A RecA Protein Surface Required for Activation of DNA Polymerase V

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Gruber, Angela J ^a   Erdem, Aysen L ^b   Sabat, Grzegorz ^a   Karata, Kiyonobu ^c   Jaszczur, Malgorzata M ^b   Vo, Dan D ^b   Olsen, Tayla M ^a   Woodgate, Roger ^c   Goodman, Myron F ^b   Cox, Michael M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DNA POLYMERASE V; PARA BENZOYL PHENYLALANINE; PHENYLALANINE; RECA PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; DNA DIRECTED DNA POLYMERASE; DNA POLYMERASE V, E COLI; ESCHERICHIA COLI PROTEIN; NUCLEOPROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR INTERACTION; MUTAGENESIS; MUTATIONAL ANALYSIS; PHARMACOLOGICAL BLOCKING; PROTEIN CROSS LINKING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; RESIDUE ANALYSIS; STRUCTURE ANALYSIS; SURFACE PROPERTY; AMINO ACID SEQUENCE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ESCHERICHIA COLI; GENETICS; METABOLISM; MUTATION; TRANSCRIPTION INITIATION;

ESCHERICHIA COLI;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; DNA DAMAGE; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTAGENESIS; MUTATION; NUCLEOPROTEINS; REC A RECOMBINASES; SOS RESPONSE (GENETICS); TRANSCRIPTIONAL ACTIVATION;

EID: 84926326430     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005066     Document Type: Article

References (97)

1. Cox MM, Higgins NP, (2004) The RecA Protein. In: The Bacterial Chromosome. Washington, D. C.: American Society of Microbiology. pp. 369–388.
2. Cox MM, Rothstein R, Aguilera A, (2007) The bacterial RecA protein: structure, function, and regulation. In: Topics in Current Genetics: Molecular Genetics of Recombination. Heidelberg: Springer-Verlag. pp. 53–94.
3. Lusetti SL, Cox MM, (2002) The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu Rev Biochem 71: 71–100. 12045091
4. Arenson TA, Tsodikov OV, Cox MM, (1999) Quantitative analysis of the kinetics of end-dependent disassembly of RecA filaments from ssDNA. J Mol Biol 288: 391–401. 10329149
5. Bork JM, Cox MM, Inman RB, (2001) RecA protein filaments disassemble in the 5' to 3' direction on single-stranded DNA. J Biol Chem 276: 45740–45743. 11574550
6. Cox MM, Lehman IR, (1981) Directionality and polarity in RecA protein-promoted branch migration. Proc Natl Acad Sci USA 78: 6018–6022. 6273839
7. Cox JM, Tsodikov OV, Cox MM, (2005) Organized unidirectional waves of ATP hydrolysis within a RecA filament. PLoS Biol 3: 231–243.
8. Lindsley JE, Cox MM, (1990) Assembly and disassembly of RecA protein filaments occurs at opposite filament ends: relationship to DNA strand exchange. J Biol Chem 265: 9043–9054. 2188972
9. Register JC, IIIGriffith J, (1985) The direction of RecA protein assembly onto single strand DNA is the same as the direction of strand assimilation during strand exchange. J Biol Chem 260: 12308–12312. 3900072
10. Bell JC, Plank JL, Dombrowski CC, Kowalczykowski SC, (2012) Direct imaging of RecA nucleation and growth on single molecules of SSB-coated ssDNA. Nature 491: 274–U144. doi: 10.1038/nature11598 23103864
11. Kim B, Little JW, (1993) LexA and lambda Cl repressors as enzymes: specific cleavage in an intermolecular reaction. Cell 73: 1165–1173. 8513500
12. Little JW, (1991) Mechanism of specific LexA cleavage—autodigestion and the role of RecA coprotease. Biochimie 73: 411–422. 1911941
13. Shinagawa H, (1996) SOS response as an adaptive response to DNA damage in prokaryotes. Exs 77: 221–235. 8856977
