Aromatic thiol-mediated cleavage of N-O bonds enables chemical ubiquitylation of folded proteins

Nature Communications

Volumn 7, Issue , 2016, Pages

  Weller, Caroline E ^a   Dhall, Abhinav ^a   Ding, Feizhi ^a   Linares, Edlaine ^b   Whedon, Samuel D ^a   Senger, Nicholas A ^a   Tyson, Elizabeth L ^a   Bagert, John D ^c   Li, Xiaosong ^a   Augusto, Ohara ^b   Chatterjee, Champak ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINOOXYETHANETHIOL; ANION; DISULFIDE; HISTONE H2B; RADICAL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUMO 3 PROTEIN; THIOL; TRACE METAL; UBIQUITIN; UNCLASSIFIED DRUG;

ALCOHOL; ANION; BIOCHEMISTRY; BIOPHYSICS; CHEMICAL BONDING; ORGANIC COMPOUND; PROTEIN;

ARTICLE; CHEMICAL BOND; HUMAN; OXIDATION REDUCTION POTENTIAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; REACTION ANALYSIS; UBIQUITINATION;

EID: 84989271352     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12979     Document Type: Article

References (49)

1. Sharp, P. M., Li, W. H. Molecular evolution of ubiquitin genes. Trends Ecol. Evol. 2, 328-332 (1987).
2. Van der Veen, A. G., Ploegh, H. L. Ubiquitin-like proteins. Annu. Rev. Biochem. 81, 323-357 (2012).
3. Li, W. et al. Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. PLoS ONE 3, e1487 (2008).
4. Komander, D., Rape, M. The ubiquitin code. Annu. Rev. Biochem. 81, 203-229 (2012).
5. Danielsen, J. M. R. et al. Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol. Cell Proteomics 10, M110.003590 (2011).
6. Weller, C. E., Pilkerton, M. E., Chatterjee, C. Chemical strategies to understand the language of ubiquitin signaling. Biopolymers 101, 144-155 (2014).
7. Abeywardana, T., Pratt, M. R. Using chemistry to investigate the molecular consequences of protein ubiquitylation. ChemBioChem 15, 1547-1554 (2014).
8. Chatterjee, C., McGinty, R. K., Pellois, J. P., Muir, T. W. Auxiliary-mediated site-specific peptide ubiquitylation. Angew. Chem. Int. Ed. Engl. 46, 2814-2818 (2007).
9. Wan, Q., Danishefsky, S. J. Free-radical-based, specific desulfurization of cysteine: a powerful advance in the synthesis of polypeptides and glycopolypeptides. Angew. Chem. Int. Ed. Engl. 46, 9248-9252 (2007).
10. Kumar, K. S. A., Harpaz, Z., Haj-Yahya, M., Brik, A. Side-chain assisted ligation in protein synthesis. Bioorg. Med. Chem. Lett. 19, 3870-3874 (2009).
11. Merkx, R. et al. Scalable synthesis of g-thiolysine starting from lysine and a side by side comparison with d-thiolysine in non-enzymatic ubiquitination. Chem. Sci. 4, 4494-4498 (2013).
12. Canne, L. E., Bark, S. J., Kent, S. B. H. Extending the applicability of native chemical ligation. J. Am. Chem. Soc. 118, 5891-5896 (1996).
13. Weller, C. E., Huang, W., Chatterjee, C. Facile synthesis of native and protease-resistant ubiquitylated peptides. ChemBioChem 15, 1263-1267 (2014).
14. Johnson, E. C. B., Kent, S. B. H. Insights into the mechanism and catalysis of the native chemical ligation reaction. J. Am. Chem. Soc. 128, 6640-6646 (2006).
15. Wang, C., Guo, Q. X., Fu, Y. Theoretical analysis of the detailed mechanism of native chemical ligation reactions. Chem. Asian J. 6, 1241-1251 (2011).
16. Jin, W. et al. A unique class of duocarmycin and CC-1065 analogues subject to reductive activation. J. Am. Chem. Soc. 129, 15391-15397 (2007).
17. Fava, A., Reichenbach, G., Peron, U. Kinetics of the thiol-disulfide exchange. II. Oxygen-promoted free-radical exchange between aromatic thiols and disulfides. J. Am. Chem. Soc. 89, 6696-6700 (1967).
18. Forni, L. G., Willson, R. L. Thiyl and phenoxyl free radicals and NADH: direct observation of one-electron oxidation. Biochem. J. 240, 897-903 (1986).
19. Zhao, R., Lind, J., Merenyi, G., Eriksen, T. E. Kinetics of one-electron oxidation of thiols and hydrogen abstraction by thiyl radicals from a-amino C-H bonds. J. Am. Chem. Soc. 116, 12010-12015 (1994).
20. Jeschke, G. EPR techniques for studying radical enzymes. Biochim. Biophys. Acta 1707, 91-102 2005.
21. Augusto, O., Bonini, M. G., Trindade, D. Spin trapping of glutathiyl and protein radicals produced from nitric oxide-derived oxidants. Free Radic. Biol. Med. 36, 1224-1232 (2004).
22. Pou, S., Rosen, G. M. Generation of thiyl radical by nitric oxide: a spin trapping study. J. Chem. Soc., Perkin Trans. 2, 1507-1512 (1998).
23. Duling, D. R. Simulation of multiple isotropic spin-trap EPR spectra. J. Magn. Reson. B 104, 105-110 (1994).
