Mechanisms Employed by Escherichia coli to Prevent Ribonucleotide Incorporation into Genomic DNA by Pol V

PLoS Genetics

Volumn 8, Issue 11, 2012, Pages

  McDonald, John P ^a   Vaisman, Alexandra ^a   Kuban, Wojciech ^a   Goodman, Myron F ^b   Woodgate, Roger ^a  

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

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DNA POLYMERASE POL IV; DNA POLYMERASE POL V; GENOMIC DNA; RECA PROTEIN; RIBONUCLEASE H; RIBONUCLEASE HII; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; ESCHERICHIA COLI; EXCISION REPAIR; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MUTAGENESIS; NONHUMAN; NUCLEOTIDE METABOLISM; PHENOTYPE; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; RADIOSENSITIVITY; RIBONUCLEOTIDE INCORPORATION;

DNA REPAIR; DNA, BACTERIAL; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENOME, BACTERIAL; MUTAGENESIS; RIBONUCLEASE H; RIBONUCLEOTIDES; ULTRAVIOLET RAYS;

ESCHERICHIA COLI;

EID: 84870714773     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003030     Document Type: Article

References (62)

1. Vaisman A, McDonald JP, Woodgate R (2012) Translesion DNA Synthesis. In: Böck A, Curtiss R, Kaper JB, Karp PD, Neidhardt FC et al., editors. EcoSal: Escherichia coli and Salmonella: cellular and molecular miology. Washington, DC: American Society for Biology.
2. Cai H, Yu H, McEntee K, Kunkel TA, Goodman MF, (1995) Purification and properties of wild-type and exonuclease-deficient DNA polymerase II from Escherichia coli. J Biol Chem 270: 15327-15335.
3. Becherel OJ, Fuchs RP, (2001) Mechanism of DNA polymerase II-mediated frameshift mutagenesis. Proc Natl Acad Sci U S A 98: 8566-8571.
4. Ohmori H, Hatada E, Qiao Y, Tsuji M, Fukuda R, (1995) dinP, a new gene in Escherichia coli, whose product shows similarities to UmuC and its homologues. Mut Res 347: 1-7.
5. Wagner J, Gruz P, Kim SR, Yamada M, Matsui K, et al. (1999) The dinB gene encodes an novel Escherichia coli DNA polymerase (DNA pol IV) involved in mutagenesis. Mol Cell 4: 281-286.
6. Kato T, Shinoura Y, (1977) Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol Gen Genet 156: 121-131.
7. Jarosz DF, Beuning PJ, Cohen SE, Walker GC, (2007) Y-family DNA polymerases in Escherichia coli. Trends Microbiol 15: 70-77.
8. Schlacher K, Goodman MF, (2007) Lessons from 50 years of SOS DNA-damage-induced mutagenesis. Nat Rev Mol Cell Biol 8: 587-594.
9. Jarosz DF, Godoy VG, Delaney JC, Essigmann JM, Walker GC, (2006) A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature 439: 225-228.
10. Friedberg EC, Walker GC, Siede W, Wood R, Schultz RA, et al. (2006) DNA Repair and Mutagenesis. Washington, DC: ASM Press.
11. Steinborn G, (1978) Uvm mutants of Escherichia coli K12 deficient in UV mutagenesis. I. Isolation of uvm mutants and their phenotypical characterization in DNA repair and mutagenesis. Mol Gen Genet 165: 87-93.
12. Woodgate R, Rajagopalan M, Lu C, Echols H, (1989) UmuC mutagenesis protein of Escherichia coli: purification and interaction with UmuD and UmuD′. Proc Natl Acad Sci U S A 86: 7301-7305.
13. 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 U S A 85: 1816-1820.
14. 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.
15. Sweasy JB, Witkin EM, Sinha N, Roegner-Maniscalco V, (1990) RecA protein of Escherichia coli has a third essential role in SOS mutator activity. J Bacteriol 172: 3030-3036.
16. 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.
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.
18. Tang M, Pham P, Shen X, Taylor J-S, 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.
