Importance of bacillithiol in the oxidative stress response of Staphylococcus aureus

Infection and Immunity

Volumn 82, Issue 1, 2014, Pages 316-332

  Posada, Ana C ^a   Kolar, Stacey L ^b   Dusi, Renata G ^c   Francois, Patrice ^d   Roberts, Alexandra A ^c   Hamilton, Chris J ^c   Liu, George Y ^b   Cheung, Ambrose ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^d GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLITHIOL; BACILLITHIOL S TRANSFERASE; BACITRACIN; BACTERIAL ENZYME; CAROTENOID; CYCLOSERINE; FOSFOMYCIN; GLYCOSYLTRANSFERASE; HYDROGEN PEROXIDE; IMIPENEM; OXACILLIN; PENICILLIN G; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; STAPHYLOXANTHIN; THIOL DERIVATIVE; TRANSCRIPTION FACTOR FOSB; UNCLASSIFIED DRUG; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM ISOLATE; BIOSYNTHESIS; BLOOD; BSHA GENE; CONTROLLED STUDY; FOSB GENE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS;

EID: 84890842489     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01074-13     Document Type: Article

References (65)

1. Shorr AF, Tabak YP, Killian AD, Gupta V, Liu LZ, Kollef MH. 2006. Healthcare-associated bloodstream infection: a distinct entity? Insights from a large U.S. database. Crit. Care Med. 34:2588-2595.
2. Babior BM, Kipnes RS, Cumvu JT. 1973. Biological defense mechanisms. J. Clin. Invest. 52:741-744. http://dx.doi.org/10.1172/JCI107236.
3. Iyer GYN, Islam M, Quastel JH. 1961. Biochemical aspects of phagocytosis. Nature 192:535-541. http://dx.doi.org/10.1038/192535a0.
4. Weber H, Engelmann S, Becher D, Hecker M. 2004. Oxidative stress triggers thiol oxidation in the glyceraldehyde-3-phosphate dehydrogenase of Staphylococcus aureus. Mol. Microbiol. 52:133-140. http://dx.doi.org/10.1111/j.1365-2958.2004.03971.x.
5. Kilili KG, Atanassova N, Vardanyan A, Clatot N, Al-Sabarna K, Kanellopoulos PN, Makris AM, Kampranis SC. 2004. Differential roles of tau class glutathione S-transferases in oxidative stress. J. Biol. Chem. 279:24540-24551. http://dx.doi.org/10.1074/jbc.M309882200.
6. Pastore A, Federici G, Bertini E, Piemonte F. 2003. Analysis of glutathione: implication in redox and detoxification. Clin. Chim. Acta 333:19-39. http://dx.doi.org/10.1016/S0009-8981(03)00200-6.
7. Rigsby RE, Fillgrove KL, Beihoffer LA, Armstrong RN. 2005. Fosfomycin resistance proteins: a nexus of glutathione transferases and epoxide hydrolases in a metalloenzyme superfamily. Methods Enzymol. 401:367-379. http://dx.doi.org/10.1016/S0076-6879(05)01023-2.
8. Meury J, Kepes A. 1982. Glutathione and the gated potassium channels of Escherichia coli. EMBO J. 1:339-343.
9. Shibayama K, Wachino J, Arakawa Y, Saidijam M, Rutherford NG, Henderson PJF. 2007. Metabolism of glutamine and glutathione via gamma-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism. Mol. Microbiol. 64:396-406. http://dx.doi.org/10.1111/j.1365-2958.2007.05661.x.
10. Newton GL, Rawat M, La Clair JJ, Jothivasan VK, Budiarto T, Hamilton CJ, Claiborne A, Helmann J, Fahey RC. 2009. Bacillithiol is an antioxidant thiol produced in bacilli. Nat. Chem. Biol. 5:625-627. http://dx.doi.org/10.1038/nchembio.189.
