1887

Abstract

Isothiocyanates (ITCs) are natural plant products generated by the enzymic hydrolysis of glucosinolates found in Brassicaceae vegetables. These natural sulfur compounds and their dithiocarbamate conjugates have been previously evaluated for their anti-cancerous properties. Their antimicrobial properties have been previously studied as well, mainly for food preservation and plant pathogen control. Recently, several revelations concerning the mode of action of ITCs in prokaryotes have emerged. This review addresses these new studies and proposes a model to summarize the current knowledge and hypotheses for the antibacterial effect of ITCs and whether they may provide the basis for the design of novel antibiotics.

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2015-02-01
2019-09-16
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References

  1. Agerbirk N. , Olsen C. E. . ( 2012; ). Glucosinolate structures in evolution. . Phytochemistry 77:, 16–45. [CrossRef] [PubMed]
    [Google Scholar]
  2. Ahn E. , Kim J. , Shin D. . ( 2001; ). Antimicrobial effects of allyl isothiocyanate on several microorganisms. . Korean J Food Sci Technol 31:, 206–211.
    [Google Scholar]
  3. Aires A. , Mota V. R. , Saavedra M. J. , Monteiro A. A. , Simões M. , Rosa E. A. , Bennett R. N. . ( 2009a; ). Initial in vitro evaluations of the antibacterial activities of glucosinolate enzymatic hydrolysis products against plant pathogenic bacteria. . J Appl Microbiol 106:, 2096–2105. [CrossRef] [PubMed]
    [Google Scholar]
  4. Aires A. , Mota V. R. , Saavedra M. J. , Rosa E. A. , Bennett R. N. . ( 2009b; ). The antimicrobial effects of glucosinolates and their respective enzymatic hydrolysis products on bacteria isolated from the human intestinal tract. . J Appl Microbiol 106:, 2086–2095. [CrossRef] [PubMed]
    [Google Scholar]
  5. Aslund F. , Berndt K. D. , Holmgren A. . ( 1997; ). Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct protein-protein redox equilibria. . J Biol Chem 272:, 30780–30786. [CrossRef] [PubMed]
    [Google Scholar]
  6. Bacon J. R. , Plumb G. W. , Howie A. F. , Beckett G. J. , Wang W. , Bao Y. . ( 2007; ). Dual action of sulforaphane in the regulation of thioredoxin reductase and thioredoxin in human HepG2 and Caco-2 cells. . J Agric Food Chem 55:, 1170–1176. [CrossRef] [PubMed]
    [Google Scholar]
  7. Baranova N. , Nikaido H. . ( 2002; ). The BaeSR two-component regulatory system activates transcription of the yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. . J Bacteriol 184:, 4168–4176. [CrossRef] [PubMed]
    [Google Scholar]
  8. Bending G. D. , Lincoln S. D. . ( 2000; ). Inhibition of soil nitrifying bacteria communities and their activities by glucosinolate hydrolysis products. . Soil Biol Biochem 32:, 1261–1269. [CrossRef]
    [Google Scholar]
  9. Borek V. , Morra M. J. , McCaffrey J. P. . ( 1996; ). Myrosinase activity in soil extracts. . Soil Sci Soc Am J 60:, 1792–1797. [CrossRef]
    [Google Scholar]
  10. Borges A. , Serra S. , Abreu A. C. , Saavedra M. J. , Salgado A. , Simões M. . ( 2014; ). Evaluation of the effects of selected phytochemicals on quorum sensing inhibition and in vitro cytotoxicity. . Biofouling 30:, 183–195. [CrossRef] [PubMed]
    [Google Scholar]
  11. Brabban A. D. , Edwards C. . ( 1995; ). The effects of glucosinolates and their hydrolysis products on microbial growth. . J Appl Bacteriol 79:, 171–177. [CrossRef] [PubMed]
    [Google Scholar]
  12. Breier A. , Ziegelhöffer A. . ( 2000; ). “Lysine is the Lord”, thought some scientists in regard to the group interacting with fluorescein isothiocyanate in ATP-binding sites of P-type ATPases but, is it not cysteine?. Gen Physiol Biophys 19:, 253–263.[PubMed]
    [Google Scholar]