19. 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 U S A 98: 8350-8354.
20. Vaisman A, Kuban W, McDonald JP, Karata K, Yang W, et al. (2012) Critical amino acids in Escherichis coli responsible for sugar discrimination and base-substitution fidelity. Nucleic Acids Res 40: 6144-6157.
21. Kuban W, Vaisman A, McDonald JP, Karata K, Yang W, et al. (2012) Escherichia coli UmuC active site mutants: effects on translesion DNA synthesis, mutagenesis and cell survival. DNA Repair 11: 726-732.
22. Brown JA, Suo Z, (2011) Unlocking the sugar "steric gate" of DNA polymerases. Biochemistry 50: 1135-1142.
23. Nick McElhinny SA, Watts BE, Kumar D, Watt DL, Lundstrom EB, et al. (2010) Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. Proc Natl Acad Sci U S A 107: 4949-4954.
24. Shen Y, Koh KD, Weiss B, Storici F, (2012) Mispaired rNMPs in DNA are mutagenic and are targets of mismatch repair and RNases H. Nat Struc Mol Biol 19: 98-104.
25. Nick McElhinny SA, Kumar D, Clark AB, Watt DL, Watts BE, et al. (2010) Genome instability due to ribonucleotide incorporation into DNA. Nat Chem Biol 6: 774-781.
26. Lazzaro F, Novarina D, Amara F, Watt DL, Stone JE, et al. (2012) RNase H and postreplication repair protect cells from ribonucleotides incorporated in DNA. Mol Cell 45: 99-110.
27. Kim N, Huang SN, Williams JS, Li YC, Clark AB, et al. (2011) Mutagenic processing of ribonucleotides in DNA by yeast topoisomerase I. Science 332: 1561-1564.
28. Kanaya S, (2009) Ribonuclease H. The FEBS journal 276: 1481.
29. Hollis T, Shaban NM (2011) Structure and functions of RNase H enzymes. In: Nicholson AW, editor. Ribonucleases: Springer. pp. 299-318.
30. Turchi JJ, Huang L, Murante RS, Kim Y, Bambara RA, (1994) Enzymatic completion of mammalian lagging-strand DNA replication. Proc Natl Acad Sci U S A 91: 9803-9807.
31. Goulian M, Richards SH, Heard CJ, Bigsby BM, (1990) Discontinuous DNA synthesis by purified mammalian proteins. J Biol Chem 265: 18461-18471.
32. Rydberg B, Game J, (2002) Excision of misincorporated ribonucleotides in DNA by RNase H (type 2) and FEN-1 in cell-free extracts. Proc Natl Acad Sci USA 99: 16654-16659.
33. Bubeck D, Reijns MA, Graham SC, Astell KR, Jones EY, et al. (2011) PCNA directs type 2 RNase H activity on DNA replication and repair substrates. Nucleic Acids Res 39: 3652-3666.
34. Nick McElhinny SA, Kissling GE, Kunkel TA, (2010) Differential correction of lagging-strand replication errors made by DNA polymerases α and δ. Proc Natl Acad Sci U S A 107: 21070-21075.
35. Clark AB, Lujan SA, Kissling GE, Kunkel TA, (2011) Mismatch repair-independent tandem repeat sequence instability resulting from ribonucleotide incorporation by DNA polymerase ε. DNA Repair 10: 476-482.
36. Itaya M, Omori A, Kanaya S, Crouch RJ, Tanaka T, et al. (1999) Isolation of RNase H genes that are essential for growth of Bacillus subtilis 168. J Bacteriol 181: 2118-2123.
37. Carl PL, Bloom L, Crouch RJ, (1980) Isolation and mapping of a mutation in Escherichia coli with altered levels of ribonuclease H. J Bacteriol 144: 28-35.
38. Itaya M, (1990) Isolation and characterization of a second RNase H (RNase HII) of Escherichia coli K-12 encoded by the rnhB gene. Proc Natl Acad Sci U S A 87: 8587-8591.
39. Asai T, Kogoma T, (1994) D-loops and R-loops: alternative mechanisms for the initiation of chromosome replication in Escherichia coli. J Bacteriol 176: 1807-1812.
40. Fernández 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.
41. Mount DW, (1977) A mutant of Escherichia coli showing constitutive expression of the lysogenic induction and error-prone DNA repair pathways. Proc Natl Acad Sci U S A 74: 300-304.
