function. Cancer 2005, 103:1195-1200.
41. Johnson A.E., Le I.P., Buchwalter A., Burnatowska-Hledin M.A. Estrogen-dependent growth and estrogen receptor (ER)-alpha concentration in T47D breast cancer cells are inhibited by VACM-1, a cul 5 gene. Mol. Cell Biochem. 2007, 301:13-20.
42. Kaelin W.G., Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 2008, 30:393-402.
43. Kamitani T., Kito K., Fukuda-Kamitani T., Yeh E.T. Targeting of NEDD8 and its conjugates for proteasomal degradation by NUB1. J. Biol. Chem. 2001, 276:46655-46660.
44. Kamitani T., Kito K., Nguyen H.P., Yeh E.T. Characterization of NEDD8, a developmentally down-regulated ubiquitin-like protein. J. Biol. Chem. 1997, 272:28557-28562.
45. Kamura T., Conrad M.N., Yan Q., Conaway R.C., Conaway J.W. The Rbx1 subunit of SCF and VHL E3 ubiquitin ligase activates Rub1 modification of cullins Cdc53 and Cul2. Genes Dev. 1999, 13:2928-2933.
46. Kamura T., Koepp D.M., Conrad M.N., Skowyra D., Moreland R.J., Iliopoulos O., Lane W.S., Kaelin W.G., Elledge S.J., Conaway R.C., Harper J.W., Conaway J.W. Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 1999, 284:657-661.
47. DDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2588-2593.
48. Kaustov L., Lukin J., Lemak A., Duan S., Ho M., Doherty R., Penn L.Z., Arrowsmith C.H. The conserved CPH domains of Cul7 and PARC are protein-protein interaction modules that bind the tetramerization domain of p53. J. Biol. Chem. 2007, 282:11300-11307.
49. Kipreos E.T., Lander L.E., Wing J.P., He W.W., Hedgecock E.M. cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 1996, 85:829-839.
50. Kito K., Yeh E.T., Kamitani T. NUB1, a NEDD8-interacting protein, is induced by interferon and down-regulates the NEDD8 expression. J. Biol. Chem. 2001, 276:20603-20609.
51. Kouvaraki M.A., Korapati A.L., Rassidakis G.Z., Tian L., Zhang Q., Chiao P., Ho L., Evans D.B., Claret F.X. Potential role of Jun activation domain-binding protein 1 as a negative regulator of p27kip1 in pancreatic adenocarcinoma. Cancer Res. 2006, 66:8581-8589.
52. Kudo Y., Kitajima S., Ogawa I., Kitagawa M., Miyauchi M., Takata T. Small interfering RNA targeting of S phase kinase-interacting protein 2 inhibits cell growth of oral cancer cells by inhibiting p27 degradation. Mol. Cancer Ther. 2005, 4:471-476.
53. Kumar S., Tomooka Y., Noda M. Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem. Biophys. Res. Commun. 1992, 185:1155-1161.
54. Kurz T., Chou Y.C., Willems A.R., Meyer-Schaller N., Hecht M.L., Tyers M., Peter M., Sicheri F. Dcn1 functions as a scaffold-type E3 ligase for cullin neddylation. Mol. Cell 2008, 29:23-35.
55. Kurz T., Ozlu N., Rudolf F., O'Rourke S.M., Luke B., Hofmann K., Hyman A.A., Bowerman B., Peter M. The conserved protein DCN-1/Dcn1p is required for cullin neddylation in C. elegans and S. cerevisiae. Nature 2005, 435:1257-1261.
56. Laney J.D., Hochstrasser M. Substrate targeting in the ubiquitin system. Cell 1999, 97:427-430.
57. Leck Y.C., Choo Y.Y., Tan C.Y., Smith P.G., Hagen T. Biochemical and cellular effects of inhibiting Nedd8 conjugation. Biochem. Biophys. Res. Commun. 2010, 398:588-593.
58. Li W., Kong A.N. Molecular mechanisms of Nrf2-mediated antioxidant response. Mol. Carcinog. 2009, 48:91-104.
59. Lisztwan J., Imbert G., Wirbelauer C., Gstaiger M., Krek W. The von Hippel-Lindau tumor suppressor protein is a component of an E3 ubiquitin-protein ligase activity. Genes Dev. 1999, 13:1822-1833.
60. Liu J., Furukawa M., Matsumoto T., Xiong Y. NEDD8 modification of CUL1 dissociates p120(CAND1), an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol. Cell 2002, 10:1511-1518.
61. Liu L., Lee S., Zhang J., Peters S.B., Hannah J., Zhang Y., Yin Y., Koff A., Ma L., Zhou P. CUL4A abrogation augments DNA damage response and protection against skin carcinogenesis. Mol. Cell 2009, 34:451-460.