  13. Bressan M. , Roncato M. A. , Bellvert F. , Comte G. , Haichar F. Z. , Achouak W. , Berge O. . ( 2009; ). Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. . ISME J 3:, 1243–1257. [CrossRef] [PubMed]
    [Google Scholar]
  14. Brown P. D. , Morra M. J. . ( 1997; ). Control of soil-borne plant pests using glucosinolate-containing plants. . Adv. Agron 61:, 167–231. [CrossRef]
    [Google Scholar]
  15. Chae C. , Sharma S. , Hoskins J. R. , Wickner S. . ( 2004; ). CbpA, a DnaJ homolog, is a DnaK co-chaperone, and its activity is modulated by CbpM. . J Biol Chem 279:, 33147–33153. [CrossRef] [PubMed]
    [Google Scholar]
  16. Chan A. C. , Ager D. , Thompson I. P. . ( 2013; ). Resolving the mechanism of bacterial inhibition by plant secondary metabolites employing a combination of whole-cell biosensors. . J Microbiol Methods 93:, 209–217. [CrossRef] [PubMed]
    [Google Scholar]
  17. Chikhi N. , Holic N. , Guellaen G. , Laperche Y. . ( 1999; ). Gamma-glutamyl transpeptidase gene organization and expression: a comparative analysis in rat, mouse, pig and human species. . Comp Biochem Physiol B Biochem Mol Biol 122:, 367–380. [CrossRef] [PubMed]
    [Google Scholar]
  18. Choesin D. N. , Boerner R. E. J. . ( 1991; ). Allyl isothiocyanate release and the allelopathic potential of Brassica napus (Brassicaceae). . Am J Bot 78:, 1083–1090. [CrossRef]
    [Google Scholar]
  19. Conaway C. C. , Krzeminski J. , Amin S. , Chung F. L. . ( 2001; ). Decomposition rates of isothiocyanate conjugates determine their activity as inhibitors of cytochrome P450 enzymes. . Chem Res Toxicol 14:, 1170–1176. [CrossRef] [PubMed]
    [Google Scholar]
  20. Conaway C. C. , Wang C. X. , Pittman B. , Yang Y. M. , Schwartz J. E. , Tian D. , McIntee E. J. , Hecht S. S. , Chung F. L. . ( 2005; ). Phenethyl isothiocyanate and sulforaphane and their N-acetylcysteine conjugates inhibit malignant progression of lung adenomas induced by tobacco carcinogens in A/J mice. . Cancer Res 65:, 8548–8557. [CrossRef] [PubMed]
    [Google Scholar]
  21. Cordeiro R. P. , Krause D. O. , Doria J. H. , Holley R. A. . ( 2014; ). Role of the BaeSR two-component regulatory system in resistance of Escherichia coli O157 : H7 to allyl isothiocyanate. . Food Microbiol 42:, 136–141. [CrossRef] [PubMed]
    [Google Scholar]
  22. David J. R. D. , Ekanayake A. , Singh I. , Farina B. , Meyer M. . ( 2013; ). Effect of white mustard essential oil on inoculated Salmonella sp. in a sauce with particulates. . J Food Prot 76:, 580–587. [CrossRef] [PubMed]
    [Google Scholar]
  23. Delaquis P. J. , Mazza G. . ( 1995; ). Antimicrobial properties of isothiocyanates in food preservation. . Food Technol 49:, 73–84.
    [Google Scholar]
  24. Delaquis P. J. , Sholberg P. L. . ( 1997; ). Antimicrobial activity of gaseous allyl isothiocyanate. . J Food Prot 60:, 943.
    [Google Scholar]
  25. Dinkova-Kostova A. T. , Kostov R. V. . ( 2012; ). Glucosinolates and isothiocyanates in health and disease. . Trends Mol Med 18:, 337–347. [CrossRef] [PubMed]
    [Google Scholar]
  26. Drobnica L. , Sturdík E. . ( 1979; ). The reaction of carbonyl cyanide phenylhydrazones with thiols. . Biochim Biophys Acta 585:, 462–476. [CrossRef] [PubMed]
    [Google Scholar]
  27. Dufour V. , Alazzam B. , Ermel G. , Thepaut M. , Rossero A. , Tresse O. , Baysse C. . ( 2012; ). Antimicrobial activities of isothiocyanates against Campylobacter jejuni isolates. . Front Cell Infect Microbiol 2:, 53. [CrossRef] [PubMed]
    [Google Scholar]
  28. Dufour V. , Stahl M. , Rosenfeld E. , Stintzi A. , Baysse C. . ( 2013; ). Insights into the mode of action of benzyl isothiocyanate on Campylobacter jejuni. . Appl Environ Microbiol 79:, 6958–6968. [CrossRef] [PubMed]
    [Google Scholar]
  29. EFSA ( 2010; ). EFSA Panel on Food Additives and Nutrient Sources added to Food (ANS): scientific opinion on the safety of allyl isothiocyanate for the proposed uses as a food additive. . EFSA Journal 8:, 1943–1983.
