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Mediators of Inflammation
Volume 2013, Article ID 710239, 14 pages
http://dx.doi.org/10.1155/2013/710239
Research Article

Flavonoids and 5-Aminosalicylic Acid Inhibit the Formation of Neutrophil Extracellular Traps

1Institute for Medical Microbiology and Hygiene, University of Lübeck, Ratzeburger Allee 160, 23538 Lübeck, Germany
2Institute of Anatomy, University of Lübeck, Ratzeburger Allee 160, 23538 Lübeck, Germany

Received 16 August 2013; Revised 18 October 2013; Accepted 30 October 2013

Academic Editor: Magdalena Klink

Copyright © 2013 Tina Kirchner et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Nathan, “Neutrophils and immunity: challenges and opportunities,” Nature Reviews Immunology, vol. 6, no. 3, pp. 173–182, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Brinkmann and A. Zychlinsky, “Neutrophil extracellular traps: is immunity the second function of chromatin?” The Journal of Cell Biology, vol. 198, no. 5, pp. 773–783, 2012. View at Google Scholar
  3. T. A. Fuchs, U. Abed, C. Goosmann et al., “Novel cell death program leads to neutrophil extracellular traps,” Journal of Cell Biology, vol. 176, no. 2, pp. 231–241, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Kirchner, S. M. Möller, M. Klinger et al., “The impact of various reactive oxygen species on the formation of neutrophil extracellular traps,” Mediators of Inflammation, vol. 2012, Article ID 849136, 10 pages, 2012. View at Publisher · View at Google Scholar
  5. H. Parker, M. Dragunow, M. B. Hampton, A. J. Kettle, and C. C. Winterbourn, “Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus,” Journal of Leukocyte Biology, vol. 92, no. 4, pp. 841–849, 2012. View at Publisher · View at Google Scholar
  6. H. Parker and C. C. Winterbourn, “Reactive oxidants and myeloperoxidase and their involvement in neutrophil extracellular traps,” Frontiers in Immunology, vol. 3, p. 424, 2013. View at Google Scholar
  7. R. S. Keshari, A. Jyoti, S. Kumar et al., “Neutrophil extracellular traps contain mitochondrial as well as nuclear DNA and exhibit inflammatory potential,” Cytometry A, vol. 81, no. 3, pp. 238–247, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. Q. Remijsen, T. V. Berghe, E. Wirawan et al., “Neutrophil extracellular trap cell death requires both autophagy and superoxide generation,” Cell Research, vol. 21, no. 2, pp. 290–304, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. L. J. Palmer, P. R. Cooper, M. R. Ling, H. J. Wright, A. Huissoon, and I. L. C. Chapple, “Hypochlorous acid regulates neutrophil extracellular trap release in humans,” Clinical and Experimental Immunology, vol. 167, no. 2, pp. 261–268, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. V. Papayannopoulos, K. D. Metzler, A. Hakkim, and A. Zychlinsky, “Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps,” Journal of Cell Biology, vol. 191, no. 3, pp. 677–691, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Gabriel, W. R. McMaster, D. Girard, and A. Descoteaux, “Leishmania donovani promastigotes evade the antimicrobial activity of neutrophil extracellular traps,” Journal of Immunology, vol. 185, no. 7, pp. 4319–4327, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Farley, J. M. . Stolley, P. Zhao, J. Cooley, and E. R. O’Donnell, “A serpinB1 regulatory mechanism is essential for restricting neutrophil extracellular trap generation,” The Journal of Immunology, vol. 189, no. 9, pp. 4574–4581, 2012. View at Publisher · View at Google Scholar
  13. F. H. Pilsczek, D. Salina, K. K. H. Poon et al., “A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus,” Journal of Immunology, vol. 185, no. 12, pp. 7413–7425, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Saffarzadeh and K. T. Preissner, “Fighting against the dark side of neutrophil extracellular traps in disease: manoeuvres for host protection,” Current Opinion in Hematology, vol. 20, no. 1, pp. 3–9, 2013. View at Google Scholar
  15. Y. Nishinaka, T. Arai, S. Adachi, A. Takaori-Kondo, and K. Yamashita, “Singlet oxygen is essential for neutrophil extracellular trap formation,” Biochemical and Biophysical Research Communications, vol. 413, no. 1, pp. 75–79, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Khandpur, C. Carmona-Rivera, A. Vivekanandan-Giri et al., “NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis,” Science Translational Medicine, vol. 5, no. 178, Article ID 178ra40, 2013. View at Publisher · View at Google Scholar
  17. G. S. Garcia-Romo, S. Caielli, B. Vega et al., “Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus,” Science Translational Medicine, vol. 3, no. 73, Article ID 73ra20, 2011. View at Publisher · View at Google Scholar
  18. C. Riganti, E. Gazzano, M. Polimeni, C. Costamagna, A. Bosia, and D. Ghigo, “Diphenyleneiodonium inhibits the cell redox metabolism and induces oxidative stress,” The Journal of Biological Chemistry, vol. 279, no. 46, pp. 47726–47731, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. M. J. Lapponi, A. Carestia, V. I. Landoni et al., “Regulation of neutrophil extracellular trap formation by anti-inflammatory drugs,” Journal of Pharmacology and Experimental Therapeutics, vol. 345, no. 3, pp. 430–437, 2013. View at Publisher · View at Google Scholar
