The Colossus of Ubiquitylation: Decrypting a Cellular Code

Molecular Cell

Volumn 49, Issue 4, 2013, Pages 591-600

  Williamson, Adam ^a   Werner, Achim ^a   Rape, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN; MOLECULAR DYNAMICS; MOLECULAR STABILITY; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEOLYSIS; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATED PROTEINS; UBIQUITINATION;

EID: 84874260416     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.01.028     Document Type: Review

References (110)

1. Ayad N.G., Rankin S., Ooi D., Rape M., Kirschner M.W. Identification of ubiquitin ligase substrates by in vitro expression cloning. Methods Enzymol. 2005, 399:404-414.
2. Behrends C., Sowa M.E., Gygi S.P., Harper J.W. Network organization of the human autophagy system. Nature 2010, 466:68-76.
3. Bekker-Jensen S., Rendtlew Danielsen J., Fugger K., Gromova I., Nerstedt A., Lukas C., Bartek J., Lukas J., Mailand N. HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat. Cell Biol. 2010, 12:80-86. 1-12.
4. Beltrao P., Albanèse V., Kenner L.R., Swaney D.L., Burlingame A., Villén J., Lim W.A., Fraser J.S., Frydman J., Krogan N.J. Systematic functional prioritization of protein posttranslational modifications. Cell 2012, 150:413-425.
5. Bennett E.J., Rush J., Gygi S.P., Harper J.W. Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 2010, 143:951-965.
6. Callow M.G., Tran H., Phu L., Lau T., Lee J., Sandoval W.N., Liu P.S., Bheddah S., Tao J., Lill J.R., et al. Ubiquitin ligase RNF146 regulates tankyrase and Axin to promote Wnt signaling. PLoS ONE 2011, 6:e22595.
7. Cano F., Bye H., Duncan L.M., Buchet-Poyau K., Billaud M., Wills M.R., Lehner P.J. The RNA-binding E3 ubiquitin ligase MEX-3C links ubiquitination with MHC-I mRNA degradation. EMBO J. 2012, 31:3596-3606.
8. Ceccarelli D.F., Tang X., Pelletier B., Orlicky S., Xie W., Plantevin V., Neculai D., Chou Y.C., Ogunjimi A., Al-Hakim A., et al. An allosteric inhibitor of the human Cdc34 ubiquitin-conjugating enzyme. Cell 2011, 145:1075-1087.
9. Chao W.C., Kulkarni K., Zhang Z., Kong E.H., Barford D. Structure of the mitotic checkpoint complex. Nature 2012, 484:208-213.
10. Chau V., Tobias J.W., Bachmair A., Marriott D., Ecker D.J., Gonda D.K., Varshavsky A. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 1989, 243:1576-1583.
11. Christianson J.C., Olzmann J.A., Shaler T.A., Sowa M.E., Bennett E.J., Richter C.M., Tyler R.E., Greenblatt E.J., Harper J.W., Kopito R.R. Defining human ERAD networks through an integrative mapping strategy. Nat. Cell Biol. 2012, 14:93-105.
12. Chuang H.W., Zhang W., Gray W.M. Arabidopsis ETA2, an apparent ortholog of the human cullin-interacting protein CAND1, is required for auxin responses mediated by the SCF(TIR1) ubiquitin ligase. Plant Cell 2004, 16:1883-1897.
13. Deng L., Wang C., Spencer E., Yang L., Braun A., You J., Slaughter C., Pickart C., Chen Z.J. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 2000, 103:351-361.
14. Deshaies R.J., Joazeiro C.A. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 2009, 78:399-434.
15. Doil C., Mailand N., Bekker-Jensen S., Menard P., Larsen D.H., Pepperkok R., Ellenberg J., Panier S., Durocher D., Bartek J., et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009, 136:435-446.
