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Current Medicinal Chemistry

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ISSN (Online): 1875-533X

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Review Article

Targeting Bacterial Antioxidant Systems for Antibiotics Development

Author(s): Xiaoyuan Ren*, Lili Zou and Arne Holmgren*

Volume 27, Issue 12, 2020

Page: [1922 - 1939] Pages: 18

DOI: 10.2174/0929867326666191007163654

Price: $65

Open Access Journals Promotions 2
Abstract

The emergence of multidrug-resistant bacteria has become an urgent issue in modern medicine which requires novel strategies to develop antibiotics. Recent studies have supported the hypothesis that antibiotic-induced bacterial cell death is mediated by Reactive Oxygen Species (ROS). The hypothesis also highlighted the importance of antioxidant systems, the defense mechanism which contributes to antibiotic resistance. Thioredoxin and glutathione systems are the two major thiol-dependent systems which not only provide antioxidant capacity but also participate in various biological events in bacteria, such as DNA synthesis and protein folding. The biological importance makes them promising targets for novel antibiotics development. Based on the idea, ebselen and auranofin, two bacterial thioredoxin reductase inhibitors, have been found to inhibit the growth of bacteria lacking the GSH efficiently. A recent study combining ebselen and silver exhibited a strong synergistic effect against Multidrug-Resistant (MDR) Gram-negative bacteria which possess both thioredoxin and glutathione systems. These drug-repurposing studies are promising for quick clinical usage due to their well-known profile.

Keywords: Multi-drug resistant bacteria, antibiotics, ROS, thioredoxin system, glutathione system, ebselen, silver.

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[1]
Fleming, A. On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzae. 1929. Bull. World Health Organ., 2001, 79(8), 780-790.
[PMID: 11545337]
[2]
Nathan, C.; Cars, O. Antibiotic resistance--problems, progress, and prospects. N. Engl. J. Med., 2014, 371(19), 1761-1763.
[http://dx.doi.org/10.1056/NEJMp1408040] [PMID: 25271470]
[3]
Levy, S.B.; Marshall, B. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med., 2004, 10(12)(Suppl.), S122-S129.
[http://dx.doi.org/10.1038/nm1145] [PMID: 15577930]
[4]
Abdelmohsen, U.R.; Balasubramanian, S.; Oelschlaeger, T.A.; Grkovic, T.; Pham, N.B.; Quinn, R.J.; Hentschel, U. Potential of marine natural products against drug-resistant fungal, viral, and parasitic infections. Lancet Infect. Dis., 2017, 17(2), e30-e41.
[http://dx.doi.org/10.1016/S1473-3099(16)30323-1] [PMID: 27979695]
[5]
Silver, L.L. Challenges of antibacterial discovery. Clin. Microbiol. Rev., 2011, 24(1), 71-109.
[http://dx.doi.org/10.1128/CMR.00030-10] [PMID: 21233508]
[6]
Kohanski, M.A.; Dwyer, D.J.; Collins, J.J. How antibiotics kill bacteria: from targets to networks. Nat. Rev. Microbiol., 2010, 8(6), 423-435.
[http://dx.doi.org/10.1038/nrmicro2333] [PMID: 20440275]
[7]
Van Acker, H.; Coenye, T. The Role of Reactive Oxygen Species in Antibiotic-Mediated Killing of Bacteria. Trends Microbiol., 2017, 25(6), 456-466.
[http://dx.doi.org/10.1016/j.tim.2016.12.008] [PMID: 28089288]
[8]
Dwyer, D.J.; Collins, J.J.; Walker, G.C. Unraveling the physiological complexities of antibiotic lethality. Annu. Rev. Pharmacol. Toxicol., 2015, 55, 313-332.
[http://dx.doi.org/10.1146/annurev-pharmtox-010814-124712] [PMID: 25251995]
[9]
Valko, M.; Rhodes, C.J.; Moncol, J.; Izakovic, M.; Mazur, M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact., 2006, 160(1), 1-40.
[http://dx.doi.org/10.1016/j.cbi.2005.12.009] [PMID: 16430879]
[10]
Pryor, W.A. Oxy-radicals and related species: their formation, lifetimes, and reactions. Annu. Rev. Physiol., 1986, 48, 657-667.
[http://dx.doi.org/10.1146/annurev.ph.48.030186.003301] [PMID: 3010829]
[11]
Kohchi, C.; Inagawa, H.; Nishizawa, T.; Soma, G. ROS and innate immunity. Anticancer Res., 2009, 29(3), 817-821.
[PMID: 19414314]
[12]
Babior, B.M.; Kipnes, R.S.; Curnutte, J.T. Biological defense mechanisms. The production by leukocytes of superoxide, a potential bactericidal agent. J. Clin. Invest., 1973, 52(3), 741-744.
[http://dx.doi.org/10.1172/JCI107236] [PMID: 4346473]
[13]
Valenti, S.; Cuttica, C.M.; Giusti, M.; Giordano, G. Nitric oxide modulates Leydig cell function in vitro: is this a way of communication between the immune and endocrine system in the testis? Ann. N. Y. Acad. Sci., 1999, 876, 298-300.
[http://dx.doi.org/10.1111/j.1749-6632.1999.tb07652.x] [PMID: 10415623]
[14]
Greenberg, J.T.; Monach, P.; Chou, J.H.; Josephy, P.D.; Demple, B. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc. Natl. Acad. Sci. USA, 1990, 87(16), 6181-6185.
