Assembly and specific recognition of K29- and K33-linked polyubiquitin

Molecular Cell

Volumn 58, Issue 1, 2015, Pages 95-109

  Michel, Martin A ^a   Elliott, Paul R ^a   Swatek, Kirby N ^a   Simicek, Michal ^a   Pruneda, Jonathan N ^a   Wagstaff, Jane L ^a   Freund, Stefan M V ^a   Komander, David ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DEUBIQUITINASE; HECT E3 LIGASE; K29 LINKED POLYUBIQUITIN; K33 LINKED POLYUBIQUITIN; LIGASE; N TERMINAL NPL4 LIKE ZINC FINGER PROTEIN; POLYUBIQUITIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; HYBRID PROTEIN; LYSINE; PROTEASOME; PROTEIN BINDING; PROTEINASE; TRABID PROTEIN, HUMAN; UBE3C PROTEIN, HUMAN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; CHEMICAL ANALYSIS; CONFORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN LOCALIZATION; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; UBIQUITINATION; X RAY CRYSTALLOGRAPHY; AMINO TERMINAL SEQUENCE; BIOCHEMICAL ANALYSIS; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CRYSTALLIZATION; HUMAN CELL; ION EXCHANGE CHROMATOGRAPHY; LIMIT OF QUANTITATION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SURFACE PLASMON RESONANCE;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; ENDOPEPTIDASES; ESCHERICHIA COLI; HEK293 CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LYSINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84949989892     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.01.042     Document Type: Article

References (56)

