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Structural analysis of the conserved ubiquitin-binding motifs (UBMs) of the translesion polymerase iota in complex with ubiquitin.

Burschowsky D, Rudolf F, Rabut G, Herrmann T, Peter M, Matthias P, Wider G
J Biol Chem 286 1364-73 (2011)
Cited: 24 times
EuropePMC logo PMID: 20929865

Abstract

Ubiquitin-binding domains (UBDs) provide specificity to the ubiquitin system, which is also involved in translesion synthesis (TLS) in eukaryotic cells. Upon DNA damage, the UBDs (UBM domains) of polymerase iota (Pol ι) interact with ubiquitinated proliferating cell nuclear antigen to regulate the interchange between processive DNA polymerases and TLS. We report a biophysical analysis and solution structures of the two conserved UBM domains located in the C-terminal tail of murine Pol ι in complex with ubiquitin. The 35-amino acid core folds into a helix-turn-helix motif, which belongs to a novel domain fold. Similar to other UBDs, UBMs bind to ubiquitin on the hydrophobic surface delineated by Leu-8, Ile-44, and Val-70, however, slightly shifted toward the C terminus. In addition, UBMs also use electrostatic interactions to stabilize binding. NMR and fluorescence spectroscopy measurements revealed that UBMs bind monoubiquitin, and Lys-63- but not Lys-48-linked chains. Importantly, these biophysical data are supported by functional studies. Indeed, yeast cells expressing ubiquitin mutants specifically defective for UBM binding are viable but sensitive to DNA damaging conditions that require TLS for repair.

Articles - 2kwu mentioned but not cited (2)

  1. Structure of monoubiquitinated PCNA: implications for DNA polymerase switching and Okazaki fragment maturation. Zhang Z, Zhang S, Lin SH, Wang X, Wu L, Lee EY, Lee MY. Cell Cycle 11 2128-2136 (2012)
  2. Structural analysis of the conserved ubiquitin-binding motifs (UBMs) of the translesion polymerase iota in complex with ubiquitin. Burschowsky D, Rudolf F, Rabut G, Herrmann T, Peter M, Wider G. J. Biol. Chem. 286 1364-1373 (2011)


Reviews citing this publication (12)

  1. Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Sale JE, Lehmann AR, Woodgate R. Nat. Rev. Mol. Cell Biol. 13 141-152 (2012)
  2. The Fanconi anaemia pathway: new players and new functions. Ceccaldi R, Sarangi P, D'Andrea AD. Nat. Rev. Mol. Cell Biol. 17 337-349 (2016)
  3. An overview of Y-Family DNA polymerases and a case study of human DNA polymerase η. Yang W. Biochemistry 53 2793-2803 (2014)
  4. Translesion DNA polymerases in eukaryotes: what makes them tick? Vaisman A, Woodgate R. Crit. Rev. Biochem. Mol. Biol. 52 274-303 (2017)
  5. Ubiquitin-family modifications in the replication of DNA damage. Lehmann AR. FEBS Lett. 585 2772-2779 (2011)
  6. Regulation of human DNA polymerase delta in the cellular responses to DNA damage. Lee MY, Zhang S, Lin SH, Chea J, Wang X, LeRoy C, Wong A, Zhang Z, Lee EY. Environ. Mol. Mutagen. 53 683-698 (2012)
  7. Crosstalk between translesion synthesis, Fanconi anemia network, and homologous recombination repair pathways in interstrand DNA crosslink repair and development of chemoresistance. Haynes B, Saadat N, Myung B, Shekhar MP. Mutat Res Rev Mutat Res 763 258-266 (2015)
  8. Structure of human DNA polymerase iota and the mechanism of DNA synthesis. Makarova AV, Kulbachinskiy AV. Biochemistry Mosc. 77 547-561 (2012)
  9. Ubiquitin and its binding domains. Randles L, Walters KJ. Front Biosci (Landmark Ed) 17 2140-2157 (2012)
  10. Biological and therapeutic relevance of nonreplicative DNA polymerases to cancer. Parsons JL, Nicolay NH, Sharma RA. Antioxid. Redox Signal. 18 851-873 (2013)
  11. Protein-Protein Interactions in Translesion Synthesis. Dash RC, Hadden K. Molecules 26 5544 (2021)
  12. The Rev1-Polζ translesion synthesis mutasome: Structure, interactions and inhibition. Rizzo AA, Korzhnev DM. Enzymes 45 139-181 (2019)

Articles citing this publication (10)

  1. Structural basis of Rev1-mediated assembly of a quaternary vertebrate translesion polymerase complex consisting of Rev1, heterodimeric polymerase (Pol) ζ, and Pol κ. Wojtaszek J, Lee CJ, D'Souza S, Minesinger B, Kim H, D'Andrea AD, Walker GC, Zhou P. J. Biol. Chem. 287 33836-33846 (2012)
  2. SUMO and ubiquitin-dependent XPC exchange drives nucleotide excision repair. van Cuijk L, van Belle GJ, Turkyilmaz Y, Poulsen SL, Janssens RC, Theil AF, Sabatella M, Lans H, Mailand N, Houtsmuller AB, Vermeulen W, Marteijn JA. Nat Commun 6 7499 (2015)
  3. Ubiquitin mediates the physical and functional interaction between human DNA polymerases η and ι. McIntyre J, Vidal AE, McLenigan MP, Bomar MG, Curti E, McDonald JP, Plosky BS, Ohashi E, Woodgate R. Nucleic Acids Res. 41 1649-1660 (2013)
  4. Posttranslational Regulation of Human DNA Polymerase ι. McIntyre J, McLenigan MP, Frank EG, Dai X, Yang W, Wang Y, Woodgate R. J. Biol. Chem. 290 27332-27344 (2015)
  5. Structures of REV1 UBM2 Domain Complex with Ubiquitin and with a Small-Molecule that Inhibits the REV1 UBM2-Ubiquitin Interaction. Vanarotti M, Grace CR, Miller DJ, Actis ML, Inoue A, Evison BJ, Vaithiyalingam S, Singh AP, McDonald ET, Fujii N. J Mol Biol 430 2857-2872 (2018)
  6. 4D APSY-HBCB(CG)CDHD experiment for automated assignment of aromatic amino acid side chains in proteins. Krähenbühl B, Hiller S, Wider G. J. Biomol. NMR 51 313-318 (2011)
  7. Sparsely-sampled, high-resolution 4-D omit spectra for detection and assignment of intermolecular NOEs of protein complexes. Wang S, Zhou P. J. Biomol. NMR 59 51-56 (2014)
  8. Small-molecules that bind to the ubiquitin-binding motif of REV1 inhibit REV1 interaction with K164-monoubiquitinated PCNA and suppress DNA damage tolerance. Vanarotti M, Evison BJ, Actis ML, Inoue A, McDonald ET, Shao Y, Heath RJ, Fujii N. Bioorg. Med. Chem. 26 2345-2353 (2018)
  9. Structural Basis for the Interaction of Mutasome Assembly Factor REV1 with Ubiquitin. Cui G, Botuyan MV, Mer G. J. Mol. Biol. 430 2042-2050 (2018)
  10. Structural insights into pro-aggregation effects of C. elegans CRAM-1 and its human ortholog SERF2. Balasubramaniam M, Ayyadevara S, Shmookler Reis RJ. Sci Rep 8 14891 (2018)


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