Click chemistry for targeted protein ubiquitylation and ubiquitin chain formation

Nature Protocols

Volumn 10, Issue 10, 2015, Pages 1594-1611

  Rösner, Daniel ^a   Schneider, Tatjana ^a   Schneider, Daniel ^a   Scheffner, Martin ^a   Marx, Andreas ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYNE; AMINO ACID DERIVATIVE; AZIDE; COMPLEMENTARY DNA; COPPER; UBIQUITIN;

ARTICLE; CATALYSIS; CLICK CHEMISTRY; CLINICAL PROTOCOL; CONTROLLED STUDY; CULTURE TECHNIQUE; CYCLOADDITION; GENETIC CODE; IN VITRO STUDY; INTERMETHOD COMPARISON; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; PROTEIN TARGETING; UBIQUITINATION; CHEMICAL ANALYSIS; CHEMISTRY; CYCLIZATION; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROCEDURES;

ALKYNES; AZIDES; CATALYSIS; CHEMISTRY TECHNIQUES, ANALYTICAL; CLICK CHEMISTRY; COPPER; CYCLIZATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; UBIQUITIN; UBIQUITINATION;

EID: 84942543892     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2015.106     Document Type: Article

References (89)

1. Gallagher, S. S., Sable, J. E., Sheetz, M. P. & Cornish, V. W. An in vivo covalent TMP-tag based on proximity-induced reactivity. ACS Chem. Biol. 4, 547-556 (2009).
2. Gautier, A. et al. An engineered protein tag for multiprotein labeling in living cells. Chem. Biol. 15, 128-136 (2008).
3. Liu, D. S. et al. Diels-Alder cycloaddition for fluorophore targeting to specific proteins inside living cells. J. Am. Chem. Soc. 134, 792-795 (2012).
4. Nikic, I. et al. Minimal tags for rapid dual-color live-cell labeling and super-resolution microscopy. Angew. Chem. Int. Ed. 53, 2245-2249 (2014).
5. Los, G. V. et al. HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem. Biol. 3, 373-382 (2008).
6. Coin, I. et al. Genetically encoded chemical probes in cells reveal the binding path of urocortin-I to CRF class B GPCR. Cell 155, 1258-1269 (2013).
7. Haruki, H., Gonzalez, M. R. & Johnsson, K. Exploiting ligand-protein conjugates to monitor ligand-receptor interactions. PLoS ONE 7, e37598 (2012).
8. Arbely, E. et al. Acetylation of lysine 120 of p53 endows DNA-binding specificity at effective physiological salt concentration. Proc. Natl. Acad. Sci. USA 108, 8251-8256 (2011).
9. Lee, S. et al. A facile strategy for selective incorporation of phosphoserine into histones. Angew. Chem. Int. Ed. 52, 5771-5775 (2013).
10. McGinty, R. K., Kim, J., Chatterjee, C., Roeder, R. G. & Muir, T. W. Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature 453, 812-816 (2008).
11. Prescher, J. A. & Bertozzi, C. R. Chemistry in living systems. Nat. Chem. Biol. 1, 13-21 (2005).
12. Hein, C. D., Liu, X. M. & Wang, D. Click chemistry, a powerful tool for pharmaceutical sciences. Pharm. Res. 25, 2216-2230 (2008).
13. Kolb, H. C., Finn, M. G. & Sharpless, K. B. Click chemistry: diverse chemical function from a few good reactions. Angew. Chem. Int. Ed. 40, 2004-2021 (2001).
14. Kolb, H. C. & Sharpless, K. B. The growing impact of click chemistry on drug discovery. Drug Discov. Today 8, 1128-1137 (2003).
15. Moses, J. E. & Moorhouse, A. D. The growing applications of click chemistry. Chem. Soc. Rev. 36, 1249-1262 (2007).
16. Huisgen, R. Kinetics and mechanism of 1,3-dipolar cycloadditions. Angew. Chem. Int. Ed. 2, 633-645 (1963).
17. Rostovtsev, V. V., Green, L. G., Fokin, V. V. & Sharpless, K. B. A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective 'ligation' of azides and terminal alkynes. Angew. Chem. Int. Ed. 41, 2596-2599 (2002).
18. Tornoe, C. W., Christensen, C. & Meldal, M. Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(i)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem. 67, 3057-3064 (2002).
