Oxidative stress, protein damage and repair in bacteria (original) (raw)

• Imlay, J. A. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat. Rev. Microbiol. 11, 443–454 (2013). This paper provides a detailed review of oxidative stress in bacteria.
  Article CAS PubMed PubMed Central Google Scholar
• Flannagan, R. S., Heit, B. & Heinrichs, D. E. Antimicrobial mechanisms of macrophages and the immune evasion strategies of Staphylococcus aureus. Pathogens 4, 826–868 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Winterbourn, C. C. & Kettle, A. J. Redox reactions and microbial killing in the neutrophil phagosome. Antioxid. Redox Signal. 18, 642–660 (2013).
  Article CAS PubMed Google Scholar
• Hurst, J. K. What really happens in the neutrophil phagosome? Free Radic. Biol. Med. 53, 508–520 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Nystrom, T. Role of oxidative carbonylation in protein quality control and senescence. EMBO J. 24, 1311–1317 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Traore, D. A. et al. Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein. Nat. Chem. Biol. 5, 53–59 (2009).
  Article CAS PubMed Google Scholar
• Feeney, M. B. & Schoneich, C. Tyrosine modifications in aging. Antioxid. Redox Signal. 17, 1571–1579 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Thurlkill, R. L., Grimsley, G. R., Scholtz, J. M. & Pace, C. N. p_K_ values of the ionizable groups of proteins. Protein Sci. 15, 1214–1218 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Winterbourn, C. C. & Hampton, M. B. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45, 549–561 (2008).
  Article CAS PubMed Google Scholar
• Nagy, P. Kinetics and mechanisms of thiol–disulfide exchange covering direct substitution and thiol oxidation-mediated pathways. Antioxid. Redox Signal. 18, 1623–1641 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Paulsen, C. E. & Carroll, K. S. Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem. Rev. 113, 4633–4679 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Roos, G. & Messens, J. Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radic. Biol. Med. 51, 314–326 (2011).
  Article CAS PubMed Google Scholar
• Imlay, J. A. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77, 755–776 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Davies, M. J. The oxidative environment and protein damage. Biochim. Biophys. Acta 1703, 93–109 (2005).
  Article CAS PubMed Google Scholar
• Lavine, T. F. The formation, resolution, and optical properties of the diastereoisomeric sulfoxides derived from L-methionine. J. Biol. Chem. 169, 477–491 (1947).
  CAS PubMed Google Scholar
• Lee, B. C. & Gladyshev, V. N. The biological significance of methionine sulfoxide stereochemistry. Free Radic. Biol. Med. 50, 221–227 (2011).
  Article CAS PubMed Google Scholar
• Vogt, W. Oxidation of methionyl residues in proteins: tools, targets, and reversal. Free Radic. Biol. Med. 18, 93–105 (1995).
  Article CAS PubMed Google Scholar
• Schoneich, C. Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer's disease. Biochim. Biophys. Acta 1703, 111–119 (2005).
  Article CAS PubMed Google Scholar
• Buxton, G. V., Greenstock, C. L., Helman, W. P. & Ross, A. B. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals in aqueous solution. J. Phys. Chem. Ref. Data 17, 513–886 (1988).
  Article CAS Google Scholar
• Pattison, D. I. & Davies, M. J. Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds. Chem. Res. Toxicol. 14, 1453–1464 (2001).
  Article CAS PubMed Google Scholar
• Padmaja, S., Squadrito, G. L., Lemercier, J. N., Cueto, R. & Pryor, W. A. Rapid oxidation of DL-selenomethionine by peroxynitrite. Free Radic. Biol. Med. 21, 317–322 (1996).
  Article CAS PubMed Google Scholar
• Collet, J. F. & Messens, J. Structure, function, and mechanism of thioredoxin proteins. Antioxid. Redox Signal. 13, 1205–1216 (2010).
  Article CAS PubMed Google Scholar
• Arts, I. S., Vertommen, D., Baldin, F., Laloux, G. & Collet, J. F. Comprehensively characterizing the thioredoxin interactome in vivo highlights the central role played by this ubiquitous oxidoreductase in redox control. Mol. Cell. Proteomics 15, 2125–2140 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Collet, J. F., D'Souza, J. C., Jakob, U. & Bardwell, J. C. Thioredoxin 2, an oxidative stress-induced protein, contains a high affinity zinc binding site. J. Biol. Chem. 278, 45325–45332 (2003).
