The CUE Domain of Cue1 Aligns Growing Ubiquitin Chains with Ubc7 for Rapid Elongation

Molecular Cell

Volumn 62, Issue 6, 2016, Pages 918-928

  von Delbrück, Maximilian ^a   Kniss, Andreas ^b   Rogov, Vladimir V ^b   Pluska, Lukas ^a   Bagola, Katrin ^d   Löhr, Frank ^b   Güntert, Peter ^b   Sommer, Thomas ^a,c   Dötsch, Volker ^b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c HUMBOLDT UNIVERSITY   (Germany)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CUE1 PROTEIN; POLYUBIQUITIN; UBC7 PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; CUE1 PROTEIN, S CEREVISIAE; MEMBRANE PROTEIN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; UBC6 PROTEIN, S CEREVISIAE; UBC7 PROTEIN, S CEREVISIAE; UBIQUITIN CONJUGATING ENZYME;

ALPHA HELIX; ANISOTROPY; ARTICLE; BINDING SITE; CROSS LINKING; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; FLUORESCENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; PROTEIN DEGRADATION; UBIQUITINATION; CHEMICAL PHENOMENA; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN DOMAIN; SACCHAROMYCES CEREVISIAE; SPECTROFLUOROMETRY; STRUCTURE ACTIVITY RELATION;

CARRIER PROTEINS; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTATION; POLYUBIQUITIN; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECTROMETRY, FLUORESCENCE; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 84974668037     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.04.031     Document Type: Article

References (45)