    [Google Scholar]
  30. Fahey R. C. , Sundquist A. R. . ( 1991; ). Evolution of glutathione metabolism. . Adv Enzymol Relat Areas Mol Biol 64:, 1–53.[PubMed]
    [Google Scholar]
  31. Fahey J. W. , Zalcmann A. T. , Talalay P. . ( 2001; ). The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. . Phytochemistry 56:, 5–51. [CrossRef] [PubMed]
    [Google Scholar]
  32. Fahey J. W. , Haristoy X. , Dolan P. M. , Kensler T. W. , Scholtus I. , Stephenson K. K. , Talalay P. , Lozniewski A. . ( 2002; ). Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. . Proc Natl Acad Sci U S A 99:, 7610–7615. [CrossRef] [PubMed]
    [Google Scholar]
  33. Fahey J. W. , Wehage S. L. , Holtzclaw W. D. , Kensler T. W. , Egner P. A. , Shapiro T. A. , Talalay P. . ( 2012; ). Protection of humans by plant glucosinolates: efficiency of conversion of glucosinolates to isothiocyanates by the gastrointestinal microflora. . Cancer Prev Res (Phila) 5:, 603–611. [CrossRef] [PubMed]
    [Google Scholar]
  34. Fahey J. W. , Stephenson K. K. , Wade K. L. , Talalay P. . ( 2013; ). Urease from Helicobacter pylori is inactivated by sulforaphane and other isothiocyanates. . Biochem Biophys Res Commun 435:, 1–7. [CrossRef] [PubMed]
    [Google Scholar]
  35. Fan J. , Crooks C. , Creissen G. , Hill L. , Fairhurst S. , Doerner P. , Lamb C. . ( 2011; ). Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis . . Science 331:, 1185–1188. [CrossRef] [PubMed]
    [Google Scholar]
  36. Fargier E. , Mac Aogáin M. , Mooij M. J. , Woods D. F. , Morrissey J. P. , Dobson A. D. , Adams C. , O’Gara F. . ( 2012; ). MexT functions as a redox-responsive regulator modulating disulfide stress resistance in Pseudomonas aeruginosa . . J Bacteriol 194:, 3502–3511. [CrossRef] [PubMed]
    [Google Scholar]
  37. Fetar H. , Gilmour C. , Klinoski R. , Daigle D. M. , Dean C. R. , Poole K. . ( 2011; ). mexEF-oprN multidrug efflux operon of Pseudomonas aeruginosa: regulation by the MexT activator in response to nitrosative stress and chloramphenicol. . Antimicrob Agents Chemother 55:, 508–514. [CrossRef] [PubMed]
    [Google Scholar]
  38. Freitas E. , Aires A. , de Santos Rosa E. A. , Saavedra M. J. . ( 2013; ). Antibacterial activity and synergistic effect between watercress extracts, 2-phenylethyl isothiocyanate and antibiotics against 11 isolates of Escherichia coli from clinical and animal source. . Lett Appl Microbiol 57:, 266–273.[PubMed]
    [Google Scholar]
  39. Gan N. , Wu Y. C. , Brunet M. , Garrido C. , Chung F. L. , Dai C. , Mi L. . ( 2010; ). Sulforaphane activates heat shock response and enhances proteasome activity through up-regulation of Hsp27. . J Biol Chem 285:, 35528–35536. [CrossRef] [PubMed]
    [Google Scholar]
  40. Ganin H. , Rayo J. , Amara N. , Levy N. , Krief P. , Meijler M. M. . ( 2013; ). Sulforaphane and erucin, natural isothiocyanates from broccoli, inhibit bacterial quorum sensing. . Med Chem Commun 4:, 175–179. [CrossRef]
    [Google Scholar]
  41. Gragerov A. , Nudler E. , Komissarova N. , Gaitanaris G. A. , Gottesman M. E. , Nikiforov V. . ( 1992; ). Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. . Proc Natl Acad Sci U S A 89:, 10341–10344. [CrossRef] [PubMed]
    [Google Scholar]
  42. Hanschen F. S. , Brüggemann N. , Brodehl A. , Mewis I. , Schreiner M. , Rohn S. , Kroh L. W. . ( 2012; ). Characterization of products from the reaction of glucosinolate-derived isothiocyanates with cysteine and lysine derivatives formed in either model systems or broccoli sprouts. . J Agric Food Chem 60:, 7735–7745. [CrossRef] [PubMed]
    [Google Scholar]
  43. Hashem F. A. , Saleh M. M. . ( 1999; ). Antimicrobial components of some cruciferae plants (Diplotaxis harra Forsk. and Erucaria microcarpa Boiss.). . Phytother Res 13:, 329–332. [CrossRef] [PubMed]
    [Google Scholar]
  44. Helmann J. D. . ( 2011; ). Bacillithiol, a new player in bacterial redox homeostasis. . Antioxid Redox Signal 15:, 123–133. [CrossRef] [PubMed]
    [Google Scholar]
  45. Hitchcock A. , Hall S. J. , Myers J. D. , Mulholland F. , Jones M. A. , Kelly D. J. . ( 2010; ). Roles of the twin-arginine translocase and associated chaperones in the biogenesis of the electron transport chains of the human pathogen Campylobacter jejuni . . Microbiology 156:, 2994–3010. [CrossRef] [PubMed]
    [Google Scholar]
  46. Holmes C. W. , Penn C. W. , Lund P. A. . ( 2010; ). The hrcA and hspR regulons of Campylobacter jejuni . . Microbiology 156:, 158–166. [CrossRef] [PubMed]
