Human neutrophils employ chlorine gas as an oxidant during phagocytosis

Journal of Clinical Investigation

Volumn 98, Issue 6, 1996, Pages 1283-1289

  Hazen, Stanley L ^a   Hsu, Fong Fu ^a   Mueller, Dianne M ^a   Crowley, Jan R ^a   Heinecke, Jay W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

atherosclerosis; hypochlorous acid; inflammation; myeloperoxidase; oxidation

Indexed keywords

CHLORINE; HYDROGEN PEROXIDE; HYPOCHLOROUS ACID; MYELOPEROXIDASE; OXIDIZING AGENT; REACTIVE OXYGEN METABOLITE;

ARTICLE; ATHEROSCLEROSIS; CYTOTOXICITY; GAS CHROMATOGRAPHY; HALOGENATION; HUMAN; HUMAN CELL; INFLAMMATION; ISCHEMIA; NEUTROPHIL; OXIDATION REDUCTION POTENTIAL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN SECRETION; REPERFUSION INJURY;

EID: 10144255096     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118914     Document Type: Article

References (50)

1. Babior, B.M. 1978. Oxygen-dependent microbial killing by phagocytes. N. Engl. J. Med. 298:659-663.
2. Klebanoff, S.J. 1980. Oxygen metabolism and the toxic properties of phagocytes. Ann. Intern. Med. 93:480-489.
3. Nauseef, W.M. 1988. Myeloperoxidase deficiency - Phagocytic defects I: Abnormalities outside of the respiratory burst. Hematol./Oncol. Clin. N. Am. 2: 135-158.
4. Weiss, S.J. 1989. Tissue destruction by neutrophils. N. Engl. J. Med. 320: 365-376.
5. Hurst, J.K., and W.C. Barrette, Jr. 1989. Leukocyte oxygen activation and microbicidal oxidative toxins. CRC Crit. Rev. Biochem. Mol. Biol. 24:271-328.
6. Ames, B.N., M.K. Shigenaga, and T.M. Hagen. 1993. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. USA. 90: 7915-7922.
7. Segal, A.W., and A. Abo. 1993. The biochemical basis of the NADPH oxidase of phagocytes. Trends Biochem. Sci. 18:43-47.
8. Heinecke, J.W. 1994. Cellular mechanisms for the oxidative modification of lipoproteins: Implications for atherogenesis. Coron. Artery Dis. 5:205-210.
9. Klebanoff, S.J., and R.A. Clark. 1978. The Neutrophil: Function and Clinical Disorders. North Holland Biomedical Press, Amsterdam. 447-451.
10. Witztum, J.L., and D. Steinberg. 1991. Role of oxidized low density lipoprotein in atherogenesis. J. Clin. Invest. 88:1785-1792.
11. Stadtman, E.R. 1992. Protein oxidation and aging. Science (Wash. DC). 257:1220-1224.
12. Agner, K. 1972. Structure and function of oxidation-reduction enzymes. Pergamon Press, New York. 329-335.
13. Harrison, J.E., and J. Schultz. 1976. Studies on the chlorinating activity of myeloperoxidase. J. Biol. Chem. 251:1371-1374.
14. Foote, C.S., T.E. Goyne, and R.I. Lehrer. 1981. Assessment of chlorination by human neutrophils. Nature (Lond.). 301:715-716.
15. Weil, I., and J.C. Morris. 1949. Kinetic studies on the chloramines. I. The rates of formation of monochloramine, N-chlormethylamine and N-chlordimethylamine. J. Am. Chem. Soc. 71:1664-1671.
16. Thomas, E.L., M.M. Jefferson, and M.B. Grisham. 1982. Myeloperoxidase-catalyzed incorporation of amines into proteins: Role of hypochlorous acid and dichloramines. Biochemistry. 21:6299-6308.
17. Weiss, S.J., R. Klein, A. Slivka, and M. Wei. 1982. Chlorination of taurine by human neutrophils. Evidence for hypochlorous acid generation. J. Clin. Invest. 70:598-607.
18. Winterbourn, C.C., J.J.M. VandenBerg, E. Roitman, and F.A. Kuypers. 1992. Chlorohydrin formation from unsaturated fatty acids reacted with hypochlorous acid. Arch. Biochem. Biophys. 296:547-555.
19. Heinecke, J.W., W.Li. D.M. Mueller, A. Bohrer and J. Turk. 1994. Cholesterol chlorohydrin synthesis by the myeloperoxidase-hydrogen peroxide-chloride system: Potential markers for lipoproteins oxidatively damaged by phagocytes. Biochemistry. 33:10127-10136.
20. Albrich, J.M., C.A. McCarthy, and J.K. Hurst. 1981. Biological reactivity of hypochlorous acid: Implications for microbicidal mechanisms of leukocyte myeloperoxidase. Proc. Natl. Acad. Sci. USA. 78:210-214.
21. White, G.C. 1972. Chemistry of chlorinalion. In Handbook of Chlorination. Van Nostrand Reinhold, New York. 182-227.
22. Heinecke, J.W., W. Li, H.L. Daehnke, and J.A. Goldstein. 1993. Dityrosine, a specific marker of oxidation, is synthesized by the myeloperoxidase-hydrogen peroxide system of human neutrophils and macrophages. J. Biol. Chem. 268:4069-4077.
23. Rakita, R.M., B.R. Michel, and H. Rosen. 1990. Differential inactivation of Escherichia coli membrane dehydrogenases by a myeloperoxidase-mediated antimicrobial system. Biochemistry. 29:1075-1080.
24. Morita, Y., H. Iwamoto, S. Aibara, T. Kobayashi, and E. Hasegawa. 1986. Crystallization and properties of myeloperoxidase from normal human leukocytes. J. Biochem. 99:761-770.
