PolA1, a putative DNA polymerase I, is coexpressed with perr and contributes to peroxide stress defenses of group A Streptococcus

Journal of Bacteriology

Volumn 195, Issue 4, 2013, Pages 717-725

  Toukoki, Chadia ^a,b   Gryllos, Ioannis ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CIPROFLOXACIN; DNA DIRECTED DNA POLYMERASE BETA; HYDROXYL RADICAL; PEROXIDE; RIFAMPICIN;

ADAPTATION; ARTICLE; BACTERIAL GENETICS; BACTERIAL SURVIVAL; CHROMOSOME DELETION; CONTROLLED STUDY; DELETION MUTANT; DNA DAMAGE; DNA REPAIR; MUTAGENESIS; NONHUMAN; OPEN READING FRAME; OPERON; OXIDATIVE STRESS; PRIORITY JOURNAL; STREPTOCOCCUS GROUP A; STRESS; ULTRAVIOLET RADIATION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CIPROFLOXACIN; DNA DAMAGE; DNA POLYMERASE I; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC VARIATION; GENOME, BACTERIAL; HYDROGEN PEROXIDE; MUTATION; NAPHTHOQUINONES; REPRESSOR PROTEINS; RIFAMPIN; STREPTOCOCCUS PYOGENES; ULTRAVIOLET RAYS;

EID: 84873557629     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01847-12     Document Type: Article

References (69)

