Methionine oxidation contributes to bacterial killing by the myeloperoxidase system of neutrophils

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 44, 2009, Pages 18686-18691

  Rosen, Henry ^a   Klebanoff, Seymour J ^a   Wang, Yi ^b   Brot, Nathan ^c,d   Heinecke, Jay W ^a   Fu, Xiaoyun ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b PUGET SOUND BLOOD CENTER   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

Bactericidal; Microbicidal

Indexed keywords

BACTERIAL PROTEIN; CHLORIDE; ENVELOPE PROTEIN; HYDROGEN PEROXIDE; MEMBRANE PROTEIN; METHIONINE; METHIONINE SULFOXIDE; METHIONINE SULFOXIDE REDUCTASE A; MYELOPEROXIDASE;

ARTICLE; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ESCHERICHIA COLI; LIQUID CHROMATOGRAPHY; NEUTROPHIL; NONHUMAN; OXIDATION; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TANDEM MASS SPECTROMETRY;

BACTERIAL PROTEINS; CELL MEMBRANE; CYTOPLASM; ESCHERICHIA COLI; HUMANS; HYDROGEN PEROXIDE; HYPOCHLOROUS ACID; METHIONINE; METHIONINE SULFOXIDE REDUCTASES; MICROBIAL VIABILITY; NEUTROPHILS; OXIDATION-REDUCTION; OXIDOREDUCTASES; PEROXIDASE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 73249129955     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0909464106     Document Type: Article

References (36)

