Two Mms2 residues cooperatively interact with ubiquitin and are critical for Lys63 polyubiquitination in vitro and in vivo

FEBS Letters

Volumn 581, Issue 28, 2007, Pages 5343-5348

  Pastushok, Landon ^a   Spyracopoulos, Leo ^b   Xiao, Wei ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Lys63 linked chain; Mms2; Protein protein interaction; Ubiquitination; UEV

Indexed keywords

LYSINE; PROTEIN; PROTEIN MMS2; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONJUGATION; CONTROLLED STUDY; GENE FUNCTION; GENE LOSS; IN VITRO STUDY; IN VIVO STUDY; MUTAGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; DIMERIZATION; DNA; DNA REPAIR; DNA REPLICATION; LIGASES; LYSINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, QUATERNARY; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUITIN; UBIQUITINATION;

EID: 36048957244     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2007.10.028     Document Type: Article

References (30)

1. Deng L., Wang C., Spencer E., Yang L., Braun A., You J., Slaughter C., Pickart C., and Chen Z.J. Activation of the IκB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103 (2000) 351-361
2. VanDemark A.P., Hofmann R.M., Tsui C., Pickart C.M., and Wolberger C. Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer. Cell 105 (2001) 711-720
3. Tenno T., Fujiwara K., Tochio H., Iwai K., Morita E.H., Hayashi H., et al. Structural basis for distinct roles of Lys63- and Lys48-linked polyubiquitin chains. Genes Cells 9 (2004) 865-875
4. Varadan R., Assfalg M., Haririnia A., Raasi S., Pickart C., and Fushman D. Solution conformation of Lys63-linked di-ubiquitin chain provides clues to functional diversity of polyubiquitin signaling. J. Biol. Chem. 279 (2004) 7055-7063
5. Andersen P.L., Zhou H., Pastushok L., Moraes T., McKenna S., Ziola B., Ellison M.J., Dixit V.M., and Xiao W. Distinct regulation of Ubc13 functions by the two ubiquitin-conjugating enzyme variants Mms2 and Uev1A. J. Cell. Biol. 170 (2005) 745-755
6. Zhou H., Wertz I., O'Rourke K., Ultsch M., Seshagiri S., Eby M., Xiao W., and Dixit V.M. Bcl10 activates the NF-κB pathway through ubiquitination of NEMO. Nature 427 (2004) 167-171
7. Bothos J., Summers M.K., Venere M., Scolnick D.M., and Halazonetis T.D. The Chfr mitotic checkpoint protein functions with Ubc13-Mms2 to form Lys63-linked polyubiquitin chains. Oncogene 22 (2003) 7101-7107
8. Syed N.A., Andersen P.L., Warrington R.C., and Xiao W. Uev1A, a ubiquitin conjugating enzyme variant, inhibits stress-induced apoptosis through NF-κB activation. Apoptosis 11 (2006) 2147-2157
9. Unk I., Hajdu I., Fatyol K., Szakal B., Blastyak A., Bermudez V., Hurwitz J., Prakash L., Prakash S., and Haracska L. Human SHPRH is a ubiquitin ligase for Mms2-Ubc13-dependent polyubiquitylation of proliferating cell nuclear antigen. Proc. Natl. Acad. Sci. USA 103 (2006) 18107-18112
10. Sancho E., Vila M.R., Sanchez-Pulido L., Lozano J.J., Paciucci R., Nadal M., et al. Role of UEV-1, an inactive variant of the E2 ubiquitin-conjugating enzymes, in in vitro differentiation and cell cycle behavior of HT-29-M6 intestinal mucosecretory cells. Mol. Cell Biol. 18 (1998) 576-589
11. Xiao W., Lin S.L., Broomfield S., Chow B.L., and Wei Y.F. The products of the yeast MMS2 and two human homologs (hMMS2 and CROC-1) define a structurally and functionally conserved Ubc-like protein family. Nucleic Acids Res. 26 (1998) 3908-3914
