Mycothiol/mycoredoxin 1-dependent reduction of the peroxiredoxin AhpE from mycobacterium tuberculosis

Journal of Biological Chemistry

Volumn 289, Issue 8, 2014, Pages 5228-5239

  Hugo, Martín ^a   Van Laer, Koen ^b,c,d   Reyes, Aníbal M ^a   Vertommen, Didier ^e   Messens, Joris ^b,c,d   Radi, Rafael ^a   Trujillo, Madia ^a  

^a UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c Brussels Center for Redox Biology   (Belgium)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^e DE DUVE INSTITUTE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS;

LOW-MOLECULAR WEIGHT; MOLECULAR LINKS; MYCOBACTERIUM TUBERCULOSIS;

DETOXIFICATION;

ALKYL HYDROXYPEROXIDE REDUCTASE E; CYSTEINE; DISULFIDE; HYDROGEN PEROXIDE; MYCOREDOXIN 1; MYCOTHIOL; MYCOTHIOL DISULFIDE REDUCTASE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; THIOL; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; DETOXIFICATION; DISULFIDE BOND; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SUBSTRATE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OXIDATION; PRIORITY JOURNAL;

HYDROGEN PEROXIDE; MYCOBACTERIUM TUBERCULOSIS; MYCOREDOXIN; MYCOTHIOL; PEROXIREDOXIN; REDOX SIGNALING; THIOL;

BACTERIAL PROTEINS; BIOCATALYSIS; CYSTEINE; DISULFIDES; GLYCOPEPTIDES; HYDROGEN PEROXIDE; HYDROGEN-ION CONCENTRATION; INOSITOL; KINETICS; MODELS, BIOLOGICAL; MYCOBACTERIUM TUBERCULOSIS; NADP; OXIDATION-REDUCTION; PEROXIREDOXINS;

EID: 84894436598     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.510248     Document Type: Article

References (48)