    [Google Scholar]
  47. Holmgren A. . ( 1985; ). Thioredoxin. . Annu Rev Biochem 54:, 237–271. [CrossRef] [PubMed]
    [Google Scholar]
  48. Hong E. , Kim G. H. . ( 2008; ). Anticancer and antimicrobial activities of β-phenylethyl isothiocyanate in Brassica rapa L. . Food Sci Technol Res 14:, 377–382. [CrossRef]
    [Google Scholar]
  49. Hwang E. S. , Jeffery E. H. . ( 2005; ). Induction of quinone reductase by sulforaphane and sulforaphane N-acetylcysteine conjugate in murine hepatoma cells. . J Med Food 8:, 198–203. [CrossRef] [PubMed]
    [Google Scholar]
  50. Jakobsen T. H. , Bragason S. K. , Phipps R. K. , Christensen L. D. , van Gennip M. , Alhede M. , Skindersoe M. , Larsen T. O. , Høiby N. . & other authors ( 2012a; ). Food as a source for quorum sensing inhibitors: iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa . . Appl Environ Microbiol 78:, 2410–2421. [CrossRef] [PubMed]
    [Google Scholar]
  51. Jakobsen T. H. , van Gennip M. , Phipps R. K. , Shanmugham M. S. , Christensen L. D. , Alhede M. , Skindersoe M. E. , Rasmussen T. B. , Friedrich K. . & other authors ( 2012b; ). Ajoene, a sulfur-rich molecule from garlic, inhibits genes controlled by quorum sensing. . Antimicrob Agents Chemother 56:, 2314–2325. [CrossRef] [PubMed]
    [Google Scholar]
  52. Jakubíková J. , Sedlák J. , Bod’o J. , Bao Y. . ( 2006; ). Effect of isothiocyanates on nuclear accumulation of NF-κB, Nrf2, and thioredoxin in Caco-2 cells. . J Agric Food Chem 54:, 1656–1662. [CrossRef] [PubMed]
    [Google Scholar]
  53. Jang M. , Hong E. , Kim G. H. . ( 2010; ). Evaluation of antibacterial activity of 3-butenyl, 4-pentenyl, 2-phenylethyl, and benzyl isothiocyanate in Brassica vegetables. . J Food Sci 75:, M412–M416. [CrossRef] [PubMed]
    [Google Scholar]
  54. Jiao D. , Ho C. T. , Foiles P. , Chung F. L. . ( 1994; ). Identification and quantification of the N-acetylcysteine conjugate of allyl isothiocyanate in human urine after ingestion of mustard. . Cancer Epidemiol Biomarkers Prev 3:, 487–492.[PubMed]
    [Google Scholar]
  55. Jiao D. , Conaway C. C. , Wang M. H. , Yang C. S. , Koehl W. , Chung F. L. . ( 1996; ). Inhibition of N-nitrosodimethylamine demethylase in rat and human liver microsomes by isothiocyanates and their glutathione, l-cysteine, and N-acetyl-l-cysteine conjugates. . Chem Res Toxicol 9:, 932–938. [CrossRef] [PubMed]
    [Google Scholar]
  56. Jimenez P. N. , Koch G. , Thompson J. A. , Xavier K. B. , Cool R. H. , Quax W. J. . ( 2012; ). The multiple signaling systems regulating virulence in Pseudomonas aeruginosa . . Microbiol Mol Biol Rev 76:, 46–65. [CrossRef] [PubMed]
    [Google Scholar]
  57. Jin S. W. , Chen G. X. , Palacz Z. , Wittmann-Liebold B. . ( 1986; ). A new sensitive Edman-type reagent: 4-(N-1-dimethylaminonaphthalene-5-sulfonylamino)phenyl isothiocyanate. Its synthesis and application for micro-sequencing of polypeptides. . FEBS Lett 198:, 150–154. [CrossRef] [PubMed]
    [Google Scholar]
  58. Kassahun K. , Davis M. , Hu P. , Martin B. , Baillie T. . ( 1997; ). Biotransformation of the naturally occurring isothiocyanate sulforaphane in the rat: identification of phase I metabolites and glutathione conjugates. . Chem Res Toxicol 10:, 1228–1233. [CrossRef] [PubMed]
    [Google Scholar]
  59. Kawakami T. , Kuroki M. , Ishii M. , Igarashi Y. , Arai H. . ( 2010; ). Differential expression of multiple terminal oxidases for aerobic respiration in Pseudomonas aeruginosa. . Environ Microbiol 12:, 1399–1412.[PubMed]
    [Google Scholar]
  60. Kim M. G. , Lee H. S. . ( 2009; ). Growth-inhibiting activities of phenethyl isothiocyanate and its derivatives against intestinal bacteria. . J Food Sci 74:, M467–M471. [CrossRef] [PubMed]
    [Google Scholar]
  61. Kjaer A. , Conti J. . ( 1954; ). Isothiocynates. VII. A convenient synthesis of erysoline (gamma-methylsulphonylbutyl isothiocyanate). . Acta Chem Scand 8:, 295–298. [CrossRef]
    [Google Scholar]
  62. Köhler T. , Michéa-Hamzehpour M. , Henze U. , Gotoh N. , Curty L. K. , Pechère J. C. . ( 1997; ). Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa . . Mol Microbiol 23:, 345–354. [CrossRef] [PubMed]
    [Google Scholar]
  63. Kojima M. , Ogawa K. . ( 1971; ). Studies on the effects of isothiocyanates and their analogues on microorganisms. . J Ferment Technol 49:, 740–746.