[http://dx.doi.org/10.1073/pnas.87.16.6181] [PMID: 1696718]
[15]
Goswami, M.; Mangoli, S.H.; Jawali, N. Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrob. Agents Chemother., 2006, 50(3), 949-954.
[http://dx.doi.org/10.1128/AAC.50.3.949-954.2006] [PMID: 16495256]
[16]
Goswami, M.; Mangoli, S.H.; Jawali, N. Effects of glutathione and ascorbic acid on streptomycin sensitivity of Escherichia coli. Antimicrob. Agents Chemother., 2007, 51(3), 1119-1122.
[http://dx.doi.org/10.1128/AAC.00779-06] [PMID: 17210778]
[17]
Utaida, S.; Dunman, P.M.; Macapagal, D.; Murphy, E.; Projan, S.J.; Singh, V.K.; Jayaswal, R.K.; Wilkinson, B.J. Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology, 2003, 149(Pt 10), 2719-2732.
[http://dx.doi.org/10.1099/mic.0.26426-0] [PMID: 14523105]
[18]
Waddell, S.J.; Stabler, R.A.; Laing, K.; Kremer, L.; Reynolds, R.C.; Besra, G.S. The use of microarray analysis to determine the gene expression profiles of Mycobacterium tuberculosis in response to anti-bacterial compounds. Tuberculosis (Edinb.), 2004, 84(3-4), 263-274.
[http://dx.doi.org/10.1016/j.tube.2003.12.005] [PMID: 15207496]
[19]
Becerra, M.C.; Albesa, I. Oxidative stress induced by ciprofloxacin in Staphylococcus aureus. Biochem. Biophys. Res. Commun., 2002, 297(4), 1003-1007.
[http://dx.doi.org/10.1016/S0006-291X(02)02331-8] [PMID: 12359254]
[20]
Albesa, I.; Becerra, M.C.; Battán, P.C.; Páez, P.L. Oxidative stress involved in the antibacterial action of different antibiotics. Biochem. Biophys. Res. Commun., 2004, 317(2), 605-609.
[http://dx.doi.org/10.1016/j.bbrc.2004.03.085] [PMID: 15063800]
[21]
Kohanski, M.A.; Dwyer, D.J.; Hayete, B.; Lawrence, C.A.; Collins, J.J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell, 2007, 130(5), 797-810.
[http://dx.doi.org/10.1016/j.cell.2007.06.049] [PMID: 17803904]
[22]
Wang, X.; Zhao, X. Contribution of oxidative damage to antimicrobial lethality. Antimicrob. Agents Chemother., 2009, 53(4), 1395-1402.
[http://dx.doi.org/10.1128/AAC.01087-08] [PMID: 19223646]
[23]
Foti, J.J.; Devadoss, B.; Winkler, J.A.; Collins, J.J.; Walker, G.C. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science, 2012, 336(6079), 315-319.
[http://dx.doi.org/10.1126/science.1219192] [PMID: 22517853]
[24]
Thomas, V.C.; Kinkead, L.C.; Janssen, A.; Schaeffer, C.R.; Woods, K.M.; Lindgren, J.K.; Peaster, J.M.; Chaudhari, S.S.; Sadykov, M.; Jones, J.; AbdelGhani, S.M.M.; Zimmerman, M.C.; Bayles, K.W.; Somerville, G.A.; Fey, P.D. A dysfunctional tricarboxylic acid cycle enhances fitness of Staphylococcus epidermidis during β-lactam stress. MBio, 2013, 4(4), e00437-e13.
[PMID: 23963176]
[25]
Liou, J.W.; Hung, Y.J.; Yang, C.H.; Chen, Y.C. The antimicrobial activity of gramicidin A is associated with hydroxyl radical formation. PLoS One, 2015, 10(1)e0117065
[http://dx.doi.org/10.1371/journal.pone.0117065] [PMID: 25622083]
[26]
Duan, X.; Huang, X.; Wang, X.; Yan, S.; Guo, S.; Abdalla, A.E.; Huang, C.; Xie, J. l-Serine potentiates fluoroquinolone activity against Escherichia coli by enhancing endogenous reactive oxygen species production. J. Antimicrob. Chemother., 2016, 71(8), 2192-2199.
[http://dx.doi.org/10.1093/jac/dkw114] [PMID: 27118777]
[27]
Kobayashi, K.; Fujikawa, M.; Kozawa, T. Oxidative stress sensing by the iron-sulfur cluster in the transcription factor, SoxR. J. Inorg. Biochem., 2014, 133, 87-91.
[http://dx.doi.org/10.1016/j.jinorgbio.2013.11.008] [PMID: 24332474]
[28]
Pomposiello, P.J.; Bennik, M.H.J.; Demple, B. Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J. Bacteriol., 2001, 183(13), 3890-3902.
[http://dx.doi.org/10.1128/JB.183.13.3890-3902.2001] [PMID: 11395452]
[29]
Choi, H.; Kim, S.; Mukhopadhyay, P.; Cho, S.; Woo, J.; Storz, G.; Ryu, S.E. Structural basis of the redox switch in the OxyR transcription factor. Cell, 2001, 105(1), 103-113.
[http://dx.doi.org/10.1016/S0092-8674(01)00300-2] [PMID: 11301006]
[30]
Fahey, R.C.; Brown, W.C.; Adams, W.B.; Worsham, M.B. Occurrence of glutathione in bacteria. J. Bacteriol., 1978, 133(3), 1126-1129.