14. Burckhardt SE, Woodgate R, Scheuermann RH, Echols H, (1988) UmuD mutagenesis protein of Escherichia coli: overproduction, purification, and cleavage by RecA. Proc Natl Acad Sci USA 85: 1811–1815. 3279417
15. Nohmi T, Battista JR, Dodson LA, Walker GC, (1988) RecA-mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation. Proc Natl Acad Sci USA 85: 1816–1820. 3279418
16. Shinagawa H, Iwasaki H, Kato T, Nakata A, (1988) RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis. Proc Natl Acad Sci USA 85: 1806–1810. 3126496
17. Jiang Q, Karata K, Woodgate R, Cox MM, Goodman MF, (2009) The active form of DNA polymerase V is UmuD′2C•RecA•ATP. Nature 460: 359–363. doi: 10.1038/nature08178 19606142
18. Janion C, (2008) Inducible SOS response system of DNA repair and mutagenesis in Escherichia coli. Int J Biol Sci 4: 338–344. 18825275
19. Bridges BA, (2005) Error-prone DNA repair and translesion DNA synthesis. II: The inducible SOS hypothesis. DNA Repair (Amst) 4: 725–726, 739. 15907776
20. McCool JD, Long E, Petrosino JF, Sandler HA, Rosenberg SM, et al. (2004) Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Mol Microbiol 53: 1343–1357. 15387814
21. Sutton MD, Smith BT, Godoy VG, Walker GC, (2000) The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu Rev Genet 34: 479–497. 11092836
22. Walker GC, Smith BT, Sutton MD, Storz G, HenggeAronis R, (2000) The SOS response to DNA damage. In: Bacterial Stress Responses. Washington, D.C.: American Society of Microbiology. pp. 131–144.
23. Friedman N, Vardi S, Ronen M, Alon U, Stavans J, (2005) Precise temporal modulation in the response of the SOS DNA repair network in individual bacteria. PLoS Biol 3: 1261–1268.
24. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC, (2001) Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158: 41–64. 11333217
25. Fernandez De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, et al. (2000) Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol 35: 1560–1572. 10760155
26. Bridges BA, (1999) DNA repair: Polymerases for passing lesions. Curr Biol 9: R475–477. 10395530
27. Delmas S, Matic I, (2006) Interplay between replication and recombination in Escherichia coli: Impact of the alternative DNA polymerases. Proc Natl Acad Sci USA 103: 4564–4569. 16537389
28. Friedberg EC, Fischhaber PL, Kisker C, (2001) Error-prone DNA polymerases: novel structures and the benefits of infidelity. Cell 107: 9–12. 11595180
29. Friedberg EC, Wagner R, Radman M, (2002) Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science 296: 1627–1630. 12040171
30. Friedberg EC, (2005) Suffering in silence: The tolerance of DNA damage. Nature Rev Mol Cell Biol 6: 943–953. 16341080
31. Hubscher U, Nasheuer HP, Syvaoja JE, (2000) Eukaryotic DNA polymerases, a growing family. Trends Biochem Sci 25: 143–147. 10694886
32. Livneh Z, (2001) DNA damage control by novel DNA polymerases: Translesion replication and mutagenesis. J Biol Chem 276: 25639–25642. 11371576
33. Patel M, Jiang QF, Woodgate R, Cox MM, Goodman MF, (2010) A new model for SOS-induced mutagenesis: how RecA protein activates DNA polymerase V. Crit Rev Biochem Mol Biol 45: 171–184. doi: 10.3109/10409238.2010.480968 20441441
34. Ramadan K, Shevelev I, Hubscher U, (2004) The DNA-polymerase-X family: controllers of DNA quality? Nature Rev Mol Cell Biol 5: 1038–1043. 15573140
35. Schlacher K, Pham P, Cox MM, Goodman MF, (2006) Roles of DNA polymerase V and RecA protein in SOS damage-induced mutation. Chem Rev 106: 406–419. 16464012