    [Google Scholar]
  64. Kolm R. H. , Danielson U. H. , Zhang Y. , Talalay P. , Mannervik B. . ( 1995; ). Isothiocyanates as substrates for human glutathione transferases: structure–activity studies. . Biochem J 311:, 453–459.[PubMed]
    [Google Scholar]
  65. Koroleva O. A. , Gibson T. M. , Cramer R. , Stain C. . ( 2010; ). Glucosinolate-accumulating S-cells in Arabidopsis leaves and flower stalks undergo programmed cell death at early stages of differentiation. . Plant J 64:, 456–469. [CrossRef] [PubMed]
    [Google Scholar]
  66. Krause G. , Holmgren A. . ( 1991; ). Substitution of the conserved tryptophan 31 in Escherichia coli thioredoxin by site-directed mutagenesis and structure–function analysis. . J Biol Chem 266:, 4056–4066.[PubMed]
    [Google Scholar]
  67. Li M. , Ni N. , Chou H.-T. , Lu C.-D. , Tai P. C. , Wang B. . ( 2008; ). Structure-based discovery and experimental verification of novel AI-2 quorum sensing inhibitors against Vibrio harveyi . . Chem Med Chem 3:, 1242–1249. [CrossRef] [PubMed]
    [Google Scholar]
  68. Li Y. , Zhang T. , Schwartz S. J. , Sun D. . ( 2011; ). Sulforaphane potentiates the efficacy of 17-allylamino 17-demethoxygeldanamycin against pancreatic cancer through enhanced abrogation of Hsp90 chaperone function. . Nutr Cancer 63:, 1151–1159. [CrossRef] [PubMed]
    [Google Scholar]
  69. Lin C. M. , Preston J. F. III , Wei C. I. . ( 2000; ). Antibacterial mechanism of allyl isothiocyanate. . J Food Prot 63:, 727–734.[PubMed]
    [Google Scholar]
  70. Luciano F. B. , Holley R. A. . ( 2009; ). Enzymatic inhibition by allyl isothiocyanate and factors affecting its antimicrobial action against Escherichia coli O157 : H7. . Int J Food Microbiol 131:, 240–245. [CrossRef] [PubMed]
    [Google Scholar]
  71. Lund P. A. . ( 2001; ). Microbial molecular chaperones. . Adv Microb Physiol 44:, 93–140. [CrossRef] [PubMed]
    [Google Scholar]
  72. MacGibbon D. B. , Beuzenberg E. J. . ( 1978; ). Location of glucosinolase in Brevicoryne brassicae and Lipaphis erysimi (Aphididae). . N Z J Sci 21:, 389–392.
