Repair of DNA damage induced by bile salts in Salmonella enterica

Genetics

Volumn 174, Issue 2, 2006, Pages 575-584

  Prieto, Ana I ^a   Ramos Morales, Francisco ^a   Casadesús, Josep ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BILE SALT; CHENODEOXYCHOLIC ACID; CHOLIC ACID; DEOXYCHOLATE SODIUM; ENDONUCLEASE; EXODEOXYRIBONUCLEASE III; GLYCOCHOLATE SODIUM; GLYCODEOXYCHOLIC ACID; TAUROCHOLIC ACID;

ANTIBACTERIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA SYNTHESIS; DRUG ACTIVITY; EXCISION REPAIR; GENE EXPRESSION; GENE INDUCTION; HOMOLOGOUS RECOMBINATION; MINIMUM INHIBITORY CONCENTRATION; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; REGULON; SALMONELLA ENTERICA;

AMINO ACID SUBSTITUTION; ANIMALS; BILE; BILE ACIDS AND SALTS; CATTLE; DNA DAMAGE; DNA REPAIR; DNA, BACTERIAL; MUTATION; SALMONELLA TYPHIMURIUM;

SALMONELLA ENTERICA;

EID: 33750432851     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.106.060889     Document Type: Article

References (87)

1. BENSON, N. R., and J. ROTH, 1994 Suppressors of recB mutations in Salmonella typhimurium. Genetics 138: 11-29.
2. BERNSTEIN, C., H. BERNSTEIN, C. M. PAYNE, S. E. BEARD and J. SCHNEIDER, 1999 Bile salt activation of stress response promoters in Escherichia coli. Curr. Microbiol. 39: 68-72.
3. BERNSTEIN, H., C. M. PAYNE, C. BERNSTEIN, J. SCHNEIDER, S. E. BEARD et al., 1999 Activation of the promoters of genes associated with DNA damage, oxidative stress, ER stress and protein malfolding by the bile salt, deoxycholate. Toxicol. Lett. 108: 37-46.
4. BERNSTEIN, H., C. BERNSTEIN, C. M. PAYNE, K. DVORAKOVA and H. GAREWAL, 2005 Bile acids as carcinogens in human gastrointestinal cancers. Mutat. Res. 589: 47-65.
5. BHATNAGAR, S. K., L. C. BULLIONS and M. J. BESSMAN, 1991 Characterization of the mutT nucleoside triphosphatase of Escherichia coli. J. Biol. Chem. 266: 9050-9054.
6. BOITEUX, S., T. R. O'CONNOR and J. LAVAL, 1987 Formamidopyrimidine-DNA glycosylase of Escherichia coli: cloning and sequencing of the fpg structural gene and overproduction of the protein. EMBO J. 6: 3177-3183.
7. BRAUN, A., and L. GROSSMAN, 1974 An endonuclease from Escherichia coli that acts preferentially on UV-irradiated DNA and is absent from the uvrA and uvrB mutants. Proc. Natl. Acad. Sci. USA 71: 1838-1842.
8. BUCHMEIER, N. A., C. J. LIPPS, M. Y. SO and F. HEFFRON, 1993 Recombination-deficient mutants of Salmonella typhimurium are avirulent and sensitive to the oxidative burst of macrophages. Mol. Microbiol. 7: 933-936.
9. CANO, D. A., M. G. PUCCIARELLI, F. GARCIA-DEL PORTILLO and J. CASADESÚS, 2002 Role of the RecBCD recombination pathway in Salmonella virulence. J. Bacteriol. 184: 592-595.
10. CHAN, R. K., D. BOTSTEIN, T. WATANABE and Y. OGATA, 1972 Specialized transduction of tetracycline by phage P22 in Salmonella typhimurium. II. Properties of a high frequency transducing lysate. Virology 50: 883-898.
11. CLARKE, N. D., M. KVAAL and E. SEEBERG, 1984 Cloning of Escherichia coli genes encoding 3-methyladenine DNA glycosylases I and II. Mol. Gen. Genet. 197: 368-372.
12. COOK, J. W., E. L. KENNAWAY and N. M. KENNAWAY, 1940 Production of tumours in mice by deoxycholic acid. Nature 145: 627.
13. CUNNINGHAM, R. P., S. M. SAPORITO, S. G. SPITZER and B. WEISS, 1986 Endonuclease IV (nfo) mutant of Escherichia coli. J. Bacteriol. 168: 1120-1127.
14. CUPPLES, C. G., and J. H. MILLER, 1989 A set of lacZ mutations that allow rapid detection of each of the six base substitutions. Proc. Natl. Acad. Sci. USA 86: 5345-5349.
15. DARWIN, K. H., and C. F. NATHAN, 2005 Role for nucleotide excision repair in virulence of Mycobacterium tuberculosis. Infect. Immun. 73: 4581-4587.
16. DATSENKO, K. A., and B. L. WANNER, 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 90: 6640-6645.
