Engineered diubiquitin synthesis reveals Lys29-isopeptide specificity of an OTU deubiquitinase

Nature Chemical Biology

Volumn 6, Issue 10, 2010, Pages 750-757

  Virdee, Satpal ^a   Ye, Yu ^a   Nguyen, Duy P ^a   Komander, David ^a   Chin, Jason W ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTEIN; ISOENZYME; LYSINE; UBIQUITIN; PEPTIDE; PROTEINASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ENZYME ENGINEERING; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SYNTHESIS; PRIORITY JOURNAL; UBIQUITINATION; CHEMISTRY; ENZYMOLOGY; FEMALE; GENETICS; HUMAN; METABOLISM; OVARY TUMOR; PROTEIN ENGINEERING; SYNTHESIS;

EUKARYOTA;

ENDOPEPTIDASES; FEMALE; HUMANS; LYSINE; OVARIAN NEOPLASMS; PEPTIDES; PROTEIN ENGINEERING; SUBSTRATE SPECIFICITY; UBIQUITINS;

EID: 77956903406     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.426     Document Type: Article

References (45)

1. Chen, Z.J. & Sun, L.J. Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 33, 275-286 (2009).
2. Komander, D. The emerging complexity of protein ubiquitination. Biochem. Soc. Trans. 37, 937-953 (2009).
3. Ikeda, F. & Dikic, I. Atypical ubiquitin chains: new molecular signals-Protein modifications: beyond the usual suspects review series. EMBO Rep. 9, 536-542 (2008).
4. Peng, J., et al. A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21, 921-926 (2003).
5. Xu, P., et al. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137, 133-145 (2009).
6. Hershko, A. & Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 67, 425-479 (1998).
7. Komander, D., et al. Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 10, 466-473 (2009).
8. Dikic, I., Wakatsuki, S. & Walters, K.J. Ubiquitin-binding domains-from structures to functions. Nat. Rev. Mol. Cell Biol. 10, 659-671 (2009).
9. Wang, H., et al. Analysis of nondegradative protein ubiquitylation with a monoclonal antibody specific for lysine-63-linked polyubiquitin. Proc. Natl. Acad. Sci. USA 105, 20197-20202 (2008).
10. Newton, K., et al. Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134, 668-678 (2008).
11. Bremm, A., Freund, S.M.V. & Komander, D. Lys11-linked ubiquitin chains adopt compact conformations and are preferentially hydrolysed by the deubiquitinase Cezanne. Nat. Struct. Mol. Biol. 17, 939-947 (2010).
12. Chatterjee, C., McGinty, R.K., Pellois, J.-P. & Muir, T.W. Auxiliary-mediated site-specific peptide ubiquitylation. Angew. Chem. Int. Edn Engl. 46, 2814-2818 (2007).
13. McGinty, R.K., Kim, J., Chatterjee, C., Roeder, R. & Muir, T. Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature 453, 812-816 (2008).
14. Yang, R., Pasunooti, K., Li, F., Liu, X. & Liu, C. Dual native chemical ligation at lysine. J. Am. Chem. Soc. 131, 13592-13593 (2009).
15. Ajish Kumar, K.S., Haj-Yahya, M., Olschewski, D., Lashuel, H.A. & Brik, A. Highly efficient and chemoselective peptide ubiquitylation. Angew. Chem. Int. Edn Engl. 48, 8090-8094 (2009).
16. Li, X., Fekner, T., Ottesen, J.J. & Chan, M.K. A pyrrolysine analogue for site-specific protein ubiquitination. Angew. Chem. Int. Edn Engl. 48, 9184-9187 (2009).
17. Hodgins, R.R., Ellison, K.S. & Ellison, M.J. Expression of a ubiquitin derivative that conjugates to protein irreversibly produces phenotypes consistent with a ubiquitin deficiency. J. Biol. Chem. 267, 8807-8812 (1992).
18. Tran, H., Hamada, F., Schwarz-Romond, T. & Bienz, M. Trabid, a new positive regulator of Wnt-induced transcription with preference for binding and cleaving K63-linked ubiquitin chains. Genes Dev. 22, 528-542 (2008).
19. Srinivasan, G., James, C.M. & Krzycki, J.A. Pyrrolysine encoded by UAG in Archaea: charging of a UAG-decoding specialized tRNA. Science 296, 1459-1462 (2002).
20. Ambrogelly, A., et al. Pyrrolysine is not hardwired for cotranslational insertion at UAG codons. Proc. Natl. Acad. Sci. USA 104, 3141-3146 (2007).