36. Vaisman A, Lehmann AR, Woodgate R, (2004) DNA polymerases eta and iota. DNA Repair Replicat 69: 205–228.
37. Yang W, (2003) Damage repair DNA polymerases Y. Curr Opin Struct Biol 13: 23–30. 12581656
38. Maor-Shoshani A, Reuven NB, Tomer G, Livneh Z, (2000) Highly mutagenic replication by DNA polymerase V (UmuC) provides a mechanistic basis for SOS untargeted mutagenesis. Proc Natl Acad Sci USA 97: 565–570. 10639119
39. Pham P, Bertram JG, O'Donnell M, Woodgate R, Goodman MF, (2001) A model for SOS-lesion-targeted mutations in Escherichia coli involving pol V, RecA, SSB, and β-sliding clamp. Nature 409: 366–370. 11201748
40. Pham P, Rangarajan S, Woodgate R, Goodman MF, (2001) Roles of DNA polymerases V and II in SOS-induced error-prone and error-free repair in Escherichia coli. Proc Natl Acad Sci USA 98: 8350–8354. 11459974
41. Walker GC, (1995) SOS-regulated proteins in translesion DNA synthesis and mutagenesis. Trends Biochem Sci 20: 416–420. 8533155
42. Bruck I, Woodgate R, McEntee K, Goodman MF, (1996) Purification of a soluble UmuD'C complex from Escherichia coli—Cooperative binding of UmuD'C to single-stranded DNA. J Biol Chem 271: 10767–10774. 8631887
43. Karata K, Vaisman A, Goodman MF, Woodgate R, (2012) Simple and efficient purification of Escherichia coli DNA polymerase V: Cofactor requirements for optimal activity and processivity in vitro. DNA Repair 11: 431–440. doi: 10.1016/j.dnarep.2012.01.012 22341652
44. Tang MJ, Bruck I, Eritja R, Turner J, Frank EG, et al. (1998) Biochemical basis of SOS-induced mutagenesis in Escherichia coli: Reconstitution of in vitro lesion bypass dependent on the UmuD′2C mutagenic complex and RecA protein. Proc Natl Acad Sci USA 95: 9755–9760. 9707548
45. Tang MJ, Shen X, Frank EG, O'Donnell M, Woodgate R, et al. (1999) UmuD′2C is an error-prone DNA polymerase, Escherichia coli pol V. Proc Natl Acad Sci USA 96: 8919–8924. 10430871
46. Erdem AL, Jaszczur M, Bertram JG, Woodgate R, Cox MM, et al. (2014) DNA polymerase V activity is autoregulated by a novel intrinsic DNA-dependent ATPase. eLife 3: e02384. doi: 10.7554/eLife.02384 24843026
47. Lawrence CW, Borden A, Woodgate R, (1996) Analysis of the mutagenic properties of the UmuDC, MucAB and RumAB proteins, using a site-specific abasic lesion. Mol Gen Genet 251: 493–498. 8709953
48. Kulaeva OI, Wootton JC, Levine AS, Woodgate R, (1995) Characterization of the Umu-complementing operon from R391. J Bacteriol 177: 2737–2743. 7751283
49. Venderbure C, Chastanet A, Boudsocq F, Sommer S, Bailone A, (1999) Inhibition of homologous recombination by the plasmid MucA'B complex. J Bacteriol 181: 1249–1255. 9973352
50. O'Grady PI, Borden A, Vandewiele D, Ozgenc A, Woodgate R, et al. (2000) Intrinsic polymerase activities of UmuD′2C and MucA′2B are responsible for their different mutagenic properties during bypass of a T-T cis-syn cyclobutane dimer. J Bacteriol 182: 2285–2291. 10735873
51. Mead S, Vaisman A, Valjavec-Gratian M, Karata K, Vandewiele D, et al. (2007) Characterization of polV(R391): a Y-family polymerase encoded by rumA'B from the IncJ conjugative transposon, R391. Mol Microbiol 63: 797–810. 17302804
52. Szekeres ES, Woodgate R, Lawrence CW, (1996) Substitution of mucAB or rumAB for umuDC alters the relative frequencies of the two classes of mutations induced by a site-specific T-T cyclobutane dimer and the efficiency of translesion DNA synthesis. J Bacteriol 178: 2559–2563. 8626322
53. Bailone A, Sommer S, Knezevic J, Dutreix M, Devoret R, (1991) A RecA Protein Mutant Deficient in its Interaction with the UmuDC Complex. Biochimie 73: 479–484. 1911948