16. Dorrello N.V., Peschiaroli A., Guardavaccaro D., Colburn N.H., Sherman N.E., Pagano M. S6K1- and betaTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science 2006, 314:467-471.
17. Duda D.M., Borg L.A., Scott D.C., Hunt H.W., Hammel M., Schulman B.A. Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 2008, 134:995-1006.
18. Dupont S., Mamidi A., Cordenonsi M., Montagner M., Zacchigna L., Adorno M., Martello G., Stinchfield M.J., Soligo S., Morsut L., et al. FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell 2009, 136:123-135.
19. Eddins M.J., Varadan R., Fushman D., Pickart C.M., Wolberger C. Crystal structure and solution NMR studies of Lys48-linked tetraubiquitin at neutral pH. J. Mol. Biol. 2007, 367:204-211.
20. Emanuele M.J., Elia A.E., Xu Q., Thoma C.R., Izhar L., Leng Y., Guo A., Chen Y.N., Rush J., Hsu P.W., et al. Global identification of modular cullin-RING ligase substrates. Cell 2011, 147:459-474.
21. Fierz B., Chatterjee C., McGinty R.K., Bar-Dagan M., Raleigh D.P., Muir T.W. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat. Chem. Biol. 2011, 7:113-119.
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. Guardavaccaro D., Frescas D., Dorrello N.V., Peschiaroli A., Multani A.S., Cardozo T., Lasorella A., Iavarone A., Chang S., Hernando E., Pagano M. Control of chromosome stability by the beta-TrCP-REST-Mad2 axis. Nature 2008, 452:365-369.
24. Gudjonsson T., Altmeyer M., Savic V., Toledo L., Dinant C., Grøfte M., Bartkova J., Poulsen M., Oka Y., Bekker-Jensen S., et al. TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 2012, 150:697-709.
25. Hamilton K.S., Ellison M.J., Barber K.R., Williams R.S., Huzil J.T., McKenna S., Ptak C., Glover M., Shaw G.S. Structure of a conjugating enzyme-ubiquitin thiolester intermediate reveals a novel role for the ubiquitin tail. Structure 2001, 9:897-904.
26. Hao H.X., Xie Y., Zhang Y., Charlat O., Oster E., Avello M., Lei H., Mickanin C., Liu D., Ruffner H., et al. ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature 2012, 485:195-200.
27. Herzog F., Primorac I., Dube P., Lenart P., Sander B., Mechtler K., Stark H., Peters J.M. Structure of the anaphase-promoting complex/cyclosome interacting with a mitotic checkpoint complex. Science 2009, 323:1477-1481.
28. Hicke L., Riezman H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 1996, 84:277-287.
29. Hjerpe R., Aillet F., Lopitz-Otsoa F., Lang V., England P., Rodriguez M.S. Efficient protection and isolation of ubiquitylated proteins using tandem ubiquitin-binding entities. EMBO Rep. 2009, 10:1250-1258.
30. Hjerpe R., Thomas Y., Kurz T. NEDD8 overexpression results in neddylation of ubiquitin substrates by the ubiquitin pathway. J. Mol. Biol. 2012, 421:27-29.
31. Hou F., Sun L., Zheng H., Skaug B., Jiang Q.X., Chen Z.J. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 2011, 146:448-461.
32. Huang S.M., Mishina Y.M., Liu S., Cheung A., Stegmeier F., Michaud G.A., Charlat O., Wiellette E., Zhang Y., Wiessner S., et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009, 461:614-620.
33. Hubner N.C., Bird A.W., Cox J., Splettstoesser B., Bandilla P., Poser I., Hyman A., Mann M. Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol. 2010, 189:739-754.
34. Husnjak K., Dikic I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 2012, 81:291-322.
35. Hutchins J.R., Toyoda Y., Hegemann B., Poser I., Hériché J.K., Sykora M.M., Augsburg M., Hudecz O., Buschhorn B.A., Bulkescher J., et al. Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 2010, 328:593-599.