11. Gaballa A, Newton GL, Antelmann H, Parsonage D, Upton H, Rawat M, Claiborne A, Fahey RC, Helmann J. 2010. Biosynthesis and functions of bacillithiol, a major low-molecular-weight thiol in bacilli. Proc. Natl. Acad. Sci. U.S.A. 107:6482-6486. http://dx.doi.org/10.1073/pnas.1000928107.
12. Parsonage D, Newton GL, Holder RC, Wallace BD, Paige C, Hamilton CJ, Dos Santos PC, Redinbo MR, Reid SD, Claiborne A. 2010. Characterization of the N-acetyl-α-D-glucosaminyl L-malate synthase and deacetylase functions for bacillithiol biosynthesis in Bacillus anthracis. Biochemistry 49:8398-8414. http://dx.doi.org/10.1021/bi100698n.
13. Newton GL, Fahey RC, Rawat M. 2012. Detoxification of toxins by bacillithiol in Staphylococcus aureus. Microbiology 158:1117-1126. http://dx.doi.org/10.1099/mic.0.055715-0.
14. Pöther D-C, Gierok P, Harms M, Mostertz J, Hochgräfe F, Antelmann H, Hamilton CJ, Borovok I, Lalk M, Aharonowitz Y, Hecker M. 2013. Distribution and infection-related functions of bacillithiol in Staphylococcus aureus. Int. J. Med. Microbiol. 303:114-123. http://dx.doi.org/10.1016/j.ijmm.2013.01.003.
15. Arca P, Reguera G, Hardisson C. 1997. Plasmid-encoded fosfomycin resistance in bacteria isolated from the urinary tract in a multicentre survey. J. Antimicrob. Chemother. 40:393-399. http://dx.doi.org/10.1093/jac/40.3.393.
16. Etienne J, Gerbaud G, Fleurette J, Courvalin P. 1991. Characterization of staphylococcal plasmids hybridizing with the fosfomycin resistance gene fosB. FEMS Microbiol. Lett. 68:119-122.
17. Lamers AP, Keithly ME, Kim K, Cook PD, Stec DF, Hines KM, Sulikowski GA, Armstrong RN. 2012. Synthesis of bacillithiol and the catalytic selectivity of FosB-type fosfomycin resistance proteins. Org. Lett. 14:5207-5209. http://dx.doi.org/10.1021/ol302327t.
18. Roberts AA, Sharma SV, Strankman AW, Duran SR, Rawat M, Hamilton CJ. 2013. Mechanistic studies of FosB: a divalent metal-dependent bacillithiol-S-transferase that mediates fosfomycin resistance in Staphylococcus aureus. Biochem. J. 451:69-79. http://dx.doi.org/10.1042/BJ20121541.
19. Sharma SV, Jothivasan VK, Newton GL, Upton H, Wakabayashi JI, Kane MG, Roberts AA, Rawat M, La Clair JJ, Hamilton CJ. 2011. Chemical and chemoenzymatic syntheses of bacillithiol: a unique lowmolecular-weight thiol amongst low G + C Gram-positive bacteria. Angew. Chem. Int. Ed. Engl. 50:7101-7104. http://dx.doi.org/10.1002/anie.201100196.
20. Scortti M, Lacharme-Lora L, Wagner M, Chico-Calero I, Losito P, Vázquez-Boland JA. 2006. Coexpression of virulence and fosfomycin susceptibility in Listeria: molecular basis of an antimicrobial in vitro-in vivo paradox. Nat. Med. 12:515-517. http://dx.doi.org/10.1038/nm1396.
21. Monk I, Shah I, Xu M, Tan M, Foster TJ. 2012. Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. mBio 3(2): e00277-11. http://dx.doi.org/10.1128/mBio.00277-11.
22. Bae T, Schneewind O. 2006. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55:58-63. http://dx.doi.org/10.1016/j.plasmid.2005.05.005.
23. Memmi G, Filipe SR, Pinho MG, Fu Z, Cheung AL. 2008. Staphylococcus aureus PBP4 is essential for beta-lactam resistance in communityacquired methicillin-resistant strains. Antimicrob. Agents Chemother. 52:3955-3966. http://dx.doi.org/10.1128/AAC.00049-08.