[http://dx.doi.org/10.1128/JB.133.3.1126-1129.1978] [PMID: 417060]
[31]
Laurent, T.C.; Moore, E.C.; Reichard, P. Enzymatic Synthesis of Deoxyribonucleotides. Iv. Isolation and Characterization of Thioredoxin, the Hydrogen Donor from Escherichia Coli B. J. Biol. Chem., 1964, 239, 3436-3444.
[PMID: 14245400]
[32]
Sengupta, R.; Holmgren, A. Thioredoxin and glutaredoxin-mediated redox regulation of ribonucleotide reductase. World J. Biol. Chem., 2014, 5(1), 68-74.
[http://dx.doi.org/10.4331/wjbc.v5.i1.68] [PMID: 24600515]
[33]
Holmgren, A.; Söderberg, B.O.; Eklund, H.; Brändén, C.I. Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.8 A resolution. Proc. Natl. Acad. Sci. USA, 1975, 72(6), 2305-2309.
[http://dx.doi.org/10.1073/pnas.72.6.2305] [PMID: 1094461]
[34]
Arnér, E.S.; Holmgren, A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem., 2000, 267(20), 6102-6109.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01701.x] [PMID: 11012661]
[35]
Holmgren, A. Thioredoxin. Annu. Rev. Biochem., 1985, 54, 237-271.
[http://dx.doi.org/10.1146/annurev.bi.54.070185.001321] [PMID: 3896121]
[36]
Williams, C.H.; Arscott, L.D.; Müller, S.; Lennon, B.W.; Ludwig, M.L.; Wang, P.F.; Veine, D.M.; Becker, K.; Schirmer, R.H. Thioredoxin reductase two modes of catalysis have evolved. Eur. J. Biochem., 2000, 267(20), 6110-6117.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01702.x] [PMID: 11012662]
[37]
Sandalova, T.; Zhong, L.; Lindqvist, Y.; Holmgren, A.; Schneider, G. Three-dimensional structure of a mammalian thioredoxin reductase: implications for mechanism and evolution of a selenocysteine-dependent enzyme. Proc. Natl. Acad. Sci. USA, 2001, 98(17), 9533-9538.
[http://dx.doi.org/10.1073/pnas.171178698] [PMID: 11481439]
[38]
Zhong, L.; Holmgren, A. Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations. J. Biol. Chem., 2000, 275(24), 18121-18128.
[http://dx.doi.org/10.1074/jbc.M000690200] [PMID: 10849437]
[39]
Arnér, E.S. Focus on mammalian thioredoxin reductases--important selenoproteins with versatile functions. Biochim. Biophys. Acta, 2009, 1790(6), 495-526.
[http://dx.doi.org/10.1016/j.bbagen.2009.01.014] [PMID: 19364476]
[40]
Lennon, B.W.; Williams, C.H., Jr; Ludwig, M.L. Twists in catalysis: alternating conformations of Escherichia coli thioredoxin reductase. Science, 2000, 289(5482), 1190-1194.
[http://dx.doi.org/10.1126/science.289.5482.1190] [PMID: 10947986]
[41]
Lu, J.; Holmgren, A. The thioredoxin antioxidant system. Free Radic. Biol. Med., 2014, 66, 75-87.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.07.036] [PMID: 23899494]
[42]
Poole, L.B.; Reynolds, C.M.; Wood, Z.A.; Karplus, P.A.; Ellis, H.R.; Li Calzi, M. AhpF and other NADH:peroxiredoxin oxidoreductases, homologues of low Mr thioredoxin reductase. Eur. J. Biochem., 2000, 267(20), 6126-6133.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01704.x] [PMID: 11012664]
[43]
Prieto-Alamo, M.J.; Jurado, J.; Gallardo-Madueno, R.; Monje-Casas, F.; Holmgren, A.; Pueyo, C. Transcriptional regulation of glutaredoxin and thioredoxin pathways and related enzymes in response to oxidative stress. J. Biol. Chem., 2000, 275(18), 13398-13405.
[http://dx.doi.org/10.1074/jbc.275.18.13398] [PMID: 10788450]
[44]
Lim, C.J.; Daws, T.; Gerami-Nejad, M.; Fuchs, J.A. Growth-phase regulation of the Escherichia coli thioredoxin gene. Biochim. Biophys. Acta, 2000, 1491(1-3), 1-6.
[http://dx.doi.org/10.1016/S0167-4781(00)00026-9] [PMID: 10760563]
[45]
Sa, J.H.; Namgung, M.A.; Lim, C.J.; Fuchs, J.A. Expression of the Escherichia coli thioredoxin gene is negatively regulated by cyclic AMP. Biochem. Biophys. Res. Commun., 1997, 234(3), 564-567.
[http://dx.doi.org/10.1006/bbrc.1997.6687] [PMID: 9175752]
[46]
Scharf, C.; Riethdorf, S.; Ernst, H.; Engelmann, S.; Völker, U.; Hecker, M. Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis. J. Bacteriol., 1998, 180(7), 1869-1877.
[http://dx.doi.org/10.1128/JB.180.7.1869-1877.1998] [PMID: 9537387]
[47]
Nakano, S.; Küster-Schöck, E.; Grossman, A.D.; Zuber, P. Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc. Natl. Acad. Sci. USA, 2003, 100(23), 13603-13608.
[http://dx.doi.org/10.1073/pnas.2235180100] [PMID: 14597697]
[48]
Li, W.; Stevenson, C.E.M.; Burton, N.; Jakimowicz, P.; Paget, M.S.B.; Buttner, M.J.; Lawson, D.M.; Kleanthous, C. Identification and structure of the anti-sigma factor-binding domain of the disulphide-stress regulated sigma factor sigma(R) from Streptomyces coelicolor. J. Mol. Biol., 2002, 323(2), 225-236.
