Gene expression and physiological role of Pseudomonas aeruginosa methionine sulfoxide reductases during oxidative stress

Journal of Bacteriology

Volumn 195, Issue 15, 2013, Pages 3299-3308

  Romsang, Adisak ^a   Atichartpongkul, Sopapan ^b   Trinachartvanit, Wachareeporn ^a   Vattanaviboon, Paiboon ^b,c   Mongkolsuk, Skorn ^a,b,c  

^a Mahidol University   (Thailand)

^b Chulabhorn Research Institute   (Thailand)

^c Center of Excellence on Environmental Health   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

METHIONINE SULFOXIDE REDUCTASE A; METHIONINE SULFOXIDE REDUCTASE B; PARAQUAT;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL MUTATION; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CONTROLLED STUDY; CORRELATION ANALYSIS; DROSOPHILA MELANOGASTER; ESSENTIAL GENE; GENE EXPRESSION; GENETIC ORGANIZATION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA;

ANIMALS; DROSOPHILA MELANOGASTER; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; METHIONINE SULFOXIDE REDUCTASES; MICROBIAL VIABILITY; OXIDANTS; OXIDATIVE STRESS; PARAQUAT; PSEUDOMONAS AERUGINOSA; SODIUM HYPOCHLORITE; STRESS, PHYSIOLOGICAL; SURVIVAL ANALYSIS; VIRULENCE; VIRULENCE FACTORS;

EID: 84880651815     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00167-13     Document Type: Article

References (60)