24. Forsyth R, Haselbeck R. 2002. A genome wide strategy for the identification of essential genes in Staphylococcus aureus. Mol. Microbiol. 43:1387-1400. http://dx.doi.org/10.1046/j.1365-2958.2002.02832.x.
25. Chi BK, Roberts AA, Huyen TT, Bäsell K, Becher D, Albrecht D, Hamilton CJ, Antelmann H. 2013. S-Bacillithiolation protects conserved and essential proteins against hypochlorite stress in Firmicutes bacteria. Antioxid. Redox Signal. 18:1273-1295. http://dx.doi.org/10.1089/ars.2012.4686.
26. Fenton SS, Fahey RC. 1986. Analysis of biological thiols: determination of thiol components of disulfides and thioesters. Anal. Biochem. 154:34-42. http://dx.doi.org/10.1016/0003-2697(86)90492-6.
27. Clinical and Laboratory Standards Institute. 2009. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard. M07-A8 29. Clinical and Laboratory Standards Institute, Wayne, PA.
28. Lithgow JK, Hayhurst EJ, Cohen G, Aharonowitz Y, Foster SJ. 2004. Role of a cysteine synthase in Staphylococcus aureus. J. Bacteriol. 186:1579-1590. http://dx.doi.org/10.1128/JB.186.6.1579-1590.2004.
29. Chang W, Small DA, Toghrol F, Bentley WE. 2006. Global transcriptome analysis of Staphylococcus aureus response to hydrogen peroxide. J. Bacteriol. 188:1648-1659. http://dx.doi.org/10.1128/JB.188.4.1648-1659.2006.
30. Ellman GL. 1959. Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82:70-77. http://dx.doi.org/10.1016/0003-9861(59)90090-6.
31. Riddles PW, Blakeley RL, Zerner B. 1983. Reassessment of Ellman's reagent. Methods Enzymol. 91:49-60. http://dx.doi.org/10.1016/S0076-6879(83)91010-8.
32. Wolff S. 1994. Ferrous ion oxidation in presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Methods Enzymol. 233:182-189. http://dx.doi.org/10.1016/S0076-6879(94)33021-2.
33. Tamber S, Schwartzman J, Cheung AL. 2010. Role of PknB kinase in antibiotic resistance and virulence in community-acquired methicillinresistant Staphylococcus aureus strain USA300. Infect. Immun. 78:3637-3646. http://dx.doi.org/10.1128/IAI.00296-10.
34. Charbonnier Y, Gettler B, François P, Bento M, Renzoni A, Vaudaux P, Schlegel W, Schrenzel J. 2005. A generic approach for the design of whole-genome oligoarrays, validated for genomotyping, deletion mapping and gene expression analysis on Staphylococcus aureus.BMCGenomics 6:95. http://dx.doi.org/10.1186/1471-2164-6-95.
35. Le Maréchal C, Seyffert N, Jardin J, Hernandez D, Jan G, Rault L, Azevedo V, François P, Schrenzel J, van de Guchte M, Even S, Berkova N, Thiéry R, Fitzgerald JR, Vautor E, Le Loir Y. 2011. Molecular basis of virulence in Staphylococcus aureus mastitis. PLoS One 6:e27354. http://dx.doi.org/10.1371/journal.pone.0027354.
36. Talaat AM, Howard ST, Hale W, IV, Lyons R, Garner H, Johnston SA. 2002. Genomic DNA standards for gene expression profiling in Mycobacterium tuberculosis. Nucleic Acids Res. 30:e104. http://dx.doi.org/10.1093/nar/30.1.1.
37. Clauditz A, Resch A, Wieland K-P, Peschel A, Götz F. 2006. Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect. Immun. 74:4950-4953. http://dx.doi.org/10.1128/IAI.00204-06.
38. Rajkarnikar A, Strankman A, Duran S, Vargas D, Roberts AA, Barretto K, Upton H, Hamilton CJ, Rawat M. 2013. Analysis of mutants disrupted in bacillithiol metabolism in Staphylococcus aureus. Biochem. Biophys. Res. Commun. 436:128-133. http://dx.doi.org/10.1016/j.bbrc.2013.04.027.