36. Jäger S., Kim D.Y., Hultquist J.F., Shindo K., LaRue R.S., Kwon E., Li M., Anderson B.D., Yen L., Stanley D., et al. Vif hijacks CBF-β to degrade APOBEC3G and promote HIV-1 infection. Nature 2012, 481:371-375.
37. Jin L., Williamson A., Banerjee S., Philipp I., Rape M. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 2008, 133:653-665.
38. Jin L., Pahuja K.B., Wickliffe K.E., Gorur A., Baumgärtel C., Schekman R., Rape M. Ubiquitin-dependent regulation of COPII coat size and function. Nature 2012, 482:495-500.
39. Kaelin W.G. The concept of synthetic lethality in the context of anticancer therapy. Nat. Rev. Cancer 2005, 5:689-698.
40. Kanie T., Onoyama I., Matsumoto A., Yamada M., Nakatsumi H., Tateishi Y., Yamamura S., Tsunematsu R., Matsumoto M., Nakayama K.I. Genetic reevaluation of the role of F-box proteins in cyclin D1 degradation. Mol. Cell. Biol. 2012, 32:590-605.
41. Kessler J.D., Kahle K.T., Sun T., Meerbrey K.L., Schlabach M.R., Schmitt E.M., Skinner S.O., Xu Q., Li M.Z., Hartman Z.C., et al. A SUMOylation-dependent transcriptional subprogram is required for Myc-driven tumorigenesis. Science 2012, 335:348-353.
42. Kim J., Guermah M., McGinty R.K., Lee J.S., Tang Z., Milne T.A., Shilatifard A., Muir T.W., Roeder R.G. RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 2009, 137:459-471.
43. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., Sowa M.E., Rad R., Rush J., Comb M.J., et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44:325-340.
44. Kirkpatrick D.S., Hathaway N.A., Hanna J., Elsasser S., Rush J., Finley D., King R.W., Gygi S.P. Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nat. Cell Biol. 2006, 8:700-710.
45. Kleiger G., Saha A., Lewis S., Kuhlman B., Deshaies R.J. Rapid E2-E3 assembly and disassembly enable processive ubiquitylation of cullin-RING ubiquitin ligase substrates. Cell 2009, 139:957-968.
46. Komander D., Rape M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81:203-229.
47. Koo B.K., Spit M., Jordens I., Low T.Y., Stange D.E., van de Wetering M., van Es J.H., Mohammed S., Heck A.J., Maurice M.M., Clevers H. Tumour suppressor RNF43 is a stem-cell E3 ligase that induces endocytosis of Wnt receptors. Nature 2012, 488:665-669.
48. Lai M.Y., Zhang D., Laronde-Leblanc N., Fushman D. Structural and biochemical studies of the open state of Lys48-linked diubiquitin. Biochim. Biophys. Acta 2012, 1823:2046-2056.
49. Lamesch P., Li N., Milstein S., Fan C., Hao T., Szabo G., Hu Z., Venkatesan K., Bethel G., Martin P., et al. hORFeome v3.1: a resource of human open reading frames representing over 10,000 human genes. Genomics 2007, 89:307-315.
50. Lander G.C., Estrin E., Matyskiela M.E., Bashore C., Nogales E., Martin A. Complete subunit architecture of the proteasome regulatory particle. Nature 2012, 482:186-191.
51. Lee P.C., Sowa M.E., Gygi S.P., Harper J.W. Alternative ubiquitin activation/conjugation cascades interact with N-end rule ubiquitin ligases to control degradation of RGS proteins. Mol. Cell 2011, 43:392-405.
52. Lipkowitz S., Weissman A.M. RINGs of good and evil: RING finger ubiquitin ligases at the crossroads of tumour suppression and oncogenesis. Nat. Rev. Cancer 2011, 11:629-643.