1. Grundmann H, Kropec A, Hartung D, Berner R, Daschner F. 1993. Pseudomonas aeruginosa in a neonatal intensive care unit: reservoirs and ecology of the nosocomial pathogen. J. Infect. Dis. 168:943-947.
2. Hassett DJ, Schweizer HP, Ohman DE. 1995. Pseudomonas aeruginosa sodA and sodB mutants defective in manganese-and iron-cofactored superoxide dismutase activity demonstrate the importance of the ironcofactored form in aerobic metabolism. J. Bacteriol. 177:6330-6337.
3. Baysse C, De Vos D, Naudet Y, Vandermonde A, Ochsner U, Meyer JM, Budzikiewicz H, Schafer M, Fuchs R, Cornelis P. 2000. Vanadium interferes with siderophore-mediated iron uptake in Pseudomonas aeruginosa. Microbiology 146:2425-2434.
4. An BC, Lee SS, Lee EM, Lee JT, Wi SG, Jung HS, Park W, Chung BY. 2010. A new antioxidant with dual functions as a peroxidase and chaperone in Pseudomonas aeruginosa. Mol. Cells 29:145-151.
5. Ochsner UA, Hassett DJ, Vasil ML. 2001. Genetic and physiological characterization of ohr, encoding a protein involved in organic hydroperoxide resistance in Pseudomonas aeruginosa. J. Bacteriol. 183:773-778.
6. Somprasong N, Jittawuttipoka T, Duang-Nkern J, Romsang A, Chaiyen P, Schweizer HP, Vattanaviboon P, Mongkolsuk S. 2012. Pseudomonas aeruginosa thiol peroxidase protects against hydrogen peroxide toxicity and displays atypical patterns of gene regulation. J. Bacteriol. 194:3904-3912.
7. Ochsner UA, Vasil ML, Alsabbagh E, Parvatiyar K, Hassett DJ. 2000. Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense andDNArepair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF. J. Bacteriol. 182:4533-4544.
8. Moskovitz J, Poston JM, Berlett BS, Nosworthy NJ, Szczepanowski R, Stadtman ER. 2000. Identification and characterization of a putative active site for peptide methionine sulfoxide reductase (MsrA) and its substrate stereospecificity. J. Biol. Chem. 275:14167-14172.
9. Grimaud R, Ezraty B, Mitchell JK, Lafitte D, Briand C, Derrick PJ, Barras F. 2001. Repair of oxidized proteins. Identification of a new methionine sulfoxide reductase. J. Biol. Chem. 276:48915-48920.
10. Boschi-Muller S, Gand A, Branlant G. 2008. The methionine sulfoxide reductases: catalysis and substrate specificities. Arch. Biochem. Biophys. 474:266-273.
11. Moskovitz J, Weissbach H, Brot N. 1996. Cloning the expression of a mammalian gene involved in the reduction of methionine sulfoxide residues in proteins. Proc. Natl. Acad. Sci. U. S. A. 93:2095-2099.
12. Rodrigo MJ, Moskovitz J, Salamini F, Bartels D. 2002. Reverse genetic approaches in plants and yeast suggest a role for novel, evolutionarily conserved, selenoprotein-related genes in oxidative stress defense. Mol. Genet. Genomics 267:613-621.
13. Kryukov GV, Kumar RA, Koc A, Sun Z, Gladyshev VN. 2002. Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proc. Natl. Acad. Sci. U. S. A. 99:4245-4250.
14. Wizemann TM, Moskovitz J, Pearce BJ, Cundell D, Arvidson CG, So M, Weissbach H, Brot N, Masure HR. 1996. Peptide methionine sulfoxide reductase contributes to the maintenance of adhesins in three major pathogens. Proc. Natl. Acad. Sci. U. S. A. 93:7985-7990.
15. Ezraty B, Aussel L, Barras F. 2005. Methionine sulfoxide reductases in prokaryotes. Biochim. Biophys. Acta 1703:221-229
16. Hassouni ME, Chambost JP, Expert D, Van Gijsegem F, Barras F. 1999. The minimal gene set member msrA, encoding peptide methionine sulfoxide reductase, is a virulence determinant of the plant pathogen Erwinia chrysanthemi. Proc. Natl. Acad. Sci. U. S. A. 96:887-892.
17. Singh VK, Moskovitz J. 2003. Multiple methionine sulfoxide reductase genes in Staphylococcus aureus: expression of activity and roles in tolerance of oxidative stress. Microbiology 149:2739-2747.
18. Douglas T, Daniel DS, Parida BK, Jagannath C, Dhandayuthapani S. 2004. Methionine sulfoxide reductase A (MsrA) deficiency affects the survival of Mycobacterium smegmatis within macrophages. J. Bacteriol. 186: 3590-3598.