19. Speers, A. E., Adam, G. C. & Cravatt, B. F. Activity-based protein profiling in vivo using a copper(i)-catalyzed azide-alkyne [3 + 2] cycloaddition. J. Am. Chem. Soc. 125, 4686-4687 (2003).
20. Speers, A. E. & Cravatt, B. F. Profiling enzyme activities in vivo using click chemistry methods. Chem. Biol. 11, 535-546 (2004).
21. Godula, K., Rabuka, D., Nam, K. T. & Bertozzi, C. R. Synthesis and microcontact printing of dual end-functionalized mucin-like glycopolymers for microarray applications. Angew. Chem. Int. Ed. 48, 4973-4976 (2009).
22. Ju, J. et al. Four-color DNA sequencing by synthesis using cleavable fluorescent nucleotide reversible terminators. Proc. Natl. Acad. Sci. USA 103, 19635-19640 (2006).
23. Tolstyka, Z. P. et al. Chemoselective immobilization of proteins by microcontact printing and bio-orthogonal click reactions. ChemBioChem 14, 2464-2471 (2013).
24. Jang, H., Fafarman, A., Holub, J. M. & Kirshenbaum, K. Click to fit: versatile polyvalent display on a peptidomimetic scaffold. Org. Lett. 7, 1951-1954 (2005).
25. Liebert, T., Hänsch, C. & Heinze, T. Click chemistry with polysaccharides. Macromol. Rapid Commun. 27, 208-213 (2006).
26. Wang, Q. et al. Bioconjugation by copper(I)-catalyzed azide-alkyne [3 + 2] cycloaddition. J. Am. Chem. Soc. 125, 3192-3193 (2003).
27. Gramlich, P. M., Wirges, C. T., Gierlich, J. & Carell, T. Synthesis of modified DNA by PCR with alkyne-bearing purines followed by a click reaction. Org. Lett. 10, 249-251 (2008).
28. Eger, S. et al. Generation of a mono-ubiquitinated PCNA mimic by click chemistry. ChemBioChem 12, 2807-2812 (2011).
29. Eger, S., Scheffner, M., Marx, A. & Rubini, M. Synthesis of defined ubiquitin dimers. J. Am. Chem. Soc. 132, 16337-16339 (2010).
30. Schneider, D., Schneider, T., Rösner, D., Scheffner, M. & Marx, A. Improving bioorthogonal protein ubiquitylation by click reaction. Bioorg. Med. Chem. 21, 3430-3435 (2013).
31. Schneider, T. et al. Dissecting ubiquitin signaling with linkage-defined and protease resistant ubiquitin chains. Angew. Chem. Int. Ed. 53, 12925-12929 (2014).
32. Spasser, L. & Brik, A. Chemistry and biology of the ubiquitin signal. Angew. Chem. Int. Ed. 51, 6840-6862 (2012).
33. Welchman, R. L., Gordon, C. & Mayer, R. J. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol. 6, 599-609 (2005).
34. Haglund, K. & Dikic, I. Ubiquitylation and cell signaling. EMBO J. 24, 3353-3359 (2005).
35. Hershko, A. & Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 67, 425-479 (1998).
36. Ciechanover, A. & Brundin, P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40, 427-446 (2003).
37. Hoeller, D., Hecker, C. M. & Dikic, I. Ubiquitin and ubiquitin-like proteins in cancer pathogenesis. Nat. Rev. Cancer 6, 776-788 (2006).
38. Glickman, M. H. & Ciechanover, A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82, 373-428 (2002).
39. Scheffner, M., Nuber, U. & Huibregtse, J. M. Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 373, 81-83 (1995).
40. Pham, A. D. & Sauer, F. Ubiquitin-activating/conjugating activity of TAFII250, a mediator of activation of gene expression in Drosophila. Science 289, 2357-2360 (2000).
41. Terrell, J., Shih, S., Dunn, R. & Hicke, L. A function for monoubiquitination in the internalization of a G protein-coupled receptor. Mol. Cell 1, 193-202 (1998).
42. Li, M. et al. Mono-versus polyubiquitination: differential control of p53 fate by Mdm2. Science 302, 1972-1975 (2003).
43. Lohrum, M. A., Woods, D. B., Ludwig, R. L., Balint, E. & Vousden, K. H. C-terminal ubiquitination of p53 contributes to nuclear export. Mol. Cell Biol. 21, 8521-8532 (2001).