12. Broomfield S., Chow B.L., and Xiao W. MMS2, encoding a ubiquitin-conjugating-enzyme-like protein, is a member of the yeast error-free postreplication repair pathway. Proc. Natl. Acad. Sci. USA 95 (1998) 5678-5683
13. Hofmann R.M., and Pickart C.M. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96 (1999) 645-653
14. Xiao W., Chow B.L., Fontanie T., Ma L., Bacchetti S., Hryciw T., and Broomfield S. Genetic interactions between error-prone and error-free postreplication repair pathways in Saccharomyces cerevisiae. Mutat. Res. 435 (1999) 1-11
15. Brusky J., Zhu Y., and Xiao W. UBC13, a DNA-damage-inducible gene, is a member of the error-free postreplication repair pathway in Saccharomyces cerevisiae. Curr. Genet. 37 (2000) 168-174
16. McKenna S., Spyracopoulos L., Moraes T., Pastushok L., Ptak C., Xiao W., and Ellison M.J. Noncovalent interaction between ubiquitin and the human DNA repair protein Mms2 is required for Ubc13-mediated polyubiquitination. J. Biol. Chem. 276 (2001) 40120-40126
17. Moraes T.F., Edwards R.A., McKenna S., Pastushok L., Xiao W., Glover J.N., and Ellison M.J. Crystal structure of the human ubiquitin conjugating enzyme complex, hMms2-hUbc13. Nat. Struct. Biol. 8 (2001) 669-673
18. McKenna S., Moraes T., Pastushok L., Ptak C., Xiao W., Spyracopoulos L., and Ellison M.J. An NMR-based model of the ubiquitin-bound human ubiquitin conjugation complex Mms2 · Ubc13. The structural basis for lysine 63 chain catalysis. J. Biol. Chem. 278 (2003) 13151-13158
19. Spyracopoulos L., Lewis M.J., and Saltibus L.F. Main chain and side chain dynamics of the ubiquitin conjugating enzyme variant human Mms2 in the free and ubiquitin-bound states. Biochemistry 44 (2005) 8770-8781
20. Eddins M.J., Carlile C.M., Gomez K.M., Pickart C.M., and Wolberger C. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat. Struct. Mol. Biol. 13 (2006) 915-920
21. Tsui C., Raguraj A., and Pickart C.M. Ubiquitin binding site of the ubiquitin E2 variant (UEV) protein Mms2 is required for DNA damage tolerance in the yeast RAD6 pathway. J. Biol. Chem. 280 (2005) 19829-19835
22. Lewis M.J., Saltibus L.F., Hau D.D., Xiao W., and Spyracopoulos L. Structural basis for non-covalent interaction between ubiquitin and the ubiquitin conjugating enzyme variant human MMS2. J. Biomol. NMR 34 (2006) 89-100
23. Pastushok L., Moraes T.F., Ellison M.J., and 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. 280 (2005) 17891-17900
24. Roche H., Gietz R.D., and Kunz B.A. Specificity of the yeast rev3Δ antimutator and REV3 dependency of the mutator resulting from a defect (rad1Δ) in nucleotide excision repair. Genetics 137 (1994) 637-646
25. Barettino D., Feigenbutz M., Valcarcel R., and Stunnenberg H.G. Improved method for PCR-mediated site-directed mutagenesis. Nucleic Acids Res. 22 (1994) 541-542
26. Gietz R.D., and Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74 (1988) 527-534
27. Hurley J.H., Lee S., and Prag G. Ubiquitin-binding domains. Biochem. J. 399 (2006) 361-372
28. Harper J.W., and Schulman B.A. Structural complexity in ubiquitin recognition. Cell 124 (2006) 1133-1136
29. McKenna S., Hu J., Moraes T., Xiao W., Ellison M.J., and Spyracopoulos L. Energetics and specificity of interactions within Ub · Uev · Ubc13 human ubiquitin conjugation complexes. Biochemistry 42 (2003) 7922-7930
30. Wooff J., Pastushok L., Hanna M., Fu Y., and Xiao W. The TRAF6 RING finger domain mediates physical interaction with Ubc13. FEBS Lett. 566 (2004) 229-233