Orthogonal Thiol Functionalization at a Single Atomic Center for Profiling Transthiolation Activity of E1 Activating Enzymes

ACS Chemical Biology

Volumn 10, Issue 6, 2015, Pages 1542-1554

  Stanley, Mathew ^a   Han, Cong ^a   Knebel, Axel ^a   Murphy, Paul ^a   Shpiro, Natalia ^a   Virdee, Satpal ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE DERIVATIVE; E1 ACTIVATING ENZYME; ENZYME; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; CYSTEINE; DIMETHYLAMINE; ETHYLENE DERIVATIVE; TETRAKIS(DIMETHYLAMINO)ETHYLENE; THIOL DERIVATIVE; UBE1 PROTEIN, HUMAN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ADDITION REACTION; ADENYLATION; ARTICLE; BIOCOMPATIBILITY; CHEMICAL MODIFICATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYCLOADDITION; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; HUMAN; IMMUNOBLOTTING; NUCLEOPHILICITY; OBSERVED RATE CONSTANT; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; TRANSTHIOLATION; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; CYSTEINE; DIMETHYLAMINES; ETHYLENES; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SULFHYDRYL COMPOUNDS; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINS;

EID: 84934990030     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00118     Document Type: Article

References (66)

1. Popovic, D., Vucic, D., and Dikic, I. (2014) Ubiquitination in disease pathogenesis and treatment Nat. Med. 20, 1242-1253
2. Hershko, A. and Ciechanover, A. (1998) The ubiquitin system Annu. Rev. Biochem. 67, 425-479
3. Curran, M. P. and McKeage, K. (2009) Bortezomib: a review of its use in patients with multiple myeloma Drugs 69, 859-888
4. Van der Veen, A. G. and Ploegh, H. L. (2012) Ubiquitin-like proteins Annu. Rev. Biochem. 81, 323-357
5. Brownell, J. E., Sintchak, M. D., Gavin, J. M., Liao, H., Bruzzese, F. J., Bump, N. J., Soucy, T. A., Milhollen, M. A., Yang, X., Burkhardt, A. L., Ma, J., Loke, H.-K., Lingaraj, T., Wu, D., Hamman, K. B., Spelman, J. J., Cullis, C. A., Langston, S. P., Vyskocil, S., Sells, T. B., Mallender, W. D., Visiers, I., Li, P., Claiborne, C. F., Rolfe, M., Bolen, J. B., and Dick, L. R. (2010) Substrate-assisted inhibition of ubiquitin-like protein-activating enzymes: the NEDD8 E1 inhibitor MLN4924 forms a NEDD8-AMP mimetic in situ Mol. Cell 37, 102-111
6. Schulman, B. A. and Harper, J. W. (2009) Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways Nat. Rev. Mol. Cell Biol. 10, 319-331
7. Haas, A. L. and Rose, I. A. (1982) The mechanism of ubiquitin activating enzyme. A kinetic and equilibrium analysis J. Biol. Chem. 257, 10329-10337
8. Haas, A. L., Warms, J. V., Hershko, A., and Rose, I. A. (1982) Ubiquitin-activating enzyme. Mechanism and role in protein-ubiquitin conjugation J. Biol. Chem. 257, 2543-2548
9. Hershko, A., Heller, H., Elias, S., and Ciechanover, A. (1983) Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown J. Biol. Chem. 258, 8206-8214
10. Deshaies, R. J. and Joazeiro, C. A. P. (2009) RING Domain E3 Ubiquitin Ligases Annu. Rev. Biochem. 78, 399-434
11. Kee, Y. and Huibregtse, J. M. (2007) Regulation of catalytic activities of HECT ubiquitin ligases Biochem. Biophys. Res. Commun. 354, 329-333
12. Smit, J. J. and Sixma, T. K. (2014) RBR E3-ligases at work EMBO Rep 15, 142-154
13. Berndsen, C. E. and Wolberger, C. (2014) New insights into ubiquitin E3 ligase mechanism Nat. Struct Mol. Biol. 21, 301-307
14. Ye, Y. and Rape, M. (2009) Building ubiquitin chains: E2 enzymes at work Nat. Rev. Mol. Cell Biol. 10, 755-764
15. Bedford, L., Lowe, J., Dick, L. R., Mayer, R. J., and Brownell, J. E. (2011) Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets Nat. Rev. Drug Discovery 10, 29-46
