Comparative study of the physiological roles of three peroxidases (NADH peroxidase, Alkyl hydroperoxide reductase and Thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of Enterococcus faecalis

Molecular Microbiology

Volumn 66, Issue 5, 2007, Pages 1148-1163

  La Carbona, Stephanie ^a   Sauvageot, Nicolas ^a   Giard, Jean Christophe ^a   Benachour, Abdellah ^a   Posteraro, Brunella ^b   Auffray, Yanick ^a   Sanguinetti, Maurizio ^b   Hartke, Axel ^a  

^a UNIVERSITÉ DE CAEN   (France)

^b CATHOLIC UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYL HYDROPEROXIDE REDUCTASE; BACTERIAL PROTEIN; GALACTOSE; GLYCEROL; HYDROGEN PEROXIDE; LACTOSE; PEROXIDASE; PROTEIN AHP; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PEROXIDASE; RIBOSE; THIOL PEROXIDASE; UNCLASSIFIED DRUG;

AEROBIC BACTERIUM; ANTIOXIDANT ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL PROTECTION; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE MODEL; ENTEROCOCCUS FAECALIS; GENE DELETION; GROWTH DISORDER; MUTANT; NONHUMAN; OXIDATIVE STRESS; PERITONEUM MACROPHAGE; PERITONITIS; PHAGOCYTE; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULON;

AEROBIOSIS; ANIMALS; ANTI-BACTERIAL AGENTS; CELLS, CULTURED; COLONY COUNT, MICROBIAL; ENTEROCOCCUS FAECALIS; GENE DELETION; HYDROGEN PEROXIDE; MACROPHAGES, PERITONEAL; MICE; MICROBIAL VIABILITY; OXIDANTS; OXIDATIVE STRESS; PERITONITIS; PEROXIDASES; PEROXIREDOXINS; REGULON; SURVIVAL ANALYSIS; VIRULENCE;

ENTEROCOCCUS FAECALIS;

EID: 36148995456     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05987.x     Document Type: Article

References (51)

