Hypochlorous acid-induced heme degradation from lactoperoxidase as a novel mechanism of free iron release and tissue injury in inflammatory diseases

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Souza, Carlos Eduardo A ^a   Maitra, Dhiman ^a   Saed, Ghassan M ^a   Diamond, Michael P ^a   Moura, Arlindo A ^b   Pennathur, Subramaniam ^c   Abu Soud, Husam M ^a,d  

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

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC ION; FERROUS ION; HEME; HYPOCHLOROUS ACID; LACTOPEROXIDASE; MYELOPEROXIDASE; THIOCYANATE; IRON; THIOCYANIC ACID DERIVATIVE;

ARTICLE; BINDING KINETICS; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME DEGRADATION; ENZYME MECHANISM; ENZYME SYNTHESIS; INFLAMMATORY DISEASE; IRON KINETICS; MOLECULAR INTERACTION; PROTEIN AGGREGATION; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; TISSUE INJURY; ANIMAL; ANTIBODY SPECIFICITY; BIOCATALYSIS; BIOLOGICAL MODEL; CATTLE; CHEMISTRY; DRUG EFFECT; FLUORESCENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INFLAMMATION; KINETICS; METABOLISM; PATHOLOGY; PROTEIN QUATERNARY STRUCTURE; SPECTROSCOPY;

MAMMALIA;

ANIMALS; BIOCATALYSIS; CATTLE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FLUORESCENCE; HEME; HYPOCHLOROUS ACID; INFLAMMATION; IRON; KINETICS; LACTOPEROXIDASE; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; PROTEIN STRUCTURE, QUATERNARY; SPECTRUM ANALYSIS; THIOCYANATES;

EID: 81555212303     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027641     Document Type: Article

References (86)