16. Bossis, G. and Melchior, F. (2006) Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes Mol. Cell 21, 349-357
17. Doris, K. S., Rumsby, E. L., and Morgan, B. A. (2012) Oxidative stress responses involve oxidation of a conserved ubiquitin pathway enzyme Mol. Cell. Biol. 32, 4472-4481
18. Tokgöz, Z., Siepmann, T. J., Streich, F., Kumar, B., Klein, J. M., and Haas, A. L. (2012) E1-E2 interactions in ubiquitin and Nedd8 ligation pathways J. Biol. Chem. 287, 311-321
19. Huang, D. T., Miller, D. W., Mathew, R., Cassell, R., Holton, J. M., Roussel, M. F., and Schulman, B. A. (2004) A unique E1-E2 interaction required for optimal conjugation of the ubiquitin-like protein NEDD8 Nat. Struct Mol. Biol. 11, 927-935
20. Olsen, S. K. and Lima, C. D. (2013) Structure of a ubiquitin e1-e2 complex: insights to e1-e2 thioester transfer Mol. Cell 49, 884-896
21. Wang, J., Taherbhoy, A. M., Hunt, H. W., Seyedin, S. N., Miller, D. W., Miller, D. J., Huang, D. T., and Schulman, B. A. (2010) Crystal structure of UBA2(ufd)-Ubc9: insights into E1-E2 interactions in Sumo pathways PLoS One 5, e15805
22. Chatterjee, C., McGinty, R. K., Fierz, B., and Muir, T. W. (2010) Disulfide-directed histone ubiquitylation reveals plasticity in hDot1L activation Nat. Chem. Biol. 6, 267-269
23. Chen, J., Ai, Y., Wang, J., Haracska, L., and Zhuang, Z. (2010) Chemically ubiquitylated PCNA as a probe for eukaryotic translesion DNA synthesis Nat. Chem. Biol. 6, 270-272
24. Tong, H., Hateboer, G., Perrakis, A., Bernards, R., and Sixma, T. K. (1997) Crystal structure of murine/human Ubc9 provides insight into the variability of the ubiquitin-conjugating system J. Biol. Chem. 272, 21381-21387
25. Chalker, J. M., Bernardes, G. J. L., Lin, Y. A., and Davis, B. G. (2009) Chemical modification of proteins at cysteine: opportunities in chemistry and biology Chem. Asian J. 4, 630-640
26. Spicer, C. D. and Davis, B. G. (2014) Selective chemical protein modification Nat. Commun. 5, 4740
27. Hoogenboom, R. (2010) Thiol-yne chemistry: a powerful tool for creating highly functional materials Angew. Chem., Int. Ed. Engl. 49, 3415-3417
28. Conte, M. L., Staderini, S., Marra, A., Sanchez-Navarro, M., Davis, B. G., and Dondoni, A. (2011) Multi-molecule reaction of serum albumin can occur through thiol-yne coupling Chem. Commun. (Cambridge, U. K.) 47, 11086
29. Li, F., Allahverdi, A., Yang, R., Lua, G. B. J., Zhang, X., Cao, Y., Korolev, N., Nordenskiöld, L., and Liu, C.-F. (2011) A Direct Method for Site-Specific Protein Acetylation Angew. Chem., Int. Ed. 50, 9611-9614
30. Koo, S., Stamenović, M. M., and Prasath, R. A. (2010) Limitations of radical thiol-ene reactions for polymer-polymer conjugation-Koo-2010-Journal of Polymer Science Part A: Polymer Chemistry-Wiley Online Library J. Polym. Sci., Part A: Polym. Chem. 48, 1699-1713
31. Grayson, D. H. and ODonnell, S. H. (2003) Addition of nucleophiles to (E)-3-phenylsulfonylprop-2-enenitrile: a route to β-substituted α, β-unsaturated nitriles and to acetals of cyanoacetaldehyde ARKIVOC 7, 4
32. Strickson, S., Campbell, D. G., Emmerich, C. H., Knebel, A., Plater, L., Ritorto, M. S., Shpiro, N., and Cohen, P. (2013) The anti-inflammatory drug BAY 11-7082 suppresses the MyD88-dependent signalling network by targeting the ubiquitin system Biochem. J. 451, 427-437
33. Shiu, H.-Y., Chan, T.-C., Ho, C.-M., Liu, Y., Wong, M.-K., and Che, C.-M. (2009) Electron-deficient alkynes as cleavable reagents for the modification of cysteine-containing peptides in aqueous medium Chemistry 15, 3839-3850
