Salmonella Typhimurium exhibits fluoroquinolone resistance mediated by the accumulation of the antioxidant molecule H2S in a CysK-dependent manner

Journal of Antimicrobial Chemotherapy

Volumn 71, Issue 12, 2016, Pages 3409-3415

  Fravega J ^a   Alvarez R ^a   Diaz F ^a   Inostroza, O ^a   Tejias C ^a   Rodas, P I ^a   Paredes Sabja, D ^a   Fuentes, J A ^a   Calderon I L ^a   Gil, F ^a  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

5,5' DITHIOBIS(2 NITROBENZOIC ACID); CYSTEINE; HYDROGEN SULFIDE; OFLOXACIN; ANTIINFECTIVE AGENT; ANTIOXIDANT; CYSTEINE SYNTHASE; QUINOLONE DERIVATIVE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ARTICLE; CHROMOSOME; CONTROLLED STUDY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; FENTON REACTION; GENE DELETION; GENE EXPRESSION; MINIMUM INHIBITORY CONCENTRATION; MUTAGENESIS; NONHUMAN; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; PHYSIOLOGY;

ANTI-BACTERIAL AGENTS; ANTIOXIDANTS; CYSTEINE; CYSTEINE SYNTHASE; DRUG RESISTANCE, BACTERIAL; FLUOROQUINOLONES; GENE DELETION; GENE EXPRESSION PROFILING; HUMANS; HYDROGEN SULFIDE; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; OFLOXACIN; SALMONELLA TYPHIMURIUM;

EID: 85019336822     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/JAC/DKW311     Document Type: Article

References (62)

