The potential role of nitric oxide in substrate switching in eosinophil peroxidase

Biochemistry

Volumn 46, Issue 2, 2007, Pages 406-415

  Galijasevic, Semira ^a   Proteasa, Gheorghe ^a   Abdulhamid, Ibrahim ^b   Abu Soud, Husam M ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; COMPUTER SIMULATION; DISEASES; HYDROGEN PEROXIDE; OXIDATION; PROTEINS; REACTION KINETICS;

EOSINOPHIL PEROXIDASE; NITRIC OXIDE; PATHOGENS; SUBSTRATE SWITCHING;

ENZYMES;

ACID; BROMIDE; BROMINE; CATION; EOSINOPHIL PEROXIDASE; FERRIC ION; HEMOPROTEIN; HYDROGEN PEROXIDE; NITRIC OXIDE; OXIDIZING AGENT;

ARTICLE; ASTHMA; BLOOD LEVEL; CATALYSIS; CELL ACTIVATION; CELL TRANSPORT; CHEMICAL MODEL; CHEMICAL REACTION KINETICS; CLINICAL FEATURE; COMPUTER SIMULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; EOSINOPHIL; HOST RESISTANCE; METABOLISM; NONHUMAN; OXIDATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; RESPIRATORY TRACT DISEASE; SUBSTRATE SWITCHING; TIME;

ANIMALS; BROMIDES; EOSINOPHIL PEROXIDASE; EOSINOPHILS; KINETICS; MODELS, MOLECULAR; NITRIC OXIDE; OXIDATION-REDUCTION; PROTEIN CONFORMATION; SPECTROPHOTOMETRY; SUBSTRATE SPECIFICITY; SWINE;

EID: 33846217423     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061177u     Document Type: Article

References (83)