[http://dx.doi.org/10.1016/S0022-2836(02)00948-8] [PMID: 12381317]
[49]
Manganelli, R.; Voskuil, M.I.; Schoolnik, G.K.; Dubnau, E.; Gomez, M.; Smith, I. Role of the extracytoplasmic-function sigma factor sigma(H) in Mycobacterium tuberculosis global gene expression. Mol. Microbiol., 2002, 45(2), 365-374.
[http://dx.doi.org/10.1046/j.1365-2958.2002.03005.x] [PMID: 12123450]
[50]
Aslund, F.; Zheng, M.; Beckwith, J.; Storz, G. Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl. Acad. Sci. USA, 1999, 96(11), 6161-6165.
[http://dx.doi.org/10.1073/pnas.96.11.6161] [PMID: 10339558]
[51]
Fernandes, A.P.; Holmgren, A. Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid. Redox Signal., 2004, 6(1), 63-74.
[http://dx.doi.org/10.1089/152308604771978354] [PMID: 14713336]
[52]
Holmgren, A. Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc. Natl. Acad. Sci. USA, 1976, 73(7), 2275-2279.
[http://dx.doi.org/10.1073/pnas.73.7.2275] [PMID: 7783]
[53]
Zheng, M.; Aslund, F.; Storz, G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science, 1998, 279(5357), 1718-1721.
[http://dx.doi.org/10.1126/science.279.5357.1718] [PMID: 9497290]
[54]
Potamitou, A.; Neubauer, P.; Holmgren, A.; Vlamis-Gardikas, A. Expression of Escherichia coli glutaredoxin 2 is mainly regulated by ppGpp and sigmaS. J. Biol. Chem., 2002, 277(20), 17775-17780.
[http://dx.doi.org/10.1074/jbc.M201306200] [PMID: 11889138]
[55]
Aslund, F.; Ehn, B.; Miranda-Vizuete, A.; Pueyo, C.; Holmgren, A. Two additional glutaredoxins exist in Escherichia coli: glutaredoxin 3 is a hydrogen donor for ribonucleotide reductase in a thioredoxin/glutaredoxin 1 double mutant. Proc. Natl. Acad. Sci. USA, 1994, 91(21), 9813-9817.
[http://dx.doi.org/10.1073/pnas.91.21.9813] [PMID: 7937896]
[56]
Fernandes, A.P.; Fladvad, M.; Berndt, C.; Andrésen, C.; Lillig, C.H.; Neubauer, P.; Sunnerhagen, M.; Holmgren, A.; Vlamis-Gardikas, A. A novel monothiol glutaredoxin (Grx4) from Escherichia coli can serve as a substrate for thioredoxin reductase. J. Biol. Chem., 2005, 280(26), 24544-24552.
[http://dx.doi.org/10.1074/jbc.M500678200] [PMID: 15833738]
[57]
Yeung, N.; Gold, B.; Liu, N.L.; Prathapam, R.; Sterling, H.J.; Willams, E.R.; Butland, G. The E. coli monothiol glutaredoxin GrxD forms homodimeric and heterodimeric FeS cluster containing complexes. Biochemistry, 2011, 50(41), 8957-8969.
[http://dx.doi.org/10.1021/bi2008883] [PMID: 21899261]
[58]
Berndt, C.; Lillig, C.H.; Holmgren, A. Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: implications for diseases in the cardiovascular system. Am. J. Physiol. Heart Circ. Physiol., 2007, 292(3), H1227-H1236.
[http://dx.doi.org/10.1152/ajpheart.01162.2006] [PMID: 17172268]
[59]
Clarke, D.J.; Ortega, X.P.; Mackay, C.L.; Valvano, M.A.; Govan, J.R.W.; Campopiano, D.J.; Langridge-Smith, P.; Brown, A.R. Subdivision of the bacterioferritin comigratory protein family of bacterial peroxiredoxins based on catalytic activity. Biochemistry, 2010, 49(6), 1319-1330.
[http://dx.doi.org/10.1021/bi901703m] [PMID: 20078128]
[60]
Arenas, F.A.; Díaz, W.A.; Leal, C.A.; Pérez-Donoso, J.M.; Imlay, J.A.; Vásquez, C.C. The Escherichia coli btuE gene, encodes a glutathione peroxidase that is induced under oxidative stress conditions. Biochem. Biophys. Res. Commun., 2010, 398(4), 690-694.
[http://dx.doi.org/10.1016/j.bbrc.2010.07.002] [PMID: 20621065]
[61]
Cheng, C.Y.; Dong, Z.M.; Han, X.; Wang, H.; Jiang, L.; Sun, J.; Yang, Y.C.; Ma, T.T.; Shao, C.Y.; Wang, X.D.; Chen, Z.W.; Fang, W.H.; Freitag, N.E.; Huang, H.R.; Song, H.H. Thioredoxin A Is Essential for Motility and Contributes to Host Infection of Listeria monocytogenes via Redox Interactions; Front Cell Infect Mi, 2017, p. 7.
[62]
Uziel, O.; Borovok, I.; Schreiber, R.; Cohen, G.; Aharonowitz, Y. Transcriptional regulation of the Staphylococcus aureus thioredoxin and thioredoxin reductase genes in response to oxygen and disulfide stress. J. Bacteriol., 2004, 186(2), 326-334.