1. Klebanoff SJ, (2005) Myeloperoxidase: friend and foe. J Leukoc Biol 77: 598-625.
2. Davies MJ, Hawkins CL, Pattison DI, Rees MD, (2008) Mammalian heme peroxidases: from molecular mechanisms to health implications. Antioxid Redox Signal 10: 1199-1234.
3. Podrez EA, Abu-Soud HM, Hazen SL, (2000) Myeloperoxidase-generated oxidants and atherosclerosis. Free Radic Biol Med 28: 1717-1725.
4. Singh AK, Singh N, Tiwari A, Sinha M, Kushwaha GS, et al. First structural evidence for the mode of diffusion of aromatic ligands and ligand-induced closure of the hydrophobic channel in heme peroxidases. J Biol Inorg Chem 15: 1099-1107.
5. Fiedler TJ, Davey CA, Fenna RE, (2000) X-ray crystal structure and characterization of halide-binding sites of human myeloperoxidase at 1.8 A resolution. J Biol Chem 275: 11964-11971.
6. Furtmuller PG, Jantschko W, Zederbauer M, Jakopitsch C, Arnhold J, et al. (2004) Kinetics of interconversion of redox intermediates of lactoperoxidase, eosinophil peroxidase and myeloperoxidase. Jpn J Infect Dis 57: S30-31.
7. Dull TJ, Uyeda C, Strosberg AD, Nedwin G, Seilhamer JJ, (1990) Molecular cloning of cDNAs encoding bovine and human lactoperoxidase. DNA Cell Biol 9: 499-509.
8. Nauseef WM, Malech HL, (1986) Analysis of the peptide subunits of human neutrophil myeloperoxidase. Blood 67: 1504-1507.
9. Everse J, Everse KE, Grisham MB, (1991) Peroxidases in chemistry and biology Boca Raton, Fla. CRC Press.
10. Marquez LA, Dunford HB, Van Wart H, (1990) Kinetic studies on the reaction of compound II of myeloperoxidase with ascorbic acid. Role of ascorbic acid in myeloperoxidase function. J Biol Chem 265: 5666-5670.
11. Abu-Soud HM, Hazen SL, (2000) Nitric oxide is a physiological substrate for mammalian peroxidases. J Biol Chem 275: 37524-37532.
12. Abu-Soud HM, Khassawneh MY, Sohn JT, Murray P, Haxhiu MA, et al. (2001) Peroxidases inhibit nitric oxide (NO) dependent bronchodilation: development of a model describing NO-peroxidase interactions. Biochemistry 40: 11866-11875.
13. Galijasevic S, Saed GM, Hazen SL, Abu-Soud HM, (2006) Myeloperoxidase metabolizes thiocyanate in a reaction driven by nitric oxide. Biochemistry 45: 1255-1262.
14. Heinecke JW, Li W, Daehnke HL 3rd, Goldstein JA, (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.
15. Weiss SJ, (1989) Tissue destruction by neutrophils. N Engl J Med 320: 365-376.
16. Galijasevic S, Saed GM, Diamond MP, Abu-Soud HM, (2004) High dissociation rate constant of ferrous-dioxy complex linked to the catalase-like activity in lactoperoxidase. J Biol Chem 279: 39465-39470.
17. Abu-Soud HM, Raushel FM, Hazen SL, (2004) A novel multistep mechanism for oxygen binding to ferrous hemoproteins: rapid kinetic analysis of ferrous-dioxy myeloperoxidase (compound III) formation. Biochemistry 43: 11589-11595.
18. Kettle AJ, Anderson RF, Hampton MB, Winterbourn CC, (2007) Reactions of superoxide with myeloperoxidase. Biochemistry 46: 4888-4897.
19. Pullar JM, Vissers MC, Winterbourn CC, (2000) Living with a killer: the effects of hypochlorous acid on mammalian cells. IUBMB Life 50: 259-266.
20. Malech HL, Gallin JI, (1987) Current concepts: immunology. Neutrophils in human diseases. N Engl J Med 317: 687-694.
21. Malle E, Buch T, Grone HJ, (2003) Myeloperoxidase in kidney disease. Kidney Int 64: 1956-1967.
22. Ohshima H, Tatemichi M, Sawa T, (2003) Chemical basis of inflammation-induced carcinogenesis. Arch Biochem Biophys 417: 3-11.
23. Weiss SJ, Klein R, Slivka A, Wei M, (1982) Chlorination of taurine by human neutrophils. Evidence for hypochlorous acid generation. J Clin Invest 70: 598-607.
24. Aruoma OI, Halliwell B, (1987) Action of hypochlorous acid on the antioxidant protective enzymes superoxide dismutase, catalase and glutathione peroxidase. Biochem J 248: 973-976.
25. Malle E, Waeg G, Schreiber R, Grone EF, Sattler W, et al. (2000) Immunohistochemical evidence for the myeloperoxidase/H2O2/halide system in human atherosclerotic lesions: colocalization of myeloperoxidase and hypochlorite-modified proteins. Eur J Biochem 267: 4495-4503.
26. Brennan ML, Hazen SL, (2003) Emerging role of myeloperoxidase and oxidant stress markers in cardiovascular risk assessment. Curr Opin Lipidol 14: 353-359.
27. Daugherty A, Dunn JL, Rateri DL, Heinecke JW, (1994) Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J Clin Invest 94: 437-444.
28. Heinecke JW, The protein cargo of HDL: implications for vascular wall biology and therapeutics. J Clin Lipidol 4: 371-375.
29. Chau LY, (2000) Iron and atherosclerosis. Proceedings of the National Science Council, Republic of China Part B, Life sciences 24: 151-155.