1. Bagola K., von Delbrück M., Dittmar G., Scheffner M., Ziv I., Glickman M.H., Ciechanover A., Sommer T. Ubiquitin binding by a CUE domain regulates ubiquitin chain formation by ERAD E3 ligases. Mol. Cell 2013, 50:528-539.
2. Bays N.W., Gardner R.G., Seelig L.P., Joazeiro C.A., Hampton R.Y. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat. Cell Biol. 2001, 3:24-29.
3. Bazirgan O.A., Hampton R.Y. Cue1p is an activator of Ubc7p E2 activity in vitro and in vivo. J. Biol. Chem. 2008, 283:12797-12810.
4. Berndsen C.E., Wolberger C. A spectrophotometric assay for conjugation of ubiquitin and ubiquitin-like proteins. Anal. Biochem. 2011, 418:102-110.
5. Biederer T., Volkwein C., Sommer T. Role of Cue1p in ubiquitination and degradation at the ER surface. Science 1997, 278:1806-1809.
6. Brown N.G., Watson E.R., Weissmann F., Jarvis M.A., VanderLinden R., Grace C.R., Frye J.J., Qiao R., Dube P., Petzold G., et al. Mechanism of polyubiquitination by human anaphase-promoting complex: RING repurposing for ubiquitin chain assembly. Mol. Cell 2014, 56:246-260.
7. Brzovic P.S., Lissounov A., Christensen D.E., Hoyt D.W., Klevit R.E. A UbcH5/ubiquitin noncovalent complex is required for processive BRCA1-directed ubiquitination. Mol. Cell 2006, 21:873-880.
8. Buetow L., Gabrielsen M., Anthony N.G., Dou H., Patel A., Aitkenhead H., Sibbet G.J., Smith B.O., Huang D.T. Activation of a primed RING E3-E2-ubiquitin complex by non-covalent ubiquitin. Mol. Cell 2015, 58:297-310.
9. Carvalho P., Goder V., Rapoport T.A. Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 2006, 126:361-373.
10. Chen Z.J., Sun L.J. Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 2009, 33:275-286.
11. Choi Y.-S., Wu K., Jeong K., Lee D., Jeon Y.H., Choi B.-S., Pan Z.-Q., Ryu K.-S., Cheong C. The human Cdc34 carboxyl terminus contains a non-covalent ubiquitin binding activity that contributes to SCF-dependent ubiquitination. J. Biol. Chem. 2010, 285:17754-17762.
12. Choi Y.-S., Lee Y.-J., Lee S.-Y., Shi L., Ha J.-H., Cheong H.-K., Cheong C., Cohen R.E., Ryu K.-S. Differential ubiquitin binding by the acidic loops of Ube2g1 and Ube2r1 enzymes distinguishes their Lys-48-ubiquitylation activities. J. Biol. Chem. 2015, 290:2251-2263.
13. Conaway R.C., Brower C.S., Conaway J.W. Emerging roles of ubiquitin in transcription regulation. Science 2002, 296:1254-1258.
14. Crosas B., Hanna J., Kirkpatrick D.S., Zhang D.P., Tone Y., Hathaway N.A., Buecker C., Leggett D.S., Schmidt M., King R.W., et al. Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities. Cell 2006, 127:1401-1413.
15. de Vries S.J., van Dijk M., Bonvin A.M. The HADDOCK web server for data-driven biomolecular docking. Nat. Protoc. 2010, 5:883-897.
16. Denic V., Quan E.M., Weissman J.S. A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 2006, 126:349-359.
17. Foresti O., Rodriguez-Vaello V., Funaya C., Carvalho P. Quality control of inner nuclear membrane proteins by the Asi complex. Science 2014, 346:751-755.
18. Haglund K., Dikic I. Ubiquitylation and cell signaling. EMBO J. 2005, 24:3353-3359.
19. Huang T.T., D'Andrea A.D. Regulation of DNA repair by ubiquitylation. Nat. Rev. Mol. Cell Biol. 2006, 7:323-334.
20. Husnjak K., Dikic I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 2012, 81:291-322.
21. Jentsch S., Rumpf S. Cdc48 (p97): a "molecular gearbox" in the ubiquitin pathway?. Trends Biochem. Sci. 2007, 32:6-11.
22. Kang R.S., Daniels C.M., Francis S.A., Shih S.C., Salerno W.J., Hicke L., Radhakrishnan I. Solution structure of a CUE-ubiquitin complex reveals a conserved mode of ubiquitin binding. Cell 2003, 113:621-630.
23. Kelly A., Wickliffe K.E., Song L., Fedrigo I., Rape M. Ubiquitin chain elongation requires E3-dependent tracking of the emerging conjugate. Mol. Cell 2014, 56:232-245.
24. Khmelinskii A., Blaszczak E., Pantazopoulou M., Fischer B., Omnus D.J., Le Dez G., Brossard A., Gunnarsson A., Barry J.D., Meurer M., et al. Protein quality control at the inner nuclear membrane. Nature 2014, 516:410-413.
25. Koegl M., Hoppe T., Schlenker S., Ulrich H.D., Mayer T.U., Jentsch S. A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell 1999, 96:635-644.
26. Komander D., Rape M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81:203-229.
27. Kostova Z., Mariano J., Scholz S., Koenig C., Weissman A.M. A Ubc7p-binding domain in Cue1p activates ER-associated protein degradation. J. Cell Sci. 2009, 122:1374-1381.
28. Kreft S.G., Hochstrasser M. An unusual transmembrane helix in the endoplasmic reticulum ubiquitin ligase Doa10 modulates degradation of its cognate E2 enzyme. J. Biol. Chem. 2011, 286:20163-20174.
29. Kreft S.G., Wang L., Hochstrasser M. Membrane topology of the yeast endoplasmic reticulum-localized ubiquitin ligase Doa10 and comparison with its human ortholog TEB4 (MARCH-VI). J. Biol. Chem. 2006, 281:4646-4653.
30. Liu S., Chen Y., Li J., Huang T., Tarasov S., King A., Weissman A.M., Byrd R.A., Das R. Promiscuous interactions of gp78 E3 ligase CUE domain with polyubiquitin chains. Structure 2012, 20:2138-2150.
31. Mansour W., Nakasone M.A., von Delbrück M., Yu Z., Krutauz D., Reis N., Kleifeld O., Sommer T., Fushman D., Glickman M.H. Disassembly of Lys11 and mixed linkage polyubiquitin conjugates provides insights into function of proteasomal deubiquitinases Rpn11 and Ubp6. J. Biol. Chem. 2015, 290:4688-4704.
32. Metzger M.B., Liang Y.-H., Das R., Mariano J., Li S., Li J., Kostova Z., Byrd R.A., Ji X., Weissman A.M. A structurally unique E2-binding domain activates ubiquitination by the ERAD E2, Ubc7p, through multiple mechanisms. Mol. Cell 2013, 50:516-527.
33. Meyer H.-J., Rape M. Enhanced protein degradation by branched ubiquitin chains. Cell 2014, 157:910-921.
34. Pastushok L., Moraes T.F., Ellison M.J., Xiao W. A single Mms2 "key" residue insertion into a Ubc13 pocket determines the interface specificity of a human Lys63 ubiquitin conjugation complex. J. Biol. Chem. 2005, 280:17891-17900.
35. Pickart C.M., Raasi S. Controlled synthesis of polyubiquitin chains. Methods Enzymol. 2005, 399:21-36.
36. Ravid T., Hochstrasser M. Autoregulation of an E2 enzyme by ubiquitin-chain assembly on its catalytic residue. Nat. Cell Biol. 2007, 9:422-427.
37. Rogov V.V., Rozenknop A., Rogova N.Y., Löhr F., Tikole S., Jaravine V., Güntert P., Dikic I., Dötsch V. A universal expression tag for structural and functional studies of proteins. ChemBioChem 2012, 13:959-963.
38. Schmidt M., Hanna J., Elsasser S., Finley D. Proteasome-associated proteins: regulation of a proteolytic machine. Biol. Chem. 2005, 386:725-737.
39. Thrower J.S., Hoffman L., Rechsteiner M., Pickart C.M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 2000, 19:94-102.
40. Varadan R., Assfalg M., Raasi S., Pickart C., Fushman D. Structural determinants for selective recognition of a Lys48-linked polyubiquitin chain by a UBA domain. Mol. Cell 2005, 18:687-698.
41. Wang Z.X., Jiang R.F. A novel two-site binding equation presented in terms of the total ligand concentration. FEBS Lett. 1996, 392:245-249.
42. Weissman A.M. Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol. 2001, 2:169-178.
43. Wickliffe K.E., Lorenz S., Wemmer D.E., Kuriyan J., Rape M. The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell 2011, 144:769-781.
44. Wright J.D., Mace P.D., Day C.L. Secondary ubiquitin-RING docking enhances Arkadia and Ark2C E3 ligase activity. Nat. Struct. Mol. Biol. 2016, 23:45-52.
45. 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.