[http://dx.doi.org/10.1128/JB.186.2.326-334.2004] [PMID: 14702300]
[63]
Ritz, D.; Patel, H.; Doan, B.; Zheng, M.; Aslund, F.; Storz, G.; Beckwith, J. Thioredoxin 2 is involved in the oxidative stress response in Escherichia coli. J. Biol. Chem., 2000, 275(4), 2505-2512.
[http://dx.doi.org/10.1074/jbc.275.4.2505] [PMID: 10644706]
[64]
Helmann, J.D. Bacillithiol, a new player in bacterial redox homeostasis. Antioxid. Redox Signal., 2011, 15(1), 123-133.
[http://dx.doi.org/10.1089/ars.2010.3562] [PMID: 20712413]
[65]
Reichard, P.; Baldesten, A.; Rutberg, L. Formation of deoxycytidine phosphates from cytidine phosphates in extracts from Escherichia coli. J. Biol. Chem., 1961, 236, 1150-1157.
[PMID: 13740426]
[66]
Kolberg, M.; Strand, K.R.; Graff, P.; Andersson, K.K. Structure, function, and mechanism of ribonucleotide reductases. Biochim. Biophys. Acta, 2004, 1699(1-2), 1-34.
[http://dx.doi.org/10.1016/S1570-9639(04)00054-8] [PMID: 15158709]
[67]
Nordlund, P.; Reichard, P. Ribonucleotide reductases. Annu. Rev. Biochem., 2006, 75, 681-706.
[http://dx.doi.org/10.1146/annurev.biochem.75.103004.142443] [PMID: 16756507]
[68]
Bjur, E.; Eriksson-Ygberg, S.; Aslund, F.; Rhen, M. Thioredoxin 1 promotes intracellular replication and virulence of Salmonella enterica serovar Typhimurium. Infect. Immun., 2006, 74(9), 5140-5151.
[http://dx.doi.org/10.1128/IAI.00449-06] [PMID: 16926406]
[69]
Pasternak, C.; Assemat, K.; Clément-Métral, J.D.; Klug, G. Thioredoxin is essential for Rhodobacter sphaeroides growth by aerobic and anaerobic respiration. Microbiology, 1997, 143(Pt 1), 83-91.
[http://dx.doi.org/10.1099/00221287-143-1-83] [PMID: 9025281]
[70]
Inaba, K.; Ito, K. Structure and mechanisms of the DsbB-DsbA disulfide bond generation machine. Biochim. Biophys. Acta, 2008, 1783(4), 520-529.
[http://dx.doi.org/10.1016/j.bbamcr.2007.11.006] [PMID: 18082634]
[71]
Rietsch, A.; Bessette, P.; Georgiou, G.; Beckwith, J. Reduction of the periplasmic disulfide bond isomerase, DsbC, occurs by passage of electrons from cytoplasmic thioredoxin. J. Bacteriol., 1997, 179(21), 6602-6608.
[http://dx.doi.org/10.1128/JB.179.21.6602-6608.1997] [PMID: 9352906]
[72]
Stewart, E.J.; Aslund, F.; Beckwith, J. Disulfide bond formation in the Escherichia coli cytoplasm: an in vivo role reversal for the thioredoxins. EMBO J., 1998, 17(19), 5543-5550.
[http://dx.doi.org/10.1093/emboj/17.19.5543] [PMID: 9755155]
[73]
Hartl, F.U.; Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science, 2002, 295(5561), 1852-1858.
[http://dx.doi.org/10.1126/science.1068408] [PMID: 11884745]
[74]
Hoffmann, J.H.; Linke, K.; Graf, P.C.; Lilie, H.; Jakob, U. Identification of a redox-regulated chaperone network. EMBO J., 2004, 23(1), 160-168.
[http://dx.doi.org/10.1038/sj.emboj.7600016] [PMID: 14685279]
[75]
Shao, F.; Bader, M.W.; Jakob, U.; Bardwell, J.C.; Dsb, G. DsbG, a protein disulfide isomerase with chaperone activity. J. Biol. Chem., 2000, 275(18), 13349-13352.
[http://dx.doi.org/10.1074/jbc.275.18.13349] [PMID: 10788443]
[76]
McCarthy, A.A.; Haebel, P.W.; Törrönen, A.; Rybin, V.; Baker, E.N.; Metcalf, P. Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nat. Struct. Biol., 2000, 7(3), 196-199.
[http://dx.doi.org/10.1038/73295] [PMID: 10700276]
[77]
Kern, R.; Malki, A.; Holmgren, A.; Richarme, G. Chaperone properties of Escherichia coli thioredoxin and thioredoxin reductase. Biochem. J., 2003, 371(Pt 3), 965-972.
[http://dx.doi.org/10.1042/bj20030093] [PMID: 12549977]
[78]
Lill, R.; Mühlenhoff, U. Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu. Rev. Cell Dev. Biol., 2006, 22, 457-486.
[http://dx.doi.org/10.1146/annurev.cellbio.22.010305.104538] [PMID: 16824008]
[79]
Lillig, C.H.; Berndt, C.; Vergnolle, O.; Lönn, M.E.; Hudemann, C.; Bill, E.; Holmgren, A. Characterization of human glutaredoxin 2 as iron-sulfur protein: a possible role as redox sensor. Proc. Natl. Acad. Sci. USA, 2005, 102(23), 8168-8173.
[http://dx.doi.org/10.1073/pnas.0500735102] [PMID: 15917333]
[80]
Tokumoto, U.; Takahashi, Y. Genetic analysis of the isc operon in Escherichia coli involved in the biogenesis of cellular iron-sulfur proteins. J. Biochem., 2001, 130(1), 63-71.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a002963] [PMID: 11432781]
[81]
Johnson, D.C.; Dean, D.R.; Smith, A.D.; Johnson, M.K. Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem., 2005, 74, 247-281.