  Article CAS PubMed Google Scholar
• Ritz, D. et al. Thioredoxin 2 is involved in the oxidative stress response in Escherichia coli. J. Biol. Chem. 275, 2505–2512 (2000).
  Article CAS PubMed Google Scholar
• Storz, G., Tartaglia, L. A. & Ames, B. N. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248, 189–194 (1990). This study reports the activation of OxyR, a transcription factor that controls an oxidative stress response, through the direct oxidation of a cysteine residue, which shows that oxidation is not always detrimental.
  Article CAS PubMed Google Scholar
• Ritz, D. & Beckwith, J. Roles of thiol-redox pathways in bacteria. Annu. Rev. Microbiol. 55, 21–48 (2001).
  Article CAS PubMed Google Scholar
• Fernandes, A. P. & Holmgren, A. Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid. Redox Signal. 6, 63–74 (2004).
  Article CAS PubMed Google Scholar
• Vlamis-Gardikas, A. The multiple functions of the thiol-based electron flow pathways of Escherichia coli: eternal concepts revisited. Biochim. Biophys. Acta 1780, 1170–1200 (2008).
  Article CAS PubMed Google Scholar
• Iwema, T. et al. Structural basis for delivery of the intact [Fe2S2] cluster by monothiol glutaredoxin. Biochemistry 48, 6041–6043 (2009).
  Article CAS PubMed Google Scholar
• Newton, G. L. & Fahey, R. C. Mycothiol biochemistry. Arch. Microbiol. 178, 388–394 (2002).
  Article CAS PubMed Google Scholar
• Newton, G. L. et al. Bacillithiol is an antioxidant thiol produced in bacilli. Nat. Chem. Biol. 5, 625–627 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Delaye, L., Becerra, A., Orgel, L. & Lazcano, A. Molecular evolution of peptide methionine sulfoxide reductases (MsrA and MsrB): on the early development of a mechanism that protects against oxidative damage. J. Mol. Evol. 64, 15–32 (2007).
  Article CAS PubMed Google Scholar
• Brot, N., Weissbach, L., Werth, J. & Weissbach, H. Enzymatic reduction of protein-bound methionine sulfoxide. Proc. Natl Acad. Sci. USA 78, 2155–2158 (1981). This work reports, for the first time, the ability of an Msr enzyme to reduce a methionine sulfoxide in a protein.
  Article CAS PubMed PubMed Central Google Scholar
• Rahman, M. A., Nelson, H., Weissbach, H. & Brot, N. Cloning, sequencing, and expression of the Escherichia coli peptide methionine sulfoxide reductase gene. J. Biol. Chem. 267, 15549–15551 (1992).
  CAS PubMed Google Scholar
• Grimaud, R. et al. Repair of oxidized proteins. Identification of a new methionine sulfoxide reductase. J. Biol. Chem. 276, 48915–48920 (2001). This study reports the identification of MsrB.
  Article CAS PubMed Google Scholar
• Lin, Z. et al. Free methionine-(R)-sulfoxide reductase from Escherichia coli reveals a new GAF domain function. Proc. Natl Acad. Sci. USA 104, 9597–9602 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Ezraty, B., Bos, J., Barras, F. & Aussel, L. Methionine sulfoxide reduction and assimilation in Escherichia coli: new role for the biotin sulfoxide reductase BisC. J. Bacteriol. 187, 231–237 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Kryukov, G. V., Kumar, R. A., Koc, A., Sun, Z. & Gladyshev, V. N. Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proc. Natl Acad. Sci. USA 99, 4245–4250 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Sharov, V. S., Ferrington, D. A., Squier, T. C. & Schoneich, C. Diastereoselective reduction of protein-bound methionine sulfoxide by methionine sulfoxide reductase. FEBS Lett. 455, 247–250 (1999).