53. Luo J., Emanuele M.J., Li D., Creighton C.J., Schlabach M.R., Westbrook T.F., Wong K.K., Elledge S.J. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 2009, 137:835-848.
54. Matsumoto M.L., Wickliffe K.E., Dong K.C., Yu C., Bosanac I., Bustos D., Phu L., Kirkpatrick D.S., Hymowitz S.G., Rape M., et al. K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol. Cell 2010, 39:477-484.
55. Matsumoto M.L., Dong K.C., Yu C., Phu L., Gao X., Hannoush R.N., Hymowitz S.G., Kirkpatrick D.S., Dixit V.M., Kelley R.F. Engineering and structural characterization of a linear polyubiquitin-specific antibody. J. Mol. Biol. 2012, 418:134-144.
56. McGarry T.J., Kirschner M.W. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 1998, 93:1043-1053.
57. McGinty R.K., Kim J., Chatterjee C., Roeder R.G., Muir T.W. Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature 2008, 453:812-816.
58. Merbl Y., Kirschner M.W. Large-scale detection of ubiquitination substrates using cell extracts and protein microarrays. Proc. Natl. Acad. Sci. USA 2009, 106:2543-2548.
59. Mercer J., Snijder B., Sacher R., Burkard C., Bleck C.K., Stahlberg H., Pelkmans L., Helenius A. RNAi screening reveals proteasome- and Cullin3-dependent stages in vaccinia virus infection. Cell Rep 2012, 2:1036-1047.
60. Nakada S., Tai I., Panier S., Al-Hakim A., Iemura S., Juang Y.C., O'Donnell L., Kumakubo A., Munro M., Sicheri F., et al. Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 2010, 466:941-946.
61. Newton K., Matsumoto M.L., Wertz I.E., Kirkpatrick D.S., Lill J.R., Tan J., Dugger D., Gordon N., Sidhu S.S., Fellouse F.A., et al. Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 2008, 134:668-678.
62. Nijman S.M., Huang T.T., Dirac A.M., Brummelkamp T.R., Kerkhoven R.M., D'Andrea A.D., Bernards R. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol. Cell 2005, 17:331-339.
63. Olsen S.K., Capili A.D., Lu X., Tan D.S., Lima C.D. Active site remodelling accompanies thioester bond formation in the SUMO E1. Nature 2010, 463:906-912.
64. Orlicky S., Tang X., Neduva V., Elowe N., Brown E.D., Sicheri F., Tyers M. An allosteric inhibitor of substrate recognition by the SCF(Cdc4) ubiquitin ligase. Nat. Biotechnol. 2010, 28:733-737.
65. Orvedahl A., Sumpter R., Xiao G., Ng A., Zou Z., Tang Y., Narimatsu M., Gilpin C., Sun Q., Roth M., et al. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 2011, 480:113-117.
66. Peng J., Schwartz D., Elias J.E., Thoreen C.C., Cheng D., Marsischky G., Roelofs J., Finley D., Gygi S.P. A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 2003, 21:921-926.
67. Persaud A., Alberts P., Amsen E.M., Xiong X., Wasmuth J., Saadon Z., Fladd C., Parkinson J., Rotin D. Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrays. Mol. Syst. Biol. 2009, 5:333.
68. Peters J.M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 2006, 7:644-656.
69. Petroski M.D., Deshaies R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2005, 6:9-20.
70. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70:503-533.
71. Pierce N.W., Kleiger G., Shan S.O., Deshaies R.J. Detection of sequential polyubiquitylation on a millisecond timescale. Nature 2009, 462:615-619.
72. Plechanovová A., Jaffray E.G., Tatham M.H., Naismith J.H., Hay R.T. Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis. Nature 2012, 489:115-120.
73. Pruneda J.N., Littlefield P.J., Soss S.E., Nordquist K.A., Chazin W.J., Brzovic P.S., Klevit R.E. Structure of an E3:E2~Ub complex reveals an allosteric mechanism shared among RING/U-box ligases. Mol. Cell 2012, 47:933-942.