17. DEMPLE, B., 1999 Radical ideas: genetic responses to oxidative stress. Clin. Exp. Pharmacol. Physiol. 26: 64-68.
18. 2-damaged Escherichia coli. Proc. Natl. Acad. Sci. USA 83: 7731-7735.
19. DIZDAROGLU, M., S. M. BURGESS, P. JARUGA, T. K. HAZRA, H. RODRIGUEZ et al., 2001 Substrate specificity and excision kinetics of Escherichia coli endonuclease VIII (Nei) for modified bases in DNA damaged by free radicals. Biochemistry 40: 12150-12156.
20. DUTTA, U., P. K. GARG, R. KUMAR and R. K. TANDON, 2000 Typhoid carriers among patients with gallstones are at increased risk for carcinoma of the gall bladder. Am. J. Gastroenterol. 95: 784-787.
21. ECHEITA, M. A., and M. A. USERA, 1998 Chromosomal rearrangements in Salmonella enterica serovar Typhi affecting molecular typing in outbreak investigations. J. Clin. Microbiol. 36: 2123-2126.
22. ELLERMEIER, C. D., A. JANAKIRAM and J. M. SLAUCH, 2002 Construction of targeted single copy lac fusions using lambda Red and FLP-mediated site-specific recombination in bacteria. Gene 290: 153-161.
23. FOWLER, R. G., S. J. WHITE, C. KOYAMA, S. C. MOORE, R. L. DUNN et al., 2003 Interactions among the Escherichia coli mutT, mut M, and mutY damage prevention pathways. DNA Repair 2: 159-173.
24. FRAM, R. J., P. S. CUSICK, J. M. WILSON and M. G. MARINUS, 1985 Mismatch repair of cis-diamminedichloroplatinum(II)-induced DNA damage. Mol. Pharmacol. 28: 51-55.
25. FRIEDBERG, E. C., G. C. WALKER and W. SIEDE, 1995 DNA Repair and Mutagenesis. American Society of Microbiology, Washington, DC.
26. GARZÓN, A., C. R. BEUZÓN, M. J. MAHAN and J. CASADESÚS, 1996 recB recJ mutants of Salmonella typhimurium are deficient in transductional recombination, DNA repair and plasmid maintenance. Mol. Gen. Genet. 270: 570-580.
27. GLICKMAN, B. W., and M. RADMAN, 1980 Escherichia coli mutator mutants deficient in methylation-instructed DNA mismatch correction. Proc. Natl. Acad. Sci. USA 77: 1063-1067.
28. GUNN, J. S., 2000 Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2: 907-913.
29. HOFMANN, A. F., 1998 Bile secretion and enterohepatic circulation of bile acids, pp. 937-948 in Sleisenger and Fordtran's Gastrointestinal Disease, Ed. 6, edited by M. FELDMAN, B. F. SCHARSCHMIDT and W. B. SLEISENGER. W. B. Saunders, Philadelphia.
30. HUNG, D. T., and J. J. MEKALANOS, 2005 Bile acids induce cholera toxin expression in Vibrio cholerae in a ToxT-independent manner. Proc. Natl. Acad. Sci. USA 102: 3028-3033.
31. KHIL, P. P., and D. CAMERINI-OTERO, 2002 Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol. Microbiol. 44: 89-115.
32. KIM, S. R., K. MATSUI, M. YAMADA, P. GRUZ and T. NOHMI, 2001 Roles of chromosomal and episomal dinB genes encoding DNA Pol IV in targeted and untargeted mutagenesis in Escherichia coli. Mol. Genet. Genomics 266: 207-215.
33. KOKUBO, K., M. YAMADA, Y. KANKE and T. NOHMI, 2005 Roles of replicative and specialized DNA polymerases in frameshift mutagenesis: mutability of Salmonella typhimurium strains lacking one or all SOS-inducible polymerases to 26 chemicals. DNA Repair 4: 1160-1171.
34. KOTHAPALLI, S., S. NAIR, S. ALOKAM, T. PANG, R. KHAKHRIA et al., 2005 Diversity of genome structure in Salmonella enterica serovar Typhi populations. J. Bacteriol. 187: 2638-2650.
35. KREUTZER, D. A., and J. M. ESSIGMANN, 1998 Oxidized, deaminated cytosines are a source of C-T transitions in vivo. Proc. Natl. Acad. Sci. USA 95: 3578-3582.
36. LALITHA, M. K., and R. JOHN, 1994 Unusual manifestations of salmonellosis - a surgical problem. Q. J. Med. 87: 301-309.
37. LEA, D., and C. A. COULSON, 1949 The distribution of numbers of mutants in bacterial populations. J. Genet. 49: 264-285.
38. LI, Z., and B. DEMPLE, 1994 SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA. J. Biol. Chem. 269: 18371-18377.