1. Ding H, Hidalgo E, Demple B. 1996. The redox state of the [2Fe-2S] clusters in SoxR protein regulates its activity as a transcription factor. J. Biol. Chem. 271:33173-33175.
2. Flint DH, Tuminello JF, Emptage MH. 1993. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J. Biol. Chem. 268:22369-22376.
3. Jang S, Imlay JA. 2007. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J. Biol. Chem. 282:929-937.
4. Tokumoto U, Kitamura S, Fukuyama K, Takahashi Y. 2004. Interchangeability and distinct properties of bacterial Fe-S cluster assembly systems: functional replacement of the isc and suf operons in Escherichia coli with the nifSU-like operon from Helicobacter pylori. J. Biochem. 136: 199-209.
5. Outten FW, Djaman O, Storz G. 2004. A suf operon requirement for Fe-S cluster assembly during iron starvation in Escherichia coli. Mol. Microbiol. 52:861-872.
6. Anbar M, Neta P. 1967. A compilation of specific bimolecular rate constants for the reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals with inorganic and organic compounds in aqueous solution. Int. J. Appl. Radiat. Isot. 18:493-523.
7. Imlay JA, Chin SM, Linn S. 1988. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240: 640-642.
8. Maki H, Sekiguchi M. 1992. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355:273-275.
9. Michaels ML, Cruz C, Grollman AP, Miller JH. 1992. Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Proc. Natl. Acad. Sci. U. S. A. 89:7022-7025.
10. Lin JJ, Sancar A. 1989. A new mechanism for repairing oxidative damage to DNA: (A)BC excinuclease removes AP sites and thymine glycols from DNA. Biochemistry 28:7979-7984.
11. Snowden A, Kow YW, Van Houten B. 1990. Damage repertoire of the Escherichia coli UvrABC nuclease complex includes abasic sites, basedamage analogues, and lesions containing adjacent 5' or 3' nicks. Biochemistry 29:7251-7259.
12. Au N, Kuester-Schoeck E, Mandava V, Bothwell LE, Canny SP, Chachu K, Colavito SA, Fuller SN, Groban ES, Hensley LA, O'Brien TC, Shah A, Tierney JT, Tomm LL, O'Gara TM, Goranov AI, Grossman AD, Lovett CM. 2005. Genetic composition of the Bacillus subtilis SOS system. J. Bacteriol. 187:7655-7666.
13. Little JW, Mount DW. 1982. The SOS regulatory system of Escherichia coli. Cell 29:11-22.
14. Little JW. 1983. The SOS regulatory system: control of its state by the level of RecA protease. J. Mol. Biol. 167:791-808.
15. Anjem A, Varghese S, Imlay JA. 2009. Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol. Microbiol. 72:844-858.
16. Chen L, Keramati L, Helmann JD. 1995. Coordinate regulation of Bacillus subtilis peroxide stress genes by hydrogen peroxide and metal ions. Proc. Natl. Acad. Sci. U. S. A. 92:8190-8194.
17. Horsburgh MJ, Clements MO, Crossley H, Ingham E, Foster SJ. 2001. PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect. Immun. 69:3744-3754.
18. Tsou CC, Chiang-Ni C, Lin YS, Chuang WJ, Lin MT, Liu CC, Wu JJ. 2008. An iron-binding protein, Dpr, decreases hydrogen peroxide stress and protects Streptococcus pyogenes against multiple stresses. Infect. Immun. 76:4038-4045.
19. Bsat N, Herbig A, Casillas-Martinez L, Setlow P, Helmann JD. 1998. Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol. Microbiol. 29:189-198.
20. Helmann JD, Wu MF, Gaballa A, Kobel PA, Morshedi MM, Fawcett P, Paddon C. 2003. The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J. Bacteriol. 185:243-253.
21. Lee JW, Helmann JD. 2006. The PerR transcription factor sensesH2O2 by metal-catalysed histidine oxidation. Nature 440:363-367.
22. Grifantini R, Toukoki C, Colaprico A, Gryllos I. 2011. Peroxide stimulon and role of PerR in group A Streptococcus. J. Bacteriol. 193: 6539 - 6551.
23. Brenot A, Weston BF, Caparon MG. 2007. A PerR-regulated metal transporter (PmtA) is an interface between oxidative stress and metal homeostasis in Streptococcus pyogenes. Mol. Microbiol. 63:1185-1196.
