Dimer exchange and cleavage specificity of the DNA damage response protein UmuD

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 2, 2013, Pages 611-620

  Ollivierre, Jaylene N ^a   Sikora, Jacquelyn L ^a   Beuning, Penny J ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

DNA damage; Heterodimer; Heterodimer cleavage; SOS mutagenesis

Indexed keywords

DIMER; HETERODIMER; HOMODIMER; PROTEIN; PROTEIN UMUD; UNCLASSIFIED DRUG;

ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA CLEAVAGE; DNA DAMAGE; ESCHERICHIA COLI; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

DNA DAMAGE; DNA, BACTERIAL; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MUTAGENESIS; PROTEIN MULTIMERIZATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84872136749     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2012.11.008     Document Type: Article

References (52)

1. K. Schlacher, and M.F. Goodman Lessons from 50 years of SOS DNA-damage-induced mutagenesis Nat. Rev. Mol. Cell Biol. 8 2007 587 594
2. E.C. Freidberg, G.C. Walker, W. Siede, R.D. Wood, R.A. Schultz, and T. Ellenberger DNA Repair and Mutagenesis 2nd ed. 2005 ASM Press Washington, DC
3. M.D. Sutton, T. Opperman, and G.C. Walker The Eschericia coli SOS mutagenesis proteins UmuD and UmuD′ interact physically with the replicative DNA polymerase Proc. Natl. Acad. Sci. U. S. A. 96 1999 12373 12378
4. H. Shinagawa, H. Iwasaki, T. Kato, and A. Nakata RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis Proc. Natl. Acad. Sci. U. S. A. 85 1988 1806 1810
5. T. Nohmi, J.R. Battista, L.A. Dodson, and G.C. Walker RecA-mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation Proc. Natl. Acad. Sci. U. S. A. 85 1988 1816 1820
6. S.E. Burckhardt, R. Woodgate, R.H. Scheuermann, and H. Echols UmuD mutagenesis protein of Eschericia coli: overproduction, purification, and cleavage by RecA Proc. Natl. Acad. Sci. U. S. A. 85 1988 1811 1815
7. M. Paetzel, and N.C. Strynadka Common protein architecture and binding sites in proteases utilizing a Ser/Lys dyad mechanism Protein Sci. 8 1999 2533 2536
8. J.W. Little Autodigestion of lexA and page λ repressors Proc. Natl. Acad. Sci. U. S. A. 81 1984 1375 1379
9. M. Gonzalez, E.G. Frank, A.S. Levine, and R. Woodgate Lon-mediated proteolysis of the Escherichia coli UmuD mutagenesis protein: in vitro degradation and identification of residues required for proteolysis Genes Dev. 12 1998 3889 3899
10. J.P. McDonald, E.G. Frank, A.S. Levine, and R. Woodgate Intermolecular cleavage by UmuD-like mutagenesis proteins Proc. Natl. Acad. Sci. U. S. A. 95 1998 1478 1483
11. J.N. Ollivierre, J.L. Sikora, and P.J. Beuning The dimeric SOS mutagenesis protein UmuD is active as a monomer J. Biol. Chem. 286 2011 3607 3617
12. P.J. Beuning, S.M. Simon, A. Zemla, D. Barsky, and G.C. Walker A non-cleavable UmuD variant that acts as a UmuD′ mimic J. Biol. Chem. 281 2006 9633 9640
13. A. Guzzo, M.H. Lee, K. Oda, and G.C. Walker Analysis of the region between amino acids 30 and 42 of intact UmuD by a monocysteine approach J. Bacteriol. 178 1996 7295 7303
14. T. Ohta, M.D. Sutton, A. Guzzo, S. Cole, A.E. Ferentz, and G.C. Walker Mutations affecting the ability of the Escherichia coli UmuD′ protein to participate in SOS mutagenesis J. Bacteriol. 181 1999 177 185
15. J.N. Ollivierre, J. Fang, and P.J. Beuning The roles of UmuD in regulating mutagenesis J. Nucleic Acids 947680 2010 12 (Article ID)