  Article CAS PubMed Google Scholar
• Moskovitz, J. et al. Identification and characterization of a putative active site for peptide methionine sulfoxide reductase (MsrA) and its substrate stereospecificity. J. Biol. Chem. 275, 14167–14172 (2000).
  Article CAS PubMed Google Scholar
• Boschi-Muller, S., Olry, A., Antoine, M. & Branlant, G. The enzymology and biochemistry of methionine sulfoxide reductases. Biochim. Biophys. Acta 1703, 231–238 (2005).
  Article CAS PubMed Google Scholar
• Boschi-Muller, S., Azza, S. & Branlant, G. E. coli methionine sulfoxide reductase with a truncated N terminus or C terminus, or both, retains the ability to reduce methionine sulfoxide. Protein Sci. 10, 2272–2279 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Kumar, R. A., Koc, A., Cerny, R. L. & Gladyshev, V. N. Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-_R_-sulfoxide reductase. J. Biol. Chem. 277, 37527–37535 (2002).
  Article CAS PubMed Google Scholar
• Kim, H. Y. & Gladyshev, V. N. Different catalytic mechanisms in mammalian selenocysteine- and cysteine-containing methionine-_R_-sulfoxide reductases. PLoS Biol. 3, e375 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Russel, M. & Model, P. The role of thioredoxin in filamentous phage assembly. Construction, isolation, and characterization of mutant thioredoxins. J. Biol. Chem. 261, 14997–15005 (1986).
  CAS PubMed Google Scholar
• Boschi-Muller, S. & Branlant, G. Methionine sulfoxide reductase: chemistry, substrate binding, recycling process and oxidase activity. Bioorg. Chem. 57, 222–230 (2014). This review describes the chemistry of Msr enzymes.
  Article CAS PubMed Google Scholar
• Lee, T. H. & Kim, H. Y. An anaerobic bacterial MsrB model reveals catalytic mechanisms, advantages, and disadvantages provided by selenocysteine and cysteine in reduction of methionine-_R_-sulfoxide. Arch. Biochem. Biophys. 478, 175–180 (2008).
  Article CAS PubMed Google Scholar
• Coudevylle, N. et al. Solution structure and backbone dynamics of the reduced form and an oxidized form of E. coli methionine sulfoxide reductase A (MsrA): structural insight of the MsrA catalytic cycle. J. Mol. Biol. 366, 193–206 (2007).
  Article CAS PubMed Google Scholar
• Ranaivoson, F. M. et al. A structural analysis of the catalytic mechanism of methionine sulfoxide reductase A from Neisseria meningitidis. J. Mol. Biol. 377, 268–280 (2008).
  Article CAS PubMed Google Scholar
• Ranaivoson, F. M. et al. Methionine sulfoxide reductase B displays a high level of flexibility. J. Mol. Biol. 394, 83–93 (2009).
  Article CAS PubMed Google Scholar
• Lowther, W. T., Weissbach, H., Etienne, F., Brot, N. & Matthews, B. W. The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat. Struct. Biol. 9, 348–352 (2002).
  CAS PubMed Google Scholar
• Mahawar, M., Tran, V., Sharp, J. S. & Maier, R. J. Synergistic roles of Helicobacter pylori methionine sulfoxide reductase and GroEL in repairing oxidant-damaged catalase. J. Biol. Chem. 286, 19159–19169 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Benoit, S. L., Bayyareddy, K., Mahawar, M., Sharp, J. S. & Maier, R. J. Alkyl hydroperoxide reductase repair by Helicobacter pylori methionine sulfoxide reductase. J. Bacteriol. 195, 5396–5401 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Khor, H. K., Fisher, M. T. & Schoneich, C. Potential role of methionine sulfoxide in the inactivation of the chaperone GroEL by hypochlorous acid (HOCl) and peroxynitrite (ONOO-). J. Biol. Chem. 279, 19486–19493 (2004).
  Article CAS PubMed Google Scholar
• Abulimiti, A., Qiu, X., Chen, J., Liu, Y. & Chang, Z. Reversible methionine sulfoxidation of Mycobacterium tuberculosis small heat shock protein Hsp16.3 and its possible role in scavenging oxidants. Biochem. Biophys. Res. Commun. 305, 87–93 (2003).