34. Shiu, H.-Y., Chong, H.-C., Leung, Y.-C., Wong, M.-K., and Che, C.-M. (2010) A highly selective FRET-based fluorescent probe for detection of cysteine and homocysteine Chemistry 16, 3308-3313
35. Truong, V. X. and Dove, A. P. (2013) Organocatalytic, regioselective nucleophilic "click" addition of thiols to propiolic acid esters for polymer-polymer coupling Angew. Chem., Int. Ed. Engl. 52, 4132-4136
36. Kuroda, H., Tomita, I., and Endo, T. (1997) A novel phosphine-catalysed polyaddition of terminal acetylenes bearing electron-withdrawing groups with dithiols. Synthesis of polymers having dithioacetal moieties in the main chain Polymer 38, 6049-6054
37. Komander, D., Clague, M. J., and Urbé, S. (2009) Breaking the chains: structure and function of the deubiquitinases Nat. Rev. Mol. Cell Biol. 10, 550-563
38. Borodovsky, A., Ovaa, H., Kolli, N., Gan-Erdene, T., Wilkinson, K. D., Ploegh, H. L., and Kessler, B. M. (2002) Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family Chem. Biol. 9, 1149-1159
39. Katrun, P. and Chiampanichayakul, S. (2010) PhI(OAc)2/KI-Mediated Reaction of Aryl Sulfinates with Alkenes, Alkynes, and α,β-Unsaturated Carbonyl Compounds: Synthesis of Vinyl Sulfones and β-Iodovinyl Sulfone Eur. J. Org. Chem. 2010, 5633-5641
40. Serafimova, I. M., Pufall, M. A., Krishnan, S., Duda, K., Cohen, M. S., Maglathlin, R. L., McFarland, J. M., Miller, R. M., Frödin, M., and Taunton, J. (2012) Reversible targeting of noncatalytic cysteines with chemically tuned electrophiles Nat. Chem. Biol. 8, 471-476
41. Skaug, B., Jiang, X., and Chen, Z. J. (2009) The role of ubiquitin in NF-kappaB regulatory pathways Annu. Rev. Biochem. 78, 769-796
42. Panier, S. and Durocher, D. (2009) Regulatory ubiquitylation in response to DNA double-strand breaks DNA Repair (Amst.) 8, 436-443
43. Chen, J. J., Tsu, C. A., Gavin, J. M., Milhollen, M. A., Bruzzese, F. J., Mallender, W. D., Sintchak, M. D., Bump, N. J., Yang, X., Ma, J., Loke, H.-K., Xu, Q., Li, P., Bence, N. F., Brownell, J. E., and Dick, L. R. (2011) Mechanistic studies of substrate-assisted inhibition of ubiquitin-activating enzyme by adenosine sulfamate analogues J. Biol. Chem. 286, 40867-40877
44. Pickart, C. M., Kasperek, E. M., Beal, R., and Kim, A. (1994) Substrate properties of site-specific mutant ubiquitin protein (G76A) reveal unexpected mechanistic features of ubiquitin-activating enzyme (E1) J. Biol. Chem. 269, 7115-7123
45. Smith, M. E. B., Schumacher, F. F., Ryan, C. P., Tedaldi, L. M., Papaioannou, D., Waksman, G., Caddick, S., and Baker, J. R. (2010) Protein Modification, Bioconjugation, and Disulfide Bridging Using Bromomaleimides J. Am. Chem. Soc. 132, 1960-1965
46. Gorin, G., Martic, P. A., and Doughty, G. (1966) Kinetics of the reaction of N-ethylmaleimide with cysteine and some congeners Arch. Biochem. Biophys. 115, 593-597
47. Huang, L., Kinnucan, E., Wang, G., Beaudenon, S., Howley, P. M., Huibregtse, J. M., and Pavletich, N. P. (1999) Structure of an E6AP-UbcH7 complex: insights into ubiquitination by the E2-E3 enzyme cascade Science 286, 1321-1326
48. Nuber, U. and Scheffner, M. (1999) Identification of determinants in E2 ubiquitin-conjugating enzymes required for hect E3 ubiquitin-protein ligase interaction J. Biol. Chem. 274, 7576-7582
49. Eletr, Z. M. and Kuhlman, B. (2007) Sequence determinants of E2-E6AP binding affinity and specificity J. Mol. Biol. 369, 419-428
50. Niphakis, M. J. and Cravatt, B. F. (2014) Enzyme inhibitor discovery by activity-based protein profiling Annu. Rev. Biochem. 83, 341-377
51. Yang, Y., Kitagaki, J., Dai, R.-M., Tsai, Y. C., Lorick, K. L., Ludwig, R. L., Pierre, S. A., Jensen, J. P., Davydov, I. V., Oberoi, P., Li, C.-C. H., Kenten, J. H., Beutler, J. A., Vousden, K. H., and Weissman, A. M. (2007) Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics Cancer Res. 67, 9472-9481
