Proteomics of the oxidative stress response induced by hydrogen peroxide and paraquat reveals a novel AhpC-like protein in Pseudomonas aeruginosa

Proteomics

Volumn 11, Issue 15, 2011, Pages 3056-3069

  Hare, Nathan J ^a   Scott, Nichollas E ^a   Shin, Eun Hye H ^a   Connolly, Angela M ^a   Larsen, Martin R ^b   Palmisano, Giuseppe ^b   Cordwell, Stuart J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Alkylhydroperoxide reductase C; Microbiology; Oxidative stress; PA3529; Pseudomonas aeruginosa

Indexed keywords

AHPC PROTEIN; ANTIOXIDANT; BACTERIAL PROTEIN; CATALASE; CYSTEINE; DIMER; DISULFIDE; HYDROGEN PEROXIDE; IRON; OXIDOREDUCTASE; PARAQUAT; PEROXIREDOXIN; PROTEIN FPTA; PROTEIN FPVA; PROTEIN PA0848; PROTEIN PA3450; PROTEIN PA3529; SIDEROPHORE; SULFONIC ACID DERIVATIVE; SUPEROXIDE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BIOSYNTHESIS; CONTROLLED STUDY; DIMERIZATION; DISULFIDE BOND; LIPID PEROXIDATION; MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEOMICS; PSEUDOMONAS AERUGINOSA; TWO DIMENSIONAL GEL ELECTROPHORESIS;

BACTERIAL PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HYDROGEN PEROXIDE; OXIDATIVE STRESS; PARAQUAT; PEROXIREDOXINS; PROTEOMICS; PSEUDOMONAS AERUGINOSA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 79960442941     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000807     Document Type: Article

References (45)

