NrdH-redoxin of Mycobacterium tuberculosis and Corynebacterium glutamicum dimerizes at high protein concentration and exclusively receives electrons from thioredoxin reductase

Journal of Biological Chemistry

Volumn 288, Issue 11, 2013, Pages 7942-7955

  Van Laer, Koen ^a,b   Dziewulska, Aleksandra M ^a,b   Fislage, Marcus ^a   Wahni, Khadija ^a,b   Hbeddou, Abderahim ^a,b   Collet, Jean Francois ^b,c,e   Versées, Wim ^a   Mateos, Luis M ^d   Dufe, Veronica Tamu ^a,b,e   Messens, Joris ^a,b  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b Brussels Center for Redox Biology   (Belgium)

^c DE DUVE INSTITUTE   (Belgium)

^d UNIVERSITY OF LEÓN   (Spain)

^e Welbio   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CORYNEBACTERIUM GLUTAMICUM; DEOXYRIBONUCLEOTIDES; MYCOBACTERIUM TUBERCULOSIS; PROTEIN CONCENTRATIONS; RIBONUCLEOTIDE REDUCTASE; SMALL ANGLE X-RAY SCATTERING; THIOL-DISULFIDE EXCHANGES; THIOREDOXIN REDUCTASE;

DIMERS; MODEL STRUCTURES; PROTEINS; TUBES (COMPONENTS);

AMINO ACIDS;

BACTERIAL PROTEIN; CYSTEINE; DIMER; MONOMER; PHENYLALANINE; PROTEIN NRDH; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG;

ACTINOBACTERIA; ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; CRYSTAL STRUCTURE; DIMERIZATION; DISULFIDE BOND; DNA TEMPLATE; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; GENE DELETION; GENE DISRUPTION; MOLECULAR WEIGHT; MUTANT; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NRDH GENE; PRIORITY JOURNAL; PROTEIN METABOLISM; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANTITUBERCULAR AGENTS; CATALYTIC DOMAIN; CLONING, MOLECULAR; CORYNEBACTERIUM GLUTAMICUM; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; DIMERIZATION; ELECTRONS; ESCHERICHIA COLI PROTEINS; GLYCOPEPTIDES; HYDROGEN-ION CONCENTRATION; INOSITOL; KINETICS; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOTIDES; SCATTERING, RADIATION; SEQUENCE HOMOLOGY, AMINO ACID; SURFACE PROPERTIES; THIOREDOXIN-DISULFIDE REDUCTASE; THIOREDOXINS; X-RAYS;

EID: 84875198694     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.392688     Document Type: Article

References (60)