52. Stieglitz, B., Morris-Davies, A. C., Koliopoulos, M. G., Christodoulou, E., and Rittinger, K. (2012) LUBAC synthesizes linear ubiquitin chains via a thioester intermediate EMBO Rep 13, 840-846
53. Wauer, T. and Komander, D. (2013) Structure of the human Parkin ligase domain in an autoinhibited state EMBO J. 32, 2099-2112
54. Park, S., Krist, D. T., and Statsyuk, A. V. (2015) Protein ubiquitination and formation of polyubiquitin chains without ATP, E1 and E2 enzymes Chem. Sci. 6, 1770-1779
55. Ekkebus, R., van Kasteren, S. I., Kulathu, Y., Scholten, A., Berlin, I., Geurink, P. P., de Jong, A., Goerdayal, S., Neefjes, J., Heck, A. J. R., Komander, D., and Ovaa, H. (2013) On terminal alkynes that can react with active-site cysteine nucleophiles in proteases J. Am. Chem. Soc. 135, 2867-2870
56. Stieglitz, B., Rana, R. R., Koliopoulos, M. G., Morris-Davies, A. C., Schaeffer, V., Christodoulou, E., Howell, S., Brown, N. R., Dikic, I., and Rittinger, K. (2013) Structural basis for ligase-specific conjugation of linear ubiquitin chains by HOIP Nature 503, 422-426
57. Kamadurai, H. B., Souphron, J., Scott, D. C., Duda, D. M., Miller, D. J., Stringer, D., Piper, R. C., and Schulman, B. A. (2009) Insights into ubiquitin transfer cascades from a structure of a UbcH5B approximately ubiquitin-HECT(NEDD4L) complex Mol. Cell 36, 1095-1102
58. Lin, D. Y.-W., Diao, J., and Chen, J. (2012) Crystal structures of two bacterial HECT-like E3 ligases in complex with a human E2 reveal atomic details of pathogen-host interactions Proc. Natl. Acad. Sci. U. S. A. 109, 1925-1930
59. 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., Rao, M., Yu, P., Dominguez-Vidana, R., Liang, A. C., Solimini, N. L., Bernardi, R. J., Yu, B., Hsu, T., Golding, I., Luo, J., Osborne, C. K., Creighton, C. J., Hilsenbeck, S. G., Schiff, R., Shaw, C. A., Elledge, S. J., and Westbrook, T. F. (2012) A SUMOylation-dependent transcriptional subprogram is required for Myc-driven tumorigenesis Science 335, 348-353
60. Geiger, T., Wehner, A., Schaab, C., Cox, J., and Mann, M. (2012) Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins Mol. Cell Proteomics 11, M111.014050
61. Wiesner, S., Ogunjimi, A. A., Wang, H.-R., Rotin, D., Sicheri, F., Wrana, J. L., and Forman-Kay, J. D. (2007) Autoinhibition of the HECT-type ubiquitin ligase Smurf2 through its C2 domain Cell 130, 651-662
62. Nguyen, D. P., Lusic, H., Neumann, H., Kapadnis, P. B., Deiters, A., and Chin, J. W. (2009) Genetic encoding and labeling of aliphatic azides and alkynes in recombinant proteins via a pyrrolysyl-tRNA Synthetase/tRNA(CUA) pair and click chemistry J. Am. Chem. Soc. 131, 8720-8721
63. Bachovchin, D. A., Brown, S. J., Rosen, H., and Cravatt, B. F. (2009) Identification of selective inhibitors of uncharacterized enzymes by high-throughput screening with fluorescent activity-based probes Nat. Biotechnol. 27, 387-394
64. Heikoop, J. C., van den Boogaart, P., Mulders, J. W., and Grootenhuis, P. D. (1997) Structure-based design and protein engineering of intersubunit disulfide bonds in gonadotropins Nat. Biotechnol. 15, 658-662
65. Xiang, Z., Ren, H., Hu, Y. S., Coin, I., Wei, J., Cang, H., and Wang, L. (2013) Adding an unnatural covalent bond to proteins through proximity-enhanced bioreactivity Nat. Methods 10, 885-888
66. Coin, I., Katritch, V., Sun, T., Xiang, Z., Siu, F. Y., Beyermann, M., Stevens, R. C., and Wang, L. (2013) Genetically encoded chemical probes in cells reveal the binding path of urocortin-I to CRF class B GPCR Cell 155, 1258-1269