Redox proteomics uncovers peroxynitrite-sensitive proteins that help escherichia coli to overcome nitrosative stress

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 19698-19714

  Lindemann, Claudia ^a   Lupilova, Nataliya ^a   Müller, Alexandra ^a   Warscheid, Bettina ^b   Meyer, Helmut E ^a   Kuhlmann, Katja ^a   Eisenacher, Martin ^a   Leichert, Lars I ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBACTERIAL PROPERTIES; CONSTITUTIVELY ACTIVES; ISOTOPE-CODED AFFINITY TAG; NITROSATIVE STRESS; PROTEOMIC APPROACHES; REACTIVE CHEMICALS; STRESS TOLERANCE; TYROSINE RESIDUES;

AMINO ACIDS; ESCHERICHIA COLI; ISOTOPES; MOLECULAR BIOLOGY;

PROTEINS;

BACTERIAL PROTEIN; CYSTEINE; DEAMINASE; ENAMINE DEAMINASE; IMINE; IMINE DEAMINASE; PEROXYNITRITE; PROTEIN ASNB; PROTEIN FRMA; PROTEIN MAEB; PROTEIN RIDA; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; IN VITRO STUDY; NITRATION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN TARGETING; PROTEOMICS; QUANTITATIVE ANALYSIS; REDOX STRESS;

MICROBIOLOGY; NITROSATIVE STRESS; PEROXYNITRITE; PROTEOMICS; REDOX; THIOL;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXYNITROUS ACID; PROTEOMICS;

EID: 84880079480     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.457556     Document Type: Article

References (49)

