MCLA-dependent chemiluminescence suggests that singlet oxygen plays a pivotal role in myeloperoxidase-catalysed bactericidal action in neutrophil phagosomes

Luminescence

Volumn 18, Issue 4, 2003, Pages 229-238

  Arisawa, Fumio ^a   Tatsuzawa, Hidetaka ^b   Kambayashi, Yasuhiro ^c   Kuwano, Hiroyuki ^a   Fujimori, Ken ^d   Nakano, Minoru ^c  

^a GUNMA UNIVERSITY   (Japan)

^b EBARA CORPORATION   (Japan)

^c JAPAN IMMUNORESEARCH LABORATORIES   (Japan)

^d UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Bactericidal action; Chemiluminescence probe; Hypochlorite; MCLA; Myeloperoxidase; Neutrophil; Phagocytosis; Phagosome; Singlet oxygen

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; CATALYSIS; CHEMILUMINESCENCE; CHLORINATION; ESCHERICHIA COLI; OXYGEN; PH;

BACTERICIDAL ACTION; CHEMILUMINESCENCE PROBE; MCLA; MYELOPEROXIDASE; NADPH OXIDASE; NEUTROPHILE; PHAGOCYTOSE; PHAGOSOMES; RESPIRATORY BURST; SINGLET OXYGEN;

CHLORINE COMPOUNDS;

AMINE; LUCIFERIN; MYELOPEROXIDASE; SINGLET OXYGEN; 2 METHYL 6 (4 METHOXYPHENYL) 3,7 DIHYDROIMIDAZO(1,2 ALPHA)PYRAZIN 3 ONE; 2-METHYL-6-(4-METHOXYPHENYL)-3,7-DIHYDROIMIDAZO(1,2-ALPHA)PYRAZIN-3-ONE; CHLORINE; HYPOCHLOROUS ACID; IMIDAZOLE DERIVATIVE; PEROXIDASE; PYRAZINE DERIVATIVE;

ARTICLE; BACTERICIDAL ACTIVITY; CATALYSIS; CHEMOLUMINESCENCE; CHLORINATION; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; NEUTROPHIL; PH MEASUREMENT; PHAGOCYTOSIS; PHAGOSOME; STAPHYLOCOCCUS AUREUS; BACTERIUM; CHEMISTRY; ENZYMOLOGY; IMMUNOLOGY; KINETICS; METABOLISM; PH; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); CYPRIDINA; CYPRIDINA LUCIFERIN; ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS;

BACTERIA; CATALYSIS; CHEMILUMINESCENT MEASUREMENTS; CHLORINE; HUMANS; HYDROGEN-ION CONCENTRATION; HYPOCHLOROUS ACID; IMIDAZOLES; KINETICS; NEUTROPHILS; PEROXIDASE; PHAGOCYTOSIS; PHAGOSOMES; PYRAZINES; SINGLET OXYGEN;

EID: 2442605692     PISSN: 15227235     EISSN: 10991271     Source Type: Journal    
DOI: 10.1002/bio.728     Document Type: Article

References (49)