  Article CAS PubMed Google Scholar
• Levine, R. L., Mosoni, L., Berlett, B. S. & Stadtman, E. R. Methionine residues as endogenous antioxidants in proteins. Proc. Natl Acad. Sci. USA 93, 15036–15040 (1996). This study proposes a theory in which methionine residues act as a shield against ROS.
  Article CAS PubMed PubMed Central Google Scholar
• Ezraty, B., Grimaud, R., El Hassouni, M., Moinier, D. & Barras, F. Methionine sulfoxide reductases protect Ffh from oxidative damages in Escherichia coli. EMBO J. 23, 1868–1877 (2004). This study reports the identification of the SRP54 homologue in bacteria as a target of the MsrAB system through the use of both biochemical and physiological approaches.
  Article CAS PubMed PubMed Central Google Scholar
• Luirink, J. et al. An alternative protein targeting pathway in Escherichia coli: studies on the role of FtsY. EMBO J. 13, 2289–2296 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Ulbrandt, N. D., Newitt, J. A. & Bernstein, H. D. The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88, 187–196 (1997).
  Article CAS PubMed Google Scholar
• Leverrier, P., Vertommen, D. & Collet, J. F. Contribution of proteomics toward solving the fascinating mysteries of the biogenesis of the envelope of Escherichia coli. Proteomics 10, 771–784 (2010).
  Article CAS PubMed Google Scholar
• Silhavy, T. J., Kahne, D. & Walker, S. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2, a000414 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Depuydt, M., Messens, J. & Collet, J. F. How proteins form disulfide bonds. Antioxid. Redox Signal. 15, 49–66 (2011).
  Article CAS PubMed Google Scholar
• Bardwell, J. C., McGovern, K. & Beckwith, J. Identification of a protein required for disulfide bond formation in vivo. Cell 67, 581–589 (1991). This study describes the identification of DsbA, a protein that catalyses the formation of disulfide bonds in the periplasm.
  Article CAS PubMed Google Scholar
• Bader, M., Muse, W., Ballou, D. P., Gassner, C. & Bardwell, J. C. Oxidative protein folding is driven by the electron transport system. Cell 98, 217–227 (1999).
  Article CAS PubMed Google Scholar
• Kadokura, H. & Beckwith, J. Detecting folding intermediates of a protein as it passes through the bacterial translocation channel. Cell 138, 1164–1173 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Shevchik, V. E., Condemine, G. & Robert-Baudouy, J. Characterization of DsbC, a periplasmic protein of Erwinia chrysanthemi and Escherichia coli with disulfide isomerase activity. EMBO J. 13, 2007–2012 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Dutton, R. J., Boyd, D., Berkmen, M. & Beckwith, J. Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc. Natl Acad. Sci. USA 105, 11933–11938 (2008). This study reveals that there is a bias for an even number of cysteine residues in proteins that are expressed in compartments in which the formation of disulfide bonds occurs. As such, counting the number of cysteine residues can be used to predict whether the formation of disulfide bonds occurs in a specific cellular compartment.
  Article CAS PubMed PubMed Central Google Scholar
• Depuydt, M. et al. A periplasmic reducing system protects single cysteine residues from oxidation. Science 326, 1109–1111 (2009). This paper reports the function of DsbG in the protection of single cysteine residues from oxidation in the periplasm.
  Article CAS PubMed Google Scholar
• Mainardi, J. L. et al. Unexpected inhibition of peptidoglycan ld-transpeptidase from Enterococcus faecium by the β-lactam imipenem. J. Biol. Chem. 282, 30414–30422 (2007).
  Article CAS PubMed Google Scholar
• Denoncin, K. et al. A new role for Escherichia coli DsbC protein in protection against oxidative stress. J. Biol. Chem. 289, 12356–12364 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Arts, I. S., Gennaris, A. & Collet, J. F. Reducing systems protecting the bacterial cell envelope from oxidative damage. FEBS Lett. 589, 1559–1568 (2015).