    [Google Scholar]
  73. Martin J. L. . ( 1995; ). Thioredoxin—a fold for all reasons. . Structure 3:, 245–250. [CrossRef] [PubMed]
    [Google Scholar]
  74. Melchini A. , Traka M. H. . ( 2010; ). Biological profile of erucin: a new promising anticancer agent from cruciferous vegetables. . Toxins 2:, 593–612. [CrossRef] [PubMed]
    [Google Scholar]
  75. Meyer D. J. , Crease D. J. , Ketterer B. . ( 1995; ). Forward and reverse catalysis and product sequestration by human glutathione S-transferases in the reaction of GSH with dietary aralkyl isothiocyanates. . Biochem J 306:, 565–569.[PubMed]
    [Google Scholar]
  76. Mi L. , Xiao Z. , Hood B. L. , Dakshanamurthy S. , Wang X. , Govind S. , Conrads T. P. , Veenstra T. D. , Chung F. L. . ( 2008; ). Covalent binding to tubulin by isothiocyanates. A mechanism of cell growth arrest and apoptosis. . J Biol Chem 283:, 22136–22146. [CrossRef] [PubMed]
    [Google Scholar]
  77. Mi L. , Di Pasqua A. J. , Chung F.-L. . ( 2011; ). Proteins as binding targets of isothiocyanates in cancer prevention. . Carcinogenesis 32:, 1405–1413. [CrossRef] [PubMed]
    [Google Scholar]
  78. Nadarajah D. , Han J. H. , Holley R. A. . ( 2005; ). Use of mustard flour to inactivate Escherichia coli O157 : H7 in ground beef under nitrogen flushed packaging. . Int J Food Microbiol 99:, 257–267. [CrossRef] [PubMed]
    [Google Scholar]
  79. Nagahara N. , Matsumura T. , Okamoto R. , Kajihara Y. . ( 2009; ). Protein cysteine modifications: (2) reactivity specificity and topics of medicinal chemistry and protein engineering. . Curr Med Chem 16:, 4490–4501. [CrossRef] [PubMed]
    [Google Scholar]
  80. Nakamura T. , Kawai Y. , Kitamoto N. , Osawa T. , Kato Y. . ( 2009; ). Covalent modification of lysine residues by allyl isothiocyanate in physiological conditions: plausible transformation of isothiocyanate from thiol to amine. . Chem Res Toxicol 22:, 536–542. [CrossRef] [PubMed]
    [Google Scholar]
  81. Newton G. L. , Arnold K. , Price M. S. , Sherrill C. , Delcardayre S. B. , Aharonowitz Y. , Cohen G. , Davies J. , Fahey R. C. , Davis C. . ( 1996; ). Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes. . J Bacteriol 178:, 1990–1995.[PubMed]
    [Google Scholar]
  82. Newton G. L. , Fahey R. C. , Rawat M. . ( 2012; ). Detoxification of toxins by bacillithiol in Staphylococcus aureus . . Microbiology 158:, 1117–1126. [CrossRef] [PubMed]
    [Google Scholar]
  83. Nowicki D. , Maciąg-Dorszyńska M. , Kobiela W. , Herman-Antosiewicz A. , Węgrzyn A. , Szalewska-Pałasz A. , Węgrzyn G. . ( 2014; ). Phenethyl isothiocyanate inhibits Shiga toxin production in enterohemorrhagic Escherichia coli by stringent response induction. . Antimicrob Agents Chemother 58:, 2304–2315. [CrossRef] [PubMed]
    [Google Scholar]
  84. Nugon-Baudon L. , Rabot S. . ( 1994; ). Glucosinolates and glucosinolate derivatives: implications for protection against chemical carcinogenesis. . Nutr Res Rev 7:, 205–231. [CrossRef] [PubMed]
    [Google Scholar]
  85. Ohtsuru M. , Tsuruo I. , Hata T. . ( 1969; ). Studies on fungous myrosinase. Part II. Effects of various reagents on its enzymatic activities. . Agric Biol Chem 33:, 1315–1319. [CrossRef]
    [Google Scholar]
  86. Palaniappan K. , Holley R. A. . ( 2010; ). Use of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. . Int J Food Microbiol 140:, 164–168. [CrossRef] [PubMed]
    [Google Scholar]
  87. Park I. K. , Choi K. S. , Kim D. H. , Choi I. H. , Kim L. S. , Bak W. C. , Choi J. W. , Shin S. C. . ( 2006; ). Fumigant activity of plant essential oils and components from horseradish (Armoracia rusticana), anise (Pimpinella anisum) and garlic (Allium sativum) oils against Lycoriella ingenua (Diptera: Sciaridae). . Pest Manag Sci 62:, 723–728. [CrossRef] [PubMed]
    [Google Scholar]
  88. Peng H. , Cheng Y. , Ni N. , Li M. , Choudhary G. , Chou H. T. , Lu C. D. , Tai P. C. , Wang B. . ( 2009; ). Synthesis and evaluation of new antagonists of bacterial quorum sensing in Vibrio harveyi . . Chem Med Chem 4:, 1457–1468. [CrossRef] [PubMed]
    [Google Scholar]
  89. Podhradský D. , Drobnica L. , Kristian P. . ( 1979; ). Reactions of cysteine, its derivatives, glutathione coenzyme A, and dihydrolipoic acid with isothiocyanates. . Experientia 35:, 154–155. [CrossRef] [PubMed]
    [Google Scholar]
  90. Roos G. , Foloppe N. , Van Laer K. , Wyns L. , Nilsson L. , Geerlings P. , Messens J. . ( 2009; ). How thioredoxin dissociates its mixed disulfide. . PLOS Comput Biol 5:, e1000461. [CrossRef] [PubMed]
    [Google Scholar]
  91. Rosa E. A. , Rodriguez P. M. . ( 1999; ). Towards a more sustainable agriculture system: the effect of glucosinolates on the control of soil-borne diseases. . J Hortic Sci Biotechnol 74:, 667–674.