25. Thomas, E.L., M.B. Grisham, and M.M. Jefferson. 1986. Preparation and characterization of chloramines. Methods Enzymol. 132:569-585.
26. Morris, J.C. 1966. The acid ionization constant of HOCl from 5-35°C. J. Phys. Chem. 70:3798-3805.
27. Hazen, S.L., F.F. Hsu, and J.W. Heinecke. 1996. p-Hydroxyphenylacetaldehyde is the major product of L-tyrosine oxidation by activated human phagocytes: a chloride-dependent mechanism for the conversion of free amino acids into reactive aldehydes by myeloperoxidase. J. Biol. Chem. 271:1861-1867.
28. Lieber, M.R., and T.L. Steek. 1989. Hemolytic holes in human erythrocytic membrane ghosts. Methods Enzymol. 173:356-376.
29. El-Saadani, M. Estyerbauer, H. El-Sayad, M. Goher, A.Y. Jurgens, and H. Jurgens. 1989. A spectrophotometric assay for lipid peroxides in serum lipoproteins using a commercially available reagent. J. Lipid. Res. 30:627-630.
30. Nelson, D.P., and L.A. Kiesow. 1972. Enthalpy of decomposition of hydrogen peroxide by calalase at 25°C. Anal. Biochem. 49:474-478.
31. Kettle, A.J., and C.C. Winterbourn. 1994. Assays for the chlorination activity of myeloperoxidase. Methods Enzymol. 233:502-512.
32. Domigan, N.M., T.S. Charlton, M.W. Duncan, C.C. Winterbourn, and A.J. Kettle. 1995. Chlorination of tyrosyl residues in peptides by myeloperoxidase and human neutrophils. J. Biol. Chem. 270:16542-16548.
33. Orton, K.J.P., and A.E. Bradfield. 1927. The chlorination of anilides: the directing influence of the acylamido-group. J. Chem. Soc. 986-997.
34. de la Mare, P.B.D. 1976. Reaction pathways involving attack by electrophilic halogens on unsaturated compounds. In Electrophilic Halogenation. Cambridge University Press, Cambridge, 118:64-95.
35. Jensen, M.S., and D.F. Bainton. 1973. Temporal changes in pH within the phagocytic vacuole of the polymorphonuclear neutrophilic leukocyte. J. Cell Biol. 56:379-388.
36. Lehrer, R.I., and P. Cech. 1984. Phagolysosomal pH of neutrophils. Blood. 63:88-95.
37. Mantovani, B. 1975. Different roles of IgG and complement receptors in phagocytosis by polymorphonuclear leukocytes. J. Immunol. 115:15-17.
38. Scribner, D.J., and D. Fahrney. 1976. Neutrophil receptors for IgG and complement: Their roles in the attachment and ingestion phases of phagocytosis. J. Immunol. 116:892-897.
39. Silverstein, S.C., R. M. Steinman, and Z.A. Cohn. 1977. Endocytosis. Ann. Rev. of Biochem. 46:669-722.
40. Wright, S.D. 1986. Methods for study of receptor-mediated phagocytosis. Methods Enzymol. 132:204-221.
41. Wright, S.D., and S.C. Silverstein. 1984. Phagocytosing macrophages exclude proteins from zones of contact with opsonized targets. Nature (Lond.). 309:359-361.
42. Loike, J.D., R. Silverstein, S.D. Wright, J.I. Weitz, A.J. Huang, and S.C. Silverstein. 1992. The role of protected extracellular compartments in interactions between leukocytes, and platelets, and fibrin/fibrinogen matrices. Ann. NY Acad. Sci. 667:163-172.
43. Hermann, M., M. E. E. Jaconi, C. Dahlgren, F. A. Waldvogel, O. Stendahl, and D. P. Lew. 1990. Neutrophil bactericidal activity against staphylococcus aureus adherent on biological surfaces: surface-bound extracellular matrix proteins activate intracellular killing by oxygen-dependent and -independent mechanisms. J. Clin. Invest. 86:942-951.
44. Nathan, C.F. 1987. Neutrophil activation on biological surfaces: massive secretion of hydrogen peroxide in response to products of macrophages and lymphocytes. J. Clin. Invest. 80:1550-1560.
45. Silver, I.A., R.J. Murrills, and D.J. Etherington. 1988. Microelectrode studies on the acid microenvironment beneath adherent macrohages and osteoclasts. Exp. Cell Res. 175:266-276.
46. Hajjar, D.P., I.C. Farber, and S.C. Smith. 1988. Oxygen tension within the arterial wall: Relationship to altered bioenergetic metabolism and lipid accumulation. Arc. Biochem. Biophys. 262:375-380.
47. Rosenfeld, M.E., W. Palinski, S. Ylaherttuala, S. Butler, and J.L. Witztum. 1990. Distribution of oxidation specific lipid-protein adducts and apolipoprotein-B in atherosclerotic lesions of varying severity from WHHL rabbits. Arteriosclerosis. 10:336-349.
48. Daugherty, A., J.L. Dunn, D.L. Rateri, and J.W. Heinecke. 1994. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J. Clin. Invest. 94:437-444.
49. Hazell, L.J., L. Arnold, D. Flowers, G. Waeg, E. Malle, and R. Stocker. 1996. Presence of hypochlorite-modified proteins in human atherosclerotic lesions. J. Clin. Invest. 97:1535-1544.
50. Hazen, S.L., F.F. Hsu, K. Duffin, and J.W. Heinecke. Molecular chlorine generated by the myeloperoxidase-hydrogen peroxide-chloride system of phagocytes converts low density lipoprotein cholesterol into a family of chlorinated sterols. J. Biol. Chem. 271:23080-23088.