  Article CAS PubMed Google Scholar
• 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. 179, 6602–6608 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Rietsch, A., Belin, D., Martin, N. & Beckwith, J. An in vivo pathway for disulfide bond isomerization in Escherichia coli. Proc. Natl Acad. Sci. USA 93, 13048–13053 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Katzen, F. & Beckwith, J. Transmembrane electron transfer by the membrane protein DsbD occurs via a disulfide bond cascade. Cell 103, 769–779 (2000).
  Article CAS PubMed Google Scholar
• Williamson, J. A. et al. Structure and multistate function of the transmembrane electron transporter CcdA. Nat. Struct. Mol. Biol. 22, 809–814 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Skaar, E. P. et al. The outer membrane localization of the Neisseria gonorrhoeae MsrA/B is involved in survival against reactive oxygen species. Proc. Natl Acad. Sci. USA 99, 10108–10113 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Olry, A. et al. Characterization of the methionine sulfoxide reductase activities of PilB, a probable virulence factor from Neisseria meningitidis. J. Biol. Chem. 277, 12016–12022 (2002).
  Article CAS PubMed Google Scholar
• Brot, N. et al. The thioredoxin domain of Neisseria gonorrhoeae PilB can use electrons from DsbD to reduce downstream methionine sulfoxide reductases. J. Biol. Chem. 281, 32668–32675 (2006).
  Article CAS PubMed Google Scholar
• Saleh, M. et al. Molecular architecture of Streptococcus pneumoniae surface thioredoxin-fold lipoproteins crucial for extracellular oxidative stress resistance and maintenance of virulence. EMBO Mol. Med. 5, 1852–1870 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Gennaris, A. et al. Repairing oxidized proteins in the bacterial envelope using respiratory chain electrons. Nature 528, 409–412 (2015). This study describes the identification of MsrPQ, which is a widely conserved enzymatic system that protects methionine residues from oxidation in the periplasm.
  Article CAS PubMed PubMed Central Google Scholar
• Brokx, S. J., Rothery, R. A., Zhang, G., Ng, D. P. & Weiner, J. H. Characterization of an Escherichia coli sulfite oxidase homologue reveals the role of a conserved active site cysteine in assembly and function. Biochemistry 44, 10339–10348 (2005).
  Article CAS PubMed Google Scholar
• Juillan-Binard, C. et al. A two-component NADPH oxidase (NOX)-like system in bacteria is involved in the electron transfer chain to the methionine sulfoxide reductase MsrP. J. Biol. Chem. 292, 2485–2494 (2017).
  Article CAS PubMed Google Scholar
• Loschi, L. et al. Structural and biochemical identification of a novel bacterial oxidoreductase. J. Biol. Chem. 279, 50391–50400 (2004).
  Article CAS PubMed Google Scholar
• Melnyk, R. A. et al. Novel mechanism for scavenging of hypochlorite involving a periplasmic methionine-rich peptide and methionine sulfoxide reductase. mBio 6, e00233–15 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Vlamis-Gardikas, A., Potamitou, A., Zarivach, R., Hochman, A. & Holmgren, A. Characterization of Escherichia coli null mutants for glutaredoxin 2. J. Biol. Chem. 277, 10861–10868 (2002).
  Article CAS PubMed Google Scholar
• Kosower, N. S., Kosower, E. M., Wertheim, B. & Correa, W. S. Diamide, a new reagent for the intracellular oxidation of glutathione to the disulfide. Biochem. Biophys. Res. Commun. 37, 593–596 (1969).
  Article CAS PubMed Google Scholar
• Lin, K. et al. Mycobacterium tuberculosis thioredoxin reductase is essential for thiol redox homeostasis but plays a minor role in antioxidant defense. PLoS Pathog. 12, e1005675 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• 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. 186, 326–334 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Marteyn, B., Domain, F., Legrain, P., Chauvat, F. & Cassier-Chauvat, C. The thioredoxin reductase–glutaredoxins–ferredoxin crossroad pathway for selenate tolerance in Synechocystis PCC6803. Mol. Microbiol. 71, 520–532 (2009).
  Article CAS PubMed Google Scholar
• Pasternak, C., Assemat, K., Clement-Metral, J. D. & Klug, G. Thioredoxin is essential for Rhodobacter sphaeroides growth by aerobic and anaerobic respiration. Microbiology 143, 83–91 (1997).