[http://dx.doi.org/10.1146/annurev.biochem.74.082803.133518] [PMID: 15952888]
[82]
Butland, G.; Babu, M.; Díaz-Mejía, J.J.; Bohdana, F.; Phanse, S.; Gold, B.; Yang, W.; Li, J.; Gagarinova, A.G.; Pogoutse, O.; Mori, H.; Wanner, B.L.; Lo, H.; Wasniewski, J.; Christopolous, C.; Ali, M.; Venn, P.; Safavi-Naini, A.; Sourour, N.; Caron, S.; Choi, J.Y.; Laigle, L.; Nazarians-Armavil, A.; Deshpande, A.; Joe, S.; Datsenko, K.A.; Yamamoto, N.; Andrews, B.J.; Boone, C.; Ding, H.; Sheikh, B.; Moreno-Hagelseib, G.; Greenblatt, J.F.; Emili, A. eSGA: E. coli synthetic genetic array analysis. Nat. Methods, 2008, 5(9), 789-795.
[http://dx.doi.org/10.1038/nmeth.1239] [PMID: 18677321]
[83]
Py, B.; Gerez, C.; Angelini, S.; Planel, R.; Vinella, D.; Loiseau, L.; Talla, E.; Brochier-Armanet, C.; Garcia Serres, R.; Latour, J.M.; Ollagnier-de Choudens, S.; Fontecave, M.; Barras, F. Molecular organization, biochemical function, cellular role and evolution of NfuA, an atypical Fe-S carrier. Mol. Microbiol., 2012, 86(1), 155-171.
[http://dx.doi.org/10.1111/j.1365-2958.2012.08181.x] [PMID: 22966982]
[84]
Boutigny, S.; Saini, A.; Baidoo, E.E.K.; Yeung, N.; Keasling, J.D.; Butland, G. Physical and functional interactions of a monothiol glutaredoxin and an iron sulfur cluster carrier protein with the sulfur-donating radical S-adenosyl-L-methionine enzyme MiaB. J. Biol. Chem., 2013, 288(20), 14200-14211.
[http://dx.doi.org/10.1074/jbc.M113.460360] [PMID: 23543739]
[85]
Yang, Y.; Bazhin, A.V.; Werner, J.; Karakhanova, S. Reactive oxygen species in the immune system. Int. Rev. Immunol., 2013, 32(3), 249-270.
[http://dx.doi.org/10.3109/08830185.2012.755176] [PMID: 23617726]
[86]
Wang, P.F.; Marcinkeviciene, J.; Williams, C.H., Jr; Blanchard, J.S. Thioredoxin reductase-thioredoxin fusion enzyme from Mycobacterium leprae: comparison with the separately expressed thioredoxin reductase. Biochemistry, 1998, 37(46), 16378-16389.
[http://dx.doi.org/10.1021/bi980754e] [PMID: 9819230]
[87]
Helbig, K.; Bleuel, C.; Krauss, G.J.; Nies, D.H. Glutathione and transition-metal homeostasis in Escherichia coli. J. Bacteriol., 2008, 190(15), 5431-5438.
[http://dx.doi.org/10.1128/JB.00271-08] [PMID: 18539744]
[88]
Cameron, J.C.; Pakrasi, H.B. Glutathione facilitates antibiotic resistance and photosystem I stability during exposure to gentamicin in cyanobacteria. Appl. Environ. Microbiol., 2011, 77(10), 3547-3550.
[http://dx.doi.org/10.1128/AEM.02542-10] [PMID: 21460113]
[89]
Liu, A.; Tran, L.; Becket, E.; Lee, K.; Chinn, L.; Park, E.; Tran, K.; Miller, J.H. Antibiotic sensitivity profiles determined with an Escherichia coli gene knockout collection: generating an antibiotic bar code. Antimicrob. Agents Chemother., 2010, 54(4), 1393-1403.
[http://dx.doi.org/10.1128/AAC.00906-09] [PMID: 20065048]
[90]
May, H.C.; Yu, J.J.; Guentzel, M.N.; Chambers, J.P.; Cap, A.P.; Arulanandam, B.P. Repurposing Auranofin, Ebselen, and PX-12 as Antimicrobial Agents Targeting the Thioredoxin System. Front. Microbiol., 2018, 9, 336.
[http://dx.doi.org/10.3389/fmicb.2018.00336] [PMID: 29556223]
[91]
Ren, X.; Zou, L.; Lu, J.; Holmgren, A. Selenocysteine in mammalian thioredoxin reductase and application of ebselen as a therapeutic. Free Radic. Biol. Med., 2018, 127, 238-247.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.05.081] [PMID: 29807162]
[92]
Azad, G.K.; Tomar, R.S. Ebselen, a promising antioxidant drug: mechanisms of action and targets of biological pathways. Mol. Biol. Rep., 2014, 41(8), 4865-4879.
[http://dx.doi.org/10.1007/s11033-014-3417-x] [PMID: 24867080]
[93]
Parnham, M.; Sies, H. Ebselen: prospective therapy for cerebral ischaemia. Expert Opin. Investig. Drugs, 2000, 9(3), 607-619.