39. Cabiscol E, Tamarit J, Ros J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 3:3-8.
40. Potter AJ, Trappetti C, Paton JC. 2012. Streptococcus pneumoniae uses glutathione to defend against oxidative stress and metal ion toxicity. J. Bacteriol. 194:6248-6254. http://dx.doi.org/10.1128/JB.01393-12.
41. Kelner MJ, Bagnelli R, Welchl KJ. 1990. Thioureas react with superoxide radicals to yield a sulfhydryl compound. J. Biol. Chem. 265:1306-1311.
42. Chi BK, Gronau K, Mäder U, Hessling B, Becher D, Antelmann H. 2011. S-Bacillithiolation protects against hypochlorite stress in Bacillus subtilis as revealed by transcriptomics and redox proteomics. Mol. Cell. Proteomics 10:M111.009506. http://dx.doi.org/10.1074/mcp.M111.009506.
43. Cosgrove K, Coutts G, Jonsson I-M, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ. 2007. Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J. Bacteriol. 189:1025-1035. http://dx.doi.org/10.1128/JB.01524-06.
44. 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. http://dx.doi.org/10.1128/IAI.69.6.3744-3754.2001.
45. Cummins I, Cole D, Edwards R. 1999. A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in blackgrass. Plant J. 18:285-292. http://dx.doi.org/10.1046/j.1365-313X.1999.00452.x.
46. Prohaska J, Ganther H. 1976. Glutathione peroxidase activity of glutathione-S-transferases purified from rat liver. Biochem. Biophys. Res. Commun. 76:437-445. http://dx.doi.org/10.1016/0006-291X(77)90744-6.
47. Singh R, Mailloux RJ, Puiseux-Dao S, Appanna VD. 2007. Oxidative stress evokes a metabolic adaptation that favors increased NADPH synthesis and decreased NADH production in Pseudomonas fluorescens. J. Bacteriol. 189:6665-6675. http://dx.doi.org/10.1128/JB.00555-07.
48. Mapson L, Isherwood F. 1963. Glutathione reductase from germinated peas. Biochem. J. 86:173-191.
49. Thomas EL. 1984. Disulfide reduction and sulfhydryl uptake by Streptococcus mutans. J. Antimicrob. Chemother. 157:240-246.
50. delCardayre SB. 1998. Coenzyme A disulfide reductase, the primary low molecular weight disulfide reductase from Staphylococcus aureus purification and characterization of the native enzyme. J. Biol. Chem. 273:5744-5751. http://dx.doi.org/10.1074/jbc.273.10.5744.
51. Liu Y, Wu N, Dong J, Gao Y, Zhang X, Shao N, Yang G. 2010. ssrA (tmRNA) acts as an antisense RNA to regulate Staphylococcus aureus pigment synthesis by base pairing with crtMN mRNA. FEBS Lett. 584:4325-4329. http://dx.doi.org/10.1016/j.febslet.2010.09.024.
52. Fey PD, Endres JL, Yajjala VK, Widhelm TJ, Boissy RJ, Bose JL, Bayles KW. 2013. A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. mBio 4(1):e00537-12. http://dx.doi.org/10.1128/mBio.00537-12.
53. Fuchs S, Zühlke D, Pané-Farré J, Kusch H, Wolf C, Reiß S, Binh LTN, Albrecht D, Riedel K, Hecker M, Engelmann S. 2013. Aureolib-a proteome signature library: towards an understanding of Staphylococcus aureus pathophysiology. PLoS One 8:e70669. http://dx.doi.org/10.1371/journal.pone.0070669.
54. Upton H, Newton GL, Gushiken M, Lo K, Holden D, Fahey RC, Rawat M. 2012. Characterization of BshA, bacillithiol glycosyltransferase from Staphylococcus aureus and Bacillus subtilis. FEBS Lett. 586:1004-1008. http://dx.doi.org/10.1016/j.febslet.2012.02.028.