  Article CAS PubMed Google Scholar
• Scharf, C. et al. Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis. J. Bacteriol. 180, 1869–1877 (1998).
  CAS PubMed PubMed Central Google Scholar
• Navarro, F. & Florencio, F. J. The cyanobacterial thioredoxin gene is required for both photoautotrophic and heterotrophic growth. Plant Physiol. 111, 1067–1075 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Kuhns, L. G., Wang, G. & Maier, R. J. Comparative roles of the two Helicobacter pylori thioredoxins in preventing macromolecule damage. Infect. Immun. 83, 2935–2943 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Potter, A. J. et al. Thioredoxin reductase is essential for protection of Neisseria gonorrhoeae against killing by nitric oxide and for bacterial growth during interaction with cervical epithelial cells. J. Infect. Dis. 199, 227–235 (2009).
  Article CAS PubMed Google Scholar
• Kraemer, P. S. et al. Genome-wide screen in Francisella novicida for genes required for pulmonary and systemic infection in mice. Infect. Immun. 77, 232–244 (2009).
  Article CAS PubMed Google Scholar
• Rocha, E. R., Tzianabos, A. O. & Smith, C. J. Thioredoxin reductase is essential for thiol/disulfide redox control and oxidative stress survival of the anaerobe Bacteroides fragilis. J. Bacteriol. 189, 8015–8023 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Ortenberg, R., Gon, S., Porat, A. & Beckwith, J. Interactions of glutaredoxins, ribonucleotide reductase, and components of the DNA replication system of Escherichia coli. Proc. Natl Acad. Sci. USA 101, 7439–7444 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Russel, M., Model, P. & Holmgren, A. Thioredoxin or glutaredoxin in Escherichia coli is essential for sulfate reduction but not for deoxyribonucleotide synthesis. J. Bacteriol. 172, 1923–1929 (1990).
  Article CAS PubMed PubMed Central Google Scholar
• Toledano, M. B., Kumar, C., Le Moan, N., Spector, D. & Tacnet, F. 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 (2007).
  Article CAS PubMed Google Scholar
• Crooke, H. & Cole, J. The biogenesis of _c_-type cytochromes in Escherichia coli requires a membrane-bound protein, DipZ, with a protein disulphide isomerase-like domain. Mol. Microbiol. 15, 1139–1150 (1995).
  Article CAS PubMed Google Scholar
• Mavridou, D. A., Ferguson, S. J. & Stevens, J. M. The interplay between the disulfide bond formation pathway and cytochrome c maturation in Escherichia coli. FEBS Lett. 586, 1702–1707 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Metheringham, R. et al. Effects of mutations in genes for proteins involved in disulphide bond formation in the periplasm on the activities of anaerobically induced electron transfer chains in Escherichia coli K12. Mol. Gen. Genet. 253, 95–102 (1996).
  CAS PubMed Google Scholar
• Beckett, C. S. et al. Four genes are required for the system II cytochrome c biogenesis pathway in Bordetella pertussis, a unique bacterial model. Mol. Microbiol. 38, 465–481 (2000).
  Article CAS PubMed Google Scholar
• Liu, Y. W. & Kelly, D. J. Cytochrome c biogenesis in Campylobacter jejuni requires cytochrome c6 (CccA; Cj1153) to maintain apocytochrome cysteine thiols in a reduced state for haem attachment. Mol. Microbiol. 96, 1298–1317 (2015).
  Article CAS PubMed Google Scholar
• Braun, M. & Thony-Meyer, L. Cytochrome c maturation and the physiological role of _c_-type cytochromes in Vibrio cholerae. J. Bacteriol. 187, 5996–6004 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Page, M. D., Saunders, N. F. & Ferguson, S. J. Disruption of the Pseudomonas aeruginosa dipZ gene, encoding a putative protein-disulfide reductase, leads to partial pleiotropic deficiency in _c_-type cytochrome biogenesis. Microbiology 143, 3111–3122 (1997).
  Article CAS PubMed Google Scholar
• Hiniker, A., Collet, J. F. & Bardwell, J. C. Copper stress causes an in vivo requirement for the Escherichia coli disulfide isomerase DsbC. J. Biol. Chem. 280, 33785–33791 (2005).