16. 2 protein DNA Repair (Amst) 1 2002 77 93
17. A.E. Ferentz, T. Opperman, G.C. Walker, and G. Wagner Dimerization of the UmuD′ protein in solution and its implications for regulation of SOS mutagenesis Nat. Struct. Biol. 4 1997 979 983
18. A.E. Ferentz, G.C. Walker, and G. Wagner Converting a DNA damage checkpoint effector (UmuD2C) into a lesion bypass polymerase (UmuD′2C) EMBO J. 20 2001 4287 4298
19. T.S. Peat, E.G. Frank, J.P. McDonald, A.S. Levine, R. Woodgate, and W.A. Hendrickson The UmuD′ protein filament and its potential role in damage induced mutagenesis Structure 4 1996 1401 1412
20. S.M. Simon, F.J. Sousa, R. Mohana-Borges, and G.C. Walker Regulation of Escherichia coli SOS mutagenesis by dimeric intrinsically disordered umuD gene products Proc. Natl. Acad. Sci. U. S. A. 105 2008 1152 1157
21. T.S. Peat, E.G. Frank, J.P. McDonald, A.S. Levine, R. Woodgate, and W.A. Hendrickson Structure of the UmuD′ protein and its regulation in response to DNA damage Nature 380 1996 727 730
22. J.N. Ollivierre, D.E. Budil, and P.J. Beuning Electron spin labeling reveals the highly dynamic N-terminal arms of the SOS mutagenesis protein UmuD Mol. Biosyst. 7 2011 3183 3186
23. J. Fang, K.D. Rand, M.C. Silva, T.E. Wales, J.R. Engen, and P.J. Beuning Conformational dynamics of the Escherichia coli DNA polymerase manager proteins UmuD and UmuD′ J. Mol. Biol. 398 2010 40 53
24. J.R. Battista, T. Ohta, T. Nohmi, W. Sun, and G.C. Walker Dominant negative umuD mutations decreasing RecA-mediated cleavage suggest roles for intact UmuD in modulation of SOS mutagenesis Proc. Natl. Acad. Sci. U. S. A. 87 1990 7190 7194
25. M.D. Sutton, I. Narumi, and G.C. Walker Posttranslational modification of the umuD-encoded subunit of Escherichia coli DNA polymerase V regulates its interactions with the beta processivity clamp Proc. Natl. Acad. Sci. U. S. A. 99 2002 5307 5312
26. V.G. Godoy, D.F. Jarosz, S.M. Simon, A. Abyzov, V. Ilyin, and G.C. Walker UmuD and RecA directly modulate the mutagenic potential of the Y family DNA polymerase DinB Mol. Cell 28 2007 1058 1070
27. S.B. Neher, R.T. Sauer, and T.A. Baker Distinct peptide signals in the UmuD and UmuD′ subunits of UmuD/D′ mediate tethering and substrate processing by the ClpXP protease Proc. Natl. Acad. Sci. U. S. A. 100 2003 13219 13224
28. N.B. Reuven, G. Arad, A. Maor-Shoshani, and Z. Livneh The mutagenesis protein UmuC is a DNA polymerase activated by UmuD′, RecA, and SSB, and is specialized for translesion replication J. Biol. Chem. 274 1999 31763 31766
29. M. Tang, X. Shen, E. Frank, M. O'Donnell, R. Woodgate, and M. Goodman UmuD′(2)C is an error-prone DNA polymerase, Escherichia coli pol V Proc. Natl. Acad. Sci. U. S. A. 96 1999 8919 8924
30. T. Opperman, S. Murli, B.T. Smith, and G.C. Walker A model for a UmuDC-dependent prokaryotic DNA damage checkpoint Proc. Natl. Acad. Sci. U. S. A. 96 1999 9218 9223
31. M.D. Sutton, and G.C. Walker umuDC-mediated cold sensitivity is a manifestation of functions of the UmuD(2)C complex involved in a DNA damage checkpoint control J. Bacteriol. 183 2001 1215 1224
32. X. Shen, R. Woodgate, and M.F. Goodman Escherichia coli DNA polymerase V subunit exchange: a post-SOS mechanism to curtail error-prone DNA synthesis J. Biol. Chem. 278 2003 52546 52550
33. E.G. Frank, D.G. Ennis, M. Gonzalez, A.S. Levine, and R. Woodgate Regulation of SOS mutagenesis by proteolysis Proc. Natl. Acad. Sci. U. S. A. 93 1996 10291 10296