1. Lehrer RI, Ganz T, Selsted WE, Babior BM, Curnutte JT. Neutrophils and host defense. Ann. Intern. Med. 1988; 109: 127-142.
2. Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 1998; 92: 3007-3017.
3. Aratani Y, Kura F, Watanabe H et al. Differential host susceptibility to pulmonary infections with bacteria and fungi in mice deficient in myeloperoxidase. J. Infect. Dis. 2000; 182: 1276-1279.
4. Aratani Y, Kura F, Watanabe H et al. Critical role of myeloperoxidase and nicotinamide adenine dinucleotide phosphate oxidase in high-burden systematic infection of mice with Candida albicans. J. Infect. Dis. 2002; 185: 1833-1837.
5. Klebanoff SJ. Myeloperoxidase-halide-hydrogen peroxide antibacterial system. J. Bacteriol. 1968; 95: 2131-2138.
6. Zgliczynski JM, Stelmaszynska T, Domanski J, Ostrowski W. Chloramines as intermediates of oxidation reaction of amino acids by myeloperoxidase. Biochim. Biophys. Acta 1971; 235: 419-424.
7. Stelmaszynska T, Zgliczynski JM. Myeloperoxidase of human neutrophilic granulocytes as chlorinating enzyme. Eur. J. Biochem. 1974; 45: 305-312.
8. Thomas EL, Grisham MB, Jefferson MM. Preparation and characterization of chloramines. Methods Enzymol. 1986; 132: 569-585.
9. Hazen SL, d'Avignon A, Anderson MM, Hsu FF, Heinecke JW. Human nuetophils employ the myeloperoxidase-hydrogen peroxide-chloride system to oxidaize α-amino acids to an family of reactive aldehydes. J. Biol. Chem. 1998; 273: 4997-5005.
10. Carr AC, Winterbourn CC. Oxidation of neutrophil glutathione and protein thiols by myeloperoxidase-derived hypochlorous acid. Biochem. J. 1997; 327: 275-281.
11. Rosen H, Crowley JR, Heinecke JW. Human neutrophils use the myeloperoxidase-hydrogen peroxide-chloride system to chlorinate but not nitrate bacterial proteins during phagocytosis. J. Biol. Chem. 2002; 277: 30463-30468.
12. Chapman ALP, Hampton MB, Senthilmohan R, Winterbourn CC, Kettle AJ. Chlorination of bacterial and neutrophil proteins during phagocytosis and killing of Staphylococcus aureus. J. Biol. Chem. 2002; 277: 9757-9762.
13. Bernofsky C. Nucleotide chloramines and neutrophil-mediated cytotoxicity. FASEB J. 1991; 5: 295-300.
14. Prutz WA. Interactions of hypochlorous acid with pyrimidine nucleotides, and secondary reactions of chlorinated pyrimidines with GSH, NADH, and other substrates. Arch. Biochem. Biophys. 1998; 349: 183-191.
15. Henderson JP, Byun J, Heinecke JW. Molecular chlorine generated by the myeloperoxidase-hydrogen peroxide-chloride system of phagocytes produces 5-chlorocytosine in bacterial RNA. J. Biol. Chem. 1999; 274: 33440-33448.
16. Masuda M, Suzuki T, Friesen MD et al. Chlorination of guanosine and other nucleosides by hypochlorous acid and myeloperoxidase of activated human neutrophils. Catalysis by nicotine and trimethylamine J. Biol. Chem. 2001; 276: 40486-40496.
17. Allen RC, Stjernholm RL, Steele RH. Evidence for the generation of an electronic excitation state(s) in human polymorphonuclear leukocytes and its participation in bactericidal activity. Biochem. Biophys. Res. Commun. 1972; 000: 679-684.
18. Krinsky NI. Singlet excited oxygen as a mediator of the antibacterial action of leukocytes. Science 1974; 186: 363-365.
19. Foote CS, Chang YC, Denny RW. Chemistry of singlet oxygen. X. Carotenoid quenching parallels biological protection. J. Am. Chem. Soc. 1970; 92: 5216-5218.
20. Tatsuzawa H, Maruyama T, Misawa N, Fujimori K, Nakano M. Quenching of singlet oxygen by carotenoid produced in Escherichia coli - attenuation of singlet oxygen-mediated bacterial killing by carotenoids. FEBS Lett. 2000; 484: 280-284.
21. Albrich JM, McCarthy CA, Hurst JK. Biological reactivity of hypochlorous acid: implications for bactericidal mechanisms of leukocyte myeloperoxidase. Proc. Natl Acad. Sci. USA 1981; 78: 210-214.
22. Steinbeck MJ, Khan AU, Karnovsky MJ. Intracellular singlet oxygen generation by phagocytosing neutrophils in response to particle coated with a chemical trap. J. Biol. Chem. 1992; 267: 13425-13433.
