The Extraintestinal Pathogenic Escherichia coli Factor RqlI Constrains the Genotoxic Effects of the RecQ-Like Helicase RqlH

PLoS Pathogens

Volumn 11, Issue 12, 2015, Pages

  Russell, Colin W ^a   Mulvey, Matthew A ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; OXYGEN; PHOSPHORIBOSYLTRANSFERASE; DNA HELICASE; ESCHERICHIA COLI PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GROWTH; CHROMATIN IMMUNOPRECIPITATION; COLONY FORMING UNIT; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; ESCHERICHIA COLI INFECTION; EXTRAINTESTINAL PATHOGENIC ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENE MUTATION; GENOTOXICITY; GROWTH INHIBITION; KLEBSIELLA OXYTOCA; MOUSE; NONHUMAN; OVERLAPPING GENE; PLASMID; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; REAL TIME POLYMERASE CHAIN REACTION; RECQ LIKE HELICASE RQLH GENE; TRANSPOSON; WESTERN BLOTTING; ZEBRA FISH; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; ESCHERICHIA COLI; FEMALE; GENETICS; IMMUNOPRECIPITATION; METABOLISM; MICROBIOLOGY; POLYMERASE CHAIN REACTION; URINARY TRACT INFECTION;

ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; DNA HELICASES; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FEMALE; IMMUNOPRECIPITATION; MICE; MICE, INBRED BALB C; POLYMERASE CHAIN REACTION; URINARY TRACT INFECTIONS;

EID: 84953270110     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005317     Document Type: Article

References (51)