1. Klebanoff, S. J., Locksley, R. M., Jong, E., and Rosen, H. (1983) Oxidative response of phagocytes to parasite invasion, Ciba Found. Symp. 99, 92-112.
2. Abraham, D., Leon, O., Schnyder-Candrian, S., Wang, C. C., Galioto, A. M., Kerepesi, L. A., Lee, J. J., and Lustigman, S. (2004) Immunoglobulin E and eosinophil-dependent protective immunity to larval Onchocerca volvulus in mice immunized with irradiated larvae, Infect. Immun. 72, 810-817.
3. Ackerman, S. J., Gleich, G. J., Loegering, D. A., Richardson, B. A., and Butterworth, A. E. (1985) Comparative toxicity of purified human eosinophil granule cationic proteins for schistosomula of Schistosoma mansoni, Am. J. Trop. Med. Hyg. 34, 735-745.
4. Betts, C. J., and Else, K. J. (1999) Mast cells, eosinophils and antibody-mediated cellular cytotoxicity are not critical in resistance to Trichuris muris, Parasite Immunol. 21, 45-52.
5. Chandrashekar, R., Rao, U. R., Parab, P. B., and Subrahmanyam. D. (1986) Brugia malayi: rat cell interactions with infective larvae mediated by complement, Exp. Parasitol. 62, 362-369.
6. Gleich, G. J., Ottesen, E. A., Leiferman, K. M., and Ackerman, S. J. (1989) Eosinophils and human disease, Int. Arch. Allergy Appl. Immunol. 88, 59-62.
7. Rothenberg, M. E. (1998) Eosinophilia, N. Engl. J. Med. 338, 1592-1600.
8. Holt, P. G., Macaubas, C., Stumbles, P. A., and Sly, P. D. (1999) The role of allergy in the development of asthma, Nature 402, B12-B17.
9. Weiss, S. J., Test, S. T., Eckmann, C. M., Ross, D., and Regiania, S. (1986) Brominating oxidants generated by human eosinophils, Science 234, 200-203.
10. Mayeno, A. N., Curran, A. J., Roberts, R. L., and Foote, C. S. (1989) Eosinophils preferentially use bromide to generate halogenating agents, J. Biol. Chem. 264, 5660-5668.
11. Agosti, J. M., Altman, L. C., Ayars, G. H., Loegering, D. A., Gleich, G. J., and Klebanoff, S. J. (1987) The injurious effect of eosinophil peroxidase, hydrogen peroxide, and halides on pneumocytes in vitro, J. Allergy Clin. Immunol. 79, 496-504.
12. Jong, E. C., Henderson, W. R., and Klebanoff, S. J. (1980) Bactericidal activity of eosinophil peroxidase, J. Immunol. 124, 1378-1382.
13. Jong, E. C., Mahmoud, A. A., and Klebanoff, S. J. (1981) Peroxidase-mediated toxicity to schistosomula of Schistosoma mansoni, J. Immunol. 126, 468-471.
14. Slungaard, A., and Mahoney, J. R., Jr. (1991) Bromide-dependent toxicity of eosinophil peroxidase for endothelium and isolated working rat hearts: a model for eosinophilic endocarditis, J. Exp. Med. 173, 117-126.
15. 2-halide system and granule basic proteins, J. Immunol. 143, 239-244.
16. Kazura, J. W., Fanning, M. M., Blumer, J. L., and Mahmoud, A. A. (1981) Role of cell-generated hydrogen peroxide in granulocyte-mediated killing of schistosomula of Schistosoma mansoni in vitro, J. Clin. Invest. 67, 93-102.
17. Samoszuk, M. K., Nguyen, V., Thomas, C., and Jacobson, D. (1994) Effects of sonicated eosinophils on the in vivo sensitivity of human lymphoma cells to glucose oxidase, Cancer Res. 54, 2650-2653.
18. Bolscher, B. G., Zoutberrg, G. R., Cuperus, R. A., and Wever, R. (1984) Vitamin C stimulates the chlorinating activity of human myeloperoxidase, Biochim. Biophys. Acta 784, 189-191.
19. Klebanoff, S. J., Waltersdorph, A. M., and Rosen, H. (1984) Antimicrobial activity of myeloperoxidase, Methods Enzymol. 105, 399-403.
20. Caulfield, J. P., Korman, G., Butterworth, A. E., Hogan, M., and David, J. R. (1980) Partial and complete detachment of neutrophils and eosinophils from schistosomula: evidence for the establishment of continuity between a fused and normal parasite membrane, J. Cell Biol 86, 46-63.
21. Arlandson, M., Decker, T., Roongta, V. A., Bonilla, L., Mayo, K. H., MacPherson, J. C., Hazen, S. L., and Slungaard, A. (2001) Eosinophil peroxidase oxidation of thiocyanate. Characterization of major reaction products and a potential sulfhydryl-targeted cytotoxicity system, J. Biol. Chem. 276, 215-224.
