A Structurally Unique E2-Binding Domain Activates Ubiquitination by the ERAD E2, Ubc7p, through Multiple Mechanisms

Molecular Cell

Volumn 50, Issue 4, 2013, Pages 516-527

  Metzger, MeredithB ^a   Liang, Yu He ^a,b   Das, Ranabir ^a   Mariano, Jennifer ^a   Li, Shengjian ^a,c   Li, Jess ^a   Kostova, Zlatka ^a   Byrd, R Andrew ^a   Ji, Xinhua ^a   Weissman, AllanM ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; PROTEIN UBC7P; THIOESTER; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CRYSTAL STRUCTURE; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; HYDROPHOBICITY; STATIC ELECTRICITY; UBIQUITINATION;

AMINO ACID SEQUENCE; BINDING SITES; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; STATIC ELECTRICITY; SUBSTRATE SPECIFICITY; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 84878170491     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.04.004     Document Type: Article

References (44)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. 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. Published online May 9, 2013. 10.1016/j.molcel.2013.04.005.
3. 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.
4. Bazirgan O.A., Hampton R.Y. Cue1p is an activator of Ubc7p E2 activity invitro and invivo. J.Biol. Chem. 2008, 283:12797-12810.
5. Biederer T., Volkwein C., Sommer T. Role of Cue1p in ubiquitination and degradation at the ER surface. Science 1997, 278:1806-1809.
6. Brodsky J.L., Skach W.R. Protein folding and quality control in the endoplasmic reticulum: recent lessons from yeast and mammalian cell systems. Curr. Opin. Cell Biol. 2011, 23:464-475.
7. Brzovic P.S., Keeffe J.R., Nishikawa H., Miyamoto K., Fox D., Fukuda M., Ohta T., Klevit R. Binding and recognition in the assembly of an active BRCA1/BARD1 ubiquitin-ligase complex. Proc. Natl. Acad. Sci. USA 2003, 100:5646-5651.
8. 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.
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 P., Johnson P., Sommer T., Jentsch S., Hochstrasser M. Multiple ubiquitin-conjugating enzymes participate in the invivo degradation of the yeast MAT alpha 2 repressor. Cell 1993, 74:357-369.
11. Cook W.J., Martin P.D., Edwards B.F., Yamazaki R.K., Chau V. Crystal structure of a class I ubiquitin conjugating enzyme (Ubc7) from Saccharomyces cerevisiae at 2.9 angstroms resolution. Biochemistry 1997, 36:1621-1627.
12. Das R., Mariano J., Tsai Y.C., Kalathur R.C., Kostova Z., Li J., Tarasov S.G., McFeeters R.L., Altieri A.S., Ji X., et al. Allosteric activation of E2-RING finger-mediated ubiquitylation by a structurally defined specific E2-binding region of gp78. Mol. Cell 2009, 34:674-685.
13. David Y., Ziv T., Admon A., Navon A. The E2 ubiquitin-conjugating enzymes direct polyubiquitination to preferred lysines. J.Biol. Chem. 2010, 285:8595-8604.
14. Deak P.M., Wolf D.H. Membrane topology and function of Der3/Hrd1p as a ubiquitin-protein ligase (E3) involved in endoplasmic reticulum degradation. J.Biol. Chem. 2001, 276:10663-10669.
15. Deshaies R.J., Joazeiro C.A. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 2009, 78:399-434.
16. Dominguez C., Bonvin A.M., Winkler G.S., van Schaik F.M., Timmers H.T., Boelens R. Structural model of the UbcH5B/CNOT4 complex revealed by combining NMR, mutagenesis, and docking approaches. Structure 2004, 12:633-644.
17. Dou H., Buetow L., Sibbet G.J., Cameron K., Huang D.T. BIRC7-E2 ubiquitin conjugate structure reveals the mechanism of ubiquitin transfer by a RING dimer. Nat. Struct. Mol. Biol. 2012, 19:876-883.
18. Eddins M.J., Carlile C.M., Gomez K.M., Pickart C.M., Wolberger C. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat. Struct. Mol. Biol. 2006, 13:915-920.
19. Eletr Z.M., Huang D.T., Duda D.M., Schulman B.A., Kuhlman B. E2 conjugating enzymes must disengage from their E1 enzymes before E3-dependent ubiquitin and ubiquitin-like transfer. Nat. Struct. Mol. Biol. 2005, 12:933-934.
20. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
21. Gardner R.G., Shearer A.G., Hampton R.Y. Invivo action of the HRD ubiquitin ligase complex: mechanisms of endoplasmic reticulum quality control and sterol regulation. Mol. Cell. Biol. 2001, 21:4276-4291.
22. Hibbert R.G., Huang A., Boelens R., Sixma T.K. E3 ligase Rad18 promotes monoubiquitination rather than ubiquitin chain formation by E2enzyme Rad6. Proc. Natl. Acad. Sci. USA 2011, 108:5590-5595.
23. Hooft R.W., Vriend G., Sander C., Abola E.E. Errors in protein structures. Nature 1996, 381:272.
24. Huyer G., Piluek W.F., Fansler Z., Kreft S.G., Hochstrasser M., Brodsky J.L., Michaelis S. Distinct machinery is required in Saccharomyces cerevisiae for the endoplasmic reticulum-associated degradation of a multispanning membrane protein and a soluble luminal protein. J.Biol. Chem. 2004, 279:38369-38378.
25. Ju T., Bocik W., Majumdar A., Tolman J.R. Solution structure and dynamics of human ubiquitin conjugating enzyme Ube2g2. Proteins 2010, 78:1291-1301.
26. 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.
27. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J.Appl. Cryst. 1993, 26:283-291.
28. Li W., Tu D., Brunger A.T., Ye Y. A ubiquitin ligase transfers preformed polyubiquitin chains from a conjugating enzyme to a substrate. Nature 2007, 446:333-337.
29. Metzger M.B., Hristova V.A., Weissman A.M. HECT and RING finger families of E3 ubiquitin ligases at a glance. J.Cell Sci. 2012, 125:531-537.
30. Olsen S.K., Lima C.D. Structure of a ubiquitin e1-e2 complex: insights to e1-e2 thioester transfer. Mol. Cell 2013, 49:884-896.
31. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
32. Ozkan E., Yu H., Deisenhofer J. Mechanistic insight into the allosteric activation of a ubiquitin-conjugating enzyme by RING-type ubiquitin ligases. Proc. Natl. Acad. Sci. USA 2005, 102:18890-18895.
33. Plechanovová A., Jaffray E.G., Tatham M.H., Naismith J.H., Hay R.T. Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis. Nature 2012, 489:115-120.
34. Prudden J., Perry J.J., Arvai A.S., Tainer J.A., Boddy M.N. Molecular mimicry of SUMO promotes DNA repair. Nat. Struct. Mol. Biol. 2009, 16:509-516.
35. Pruneda J.N., Littlefield P.J., Soss S.E., Nordquist K.A., Chazin W.J., Brzovic P.S., Klevit R.E. Structure of an E3:E2~Ub complex reveals an allosteric mechanism shared among RING/U-box ligases. Mol. Cell 2012, 47:933-942.
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. Reverter D., Lima C.D. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 2005, 435:687-692.
38. Sekiyama N., Arita K., Ikeda Y., Hashiguchi K., Ariyoshi M., Tochio H., Saitoh H., Shirakawa M. Structural basis for regulation of poly-SUMO chain by a SUMO-like domain of Nip45. Proteins 2010, 78:1491-1502.
39. Shih S.C., Prag G., Francis S.A., Sutanto M.A., Hurley J.H., Hicke L. A ubiquitin-binding motif required for intramolecular monoubiquitylation, the CUE domain. EMBO J. 2003, 22:1273-1281.
40. Smith M.H., Ploegh H.L., Weissman J.S. Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 2011, 334:1086-1090.
41. Swanson R., Locher M., Hochstrasser M. A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matalpha2 repressor degradation. Genes Dev. 2001, 15:2660-2674.
42. Wenzel D.M., Stoll K.E., Klevit R.E. E2s: structurally economical and functionally replete. Biochem. J. 2011, 433:31-42.
43. Williams C., van den Berg M., Panjikar S., Stanley W.A., Distel B., Wilmanns M. Insights into ubiquitin-conjugating enzyme/ co-activator interactions from the structure of the Pex4p:Pex22p complex. EMBO J. 2012, 31:391-402.
44. Zheng N., Wang P., Jeffrey P.D., Pavletich N.P. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 2000, 102:533-539.