39. LIOCHEV, S. I., and I. FRIDOVICH, 1992 Fumarase C, the stable fumarase of Escherichia coli, is controlled by the soxRS regulon. Proc. Natl. Acad. Sci. USA 89: 5892-5896.
40. LOMOVSKAYA, O., and K. LEWIS, 1992 Emr, an Escherichia coli locus for multidrug resistance. Proc. Natl. Acad. Sci. USA 89: 8938-8942.
41. MA, D., D. N. COOK and H. NIKAIDO, 1994 Efflux pumps and drug resistance in gram-negative bacteria. Trends Microbiol. 2: 489-493.
42. MAHAN, M. J., and J. R. ROTH, 1989 The recB and recJ genes of Salmonella typhimurium. J. Bacteriol. 171: 612-615.
43. + hosts. Mol. Gen. Genet. 232: 470-478.
44. MCCLELLAND, M., K. E. SANDERSON, J. SPIETH, S. W. CLIFTON, P. LATREILLE et al., 2001 Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
45. MCPARTLAND, A., L. GREEN and H. ECHOLS, 1980 Control of recA gene RNA in E. coli: regulatory and signal genes. Cell 20: 731-737.
46. MERINO, D., H. REGLIER-POUPET, P. BERCHE and A. CHARBIT, 2002 A hypermutator phenotype attenuates the virulence of Listeria monocytogenes. Mol. Microbiol. 44: 877-887.
47. MICHAELS, M. L., and J. H. MILLER, 1992 The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J. Bacteriol. 174: 6321-6325.
48. MICHEL, B., S. D. EHRLICH and M. UZEST, 1997 DNA double-strand breaks caused by replication arrest. EMBO J. 17: 430-438.
49. MIESEL, L., and J. R. ROTH, 1994 Salmonella typhimurium recD mutations increase recombination in a short-sequence transduction assay. J. Bacteriol. 176: 4092-4103.
50. Miller, J. H., 1972 Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
51. MOL, C. D., D. J. HOSFIELD and J. A. TAINER, 2000 Abasic site recognition by two apurinic/apyrimidinic endonuclease families in base excision repair: the 39 ends justify the means. Mutat. Res. 460: 211-229.
52. NG, I., L. SHU-LIN and K. E. SANDERSON, 1999 Role of genomic rearrangements in producing new ribotypes of Salmonella typhi. J. Bacteriol. 181: 3536-3541.
53. NOWOSIELSKA, A., and M. G. MARINUS, 2005 Cisplatin induces double-strand break formation in Escherichia coli dam mutants. DNA Repair 4: 773-781.
54. O'ROURKE, E. J., C. CHEVALIER, A. V. PINTO, J. M. THIBERGE, L. IELPI et al., 2003 Pathogen DNA as target for host-generated oxidative stress: role for repair of DNA damage in Helicobacter pylori colonization. Proc. Natl. Acad. Sci. USA 100: 2789-2794.
55. PICKEN, R. N., and I. R. BEACHAM, 1977 Bacteriophage-resistant mutants of Escherichia coli K-12. Location of receptors within the lypopolysaccharide. J. Gen. Microbiol. 102: 305-318.
56. PONDER, R. G., N. C. FONVILLE and S. M. ROSENBERG, 2005 A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Mol. Cell 19: 791-804.
57. POPE, L. M., K. E. REED and S. M. PAYNE, 1995 Increased protein secretion and adherence to HeLa cells by Shigella spp. following growth in the presence of bile salts. Infect. Immun. 63: 3642-3648.
58. PRIETO, A. I., F. RAMOS-MORALES and J. CASADESÚS, 2004 Bile-induced DNA damage in Salmonella enterica. Genetics 168: 1787-1794.
59. PROUTY, A. M., and J. S. GUNN, 2000 Salmonella enterica serovar Typhimurium invasion is repressed in the presence of bile. Infect. Immun. 68: 6763-6769.
60. PROUTY, A. M., J. C. VAN VELKINBURGH and J. S. GUNN, 2002 Salmonella enterica serovar Typhimurium resistance to bile: identification and characterization of the tolQRA cluster. J. Bacteriol. 184: 1270-1276.
61. PROUTY, A. M., W. H. SCHWESINGER and J. S. GUNN, 2003 Biofilm formation and interaction with the surface of gallstones by Salmonella spp. Infect. Immun. 70: 2640-2649.
62. PROUTY, A. M., I. E. BRODSKY, J. MANOS, R. BELAS, S. FALKOW et al., 2004 Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol. Med. Microbiol. 41: 177-185.