54. Bailone A, Devoret R, Sommer S (1995) New RecA Mutants Resistant to UmuD'C Proteins. J Cell Biochem: 346–346.
55. Dutreix M, Moreau PL, Bailone A, Galibert F, Battista JR, et al. (1989) New recA mutations that dissociate the various RecA protein activities in Escherichia coli provide evidence for an additional role for RecA protein in UV mutagenesis. J Bacteriol 171: 2415–2423. 2651400
56. Dutreix M, Burnett B, Bailone A, Radding CM, Devoret R, (1992) A partially deficient mutant, recA1730, that fails to form normal nucleoprotein filaments. Mol Gen Genet 232: 489–497. 1534140
57. Sommer S, Boudsocq F, Devoret R, Bailone A, (1998) Specific RecA amino acid changes affect RecA-UmuD'C interaction. Mol Microbiol 28: 281–291. 9622353
58. Sommer S, Coste G, Bailone A, (2000) Specific amino acid changes enhance the anti-recombination activity of the UmuD'C complex. Mol Microbiol 35: 1443–1453. 10760145
59. Sommer S, Becherel OJ, Coste GV, Bailone A, Fuchs RPP, (2003) Altered translesion synthesis in E-coli Pol V mutants selected for increased recombination inhibition. DNA Repair 2: 1361–1369. 14642565
60. Sommer S, Bailone A, Devoret R, (1993) The appearance of the UmuD'C protein complex in Escherichia coli switches repair from homologous recombination to SOS mutagenesis. Mol Microbiol 10: 963–971. 7934872
61. Rehrauer WM, Bruck I, Woodgate R, Goodman MF, Kowalczykowski SC, (1998) Modulation of RecA nucleoprotein function by the mutagenic UmuD'C protein complex. J Biol Chem 273: 32384–32387. 9829966
62. Pham P, Seitz EM, Saveliev S, Shen X, Woodgate R, et al. (2002) Two distinct modes of RecA action are required for DNA polymerase V-catalyzed translesion synthesis. Proc Natl Acad Sci USA 99: 11061–11066. 12177433
63. Schlacher K, Leslie K, Wyman C, Woodgate R, Cox MM, et al. (2005) DNA polymerase V and RecA protein, a minimal mutasome. Mol Cell 17: 561–572. 15721259
64. Schlacher K, Cox MM, Woodgate R, Goodman MF, (2006) RecA acts in trans to allow replication of damaged DNA by DNA polymerase V. Nature 442: 883–887. 16929290
65. Bakhlanova IV, Dudkina AV, Baitin DM, Knight KL, Cox MM, et al. (2010) Modulating cellular recombination potential through alterations in RecA structure and regulation. Mol Microbiol 78: 1523–1538. doi: 10.1111/j.1365-2958.2010.07424.x 21143322
66. Bates H, Bridges BA, (1991) Mutagenic DNA repair in Escherichia coli.19. On the roles of RecA protein in ultraviolet light mutagenesis. Biochimie 73: 485–489. 1911949
67. Chen ZC, Yang HJ, Pavletich NP, (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453: 489–494. doi: 10.1038/nature06971 18497818
68. Tang M, Pham P, Shen X, Taylor JS, O'Donnell M, et al. (2000) Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis. Nature 404: 1014–1018. 10801133
69. Becherel OJ, Fuchs RPP, Wagner J, (2002) Pivotal role of the beta-clamp in translesion DNA synthesis and mutagenesis in E-coli cells. DNA Repair 1: 703–708. 12509274
70. Beuning PJ, Sawicka D, Barsky D, Walker GC, (2006) Two processivity clamp interactions differentially alter the dual activities of UmuC. Mol Microbiol 59: 460–474. 16390442
71. Fujii S, Gasser W, Fuchs RP, (2004) The biochemical requirements of DNA polymerase V-mediated translesion synthesis revisited. J Mol Biol 341: 405–417. 15276832
72. Maor-Shoshani A, Livneh Z, (2002) Analysis of the stimulation of DNA polymerase V of Escherichia coli by processivity proteins. Biochemistry 41: 14438–14446. 12450411
73. Sutton MD, Farrow MF, Burton BM, Walker GC, (2001) Genetic interactions between the Escherichia coli umuDC gene products and the beta processivity clamp of the replicative DNA polymerase. J Bacteriol 183: 2897–2909. 11292811
74. Sutton MD, Narumi I, Walker GC, (2002) 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 USA 99: 5307–5312. 11959982