1. Andersson MI, MacGowan AP. Development of the quinolones. J Antimicrob Chemother 2003; 1: 1-11
2. Hooper DC. Emerging mechanisms of fluoroquinolone resistance. Emerg Infect Dis 2001; 7: 337-41
3. Castora FJ, Vissering FF, Simpson MV. The effect of bacterial DNA gyrase inhibitors on DNA synthesis in mammalian mitochondria. Biochim Biophys Acta 1983; 740: 417-27
4. Bergan T. Pharmacokinetics of fluorinated quinolones. In: Andriole VT, ed. The Quinolones. London, Academic Press, 1988; 119-54
5. Suto MJ, Domagala JM, Roland GE et al. Fluoroquinolones: relationships between structural variations, mammalian cell cytotoxicity, and antimicrobial activity. J Med Chem 1992; 35: 4745-50
6. Sato K, Matsuura Y, Inoue M et al. In vitro and in vivo activity of DL-8280, a new oxazine derivative. Antimicrob Agents Chemother 1982; 22: 548-53
7. Fu KP, Hilliard J, Isaacson D et al. In-vivo evaluation of ofloxacin in Salmonella typhimurium infection in mice. J Antimicrob Chemother 1990; 25: 263-8
8. Chandey M, Multani AS. Comparative study of efficacy and safety of azithromycin and ofloxacin in uncomplicated typhoid fever: a randomised, open labelled study. J Clin Diagn Res 2012; 6: 1736-9
9. Shatalin K, Shatalina E, Mironov A et al. H2S: a universal defense against antibiotics in bacteria. Science 2011; 18: 986-90
10. Park S, Imlay JA. High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J Bacteriol 2003; 185: 1942-50
11. Álvarez R, Neumann G, Frávega J et al. CysB-dependent upregulation of the Salmonella Typhimurium cysJIH operon in response to antimicrobial compounds that induce oxidative stress. Biochem Biophys Res Commun 2015; 458: 46-51
12. Hryniewicz MM, Kredich NM. Stoichiometry of binding of CysB to the cysJIH, cysK, and cysP promoter regions of Salmonella typhimurium. J Bacteriol 1994; 176: 3673-82
13. Haverkamp T, Schwenn JD. Structure and function of a cysBJIH gene cluster in the purple sulphur bacterium Thiocapsa roseopersicina. Microbiology 1999; 145: 115-25
14. Álvarez R, Frávega J, Fuentes JA et al. Participation of S. Typhimurium cysJIH operon in the H2S-mediated ciprofloxacin resistance in presence of sulfate as sulfur source. Antibiotics 2015; 4: 321-8
15. van der Ploeg JR, Weiss MA, Saller E et al. Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source. J Bacteriol 1996; 178: 5438-46
16. van der Ploeg JR, Cummings NJ, Leisinger T et al. Bacillus subtilis genes for the utilization of sulfur from aliphatic sulfonates. Microbiology 1998; 144: 2555-61
17. Fimmel AL, Loughlin RE. Isolation and characterization of cysK mutants of Escherichia coli K12. J Gen Microbiol 1977; 103: 37-43
18. Hulanicka MD, Kredich NM, Treiman DM. The structural gene for O-acetylserine sulfhydrylase A in Salmonella typhimurium. Identity with the trzA locus. J Biol Chem 1974; 249: 867-72
19. Hulanicka MD, Garrett C, Jagura-Burdzy G et al. Cloning and characterization of the cysAMK region of Salmonella typhimurium. J Bacteriol 1986; 168: 322-7
20. Nakamura T, Kon Y, Iwahashi H et al. Evidence that thiosulfate assimilation by Salmonella typhimurium is catalyzed by cysteine synthase B. J Bacteriol 1983; 156: 656-62
21. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 2000; 97: 6640-5
22. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-third Informational Supplement M100-S23. CLSI, Wayne, PA, USA, 2013
23. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959; 82: 70-7
24. Guerrero P, Collao B, Alvarez R et al. The Salmonella Typhimurium BaeSR two-component system positively regulates sodA in response to ciprofloxacin. Microbiology 2013; 159: 2049-57
25. Calderón IL, Morales EH, Collao B et al. Role of Salmonella Typhimurium small RNAs RyhB-1 and RyhB-2 in the oxidative stress response. Res Microbiol 2014; 165: 30-40
26. PfafflMW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29: e45
27. Aruoma OI, Halliwell B, Gajewski E et al. Damage to the bases in DNA induced by hydrogen peroxide and ferric ion chelates. J Biol Chem 1989; 264: 20509-12
28. Liochev SI, Fridovich I. Superoxide and iron: partners in crime. IUBMB Life 1999; 48: 157-61
29. Imlay JA. Pathways of oxidative damage. Annu Rev Microbiol 2003; 57: 395-418
30. Gusarov I, Nudler E. NO-mediated cytoprotection: instant adaptation to oxidative stress in bacteria. Proc Natl Acad Sci USA 2005; 102: 13855-60
31. Kohanski MA, Dwyer DJ, Hayete B et al. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 2007; 130: 797-810
32. Kohanski MA, Dwyer DJ, Collins JJ. How antibiotics kill bacteria: from targets to networks. Nat Rev Microbiol 2010; 8: 423-35
33. Davies BW, Kohanski MA, Simmons LA et al. Hydroxyurea induces hydroxyl radical-mediated cell death in Escherichia coli. Mol Cell 2009; 36: 845-60
34. Chang HH, Cohen T, Grad YH et al. Origin and proliferation of multipledrug resistance in bacterial pathogens. Microbiol Mol Biol Rev 2015; 79: 101-16
35. Roca I, AkovaM, Baquero F et al. The global threat of antimicrobial resistance: science for intervention. New Microbes New Infect 2015; 6: 22-9
36. Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 2010; 74: 417-33
37. Conlon BP, Nakayasu ES, Fleck LE et al. Activated ClpP kills persisters and eradicates a chronic biofilm infection. Nature 2013; 503: 365-70
38. Nelson JM, Chiller TM, Powers JH et al. Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a public health success story. Clin Infect Dis 2007; 44: 977-80
39. Robicsek A, Jacoby GA, Hooper DC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis 2006; 6: 629-40
40. Morita Y, Kodama K, Shiota S et al. NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrob Agents Chemother 1998; 42: 1778-82
41. Hassett DJ, Imlay JA. Bactericidal antibiotics and oxidative stress: a radical proposal. ACS Chem Biol 2007; 2: 708-10
42. Christman MF, Morgan RW, Jacobson FS et al. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 1985; 41: 753-62
43. Greenberg JT, Monach P, Chou JH et al. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc Natl Acad Sci USA 1990; 87: 6181-5
44. Farr SB, Kogoma T. Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol Rev 1991; 55: 561-85
45. Zheng M, Storz G. Redox sensing by prokaryotic transcription factors. Biochem Pharmacol 2000; 59: 1-6
46. Pomposiello PJ, Demple B. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 2001; 19: 109-14
47. Lushchak VI. Oxidative stress and mechanisms of protection against it in bacteria. Biochemistry (Mosc) 2001; 66: 476-89
48. Kredich N. Biosynthesis of cysteine. In: Neidhardt FC, Curtiss R, eds. Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. Washington, DC: ASM Press, 1996; 514-27
49. Fuentes DE, Fuentes EL, Castro ME et al. Cysteine metabolism-related genes and bacterial resistance to potassium tellurite. J Bacteriol 2007; 189: 8953-60
50. Carmel-Harel O, Storz G. Roles of the glutathione-and thioredoxindependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 2000; 54: 439-61
51. Gleason F, Holmgren A. Thioredoxin and related proteins in procaryotes. FEMS Microbiol Rev 1988; 4: 271-97
52. Penninckx M, Elskens M. Metabolism and functions of glutathione in microorganisms. Adv Microbiol Physiol 1993; 34: 239-301
53. Turnbull AL, Surette MG. L-Cysteine is required for induced antibiotic resistance in actively swarming Salmonella enterica serovar Typhimurium. Microbiology 2008; 154: 3410-9
54. Yamamoto K, Oshima T, Nonaka G et al. Induction of the Escherichia coli cysK gene by genetic and environmental factors. FEMS Microbiol Lett 2011; 323: 88-95
55. Sturgill G, Toutain CM, Komperda J et al. Role of CysE in production of an extracellular signaling molecule in Providencia stuartii and Escherichia coli: loss of CysE enhances biofilm formation in Escherichia coli. J Bacteriol 2004; 186: 7610-7
56. Rakonjac J, Milic M, Savic DJ. cysB and cysE mutants of Escherichia coli K12 show increased resistance to novobiocin. Mol Gen Genet 1991; 228: 307-11
57. Oppezzo OJ, Antón DN. Involvement of cysB and cysE genes in the sensitivity of Salmonella typhimurium to mecillinam. J Bacteriol 1995; 177: 4524-7
58. Antón DN. Induction of the cysteine regulon of Salmonella typhimurium in LB medium affects the response of cysB mutants to mecillinam. Curr Microbiol 2000; 40: 72-7
59. Lilic M, Jovanovic M, Jovanovic G et al. Identification of the CysB-regulated gene, hslJ, related to the Escherichia coli novobiocin resistance phenotype. FEMS Microbiol Lett 2003; 224: 239-46
60. Costa CS, Antón DN. High-level resistance to mecillinam produced by inactivation of soluble lytic transglycosylase in Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett 2006; 256: 311-7
61. Eriksson S, Lucchini S, Thompson A et al. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 2003; 47: 103-18
62. Srikumar S, Kröger C, Hébrard M et al. RNA-seq brings new insights to the intra-macrophage transcriptome of Salmonella Typhimurium. PLoS Pathog 2015; 11: e1005262