63. PUCCIARELLI, M. G., A. I. PRIETO, J. CASADESÚS and F. GARCÍA-DEL PORTILLO, 2002 Envelope instability in DNA adenine methylase mutants of Salmonella enterica. Microbiology 148: 1171-1182.
64. PURMAL, A. A., G. W. LAMPMAN, J. P. BOND, Z. HATAHET and S. S. WALLACE, 1998 Enzymatic processing of uracil glycol, a major oxidative product of DNA cytosine. J. Biol. Chem. 273: 10026-10035.
65. RAMOS-MORALES, F., A. I. PRIETO, C. BEUZÓN, D. W. HOLDEN and J. CASADESÚS, 2003 Role for Salmonella enterobacterial common antigen in bile resistance and virulence. J. Bacteriol. 185: 5328-5332.
66. ROSENBERG, S. M., and P. J. HASTINGS, 2003 Modulating mutation rates in the wild. Science 300: 1382-1383.
67. ROSENBERG, E. Y., D. BERTENTHAL, M. W. NILLES, K. P. BERTRAND and H. NIKAIDO, 2003 Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein. Mol. Microbiol. 48: 1609-1619.
68. SAINT-RUF, C., and I. MATIC, 2006 Environmental tuning of mutation rates. Environ. Microbiol. 8: 193-199.
69. SAITO, Y., F. URAKI, S. NAKAJIMA, A. ASAEDA, K. ONO et al., 1997 Characterization of endonuclease III (nth) and endonuclease VIII (nei) mutants of Escherichia coli K-12. J. Bacteriol. 179: 3783-3785.
70. SAMSON, L., 1992 The suicidal DNA repair methyltransferases of microbes. Mol. Microbiol. 7: 825-831.
71. SCHAPIRO, J. M., S. J. LIBBY and F. C. FANG, 2003 Inhibition of bacterial DNA replication by zinc mobilization during nitrosative stress. Proc. Natl. Acad. Sci. USA 100: 8496-8501.
72. SCHMIEGER, H., 1972 Phage P22 mutants with increased or decreased transducing abilities. Mol. Gen. Genet. 119: 75-88.
73. SEEBERG, E., 1978 Reconstitution of an Escherichia coli repair endonuclease activiy from the separated uvrA and uvrB/uvrC gene products. Proc. Natl. Acad. Sci. USA 75: 2569-2573.
74. SEIGNEUR, M., V. BIDNENKO, S. D. EHRLICH and B. MICHEL, 1998 RuvA acts at arrested replication forks. Cell 95: 419-430.
75. SHIBUTANI, S., M. TAKESHITA and A. P. GROLLMAN, 1991 Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349: 431-434.
76. STOCKER, R., Y. YAMAMOTO, A. F. MCDONAGH, A. N. GLAZER and B. N. AMES, 1987 Bilirubin is an antioxidant of possible physiological importance. Science 235: 1043-1046.
77. STORZ, G., and A. IMLAY, 1999 Oxidative stress. Curr. Opin. Microbiol. 2: 188-194.
78. SUTTON, M. D., B. T. SMITH, V. G. GODOY and G. C. WALKER, 2000 The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu. Rev. Genet. 34: 479-497.
79. SUVARNAPUNYA, A. E., H. A. D. LAGASSÉ and M. A. STEIN, 2003 The role of DNA base excision repair in the pathogenesis of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 48: 549-559.
80. UZEST, M., S. D. EHRLICH and B. MICHEL, 1995 Lethality of rep recB and rep recC double mutants in Escherichia coli. Mol. Microbiol. 17: 1177-1188.
81. VAZQUEZ-TORRES, A., and F. C. FANG, 2000 Oxygen-dependent anti-Salmonella activity of macrophages. Trends Microbiol. 9: 29-33.
82. VISWANATHAN, M., and S. T. LOVETT, 1998 Single-strand DNA-specific exonucleases in E. coli: roles in repair and mutation avoidance. Genetics 149: 7-16.
83. VOGEL, H., and D. BONNER, 1956 Acetylornithase of Escherichia coli: partial purification and some properties. J. Biol. Chem. 218: 97-106.
84. VOLKERT, M. R., and P. LANDINI, 2001 Transcriptional responses to DNA damage. Curr. Opin. Microbiol. 4: 178-185.
85. WHITE, B. J., S. J. HOCHHAUSER, N. M. CINTRON and B. WEISS, 1976 Genetic mapping of xthA, the structural gene for exonuclease III in Escherichia coli K-12. J. Bacteriol. 126: 1082-1088.
86. WYRZYKOWSKI, J., and M. R. VOLKERT, 2003 The Escherichia coli methyl-directed mismatch repair system repairs base pairs containing oxidative lesions. J. Bacteriol. 185: 1701-1704.
87. ZHENG, M., X. WANG, L. J. TEMPLETON, D. R. SMULSKI, R. A. LAROSSA et al., 2001 DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183: 4562-4570.