UBC13

Summary

Gene Symbol: UBC13
Description: E2 ubiquitin-conjugating protein UBC13
Alias: E2 ubiquitin-conjugating protein UBC13
Species: Saccharomyces cerevisiae S288c
Products:     UBC13

Top Publications

  1. Hofmann R, Pickart C. In vitro assembly and recognition of Lys-63 polyubiquitin chains. J Biol Chem. 2001;276:27936-43 pubmed
    ..We showed previously that the products of the UBC13 and MMS2 genes function in error-free post-replicative DNA repair in the yeast Saccharomyces cerevisiae and form a ..
  2. Daigaku Y, Davies A, Ulrich H. Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature. 2010;465:951-5 pubmed publisher
    ..Our approach has revealed the distribution of PRR tracts in a synchronized cell population. It will allow an in-depth mechanistic analysis of how cells manage the processing of lesions to their genomes during and after replication. ..
  3. Xiao W, Chow B, Broomfield S, Hanna M. The Saccharomyces cerevisiae RAD6 group is composed of an error-prone and two error-free postreplication repair pathways. Genetics. 2000;155:1633-41 pubmed
    ..Our data also suggest that MMS2 and UBC13 play a key role in coordinating the response of the error-free subpathways; Mms2 and Ubc13 form a complex required ..
  4. Gangavarapu V, Haracska L, Unk I, Johnson R, Prakash S, Prakash L. Mms2-Ubc13-dependent and -independent roles of Rad5 ubiquitin ligase in postreplication repair and translesion DNA synthesis in Saccharomyces cerevisiae. Mol Cell Biol. 2006;26:7783-90 pubmed
    ..PRR) of discontinuities that form in the newly synthesized DNA opposite from DNA lesions, mediated by the Mms2-Ubc13 ubiquitin-conjugating enzyme and Rad5...
  5. Parker J, Ulrich H. Mechanistic analysis of PCNA poly-ubiquitylation by the ubiquitin protein ligases Rad18 and Rad5. EMBO J. 2009;28:3657-66 pubmed publisher
    ..the mechanism of poly-ubiquitylation of the replication clamp PCNA by two cooperating E2-E3 pairs, Rad6-Rad18 and Ubc13-Mms2-Rad5...
  6. Eddins M, Carlile C, Gomez K, Pickart C, Wolberger C. Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkage-specific polyubiquitin chain formation. Nat Struct Mol Biol. 2006;13:915-20 pubmed
    ..We have determined the crystal structure of an Mms2-Ubc13-ubiquitin (UEV-E2-Ub) covalent intermediate with donor ubiquitin linked to the active site residue of Ubc13...
  7. Chen S, Davies A, Sagan D, Ulrich H. The RING finger ATPase Rad5p of Saccharomyces cerevisiae contributes to DNA double-strand break repair in a ubiquitin-independent manner. Nucleic Acids Res. 2005;33:5878-86 pubmed
  8. Hofmann R, Pickart C. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell. 1999;96:645-53 pubmed
    ..We show that Mms2p forms a specific heteromeric complex with the UBC13-encoded E2 and is required for the Ubc13p-dependent assembly of polyubiquitin chains linked through lysine 63...
  9. VanDemark A, Hofmann R, Tsui C, Pickart C, Wolberger C. Molecular insights into polyubiquitin chain assembly: crystal structure of the Mms2/Ubc13 heterodimer. Cell. 2001;105:711-20 pubmed
    ..The crystal structure of the Mms2/Ubc13 heterodimer shows the active site of Ubc13 at the intersection of two channels that are potential binding sites ..

More Information

Publications50

  1. Karras G, Jentsch S. The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell. 2010;141:255-67 pubmed publisher
    ..We therefore propose that the RAD6 pathway acts on single-stranded gaps left behind newly restarted replication forks. ..
  2. Loring G, Christensen K, Gerber S, Brenner C. Yeast Chfr homologs retard cell cycle at G1 and G2/M via Ubc4 and Ubc13/Mms2-dependent ubiquitination. Cell Cycle. 2008;7:96-105 pubmed
    ..In contrast, Ubc13/Mms2 is required for G(2) delay and does not contribute to Chf protein turnover...