1. Aderem, A. Underhill, D.M. (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17 : 593 623.
2. Antelmann, H., Engelmann, S., Schmid, R. Hecker, M. (1996) General and oxidative stress responses in Bacillus subtilis: cloning, expression, and mutation of the alkyl hydroperoxide reductase operon. J Bacteriol 178 : 6571 6578.
3. Arnaud, M., Chastanet, A. Debarbouille, M. (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70 : 6887 6891.
4. Baker, L.M. Poole, L.B. (2003) Catalytic mechanism of thiol peroxidase from Escherichia coli. Sulfenic acid formation and overoxidation of essential CYS61. J Biol Chem 278 : 9203 9211.
5. Benachour, A., Auffray, Y. Hartke, A. (2007) Construction of plasmid vectors for screening replicons from Gram-positive bacteria and their use as shuttle cloning vectors. Curr Microbiol 54 : 342 347.
6. Bsat, N., Chen, L. Helmann, J.D. (1996) Mutation of the Bacillus subtilis alkyl hydroperoxide reductase (ahpCF) operon reveals compensatory interactions among hydrogen peroxide stress genes. J Bacteriol 178 : 6579 6586.
7. Cha, M.K., Kim, H.K. Kim, I.H. (1995) Thioredoxin-linked 'thiol peroxidase' from periplasmic space of Escherichia coli. J Biol Chem 270 : 28635 28641.
8. Cha, M.K., Kim, H.K. Kim, I.H. (1996) Mutation and mutagenesis of thiol peroxidase of Escherichia coli and a new type of thiol peroxidase family. J Bacteriol 178 : 5610 5614.
9. Cha, M.K., Kim, W.C., Lim, C.J., Kim, K. Kim, I.H. (2004) Escherichia coli periplasmic thiol peroxidase acts as lipid hydroperoxide peroxidase and the principal antioxidative function during anaerobic growth. J Biol Chem 279 : 8769 8778.
10. Christman, M.F., Morgan, R.W., Jacobson, F.S. Ames, B.N. (1985) Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41 : 753 762.
11. Claiborne, A., Ross, R.P. Parsonage, D. (1992) Flavin-linked peroxide reductases: protein-sulfenic acids and the oxidative stress response. Trends Biochem Sci 17 : 183 186.
12. Claiborne, A., Yeh, J.I., Mallett, T.C., Luba, J., Crane, E.J., et al. (1999) Protein-sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulation. Biochemistry 38 : 15407 15416.
13. Cosgrove, K., Coutts, G., Jonsson, I.-M., Tarkowski, A., Kokai-Kun, J.F., Mond, J.J. Foster, S.J. (2007) Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189 : 1025 1035.
14. 2 stress proteins. Lett Appl Microbiol 26 : 259 264.
15. Frankenberg, L., Brugna, M. Hederstedt, L. (2002) Enterococcus faecalis heme-dependent catalase. J Bacteriol 184 : 6351 6356.
16. Gentry-Weeks, C.R., Karkhoff-Schweizer, R., Pikis, A., Estay, M. Keith, J.M. (1999) Survival of Enterococcus faecalis in mouse peritoneal macrophages. Infect Immun 67 : 2160 2165.
17. Gilmore, M.S., Coburn, P.S., Nallapareddy, S.R. Murray, B.E. (2002) Enterococcal virulence. In The Enterococci: Pathogenesis, Molecular Biology, Antibiotic Resistance and Infection Control. Gilmore, M.S., Clewell, D.B., Courvalin, P.M., Dunny, G.M., Murray, B.E. Rice, L.B. (eds). Washington, DC : American Society for Microbiology Press, 301 354.
18. Gordon, J., Holman, R.A. McLeod, J.W. (1953) Further observations on the production of hydrogen peroxide by anaerobic bacteria. J Pathol Bacteriol 66 : 527 537.
19. Hassett, D.J. Cohen, M.S. (1989) Bacterial adaptation to oxidative stress: implications for pathogenesis and interaction with phagocytic cells. FASEB J 3 : 2574 2582.
20. Huycke, M.M., Moore, D., Joyce, W., Wise, P., Shepard, L., Kotake, Y. Gilmore, M.S. (2001) Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol Microbiol 42 : 729 740.
21. Huycke, M.M., Abrams, V. Moore, D.R. (2002) Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damage colonic epithelial cell DNA. Carcinogenesis 23 : 529 536.
22. Jacobs, N.J. Vandemark, P.J. (1960a) The purification and properties of the alpha-glycerophosphate-oxidizing enzyme of Streptococcus faecalis 10C1. Arch Biochem Biophys 88 : 250 255.
23. Jacobs, N.J. Vandemark, P.J. (1960b) Comparison of the mechanism of glycerol oxidation in aerobically and anaerobically grown Streptococcus faecalis. J Bacteriol 79 : 532 538.
24. Jacobson, F.S., Morgan, R.W., Christman, M.F. Ames, B.N. (1989) An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. J Biol Chem 264 : 1488 1496.
25. Kim, H.K., Kim, S.J., Lee, J.W., Lee, J.W., Cha, M.K. Kim, I.H. (1996) Identification of promoter in the 5′-flanking region of the Escherichia coli thioredoxin-linked thiol peroxidase gene: evidence for the existence of oxygen-related transcriptional regulatory protein. Biochem Biophys Res Commun 221 : 641 646.