21. Neumann, H., Peak-Chew, S.Y. & Chin, J.W. Genetically encoding N(epsilon)-acetyllysine in recombinant proteins. Nat. Chem. Biol. 4, 232-234 (2008).
22. Polycarpo, C.R., et al. Pyrrolysine analogues as substrates for pyrrolysyl-tRNA synthetase. FEBS Lett. 580, 6695-6700 (2006).
23. Kawakami, T., et al. Polypeptide synthesis using an expressed peptide as a building block for condensation with a peptide thioester: application to the synthesis of phosphorylated p21Max protein(1-101). J. Pept. Sci. 7, 474-487 (2001).
24. Aimoto, S. Polypeptide synthesis by the thioester method. Biopolymers 51, 247-265 (1999).
25. Tan, Z., Shang, S., Halkina, T., Yuan, Y. & Danishefsky, S.J. Toward homogeneous erythropoietin: non-NCL-based chemical synthesis of the Gln(78)-Arg(166) glycopeptide domain. J. Am. Chem. Soc. 131, 5424-5431 (2009).
26. Tam, J.P., Heath, W.F. & Merrifield, R.B. Mechanisms for the removal of benzyl protecting groups in synthetic peptides by trifluoromethanesulfonic acid trifluoroacetic-acid dimethyl sulfide. J. Am. Chem. Soc. 8, 5242-5251 (1986).
27. Pickart, C.M. & Raasi, S. Controlled synthesis of polyubiquitin Chains. Methods Enzymol. 399, 21-36 (2005).
28. Komander, D., Clague, M.J. & Urbe, S. Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550-563 (2009).
29. Fushman, D. & Walker, O. Exploring linkage dependence of polyubiquitin conformations using molecular modeling. J. Mol. Biol. 395, 803-814 (2010).
30. Wang, T., et al. Evidence for bidentate substrate binding as the basis for the K48 linkage specificity of otubain 1. J. Mol. Biol. 386, 1011-1023 (2009).
31. Cooper, E.M., et al. K63-specific deubiquitination by two JAMM/MPN+ complexes: BRISC-associated Brcc36 and proteasomal Poh1. EMBO J. 28, 621-631 (2009).
32. Popp, M.W., Artavanis-Tsakonas, K. & Ploegh, H.L. Substrate filtering by the active site crossover loop in UCHL3 revealed by sortagging and gain-of-function mutations. J. Biol. Chem. 284, 3593-3602 (2009).
33. Reyes-Turcu, F.E., et al. The ubiquitin binding domain ZnF UBP recognizes the C-terminal diglycine motif of unanchored ubiquitin. Cell 124, 1197-1208 (2006).
34. Komander, D., et al. The structure of the CYLD USP domain explains its specificity for Lys63-linked polyubiquitin and reveals a B box module. Mol. Cell 29, 451-464 (2008).
35. McCullough, J., Clague, M.J. & Urbe, S. AMSH is an endosome-associated ubiquitin isopeptidase. J. Cell Biol. 166, 487-492 (2004).
36. Sato, Y., et al. Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains. Nature 455, 358-362 (2008).
37. Winborn, B.J., et al. The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J. Biol. Chem. 283, 26436-26443 (2008).
38. Komander, D., et al. Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 10, 466-473 (2009).
39. Wang, T., et al. Evidence for bidentate substrate binding as the basis for the K48 linkage specificity of otubain 1. J. Mol. Biol. 386, 1011-1023 (2009).
40. Cooper, E.M., Boeke, J.D. & Cohen, R.E. Specificity of the BRISC deubiquitinating enzyme is not due to selective binding to Lys63-linked polyubiquitin. J. Biol. Chem. 285, 10344-10352 (2010).
41. Cook, W.J., Jeffrey, L.C., Carson, M., Chen, Z. & Pickart, C.M. Structure of a diubiquitin conjugate and a model for interaction with ubiquitin conjugating enzyme (E2). J. Biol. Chem. 267, 16467-16471 (1992).
42. 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. 367, 204-211 (2007).
43. Wu-Baer, F., Lagrazon, K., Yuan, W. & Baer, R. The BRCA1/BARD1 heterodimer assembles polyubiquitin chains through an unconventional linkage involving lysine residue K6 of ubiquitin. J. Biol. Chem. 278, 34743-34746 (2003).
44. Nishikawa, H., et al. BRCA1-associated protein 1 interferes with BRCA1/BARD1 RING heterodimer activity. Cancer Res. 69, 111-119 (2009).
45. Hermanson, G.T. Bioconjugate Techniques 2nd ed. (Academic Press, 2008).