44. Bavikar, S. N. et al. Chemical synthesis of ubiquitinated peptides with varying lengths and types of ubiquitin chains to explore the activity of deubiquitinases. Angew. Chem. Int. Ed. 51, 758-763 (2012).
45. Hoege, C., Pfander, B., Moldovan, G. L., Pyrowolakis, G. & Jentsch, S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135-141 (2002).
46. Kannouche, P. L., Wing, J. & Lehmann, A. R. Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14, 491-500 (2004).
47. Ulrich, H. D. & Jentsch, S. Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 19, 3388-3397 (2000).
48. Kirisako, T. et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25, 4877-4887 (2006).
49. Peng, J. et al. A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21, 921-926 (2003).
50. Thrower, J. S., Hoffman, L., Rechsteiner, M. & Pickart, C. M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19, 94-102 (2000).
51. Ikeda, F. et al. SHARPIN forms a linear ubiquitin ligase complex regulating NF-kappaB activity and apoptosis. Nature 471, 637-641 (2011).
52. Iwai, K. Linear polyubiquitin chains: a new modifier involved in NFkappaB activation and chronic inflammation, including dermatitis. Cell Cycle 10, 3095-3104 (2011).
53. Komander, D. & Rape, M. The ubiquitin code. Annu. Rev. Biochem. 81, 203-229 (2012).
54. Pickart, C. M. & Raasi, S. Controlled synthesis of polyubiquitin chains. Methods Enzymol. 399, 21-36 (2005).
55. Rape, M. Assembly of k11-linked ubiquitin chains by the anaphase-promoting complex. Subcell. Biochem. 54, 107-115 (2010).
56. Kim, J. et al. RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 137, 459-471 (2009).
57. Kumar, K. S. et al. Total chemical synthesis of a 304 amino acid K48-linked tetraubiquitin protein. Angew. Chem. Int. Ed. 50, 6137-6141 (2011).
58. Moyal, T., Bavikar, S. N., Karthikeyan, S. V., Hemantha, H. P. & Brik, A. Polymerization behavior of a bifunctional ubiquitin monomer as a function of the nucleophile site and folding conditions. J. Am. Chem. Soc. 134, 16085-16092 (2012).
59. Haj-Yahya, M. et al. Synthetic polyubiquitinated alpha-Synuclein reveals important insights into the roles of the ubiquitin chain in regulating its pathophysiology. Proc. Natl. Acad. Sci. USA 110, 17726-17731 (2013).
60. Hemantha, H. P. et al. Nonenzymatic polyubiquitination of expressed proteins. J. Am. Chem. Soc. 136, 2665-2673 (2014).
61. Chatterjee, C., McGinty, R. K., Fierz, B. & Muir, T. W. Disulfide-directed histone ubiquitylation reveals plasticity in hDot1L activation. Nat. Chem. Biol. 6, 267-269 (2010).
62. Chen, J., Ai, Y., Wang, J., Haracska, L. & Zhuang, Z. Chemically ubiquitylated PCNA as a probe for eukaryotic translesion DNA synthesis. Nat. Chem. Biol. 6, 270-272 (2010).
63. Yang, K., Gong, P., Gokhale, P. & Zhuang, Z. Chemical protein polyubiquitination reveals the role of a noncanonical polyubiquitin chain in DNA damage tolerance. ACS Chem. Biol. 9, 1685-1691 (2014).
64. Shanmugham, A. et al. Nonhydrolyzable ubiquitin-isopeptide isosteres as deubiquitinating enzyme probes. J. Am. Chem. Soc. 132, 8834-8835 (2010).
65. Jung, J. E. et al. Functional ubiquitin conjugates with lysine-epsilon-amino-specific linkage by thioether ligation of cysteinyl-ubiquitin peptide building blocks. Bioconjug. Chem. 20, 1152-1162 (2009).
66. Trang, V. H. et al. Nonenzymatic polymerization of ubiquitin: single-step synthesis and isolation of discrete ubiquitin oligomers. Angew. Chem. Int. Ed. 51, 13085-13088 (2012).
67. Castaneda, C. et al. Nonenzymatic assembly of natural polyubiquitin chains of any linkage composition and isotopic labeling scheme. J. Am. Chem. Soc. 133, 17855-17868 (2011).