1. Zheng, M., Aslund, F., and Storz, G. (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279, 1718-1721
2. Zheng, M., and Storz, G. (2000) Redox sensing by prokaryotic transcription factors. Biochem. Pharmacol. 59, 1-6
3. Seth, D., Hausladen, A., Wang, Y.-J., and Stamler, J. S. (2012) Endogenous protein S-nitrosylation in E. coli: regulation by OxyR. Science 336, 470-473
4. Antelmann, H., and Helmann, J. D. (2011) Thiol-based redox switches and gene regulation. Antioxid. Redox Signal. 14, 1049-1063
5. Brandes, N., Schmitt, S., and Jakob, U. (2009) Thiol-based redox switches in eukaryotic proteins. Antioxid. Redox Signal. 11, 997-1014
6. Burgoyne, J. R., Madhani, M., Cuello, F., Charles, R. L., Brennan, J. P., Schröder, E., Browning, D. D., and Eaton, P. (2007) Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science 317, 1393-1397
7. Jakob, U., Muse, W., Eser, M., and Bardwell, J. C. (1999) Chaperone activity with a redox switch. Cell 96, 341-352
8. Leichert, L. I., Gehrke, F., Gudiseva, H. V., Blackwell, T., Ilbert, M., Walker, A. K., Strahler, J. R., Andrews, P. C., and Jakob, U. (2008) Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc. Natl. Acad. Sci. U.S.A. 105, 8197-8202
9. Brandes, N., Rinck, A., Leichert, L. I., and Jakob, U. (2007) Nitrosative stress treatment of E. coli targets distinct set of thiol-containing proteins. Mol. Microbiol. 66, 901-914
10. Wood, P. M. (1988) The potential diagram for oxygen at pH 7. Biochem. J. 253, 287-289
11. Ischiropoulos, H., Zhu, L., and Beckman, J. S. (1992) Peroxynitrite formation from macrophage-derived nitric oxide. Arch. Biochem. Biophys. 298, 446-451
12. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A. (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U.S.A. 87, 1620-1624
13. Alvarez, B., and Radi, R. (2003) Peroxynitrite reactivity with amino acids and proteins. Amino Acids 25, 295-311
14. McLean, S., Bowman, L. A., Sanguinetti, G., Read, R. C., and Poole, R. K. (2010) Peroxynitrite toxicity in Escherichia coli K12 elicits expression of oxidative stress responses and protein nitration and nitrosylation. J. Biol. Chem. 285, 20724-20731
15. Lambrecht, J. A., Flynn, J. M., and Downs, D. M. (2012) Conserved YjgF protein family deaminates reactive enamine/imine intermediates of pyridoxal 5-phosphate (PLP)-dependent enzyme reactions. J. Biol. Chem. 287, 3454-3461
16. Neidhardt, F. C., Bloch, P. L., and Smith, D. F. (1974) Culture medium for enterobacteria. J. Bacteriol. 119, 736-747
17. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L., and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006.0008
18. Sternberg, N. L., and Maurer, R. (1991) Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol. 204, 18-43
19. Lindemann, C., and Leichert, L. I. (2012) Quantitative redox proteomics: the NOxICAT method. Methods Mol. Biol. 893, 387-403
20. Gygi, S. P., Rist, B., Gerber, S. A., Turecek, F., Gelb, M. H., and Aebersold, R. (1999) Quantitative analysis of complex protein mixtures using isotopecoded affinity tags. Nat. Biotechnol. 17, 994-999
21. Zhou, J., and Rudd, K. E. (2013) EcoGene 3.0. Nucleic Acids Res. 41, D613-D624
22. Mortensen, P., Gouw, J. W., Olsen, J. V., Ong, S.-E., Rigbolt, K. T., Bunkenborg, J., Cox, J., Foster, L. J., Heck, A. J., Blagoev, B., Andersen, J. S., and Mann, M. (2010) MSQuant, an Open Source Platform for Mass Spectrometry-Based Quantitative Proteomics. J. Proteome Res. 9, 393-403
23. Wilkins, M. R., Gasteiger, E., Bairoch, A., Sanchez, J. C., Williams, K. L., Appel, R. D., and Hochstrasser, D. F. (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol. Biol. 112, 531-552
24. Creighton, T. E. (1990) in Protein Structure, A Practical Approach (Creighton, T. E., ed) 1st Ed. pp. 155-166, IRL Press at Oxford University Press, Oxford
25. Wong, C., Sridhara, S., Bardwell, J. C., and Jakob, U. (2000) Heating greatly speeds Coomassie Blue staining and destaining. BioTechniques 28, 426-428
26. Ischiropoulos, H., Zhu, L., Chen, J., Tsai, M., Martin, J. C., Smith, C. D., and Beckman, J. S. (1992) Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 298, 431-437
27. Goldstein, S., Lind, J., and Merényi, G. (2005) Chemistry of peroxynitrites as compared to peroxynitrates. Chem. Rev. 105, 2457-2470