75. Wang JY, Xie JM, Schultz PG, (2006) A genetically encoded fluorescent amino acid. J Amer Chem Soc 128: 8738–8739.
76. Wang L, Xie J, Schultz PG, (2006) Expanding the genetic code. Annu Rev Biophys Biomol Struct. 35: 225–249. 16689635
77. Chin JW, Martin AB, King DS, Wang L, Schultz PG, (2002) Addition of a photocrosslinking amino acid to the genetic code of Escherichia coli. Proc Natl Acad Sci USA 99: 11020–11024. 12154230
78. Chin JW, Santoro SW, Martin AB, King DS, Wang L, et al. (2002) Addition of p-azido-L-phenylaianine to the genetic code of Escherichia coli. J Amer Chem Soc 124: 9026–9027.
79. Kelley LA, Sternberg MJE, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 4: 363–371. doi: 10.1038/nprot.2009.2 19247286
80. Ling H, Boudsocq F, Woodgate R, Yang W, (2001) Crystal structure of a Y-family DNA polymerase in action: A mechanism for error-prone and lesion-bypass replication. Cell 107: 91–102. 11595188
81. Boudsocq F, Campbell M, Devoret R, Bailone A, (1997) Quantitation of the inhibition of Hfr X F-recombination by the mutagenesis complex UmuD'C. J Mol Biol 270: 201–211. 9236122
82. Boudsocq F, Ling H, Yang W, Woodgate R, (2002) Structure-based interpretation of missense mutations in Y-family DNA polymerases and their implications for polymerase function and lesion bypass. DNA Repair 1: 343–358. 12509239
83. Drees JC, Lusetti SL, Chitteni-Pattu S, Inman RB, Cox MM, (2004) A RecA filament capping mechanism for RecX protein. Mol Cell 15: 789–798. 15350222
84. Senecoff JF, Rossmeissl PJ, Cox MM, (1988) DNA recognition by the FLP recombinasse of the yeast 2-mμ plasmid—a mutational analysis of the FLP binding-site. J Mol Biol 201: 405–421. 3047402
85. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640–6645. 10829079
86. Lohman TM, Overman LB, (1985) Two binding modes in Escherichia coli single strand binding protein-single stranded DNA complexes. Modulation by NaCl concentration. J Biol Chem 260: 3594–3603. 3882711
87. Craig NL, Roberts JW, (1981) Function of nucleoside triphosphate and polynucleotide in Escherichia coli recA protein-directed cleavage of phage lambda repressor. J Biol Chem 256: 8039–8044. 6455420
88. Lohman TM, Green JM, Beyer RS, (1986) Large-scale overproduction and rapid purification of the Escherichia coli ssb gene product. Expression of the ssb gene under l PL control. Biochemistry 25: 21–25. 3006753
89. Ryu YH, Schultz PG, (2006) Efficient incorporation of unnatural amino acids into proteins in Escherichia coli. Nature Methods 3: 263–265. 16554830
90. Ma WT, Sandri GV, Sarkar S, (1992) Analysis of the Luria-Delbruck Distribution using Discrete Convolution Powers. J Appl Prob 29: 255–267.
91. Sarkar S, Ma WT, Sandri GV, (1992) On Fluctuation Analysis—A New, Simple, and Efficient Method for Computing the Expected Number of Mutants. Genetica 85: 173–179. 1624139
92. Hall BM, Ma CX, Liang P, Singh KK, (2009) Fluctuation AnaLysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics 25: 1564–1565. doi: 10.1093/bioinformatics/btp253 19369502
93. Foster PL, Campbell JL, Modrich P, (2006) Methods for determining spontaneous mutation rates. In: DNA Repair, Pt B. pp. 195–213.
94. Opperman T, Murli S, Walker GC, (1996) The genetic requirements for UmuDC-mediated cold sensitivity are distinct from those for SOS mutagenesis. J Bacteriol 178: 4400–4411. 8755866
95. McDonald JP, Maury EE, Levine AS, Woodgate R, (1998) Regulation of UmuD cleavage: Role of the amino-terminal tail. J Mol Biol 282: 721–730. 9743621
96. Miller JH, (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
97. Morrical SW, Lee J, Cox MM, (1986) Continuous association of Escherichia coli single-stranded DNA binding protein with stable complexes of RecA protein and single-stranded DNA. Biochemistry 25: 1482–1494. 2939874