1. Barber AE, Norton JP, Spivak AM, Mulvey MA, (2013) Urinary tract infections: current and emerging management strategies. Clin Infect Dis 57: 719–724. doi: 10.1093/cid/cit284 23645845
2. Wiles TJ, Kulesus RR, Mulvey MA, (2008) Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol 85: 11–19. doi: 10.1016/j.yexmp.2008.03.007 18482721
3. Foxman B, Barlow R, D'Arcy H, Gillespie B, Sobel JD, (2000) Urinary tract infection: self-reported incidence and associated costs. Ann Epidemiol 10: 509–515. 11118930
4. Foxman B, (2010) The epidemiology of urinary tract infection. Nat Rev Urol 7: 653–660. doi: 10.1038/nrurol.2010.190 21139641
5. Laupland KB, (2013) Incidence of bloodstream infection: a review of population-based studies. Clin Microbiol Infect 19: 492–500. doi: 10.1111/1469-0691.12144 23398633
6. Mylotte JM, Tayara A, Goodnough S, (2002) Epidemiology of bloodstream infection in nursing home residents: evaluation in a large cohort from multiple homes. Clin Infect Dis 35: 1484–1490. 12471567
7. Siegman-Igra Y, Fourer B, Orni-Wasserlauf R, Golan Y, Noy A, et al. (2002) Reappraisal of community-acquired bacteremia: a proposal of a new classification for the spectrum of acquisition of bacteremia. Clin Infect Dis 34: 1431–1439. 12015688
8. Hilali F, Ruimy R, Saulnier P, Barnabe C, Lebouguenec C, et al. (2000) Prevalence of virulence genes and clonality in Escherichia coli strains that cause bacteremia in cancer patients. Infect Immun 68: 3983–3989. 10858212
9. Simonsen KA, Anderson-Berry AL, Delair SF, Davies HD, (2014) Early-onset neonatal sepsis. Clin Microbiol Rev 27: 21–47. doi: 10.1128/CMR.00031-13 24396135
10. Nicolas-Chanoine MH, Bertrand X, Madec JY, (2014) Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 27: 543–574. doi: 10.1128/CMR.00125-13 24982321
11. Salipante SJ, Roach DJ, Kitzman JO, Snyder MW, Stackhouse B, et al. (2015) Large-scale genomic sequencing of extraintestinal pathogenic Escherichia coli strains. Genome Res 25: 119–128. doi: 10.1101/gr.180190.114 25373147
12. Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF, et al. (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190: 6881–6893. doi: 10.1128/JB.00619-08 18676672
13. van Opijnen T, Lazinski DW, Camilli A, (2015) Genome-Wide Fitness and Genetic Interactions Determined by Tn-seq, a High-Throughput Massively Parallel Sequencing Method for Microorganisms. Curr Protoc Microbiol 36: 1E 3 1–1E 3 24.
14. Wiles TJ, Norton JP, Russell CW, Dalley BK, Fischer KF, et al. (2013) Combining quantitative genetic footprinting and trait enrichment analysis to identify fitness determinants of a bacterial pathogen. PLoS Genet 9: e1003716. doi: 10.1371/journal.pgen.1003716 23990803
15. Schnoes AM, Brown SD, Dodevski I, Babbitt PC, (2009) Annotation error in public databases: misannotation of molecular function in enzyme superfamilies. PLoS Comput Biol 5: e1000605. doi: 10.1371/journal.pcbi.1000605 20011109
16. van Opijnen T, Camilli A, (2012) A fine scale phenotype-genotype virulence map of a bacterial pathogen. Genome Res 22: 2541–2551. doi: 10.1101/gr.137430.112 22826510
17. Deutschbauer A, Price MN, Wetmore KM, Tarjan DR, Xu Z, et al. (2014) Towards an informative mutant phenotype for every bacterial gene. J Bacteriol 196: 3643–3655. doi: 10.1128/JB.01836-14 25112473
18. Kisker C, Schindelin H, Rees DC, (1997) Molybdenum-cofactor-containing enzymes: structure and mechanism. Annu Rev Biochem 66: 233–267. 9242907
19. Karudapuram S, Zhao X, Barcak GJ, (1995) DNA sequence and characterization of Haemophilus influenzae dprA+, a gene required for chromosomal but not plasmid DNA transformation. J Bacteriol 177: 3235–3240. 7768823
20. Janion C, (2008) Inducible SOS response system of DNA repair and mutagenesis in Escherichia coli. Int J Biol Sci 4: 338–344. 18825275
21. Ordonez H, Unciuleac M, Shuman S, (2012) Mycobacterium smegmatis RqlH defines a novel clade of bacterial RecQ-like DNA helicases with ATP-dependent 3'-5' translocase and duplex unwinding activities. Nucleic Acids Res 40: 4604–4614. doi: 10.1093/nar/gks046 22287622
22. Luria SE, Delbruck M, (1943) Mutations of Bacteria from Virus Sensitivity to Virus Resistance. Genetics 28: 491–511. 17247100
23. Jones HM, Gunsalus RP, (1985) Transcription of the Escherichia coli fumarate reductase genes (frdABCD) and their coordinate regulation by oxygen, nitrate, and fumarate. J Bacteriol 164: 1100–1109. 2999070
24. Yampolsky LY, Stoltzfus A, (2005) The exchangeability of amino acids in proteins. Genetics 170: 1459–1472. 15944362