34. S. Sommer, A. Bailone, and R. Devoret The appearance of the UmuD′C protein complex in Escherichia coli switches repair from homologous recombination to SOS mutagenesis Mol. Microbiol. 10 1993 963 971
35. H. Szpilewska, P. Bertrand, A. Bailone, and M. Dutreix In vitro inhibition of RecA-mediated homologous pairing by UmuD′C proteins Biochimie 77 1995 848 853
36. M. Gonzalez, E.G. Frank, J.P. McDonald, A.S. Levine, and R. Woodgate Structural insights into the regulation of SOS mutagenesis Acta Biochim. Pol. 45 1998 163 172
37. M. Gonzalez, F. Rasulova, M.R. Maurizi, and R. Woodgate Subunit-specific degradation of the UmuD/D′ heterodimer by the ClpXP protease: the role of trans recognition in UmuD′ stability EMBO J. 19 2000 5251 5258
38. P.J. Beuning, S.M. Simon, V.G. Godoy, D.F. Jarosz, and G.C. Walker Characterization of Escherichia coli translesion synthesis polymerases and their accessory factors Methods Enzymol. 408 2006 318 340
39. P.J. Beuning, S. Chan, L.S. Waters, H. Addepalli, J.N. Ollivierre, and G.C. Walker Characterization of novel alleles of the Escherichia coli umuDC genes identifies additional interaction sites of UmuC with the beta clamp J. Bacteriol. 191 2009 5910 5920
40. S.F. Singleton, R.A. Simonette, N.C. Sharma, and A.I. Roca Intein-mediated affinity-fusion purification of the Escherichia coli RecA protein Protein Expr. Purif. 26 2002 476 488
41. S. Sommer, J. Knezevic, A. Bailone, and R. Devoret Induction of only one SOS operon, umuDC, is required for SOS mutagenesis in Escherichia coli Mol. Gen. Genet. 239 1993 137 144
42. J.A. Goodrich, and J.F. Kugel Binding and Kinetics for Molecular Biologists 2007 CSHL Press Cold Spring Harbor, NY
43. M.H. Lee, T. Ohta, and G.C. Walker A monocysteine approach for probing the structure and interactions of the UmuD protein J. Bacteriol. 176 1994 4825 4837
44. J.P. McDonald, E.E. Maury, A.S. Levine, and R. Woodgate Regulation of UmuD cleavage: role of the amino-terminal tail J. Mol. Biol. 282 1998 721 730
45. M.H. Lee, A. Guzzo, and G.C. Walker Inhibition of RecA-mediated cleavage in covalent dimers of UmuD J. Bacteriol. 178 1996 7304 7307
46. M.D. Sutton, and J.M. Duzen Specific amino acid residues in the beta sliding clamp establish a DNA polymerase usage hierarchy in Escherichia coli DNA Repair (Amst) 5 2006 312 323
47. R. Woodgate, and D.G. Ennis Levels of chromosomally encoded Umu proteins and requirements for in vivo UmuD cleavage Mol. Gen. Genet. 229 1991 10 16
48. U.B. Ericsson, B.M. Hallberg, G.T. Detitta, N. Dekker, and P. Nordlund Thermofluor-based high-throughput stability optimization of proteins for structural studies Anal. Biochem. 357 2006 289 298
49. J. Cairns, and P.L. Foster Adaptive reversion of a frameshift mutation in Escherichia coli Genetics 128 1991 695 701
50. N. Friedman, S. Vardi, M. Ronen, U. Alon, and J. Stavans Precise temporal modulation in the response of the SOS DNA repair network in individual bacteria PLoS Biol. 3 2005 e238
51. T. Baba, T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K.A. Datsenko, M. Tomita, B.L. Wanner, and H. Mori Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection Mol. Syst. Biol. 2 2006 (2006.0008)
52. G. Churchward, D. Belin, and Y. Nagamine A pSC101-derived plasmid which shows no sequence homology to other commonly used cloning vectors Gene 31 1984 165 171