42. Kim SR, Matsui K, Yamada M, Gruz P, Nohmi T, (2001) Roles of chromosomal and episomal dinB genes encoding DNA pol IV in targeted and untargeted mutagenesis in Escherichia coli. Mol Gen Genomics 266: 207-215.
43. Kuban W, Banach-Orlowska M, Schaaper RM, Jonczyk P, Fijalkowska IJ, (2006) Role of DNA polymerase IV in Escherichia coli SOS mutator activity. J Bacteriol 188: 7977-7980.
44. Welch MM, McHenry CS, (1982) Cloning and identification of the product of the dnaE gene of Escherichia coli. J Bacteriol 152: 351-356.
45. Karata K, Vidal AE, Woodgate R, (2009) Construction of a circular single-stranded DNA template containing a defined lesion. DNA Repair 8: 852-856.
46. Karata K, Vaisman A, Goodman MF, Woodgate R, (2012) Simple and efficient purification of E.coli DNA polymerase V: cofactor requirements for optimal activity and processivity in vitro. DNA Repair 11: 431-440.
47. Woodgate R, Ennis DG, (1991) Levels of chromosomally encoded Umu proteins and requirements for in vivo UmuD cleavage. Mol Gen Genet 229: 10-16.
48. Fijalkowska IJ, Dunn RL, Schaaper RM, (1997) Genetic requirements and mutational specificity of the Escherichia coli SOS mutator activity. J Bacteriol 179: 7435-7445.
49. Vlašić I, Šimatović A, Brčić-Kostić K, (2011) Genetic requirements for high constitutive SOS expression in recA730 mutants of Escherichia coli. J Bacteriol 193: 4643-4651.
50. Qiu J, Qian Y, Frank P, Wintersberger U, Shen B, (1999) Saccharomyces cerevisiae RNase H(35) functions in RNA primer removal during lagging-strand DNA synthesis, most efficiently in cooperation with Rad27 nuclease. Mol Cell Biol 19: 8361-8371.
51. Chen JZ, Qiu J, Shen B, Holmquist GP, (2000) Mutational spectrum analysis of RNase H(35) deficient Saccharomyces cerevisiae using fluorescence-based directed termination PCR. Nucleic Acids Res 28: 3649-3656.
52. Mead S, Vaisman A, Valjavec-Gratian M, Karata K, Vandewiele D, et al. (2007) Characterization of polVR391: a Y-family polymerase encoded by rumA′B from the IncJ conjugative transposon, R391. Mol Microbiol 63: 797-810.
53. Miller JH (1992) A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor, N.Y: Cold Spring Harbor Laboratory Press.
54. Curti E, McDonald JP, Mead S, Woodgate R, (2009) DNA polymerase switching: effects on spontaneous mutagenesis in Escherichia coli. Mol Microbiol 71: 315-331.
55. Itaya M, Crouch RJ, (1991) A combination of RNase H (rnh) and recBCD or sbcB mutations in Escherichia coli K12 adversely affects growth. Mol Gen Genet 227: 424-432.
56. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
57. Churchward G, Belin D, Nagamine Y, (1984) A pSC101-derived plasmid which shows no sequence homology to other commonly used cloning vectors. Gene 31: 165-171.
58. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory.
59. Davis BD, Mingioli ES, (1950) Mutants of Escherichia coli requiring methionine or vitamin B12. J Bacteriol 60: 17-28.
60. Sedgwick SG, Bridges BA, (1972) Survival, mutation and capacity to repair single strand DNA breaks after gamma irradiation in different exr- strains of Escherichia coli. Mol Gen Genet 119: 93-102.
61. Rangarajan S, Woodgate R, Goodman MF, (1999) A phenotype for enigmatic DNA polymerase II: a pivotal role for pol II in replication restart in UV-irradiated Escherichia coli. Proc Natl Acad Sci U S A 96: 9224-9229.
62. Borden A, O'Grady PI, Vandewiele D, Fernández de Henestrosa AR, Lawrence CW, et al. (2002) Escherichia coli DNA polymerase III can replicate efficiently past a T-T cis-syn dimer if DNA polymerase V and the 3′ to 5′ exonuclease proofreading function encoded by dnaQ are inactivated. J Bacteriol 184: 2674-2681.