24. Gryllos I, Grifantini R, Colaprico A, Cary ME, Hakansson A, Carey DW, Suarez-Chavez M, Kalish LA, Mitchell PD, White GL, Wessels MR. 2008. PerR confers phagocytic killing resistance and allows pharyngeal colonization by group A Streptococcus. PLoS Pathog. 4:e1000145. doi: 10.1371/journal.ppat.1000145.
25. 2+ signalling defines the group A streptococcal CsrRS (CovRS) regulon. Mol. Microbiol. 65:671-683.
26. 2+. Proc. Natl. Acad. Sci. U. S. A. 100:4227-4232.
27. Beres SB, Sylva GL, Barbian KD, Lei B, Hoff JS, Mammarella ND, Liu MY, Smoot JC, Porcella SF, Parkins LD, Campbell DS, Smith TM, McCormick JK, Leung DY, Schlievert PM, Musser JM. 2002. Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc. Natl. Acad. Sci. U. S. A. 99:10078-10083.
28. Sabelnikov AG, Greenberg B, Lacks SA. 1995. An extended -10 promoter alone directs transcription of the DpnII operon of Streptococcus pneumoniae. J. Mol. Biol. 250:144-155.
29. Kanehisa M, Goto S. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28:27-30.
30. Letunic I, Doerks T, Bork P. 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40:D302-D305.
31. Schultz J, Milpetz F, Bork P, Ponting CP. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U. S. A. 95:5857-5864.
32. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
33. Diaz A, Lacks SA, Lopez P. 1992. The 5' to 3' exonuclease activity of DNA polymerase I is essential for Streptococcus pneumoniae. Mol. Microbiol. 6:3009-3019.
34. Holtmann G, Bremer E. 2004. Thermoprotection of Bacillus subtilis by exogenously provided glycine betaine and structurally related compatible solutes: involvement of Opu transporters. J. Bacteriol. 186: 1683-1693.
35. van der Heide T, Poolman B. 2000. Osmoregulated ABC-transport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane. Proc. Natl. Acad. Sci. U. S. A. 97:7102-7106.
36. Delarue M, Poch O, Tordo N, Moras D, Argos P. 1990. An attempt to unify the structure of polymerases. Protein Eng. 3:461-467.
37. Patel PH, Suzuki M, Adman E, Shinkai A, Loeb LA. 2001. Prokaryotic DNA polymerase I: evolution, structure, and "base flipping" mechanism for nucleotide selection. J. Mol. Biol. 308:823-837.
38. Chen CR, Malik M, Snyder M, Drlica K. 1996. DNA gyrase and topoisomerase IV on the bacterial chromosome: quinolone-induced DNA cleavage. J. Mol. Biol. 258:627-637.
39. King KY, Horenstein JA, Caparon MG. 2000. Aerotolerance and peroxide resistance in peroxidase and PerR mutants of Streptococcus pyogenes. J. Bacteriol. 182:5290-5299.
40. Ricci S, Janulczyk R, Bjorck L. 2002. The regulator PerR is involved in oxidative stress response and iron homeostasis and is necessary for full virulence of Streptococcus pyogenes. Infect. Immun. 70:4968-4976.
41. Pulliainen AT, Hytonen J, Haataja S, Finne J. 2008. Deficiency of the Rgg regulator promotes H2O2 resistance, AhpCF-mediated H2O2 decomposition, and virulence in Streptococcus pyogenes. J. Bacteriol. 190: 3225-3235.
42. Touati D, Jacques M, Tardat B, Bouchard L, Despied S. 1995. Lethal oxidative damage and mutagenesis are generated by iron in delta fur mutants of Escherichia coli: protective role of superoxide dismutase. J. Bacteriol. 177:2305-2314.
43. Amblar M, de Lacoba MG, Corrales MA, Lopez P. 2001. Biochemical analysis of point mutations in the 5=-3= exonuclease of DNA polymerase I of Streptococcus pneumoniae. Functional and structural implications. J. Biol. Chem. 276:19172-19181.
44. Xu Y, Derbyshire V, Ng K, Sun XC, Grindley ND, Joyce CM. 1997. Biochemical and mutational studies of the 5'-3' exonuclease of DNA polymerase I of Escherichia coli. J. Mol. Biol. 268:284-302.
45. Lopez de Saro FJ, O'Donnell M. 2001. Interaction of the beta sliding clamp with MutS, ligase, and DNA polymerase I. Proc. Natl. Acad. Sci. U. S. A. 98:8376-8380.
46. Tamanoi F, Okazaki T, Okazaki R. 1977. Persistence of RNA attached to nascent short DNA pieces in Bacillus subtilis cells defective in DNA polymerase I. Biochem. Biophys. Res. Commun. 77:290-297.
47. Derbyshire V, Grindley ND, Joyce CM. 1991. The 3'-5' exonuclease of DNA polymerase I of Escherichia coli: contribution of each amino acid at the active site to the reaction. EMBO J. 10:17-24.