62. Liu Y.C., Pan J., Zhang C., Fan W., Collinge M., Bender J.R., Weissman S.M. A MHC-encoded ubiquitin-like protein (FAT10) binds noncovalently to the spindle assembly checkpoint protein MAD2. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:4313-4318.
63. Loeb K.R., Haas A.L. The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J. Biol. Chem. 1992, 267:7806-7813.
64. Lyapina S., Cope G., Shevchenko A., Serino G., Tsuge T., Zhou C., Wolf D.A., Wei N., Deshaies R.J. Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 2001, 292:1382-1385.
65. Melchor L., Saucedo-Cuevas L.P., Munoz-Repeto I., Rodriguez-Pinilla S.M., Honrado E., Campoverde A., Palacios J., Nathanson K.L., Garcia M.J., Benitez J. Comprehensive characterization of the DNA amplification at 13q34 in human breast cancer reveals TFDP1 and CUL4A as likely candidate target genes. Breast Cancer Res. 2009, 11:R86.
66. Mendoza H.M., Shen L.N., Botting C., Lewis A., Chen J., Ink B., Hay R.T. NEDP1, a highly conserved cysteine protease that deNEDDylates Cullins. J. Biol. Chem. 2003, 278:25637-25643.
67. Milhollen M.A., Traore T., Adams-Duffy J., Thomas M.P., Berger A.J., Dang L., Dick L.R., Garnsey J.J., Koenig E., Langston S.P., Manfredi M., Narayanan U., Rolfe M., Staudt L.M., Soucy T.A., Yu J., Zhang J., Bolen J.B., Smith P.G. 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 2010, 116:1515-1523.
68. Mizushima N., Noda T., Yoshimori T., Tanaka Y., Ishii T., George M.D., Klionsky D.J., Ohsumi M., Ohsumi Y. A protein conjugation system essential for autophagy. Nature 1998, 395:395-398.
69. Morimoto M., Nishida T., Honda R., Yasuda H. Modification of cullin-1 by ubiquitin-like protein Nedd8 enhances the activity of SCF(skp2) toward p27(kip1). Biochem. Biophys. Res. Commun. 2000, 270:1093-1096.
70. Morimoto M., Nishida T., Nagayama Y., Yasuda H. Nedd8-modification of Cul1 is promoted by Roc1 as a Nedd8-E3 ligase and regulates its stability. Biochem. Biophys. Res. Commun. 2003, 301:392-398.
71. Murata T., Takayama K., Katayama S., Urano T., Horie-Inoue K., Ikeda K., Takahashi S., Kawazu C., Hasegawa A., Ouchi Y., Homma Y., Hayashizaki Y., Inoue S. miR-148a is an androgen-responsive microRNA that promotes LNCaP prostate cell growth by repressing its target CAND1 expression. Prostate Cancer Prostatic Dis. 2010, 13:356-361.
72. Okabe H., Lee S.H., Phuchareon J., Albertson D.G., McCormick F., Tetsu O. A critical role for FBXW8 and MAPK in cyclin D1 degradation and cancer cell proliferation. PLoS One 2006, 1:e128.
73. Osaka F., Kawasaki H., Aida N., Saeki M., Chiba T., Kawashima S., Tanaka K., Kato S. A new NEDD8-ligating system for cullin-4A. Genes Dev. 1998, 12:2263-2268.
74. Oved S., Mosesson Y., Zwang Y., Santonico E., Shtiegman K., Marmor M.D., Kochupurakkal B.S., Katz M., Lavi S., Cesareni G., Yarden Y. Conjugation to Nedd8 instigates ubiquitylation and down-regulation of activated receptor tyrosine kinases. J. Biol. Chem. 2006, 281:21640-21651.
75. Pagano M. Cell cycle regulation by the ubiquitin pathway. FASEB J. 1997, 11:1067-1075.
76. Panattoni M., Sanvito F., Basso V., Doglioni C., Casorati G., Montini E., Bender J.R., Mondino A., Pardi R. Targeted inactivation of the COP9 signalosome impairs multiple stages of T cell development. J. Exp. Med. 2008, 205:465-477.
77. Pintard L., Willis J.H., Willems A., Johnson J.L., Srayko M., Kurz T., Glaser S., Mains P.E., Tyers M., Bowerman B., Peter M. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 2003, 425:311-316.
78. Podust V.N., Brownell J.E., Gladysheva T.B., Luo R.S., Wang C., Coggins M.B., Pierce J.W., Lightcap E.S., Chau V. A Nedd8 conjugation pathway is essential for proteolytic targeting of p27Kip1 by ubiquitination. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:4579-4584.
79. Rabut G., Peter M. Function and regulation of protein neddylation. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep. 2008, 9:969-976.