74. Rodrigo-Brenni M.C., Morgan D.O. Sequential E2s drive polyubiquitin chain assembly on APC targets. Cell 2007, 130:127-139.
75. Rotin D., Kumar S. Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2009, 10:398-409.
76. Saha A., Deshaies R.J. Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation. Mol. Cell 2008, 32:21-31.
77. Saha A., Lewis S., Kleiger G., Kuhlman B., Deshaies R.J. Essential role for ubiquitin-ubiquitin-conjugating enzyme interaction in ubiquitin discharge from Cdc34 to substrate. Mol. Cell 2011, 42:75-83.
78. Sato Y., Yoshikawa A., Yamagata A., Mimura H., Yamashita M., Ookata K., Nureki O., Iwai K., Komada M., Fukai S. Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains. Nature 2008, 455:358-362.
79. Schreiber A., Stengel F., Zhang Z., Enchev R.I., Kong E.H., Morris E.P., Robinson C.V., da Fonseca P.C., Barford D. Structural basis for the subunit assembly of the anaphase-promoting complex. Nature 2011, 470:227-232.
80. Schulman B.A., Harper J.W. Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat. Rev. Mol. Cell Biol. 2009, 10:319-331.
81. Sims J.J., Scavone F., Cooper E.M., Kane L.A., Youle R.J., Boeke J.D., Cohen R.E. Polyubiquitin-sensor proteins reveal localization and linkage-type dependence of cellular ubiquitin signaling. Nat. Methods 2012, 9:303-309.
82. Sloper-Mould K.E., Jemc J.C., Pickart C.M., Hicke L. Distinct functional surface regions on ubiquitin. J. Biol. Chem. 2001, 276:30483-30489.
83. Song L., Rape M. Regulated degradation of spindle assembly factors by the anaphase-promoting complex. Mol. Cell 2010, 38:369-382.
84. Song E.J., Werner S.L., Neubauer J., Stegmeier F., Aspden J., Rio D., Harper J.W., Elledge S.J., Kirschner M.W., Rape M. The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev. 2010, 24:1434-1447.
85. Sowa M.E., Bennett E.J., Gygi S.P., Harper J.W. Defining the human deubiquitinating enzyme interaction landscape. Cell 2009, 138:389-403.
86. Spence J., Gali R.R., Dittmar G., Sherman F., Karin M., Finley D. Cell cycle-regulated modification of the ribosome by a variant multiubiquitin chain. Cell 2000, 102:67-76.
87. Stegmeier F., Rape M., Draviam V.M., Nalepa G., Sowa M.E., Ang X.L., McDonald E.R., Li M.Z., Hannon G.J., Sorger P.K., et al. Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature 2007, 446:876-881.
88. Stewart G.S., Panier S., Townsend K., Al-Hakim A.K., Kolas N.K., Miller E.S., Nakada S., Ylanko J., Olivarius S., Mendez M., et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009, 136:420-434.
89. Tagwerker C., Flick K., Cui M., Guerrero C., Dou Y., Auer B., Baldi P., Huang L., Kaiser P. A tandem affinity tag for two-step purification under fully denaturing conditions: application in ubiquitin profiling and protein complex identification combined with in vivocross-linking. Mol. Cell. Proteomics 2006, 5:737-748.
90. Tan X., Calderon-Villalobos L.I., Sharon M., Zheng C., Robinson C.V., Estelle M., Zheng N. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 2007, 446:640-645.
91. Tokunaga F., Sakata S., Saeki Y., Satomi Y., Kirisako T., Kamei K., Nakagawa T., Kato M., Murata S., Yamaoka S., et al. Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 2009, 11:123-132.