    [Google Scholar]
  92. Saavedra M. J. , Borges A. , Dias C. , Aires A. , Bennett R. N. , Rosa E. S. , Simões M. . ( 2010; ). Antimicrobial activity of phenolics and glucosinolate hydrolysis products and their synergy with streptomycin against pathogenic bacteria. . Med Chem 6:, 174–183. [CrossRef] [PubMed]
    [Google Scholar]
  93. Sarkar R. , Mukherjee S. , Biswas J. , Roy M. . ( 2012; ). Sulphoraphane, a naturally occurring isothiocyanate induces apoptosis in breast cancer cells by targeting heat shock proteins. . Biochem Biophys Res Commun 427:, 80–85. [CrossRef] [PubMed]
    [Google Scholar]
  94. Schreiner R. P. , Koide R. T. . ( 1993; ). Mustard, mustard oils and mycorrhizas. . New Phytol 123:, 107–113. [CrossRef]
    [Google Scholar]
  95. Sellam A. , Poupard P. , Simoneau P. . ( 2006; ). Molecular cloning of AbGst1 encoding a glutathione transferase differentially expressed during exposure of Alternaria brassicicola to isothiocyanates. . FEMS Microbiol Lett 258:, 241–249. [CrossRef] [PubMed]
    [Google Scholar]
  96. Sheehan D. , Meade G. , Foley V. M. , Dowd C. A. . ( 2001; ). Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. . Biochem J 360:, 1–16. [CrossRef] [PubMed]
    [Google Scholar]
  97. Shin J. , Harte B. , Ryser E. , Selke S. . ( 2010; ). Active packaging of fresh chicken breast, with allyl isothiocyanate (AITC) in combination with modified atmosphere packaging (MAP) to control the growth of pathogens. . J Food Sci 75:, M65–M71. [CrossRef] [PubMed]
    [Google Scholar]
  98. Singh S. V. , Singh K. . ( 2012; ). Cancer chemoprevention with dietary isothiocyanates mature for clinical translational research. . Carcinogenesis 33:, 1833–1842. [CrossRef] [PubMed]
    [Google Scholar]
  99. Snyder G. H. , Cennerazzo M. J. , Karalis A. J. , Locey D. . ( 1981; ). Electrostatic influence of local cysteine environments on disulfide exchange kinetics. . Biochemistry 20:, 6509–6519. [CrossRef] [PubMed]
    [Google Scholar]
  100. Sofrata A. , Santangelo E. M. , Azeem M. , Borg-Karlson A. K. , Gustafsson A. , Pütsep K. . ( 2011; ). Benzyl isothiocyanate, a major component from the roots of Salvadora persica is highly active against Gram-negative bacteria. . PLoS ONE 6:, e23045. [CrossRef] [PubMed]
    [Google Scholar]
  101. Tajima H. , Kimoto H. , Taketo Y. , Taketo A. . ( 1998; ). Effects of synthetic hydroxy isothiocyanates on microbial systems. . Biosci Biotechnol Biochem 62:, 491–495. [CrossRef] [PubMed]
    [Google Scholar]
  102. Tajima H. , Kimoto H. , Taketo A. . ( 2001; ). Specific antimicrobial synergism of synthetic hydroxy isothiocyanates with aminoglycoside antibiotics. . Biosci Biotechnol Biochem 65:, 1886–1888. [CrossRef] [PubMed]
    [Google Scholar]
  103. Tajima H. , Kimoto H. , Taketo A. . ( 2003; ). Paradoxical effect of synthetic hydroxy isothiocyanates on antimicrobial action of aminoglycosides. . Biosci Biotechnol Biochem 67:, 1844–1846. [CrossRef] [PubMed]
    [Google Scholar]
  104. Tani N. , Ohtsuru M. , Hata T. . ( 1974a; ). Isolation of myrosinase producing microorganism. . Agric Biol Chem 38:, 1617–1622. [CrossRef]
    [Google Scholar]
  105. Tani N. , Ohtsuru M. , Hata T. . ( 1974b; ). Purification and general characteristics of bacterial myrosinase produced by Enterobacter cloacae . . Agric Biol Chem 38:, 1623–1630. [CrossRef]
    [Google Scholar]
  106. Tanito M. , Masutani H. , Kim Y. C. , Nishikawa M. , Ohira A. , Yodoi J. . ( 2005; ). Sulforaphane induces thioredoxin through the antioxidant-responsive element and attenuates retinal light damage in mice. . Invest Ophthalmol Vis Sci 46:, 979–987. [CrossRef] [PubMed]
    [Google Scholar]
  107. Tate S. S. , Meister A. . ( 1981; ). γ-Glutamyl transpeptidase: catalytic, structural and functional aspects. . Mol Cell Biochem 39:, 357–368. [CrossRef] [PubMed]