  3. Ulrich H. The srs2 suppressor of UV sensitivity acts specifically on the RAD5- and MMS2-dependent branch of the RAD6 pathway. Nucleic Acids Res. 2001;29:3487-94 pubmed
    ..A sub-branch within the RAD6 pathway is mediated by RAD5, UBC13 and MMS2, and a comprehensive analysis of the srs2 effect on other known members of the RAD6 pathway reported here ..
  4. Stelter P, Ulrich H. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature. 2003;425:188-91 pubmed
    ..Our findings assign a function to SUMO during S phase and demonstrate how ubiquitin and SUMO, by regulating the accuracy of replication and repair, contribute to overall genomic stability. ..
  5. Carlile C, Pickart C, Matunis M, Cohen R. Synthesis of free and proliferating cell nuclear antigen-bound polyubiquitin chains by the RING E3 ubiquitin ligase Rad5. J Biol Chem. 2009;284:29326-34 pubmed publisher
    ..ubiquitin moiety of monoubiquitinated proliferating cell nuclear antigen (monoUb-PCNA) by the E2-E3 complex of (Ubc13-Mms2)-Rad5. This promotes error-free bypass of DNA damage lesions...
  6. Ulrich H. Protein-protein interactions within an E2-RING finger complex. Implications for ubiquitin-dependent DNA damage repair. J Biol Chem. 2003;278:7051-8 pubmed
    The RING finger protein RAD5 interacts and cooperates with the UBC13-MMS2 ubiquitin-conjugating enzyme in postreplication DNA damage repair in yeast...
  7. McKenna S, Spyracopoulos L, Moraes T, Pastushok L, Ptak C, Xiao W, et al. Noncovalent interaction between ubiquitin and the human DNA repair protein Mms2 is required for Ubc13-mediated polyubiquitination. J Biol Chem. 2001;276:40120-6 pubmed
    ..enzyme variant that is involved in the error-free DNA postreplicative repair pathway through its association with Ubc13, an E2...
  8. Papouli E, Chen S, Davies A, Huttner D, Krejci L, Sung P, et al. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol Cell. 2005;19:123-33 pubmed
    ..Our findings suggest a mechanism by which SUMO and ubiquitin cooperatively control the choice of pathway for the processing of DNA lesions during replication. ..
  9. Ball L, Xu X, Blackwell S, Hanna M, Lambrecht A, Xiao W. The Rad5 helicase activity is dispensable for error-free DNA post-replication repair. DNA Repair (Amst). 2014;16:74-83 pubmed publisher
    ..polyubiquitinated PCNA to signal lesion bypass through template switch, a process thought to be dependent on Mms2-Ubc13 and a RING finger motif of the Rad5 ubiquitin ligase...
  10. Ramsey K, Smith J, Dasgupta A, Maqani N, Grant P, Auble D. The NEF4 complex regulates Rad4 levels and utilizes Snf2/Swi2-related ATPase activity for nucleotide excision repair. Mol Cell Biol. 2004;24:6362-78 pubmed
    ..Moreover, the E2s Ubc9 and Ubc13 were linked to the NEF4 repair pathway by genetic criteria...
  11. Brusky J, Zhu Y, Xiao W. UBC13, a DNA-damage-inducible gene, is a member of the error-free postreplication repair pathway in Saccharomyces cerevisiae. Curr Genet. 2000;37:168-74 pubmed
    The Ubc13 protein was recently identified for its unique role in ubiquitin (Ub) chain assembly at the Ub Lys-63 residue instead of the conventional Lys-48 residue...
  12. Ulrich H, Jentsch S. Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 2000;19:3388-97 pubmed
    Two ubiquitin-conjugating enzymes, RAD6 and the heteromeric UBC13-MMS2 complex, have been implicated in post-replicative DNA damage repair in yeast. Here we provide a mechanistic basis for cooperation between the two enzymes...