  Article CAS PubMed Google Scholar
• Missiakas, D., Schwager, F. & Raina, S. Identification and characterization of a new disulfide isomerase-like protein (DsbD) in Escherichia coli. EMBO J. 14, 3415–3424 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Leverrier, P. et al. Crystal structure of the outer membrane protein RcsF, a new substrate for the periplasmic protein-disulfide isomerase DsbC. J. Biol. Chem. 286, 16734–16742 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Kumar, P., Sannigrahi, S., Scoullar, J., Kahler, C. M. & Tzeng, Y. L. Characterization of DsbD in Neisseria meningitidis. Mol. Microbiol. 79, 1557–1573 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Vertommen, D. et al. The disulphide isomerase DsbC cooperates with the oxidase DsbA in a DsbD-independent manner. Mol. Microbiol. 67, 336–349 (2008).
  CAS PubMed Google Scholar
• Denoncin, K., Vertommen, D., Paek, E. & Collet, J. F. The protein-disulfide isomerase DsbC cooperates with SurA and DsbA in the assembly of the essential β-barrel protein LptD. J. Biol. Chem. 285, 29425–29433 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Missiakas, D., Georgopoulos, C. & Raina, S. The Escherichia coli dsbC (xprA) gene encodes a periplasmic protein involved in disulfide bond formation. EMBO J. 13, 2013–2020 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• An, R., Sreevatsan, S. & Grewal, P. S. Moraxella osloensis gene expression in the slug host Deroceras reticulatum. BMC Microbiol. 8, 19 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Guo, W. et al. Identification of seven Xanthomonas oryzae pv. oryzicola genes potentially involved in pathogenesis in rice. Microbiology 158, 505–518 (2012).
  Article CAS PubMed Google Scholar
• Vincent-Sealy, L. V., Thomas, J. D., Commander, P. & Salmond, G. P. Erwinia carotovora DsbA mutants: evidence for a periplasmic-stress signal transduction system affecting transcription of genes encoding secreted proteins. Microbiology 145, 1945–1958 (1999).
  Article CAS PubMed Google Scholar
• Zhao, C. et al. Role of methionine sulfoxide reductases A and B of Enterococcus faecalis in oxidative stress and virulence. Infect. Immun. 78, 3889–3897 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Denkel, L. A. et al. Methionine sulfoxide reductases are essential for virulence of Salmonella Typhimurium. PLoS ONE 6, e26974 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Dhandayuthapani, S., Blaylock, M. W., Bebear, C. M., Rasmussen, W. G. & Baseman, J. B. Peptide methionine sulfoxide reductase (MsrA) is a virulence determinant in Mycoplasma genitalium. J. Bacteriol. 183, 5645–5650 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Vattanaviboon, P., Seeanukun, C., Whangsuk, W., Utamapongchai, S. & Mongkolsuk, S. Important role for methionine sulfoxide reductase in the oxidative stress response of Xanthomonas campestris pv. phaseoli. J. Bacteriol. 187, 5831–5836 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Moskovitz, J. et al. Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage. J. Bacteriol. 177, 502–507 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Romsang, A., Atichartpongkul, S., Trinachartvanit, W., Vattanaviboon, P. & Mongkolsuk, S. Gene expression and physiological role of Pseudomonas aeruginosa methionine sulfoxide reductases during oxidative stress. J. Bacteriol. 195, 3299–3308 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Trivedi, R. N. et al. Methionine sulfoxide reductase A (MsrA) contributes to Salmonella Typhimurium survival against oxidative attack of neutrophils. Immunobiology 220, 1322–1327 (2015).
  Article CAS PubMed Google Scholar
• Dhandayuthapani, S., Jagannath, C., Nino, C., Saikolappan, S. & Sasindran, S. J. Methionine sulfoxide reductase B (MsrB) of Mycobacterium smegmatis plays a limited role in resisting oxidative stress. Tuberculosis (Edinb.) 89 (Suppl. 1), S26–S32 (2009).