48. Caron PR, Kushner SR, Grossman L. 1985. Involvement of helicase II (uvrD gene product) and DNA polymerase I in excision mediated by the uvrABC protein complex. Proc. Natl. Acad. Sci. U. S. A. 82:4925-4929.
49. Imlay JA, Linn S. 1986. Bimodal pattern of killing of DNA-repairdefective or anoxically grown Escherichia coli by hydrogen peroxide. J. Bacteriol. 166:519-527.
50. Kuzminov A. 1999. Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol. Mol. Biol. Rev. 63:751-813.
51. Barfknecht TR, Smith KC. 1978. The involvement of DNA polymerase I in the postreplication repair of ultraviolet radiation-induced damage in Escherichia coli K-12. Mol. Gen. Genet. 167:37-41.
52. Ennis DG, Amundsen SK, Smith GR. 1987. Genetic functions promoting homologous recombination in Escherichia coli: a study of inversions in phage lambda. Genetics 115:11-24.
53. Bruck I, O'Donnell M. 2000. The DNA replication machine of a grampositive organism. J. Biol. Chem. 275:28971-28983.
54. Sanders GM, Dallmann HG, McHenry CS. 2010. Reconstitution of the B. subtilis replisome with 13 proteins including two distinct replicases. Mol. Cell 37:273-281.
55. Bruck I, Goodman MF, O'Donnell M. 2003. The essential C family DnaE polymerase is error-prone and efficient at lesion bypass. J. Biol. Chem. 278:44361-44368.
56. Bloom LB, Chen X, Fygenson DK, Turner J, O'Donnell M, Goodman MF. 1997. Fidelity of Escherichia coli DNA polymerase III holoenzyme. The effects of beta, gamma complex processivity proteins and epsilon proofreading exonuclease on nucleotide misincorporation efficiencies. J. Biol. Chem. 272:27919-27930.
57. Tippin B, Pham P, Goodman MF. 2004. Error-prone replication for better or worse. Trends Microbiol. 12:288-295.
58. 2Cis an error-proneDNApolymerase, Escherichia coli pol V. Proc. Natl. Acad. Sci. U. S. A. 96:8919-8924.
59. Wagner J, Gruz P, Kim SR, Yamada M, Matsui K, Fuchs RP, Nohmi T. 1999. The dinB gene encodes a novel E. coliDNApolymerase, DNApol IV, involved in mutagenesis. Mol. Cell 4:281-286.
60. Ohmori H, Friedberg EC, Fuchs RP, Goodman MF, Hanaoka F, Hinkle D, Kunkel TA, Lawrence CW, Livneh Z, Nohmi T, Prakash L, Prakash S, Todo T, Walker GC, Wang Z, Woodgate R. 2001. The Y-family of DNA polymerases. Mol. Cell 8:7-8.
61. Tang M, Pham P, Shen X, Taylor JS, O'Donnell M, Woodgate R, Goodman F. 2000. Roles of E. coli DNA polymerases IV and V in lesiontargeted and untargeted SOS mutagenesis. Nature 404:1014-1018.
62. Sung HM, Yeamans G, Ross CA, Yasbin RE. 2003. Roles of YqjH and YqjW, homologs of the Escherichia coli UmuC/DinB or Y superfamily of DNApolymerases, in stationary-phase mutagenesis and UV-induced mutagenesis of Bacillus subtilis. J. Bacteriol. 185:2153-2160.
63. Duigou S, Ehrlich SD, Noirot P, Noirot-Gros MF. 2004. Distinctive genetic features exhibited by the Y-family DNA polymerases in Bacillus subtilis. Mol. Microbiol. 54:439-451.
64. Duigou S, Ehrlich SD, Noirot P, Noirot-Gros MF. 2005. DNA polymerase I acts in translesion synthesis mediated by the Y-polymerases in Bacillus subtilis. Mol. Microbiol. 57:678-690.
65. Varhimo E, Savijoki K, Jalava J, Kuipers OP, Varmanen P. 2007. Identification of a novel streptococcal gene cassette mediating SOS mutagenesis in Streptococcus uberis. J. Bacteriol. 189:5210-5222.
66. Rand L, Hinds J, Springer B, Sander P, Buxton RS, Davis EO. 2003. The majority of inducible DNA repair genes in Mycobacterium tuberculosis are induced independently of RecA. Mol. Microbiol. 50:1031-1042.
67. Boshoff HI, Reed MB, CEBarry, III, Mizrahi V. 2003. DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance in Mycobacterium tuberculosis. Cell 113:183-193.
68. Le Chatelier E, Becherel OJ, D'Alencon E, Canceill D, Ehrlich SD, Fuchs RP, Janniere L. 2004. Involvement of DnaE, the second replicative DNA polymerase from Bacillus subtilis, in DNA mutagenesis. J. Biol. Chem. 279:1757-1767.
69. Brenot A, King KY, Caparon MG. 2005. The PerR regulon in peroxide resistance and virulence of Streptococcus pyogenes. Mol. Microbiol. 55: 221-234.