  13. Renaud Young M, Lloyd D, Chatfield Reed K, George I, Chua G, Cobb J. The NuA4 complex promotes translesion synthesis (TLS)-mediated DNA damage tolerance. Genetics. 2015;199:1065-76 pubmed publisher
    ..sensitivity to MMS when NuA4 alleles, esa1-L254P and yng2Δ, were combined with the error-free bypass mutant ubc13Δ...
  14. Santa Maria S, Gangavarapu V, Johnson R, Prakash L, Prakash S. Requirement of Nse1, a subunit of the Smc5-Smc6 complex, for Rad52-dependent postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol Cell Biol. 2007;27:8409-18 pubmed
    In Saccharomyces cerevisiae, postreplication repair (PRR) of UV-damaged DNA occurs by a Rad6-Rad18- and an Mms2-Ubc13-Rad5-dependent pathway or by a Rad52-dependent pathway...
  15. Chahwan R, Gravel S, Matsusaka T, Jackson S. Dma/RNF8 proteins are evolutionarily conserved E3 ubiquitin ligases that target septins. Cell Cycle. 2013;12:1000-8 pubmed publisher
    ..Together, these findings reveal evolutionary and functional conservation of Dma proteins, and suggest that RNF8 maintains genome stability through independent, yet analogous, nuclear and cytoplasmic ubiquitylation activities. ..
  16. Tsui C, Raguraj A, Pickart C. 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. 2005;280:19829-35 pubmed
    ..Chain formation is catalyzed by the Mms2/Ubc13 conjugating enzyme variant/conjugating enzyme (UEV.E2) complex together with the Rad5 ubiquitin ligase...
  17. Sayama K, Yamamoto M, Shirakata Y, Hanakawa Y, Hirakawa S, Dai X, et al. E2 Polyubiquitin-conjugating enzyme Ubc13 in keratinocytes is essential for epidermal integrity. J Biol Chem. 2010;285:30042-9 pubmed publisher
    The E2 polyubiquitin-conjugating enzyme Ubc13 is a mediator of innate immune reactions. Ubc13 mediates the conjugation of keratin (K)63-linked polyubiquitin chains onto TNF receptor-associated factor 6 and IKK? during NF-?B activation...
  18. Gonzalez Huici V, Szakal B, Urulangodi M, Psakhye I, Castellucci F, Menolfi D, et al. DNA bending facilitates the error-free DNA damage tolerance pathway and upholds genome integrity. EMBO J. 2014;33:327-40 pubmed publisher
    ..Together, the results suggest that replication-associated topological changes involving the molecular DNA bender, Hmo1, set the stage for dedicated repair reactions that limit errors during replication and impact on genome stability. ..
  19. Berndsen C, Wolberger C. A spectrophotometric assay for conjugation of ubiquitin and ubiquitin-like proteins. Anal Biochem. 2011;418:102-10 pubmed publisher
    ..The kinetics of polyubiquitin chain formation by Ubc13-Mms2 measured by this assay are similar to those determined by gel-based assays, indicating that the data produced ..
  20. Martini E, Keeney S, Osley M. A role for histone H2B during repair of UV-induced DNA damage in Saccharomyces cerevisiae. Genetics. 2002;160:1375-87 pubmed
    ..When combined with a ubc13Delta mutation, which is also epistatic with rad5Delta, the htb1-3 mutation enhanced UV-induced cell killing. These results suggest that histone H2B acts in a novel RAD5-dependent branch of PRR. ..
  21. Saugar I, Parker J, Zhao S, Ulrich H. The genome maintenance factor Mgs1 is targeted to sites of replication stress by ubiquitylated PCNA. Nucleic Acids Res. 2012;40:245-57 pubmed publisher
    ..Our identification of Mgs1 as a UBZ-dependent downstream effector of ubiquitylated PCNA suggests an explanation for the ambivalent role of the protein in damage processing. ..
  22. Hoopes J, Hughes A, Hobson L, Cortez L, Brown A, Roberts S. Avoidance of APOBEC3B-induced mutation by error-free lesion bypass. Nucleic Acids Res. 2017;45:5243-5254 pubmed publisher
    ..However, strains without error-free lesion bypass proteins Ubc13, Mms2 and Mph1 displayed respective 4.9-, 2.8- and 7.8-fold higher frequency of APOBEC3B-induced CanR...