22. Abu-Soud, H. M., Khassawneh, M. Y., Sohn, J. T., Murray, P., Haxhiu, M. A., and Hazen, S. L. (2001) Peroxidases inhibit nitric oxide (NO) dependent bronchodilation: development of a model describing NO-peroxidase interactions, Biochemistry 40, 11866-11875.
23. Abu-Soud, H. M., and Hazen, S. L. (2000) Nitric oxide is a physiological substrate for mammalian peroxidases, J. Biol. Chem. 275, 37524-37532.
24. Abu-Soud, H. M., and Hazen, S. L. (2000) Nitric oxide modulates the catalytic activity of myeloperoxidase, J. Biol. Chem. 275, 5425-5430.
25. Galijasevic, S., Saed, G. M., Diamond, M. P., and Abu-Soud, H. M. (2003) Myeloperoxidase up-regulates the catalytic activity of inducible nitric oxide synthase by preventing nitric oxide feedback inhibition, Proc. Natl. Acad. Sci. U.S.A. 100, 14766-14771.
26. Galijasevic, S.: Saed, G. M., Hazen, S. L., and Abu-Soud, H. M. (2006) Myeloperoxidase metabolizes thiocyanate in a reaction driven by nitric oxide, Biochemistry 45, 1255-1262.
27. Teitz, N. W. (1999) Drugs: Therapeutic and Toxic, in Teitz Textbook of Clinical Chemistry (Burtis, C.A., and Ashwood, E.R., Eds.) p 1097, W.B. Saunders Co., Philadelphia.
28. Faulkner, D. J. (1998) Marine natural products, Nat. Prod. Rep. 15, 113-158.
29. van Leeuwen, F. X., den Tonkelaar, E. M., and van Logten, M. J. (1983) Toxicity of sodium bromide in rats: effects on endocrine system and reproduction, Food Chem. Toxicol. 21, 383-389.
30. Nielsen, F. H. (1996) Other Trace Elements, in Present Knowledge in Nutrition (Ziegler, E. E., and Filer, L. L. Jr., Eds.) 7th ed., pp 353 -377, ILSI Press: Washington, DC.
31. Alumot, E., Nachtomi, E., Kempenich-Pinto, O., Mandel, E., and Schindler, H. (1968) The effect of ethylene dibromide in feed on the growth, sexual development and fertility of chickens, Poult. Sci. 47, 1979-1985.
32. Pavelka, S. (2004) Metabolism of bromide and its interference with the metabolism of iodine, Physiol. Res. 53 Suppl. 1, S81-S90.
33. Buchberger, W., Holler, W., and Winsauer, K. (1990) Effects of sodium bromide on the biosynthesis of thyroid hormones and brominated/iodinated thyronines, J. Trace Elem. Electrolytes Health Dis. 4, 25-30.
34. Wu, W., Chen, Y., d' Avignon, A., and Hazen. S. L. (1999) 3-Bromotyrosine and 3,5-dibromotyrosine are major products of protein oxidation by eosinophil peroxidase: potential markers for eosinophil-dependent tissue injury in vivo, Biochemistry 38, 3538-3548.
35. Wu, W., Samoszuk, M. K., Comhair, S. A., Thomassen, M. J., Farver, C. F., Dweik, R. A., Kavuru, M. S., Erzurum, S. C., Hazen, S. L. (2000) Eosinophils generate brominating oxidants in allergen-induced asthma, J. Clin. Invest. 105, 1455-1463.
36. MacPherson, J. C., Comhair, S. A., Erzurum, S. C., Klein, D. F., Lipscomb, M. F., Kavuru, M. S., Samoszuk, M. K., and Hazen, S. L. (2001) Eosinophils are a major source of nitric oxide-derived oxidants in severe asthma: characterization of pathways available to eosinophils for generating reactive nitrogen species, J. Immunol. 166, 5763-5772.
37. Henderson, J. P., Byun, J., Williams, M. V., McCormick, M. L., Parks, W. C., Ridnour, L. A., and Heinecke, J. W. (2001) Bromination of deoxycytidine by eosinophil peroxidase: a mechanism for mutagenesis by oxidative damage of nucleotide precursors, Proc. Natl. Acad. Sci. U.S.A. 98, 1631-1636.
38. Stuehr, D. J. (1999) Mammalian nitric oxide synthases, Biochim. Biophys. Acta 1411, 217-230.
39. Nathan, C., and Xie, Q. W. (1994) Nitric oxide synthases: roles, tolls, and controls, Cell 78, 915-918.
40. Abu-Soud, H. M., Ichimori, K., Nakazawa, H., and Stuehr, D. J. (2001) Regulation of inducible nitric oxide synthase by self-generated NO, Biochemistry 40, 6876-6881.
41. Hurshman, A. R., and Marietta, M. A. (1995) Nitric oxide complexes of inducible nitric oxide synthase: spectral characterization and effect on catalytic activity, Biochemistry 34, 5627-5634.
42. Mitra, S. N., Slungaard, A., and Hazen, S. L. (2000) Role of eosinophil peroxidase in the origins of protein oxidation in asthma, Redox. Rep. 5, 215-224.