  Article Google Scholar
• Atack, J. M. & Kelly, D. J. Contribution of the stereospecific methionine sulphoxide reductases MsrA and MsrB to oxidative and nitrosative stress resistance in the food-borne pathogen Campylobacter jejuni. Microbiology 154, 2219–2230 (2008).
  Article CAS PubMed Google Scholar
• Lee, W. L. et al. Mycobacterium tuberculosis expresses methionine sulphoxide reductases A and B that protect from killing by nitrite and hypochlorite. Mol. Microbiol. 71, 583–593 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Pericone, C. D., Overweg, K., Hermans, P. W. & Weiser, J. N. Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect. Immun. 68, 3990–3997 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Hassouni, M. E., Chambost, J. P., Expert, D., Van Gijsegem, F. & Barras, F. The minimal gene set member msrA, encoding peptide methionine sulfoxide reductase, is a virulence determinant of the plant pathogen Erwinia chrysanthemi. Proc. Natl Acad. Sci. USA 96, 887–892 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Das, K., De la Garza, G., Maffi, S., Saikolappan, S. & Dhandayuthapani, S. Methionine sulfoxide reductase A (MsrA) deficient Mycoplasma genitalium shows decreased interactions with host cells. PLoS ONE 7, e36247 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Singh, V. K. et al. Significance of four methionine sulfoxide reductases in Staphylococcus aureus. PLoS ONE 10, e0117594 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Wizemann, T. M. et al. Peptide methionine sulfoxide reductase contributes to the maintenance of adhesins in three major pathogens. Proc. Natl Acad. Sci. USA 93, 7985–7990 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Alamuri, P. & Maier, R. J. Methionine sulphoxide reductase is an important antioxidant enzyme in the gastric pathogen Helicobacter pylori. Mol. Microbiol. 53, 1397–1406 (2004).
  Article CAS PubMed Google Scholar
• Beloin, C. et al. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol. Microbiol. 51, 659–674 (2004).
  Article CAS PubMed Google Scholar
• Hitchcock, A. et al. 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 (2010).
  Article CAS PubMed Google Scholar
• Chiarugi, P. & Cirri, P. Redox regulation of protein tyrosine phosphatases during receptor tyrosine kinase signal transduction. Trends Biochem. Sci. 28, 509–514 (2003).
  Article CAS PubMed Google Scholar
• Tanner, J. J., Parsons, Z. D., Cummings, A. H., Zhou, H. & Gates, K. S. Redox regulation of protein tyrosine phosphatases: structural and chemical aspects. Antioxid. Redox Signal. 15, 77–97 (2011).
  Article CAS PubMed Google Scholar
• Rhee, S. G. Cell signaling. H2O2, a necessary evil for cell signaling. Science 312, 1882–1883 (2006).
  Article PubMed Google Scholar
• Mongkolsuk, S. & Helmann, J. D. Regulation of inducible peroxide stress responses. Mol. Microbiol. 45, 9–15 (2002).
  Article CAS PubMed Google Scholar
• Antelmann, H. & Helmann, J. D. Thiol-based redox switches and gene regulation. Antioxid. Redox Signal. 14, 1049–1063 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Storz, G. & Imlay, J. A. Oxidative stress. Curr. Opin. Microbiol. 2, 188–194 (1999).
  Article CAS PubMed Google Scholar
• Choi, H. et al. Structural basis of the redox switch in the OxyR transcription factor. Cell 105, 103–113 (2001).
  Article CAS PubMed Google Scholar
• Zheng, M., Aslund, F. & Storz, G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279, 1718–1721 (1998).
  Article CAS PubMed Google Scholar
• Gebendorfer, K. M. et al. Identification of a hypochlorite-specific transcription factor from Escherichia coli. J. Biol. Chem. 287, 6892–6903 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Drazic, A. et al. Methionine oxidation activates a transcription factor in response to oxidative stress. Proc. Natl Acad. Sci. USA 110, 9493–9498 (2013). This study reports the first example of the activation of a regulatory protein through methionine oxidation.
  Article CAS PubMed PubMed Central Google Scholar
• Drazic, A. et al. Tetramers are the activation-competent species of the HOCl-specific transcription factor HypT. J. Biol. Chem. 289, 977–986 (2014).
  Article CAS PubMed Google Scholar