  23. Godin S, Zhang Z, Herken B, Westmoreland J, Lee A, Mihalevic M, et al. The Shu complex promotes error-free tolerance of alkylation-induced base excision repair products. Nucleic Acids Res. 2016;44:8199-215 pubmed publisher
    ..Together, our work demonstrates that the Shu complex's promotion of Rad51 pre-synaptic filaments is critical for high-fidelity bypass of multiple replication-blocking lesion. ..
  24. Wen R, Torres Acosta J, Pastushok L, Lai X, Pelzer L, Wang H, et al. Arabidopsis UEV1D promotes Lysine-63-linked polyubiquitination and is involved in DNA damage response. Plant Cell. 2008;20:213-27 pubmed publisher
    ..The ubiquitin-conjugating enzyme Ubc13 and the Ubc enzyme variant (Uev) methyl methanesulfonate2 (Mms2) are required for this process...
  25. Putnam C, Hayes T, Kolodner R. Post-replication repair suppresses duplication-mediated genome instability. PLoS Genet. 2010;6:e1000933 pubmed publisher
    ..Here, we found that the RAD6- and RAD18-dependent post-replication repair (PRR) and the RAD5-, MMS2-, UBC13-dependent error-free PRR branch acted in concert with the replication stress checkpoint to suppress duplication-..
  26. Choi K, Batke S, Szakal B, Lowther J, Hao F, Sarangi P, et al. Concerted and differential actions of two enzymatic domains underlie Rad5 contributions to DNA damage tolerance. Nucleic Acids Res. 2015;43:2666-77 pubmed publisher
    ..These findings delineate how two Rad5 enzymatic domains concertedly influence PCNA modification, and unveil their discrete contributions to stress tolerance. ..
  27. Hiraishi H, Mochizuki M, Takagi H. Enhancement of stress tolerance in Saccharomyces cerevisiae by overexpression of ubiquitin ligase Rsp5 and ubiquitin-conjugating enzymes. Biosci Biotechnol Biochem. 2006;70:2762-5 pubmed
    ..cerevisiae cells overexpressing essential ubiquitin ligase Rsp5 or ubiquitin-conjugating enzymes (Ubc1-Ubc13) showed tolerance to various stresses...
  28. Daee D, Ferrari E, Longerich S, Zheng X, Xue X, Branzei D, et al. Rad5-dependent DNA repair functions of the Saccharomyces cerevisiae FANCM protein homolog Mph1. J Biol Chem. 2012;287:26563-75 pubmed publisher
    ..These studies reveal the functional conservation of the FA pathway and validate the yeast model for future studies to further elucidate the mechanism of the FA pathway. ..
  29. Xu X, Lin A, Zhou C, Blackwell S, Zhang Y, Wang Z, et al. Involvement of budding yeast Rad5 in translesion DNA synthesis through physical interaction with Rev1. Nucleic Acids Res. 2016;44:5231-45 pubmed publisher
    ..This study indicates that Rad5 plays a critical role in pathway choice between TLS and error-free DDT. ..
  30. Bi X, Yu Q, Siler J, Li C, Khan A. Functions of Fun30 chromatin remodeler in regulating cellular resistance to genotoxic stress. PLoS ONE. 2015;10:e0121341 pubmed publisher
    ..the other hand, we show that Fun30 deletion suppresses the MMS- and HU-sensitivity of cells lacking the Rad5/Mms2/Ubc13-dependent error-free DNA damage tolerance mechanism...
  31. Sharma N, Kochenova O, Shcherbakova P. The non-canonical protein binding site at the monomer-monomer interface of yeast proliferating cell nuclear antigen (PCNA) regulates the Rev1-PCNA interaction and Pol?/Rev1-dependent translesion DNA synthesis. J Biol Chem. 2011;286:33557-66 pubmed publisher
    ..The new mode of Rev1-PCNA binding described here suggests a mechanism by which Rev1 adopts a catalytically inactive configuration at the replication fork. ..