    [Google Scholar]
  108. Tierens K. F. , Thomma B. P. , Brouwer M. , Schmidt J. , Kistner K. , Porzel A. , Mauch-Mani B. , Cammue B. P. , Broekaert W. F. . ( 2001; ). Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. . Plant Physiol 125:, 1688–1699. [CrossRef] [PubMed]
    [Google Scholar]
  109. Toledano M. B. , Kumar C. , Le Moan N. , Spector D. , Tacnet F. . ( 2007; ). The system biology of thiol redox system in Escherichia coli and yeast: differential functions in oxidative stress, iron metabolism and DNA synthesis. . FEBS Lett 581:, 3598–3607. [CrossRef] [PubMed]
    [Google Scholar]
  110. Uda Y. , Matsuoka H. , Kumagami H. , Shims H. , Meede Y. . ( 1993; ). Stability and antimicrobial property of 4-methylthio-8-butenyl isothiocyanate, the pungent principle in radish. . Nippon Shokuhin Kogyo Gakkaishi 40:, 743–746.[CrossRef]
    [Google Scholar]
  111. Wiktelius E. , Stenberg G. . ( 2007; ). Novel class of glutathione transferases from cyanobacteria exhibit high catalytic activities towards naturally occurring isothiocyanates. . Biochem J 406:, 115–123. [CrossRef] [PubMed]
    [Google Scholar]
  112. Wilson E. A. , Ennahar S. , Marchioni E. , Bergaentzlé M. , Bindler F. . ( 2012; ). Improvement in determination of isothiocyanates using high-temperature reversed-phase HPLC. . J Sep Sci 35:, 2026–2031. [CrossRef] [PubMed]
    [Google Scholar]
  113. Yamasaki M. , Igimi S. , Katayama Y. , Yamamoto S. , Amano F. . ( 2004; ). Identification of an oxidative stress-sensitive protein from Campylobacter jejuni, homologous to rubredoxin oxidoreductase/rubrerythrin. . FEMS Microbiol Lett 235:, 57–63. [CrossRef] [PubMed]
    [Google Scholar]
  114. Ye L. , Zhang Y. . ( 2001; ). Total intracellular accumulation levels of dietary isothiocyanates determine their activity in elevation of cellular glutathione and induction of Phase 2 detoxification enzymes. . Carcinogenesis 22:, 1987–1992. [CrossRef] [PubMed]
    [Google Scholar]
  115. Yu E. Y. , Pickering I. J. , George G. N. , Prince R. C. . ( 2001; ). In situ observation of the generation of isothiocyanates from sinigrin in horseradish and wasabi. . Biochim Biophys Acta 1527:, 156–160. [CrossRef] [PubMed]
    [Google Scholar]
  116. Zeller T. , Klug G. . ( 2006; ). Thioredoxins in bacteria: functions in oxidative stress response and regulation of thioredoxin genes. . Naturwissenschaften 93:, 259–266. [CrossRef] [PubMed]
    [Google Scholar]
  117. Zhang Y. . ( 2000; ). Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells. . Carcinogenesis 21:, 1175–1182. [CrossRef] [PubMed]
    [Google Scholar]
  118. Zhang Y. . ( 2012; ). The molecular basis that unifies the metabolism, cellular uptake and chemopreventive activities of dietary isothiocyanates. . Carcinogenesis 33:, 2–9. [CrossRef] [PubMed]
    [Google Scholar]
  119. Zhang Y. , Talalay P. . ( 1998; ). Mechanism of differential potencies of isothiocyanates as inducers of anticarcinogenic Phase 2 enzymes. . Cancer Res 58:, 4632–4639.[PubMed]
    [Google Scholar]
  120. Zhang J. , Svehlíková V. , Bao Y. , Howie A. F. , Beckett G. J. , Williamson G. . ( 2003; ). Synergy between sulforaphane and selenium in the induction of thioredoxin reductase 1 requires both transcriptional and translational modulation. . Carcinogenesis 24:, 497–503. [CrossRef] [PubMed]
    [Google Scholar]
  121. Zoetendal E. G. , Smith A. H. , Sundset M. A. , Mackie R. I. . ( 2008; ). The BaeSR two-component regulatory system mediates resistance to condensed tannins in Escherichia coli . . Appl Environ Microbiol 74:, 535–539. [CrossRef] [PubMed]
    [Google Scholar]
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