1. World Health Organization. (2012) Global Tuberculosis Report
2. Nathan, C. (2009) Taming tuberculosis: a challenge for science and society. Cell Host Microbe. 5, 220-224
3. Alvarez, M. N., Peluffo, G., Piacenza, L., and Radi, R. (2011) Intraphagosomal peroxynitrite as a macrophage-derived cytotoxin against internalized Trypanosoma cruzi: consequences for oxidative killing and role of microbial peroxiredoxins in infectivity. J. Biol. Chem. 286, 6627-6640
4. Fang, F. C. (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2, 820-832
5. Nathan, C., and Shiloh, M. U. (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. U.S.A. 97, 8841-8848
6. Newton, G. L., and Fahey, R. C. (2002) Mycothiol biochemistry. Arch. Microbiol. 178, 388-394
7. Van Laer, K., Hamilton, C. J., and Messens, J. (2013) Low-molecularweight thiols in thiol-disulfide exchange. Antioxid. Redox Signal. 18, 1642-1653
8. Patel, M. P., and Blanchard, J. S. (1999) Expression, purification, and characterization of Mycobacterium tuberculosis mycothione reductase. Biochemistry 38, 11827-11833
9. Rawat, M., Johnson, C., Cadiz, V., and Av-Gay, Y. (2007) Comparative analysis of mutants in the mycothiol biosynthesis pathway in Mycobacterium smegmatis. Biochem. Biophys. Res. Commun. 363, 71-76
10. Rawat, M., Kovacevic, S., Billman-Jacobe, H., and Av-Gay, Y. (2003) Inactivation of mshB, a key gene in the mycothiol biosynthesis pathway in Mycobacterium smegmatis. Microbiology 149, 1341-1349
11. Rawat, M., Newton, G. L., Ko, M., Martinez, G. J., Fahey, R. C., and Av-Gay, Y. (2002) Mycothiol-deficient Mycobacterium smegmatis mutants are hypersensitive to alkylating agents, free radicals, and antibiotics. Antimicrob Agents Chemother 46, 3348-3355
12. Ta, P., Buchmeier, N., Newton, G. L., Rawat, M., and Fahey, R. C. (2011) Organic hydroperoxide resistance protein and ergothioneine compensate for loss of mycothiol in Mycobacterium smegmatis mutants. J. Bacteriol. 193, 1981-1990
13. Jaeger, T., Budde, H., Flohé, L., Menge, U., Singh, M., Trujillo, M., and Radi, R. (2004) Multiple thioredoxin-mediated routes to detoxify hydroperoxides in Mycobacterium tuberculosis. Arch. Biochem. Biophys. 423, 182-191
14. Cole, S. T., and Barrell, B. G. (1998) Analysis of the genome of Mycobacterium tuberculosis H37Rv. Novartis Found Symp. 217, 160-172; discussion 172-167
15. Van Laer, K., Buts, L., Foloppe, N., Vertommen, D., Van Belle, K., Wahni, K., Roos, G., Nilsson, L., Mateos, L. M., Rawat, M., van Nuland, N. A., and Messens, J. (2012) Mycoredoxin-1 is one of the missing links in the oxidative stress defense mechanism of Mycobacteria. Mol. Microbiol. 86, 787-804
16. Ordoñez, E., Van Belle, K., Roos, G., De Galan, S., Letek, M., Gil, J. A., Wyns, L., Mateos, L. M., and Messens, J. (2009) Arsenate reductase, mycothiol, and mycoredoxin concert thiol/disulfide exchange. J. Biol. Chem. 284, 15107-15116
17. Chi, B. K., Busche, T., Laer, K. V., Basell, K., Becher, D., Clermont, L., Seibold, G. M., Persicke, M., Kalinowski, J., Messens, J., and Antelmann, H. (2013) Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxid. Redox Signal., In press
18. Hugo, M., Radi, R., and Trujillo, M. (2012) Thiol dependent peroxidases in Mycobacterium tuberculosis in Understanding Tuberculosis: Deciphering the Secret Life of the Bacilli (Cardona, P.-J., ed.), InTech. pp. 293-316
19. Soito, L., Williamson, C., Knutson, S. T., Fetrow, J. S., Poole, L. B., and Nelson, K. J. (2011) PREX: PeroxiRedoxin classification indEX, a database of subfamily assignments across the diverse peroxiredoxin family. Nucleic Acids Res. 39, D332-337
20. Oliva, M., Theiler, G., Zamocky, M., Koua, D., Margis-Pinheiro, M., Passardi, F., and Dunand, C. (2009) PeroxiBase: a powerful tool to collect and analyse peroxidase sequences from Viridiplantae. J. Exp. Bot. 60, 453-459
21. Li, S., Peterson, N. A., Kim, M. Y., Kim, C. Y., Hung, L. W., Yu, M., Lekin, T., Segelke, B. W., Lott, J. S., and Baker, E. N. (2005) Crystal Structure of AhpE from Mycobacterium tuberculosis, a 1-Cys peroxiredoxin. J. Mol. Biol. 346, 1035-1046
22. Hugo, M., Turell, L., Manta, B., Botti, H., Monteiro, G., Netto, L. E., Alvarez, B., Radi, R., and Trujillo, M. (2009) Thiol and sulfenic acid oxidation of AhpE, the one-cysteine peroxiredoxin from Mycobacterium tuberculosis: kinetics, acidity constants, and conformational dynamics. Biochemistry 48, 9416-9426
23. Reyes, A. M., Hugo, M., Trostchansky, A., Capece, L., Radi, R., and Trujillo, M. (2011) Oxidizing substrate specificity of Mycobacterium tuberculosis alkyl hydroperoxide reductase E: kinetics and mechanisms of oxidation and overoxidation. Free Radic. Biol. Med. 51, 464-473
24. Hildebraundt, A. G., and Roots, I. (1975) Reduced nicotinamide adenine dinucleotide phosphate (NADPH) dependent formation and breakdown of hydrogen peroxide during mixed function oxidation reactions in liver microsomes. Arch. Biochem. Biophys. 171, 385-397
25. Schonbaum, G. R., and Lo, S. (1972) Interaction of peroxidases with aromatic peracids and alkyl peroxides. Product analysis. J. Biol. Chem. 247, 3353-3360