  32. Andersen P, Zhou H, Pastushok L, Moraes T, McKenna S, Ziola B, et al. Distinct regulation of Ubc13 functions by the two ubiquitin-conjugating enzyme variants Mms2 and Uev1A. J Cell Biol. 2005;170:745-55 pubmed
    b>Ubc13, a ubiquitin-conjugating enzyme (Ubc), requires the presence of a Ubc variant (Uev) for polyubiquitination...
  33. Menolfi D, Delamarre A, Lengronne A, Pasero P, Branzei D. Essential Roles of the Smc5/6 Complex in Replication through Natural Pausing Sites and Endogenous DNA Damage Tolerance. Mol Cell. 2015;60:835-46 pubmed publisher
  34. Wen R, Li J, Xu X, Cui Z, Xiao W. Zebrafish Mms2 promotes K63-linked polyubiquitination and is involved in p53-mediated DNA-damage response. DNA Repair (Amst). 2012;11:157-66 pubmed publisher
    The ubiquitin-conjugating enzyme Ubc13 together with a Ubc/E2 variant (Uev) form a stable complex and mediate K63-linked polyubiquitination, which is implicated in DNA damage tolerance in yeast and mammalian cells...
  35. Halas A, Podlaska A, Derkacz J, McIntyre J, Skoneczna A, Sledziewska Gojska E. The roles of PCNA SUMOylation, Mms2-Ubc13 and Rad5 in translesion DNA synthesis in Saccharomyces cerevisiae. Mol Microbiol. 2011;80:786-97 pubmed publisher
    Mms2, in concert with Ubc13 and Rad5, is responsible for polyubiquitination of replication processivity factor PCNA. This modification activates recombination-like DNA damage-avoidance mechanisms, which function in an error-free manner...
  36. Pastushok L, Hanna M, Xiao W. Constitutive fusion of ubiquitin to PCNA provides DNA damage tolerance independent of translesion polymerase activities. Nucleic Acids Res. 2010;38:5047-58 pubmed publisher
    ..As expected, the DNA damage resistance provided by PCNA.Ub is not dependent on RAD18 or UBC13. Surprisingly, inactivation of TLS polymerases did not abolish PCNA.Ub resistance to DNA damage, nor did PCNA...
  37. Davies A, Neiss A, Ulrich H. Ubiquitylation of the 9-1-1 checkpoint clamp is independent of rad6-rad18 and DNA damage. Cell. 2010;141:1080-7 pubmed publisher
    ..Instead, our findings suggest that ubiquitylation of the 9-1-1 complex may be a background reaction that in some cases can mediate proteasomal degradation. ..
  38. Hochstrasser M. Ubiquitin-dependent protein degradation. Annu Rev Genet. 1996;30:405-39 pubmed
    ..This diversity underlies both the high substrate specificity of the ubiquitin system and the variety of regulatory mechanisms that it serves. ..
  39. Huang J, Huen M, Kim H, Leung C, Glover J, Yu X, et al. RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nat Cell Biol. 2009;11:592-603 pubmed publisher
    ..Together, our data uncovers RAD18 as a key factor that orchestrates HRR through surveillance of the DNA damage signal. ..
  40. Paek A, Jones H, Kaochar S, Weinert T. The role of replication bypass pathways in dicentric chromosome formation in budding yeast. Genetics. 2010;186:1161-73 pubmed publisher
    ..Fourth, by studying genes implicated in suppression of GCRs in other studies, we found that inverted repeat fusion has a profile of genetic regulation distinct from these other major forms of GCR formation. ..
  41. O Neill B, Hanway D, Winzeler E, Romesberg F. Coordinated functions of WSS1, PSY2 and TOF1 in the DNA damage response. Nucleic Acids Res. 2004;32:6519-30 pubmed
    ..Tof1 is known to be involved in stabilizing stalled replication forks and our data suggest that Wss1 and Psy2 similarly function to stabilize or process stalled or collapsed replication forks. ..