19. Dhandayuthapani S, Blaylock MW, Bebear CM, Rasmussen WG, Baseman JB. 2001. Peptide methionine sulfoxide reductase (MsrA) is a virulence determinant in Mycoplasma genitalium. J. Bacteriol. 183:5645-5650.
20. Rosen H, Klebanoff SJ, Wang Y, Brot N, Heinecke JW, Fu X. 2009. Methionine oxidation contributes to bacterial killing by the myeloperoxidase system of neutrophils. Proc. Natl. Acad. Sci. U. S. A. 106:18686-18691.
21. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Choi KH, Schweizer HP. 2006. Mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat. Protoc. 1:153-161.
23. Buranajitpakorn S, Piwkam A, Charoenlap N, Vattanaviboon P, Mongkolsuk S. 2011. Genes for hydrogen peroxide detoxification and adaptation contribute to protection against heat shock in Xanthomonas campestris pv. campestris. FEMS Microbiol. Lett. 317:60-66.
24. Alexeyev MF. 1999. The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of gram-negative bacteria. Biotechniques 26:824-826, 828.
25. Marx CJ, Lidstrom ME. 2002. Broad-host-range cre-lox system for antibiotic marker recycling in gram-negative bacteria. Biotechniques 33: 1062-1067.
26. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, II, Peterson KM. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
27. DeFeyter R, Kado CI, Gabriel DW. 1990. Small, stable shuttle vectors for use in Xanthomonas. Gene 88:65-72.
28. Prapagdee B, Vattanaviboon P, Mongkolsuk S. 2004. The role of a bifunctional catalase-peroxidase KatA in protection of Agrobacterium tumefaciens from menadione toxicity. FEMS Microbiol. Lett. 232:217-223.
29. McCord JM, Fridovich I. 1969. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244:6049-6055.
30. D'Argenio DA, Gallagher LA, Berg CA, Manoil C. 2001. Drosophila as a model host for Pseudomonas aeruginosa infection. J. Bacteriol. 183:1466-1471.
31. Apidianakis Y, Rahme LG. 2009. Drosophila melanogaster as a model host for studying Pseudomonas aeruginosa infection. Nat. Protoc. 4:1285-1294.
32. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock RE, Lory S, Olson MV. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959-964.
33. Moskovitz J, Rahman MA, Strassman J, Yancey SO, Kushner SR, Brot N, Weissbach H. 1995. Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage. J. Bacteriol. 177:502-507.
34. Lowther WT, Brot N, Weissbach H, Matthews BW. 2000. Structure and mechanism of peptide methionine sulfoxide reductase, an 'antioxidation' enzyme. Biochemistry 39:13307-13312.
35. Kim HY, Gladyshev VN. 2005. Role of structural and functional elements of mouse methionine-S-sulfoxide reductase in its subcellular distribution. Biochemistry 44:8059-8067.
36. Ranaivoson FM, Neiers F, Kauffmann B, Boschi-Muller S, Branlant G, Favier F. 2009. Methionine sulfoxide reductase B displays a high level of flexibility. J. Mol. Biol. 394:83-93.
37. Moskovitz J, Singh VK, Requena J, Wilkinson BJ, Jayaswal RK, Stadtman ER. 2002. Purification and characterization of methionine sulfoxide reductases from mouse and Staphylococcus aureus and their substrate stereospecificity. Biochem. Biophys. Res. Commun. 290:62-65.
38. Lan L, Murray TS, Kazmierczak BI, He C. 2010. Pseudomonas aeruginosa OspR is an oxidative stress sensing regulator that affects pigment production, antibiotic resistance and dissemination during infection. Mol. Microbiol. 75:76-91.
39. Lee WL, Gold B, Darby C, Brot N, Jiang X, de Carvalho LP, Wellner D, St John G, Jacobs WR, Jr, Nathan C. 2009. Mycobacterium tuberculosis expresses methionine sulphoxide reductases A and B that protect from killing by nitrite and hypochlorite. Mol. Microbiol. 71:583-593.
40. Singh VK, Moskovitz J, Wilkinson BJ, Jayaswal RK. 2001. Molecular characterization of a chromosomal locus in Staphylococcus aureus that contributes to oxidative defence and is highly induced by the cell-wallactiveantibiotic oxacillin. Microbiology 147:3037-3045.
41. Vattanaviboon P, Seeanukun C, Whangsuk W, Utamapongchai S, Mongkolsuk S. 2005. Important role for methionine sulfoxide reductase in the oxidative stress response of Xanthomonas campestris pv. phaseoli. J. Bacteriol. 187:5831-5836.