26. Link, A.J., Robison, K. Church, G.M. (1997) Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12. Electrophoresis 18 : 1259 1313.
27. Monqkolsuk, S. Helmann, J.D. (2002) Regulation of inducible peroxide stress responses. Mol Microbiol 45 : 9 15.
28. Morgan, R.W., Christman, M.F., Jacobson, F.S., Storz, G. Ames, B.N. (1986) Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc Natl Acad Sci USA 83 : 8059 8063.
29. Nathan, C. Shiloh, M.U. (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 97 : 8841 8848.
30. Pai, S.R., Singh, K.V. Murray, B.E. (2003) In vivo efficacy of the ketolide ABT-773 (Cethromycin) against enterococci in a mouse peritonitis model. Antimicrobial Agents Chemother 47 : 2706 2709.
31. Pericone, C.D., Park, S., Imlay, J.A. Weiser, J.N. (2003) Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the Fenton reaction. J Bacteriol 185 : 6815 6825.
32. Poole, L.B. (2005) Bacterial defenses against oxidants: mechanistic features of cystein-based peroxidases and their flavoprotein reductases. Arch Biochem Biophys 433 : 240 254.
33. Pugh, S.Y. Knowles, C.J. (1982) Growth of Streptococcus faecalis var. zymogenes on glycerol: the effect of aerobic and anaerobic growth in the presence and absence of haematin on enzyme synthesis. J Gen Microbiol 128 : 1009 1017.
34. Reed, L.J. Muench, H. (1938) A simple method of estimating fifty percent endpoints. Am J Hyg 27 : 493 497.
35. Rho, B.S., Hung, L.W., Holton, J.M., Vigil, D., Kim, S.I., Park, M.S., et al. (2006) Functional and structural characterization of a thiol peroxidase from Mycobacterium tuberculosis. J Mol Biol 361 : 850 863.
36. Riboulet, E., Verneuil, N., La Carbona, S., Sauvageot, N., Auffray, Y., Hartke, A. Giard, J.-C. (2007) Relationships between oxidative stress response and virulence in Enterococcus faecalis. J Mol Microbiol Biotechnol 13 : 140 146.
37. Richards, M.J., Edwards, J.R., Culver, D.H. Gaynes, R.P. (2000) Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol 21 : 510 515.
38. Rosenkrands, I., King, A., Weldingh, K., Moniatte, M., Moertz, E. Andersen, P. (2000a) Towards the proteome of Mycobacterium tuberculosis. Electrophoresis 21 : 3740 3756.
39. Rosenkrands, I., Weldingh, K., Jacobsen, S., Hansen, C.V., Florio, W., Gianetri, I. Andersen, P. (2000b) Mapping and identification of Mycobacterium tuberculosis proteins by two-dimensional gel electrophoresis, microsequencing and immunodetection. Electrophoresis 21 : 935 948.
40. Ross, R.P. Claiborne, A. (1997) Evidence for regulation of the NADH peroxidase gene (npr) from Enterococcus faecalis by OxyR. FEMS Microbiol Lett 151 : 177 183.
41. 2O-forming NADH oxidase from Streptococcus faecalis. Eur J Biochem 156 : 149 155.
42. Seaver, L.C. Imlay, J.A. (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183 : 7173 7181.
43. Storz, G. Imlay, J.A. (1999) Oxidative stress. Curr Opin Microbiol 2 : 188 194.
44. Stuart, C.H., Schwartz, S.A., Beeson, T.J. Owatz, C.B. (2006) Enterococcus faecalis: its role in root canal treatment failure and current concepts in retreatment. J Endod 32 : 93 98.
45. Teng, F., Wang, L., Singh, K.V., Murray, B.E. Weinstock, G.M. (2002) Involvement of PhoP-PhoS homologs in Enterococcus faecalis virulence. Infect Immun 70 : 1991 1996.
46. Terzaghi, B.E. Sandine, W.E. (1975) Improved medium for lactic Streptococci and their bacteriophages. Appl Microbiol 29 : 807 813.
47. Verneuil, N., Sanguinetti, M., Le Breton, Y., Posteraro, B., Fadda, G., Auffray, Y., et al. (2004) Effects of the Enterococcus faecalis hypR gene encoding a new transcriptional regulator on oxidative stress response and intracellular survival within macrophages. Infect Immun 72 : 4424 4431.
48. Verneuil, N., Maze, A., Sanguinetti, M., Laplace, J.M., Benachour, A., Auffray, Y., et al. (2006) Implication of (Mn) superoxide dismutase of Enterococcus faecalis in oxidative stress responses and survival inside macrophages. Microbiology 152 : 2579 2589.
49. Weldingh, K., Rosenkrands, I., Jacobsen, S., Rasmussen, P.B., Elhay, M.J. Andersen, P. (1998) Two-dimensional electrophoresis for analysis of Mycobacterium tuberculosis culture filtrate and purification and characterization of six novel proteins. Infect Immun 66 : 3492 3500.
50. Wells, C.L., Jechorek, R.P. Erlandsen, S.L. (1990) Evidence for the translocation of Enterococcus faecalis across the mouse intestinal tract. J Infect Dis 162 : 82 90.
51. Yagi, Y. Clewell, D.B. (1980) Recombination-deficient mutant of Streptococcus faecalis. J Bacteriol 143 : 966 970.