25. Wu Y, Brosh RM, Jr. (2010) Helicase-inactivating mutations as a basis for dominant negative phenotypes. Cell Cycle 9: 4080–4090. doi: 10.4161/cc.9.20.13667 20980836
26. Albenberg L, Esipova TV, Judge CP, Bittinger K, Chen J, et al. (2014) Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota. Gastroenterology 147: 1055–1063 e1058. doi: 10.1053/j.gastro.2014.07.020 25046162
27. Hagan EC, Lloyd AL, Rasko DA, Faerber GJ, Mobley HL, (2010) Escherichia coli global gene expression in urine from women with urinary tract infection. PLoS Pathog 6: e1001187. doi: 10.1371/journal.ppat.1001187 21085611
28. Croteau DL, Popuri V, Opresko PL, Bohr VA, (2014) Human RecQ helicases in DNA repair, recombination, and replication. Annu Rev Biochem 83: 519–552. doi: 10.1146/annurev-biochem-060713-035428 24606147
29. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, et al. (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102: 11070–11075. 16033867
30. Krych L, Hansen CH, Hansen AK, van den Berg FW, Nielsen DS, (2013) Quantitatively different, yet qualitatively alike: a meta-analysis of the mouse core gut microbiome with a view towards the human gut microbiome. PLoS One 8: e62578. doi: 10.1371/journal.pone.0062578 23658749
31. Holden JA, Harriman PD, Wall JD, (1976) Escherichia coli mutants deficient in guanine-xanthine phosphoribosyltransferase. J Bacteriol 126: 1141–1148. 820683
32. Mortier-Barriere I, Velten M, Dupaigne P, Mirouze N, Pietrement O, et al. (2007) A key presynaptic role in transformation for a widespread bacterial protein: DprA conveys incoming ssDNA to RecA. Cell 130: 824–836. 17803906
33. Smeets LC, Becker SC, Barcak GJ, Vandenbroucke-Grauls CM, Bitter W, et al. (2006) Functional characterization of the competence protein DprA/Smf in Escherichia coli. FEMS Microbiol Lett 263: 223–228. 16978360
34. Londono-Vallejo JA, Dubnau D, (1993) comF, a Bacillus subtilis late competence locus, encodes a protein similar to ATP-dependent RNA/DNA helicases. Mol Microbiol 9: 119–131. 8412657
35. Tomb JF, el-Hajj H, Smith HO, (1991) Nucleotide sequence of a cluster of genes involved in the transformation of Haemophilus influenzae Rd. Gene 104: 1–10. 1916268
36. Etchuuya R, Ito M, Kitano S, Shigi F, Sobue R, et al. (2011) Cell-to-cell transformation in Escherichia coli: a novel type of natural transformation involving cell-derived DNA and a putative promoting pheromone. PLoS One 6: e16355. doi: 10.1371/journal.pone.0016355 21283723
37. Sun D, Zhang Y, Mei Y, Jiang H, Xie Z, et al. (2006) Escherichia coli is naturally transformable in a novel transformation system. FEMS Microbiol Lett 265: 249–255. 17069625
38. Sinha S, Redfield RJ, (2012) Natural DNA uptake by Escherichia coli. PLoS One 7: e35620. doi: 10.1371/journal.pone.0035620 22532864
39. Unterholzner SJ, Poppenberger B, Rozhon W, (2013) Toxin-antitoxin systems: Biology, identification, and application. Mob Genet Elements 3: e26219. 24251069
40. Norton JP, Mulvey MA, (2012) Toxin-antitoxin systems are important for niche-specific colonization and stress resistance of uropathogenic Escherichia coli. PLoS Pathog 8: e1002954. doi: 10.1371/journal.ppat.1002954 23055930
41. Sberro H, Leavitt A, Kiro R, Koh E, Peleg Y, et al. (2013) Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning. Mol Cell 50: 136–148. doi: 10.1016/j.molcel.2013.02.002 23478446
42. Murphy KC, Campellone KG, (2003) Lambda Red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli. BMC Mol Biol 4: 11. 14672541
43. Li XT, Thomason LC, Sawitzke JA, Costantino N, Court DL, (2013) Positive and negative selection using the tetA-sacB cassette: recombineering and P1 transduction in Escherichia coli. Nucleic Acids Res 41: e204. doi: 10.1093/nar/gkt1075 24203710
44. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640–6645. 10829079
45. Studdert CA, Parkinson JS, (2005) Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies. Proc Natl Acad Sci U S A 102: 15623–15628. 16230637
46. Guzman LM, Belin D, Carson MJ, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121–4130. 7608087
47. Bryksin A, Matsumura I, (2013) Overlap extension PCR cloning. Methods Mol Biol 1073: 31–42. doi: 10.1007/978-1-62703-625-2_4 23996437
48. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675. 22930834
49. Zhang X, Bremer H, (1995) Control of the Escherichia coli rrnB P1 promoter strength by ppGpp. J Biol Chem 270: 11181–11189. 7538113
50. 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
51. Cock PJ, Antao T, Chang JT, Chapman BA, Cox CJ, et al. (2009) Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25: 1422–1423. doi: 10.1093/bioinformatics/btp163 19304878