68. Dixon, E. K., Castañeda, C. A., Kashyap, T. R., Wang, Y. & Fushman, D. Nonenzymatic assembly of branched polyubiquitin chains for structural and biochemical studies. Bioorg. Med. Chem. 21, 3421-3429 (2013).
69. Singh, R. K., Sundar, A. & Fushman, D. Nonenzymatic rubylation and ubiquitination of proteins for structural and functional studies. Angew. Chem. Int. Ed. 53, 6120-6125 (2014).
70. 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. 6, 750-757 (2010).
71. Sommer, S., Weikart, N. D., Brockmeyer, A., Janning, P. & Mootz, H. D. Expanded click conjugation of recombinant proteins with ubiquitin-like modifiers reveals altered substrate preference of SUMO2-modified Ubc9. Angew. Chem. Int. Ed. 50, 9888-9892 (2011).
72. Weikart, N. D., Sommer, S. & Mootz, H. D. Click synthesis of ubiquitin dimer analogs to interrogate linkage-specific UBA domain binding. Chem. Commun. 48, 296-298 (2012).
73. Brik, A. et al. 1,2,3-Triazole as a peptide surrogate in the rapid synthesis of HIV-1 protease inhibitors. Chembiochem 6, 1167-1169 (2005).
74. Bock, V. D., Perciaccante, R., Jansen, T. P., Hiemstra, H. & van Maarseveen, J. H. Click chemistry as a route to cyclic tetrapeptide analogues: synthesis of cyclo-[Pro-Val-psi(triazole)-Pro-Tyr]. Org. Lett. 8, 919-922 (2006).
75. Horne, W. S., Stout, C. D. & Ghadiri, M. R. A heterocyclic peptide nanotube. J. Am. Chem. Soc. 125, 9372-9376 (2003).
76. Horne, W. S., Yadav, M. K., Stout, C. D. & Ghadiri, M. R. Heterocyclic peptide backbone modifications in an alpha-helical coiled coil. J. Am. Chem. Soc. 126, 15366-15367 (2004).
77. Dresselhaus, T., Weikart, N. D., Mootz, H. D. & Waller, M. P. Naturally and synthetically linked lys48 diubiquitin: a QM/MM study. RCS Adv. 3, 16122-16129 (2013).
78. Bekes, M. et al. DUB-resistant ubiquitin to survey ubiquitination switches in mammalian cells. Cell Rep. 5, 826-838 (2013).
79. Young, T. S., Ahmad, I., Yin, J. A. & Schultz, P. G. An enhanced system for unnatural amino acid mutagenesis in E. coli. J. Mol. Biol. 395, 361-374 (2010).
80. Hong, V., Presolski, S. I., Ma, C. & Finn, M. G. Analysis and optimization of copper-catalyzed azide-alkyne cycloaddition for bioconjugation. Angew. Chem. Int. Ed. 48, 9879-9883 (2009).
81. Nguyen, D. P. et al. 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 (2009).
82. Dower, W. J., Miller, J. F. & Ragsdale, C. W. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 16, 6127-6145 (1988).
83. Johnson, D. B. et al. RF1 knockout allows ribosomal incorporation of unnatural amino acids at multiple sites. Nat. Chem. Biol. 7, 779-786 (2011).
84. Lajoie, M. J. et al. Genomically recoded organisms expand biological functions. Science 342, 357-360 (2013).
85. Pott, M., Schmidt, M. J. & Summerer, D. Evolved sequence contexts for highly efficient amber suppression with noncanonical amino acids. ACS Chem. Biol. 9, 2815-2822 (2014).
86. Lim, S. I., Mizuta, Y., Takasu, A., Kim, Y. H. & Kwon, I. Site-specific bioconjugation of a murine dihydrofolate reductase enzyme by copper(I)-catalyzed azide-alkyne cycloaddition with retained activity. PLoS ONE 9, e98403 (2014).
87. Bundy, B. C. & Swartz, J. R. Site-specific incorporation of p-propargyloxyphenylalanine in a cell-free environment for direct protein-protein click conjugation. Bioconjug. Chem. 21, 255-263 (2010).
88. Schoffelen, S., Lambermon, M. H., van Eldijk, M. B. & van Hest, J. C. Site-specific modification of Candida antarctica lipase B via residue-specific incorporation of a non-canonical amino acid. Bioconjug. Chem. 19, 1127-1131 (2008).
89. Uttamapinant, C. et al. Fast, cell-compatible click chemistry with copper-chelating azides for biomolecular labeling. Angew. Chem. Int. Ed. 51, 5852-5856 (2012).