43. Thayer, J. R., and Huffaker, R. C. (1980) Determination of nitrate and nitrite by high-pressure liquid chromatography: comparison with other methods for nitrate determination, Anal. Biochem. 102, 110-119.
44. Jorg, A., Pasquier, J. M., and Kelebanoff, S. J. (1982) Purification of horse eosinophil peroxidase, Biochim. Biophys. Acta 701, 185-191.
45. van Dalen, C. J., Whitehouse, M. W., Winterbourn, C. C., and Kettle, A. J. (1997) Thiocyanate and chloride as competing substrates for myeloperoxidase, Biochem. J. 327, 487-492.
46. Bolscher, B. G., Plat, H., and Wever, R. (1984) Some properties of human eosinophil peroxidase, a comparison with other peroxidases, Biochim. Biophys. Acta 784, 177-186.
47. Carlson, M. G., Peterson, C. G., and Venge, P. (1985) Human eosinophil peroxidase: purification and characterization, J. Immunol. 134, 1875-1879.
48. Furtmuller, P. G., Burner, U., Regelsberger, G., Obinger, C. (2000) Spectral and kinetic studies on the formation of eosinophil peroxidase compound I and its reaction with halides and thiocyanate, Biochemistry 39, 15578-15584.
49. Furtmuller, P. G., Jantschko, W., Regelsberger, G., and Obinger, C. (2001) Spectral and kinetic studies on eosinophil peroxidase compounds I and II and their reaction with ascorbate and tyrosine, Biochim. Biophys. Acta 1548, 121-128.
50. Abu-Soud, H. M., and Hazen, S. L. (2001) Interrogation of heme pocket environment of mammalian peroxidases with diatomic ligands, Biochemistry 40, 10747-10755.
51. Furtmuller, P. G., Zederbauer, M., Jantschko, W., Helm, J., Bogner, M., Jakopitsch, C., and Obinger, C. (2005) Active site structure and catalytic mechanisms of human peroxidases, Arch. Biochem. Biophys. 445, 199-213.
52. Kettle, A. J., and Winterbourn, C. C. (2001) A kinetic analysis of the catalase activity of myeloperoxidase, Biochemistry 40, 10204-10212.
53. Andreadis, A. A., Hazen, S. L., Comhair, S. A., and Erzurum, S. C. (2003) Oxidative and nitrosative events in asthma, Free Radic. Biol. Med. 35, 213-225.
54. Brennan, M. -. L., Wu, W., Fu, X., Shen, Z., Song, W., Frost, H., Vadseth, C., Narine. L., Lenkiewicz, E., Borchers, M. T., Lusis, A. J., Lee, J. J., Lee, N. A., Abu-Soud, H. M., Ischiropoulos, H., and Hazen, S. L. (2002) A tale of two controversies. Defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species, J. Biol. Chem. 277, 17415-17427.
55. van der Vliet, A., Eiserich, J. P., and Cross, C. E. (2000) Nitric oxide: a pro-inflammatory mediator in lung disease? Respir. Res. 1, 67-72.
56. Xu, W., Zheng, S., Dweik, R. A. and Erzurum, S. C. (2006) The role of epithelial NO in airway viral infection, Free Radic. Biol. Med. 41, 19-28.
57. Tahboub, Y. R., Galijasevic, S., Diamond, M. P., and Abu-Soud, H. M. (2005) Thiocyanate modulates the catalytic activity of mammalian peroxidases, J. Biol. Chem. 280, 26129-26136.
58. Zeng, J., and Fenna, R. E. (1992) X-ray crystal structure of canine myeloperoxidase at 3 A resolution, J. Mol. Biol. 226, 185-207.
59. Davey, C. A., and Fenna, R. E. (1996) 2.3 A resolution X-ray crystal structure of the bisubstrate analogue inhibitor salicylhydroxamic acid bound to human myeloperoxidase: a model for a prereaction complex with hydrogen peroxide, Biochemistry 35, 10967-1097.
60. Fiedler, T. J., Davey, C. A., and Fenna, R. E. (2000) X-ray crystal structure and characterization of halide-binding sites of human myeloperoxidase at 1.8 Å resolution, J. Biol. Chem. 275, 11964-11971.
61. Bakkenist, A. R. J., De B.oer, J. E. G., Plat, H., and Wever, R. (1980) The halide complexes of myeloperoxidase and the mechanism of the halogenation reactions, Biochim. Biophys. Acta 613, 337-348.
62. van der Vliet, A., Eiserich, J. P., Halliwell, B., and Cross, C. E. (1997) Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity, J. Biol. Chem. 272, 7617-7625.
63. van Dalen, C. J., Winterbourn, C. C., and Kettle, A. J. (2006) Mechanism of nitrite oxidation by eosinophil peroxidase: implications for oxidant production and nitration by eosinophils, Biochem. J. 394, 707-713.