42. Gebendorfer KM, Drazic A, Le Y, Gundlach J, Bepperling A, Kastenmuller A, Ganzinger KA, Braun N, Franzmann TM, Winter J. 2012. Identification of a hypochlorite-specific transcription factor from Escherichia coli. J. Biol. Chem. 287:6892-6903.
43. Alvarez-Martinez CE, Baldini RL, Gomes SL. 2006. A Caulobacter crescentus extracytoplasmic function sigma factor mediating the response to oxidative stress in stationary phase. J. Bacteriol. 188:1835-1846.
44. Huis in't Veld RA, Willemsen AM, van Kampen AH, Bradley EJ, Baas F, Pannekoek Y, van der Ende A. 2011. Deep sequencing whole transcriptome exploration of the ΣE regulon in Neisseria meningitidis. PLoS One 6:e29002. doi:10.1371/journal.pone.0029002.
45. Alamuri P, Maier RJ. 2006. Methionine sulfoxide reductase in Helicobacter pylori: interaction with methionine-rich proteins and stress-induced expression. J. Bacteriol. 188:5839-5850.
46. Kwak GH, Hwang KY, Kim HY. 2012. Analyses of methionine sulfoxide reductase activities towards free and peptidyl methionine sulfoxides. Arch. Biochem. Biophys. 527:1-5.
47. Assinger A, Koller F, Schmid W, Zellner M, Koller E, Volf I. 2010. Hypochlorite-oxidized LDL induces intraplatelet ROS formation and surface exposure of CD40L-a prominent role of CD36. Atherosclerosis 213: 129-134.
48. Dukan S, Touati D. 1996. Hypochlorous acid stress in Escherichia coli: resistance, DNA damage, and comparison with hydrogen peroxide stress. J. Bacteriol. 178:6145-6150.
49. Chesney JA, Eaton JW, Mahoney JR Jr. 1996. Bacterial glutathione: a sacrificial defense against chlorine compounds. J. Bacteriol. 178:2131-2135
50. Small DA, Chang W, Toghrol F, Bentley WE. 2007. Toxicogenomic analysis of sodium hypochlorite antimicrobial mechanisms in Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol. 74:176-185.
51. Rutala WA. 1996. APIC guideline for selection and use of disinfectants. 1994, 1995, and 1996 APIC Guidelines Committee. Association for Professionals in Infection Control and Epidemiology, Inc. Am. J. Infect. Control 24:313-342.
52. Le HT, Chaffotte AF, Demey-Thomas E, Vinh J, Friguet B, Mary J. 2009. Impact of hydrogen peroxide on the activity, structure, and conformational stability of the oxidized protein repair enzyme methionine sulfoxide reductase A. J. Mol. Biol. 393:58-66.
53. Atack JM, Kelly DJ. 2008. Contribution of the stereospecific methionine sulphoxide reductases MsrA and MsrB to oxidative and nitrosative stress resistance in the food-borne pathogen Campylobacter jejuni. Microbiology 154:2219-2230.
54. Bobrowski K, Hug GL, Pogocki D, Marciniak B, Schoneich C. 2007. Stabilization of sulfide radical cations through complexation with the peptide bond: mechanisms relevant to oxidation of proteins containing multiple methionine residues. J. Phys. Chem. B. 111:9608-9620.
55. Gu M, Imlay JA. 2011. The SoxRS response of Escherichia coli is directly activated by redox-cycling drugs rather than by superoxide. Mol. Microbiol. 79:1136-1150.
56. Tao L, Jackson RE, Cheng Q. 2005. Directed evolution of copy number of a broad host range plasmid for metabolic engineering. Metab. Eng. 7:10-17.
57. Lim JC, You Z, Kim G, Levine RL. 2011. Methionine sulfoxide reductase A is a stereospecific methionine oxidase. Proc. Natl. Acad. Sci. U. S. A. 108:10472-10477.
58. Denkel LA, Horst SA, Rouf SF, Kitowski V, Bohm OM, Rhen M, Jager T, Bange FC. 2011. Methionine sulfoxide reductases are essential for virulence of Salmonella Typhimurium. PLoS One 6:e26974. doi:10.1371/journal.pone.0026974.
59. Zhao C, Hartke A, La Sorda M, Posteraro B, Laplace JM, Auffray Y, Sanguinetti M. 2010. Role of methionine sulfoxide reductases A and B of Enterococcus faecalis in oxidative stress and virulence. Infect. Immun. 78: 3889-3897.
60. Metcalf WW, Jiang W, Daniels LL, Kim SK, Haldimann A, Wanner BL. 1996. Conditionally replicative and conjugative plasmids carrying lacZα for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35: 1-13.