55. Nakano S, Küster-Schöck E, Grossman AD, Zuber P. 2003. Spxdependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 100:13603-13608. http://dx.doi.org/10.1073/pnas.2235180100.
56. Gaballa A, Antelmann H, Hamilton CJ, Helmann J. 2013. Regulation of Bacillus subtilis bacillithiol biosynthesis operons by Spx. Microbiology 159(Pt 10):2025-2035. http://dx.doi.org/10.1099/mic.0.070482-0.
57. Olivier A, Lemaire S, Van Bambeke F, Tulkens PM, Oldfield E. 2009. Role of rsbU and staphyloxanthin in phagocytosis and intracellular growth of Staphylococcus aureus in human macrophages and endothelial cells. J. Infect. Dis. 200:1367-1370. http://dx.doi.org/10.1086/606012.
58. Uziel O, Borovok I, Schreiber R, Cohen G, Aharonowitz Y. 2004. Transcriptional regulation of the Staphylococcus aureus thioredoxin and thioredoxin reductase genes in response to oxygen and disulfide stress. J. Bacteriol. 186:326-334. http://dx.doi.org/10.1128/JB.186.2.326-334.2004.
59. Vaish M, Singh VK. 2013. Antioxidant functions of nitric oxide synthase in a methicillin sensitive Staphylococcus aureus. Int. J. Microbiol. 2013:312146. http://dx.doi.org/10.1155/2013/312146.
60. Kreiswirth BN, Betley M, O'Reilly M. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712. http://dx.doi.org/10.1038/305709a0.
61. Tenover F, McDougal L, Goering R. 2006. Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States. J. Clin. Microbiol. 44:108-118. http://dx.doi.org/10.1128/JCM.44.1.108-118.2006.
62. Highlander SK, Hultén KG, Qin X, Jiang H, Yerrapragada S, Mason EO, Shang Y, Williams TM, Fortunov RM, Liu Y, Igboeli O, Petrosino J, Tirumalai M, Uzman A, Fox GE, Cardenas AM, Muzny DM, Hemphill L, Ding Y, Dugan S, Blyth PR, Buhay CJ, Dinh HH, Hawes AC, Holder M, Kovar CL, Lee SL, Liu W, Nazareth LV, Wang Q, Zhou J, Kaplan SL, Weinstock GM. 2007. Subtle genetic changes enhance virulence of methicillin resistant and sensitive Staphylococcus aureus. BMC Microbiol. 7:99. http://dx.doi.org/10.1186/1471-2180-7-99.
63. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J, Paulsen IT, Kolonay JF, Brinkac L, Beanan M, Dodson RJ, Daugherty SC, Madupu R, Angiuoli SV, Durkin AS, Haft DH, Vamathevan J, Khouri H, Utterback T, Lee C, Dimitrov G, Jiang L, Qin H, Weidman J, Tran K, Kang K, Hance IR, Nelson KE, Fraser CM. 2005. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilmproducing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187:2426-2438. http://dx.doi.org/10.1128/JB.187.7.2426-2438.2005.
64. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, Kobayashi I, Cui L, Oguchi A, Aoki K, Nagai Y, Lian J, Ito T, Kanamori M, Matsumaru H, Maruyama A, Murakami H, Hosoyama A, Mizutani-Ui Y, Takahashi NK, Sawano T, Inoue R, Kaito C, Sekimizu K, Hirakawa H, Kuhara S, Goto S, Yabuzaki J, Kanehisa M, Yamashita A, Oshima K, Furuya K, Yoshino C, Shiba T, Hattori M, Ogasawara N, Hayashi H, Hiramatsu K. 2001. Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357:1225-1240. http://dx.doi.org/10.1016/S0140-6736(00)04403-2.
65. Horsburgh MJ, Aish JL, White IJ, Shaw L, Lithgow JK, Foster SJ, England S. 2002. σB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J. Bacteriol. 184:5457-5467. http://dx.doi.org/10.1128/JB.184.19.5457-5467.2002.