26. Ellman, G. L. (1959) Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77
27. Riddles, P. W., Blakeley, R. L., and Zerner, B. (1979) Ellman's reagent: 5,5dithiobis(2-nitrobenzoic acid)-a reexamination. Anal. Biochem. 94, 75-81
28. Pyr Dit Ruys, S., Wang, X., Smith, E. M., Herinckx, G., Hussain, N., Rider, M. H., Vertommen, D., and Proud, C. G. (2012) Identification of autophosphorylation sites in eukaryotic elongation factor-2 kinase. Biochem. J. 442, 681-692
29. Choi, S., Jeong, J., Na, S., Lee, H. S., Kim, H. Y., Lee, K. J., and Paek, E. (2010) New algorithm for the identification of intact disulfide linkages based on fragmentation characteristics in tandem mass spectra. J. Proteome Res. 9, 626-635
30. Mendes, P. (1993) GEPASI: a software package for modelling the dynamics, steady states and control of biochemical and other systems. Comput. Appl. Biosci. 9, 563-571
31. Roos, G., Garcia-Pino, A., Van Belle, K., Brosens, E., Wahni, K., Vandenbussche, G., Wyns, L., Loris, R., and Messens, J. (2007) The conserved active site proline determines the reducing power of Staphylococcus aureus thioredoxin. J. Mol. Biol. 368, 800-811
32. Piñeyro, M. D., Arcari, T., Robello, C., Radi, R., and Trujillo, M. (2011) Tryparedoxin peroxidases from Trypanosoma cruzi: high efficiency in the catalytic elimination of hydrogen peroxide and peroxynitrite. Arch. Biochem. Biophys. 507, 287-295
33. Villadangos, A. F., Van Belle, K., Wahni, K., Dufe, V. T., Freitas, S., Nur, H., De Galan, S., Gil, J. A., Collet, J. F., Mateos, L. M., and Messens, J. (2011) Corynebacterium glutamicum survives arsenic stress with arsenate reductases coupled to two distinct redox mechanisms. Mol. Microbiol. 82, 998-1014
34. Gu, S., Chen, J., Dobos, K. M., Bradbury, E. M., Belisle, J. T., and Chen, X. (2003) Comprehensive proteomic profiling of the membrane constituents of a Mycobacterium tuberculosis strain. Mol. Cell Proteomics 2, 1284-1296
35. Winterbourn, C. C., and Metodiewa, D. (1999) Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic Biol. Med. 27, 322-328
36. Trujillo, M., Mauri, P., Benazzi, L., Comini, M., De Palma, A., Flohé, L., Radi, R., Stehr, M., Singh, M., Ursini, F., and Jaeger, T. (2006) The mycobacterial thioredoxin peroxidase can act as a one-cysteine peroxiredoxin. J. Biol. Chem. 281, 20555-20566
37. Rouhier, N., Gelhaye, E., and Jacquot, J. P. (2002) Glutaredoxin- dependent peroxiredoxin from poplar: protein-protein interaction and catalytic mechanism. J. Biol. Chem. 277, 13609-13614
38. Pedrajas, J. R., Padilla, C. A., McDonagh, B., and Bárcena, J. A. (2010) Glutaredoxin participates in the reduction of peroxides by the mitochondrial 1-CYS peroxiredoxin in Saccharomyces cerevisiae. Antioxid Redox Signal 13, 249-258
39. Hanschmann, E. M., Lönn, M. E., Schütte, L. D., Funke, M., Godoy, J. R., Eitner, S., Hudemann, C., and Lillig, C. H. (2010) Both thioredoxin 2 and glutaredoxin 2 contribute to the reduction of the mitochondrial 2-Cys peroxiredoxin Prx3. J. Biol. Chem. 285, 40699-40705
40. Reeves, S. A., Parsonage, D., Nelson, K. J., and Poole, L. B. (2011) Kinetic and thermodynamic features reveal that Escherichia coli BCP is an unusually versatile peroxiredoxin. Biochemistry 50, 8970-8981
41. Reynolds, C. M., Meyer, J., and Poole, L. B. (2002) An NADH-dependent bacterial thioredoxin reductase-like protein in conjunction with a glutaredoxin homologue form a unique peroxiredoxin (AhpC) reducing system in Clostridium pasteurianum. Biochemistry 41, 1990-2001
42. Bryk, R., Lima, C. D., Erdjument-Bromage, H., Tempst, P., and Nathan, C. (2002) Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295, 1073-1077
43. Dormeyer, M., Reckenfelderbäumer, N., Ludemann, H., and Krauth-Siegel, R. L. (2001) Trypanothione-dependent synthesis of deoxyribonucleotides by Trypanosoma brucei ribonucleotide reductase. J. Biol. Chem. 276, 10602-10606
44. Holmgren, A. (1979) Glutathione-dependent synthesis of deoxyribonucleotides. Characterization of the enzymatic mechanism of Escherichia coli glutaredoxin. J. Biol. Chem. 254, 3672-3678
45. Van Laer, K., Dziewulska, A. M., Fislage, M., Wahni, K., Hbeddou, A., Collet, J. F., Versées, W., Mateos, L. M., Tamu Dufe, V., and Messens, J. (2013) NrdH-redoxin of Mycobacterium tuberculosis and Corynebacterium glutamicum dimerizes at high protein concentration and exclusively receives electrons from thioredoxin reductase. J. Biol. Chem. 288, 7942-7955
46. Delaunay, A., Pflieger, D., Barrault, M. B., Vinh, J., and Toledano, M. B. (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111, 471-481
47. Fomenko, D. E., Koc, A., Agisheva, N., Jacobsen, M., Kaya, A., Malinouski, M., Rutherford, J. C., Siu, K. L., Jin, D. Y., Winge, D. R., and Gladyshev, V. N. (2011) Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide. Proc. Natl. Acad. Sci. U.S.A. 108, 2729-2734
48. Azevedo, D., Tacnet, F., Delaunay, A., Rodrigues-Pousada, C., and Toledano, M. B. (2003) Two redox centers within Yap1 for H2O2 and thiolreactive chemicals signaling. Free Radic Biol. Med. 35, 889-900