92. Uzunova K., Dye B.T., Schutz H., Ladurner R., Petzold G., Toyoda Y., Jarvis M.A., Brown N.G., Poser I., Novatchkova M., et al. APC15 mediates CDC20 autoubiquitylation by APC/C(MCC) and disassembly of the mitotic checkpoint complex. Nat. Struct. Mol. Biol. 2012, 19:1116-1123.
93. van Wijk S.J., Fiskin E., Putyrski M., Pampaloni F., Hou J., Wild P., Kensche T., Grecco H.E., Bastiaens P., Dikic I. Fluorescence-based sensors to monitor localization and functions of linear and K63-linked ubiquitin chains in cells. Mol. Cell 2012, 47:797-809.
94. Varadan R., Assfalg M., Haririnia A., Raasi S., Pickart C., Fushman D. Solution conformation of Lys63-linked di-ubiquitin chain provides clues to functional diversity of polyubiquitin signaling. J. Biol. Chem. 2004, 279:7055-7063.
95. Virdee S., Ye Y., Nguyen D.P., Komander D., Chin J.W. Engineered diubiquitin synthesis reveals Lys29-isopeptide specificity of an OTU deubiquitinase. Nat. Chem. Biol. 2010, 6:750-757.
96. Wagner S.A., Beli P., Weinert B.T., Nielsen M.L., Cox J., Mann M., Choudhary C. A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell. Proteomics 2011, 10. M111, 013284.
97. Wenzel D.M., Lissounov A., Brzovic P.S., Klevit R.E. UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature 2011, 474:105-108.
98. Wickliffe K.E., Lorenz S., Wemmer D.E., Kuriyan J., Rape M. The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell 2011, 144:769-781.
99. Williamson A., Wickliffe K.E., Mellone B.G., Song L., Karpen G.H., Rape M. Identification of a physiological E2 module for the human anaphase-promoting complex. Proc. Natl. Acad. Sci. USA 2009, 106:18213-18218.
100. Williamson A., Banerjee S., Zhu X., Philipp I., Iavarone A.T., Rape M. Regulation of ubiquitin chain initiation to control the timing of substrate degradation. Mol. Cell 2011, 42:744-757.
101. Xu M., Skaug B., Zeng W., Chen Z.J. A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta. Mol. Cell 2009, 36:302-314.
102. Xu P., Duong D.M., Seyfried N.T., Cheng D., Xie Y., Robert J., Rush J., Hochstrasser M., Finley D., Peng J. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009, 137:133-145.
103. Xu G., Paige J.S., Jaffrey S.R. Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat. Biotechnol. 2010, 28:868-873.
104. Ye Y., Rape M. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 2009, 10:755-764.
105. Ye Y., Blaser G., Horrocks M.H., Ruedas-Rama M.J., Ibrahim S., Zhukov A.A., Orte A., Klenerman D., Jackson S.E., Komander D. Ubiquitin chain conformation regulates recognition and activity of interacting proteins. Nature 2012, 492:266-270.
106. Yen H.C., Elledge S.J. Identification of SCF ubiquitin ligase substrates by global protein stability profiling. Science 2008, 322:923-929.
107. Yen H.C., Xu Q., Chou D.M., Zhao Z., Elledge S.J. Global protein stability profiling in mammalian cells. Science 2008, 322:918-923.
108. Zeng X., Sigoillot F., Gaur S., Choi S., Pfaff K.L., Oh D.C., Hathaway N., Dimova N., Cuny G.D., King R.W. Pharmacologic inhibition of the anaphase-promoting complex induces a spindle checkpoint-dependent mitotic arrest in the absence of spindle damage. Cancer Cell 2010, 18:382-395.
109. Zhang Y., Liu S., Mickanin C., Feng Y., Charlat O., Michaud G.A., Schirle M., Shi X., Hild M., Bauer A., et al. RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat. Cell Biol. 2011, 13:623-629.
110. Zou H., McGarry T.J., Bernal T., Kirschner M.W. Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science 1999, 285:418-422.