Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress

Chi BK, Busche T, Van Laer K, Baesell K, Becher D, Clermont L, Seibold GM, Persicke M, Kalinowski J, Messens J, Antelmann H (2014)
Antioxidants & Redox Signaling 20(4): 589-605.

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Aims: Protein S-bacillithiolation was recently discovered as important thiol protection and redox-switch mechanism in response to hypochlorite stress in Firmicutes bacteria. Here we used transcriptomics to analyze the NaOCl stress response in the mycothiol (MSH)-producing Corynebacterium glutamicum. We further applied thiol-redox proteomics and mass spectrometry (MS) to identify protein S-mycothiolation. Results: Transcriptomics revealed the strong upregulation of the disulfide stress sigma(H) regulon by NaOCl stress in C. glutamicum, including genes for the anti sigma factor (rshA), the thioredoxin and MSH pathways (trxB1, trxC, cg1375, trxB, mshC, mca, mtr) that maintain the redox balance. We identified 25 S-mycothiolated proteins in NaOCl-treated cells by liquid chromatography-tandem mass spectrometry (LC-MS/MS), including 16 proteins that are reversibly oxidized by NaOCl in the thiol-redox proteome. The S-mycothiolome includes the methionine synthase (MetE), the maltodextrin phosphorylase (MalP), the myoinositol-1-phosphate synthase (Ino1), enzymes for the biosynthesis of nucleotides (GuaB1, GuaB2, PurL, NadC), and thiamine (ThiD), translation proteins (TufA, PheT, RpsF, RplM, RpsM, RpsC), and antioxidant enzymes (Tpx, Gpx, MsrA). We further show that S-mycothiolation of the thiol peroxidase (Tpx) affects its peroxiredoxin activity in vitro that can be restored by mycoredoxin1. LC-MS/MS analysis further identified 8 proteins with S-cysteinylations in the mshC mutant suggesting that cysteine can be used for S-thiolations in the absence of MSH. Innovation and Conclusion: We identified widespread protein S-mycothiolations in the MSH-producing C. glutamicum and demonstrate that S-mycothiolation reversibly affects the peroxidase activity of Tpx. Interestingly, many targets are conserved S-thiolated across bacillithiol- and MSH-producing bacteria, which could become future drug targets in related pathogenic Gram-positives.
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Chi BK, Busche T, Van Laer K, et al. Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling. 2014;20(4):589-605.
Chi, B. K., Busche, T., Van Laer, K., Baesell, K., Becher, D., Clermont, L., Seibold, G. M., et al. (2014). Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling, 20(4), 589-605. doi:10.1089/ars.2013.5423
Chi, B. K., Busche, T., Van Laer, K., Baesell, K., Becher, D., Clermont, L., Seibold, G. M., Persicke, M., Kalinowski, J., Messens, J., et al. (2014). Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling 20, 589-605.
Chi, B.K., et al., 2014. Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling, 20(4), p 589-605.
B.K. Chi, et al., “Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress”, Antioxidants & Redox Signaling, vol. 20, 2014, pp. 589-605.
Chi, B.K., Busche, T., Van Laer, K., Baesell, K., Becher, D., Clermont, L., Seibold, G.M., Persicke, M., Kalinowski, J., Messens, J., Antelmann, H.: Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling. 20, 589-605 (2014).
Chi, Bui Khanh, Busche, Tobias, Van Laer, Koen, Baesell, Katrin, Becher, Doerte, Clermont, Lina, Seibold, Gerd M., Persicke, Marcus, Kalinowski, Jörn, Messens, Joris, and Antelmann, Haike. “Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress”. Antioxidants & Redox Signaling 20.4 (2014): 589-605.
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19 Citations in Europe PMC

Data provided by Europe PubMed Central.