64. Proteasa, G., Tahboub, Y. R., Galijasevic S., Raushel, F. M., and Abu-Soud, H. M. (2006) Kinetic evidence supports the existence of two halide-binding sites that display distinct impact on the heme iron microenvironment in myeloperoxidase, Biochemistry, in press.
65. Andrews, P. C., and Krinsky, N. I. (1982) A kinetic analysis of the interaction of human myeloperoxidase with hydrogen peroxide, chloride ions, and protons, J. Biol. Chem. 257, 13240-13245.
66. Harrison, J. E., and Schultz, J. (1976) Studies on the chlorinating activity of myeloperoxidase, J. Biol. Chem. 251, 1371-1374.
67. Wever, R., Kast, W. M., Kasinoedin, J. H., and Boelens, R. (1982) The peroxidation of thiocyanate catalysed by myeloperoxidase and lactoperoxidase, Biochim. Biophys. Acta 709, 212-219.
68. Singh, A. K., Singh, N., Bhushan, A., Singh, T. P. Structure of Bovine Lactoperoxidase at 2.3 Å resolution, in press.
69. De Gioia, L., Ghibaudi, E. M., Laurenti, E., Salmona, M., and Ferrari, R. P. (1996) A theoretical three-dimensional model for lactoperoxidase and eosinophil peroxidase, built on the scaffold of the myeloperoxidase X-ray structure, J. Biol. Inorg. Chem. 1, 476-485.
70. Kunishima, N., Fukuyama, K., Matsubara, H., Hatanaka, H., Shibano, Y., and Amachi, T. (1994) Crystal structure of the fungal peroxidase from Arthromyces ramosus at 1.9 Å resolution. Structural comparisons with the lignin and cytochrome c peroxidases, J. Mol. Biol. 235, 331-344.
71. Patterson, W. R., and Poulos, T. L. (1995) Crystal structure of recombinant pea cytosolic ascorbate peroxidase, Biochemistry 34, 4331-4341.
72. Schuller, D. J., Ban, N., Huystee, R. B., McPherson, A., and Poulos, T. L. (1996) The crystal structure of peanut peroxidase, Structure 4, 311-321.
73. Bosshard, H. R., Anni, H., and Yonetani, T. (1991) Peroxidases in Chemistry and Biology, Vol. II, pp 51-84, CRC Press, Boca Raton, FL.
74. Finzel, B. C., Poulos, T. L., and Kraut, J. (1984) Crystal structure of yeast cytochrome c peroxidase refined at 1.7-A resolution, J. Biol. Chem. 259, 13027-13036.
75. Gajhede, M., Schuller, D. J., Henriksen, A., Smith, A. T., and Poulos, T. L. (1997) Crystal structure of horseradish peroxidase C at 2.15 A resolution, Nat. Struct. Biol. 4, 1032-1038.
76. Mozzarelli, A., and Rossi, G. L. (1996) Protein function in the crystal, Annu. Rev. Biophys. Biomol. Struct. 25, 343-365.
77. Barrick, D. (1995) Depletion and replacement of protein metal ligands, Curr. Opin. Biotechnol. 6, 411-418.
78. Cooper, C. E. (1999) Nitric oxide and iron proteins, Biochim. Biophys. Acta 1411, 290-309.
79. Abu-Soud, H. M., Wu, C., Ghosh, D. K., and Stuehr, D. J. (1998) Stopped-flow analysis of CO and NO binding to inducible nitric oxide synthase, Biochemistry 37, 3777-37786.
80. Uetani, K., Der, S. D., Zamanian-Daryoush, M., de La Motteqq, C., Lieberman, B. Y., Williams, B. R., and Erzurum, S. C. (2000) Central role of double-stranded RNA-activated protein kinase in microbial induction of nitric oxide synthase, J. Immunol. 165, 988-996.
81. Zheng, S., De, B. P., Choudhary, S., Comhair, S. A., Goggans, T., Slee, R., Williams, B. R., Pilewski, J., Haque, S. J., and Erzurum, S. C. (2003) Impaired innate host defense causes susceptibility to respiratory virus infections in cystic fibrosis, Immunity 18, 619-630.
82. Guo, F. H., Comhair, S. A., Zheng, S., Dweik, R. A., Eissa, N. T., Thomassen, M. J., Calhoun, W., and Erzurum, S. C. (2000) Molecular mechanisms of increased nitric oxide (NO) in asthma: evidence for transcriptional and post-translational regulation of NO synthesis, J. Immunol. 164, 5970-5980.
83. Dweik, R. A., Comhair, S. A., Gaston, B., Thunnissen, F. B., Farver, C., Thomassen, M. J., Kavuru, M., Hammel, J., Abu-Soud, H. M., and Erzurum, S. C. (2001) NO chemical events in the human airway during the immediate and late antigen-induced asthmatic response, Proc. Natl. Acad. Sci. U.S.A. 98, 2622-2627.