28. Larsen, T. M., Boehlein, S. K., Schuster, S. M., Richards, N. G., Thoden, J. B., Holden, H. M., and Rayment, I. (1999) Three-dimensional structure of Escherichia coli asparagine synthetase B: Ashort journey from substrate to product. Biochemistry 38, 16146-16157
29. Boehlein, S. K., Richards, N. G., and Schuster, S. M. (1994) Glutamine-dependent nitrogen transfer in Escherichia coli asparagine synthetase B. Searching for the catalytic triad. J. Biol. Chem. 269, 7450-7457
30. Liu, L., Hausladen, A., Zeng, M., Que, L., Heitman, J., and Stamler, J. S. (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490-494
31. Lu, P., Vogel, C., Wang, R., Yao, X., and Marcotte, E. M. (2007) Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 25, 117-124
32. Marla, S. S., Lee, J., and Groves, J. T. (1997) Peroxynitrite rapidly permeates phospholipid membranes. Proc. Natl. Acad. Sci. U.S.A. 94, 14243-14248
33. Schmiedeknecht, G., Kerkhoff, C., Orsó, E., Stöhr, J., Aslanidis, C., Nagy, G. M., Knuechel, R., and Schmitz, G. (1996) Isolation and characterization of a 14.5-kDa trichloroacetic-acid-soluble translational inhibitor protein from human monocytes that is up-regulated upon cellular differentiation. Eur. J. Biochem. 242, 339-351
34. Melloni, E., Michetti, M., Salamino, F., and Pontremoli, S. (1998) Molecular and functional properties of a calpain activator protein specific for μ-isoforms. J. Biol. Chem. 273, 12827-12831
35. Morishita, R., Kawagoshi, A., Sawasaki, T., Madin, K., Ogasawara, T., Oka, T., and Endo, Y. (1999) Ribonuclease activity of rat liver perchloric acidsoluble protein, a potent inhibitor of protein synthesis. J. Biol. Chem. 274, 20688-20692
36. Farkas, A., Nardai, G., Csermely, P., Tompa, P., and Friedrich, P. (2004) DUK114, the Drosophila orthologue of bovine brain calpain activator protein, is a molecular chaperone. Biochem. J. 383, 165-170
37. Volz, K. (1999) A test case for structure-based functional assignment: the 1.2 Å crystal structure of the yjgF gene product from Escherichia coli. Protein Sci. 8, 2428-2437
38. Ferrer-Sueta, G., and Radi, R. (2009) Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem. Biol. 4, 161-177
39. Hurst, J. K., and Lymar, S. V. (1997) Toxicity of peroxynitrite and related reactive nitrogen species toward Escherichia coli. Chem. Res. Toxicol. 10, 802-810
40. Held, J. M., and Gibson, B. W. (2012) Regulatory control or oxidative damage? Proteomic approaches to interrogate the role of cysteine oxidation status in biological processes. Mol. Cell. Proteomics 11, R111.013037
41. Butterfield, D. A., and Dalle-Donne, I. (2012) Redox proteomics. Antioxid. Redox Signal. 17, 1487-1489
42. Leichert, L. I., and Müller, A. (2013) in Oxidative Stress and Redox Regulation (Jakob, U., and Reichmann, D., eds) pp. 157-186, Springer, Dordrecht
43. Conte, Lo, M., and Carroll, K. S. (2012) in Oxidative Stress and Redox Regulation (Jakob, U., and Reichmann, D., eds) pp. 1-42, Springer, Dordrecht, Heidelberg, New York, London
44. Singh, R., Lemire, J., Mailloux, R. J., and Appanna, V. D. (2008) A novel strategy involved anti-oxidative defense: The conversion of NADH into NADPH by a metabolic network. PLoS ONE 3, e2682
45. Ishihama, Y., Schmidt, T., Rappsilber, J., Mann, M., Hartl, F. U., Kerner, M. J., and Frishman, D. (2008) Protein abundance profiling of the Escherichia coli cytosol. BMC Genomics 9, 102
46. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Lu, F., Marchler, G. H., Mullokandov, M., Omelchenko, M. V., Robertson, C. L., Song, J. S., Thanki, N., Yamashita, R. A., Zhang, D., Zhang, N., Zheng, C., and Bryant, S. H. (2011) CDD: A Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229
47. Brandes, N., Reichmann, D., Tienson, H., Leichert, L. I., and Jakob, U. (2011) Using quantitative redox proteomics to dissect the yeast redoxome. J. Biol. Chem. 286, 41893-41903
48. Wang, H., Wang, S., Lu, Y., Alvarez, S., Hicks, L. M., Ge, X., and Xia, Y. (2012) Proteomic analysis of early-responsive redox-sensitive proteins in Arabidopsis. J. Proteome Res. 11, 412-424
49. Wolf, C., Hochgräfe, F., Kusch, H., Albrecht, D., Hecker, M., and Engelmann, S. (2008) Proteomic analysis of antioxidant strategies of Staphylococcus aureus: Diverse responses to different oxidants. Proteomics 8, 3139-3153