30. Stanley N, Stadler N, Woods AA, Bannon PG, Davies MJ, (2006) Concentrations of iron correlate with the extent of protein, but not lipid, oxidation in advanced human atherosclerotic lesions. Free Radic Biol Med 40: 1636-1643.
31. Trinder D, Fox C, Vautier G, Olynyk JK, (2002) Molecular pathogenesis of iron overload. Gut 51: 290-295.
32. Galijasevic S, Maitra D, Lu T, Sliskovic I, Abdulhamid I, et al. (2009) Myeloperoxidase interaction with peroxynitrite: chloride deficiency and heme depletion. Free Radic Biol Med 47: 431-439.
33. Shishehbor MH, Hazen SL, (2004) Inflammatory and oxidative markers in atherosclerosis: relationship to outcome. Curr Atheroscler Rep 6: 243-250.
34. Conner GE, Wijkstrom-Frei C, Randell SH, Fernandez VE, Salathe M, (2007) The lactoperoxidase system links anion transport to host defense in cystic fibrosis. FEBS Lett 581: 271-278.
35. Furtmuller PG, Arnhold J, Jantschko W, Zederbauer M, Jakopitsch C, et al. (2005) Standard reduction potentials of all couples of the peroxidase cycle of lactoperoxidase. J Inorg Biochem 99: 1220-1229.
36. Maitra D, Byun J, Andreana PR, Abdulhamid I, Diamond MP, et al. Reaction of hemoglobin with HOCl: mechanism of heme destruction and free iron release. Free Radic Biol Med 51: 374-386.
37. Maitra D, Byun J, Andreana PR, Abdulhamid I, Saed GM, et al. Mechanism of hypochlorous acid-mediated heme destruction and free iron release. Free Radic Biol Med 51: 364-373.
38. Gerson C, Sabater J, Scuri M, Torbati A, Coffey R, et al. (2000) The lactoperoxidase system functions in bacterial clearance of airways. Am J Respir Cell Mol Biol 22: 665-671.
39. Ihalin R, Loimaranta V, Tenovuo J, (2006) Origin, structure, and biological activities of peroxidases in human saliva. Arch Biochem Biophys 445: 261-268.
40. Tenovuo J, Lumikari M, Soukka T, (1991) Salivary lysozyme, lactoferrin and peroxidases: antibacterial effects on cariogenic bacteria and clinical applications in preventive dentistry. Proc Finn Dent Soc 87: 197-208.
41. Lee JY, Kim YY, Chang JY, Park MS, Kho HS, The effects of peroxidase on the enzymatic and candidacidal activities of lysozyme. Arch Oral Biol 55: 607-612.
42. El-Chemaly S, Salathe M, Baier S, Conner GE, Forteza R, (2003) Hydrogen peroxide-scavenging properties of normal human airway secretions. Am J Respir Crit Care Med 167: 425-430.
43. Subramani S, (1992) Targeting of proteins into the peroxisomal matrix. J Membr Biol 125: 99-106.
44. Reid DW, Lam QT, Schneider H, Walters EH, (2004) Airway iron and iron-regulatory cytokines in cystic fibrosis. Eur Respir J 24: 286-291.
45. Ekmekci OB, Donma O, Sardogan E, Yildirim N, Uysal O, et al. (2004) Iron, nitric oxide, and myeloperoxidase in asthmatic patients. Biochemistry (Mosc) 69: 462-467.
46. Gray RD, Duncan A, Noble D, Imrie M, O'Reilly DS, et al. Sputum trace metals are biomarkers of inflammatory and suppurative lung disease. Chest 137: 635-641.
47. Furtmuller PG, Jantschko W, Regelsberger G, Jakopitsch C, Arnhold J, et al. (2002) Reaction of lactoperoxidase compound I with halides and thiocyanate. Biochemistry 41: 11895-11900.
48. Kettle AJ, Winterbourn CC, (1994) Assays for the chlorination activity of myeloperoxidase. Methods Enzymol 233: 502-512.
49. Clark RA, (2008) Oxidative stress and "senescent" fibroblasts in non-healing wounds as potential therapeutic targets. J Invest Dermatol 128: 2361-2364.
50. Crichton RR, Wilmet S, Legssyer R, Ward RJ, (2002) Molecular and cellular mechanisms of iron homeostasis and toxicity in mammalian cells. J Inorg Biochem 91: 9-18.
51. Kumar S, Bandyopadhyay U, (2005) Free heme toxicity and its detoxification systems in human. Toxicol Lett 157: 175-188.
52. Ong WY, Halliwell B, (2004) Iron, atherosclerosis, and neurodegeneration: a key role for cholesterol in promoting iron-dependent oxidative damage? Ann N Y Acad Sci 1012: 51-64.
53. Yamaguchi K, Mandai M, Toyokuni S, Hamanishi J, Higuchi T, et al. (2008) Contents of endometriotic cysts, especially the high concentration of free iron, are a possible cause of carcinogenesis in the cysts through the iron-induced persistent oxidative stress. Clin Cancer Res 14: 32-40.
54. Defrere S, Lousse JC, Gonzalez-Ramos R, Colette S, Donnez J, et al. (2008) Potential involvement of iron in the pathogenesis of peritoneal endometriosis. Mol Hum Reprod 14: 377-385.
55. Nagababu E, Rifkind JM, (2004) Heme degradation by reactive oxygen species. Antioxid Redox Signal 6: 967-978.
56. Hu S, Kincaid JR, (1991) Resonance Raman structural characterization and the mechanism of formation of lactoperoxidase compound III. Journal of the American Chemical Society 113: 7189-7194.
57. Chapman AL, Winterbourn CC, Brennan SO, Jordan TW, Kettle AJ, (2003) Characterization of non-covalent oligomers of proteins treated with hypochlorous acid. Biochem J 375: 33-40.