1. Stover, C. K., Pham, X. Q., Erwin, A. L., Mizoguchi, S. D. et al., Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 2000, 406, 959-964.
2. Hare, N. J., Cordwell, S. J., Proteomics of bacterial pathogens: Pseudomonas aeruginosa infections in cystic fibrosis - a case study. Proteomics Clin. Appl. 2010, 4, 1-21.
3. Bleves, S., Viarre, V., Salacha, R., Michel, G. P. et al., Protein secretion systems in Pseudomonas aeruginosa: a wealth of pathogenic weapons. Int. J. Med. Microbiol. 2010, 300, 534-543.
4. Lyczak, J. B., Cannon, C. L., Pier, G. B., Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2000, 2, 1051-1060.
5. Kerr, K. G., Snelling, A. M., Pseudomonas aeruginosa: a formidable and ever-present adversary. J. Hosp. Infect. 2009, 73, 338-344.
6. Strateva, T., Yordanov, D., Pseudomonas aeruginosa - a phenomenon of bacterial resistance. J. Med. Microbiol. 2009, 58, 1133-1148.
7. Lyczak, J. B., Cannon, C. L., Pier, G. B., Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 2002, 15, 194-222.
8. Rommens, J. M., Iannuzzi, M. C., Kerem, B., Drumm, M. L. et al., Identification of the cystic fibrosis gene: chromosome walking and jumping. Science 1989, 245, 1059-1065.
9. Döring, G., Parameswaran, I. G., Murphy, T. F., Differential adaptation of microbial pathogens to airways of patients with cystic fibrosis and chronic obstructive pulmonary disease. FEMS Microbiol. Rev. 2011, 35, 124-146.
10. Miller, R. A., Britigan, B. E., Role of oxidants in microbial pathophysiology. Clin. Microbiol. Rev. 1997, 1, 1-18.
11. Hassett, D. J., Schweizer, H. P., Ohman, D. E., Pseudomonas aeruginosa sodA and sodB mutants defective in manganese- and iron-cofactored superoxide dismutase activity demonstrate the importance of the iron-cofactored form in aerobic metabolism. J. Bacteriol. 1995, 177, 6330-6337.
12. Heo, Y. J., Chung, I. Y., Cho, W. J., Lee, B. Y. et al., The major catalase gene (katA) of Pseudomonas aeruginosa PA14 is under both positive and negative control of the global transactivator OxyR in response to hydrogen peroxide. J. Bacteriol. 2010, 192, 381-390.
13. Brown, S. M., Howell, M. L., Vasil, M. L., Anderson, A. J., Hassett, D. J., Cloning and characterization of the katB gene of Pseudomonas aeruginosa encoding a hydrogen peroxide-inducible catalase: purification of KatB, cellular localization, and demonstration that it is essential for optimal resistance to hydrogen peroxide. J. Bacteriol. 1995, 177, 6536-6544.
14. Ochsner, U. A., Vasil, M. L., Alsabbagh, E., Parvatiyar, K., Hassett, D. J., Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB-ankB, ahpB and ahpC-ahpF. J. Bacteriol. 2000, 182, 4533-4544.
15. Palma, M., DeLuca, D., Worgall, S., Quadri, L. E. N., Transcriptome analysis of the response of Pseudomonas aeruginosa to hydrogen peroxide. J. Bacteriol. 2004, 186, 248-252.
16. Christman, M. F., Storz, G., Ames, B. N., OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc. Natl. Acad. Sci. USA 1989, 86, 3484-3488.
17. Wu, J., Weiss, B., Two divergently transcribed genes, soxR and soxS, control a superoxide response regulon of Escherichia coli. J. Bacteriol. 1991, 173, 2864-2871.
18. Palma, M., Zurita, J., Ferreras, J. A., Worgall, S. et al., Pseudomonas aeruginosa SoxR does not conform to the archetypal paradigm for SoxR-dependent regulation of the bacterial oxidative stress response. Infect. Immun. 2005, 73, 2958-2966.
19. Hall, A., Karplus, P. A., Poole, L. B., Typical 2-Cys peroxiredoxins - structures, mechanisms and functions. FEBS J. 2009, 276, 2469-2477.
20. Poole, L. B., Bacterial defences against oxidants: mechanistic features of cysteine-based peroxidises and their flavoprotein reductases. Arch. Biochem. Biophys. 2005, 433, 240-254.
21. Wagner, E., Luche, S., Penna, L., Chevallet, M. et al., A method for detection of overoxidation of cysteines: peroxiredoxins are oxidized in vivo at the active-site cysteine during oxidative stress. Biochem. J. 2002, 366, 777-785.
22. Chevallet, M., Wagner, E., Luche, S., van Dorsselaer, A. et al., Regeneration of peroxiredoxins during recovery after oxidative stress. J. Biol. Chem. 2003, 278, 37146-37153.
23. Chang, W., Small, D. A., Toghrol, F., Bentley, W. E., Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide. Biomed. Chromatogr. Genomics 2005, 6, 115.
24. Salunkhe, P., Topfer, T., Buer, J., Tümmler, B., Genome-wide transcriptional profiling of the steady-state response of Pseudomonas aeruginosa to hydrogen peroxide. J. Bacteriol. 2005, 187, 2565-2572.
25. Salunkhe, P., von Götz, F., Wiehlmann, L., Lauber, J., Buer, J., Tümmler, B., GeneChip expression analysis of the response of Pseudomonas aeruginosa to paraquat-induced superoxide stress. Genome Lett. 2002, 1, 165-174.
26. Gorman, J. J., Wallis, T. P., Pitt, J. J., Protein disulfide bond determination by mass spectrometry. Mass Spectrom. Rev. 2002, 21, 183-216.
27. Nouwens, A. S., Willcox, M. D. P., Walsh, B. J., Cordwell, S. J., Proteomic comparison of membrane and extracellular proteins from invasive (PAO1) and cytotoxic (6206) strains of Pseudomonas aeruginosa. Proteomics 2002, 2, 1325-1346.
28. Cordwell, S. J., Len, A. C., Touma, R. G., Scott, N. E. et al., Identification of membrane-associated proteins from Campylobacter jejuni strains using complementary proteomics technologies. Proteomics 2008, 8, 122-139.
29. Chen, Y., Zhang, J., Xing, G., Zhao, Y., MASCOT-derived false positive peptide identifications revealed by manual analysis of tandem mass spectra. J. Proteome Res. 2009, 8, 3141-3147.
30. Jeong, J., Jung, Y., Na, S., Jeong, J. et al., Novel oxidative modifications in redox-active cysteine residues. Mol. Cell. Proteomics 2011, 10, M110.000513.
31. Saito, K., Yasuo, I., Uchimura, H., Koide-Yoshida, S. et al., Verification of protein disulfide bond arrangement by in-gel tryptic digestion under entirely neutral pH conditions. Proteomics 2010, 10, 1-5.
32. Mathee, K., Ciofu, O., Sternberg, C., Lindum, P. W. et al., Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 1999, 145, 1349-1357.
33. Bjarnsholt, T., Jensen, P. Ø., Burmølle, M., Hentzer, H. et al., Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 2005, 151, 373-383.
34. Elkins, J. G., Hassett, D. J., Stewart, P. S., Schweizer, H. P., McDermott, T. R., Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide. Appl. Environ. Microbiol. 1999, 65, 4594-4600.
35. Schwarzer, C., Fischer, H., Kim, E. J., Barber, K. J. et al., Oxidative stress caused by pyocyanin impairs CFTR Cl-transport in human bronchial epithelial cells. Free Radic. Biol. Med. 2008, 45, 1653-1662.
36. Vinckx, T., Matthijs, S., Cornelis, P., Loss of the oxidative stress regulator OxyR in Pseudomonas aeruginosa PAO1 impairs growth under iron-limited conditions. FEMS Microbiol. Lett. 2008, 288, 258-265.
37. Reid, D. W., Anderson, G. J., Lamont, I. L., Role of lung iron in determining the bacterial and host struggle in cystic fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297, L795-L802.
38. Ankenbauer, R. G., Quan, H. N., FptA, the Fe(III)-pyochelin receptor of Pseudomonas aeruginosa: a phenolate siderophore receptor homologous to hydroxamate siderophore receptors. J. Bacteriol. 1994, 176, 307-319.
39. Schalk, I. J., Lamont, I. L., Cobessi, D., Structure - function relationships in the bifunctional ferrisiderophore FpvA receptor from Pseudomonas aeruginosa. Biometals 2009, 22, 671-678.
40. Ochsner, U. A., Johnson, Z., Vasil, A. I., Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiology 2000, 146, 185-198.
41. Ratliff, M., Zhu, W., Deshmukh, R., Wilks, A., Stojiljkovic, I., Homologues of neisserial heme oxygenase in Gram-negative bacteria: degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa. J. Bacteriol. 2001, 183, 6394-6403.
42. + reductase and not ferredoxin is the redox partner of heme oxygenase under iron-starvation conditions. Biochemistry 2007, 46, 12198-12211.
43. Ochsner, U. A., Wilderman, P. J., Vasil, A. I., Vasil, M. L., GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol. Microbiol. 2002, 45, 1277-1287.
44. Weber, H., Engelmann, S., Becher, D., Hecker, M., Oxidative stress triggers thiol oxidation in the glyceraldehyde-3-phosphate dehydrogenase of Staphylococcus aureus. Mol. Microbiol. 2004, 52, 133-140.
45. Hall, A., Nelson, K., Poole, L., Karplus, P. A., Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid. Redox. Signal. 2011, Apr 20 Epub.