23. g) generator, 3-(4′-methyl-1′-naphthyl)-propionic acid, 1′,4′- endoperoxide (NEPO), for dioxygenation of squalene (a skin surface lipid) in an organic solvent and bacterial killing in aqueous medium. FEBS Lett. 1998; 432: 9-12.
24. Tatsuzawa H, Maruyama T, Misawa N et al. Inactivation of bacterial respiratory chain enzymes by singlet oxygen. FEBS Lett. 1998; 439: 329-333.
25. 2) Biochem. Biophys. Res. Commun. 1999; 262: 647-650.
26. Kanofsky JR, Wright J, Miles-Richardson GE, Tauber AI. Biochemical requirements for singlet oxygen production by purified human myeloperoxidase. J. Clin. Invest. 1984; 74: 1489-1495.
27. 2-chloride system. FEBS Lett. 1999; 443: 154-158.
28. Segal AW, Geisow M, Garcia R, Harper A, Miller R. The respiratory burst of phagocytic cells is associated with a rise in vacuolar pH. Nature 1981; 290: 406-409.
29. Kettle AJ, Winterbourn CC. Influence of superoxide on myeloperoxidase kinetics measured with a hydrogen peroxide electrode. Biochem. J. 1989; 263: 823-828.
30. Kettle AJ, Winterbourn CC. A kinetic analysis of the catalase activity of myeloperoxidase. Biochemistry 2001; 40: 10204-10212.
31. Kajiwara T, Kearns DR. Direct spectroscopic evidence for a deuterium solvent effect on the lifetime of singlet oxygen in water. J. Am. Chem. Soc. 1973; 95: 59865890.
32. Held AM, Halko DJ, Hurst JK. Mechanism of chlorine oxidation of hydrogen peroxide. J. Am. Chem. Soc. 1978; 100: 5732-5739.
33. Mashiko S, Suzuki N, Koga S et al. J. Biolumin. Chemilumin. 1991; 6: 69-72.
34. Akutsu K, Nakajima H, Katoh T, Kino S, Fujimori K, Chemiluminescence of Cypridina luciferin analogues. Part 2. Kinetic studies on the reaction of 2-methyl-6-phenylimidazo[1,2-α]pyrazin-3(7H)-one (CLA) with superoxide: hydroperoxyl radical is an actual active species used to initiate the reaction, J. Chem. Soc., Perkin Trans. 1995; 2: 1699-1706.
35. Ellerby LM, Cabelli DE, Graden JA, Valentine JS. Copper-zinc superoxide dismutase: why not pH-dependent? J. Am. Chem. Soc. 1996; 118: 6556-6561.
36. Glasoe PK, Long FA. Use of glass electrodes to measure acidities in deuterium oxide. J. Phys. Chem. 1960; 64: 188-191.
37. Morita Y, Iwamoto H, Aibara S, Kobayashi T, Hsegawa E. Crystallization and properties of myeloperoxidase from normal human leukocytes. J. Biochem. 1986; 99: 761-770.
38. Klebanoff SJ, Waethersdorph AM, Rosen H. Antimicrobial activity of myeloperoxidase. Methods Enzymol. 1984; 105: 399-403.
39. Nakano M. Determination of superoxide radical and singlet oxygen based on chemiluminescence of luciferin analogs. Methods Enzymol. 1990; 186: 585-591.
40. Fujimori K, Komiyama T, Tabata H et al. Chemiluminescence of Cypridina luciferin analogs. Part 3. MCLA chemiluminescence with singlet oxygen generated by the retro-Diels-Alder reaction of a naphthalene endoperoxide. Photochem. Photobiol. 1998; 68: 143-149.
41. 2 from phagocytosing human polymorphonuclear leukocytes. Blood 1982; 60: 446-453.
42. Jensen MS, Bainton DF. Temporal changees in pH within thephagocytic vacuole of the polymorphonuclear neutrophilic leukocyte. J. Cell Biol. 1973; 56: 379-388.
43. Cech P, Lehler I. Phogosomal pH of human neutrophils. Blood 1984; 63: 88-95.
44. Bassoe CF, Bjerkness R. Phagocytosis by human leukocytes, phagosomal pH and degradation of seven species of bacteria measured by flow cytometry. J. Med. Microbiol. 1985; 19: 115-125.
45. Furtmuller PG, Oblinger C, Hsuanyu Y, Dunford HB. Mechanism of reaction of myeloperoxidase with hydrogen peroxide and chloride ion. Eur. J. Biochem. 2000; 267: 5858-5864.
46. 2O bei bakterien (E. coli), Z. Naturforsch. C. 1989; 44: 1053-1057.
47. Foote CS, Goyne TE, Lehrer RI. Assesment of chlorination by human neutrophils. Nature 1983; 301: 715-716.
48. Foote CS. Mechanisms of photo-oxidation. In Singlet Oxygen, Ranby B, Rabek JF (eds). Wiley: New York, 1978; 135-146.
49. Hampton MB, Kettle AJ, Winterbourn CC. Involvement of superoxide and myeloperoxidase in oxygen-dependent killing of Staphylococcus aureus by neutrophils. Infect. Immun. 1996; 64: 3512-3517.