58. Stadtman ER, Berlett BS, (1997) Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol 10: 485-494.
59. Horwich A, (2002) Protein aggregation in disease: a role for folding intermediates forming specific multimeric interactions. J Clin Invest 110: 1221-1232.
60. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, et al. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277: 1990-1993.
61. Koo EH, Lansbury PT Jr, Kelly JW, (1999) Amyloid diseases: abnormal protein aggregation in neurodegeneration. Proc Natl Acad Sci U S A 96: 9989-9990.
62. Tahboub YR, Galijasevic S, Diamond MP, Abu-Soud HM, (2005) Thiocyanate modulates the catalytic activity of mammalian peroxidases. J Biol Chem 280: 26129-26136.
63. Adak S, Mazumdar A, Banerjee RK, (1997) Low catalytic turnover of horseradish peroxidase in thiocyanate oxidation. Evidence for concurrent inactivation by cyanide generated through one-electron oxidation of thiocyanate. J Biol Chem 272: 11049-11056.
64. Aune TM, Thomas EL, (1977) Accumulation of hypothiocyanite ion during peroxidase-catalyzed oxidation of thiocyanate ion. Eur J Biochem 80: 209-214.
65. Newman AA, (1975) Chemistry and biochemistry of thiocyanic acid and its derivatives London; New York Academic Press pp. xiv, 351.
66. Chung J, Wood JL, (1970) Oxidation of thiocyanate to cyanide and sulfate by the lactoperoxidase-hydrogen peroxide system. Arch Biochem Biophys 141: 73-78.
67. Ashby MT, Carlson AC, Scott MJ, (2004) Redox Buffering of Hypochlorous Acid by Thiocyanate in Physiologic Fluids. Journal of the American Chemical Society 126: 15976-15977.
68. Conner GE, Salathe M, Forteza R, (2002) Lactoperoxidase and hydrogen peroxide metabolism in the airway. Am J Respir Crit Care Med 166: S57-61.
69. Wijkstrom-Frei C, El-Chemaly S, Ali-Rachedi R, Gerson C, Cobas MA, et al. (2003) Lactoperoxidase and human airway host defense. Am J Respir Cell Mol Biol 29: 206-212.
70. Mertz W, Underwood EJ, (1986) Trace elements in human and animal nutrition Orlando Academic Press.
71. Gould NS, Gauthier S, Kariya CT, Min E, Huang J, et al. Hypertonic saline increases lung epithelial lining fluid glutathione and thiocyanate: two protective CFTR-dependent thiols against oxidative injury. Respir Res 11: 119.
72. Moskwa P, Lorentzen D, Excoffon KJ, Zabner J, McCray PB Jr, et al. (2007) A novel host defense system of airways is defective in cystic fibrosis. Am J Respir Crit Care Med 175: 174-183.
73. Thomson E, Brennan S, Senthilmohan R, Gangell CL, Chapman AL, et al. Identifying peroxidases and their oxidants in the early pathology of cystic fibrosis. Free Radic Biol Med 49: 1354-1360.
74. Pattison DI, Hawkins CL, Davies MJ, (2009) What are the plasma targets of the oxidant hypochlorous acid? A kinetic modeling approach. Chem Res Toxicol 22: 807-817.
75. Van Der Vliet A, Nguyen MN, Shigenaga MK, Eiserich JP, Marelich GP, et al. (2000) Myeloperoxidase and protein oxidation in cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 279: L537-546.
76. Reid DW, Anderson GJ, Lamont IL, (2008) Cystic fibrosis: ironing out the problem of infection? Am J Physiol Lung Cell Mol Physiol 295: L23-24.
77. Agbai O, (1986) Anti-sickling effect of dietary thiocyanate in prophylactic control of sickle cell anemia. J Natl Med Assoc 78: 1053-1056.
78. Pennathur S, Maitra D, Byun J, Sliskovic I, Abdulhamid I, et al. Potent antioxidative activity of lycopene: A potential role in scavenging hypochlorous acid. Free Radic Biol Med 49: 205-213.
79. Schaffer SW, Azuma J, Mozaffari M, (2009) Role of antioxidant activity of taurine in diabetes. Can J Physiol Pharmacol 87: 91-99.
80. Bouckenooghe T, Remacle C, Reusens B, (2006) Is taurine a functional nutrient? Curr Opin Clin Nutr Metab Care 9: 728-733.
81. Bolscher BG, Plat H, Wever R, (1984) Some properties of human eosinophil peroxidase, a comparison with other peroxidases. Biochim Biophys Acta 784: 177-186.
82. Carter P, (1971) Spectrophotometric determination of serum iron at the submicrogram level with a new reagent (ferrozine). Anal Biochem 40: 450-458.
83. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
84. Wang L, Bassiri M, Najafi R, Najafi K, Yang J, et al. (2007) Hypochlorous acid as a potential wound care agent: part I. Stabilized hypochlorous acid: a component of the inorganic armamentarium of innate immunity. J Burns Wounds 6: e5.
85. Furman CS, Margerum DW, (1998) Mechanism of Chlorine Dioxide and Chlorate Ion Formation from the Reaction of Hypobromous Acid and Chlorite Ion. Inorg Chem 37: 4321-4327.
86. Jantschko W, Furtmuller PG, Zederbauer M, Neugschwandtner K, Jakopitsch C, et al. (2005) Reaction of ferrous lactoperoxidase with hydrogen peroxide and dioxygen: an anaerobic stopped-flow study. Arch Biochem Biophys 434: 51-59.