1. Al-Hakim A.K., Zagorska A., Chapman L., Deak M., Peggie M., Alessi D.R. Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains. Biochem. J. 2008, 411:249-260.
2. Alam S.L., Sun J., Payne M., Welch B.D., Blake B.K., Davis D.R., Meyer H.H., Emr S.D., Sundquist W.I. Ubiquitin interactions of NZF zinc fingers. EMBO J. 2004, 23:1411-1421.
3. Berndsen C.E., Wolberger C. New insights into ubiquitin E3 ligase mechanism. Nat. Struct. Mol. Biol. 2014, 21:301-307.
4. Bremm A., Komander D. Emerging roles for Lys11-linked polyubiquitin in cellular regulation. Trends Biochem. Sci. 2011, 36:355-363.
5. Bremm A., Freund S.M.V., Komander D. Lys11-linked ubiquitin chains adopt compact conformations and are preferentially hydrolyzed by the deubiquitinase Cezanne. Nat. Struct. Mol. Biol. 2010, 17:939-947.
6. Christianson J.C., Ye Y. Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat. Struct. Mol. Biol. 2014, 21:325-335.
7. Clague M.J., Barsukov I., Coulson J.M., Liu H., Rigden D.J., Urbé S. Deubiquitylases from genes to organism. Physiol. Rev. 2013, 93:1289-1315.
8. Deshaies R.J., Joazeiro C.A.P. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 2009, 78:399-434.
9. 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. 2013, 21:3421-3429.
10. Favier A., Brutscher B. Recovering lost magnetization: polarization enhancement in biomolecular NMR. J.Biomol. NMR 2011, 49:9-15.
11. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
12. 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.
13. Hospenthal M.K., Freund S.M.V., Komander D. Assembly, analysis and architecture of atypical ubiquitin chains. Nat. Struct. Mol. Biol. 2013, 20:555-565.
14. Huang H., Jeon M.-S., Liao L., Yang C., Elly C., Yates J.R., Liu Y.-C. K33-linked polyubiquitination of Tcell receptor-zeta regulates proteolysis-independent Tcell signaling. Immunity 2010, 33:60-70.
15. Husnjak K., Dikic I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 2012, 81:291-322.
16. Iwai K., Fujita H., Sasaki Y. Linear ubiquitin chains: NF-κB signalling, cell death and beyond. Nat. Rev. Mol. Cell Biol. 2014, 15:503-508.
17. Kamadurai H.B., Souphron J., Scott D.C., Duda D.M., Miller D.J., Stringer D., Piper R.C., Schulman B.A. Insights into ubiquitin transfer cascades from a structure of a UbcH5B approximately ubiquitin-HECT(NEDD4L) complex. Mol. Cell 2009, 36:1095-1102.
18. Kamadurai H.B., Qiu Y., Deng A., Harrison J.S., Macdonald C., Actis M., Rodrigues P., Miller D.J., Souphron J., Lewis S.M., et al. Mechanism of ubiquitin ligation and lysine prioritization by a HECT E3. eLife 2013, 2. e00828-e00828.
19. Keusekotten K., Elliott P.R., Glockner L., Fiil B.K., Damgaard R.B., Kulathu Y., Wauer T., Hospenthal M.K., Gyrd-Hansen M., Krappmann D., et al. OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 2013, 153:1312-1326.
20. Kim H.C., Huibregtse J.M. Polyubiquitination by HECT E3s and the determinants of chain type specificity. Mol. Cell. Biol. 2009, 29:3307-3318.
21. 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.
22. Kim J.B., Kim S.Y., Kim B.M., Lee H., Kim I., Yun J., Jo Y., Oh T., Jo Y., Chae H.D., Shin D.Y. Identification of a novel anti-apoptotic E3 ubiquitin ligase that ubiquitinates antagonists of inhibitor of apoptosis proteins SMAC, HtrA2, and ARTS. J.Biol. Chem. 2013, 288:12014-12021.
23. Kirkpatrick D.S., Hathaway N.A., Hanna J., Elsasser S., Rush J., Finley D., King R.W., Gygi S.P. Quantitative analysis of invitro ubiquitinated cyclin B1 reveals complex chain topology. Nat. Cell Biol. 2006, 8:700-710.
24. Komander D., Rape M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81:203-229.
25. Komander D., Clague M.J., Urbé S. Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 2009, 10:550-563.
26. Kulathu Y., Komander D. Atypical ubiquitylation - the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 2012, 13:508-523.
27. Kulathu Y., Akutsu M., Bremm A., Hofmann K., Komander D. Two-sided ubiquitin binding explains specificity of the TAB2 NZF domain. Nat. Struct. Mol. Biol. 2009, 16:1328-1330.
28. Licchesi J.D.F., Mieszczanek J., Mevissen T.E.T., Rutherford T.J., Akutsu M., Virdee S., El Oualid F., Chin J.W., Ovaa H., Bienz M., Komander D. An ankyrin-repeat ubiquitin-binding domain determines TRABID's specificity for atypical ubiquitin chains. Nat. Struct. Mol. Biol. 2012, 19:62-71.
29. Maspero E., Valentini E., Mari S., Cecatiello V., Soffientini P., Pasqualato S., Polo S. Structure of a ubiquitin-loaded HECT ligase reveals the molecular basis for catalytic priming. Nat. Struct. Mol. Biol. 2013, 20:696-701.
30. Mattiroli F., Sixma T.K. Lysine-targeting specificity in ubiquitin and ubiquitin-like modification pathways. Nat. Struct. Mol. Biol. 2014, 21:308-316.
31. Mevissen T.E.T., Hospenthal M.K., Geurink P.P., Elliott P.R., Akutsu M., Arnaudo N., Ekkebus R., Kulathu Y., Wauer T., El Oualid F., et al. OTU deubiquitinases reveal mechanisms of linkage specificity and enable ubiquitin chain restriction analysis. Cell 2013, 154:169-184.
32. Ritorto M.S., Ewan R., Perez-Oliva A.B., Knebel A., Buhrlage S.J., Wightman M., Kelly S.M., Wood N.T., Virdee S., Gray N.S., et al. Screening of DUB activity and specificity by MALDI-TOF mass spectrometry. Nat. Commun. 2014, 5:4763.
33. Rivkin E., Almeida S.M., Ceccarelli D.F., Juang Y.-C., MacLean T.A., Srikumar T., Huang H., Dunham W.H., Fukumura R., Xie G., et al. The linear ubiquitin-specific deubiquitinase gumby regulates angiogenesis. Nature 2013, 498:318-324.
34. Rotin D., Kumar S. Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2009, 10:398-409.
35. Sato Y., Yoshikawa A., Yamashita M., Yamagata A., Fukai S. Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by NZF domains of TAB2 and TAB3. EMBO J. 2009, 28:3903-3909.
36. Sato Y., Fujita H., Yoshikawa A., Yamashita M., Yamagata A., Kaiser S.E., Iwai K., Fukai S. Specific recognition of linear ubiquitin chains by the Npl4 zinc finger (NZF) domain of the HOIL-1L subunit of the linear ubiquitin chain assembly complex. Proc. Natl. Acad. Sci. USA 2011, 108:20520-20525.
37. Scheffner M., Huibregtse J.M., Vierstra R.D., Howley P.M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993, 75:495-505.
38. 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.
39. Shaid S., Brandts C.H., Serve H., Dikic I. Ubiquitination and selective autophagy. Cell Death Differ. 2013, 20:21-30.
40. 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.
41. 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. 2008, 22:528-542.
42. Tran H., Bustos D., Yeh R., Rubinfeld B., Lam C., Shriver S., Zilberleyb I., Lee M.W., Phu L., Sarkar A.A., et al. HectD1 E3 ligase modifies adenomatous polyposis coli (APC) with polyubiquitin to promote the APC-axin interaction. J.Biol. Chem. 2013, 288:3753-3767.
43. Tsuchiya H., Tanaka K., Saeki Y. The parallel reaction monitoring method contributes to a highly sensitive polyubiquitin chain quantification. Biochem. Biophys. Res. Commun. 2013, 436:223-229.
44. van Wijk S.J.L., 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.
45. Varadan R., Walker O., Pickart C., Fushman D. Structural properties of polyubiquitin chains in solution. J.Mol. Biol. 2002, 324:637-647.
46. 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.
47. Vijay-Kumar S., Bugg C.E., Cook W.J. Structure of ubiquitin refined at 1.8 A resolution. J.Mol. Biol. 1987, 194:531-544.
48. 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.
49. Wagner S.A., Beli P., Weinert B.T., Nielsen M.L., Cox J., Mann M., Choudhary C. A proteome-wide, quantitative survey of invivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 2011, M111.013284.
50. Wickliffe K.E., Williamson A., Meyer H.-J., Kelly A., Rape M. K11-linked ubiquitin chains as novel regulators of cell division. Trends Cell Biol. 2011, 21:656-663.
51. Williamson M.P. Using chemical shift perturbation to characterise ligand binding. Prog. Nucl. Magn. Reson. Spectrosc. 2013, 73:1-16.
52. 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.
53. Ye Y., Rape M. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 2009, 10:755-764.
54. 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.
55. You J., Pickart C.M. A HECT domain E3 enzyme assembles novel polyubiquitin chains. J.Biol. Chem. 2001, 276:19871-19878.
56. Yuan W.-C., Lee Y.-R., Lin S.-Y., Chang L.-Y., Tan Y.P., Hung C.-C., Kuo J.-C., Liu C.-H., Lin M.-Y., Xu M., et al. K33-Linked Polyubiquitination of Coronin 7 by Cul3-KLHL20Ubiquitin E3 Ligase Regulates Protein Trafficking. Mol. Cell 2014, 54:586-600.