Protein S-Bacillithiolation Functions in Thiol Protection and Redox Regulation of the Glyceraldehyde-3-Phosphate Dehydrogenase Gap in Staphylococcus aureus Under Hypochlorite Stress.
Imber M, Huyen NTT, Pietrzyk-Brzezinska AJ, Loi VV, Hillion M, Bernhardt J, Thärichen L, Kolšek K, Saleh M, Hamilton CJ, Adrian L, Gräter F, Wahl MC, Antelmann H., Antioxid Redox Signal 28(6), 2018
PMID: 27967218
The Role of Bacillithiol in Gram-Positive Firmicutes.
Chandrangsu P, Loi VV, Antelmann H, Helmann JD., Antioxid Redox Signal 28(6), 2018
PMID: 28301954
Chemistry and Redox Biology of Mycothiol.
Reyes AM, Pedre B, De Armas MI, Tossounian MA, Radi R, Messens J, Trujillo M., Antioxid Redox Signal 28(6), 2018
PMID: 28372502
Redox-Sensing Under Hypochlorite Stress and Infection Conditions by the Rrf2-Family Repressor HypR in Staphylococcus aureus.
Van Loi V, Busche T, Tedin K, Bernhardt J, Wollenhaupt J, Huyen NTT, Weise C, Kalinowski J, Wahl MC, Fulde M, Antelmann H., Antioxid Redox Signal (), 2018
PMID: 29237286
Graded Response of the Multifunctional 2-Cysteine Peroxiredoxin, CgPrx, to Increasing Levels of Hydrogen Peroxide in Corynebacterium glutamicum.
Si M, Wang T, Pan J, Lin J, Chen C, Wei Y, Lu Z, Wei G, Shen X., Antioxid Redox Signal 26(1), 2017
PMID: 27324811
European contribution to the study of ROS: A summary of the findings and prospects for the future from the COST action BM1203 (EU-ROS).
Egea J, Fabregat I, Frapart YM, Ghezzi P, Görlach A, Kietzmann T, Kubaichuk K, Knaus UG, Lopez MG, Olaso-Gonzalez G, Petry A, Schulz R, Vina J, Winyard P, Abbas K, Ademowo OS, Afonso CB, Andreadou I, Antelmann H, Antunes F, Aslan M, Bachschmid MM, Barbosa RM, Belousov V, Berndt C, Bernlohr D, Bertrán E, Bindoli A, Bottari SP, Brito PM, Carrara G, Casas AI, Chatzi A, Chondrogianni N, Conrad M, Cooke MS, Costa JG, Cuadrado A, My-Chan Dang P, De Smet B, Debelec-Butuner B, Dias IHK, Dunn JD, Edson AJ, El Assar M, El-Benna J, Ferdinandy P, Fernandes AS, Fladmark KE, Förstermann U, Giniatullin R, Giricz Z, Görbe A, Griffiths H, Hampl V, Hanf A, Herget J, Hernansanz-Agustín P, Hillion M, Huang J, Ilikay S, Jansen-Dürr P, Jaquet V, Joles JA, Kalyanaraman B, Kaminskyy D, Karbaschi M, Kleanthous M, Klotz LO, Korac B, Korkmaz KS, Koziel R, Kračun D, Krause KH, Křen V, Krieg T, Laranjinha J, Lazou A, Li H, Martínez-Ruiz A, Matsui R, McBean GJ, Meredith SP, Messens J, Miguel V, Mikhed Y, Milisav I, Milković L, Miranda-Vizuete A, Mojović M, Monsalve M, Mouthuy PA, Mulvey J, Münzel T, Muzykantov V, Nguyen ITN, Oelze M, Oliveira NG, Palmeira CM, Papaevgeniou N, Pavićević A, Pedre B, Peyrot F, Phylactides M, Pircalabioru GG, Pitt AR, Poulsen HE, Prieto I, Rigobello MP, Robledinos-Antón N, Rodríguez-Mañas L, Rolo AP, Rousset F, Ruskovska T, Saraiva N, Sasson S, Schröder K, Semen K, Seredenina T, Shakirzyanova A, Smith GL, Soldati T, Sousa BC, Spickett CM, Stancic A, Stasia MJ, Steinbrenner H, Stepanić V, Steven S, Tokatlidis K, Tuncay E, Turan B, Ursini F, Vacek J, Vajnerova O, Valentová K, Van Breusegem F, Varisli L, Veal EA, Yalçın AS, Yelisyeyeva O, Žarković N, Zatloukalová M, Zielonka J, Touyz RM, Papapetropoulos A, Grune T, Lamas S, Schmidt HHHW, Di Lisa F, Daiber A., Redox Biol 13(), 2017
PMID: 28577489
The antibacterial prodrug activator Rv2466c is a mycothiol-dependent reductase in the oxidative stress response of Mycobacterium tuberculosis.
Rosado LA, Wahni K, Degiacomi G, Pedre B, Young D, de la Rubia AG, Boldrin F, Martens E, Marcos-Pascual L, Sancho-Vaello E, Albesa-Jové D, Provvedi R, Martin C, Makarov V, Versées W, Verniest G, Guerin ME, Mateos LM, Manganelli R, Messens J., J Biol Chem 292(32), 2017
PMID: 28620052
The glyceraldehyde-3-phosphate dehydrogenase GapDH of Corynebacterium diphtheriae is redox-controlled by protein S-mycothiolation under oxidative stress.
Hillion M, Imber M, Pedre B, Bernhardt J, Saleh M, Loi VV, Maaß S, Becher D, Astolfi Rosado L, Adrian L, Weise C, Hell R, Wirtz M, Messens J, Antelmann H., Sci Rep 7(1), 2017
PMID: 28694441
One- and two-electron oxidation of thiols: mechanisms, kinetics and biological fates.
Trujillo M, Alvarez B, Radi R., Free Radic Res 50(2), 2016
PMID: 26329537
Lack of mycothiol and ergothioneine induces different protective mechanisms in Mycobacterium smegmatis.
Singh AR, Strankman A, Orkusyan R, Purwantini E, Rawat M., Biochem Biophys Rep 8(), 2016
PMID: 28220152
Corynebacterium glutamicum methionine sulfoxide reductase A uses both mycoredoxin and thioredoxin for regeneration and oxidative stress resistance.
Si M, Zhang L, Chaudhry MT, Ding W, Xu Y, Chen C, Akbar A, Shen X, Liu SJ., Appl Environ Microbiol 81(8), 2015
PMID: 25681179
Corynebacterium diphtheriae methionine sulfoxide reductase a exploits a unique mycothiol redox relay mechanism.
Tossounian MA, Pedre B, Wahni K, Erdogan H, Vertommen D, Van Molle I, Messens J., J Biol Chem 290(18), 2015
PMID: 25752606
Redox regulation by reversible protein S-thiolation in bacteria.
Loi VV, Rossius M, Antelmann H., Front Microbiol 6(), 2015
PMID: 25852656
The Corynebacterium glutamicum mycothiol peroxidase is a reactive oxygen species-scavenging enzyme that shows promiscuity in thiol redox control.
Pedre B, Van Molle I, Villadangos AF, Wahni K, Vertommen D, Turell L, Erdogan H, Mateos LM, Messens J., Mol Microbiol 96(6), 2015
PMID: 25766783
Thiol-based redox switches in prokaryotes.
Hillion M, Antelmann H., Biol Chem 396(5), 2015
PMID: 25720121
NrdH Redoxin enhances resistance to multiple oxidative stresses by acting as a peroxidase cofactor in Corynebacterium glutamicum.
Si MR, Zhang L, Yang ZF, Xu YX, Liu YB, Jiang CY, Wang Y, Shen XH, Liu SJ., Appl Environ Microbiol 80(5), 2014
PMID: 24375145