1. NauseefWM(2007) How human neutrophils kill and degrade microbes: An integrated view. Immunol Rev 219:88-102.
2. Klebanoff SJ (2005) Myeloperoxidase: Friend and foe. J Leukoc Biol 77:598-625.
3. Klebanoff SJ, Clark RA (1978) The Neutrophil (North-Holland Publishing, Amsterdam).
4. Harrison JE, Schultz J (1976) Studies on the chlorinating activity of myeloperoxidase. J Biol Chem 251:1371-1374.
5. Chapman AL, Hampton MB, Senthilmohan R, Winterbourn CC, Kettle AJ (2002) Chlorination of bacterial and neutrophil proteins during phagocytosis and killing of Staphylococcus aureus. J Biol Chem 277:9757-9762.
6. Rosen H, Crowley JR, HeineckeJW(2002)Humanneutrophils use the myeloperoxidasehydrogen peroxide-chloride system to chlorinate but not nitrate bacterial proteins during phagocytosis. J Biol Chem 277:30463-30468.
7. Camper AK, McFeters GA (1979) Chlorine injury and the enumeration of waterborne coliform bacteria. Appl Environ Microbiol 37:633-641.
8. Hurst JK, Barrette WC, Jr (1989) Leukocytic oxygen activation and microbicidal oxidative toxins. CRC Crit Rev Biochem Mol Biol 24:271-328.
9. Klebanoff SJ (1967) Iodination of bacteria: A bactericidal mechanism. J Exp Med 126:1063-1078.
10. Klebanoff SJ, White LR (1969) Iodination defect in the leukocytes of a patient with chronic granulomatous disease of childhood. N Engl J Med 280:460-466.
11. DomiganNM,Charlton TS, DuncanMW,Winterbourn CC, Kettle AJ (1995) Chlorination of tyrosyl residues in peptides by myeloperoxidase and human neutrophils. J Biol Chem 270:16542-16548.
12. Hazen SL, Hsu FF, Mueller DM, Crowley JR, Heinecke JW (1996) Human neutrophils employ chlorine gas as an oxidant during phagocytosis. J Clin Invest 98:1283-1289.
13. Winterbourn CC,HamptonMB(2008) Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45:549-561.
14. Pattison DI, Davies MJ (2006) Reactions of myeloperoxidase-derived oxidants with biological substrates: Gaining chemical insight intohumaninflammatory diseases. Curr Med Chem 13:3271-3290.
15. Rahman MA, Nelson H, Weissbach H, Brot N (1992) Cloning, sequencing, and expression of the Escherichia coli peptide methionine sulfoxide reductase gene. J Biol Chem 267:15549-15551.
16. Reeves EP, et al. (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416:291-297.
17. Reeves EP, Nagl M, Godovac-Zimmermann J, Segal AW (2003) Reassessment of the microbicidal activity of reactive oxygen species and hypochlorous acid with reference to the phagocytic vacuole of the neutrophil granulocyte. JMed Microbiol 52:643-651.
18. Bielski BH, Shiue GG (1978) Reaction rates of superoxide radicals with the essential amino acids. Ciba Found Symp 65:43-56.
19. Pan B, et al. (2006) Comparative oxidation studies of methionine residues reflect a structural effect on chemical kinetics in rhG-CSF. Biochemistry 45:15430-15443.
20. Pattison DI, Davies MJ (2001) Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds. Chem Res Toxicol 14:1453-1464.
21. Driessen AJ, Nouwen N (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77:643-667.
22. Bieker KL, Silhavy TJ (1990) PrlA (SecY) and PrlG (SecE) interact directly and function sequentially during protein translocation in E. coli. Cell 61:833-842.
23. Emr SD, Silhavy TJ (1980) Mutations affecting localization of an Escherichia coli outer membrane protein, the bacteriophage lambda receptor. J Mol Biol 141:63-90.
24. Silhavy TJ, Shuman HA, Beckwith J, Schwartz M (1977) Use of gene fusions to study outer membrane protein localization in Escherichia coli. Proc Natl Acad Sci USA 74:5411-5415.
25. Snyder WB, Silhavy TJ (1995) Beta-galactosidase is inactivated by intermolecular disulfide bonds and is toxic when secreted to the periplasm of Escherichia coli. J Bacteriol 177:953-963.
26. Barrette WC, Jr, Hannum DM, Wheeler WD, Hurst JK (1989) General mechanism for the bacterial toxicity of hypochlorous acid: Abolition of ATP production. Biochemistry 28:9172-9178.
27. Fu X, Mueller DM, Heinecke JW (2002) Generation of intramolecular and intermolecular sulfenamides, sulfinamides, and sulfonamides by hypochlorous acid: A potential pathway for oxidative cross-linking of low-density lipoprotein by myeloperoxidase. Biochemistry 41:1293-1301.
28. Bowers CW, Lau F, Silhavy TJ (2003) Secretion of LamB-LacZ by the signal recognition particle pathway of Escherichia coli. J Bacteriol 185:5697-5705. 29. Johnson JR, Clabots C, Rosen H (2006) Effect of inactivation of the global oxidative stress regulator oxyR on the colonization ability of Escherichia coli O1:K1:H7 in amouse model of ascending urinary tract infection. Infect Immun 74:461-468.
29. Welch RA, et al. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99:17020 - 17024.
30. Hickstein DD, et al. (1987) Isolation and characterization of the receptor on human neutrophils that mediates cellular adherence. J Biol Chem 262:5576-5580.
31. Rakita RM, Michel BR, Rosen H (1990) Differential inactivation of Escherichia coli membrane dehydrogenases by a myeloperoxidase-mediated antimicrobial system. Biochemistry 29:1075-1080.
32. Kooter IM, et al. (1999) The sulfonium ion linkage in myeloperoxidase. Direct spectro-scopic detection by isotopic labeling and effect of mutation. J Biol Chem 274:26794-26802.
33. Staudinger BJ, OberdoersterMA,Lewis PJ, RosenH(2002)mRNAexpression profiles for Escherichia coli ingested by normal and phagocyte oxidase-deficient human neutro-phils. J Clin Invest 110:1151-1163.
34. Decleva E, Menegazzi R, Busetto S, Patriarca P, Dri P (2006) Common methodology is inadequate for studies on the microbicidal activity of neutrophils. J Leukoc Biol 79:87-94.
35. Ingraham JL, Maaloe O, Neidhardt FC (1983) in Growth of the Bacterial Cell (Sinauer Associates, Sunderland, MA), pp 1-48.
36. Cox RA (2004) Quantitative relationships for specific growth rates and macromolecular compositions of Mycobacterium tuberculosis, Streptomyces coelicolor A3(2) and Escherichia coli B/r: An integrative theoretical approach. Microbiology 150:1413-1426.