1. Lundin, D., Torrents, E., Poole, A. M., and Sjöberg, B. M. (2009) RNRdb, a curated database of the universal enzyme family ribonucleotide reductase, reveals a high level of misannotation in sequences deposited to GenBank. BMC Genomics 10, 589
2. Nordlund, P., and Reichard, P. (2006) Ribonucleotide reductases. Annu. Rev. Biochem. 75, 681-706
3. Eklund, H., Uhlin, U., Färnegardh, M., Logan, D. T., and Nordlund, P. (2001) Structure and function of the radical enzyme ribonucleotide reductase. Prog. Biophys. Mol. Biol. 77, 177-268
4. Reichard, P., and Ehrenberg, A. (1983) Ribonucleotide reductase.Aradical enzyme. Science 221, 514-519
5. Nilsson, O., Lundqvist, T., Hahne, S., and Sjöberg, B. M. (1988) Structurefunction studies of the large subunit of ribonucleotide reductase from Escherichia coli. Biochem. Soc. Trans. 16, 91-94
6. Jordan, A., Pontis, E., Atta, M., Krook, M., Gibert, I., Barbé, J., and Reichard, P. (1994) A second class I ribonucleotide reductase in Enterobacteriaceae. Characterization of the Salmonella typhimurium enzyme. Proc. Natl. Acad. Sci. U.S.A. 91, 12892-12896
7. Mowa, M. B., Warner, D. F., Kaplan, G., Kana, B. D., and Mizrahi, V. (2009) Function and regulation of class I ribonucleotide reductase-encoding genes in mycobacteria. J. Bacteriol. 191, 985-995
8. Kolberg, M., Strand, K. R., Graff, P., and Andersson, K. K. (2004) Structure, function, and mechanism of ribonucleotide reductases. Biochim. Biophys. Acta 1699, 1-34
9. Stehr, M., and Lindqvist, Y. (2004) NrdH-redoxin of Corynebacterium ammoniagenes forms a domain-swapped dimer. Proteins 55, 613-619
10. Jordan, A., Aslund, F., Pontis, E., Reichard, P., and Holmgren, A. (1997) Characterization of Escherichia coli NrdH. A glutaredoxin-like protein with a thioredoxin-like activity profile. J. Biol. Chem. 272, 18044-18050
11. Rabinovitch, I., Yanku, M., Yeheskel, A., Cohen, G., Borovok, I., and Aharonowitz, Y. (2010) Staphylococcus aureus NrdH redoxin is a reductant of the class Ib ribonucleotide reductase. J. Bacteriol. 192, 4963-4972
12. Boal, A. K., Cotruvo, J. A., Jr., Stubbe, J., and Rosenzweig, A. C. (2010) Structural basis for activation of class Ib ribonucleotide reductase. Science 329, 1526-1530
13. Van Laer, K., Hamilton, C. J., and Messens, J. (2012) Low-molecularweight thiols in thiol-disulfide exchange. Antioxid. Redox. Signal., doi:10.1089/ars.2012.4964
14. Newton, G. L., Rawat, M., La Clair, J. J., Jothivasan, V. K., Budiarto, T., Hamilton, C. J., Claiborne, A., Helmann, J. D., and Fahey, R. C. (2009) Bacillithiol is an antioxidant thiol produced in Bacilli. Nat. Chem. Biol. 5, 625-627
15. Gustafsson, T. N., Sahlin, M., Lu, J., Sjöberg, B. M., and Holmgren, A. (2012) Bacillus anthracis thioredoxin systems, characterization and role as electron donors for ribonucleotide reductase. J. Biol. Chem. 287, 39686-39697
16. Ordóñez, 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. 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 defence mechanism of Mycobacteria. Mol. Microbiol. 86, 787-804
18. 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
19. Kabsch, W. (1988) Evaluation of single-crystal X-ray-diffraction data from a position-sensitive detector. J. Appl. Crystallogr. 21, 916-924
20. Long, F., Vagin, A. A., Young, P., and Murshudov, G. N. (2008) BALBES.A molecular-replacement pipeline. Acta Crystallogr. D Biol. Crystallogr. 64, 125-132
21. Stehr, M., Schneider, G., Aslund, F., Holmgren, A., and Lindqvist, Y. (2001) Structural basis for the thioredoxin-like activity profile of the glutaredoxin-like NrdH-redoxin from Escherichia coli. J. Biol. Chem. 276, 35836-35841
22. Eklund, H., Ingelman, M., Söderberg, B. O., Uhlin, T., Nordlund, P., Nikkola, M., Sonnerstam, U., Joelson, T., and Petratos, K. (1992) Structure of oxidized bacteriophage T4 glutaredoxin (thioredoxin). Refinement of native and mutant proteins. J. Mol. Biol. 228, 596-618
23. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for x-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179
24. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
25. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
26. Painter, J., and Merritt, E. A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D 62, 439-450
27. Painter, J., and Merritt, E. A. (2006) TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr. 39, 109-111
28. Lassmann, T., and Sonnhammer, E. L. (2005) Kalign. An accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 6, 298
29. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U., and Sali, A. (2006) Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics, Chapter 5, Unit 5.6
30. Lennon, B. W., Williams, C. H., Jr., and Ludwig, M. L. (2000) Twists in catalysis. Alternating conformations of Escherichia coli thioredoxin reductase. Science 289, 1190-1194
