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Research Paper

Deletion of glutaredoxin promotes oxidative tolerance and intracellular infection in Listeria monocytogenes

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Pages 910-924 | Received 21 Feb 2019, Accepted 13 Sep 2019, Published online: 02 Nov 2019

References

  • Fahey RC. Glutathione analogs in prokaryotes. Biochim Biophys Acta. 2013;1830:3182–3198.
  • Van Laer K, Hamilton CJ, Messens J. Low-molecular-weight thiols in thiol-disulfide exchange. Antioxid Redox Signal. 2013;18:1642–1653.
  • Ezraty B, Gennaris A, Barras F, et al. Oxidative stress, protein damage and repair in bacteria. Nat Rev Microbiol. 2017;15:385–396.
  • Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol. 2013;11:443–454.
  • Radoshevich L, Cossart P. Listeria monocytogenes: towards a complete picture of its physiology and pathogenesis. Nat Rev Microbiol. 2018;16:32–46.
  • Chen C, Nguyen BN, Mitchell G, et al. The listeriolysin O PEST-like sequence Co-opts AP-2-mediated endocytosis to prevent plasma membrane damage during listeria infection. Cell Host Microbe. 2018;23:786–795 e785.
  • Cheng C, Dong Z, Han X, et al. Listeria monocytogenes 10403S arginine repressor ArgR finely tunes arginine metabolism regulation under acidic conditions. Front Microbiol. 2017;8:145.
  • Cheng C, Dong Z, Han X, et al. Thioredoxin A is essential for motility and contributes to host infection of listeria monocytogenes via redox interactions. Front Cell Infect Microbiol. 2017;7:287.
  • Lu J, Holmgren A. The thioredoxin antioxidant system. Free Radical Bio Med. 2014;66:75–87.
  • Ouyang Y, Peng Y, Li J, et al. Modulation of thiol-dependent redox system by metal ions via thioredoxin and glutaredoxin systems. Metallomics. 2018;10:218–228.
  • Begas P, Liedgens L, Moseler A, et al. Glutaredoxin catalysis requires two distinct glutathione interaction sites. Nat Commun. 2017;8:14835.
  • Vlamis-Gardikas A. The multiple functions of the thiol-based electron flow pathways of Escherichia coli: eternal concepts revisited. Biochim Biophys Acta. 2008;1780:1170–1200.
  • Iwema T, Picciocchi A, Traore DA, et al. Structural basis for delivery of the intact [Fe2S2] cluster by monothiol glutaredoxin. Biochemistry-us. 2009;48:6041–6043.
  • Vlamis-Gardikas A, Potamitou A, Zarivach R, et al. Characterization of Escherichia coli null mutants for glutaredoxin 2. J Biol Chem. 2002;277:10861–10868.
  • Gopal S, Srinivas V, Zameer F, et al. Prediction of proteins putatively involved in the thiol: disulfide redox metabolism of a bacterium (Listeria): the CXXC motif as query sequence. In Silico Biol. 2009;9:407–414.
  • Cheng C, Jiang L, Ma T, et al. Carboxyl-terminal residues N478 and V479 required for the cytolytic activity of listeriolysin O play a critical role in listeria monocytogenes pathogenicity. Front Immunol. 2017;8:1439.
  • Gao XH, Zaffagnini M, Bedhomme M, et al. Biochemical characterization of glutaredoxins from Chlamydomonas reinhardtii: kinetics and specificity in deglutathionylation reactions. Febs Lett. 2010;584:2242–2248.
  • Zaffagnini M, Michelet L, Massot V, et al. Biochemical characterization of glutaredoxins from Chlamydomonas reinhardtii reveals the unique properties of a chloroplastic CGFS-type glutaredoxin. J Biol Chem. 2008;283:8868–8876.
  • Jaradat ZW, Bhunia AK. Adhesion, invasion, and translocation characteristics of Listeria monocytogenes serotypes in Caco-2 cell and mouse models. Appl Environ Microbiol. 2003;69:3640–3645.
  • Carmel-Harel O, Storz G. Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol. 2000;54:439–461.
  • Lecuit M, Ohayon H, Braun L, et al. Internalin of Listeria monocytogenes with an intact leucine-rich repeat region is sufficient to promote internalization. Infect Immun. 1997;65:5309–5319.
  • Lu J, Holmgren A. The thioredoxin superfamily in oxidative protein folding. Antioxid Redox Signal. 2014;21:457–470.
  • Fernandes AP, Holmgren A. Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal. 2004;6:63–74.
  • Ritz D, Beckwith J. Roles of thiol-redox pathways in bacteria. Annu Rev Microbiol. 2001;55:21–48.
  • Holmgren A. Antioxidant function of thioredoxin and glutaredoxin systems. Antioxid Redox Signal. 2000;2:811–820.
  • Lin K, O’Brien KM, Trujillo C, et al. Mycobacterium tuberculosis thioredoxin reductase is essential for thiol redox homeostasis but plays a minor role in antioxidant defense. PLoS Pathog. 2016;12:e1005675.
  • Imlay JA. Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem. 2008;77:755–776.