80. Rao-Naik C., delaCruz W., Laplaza J.M., Tan S., Callis J., Fisher A.J. The rub family of ubiquitin-like proteins. Crystal structure of Arabidopsis rub1 and expression of multiple rubs in Arabidopsis. J. Biol. Chem. 1998, 273:34976-34982.
81. Read M.A., Brownell J.E., Gladysheva T.B., Hottelet M., Parent L.A., Coggins M.B., Pierce J.W., Podust V.N., Luo R.S., Chau V., Palombella V.J. Nedd8 modification of cul-1 activates SCF(beta(TrCP))-dependent ubiquitination of IkappaBalpha. Mol. Cell Biol. 2000, 20:2326-2333.
82. Richardson P.G., Sonneveld P., Schuster M.W., Irwin D., Stadtmauer E.A., Facon T., Harousseau J.L., Ben-Yehuda D., Lonial S., Goldschmidt H., Reece D., San-Miguel J.F., Blade J., Boccadoro M., Cavenagh J., Dalton W.S., Boral A.L., Esseltine D.L., Porter J.B., Schenkein D., Anderson K.C. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N. Engl. J. Med. 2005, 352:2487-2498.
83. Salon C., Brambilla E., Brambilla C., Lantuejoul S., Gazzeri S., Eymin B. Altered pattern of Cul-1 protein expression and neddylation in human lung tumours: relationships with CAND1 and cyclin E protein levels. J. Pathol. 2007, 213:303-310.
84. San Miguel J.F., Schlag R., Khuageva N.K., Dimopoulos M.A., Shpilberg O., Kropff M., Spicka I., Petrucci M.T., Palumbo A., Samoilova O.S., Dmoszynska A., Abdulkadyrov K.M., Schots R., Jiang B., Mateos M.V., Anderson K.C., Esseltine D.L., Liu K., Cakana A., van de Velde H., Richardson P.G. Bortezomib plus melphalan and prednisone for initial treatment of multiple myeloma. N. Engl. J. Med. 2008, 359:906-917.
85. Schwechheimer C., Serino G., Callis J., Crosby W.L., Lyapina S., Deshaies R.J., Gray W.M., Estelle M., Deng X.W. Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIRI in mediating auxin response. Science 2001, 292:1379-1382.
86. Scott D.C., Monda J.K., Grace C.R., Duda D.M., Kriwacki R.W., Kurz T., Schulman B.A. A dual E3 mechanism for Rub1 ligation to Cdc53. Mol. Cell 2010, 39:784-796.
87. Shibata T., Ohta T., Tong K.I., Kokubu A., Odogawa R., Tsuta K., Asamura H., Yamamoto M., Hirohashi S. Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:13568-13573.
88. Singer J.D., Gurian-West M., Clurman B., Roberts J.M. Cullin-3 targets cyclin E for ubiquitination and controls S phase in mammalian cells. Genes Dev. 1999, 13:2375-2387.
89. Skaar J.R., D'Angiolella V., Pagan J.K., Pagano M. SnapShot: F Box Proteins II. Cell 2009, 137:1358. 1358.e1.
90. Soucy T.A., Smith P.G., Milhollen M.A., Berger A.J., Gavin J.M., Adhikari S., Brownell J.E., Burke K.E., Cardin D.P., Critchley S., Cullis C.A., Doucette A., Garnsey J.J., Gaulin J.L., Gershman R.E., Lublinsky A.R., McDonald A., Mizutani H., Narayanan U., Olhava E.J., Peluso S., Rezaei M., Sintchak M.D., Talreja T., Thomas M.P., Traore T., Vyskocil S., Weatherhead G.S., Yu J., Zhang J., Dick L.R., Claiborne C.F., Rolfe M., Bolen J.B., Langston S.P. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 2009, 458:732-736.
91. Stebbins C.E., Kaelin W.G., Pavletich N.P. Structure of the VHL-ElonginC-ElonginB complex: implications for VHL tumor suppressor function. Science 1999, 284:455-461.
92. Sugasawa K., Okuda Y., Saijo M., Nishi R., Matsuda N., Chu G., Mori T., Iwai S., Tanaka K., Hanaoka F. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 2005, 121:387-400.
93. Swords R.T., Kelly K.R., Smith P.G., Garnsey J.J., Mahalingam D., Medina E., Oberheu K., Padmanabhan S., O'Dwyer M., Nawrocki S.T., Giles F.J., Carew J.S. Inhibition of NEDD8-activating enzyme: a novel approach for the treatment of acute myeloid leukemia. Blood 2010, 115:3796-3800.