60 References

Data provided by Europe PubMed Central.

Glycogen formation in Corynebacterium glutamicum and role of ADP-glucose pyrophosphorylase.
Seibold G, Dempf S, Schreiner J, Eikmanns BJ., Microbiology (Reading, Engl.) 153(Pt 4), 2007
PMID: 17379737
Roles of maltodextrin and glycogen phosphorylases in maltose utilization and glycogen metabolism in Corynebacterium glutamicum.
Seibold GM, Wurst M, Eikmanns BJ., Microbiology (Reading, Engl.) 155(Pt 2), 2009
PMID: 19202084
Genesis: cluster analysis of microarray data.
Sturn A, Quackenbush J, Trajanoski Z., Bioinformatics 18(1), 2002
PMID: 11836235
Mycoredoxin-1 is one of the missing links in the oxidative stress defence mechanism of Mycobacteria.
Van Laer K, Buts L, Foloppe N, Vertommen D, Van Belle K, Wahni K, Roos G, Nilsson L, Mateos LM, Rawat M, van Nuland NA, Messens J., Mol. Microbiol. 86(4), 2012
PMID: 22970802
Low-molecular-weight thiols in thiol-disulfide exchange.
Van Laer K, Hamilton CJ, Messens J., Antioxid. Redox Signal. 18(13), 2013
PMID: 23075082
Redox active thiol sensors of oxidative and nitrosative stress.
Vazquez-Torres A., Antioxid. Redox Signal. 17(9), 2012
PMID: 22257022
Corynebacterium glutamicum survives arsenic stress with arsenate reductases coupled to two distinct redox mechanisms.
Villadangos AF, Van Belle K, Wahni K, Dufe VT, Freitas S, Nur H, De Galan S, Gil JA, Collet JF, Mateos LM, Messens J., Mol. Microbiol. 82(4), 2011
PMID: 22032722

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