[http://dx.doi.org/10.1517/13543784.9.3.607] [PMID: 11060699]
[94]
Zhao, R.; Masayasu, H.; Holmgren, A. Ebselen: a substrate for human thioredoxin reductase strongly stimulating its hydroperoxide reductase activity and a superfast thioredoxin oxidant. Proc. Natl. Acad. Sci. USA, 2002, 99(13), 8579-8584.
[http://dx.doi.org/10.1073/pnas.122061399] [PMID: 12070343]
[95]
Arteel, G.E.; Briviba, K.; Sies, H. Function of thioredoxin reductase as a peroxynitrite reductase using selenocystine or ebselen. Chem. Res. Toxicol., 1999, 12(3), 264-269.
[http://dx.doi.org/10.1021/tx980223r] [PMID: 10077489]
[96]
Nozawa, R.; Yokota, T.; Fujimoto, T. Susceptibility of methicillin-resistant Staphylococcus aureus to the selenium-containing compound 2-phenyl-1,2-benzoisoselenazol-3(2H)-one (PZ51). Antimicrob. Agents Chemother., 1989, 33(8), 1388-1390.
[http://dx.doi.org/10.1128/AAC.33.8.1388] [PMID: 2802564]
[97]
Lu, J.; Vlamis-Gardikas, A.; Kandasamy, K.; Zhao, R.; Gustafsson, T.N.; Engstrand, L.; Hoffner, S.; Engman, L.; Holmgren, A. Inhibition of bacterial thioredoxin reductase: an antibiotic mechanism targeting bacteria lacking glutathione. FASEB J., 2013, 27(4), 1394-1403.
[http://dx.doi.org/10.1096/fj.12-223305] [PMID: 23248236]
[98]
Eriksson, S.; Prigge, J.R.; Talago, E.A.; Arnér, E.S.J.; Schmidt, E.E. Dietary methionine can sustain cytosolic redox homeostasis in the mouse liver. Nat. Commun., 2015, 6, 6479.
[http://dx.doi.org/10.1038/ncomms7479] [PMID: 25790857]
[99]
Gustafsson, T.N.; Osman, H.; Werngren, J.; Hoffner, S.; Engman, L.; Holmgren, A. Ebselen and analogs as inhibitors of Bacillus anthracis thioredoxin reductase and bactericidal antibacterials targeting Bacillus species, Staphylococcus aureus and Mycobacterium tuberculosis. Biochim. Biophys. Acta, 2016, 1860(6), 1265-1271.
[http://dx.doi.org/10.1016/j.bbagen.2016.03.013] [PMID: 26971857]
[100]
Thangamani, S.; Younis, W.; Seleem, M.N. Repurposing Clinical Molecule Ebselen to Combat Drug Resistant Pathogens. PLoS One, 2015, 10(7)e0133877
[http://dx.doi.org/10.1371/journal.pone.0133877] [PMID: 26222252]
[101]
Rock, K.L.; Kono, H. The inflammatory response to cell death. Annu. Rev. Pathol., 2008, 3, 99-126.
[http://dx.doi.org/10.1146/annurev.pathmechdis.3.121806.151456] [PMID: 18039143]
[102]
Mittal, M.; Siddiqui, M.R.; Tran, K.; Reddy, S.P.; Malik, A.B. Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox Signal., 2014, 20(7), 1126-1167.
[http://dx.doi.org/10.1089/ars.2012.5149] [PMID: 23991888]
[103]
Noguchi, N. Ebselen, a useful tool for understanding cellular redox biology and a promising drug candidate for use in human diseases. Arch. Biochem. Biophys., 2016, 595, 109-112.
[http://dx.doi.org/10.1016/j.abb.2015.10.024] [PMID: 27095225]
[104]
Walther, M.; Holzhütter, H.G.; Kuban, R.J.; Wiesner, R.; Rathmann, J.; Kühn, H. The inhibition of mammalian 15-lipoxygenases by the anti-inflammatory drug ebselen: dual-type mechanism involving covalent linkage and alteration of the iron ligand sphere. Mol. Pharmacol., 1999, 56(1), 196-203.
[http://dx.doi.org/10.1124/mol.56.1.196] [PMID: 10385701]
[105]
Zou, L.; Lu, J.; Wang, J.; Ren, X.; Zhang, L.; Gao, Y.; Rottenberg, M.E.; Holmgren, A. Synergistic antibacterial effect of silver and ebselen against multidrug-resistant Gram-negative bacterial infections. EMBO Mol. Med., 2017, 9(8), 1165-1178.
[http://dx.doi.org/10.15252/emmm.201707661] [PMID: 28606995]
[106]
Morones-Ramirez, J.R.; Winkler, J.A.; Spina, C.S.; Collins, J.J. Silver enhances antibiotic activity against gram-negative bacteria. Sci. Transl. Med., 2013, 5(190)190ra81
[http://dx.doi.org/10.1126/scitranslmed.3006276] [PMID: 23785037]
[107]
Zhao, H.Z.; Ning, Y.T. China’s ancient gold drugs. Gold Bull., 2001, 34(1), 24-29.
[http://dx.doi.org/10.1007/BF03214805]
[108]
Benedek, T.G. The history of gold therapy for tuberculosis. J. Hist. Med. Allied Sci., 2004, 59(1), 50-89.
[http://dx.doi.org/10.1093/jhmas/jrg042] [PMID: 15011812]
[109]
Novelli, F.; Recine, M.; Sparatore, F.; Juliano, C. Gold(I) complexes as antimicrobial agents. Farmaco, 1999, 54(4), 232-236.