  • Storz G, Tartaglia LA, Ames BN. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science. 1990;248:189–194.
  • Imlay JA. Transcription factors that defend bacteria against reactive oxygen species. Annu Rev Microbiol. 2015;69:93–108.
  • Lee JW, Helmann JD. The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature. 2006;440:363–367.
  • Ahn BE, Baker TA. Oxidization without substrate unfolding triggers proteolysis of the peroxide-sensor, PerR. Proc Natl Acad Sci U S A. 2016;113:E23–31.
  • Horsburgh MJ, Clements MO, Crossley H, et al. PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect Immun. 2001;69:3744–3754.
  • Rea RB, Gahan CG, Hill C. Disruption of putative regulatory loci in Listeria monocytogenes demonstrates a significant role for Fur and PerR in virulence. Infect Immun. 2004;72:717–727.
  • Rea R, Hill C, Gahan CG. Listeria monocytogenes PerR mutants display a small-colony phenotype, increased sensitivity to hydrogen peroxide, and significantly reduced murine virulence. Appl Environ Microbiol. 2005;71:8314–8322.
  • Turner AK, Barber LZ, Wigley P, et al. Contribution of proton-translocating proteins to the virulence of Salmonella enterica serovars typhimurium, gallinarum, and Dublin in chickens and mice. Infect Immun. 2003;71:3392–3401.
  • Shi L, Sohaskey CD, Kana BD, et al. Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc Natl Acad Sci U S A. 2005;102:15629–15634.
  • Way SS, Sallustio S, Magliozzo RS, et al. Impact of either elevated or decreased levels of cytochrome bd expression on Shigella flexneri virulence. J Bacteriol. 1999;181:1229–1237.
  • Yamamoto Y, Poyart C, Trieu-Cuot P, et al. Respiration metabolism of Group B Streptococcus is activated by environmental haem and quinone and contributes to virulence. Mol Microbiol. 2005;56:525–534.
  • Larsen MH, Kallipolitis BH, Christiansen JK, et al. The response regulator ResD modulates virulence gene expression in response to carbohydrates in Listeria monocytogenes. Mol Microbiol. 2006;61:1622–1635.
  • Corbett D, Goldrick M, Fernandes VE, et al. Listeria monocytogenes has both a bd-type and an aa3 -type terminal oxidase which allow growth in different oxygen levels and both are important in infection. Infect Immun. 2017;85:pii: e00354-17.
  • Lindqvist A, Membrillo-Hernandez J, Poole RK, et al. Roles of respiratory oxidases in protecting Escherichia coli K12 from oxidative stress. Antonie Van Leeuwenhoek. 2000;78:23–31.
  • Sun YH, de Jong MF, Den Hartigh AB, et al. The small protein CydX is required for function of cytochrome bd oxidase in Brucella abortus. Front Cell Infect Microbiol. 2012;2:47.
  • Kuhns LG, Wang G, Maier RJ. Comparative roles of the two helicobacter pylori thioredoxins in preventing macromolecule damage. Infect Immun. 2015;83:2935–2943.
  • Potter AJ, Kidd SP, Edwards JL, 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. 2009;199:227–235.
  • Kraemer PS, Mitchell A, Pelletier MR, et al. Genome-wide screen in Francisella novicida for genes required for pulmonary and systemic infection in mice. Infect Immun. 2009;77:232–244.
  • Rocha ER, Tzianabos AO, Smith CJ. Thioredoxin reductase is essential for thiol/disulfide redox control and oxidative stress survival of the anaerobe Bacteroides fragilis. J Bacteriol. 2007;189:8015–8023.
  • Reniere ML, Whiteley AT, Hamilton KL, et al. Glutathione activates virulence gene expression of an intracellular pathogen. Nature. 2015;517:170–173.
  • Hall M, Grundstrom C, Begum A, et al. Structural basis for glutathione-mediated activation of the virulence regulatory protein PrfA in Listeria. Proc Natl Acad Sci U S A. 2016;113:14733–14738.
  • Lingnau A, Domann E, Hudel M, et al. Expression of the Listeria monocytogenes EGD inlA and inlB genes, whose products mediate bacterial entry into tissue culture cell lines, by PrfA-dependent and -independent mechanisms. Infect Immun. 1995;63:3896–3903.
  • Kim H, Marquis H, Boor KJ. SigmaB contributes to Listeria monocytogenes invasion by controlling expression of inlA and inlB. Microbiology. 2005;151:3215–3222.
  • Conte MP, Petrone G, Di Biase AM, et al. Acid tolerance in Listeria monocytogenes influences invasiveness of enterocyte-like cells and macrophage-like cells. Microb Pathog. 2000;29:137–144.
  • Gahan CG, O’Driscoll B, Hill C. Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation. Appl Environ Microbiol. 1996;62:3128–3132.
  • Degnan BA, Fontaine MC, Doebereiner AH, et al. Characterization of an isogenic mutant of Streptococcus pyogenes Manfredo lacking the ability to make streptococcal acid glycoprotein. Infect Immun. 2000;68:2441–2448.