24. Mile, B., Rowlands, C. C., Sillman, P. D., Fildes, M. The EPR spectra of thiyl radical spin adducts produced by photolysis of disulfides in the presence of 2,4,6-tri-tert-butynitrosobenrene and 5,5-dimethyl-1-pyrroline N-oxide. J. Chem. Soc. Perkin Trans. 2, 1431-1437 (1992).
25. Wu, M., Begley, T. P. b-scission of the N-O bond in alkyl hydroxamate radicals: a fast radical trap. Org. Lett. 2, 1345-1348 (2000).
26. Gaspari, G., Granzow, A. The flash photolysis of mercaptans in aqueous solution. J. Phys. Chem. 74, 836-839 (1970).
27. Bitter, F. High-field EPR detection of a disulfide radical anion in the reduction of cytidine 5'-diphosphate by the E441Q R1 mutant of Escherichia coli ribonucleotide reductase. Proc. Natl Acad. Sci. USA 96, 8979-8984 (1999).
28. Tung, T.-L., Stone, J. A. The formation and reactions of disulfide radical anions in aqueous solution. Can. J. Chem. 53, 3153-3157 (1975).
29. Thompson, R. E. et al. Trifluoroethanethiol: an additive for efficient one-pot peptide ligation-desulfurization chemistry. J. Am. Chem. Soc. 136, 8161-8164 (2014).
30. Petlicki, J., van de Ven, T. G. M. The equilibrium between the oxidation of hydrogen peroxide by oxygen and the dismutation of peroxyl or superoxide radicals in aqueous solutions in contact with oxygen. J. Chem. Soc., Faraday Trans. 94, 2763-2767 (1998).
31. Kuppusamy, P., Zweier, J. L. Characterization of free radical generation by xanthine oxidase. J. Biol. Chem. 264, 9880-9884 (1989).
32. Purdie, J. W., Gillis, H. A., Klassen, N. V. Pulse radiolysis of penicillamine in aqueous solution: the thiyl radical and the disulphide radical anion. Chem. Commun. 51, 1163-1165 (1971).
33. Antonello, S., Daasbjerg, K., Jensen, H., Taddei, F., Maran, F. Formation and cleavage of aromatic disulfide radical anions. J. Am. Chem. Soc. 125, 14905-14916 (2003).
34. Goldstein, S., Meyerstein, D., Czapski, G. The Fenton reagents. Free Radic. Biol. Med. 15, 435-445 (1993).
35. Paulsen, C. E., Carroll, K. S. Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem. Rev. 113, 4633-4679 (2013).
36. Gaussian Development Version. Revision H.36 v. 9.0 (Gaussian Inc., 2014).
37. Moyal, T., Hemantha, H. P., Siman, P., Refua, M., Brik, A. Highly efficient one-pot ligation and desulfurization. Chem. Sci. 4, 2496-2501 (2013).
38. Shiio, Y., Eisenman, R. N. Histone sumoylation is associated with transcriptional repression. Proc. Natl Acad. Sci. USA 100, 13225-13230 (2003).
39. Dhall, A. et al. Sumoylated human histone H4 prevents chromatin compaction by inhibiting long-range internucleosomal interactions. J. Biol. Chem. 289, 33827-33837 (2014).
40. Zheng, J. S., Tang, S., Qi, Y. K., Wang, Z. P., Liu, L. Chemical synthesis of proteins using peptide hydrazides as thioester surrogates. Nat. Protoc. 8, 2483-2495 (2013).
41. Lang, K., Chin, J. W. Cellular incorporation of unnatural amino acids and bioorthogonal labeling of proteins. Chem. Rev. 114, 4764-4806 (2014).
42. Hendriks, I. A. et al. Uncovering global SUMOylation signaling networks in a site-specific manner. Nat. Struct. Mol. Biol. 21, 927-936 (2014).
43. Chandrasekharan, M. B., Huang, F., Sun, Z. W. Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc. Natl Acad. Sci. USA 106, 16686-16691 (2009).
44. Mattingly, P. G., Miller, M. J. Titanium trichloride reduction of substituted N-hydroxy-2-azetidinones and other hydroxamic acids. J. Org. Chem. 45, 410-415 (1980).
45. Denmark, S. E., Stolle, A., Dixon, J. A. Tandem inter [4\+2]/Intra [3\+2] cycloadditions. 6. The bridged mode. J. Am. Chem. Soc. 117, 2100-2101 (1995).
46. Keck, G. E., Fleming, S., Nickell, D.,Weider, P. Mild and efficient methods for the reductive cleavage of nitrogen-oxygen bonds. Syn. Commun. 9, 281-286 (1979).
47. Keck, G. E., Wager, T. T., McHardy, S. F. Reductive cleavage of N-o bonds in hydroxylamines and hydroxamic acid derivatives using samarium diiodide. Tet. Lett. 55, 11755-11772 (1999).
48. Cutulic, S., Murphy, J., Farwaha, H., Zhou, S.-Z., Chrystal, E. Metal-Free reductive cleavage of N-O bonds in weinreb amides by an organic neutral super-electron donor. Synlett 2008, 2132-2136 (2008).
49. Watanabe, T., Honda, K. Measurement of the extinction coefficient of the methyl viologen cation radical and the efficiency of its formation by semiconductor photocatalysis. J. Phys. Chem. 86, 2617-2619 (1982).