[http://dx.doi.org/10.1016/S0014-827X(99)00019-1] [PMID: 10384716]
[110]
Jackson-Rosario, S.; Cowart, D.; Myers, A.; Tarrien, R.; Levine, R.L.; Scott, R.A.; Self, W.T. Auranofin disrupts selenium metabolism in Clostridium difficile by forming a stable Au-Se adduct. J. Biol. Inorg. Chem., 2009, 14(4), 507-519.
[http://dx.doi.org/10.1007/s00775-009-0466-z] [PMID: 19165513]
[111]
Jackson-Rosario, S.; Self, W.T. Inhibition of selenium metabolism in the oral pathogen Treponema denticola. J. Bacteriol., 2009, 191(12), 4035-4040.
[http://dx.doi.org/10.1128/JB.00164-09] [PMID: 19363113]
[112]
Hokai, Y.; Jurkowicz, B.; Fernández-Gallardo, J.; Zakirkhodjaev, N.; Sanaú, M.; Muth, T.R.; Contel, M. Auranofin and related heterometallic gold(I)-thiolates as potent inhibitors of methicillin-resistant Staphylococcus aureus bacterial strains. J. Inorg. Biochem., 2014, 138, 81-88.
[http://dx.doi.org/10.1016/j.jinorgbio.2014.05.008] [PMID: 24935090]
[113]
Cassetta, M.I.; Marzo, T.; Fallani, S.; Novelli, A.; Messori, L. Drug repositioning: auranofin as a prospective antimicrobial agent for the treatment of severe staphylococcal infections. Biometals, 2014, 27(4), 787-791.
[http://dx.doi.org/10.1007/s10534-014-9743-6] [PMID: 24820140]
[114]
Harbut, M.B.; Vilchèze, C.; Luo, X.; Hensler, M.E.; Guo, H.; Yang, B.; Chatterjee, A.K.; Nizet, V.; Jacobs, W.R., Jr; Schultz, P.G.; Wang, F. Auranofin exerts broad-spectrum bactericidal activities by targeting thiol-redox homeostasis. Proc. Natl. Acad. Sci. USA, 2015, 112(14), 4453-4458.
[http://dx.doi.org/10.1073/pnas.1504022112] [PMID: 25831516]
[115]
Angelucci, F.; Sayed, A.A.; Williams, D.L.; Boumis, G.; Brunori, M.; Dimastrogiovanni, D.; Miele, A.E.; Pauly, F.; Bellelli, A. Inhibition of Schistosoma mansoni thioredoxin-glutathione reductase by auranofin: structural and kinetic aspects. J. Biol. Chem., 2009, 284(42), 28977-28985.
[http://dx.doi.org/10.1074/jbc.M109.020701] [PMID: 19710012]
[116]
Jaeger, T.; Budde, H.; Flohé, L.; Menge, U.; Singh, M.; Trujillo, M.; Radi, R. Multiple thioredoxin-mediated routes to detoxify hydroperoxides in Mycobacterium tuberculosis. Arch. Biochem. Biophys., 2004, 423(1), 182-191.
[http://dx.doi.org/10.1016/j.abb.2003.11.021] [PMID: 14871480]
[117]
Torrents, E. Ribonucleotide reductases: essential enzymes for bacterial life; Front Cell Infect Mi, 2014, p. 4.
[118]
Sasindran, S.J.; Saikolappan, S.; Dhandayuthapani, S. Methionine sulfoxide reductases and virulence of bacterial pathogens. Future Microbiol., 2007, 2(6), 619-630.
[http://dx.doi.org/10.2217/17460913.2.6.619] [PMID: 18041903]
[119]
Ilari, A.; Baiocco, P.; Messori, L.; Fiorillo, A.; Boffi, A.; Gramiccia, M.; Di Muccio, T.; Colotti, G. A gold-containing drug against parasitic polyamine metabolism: the X-ray structure of trypanothione reductase from Leishmania infantum in complex with auranofin reveals a dual mechanism of enzyme inhibition. Amino Acids, 2012, 42(2-3), 803-811.
[http://dx.doi.org/10.1007/s00726-011-0997-9] [PMID: 21833767]
[120]
De Luca, A.; Hartinger, C.G.; Dyson, P.J.; Lo Bello, M.; Casini, A. A new target for gold(I) compounds: glutathione-S-transferase inhibition by auranofin. J. Inorg. Biochem., 2013, 119, 38-42.
[http://dx.doi.org/10.1016/j.jinorgbio.2012.08.006] [PMID: 23183361]
[121]
Chircorian, A.; Barrios, A.M. Inhibition of lysosomal cysteine proteases by chrysotherapeutic compounds: a possible mechanism for the antiarthritic activity of Au(I). Bioorg. Med. Chem. Lett., 2004, 14(20), 5113-5116.
[http://dx.doi.org/10.1016/j.bmcl.2004.07.073] [PMID: 15380210]
[122]
Krishnamurthy, D.; Karver, M.R.; Fiorillo, E.; Orrú, V.; Stanford, S.M.; Bottini, N.; Barrios, A.M. Gold(I)-mediated inhibition of protein tyrosine phosphatases: a detailed in vitro and cellular study. J. Med. Chem., 2008, 51(15), 4790-4795.
[http://dx.doi.org/10.1021/jm800101w] [PMID: 18605719]
[123]
Thangamani, S.; Mohammad, H.; Abushahba, M.F.N.; Sobreira, T.J.P.; Hedrick, V.E.; Paul, L.N.; Seleem, M.N. Antibacterial activity and mechanism of action of auranofin against multi-drug resistant bacterial pathogens; Sci Rep-UK, 2016, p. 6.

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