31. Akif, M., Suhre, K., Verma, C., and Mande, S. C. (2005) Conformational flexibility of Mycobacterium tuberculosis thioredoxin reductase. Crystal structure and normal-mode analysis. Acta Crystallogr. D Biol. Crystallogr. 61, 1603-1611
32. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4. Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447
33. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR. An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res. 32, W665-W667
34. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems. Application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
35. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) ClustalW and ClustalX version 2.0. Bioinformatics 23, 2947-2948
36. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J., and Svergun, D. I. (2003) PRIMUS. A Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282
37. Guinier, A., and Fournet, G. (1955) Small-angle Scattering of X-rays, John Wiley & Sons, Inc., New York
38. Porod, G. (1982) Small Angle X-ray Scattering, pp. 17-51, Academic Press, Inc., New York
39. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
40. Konarev, P. V., Petoukhov, M. V., Volkov, V. V., and Svergun, D. I. (2006) ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 39, 277-286
41. Fernández-Gonzalez, C., Gil, J. A., Mateos, L. M., Schwarzer, A., Schäfer, A., Kalinowski, J., Pühler, A., and Martín, J. F. (1996) Construction of L-lysine-overproducing strains of Brevibacterium lactofermentum by targeted disruption of the hom and thrB genes. Appl. Microbiol. Biotechnol. 46, 554-558
42. Jäger, W., Schäfer, A., Pühler, A., Labes, G., and Wohlleben, W. (1992) Expression of the Bacillus subtilis sacB gene leads to sucrose sensitivity in the gram-positive bacterium Corynebacterium glutamicum but not in Streptomyces lividans. J. Bacteriol. 174, 5462-5465
43. Ordóñez, E., Thiyagarajan, S., Cook, J. D., Stemmler, T. L., Gil, J. A., Mateos, L. M., and Rosen, B. P. (2008) Evolution of metal(loid) binding sites in transcriptional regulators. J. Biol. Chem. 283, 25706-25714
44. Patel, M. P., and Blanchard, J. S. (1999) Expression, purification, and characterization of Mycobacterium tuberculosis mycothione reductase. Biochemistry 38, 11827-11833
45. Akif, M., Khare, G., Tyagi, A. K., Mande, S. C., and Sardesai, A. A. (2008) Functional studies of multiple thioredoxins from Mycobacterium tuberculosis. J. Bacteriol. 190, 7087-7095
46. Garcia-Pino, A., Martinez-Rodriguez, S., Wahni, K., Wyns, L., Loris, R., and Messens, J. (2009) Coupling of domain swapping to kinetic stability in a thioredoxin mutant. J. Mol. Biol. 385, 1590-1599
47. Rousseau, F., Schymkowitz, J. W., and Itzhaki, L. S. (2003) The unfolding story of three-dimensional domain swapping. Structure 11, 243-251
48. Liu, Y., and Eisenberg, D. (2002) 3D domain swapping. As domains continue to swap. Protein Sci. 11, 1285-1299
49. Newcomer, M. E. (2001) Trading places. Nat. Struct. Biol. 8, 282-284
50. Kiefer, F., Arnold, K., Künzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res. 37, D387-D392
51. Leiting, W. U., and Jianping, X. I. (2010) Comparative genomics analysis of Mycobacterium NrdH-redoxins. Microb. Pathog. 48, 97-102
52. Jensen, K. S., Hansen, R. E., and Winther, J. R. (2009) Kinetic and thermodynamic aspects of cellular thiol-disulfide redox regulation. Antioxid. Redox. Signal. 11, 1047-1058
53. Roos, G., Foloppe, N., and Messens, J. (2013) Understanding the pKa of redox cysteines. The key role of hydrogen bonding. Antioxid. Redox. Signal. 18, 94-127
54. Collet, J. F., and Messens, J. (2010) Structure, function, and mechanism of thioredoxin proteins. Antioxid. Redox. Signal. 13, 1205-1216
55. Roos, G., Loverix, S., and Geerlings, P. (2006) Origin of the pKa perturbation of N-terminal cysteine in α- and 310-helices. A computational DFT study. J. Phys. Chem. B 110, 557-562
56. Roos, G., Foloppe, N., Van Laer, K., Wyns, L., Nilsson, L., Geerlings, P., and Messens, J. (2009) How thioredoxin dissociates its mixed disulfide. PLoS Comput. Biol. 5, e1000461
57. Sassetti, C. M., Boyd, D. H., and Rubin, E. J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48, 77-84
58. Harris, T. K., and Turner, G. J. (2002) Structural basis of perturbed pKa values of catalytic groups in enzyme active sites. IUBMB Life 53, 85-98
59. Williams, C. H., Arscott, L. D., Müller, S., Lennon, B. W., Ludwig, M. L., Wang, P. F., Veine, D. M., Becker, K., and Schirmer, R. H. (2000) Thioredoxin reductase two modes of catalysis have evolved. Eur. J. Biochem. 267, 6110-6117
60. Chebotareva, N. A., Kurganov, B. I., and Livanova, N. B. (2004) Biochemical effects of molecular crowding. Biochemistry 69, 1239-1251