94. Tanaka T., Kawashima H., Yeh E.T., Kamitani T. Regulation of the NEDD8 conjugation system by a splicing variant, NUB1L. J. Biol. Chem. 2003, 278:32905-32913.
95. Tanji K., Tanaka T., Kamitani T. Interaction of NUB1 with the proteasome subunit S5a. Biochem. Biophys. Res. Commun. 2005, 337:116-120.
96. Tomoda K., Kubota Y., Arata Y., Mori S., Maeda M., Tanaka T., Yoshida M., Yoneda-Kato N., Kato J.Y. The cytoplasmic shuttling and subsequent degradation of p27Kip1 mediated by Jab1/CSN5 and the COP9 signalosome complex. J. Biol. Chem. 2002, 277:2302-2310.
97. Tomoda K., Kubota Y., Kato J. Degradation of the cyclin-dependent-kinase inhibitor p27Kip1 is instigated by Jab1. Nature 1999, 398:160-165.
98. Wada H., Yeh E.T., Kamitani T. Identification of NEDD8-conjugation site in human cullin-2. Biochem. Biophys. Res. Commun. 1999, 257:100-105.
99. Wada H., Yeh E.T., Kamitani T. The von Hippel-Lindau tumor suppressor gene product promotes, but is not essential for, NEDD8 conjugation to cullin-2. J. Biol. Chem. 1999, 274:36025-36029.
100. Wada H., Yeh E.T., Kamitani T. A dominant-negative UBC12 mutant sequesters NEDD8 and inhibits NEDD8 conjugation in vivo. J. Biol. Chem. 2000, 275:17008-17015.
101. Walden H., Podgorski M.S., Huang D.T., Miller D.W., Howard R.J., Minor D.L., Holton J.M., Schulman B.A. The structure of the APPBP1-UBA3-NEDD8-ATP complex reveals the basis for selective ubiquitin-like protein activation by an E1. Mol. Cell 2003, 12:1427-1437.
102. Watson I.R., Blanch A., Lin D.C., Ohh M., Irwin M.S. Mdm2-mediated NEDD8 modification of TAp73 regulates its transactivation function. J. Biol. Chem. 2006, 281:34096-34103.
103. Watson I.R., Li B.K., Roche O., Blanch A., Ohh M., Irwin M.S. Chemotherapy induces NEDP1-mediated destabilization of MDM2. Oncogene 2010, 29:297-304.
104. Westbrook T.F., Hu G., Ang X.L., Mulligan P., Pavlova N.N., Liang A., Leng Y., Maehr R., Shi Y., Harper J.W., Elledge S.J. SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 2008, 452:370-374.
105. Whitby F.G., Xia G., Pickart C.M., Hill C.P. Crystal structure of the human ubiquitin-like protein NEDD8 and interactions with ubiquitin pathway enzymes. J. Biol. Chem. 1998, 273:34983-34991.
106. Willam C., Nicholls L.G., Ratcliffe P.J., Pugh C.W., Maxwell P.H. The prolyl hydroxylase enzymes that act as oxygen sensors regulating destruction of hypoxia-inducible factor alpha. Adv. Enzyme Regul. 2004, 44:75-92.
107. Xirodimas D.P., Saville M.K., Bourdon J.C., Hay R.T., Lane D.P. Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell 2004, 118:83-97.
108. Xu X., Sarikas A., Dias-Santagata D.C., Dolios G., Lafontant P.J., Tsai S.C., Zhu W., Nakajima H., Nakajima H.O., Field L.J., Wang R., Pan Z.Q. The CUL7 E3 ubiquitin ligase targets insulin receptor substrate 1 for ubiquitin-dependent degradation. Mol. Cell 2008, 30:403-414.
109. Yang G., Ayala G., De Marzo A., Tian W., Frolov A., Wheeler T.M., Thompson T.C., Harper J.W. Elevated Skp2 protein expression in human prostate cancer: association with loss of the cyclin-dependent kinase inhibitor p27 and PTEN and with reduced recurrence-free survival. Clin. Cancer Res. 2002, 8:3419-3426.
110. Yang X., Zhou J., Sun L., Wei Z., Gao J., Gong W., Xu R.M., Rao Z., Liu Y. Structural basis for the function of DCN-1 in protein neddylation. J. Biol. Chem. 2007, 282:24490-24494.
111. Yeh E.T., Gong L., Kamitani T. Ubiquitin-like proteins: new wines in new bottles. Gene 2000, 248:1-14.
112. Yen H.C., Elledge S.J. Identification of SCF ubiquitin ligase substrates by global protein stability profiling. Science 2008, 322:923-929.
113. Zhong W., Feng H., Santiago F.E., Kipreos E.T. CUL-4 ubiquitin ligase maintains genome stability by restraining DNA-replication licensing. Nature 2003, 423:885-889.