  20. A. Hosseinzadeh, P. K. Messer, and C. F. Urban, “Stable redox-cycling nitroxide tempol inhibits NET formation,” Frontiers in Immunology, vol. 3, p. 391, 2012. View at Google Scholar
  21. C. Schorn et al., “Bonding the foe—NETting neutrophils immobilize the pro-inflammatory monosodium urate crystals,” Frontiers in Immunology, vol. 3, p. 376, 2012. View at Google Scholar
  22. S. Patel, S. Kumar, A. Jyoti et al., “Nitric oxide donors release extracellular traps from human neutrophils by augmenting free radical generation,” Nitric Oxide, vol. 22, no. 3, pp. 226–234, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. A. J. Kettle and C. C. Winterbourn, “Mechanism of inhibition of myeloperoxidase by anti-inflammatory drugs,” Biochemical Pharmacology, vol. 41, no. 10, pp. 1485–1492, 1991. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Shiba, T. Kinoshita, H. Chuman et al., “Flavonoids as substrates and inhibitors of myeloperoxidase: molecular actions of aglycone and metabolites,” Chemical Research in Toxicology, vol. 21, no. 8, pp. 1600–1609, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Tamai, J. F. Kachur, M. B. Grisham, and T. S. Gaginella, “Scavenging effect of 5-aminosalicylic acid on neutrophil-derived oxidants. Possible contribution to the mechanism of action in inflammatory bowel disease,” Biochemical Pharmacology, vol. 41, no. 6-7, pp. 1001–1006, 1991. View at Google Scholar · View at Scopus
  26. N. Parij, A.-M. Nagy, P. Fondu, and J. Nève, “Effects of non-steroidal anti-inflammatory drugs on the luminol and lucigenin amplified chemiluminescence of human neutrophils,” European Journal of Pharmacology, vol. 352, no. 2-3, pp. 299–305, 1998. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Peake and K. Suzuki, “Neutrophil activation, antioxidant supplements and exercise-induced oxidative stress,” Exercise Immunology Review, vol. 10, pp. 129–141, 2004. View at Google Scholar · View at Scopus
  28. R. J. Reiter, D.-X. Tan, J. C. Mayo, R. M. Sainz, J. Leon, and Z. Czarnocki, “Melatonin as an antioxidant: biochemical mechanisms and pathophysiological implications in humans,” Acta Biochimica Polonica, vol. 50, no. 4, pp. 1129–1146, 2003. View at Google Scholar · View at Scopus
  29. E. Aga, D. M. Katschinski, G. Van Zandbergen et al., “Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major,” Journal of Immunology, vol. 169, no. 2, pp. 898–905, 2002. View at Google Scholar · View at Scopus
  30. P. Stevens and D. Hong, “The role of myeloperoxidase and superoxide anion in the luminol- and lucigenin-dependent chemiluminescence of human neutrophils,” Microchemical Journal, vol. 30, no. 2, pp. 135–146, 1984. View at Google Scholar · View at Scopus
  31. H. Gyllenhammar, “Lucigenin chemiluminescence in the assessment of neutrophil superoxide production,” Journal of Immunological Methods, vol. 97, no. 2, pp. 209–213, 1987. View at Google Scholar · View at Scopus
  32. F. Caldefie-Chézet, S. Walrand, C. Moinard, A. Tridon, J. Chassagne, and M.-P. Vasson, “Is the neutrophil reactive oxygen species production measured by luminol and lucigenin chemiluminescence intra or extracellular? Comparison with DCFH-DA flow cytometry and cytochrome c reduction,” Clinica Chimica Acta, vol. 319, no. 1, pp. 9–17, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. V. Brinkmann, U. Reichard, C. Goosmann et al., “Neutrophil extracellular traps kill bacteria,” Science, vol. 303, no. 5663, pp. 1532–1535, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Bianchi, A. Hakkim, V. Brinkmann et al., “Restoration of NET formation by gene therapy in CGD controls aspergillosis,” Blood, vol. 114, no. 13, pp. 2619–2622, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. M. B. H. Lim, J. W. P. Kuiper, A. Katchky, H. Goldberg, and M. Glogauer, “Rac2 is required for the formation of neutrophil extracellular traps,” Journal of Leukocyte Biology, vol. 90, no. 4, pp. 771–776, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. O. H. Nielsen, P. N. Bouchelouche, D. Berild, and I. Ahnfelt-Ronne, “Effect of 5-aminosalicylic acid and analogous substances on superoxide generation and intracellular free calcium in human neutrophilic granulocytes,” Scandinavian Journal of Gastroenterology, vol. 28, no. 6, pp. 527–532, 1993. View at Google Scholar · View at Scopus
  37. P. Washko, D. Rotrosen, and M. Levine, “Ascorbic acid in human neutrophils,” American Journal of Clinical Nutrition, vol. 54, supplement 6, 1991. View at Google Scholar · View at Scopus
  38. L. Selloum, H. Bouriche, C. Tigrine, and C. Boudoukha, “Anti-inflammatory effect of rutin on rat paw oedema, and on neutrophils chemotaxis and degranulation,” Experimental and Toxicologic Pathology, vol. 54, no. 4, pp. 313–318, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Kirchner, J. Flemmig, P. G. Furtmüller, C. Obinger, and J. Arnhold, “(-)-Epicatechin enhances the chlorinating activity of human myeloperoxidase,” Archives of Biochemistry and Biophysics, vol. 495, no. 1, pp. 21–27, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. Z. Varga, E. Kosaras, E. Komodi et al., “Effects of tocopherols and 2,2′-carboxyethyl hydroxychromans on phorbol-ester-stimulated neutrophils,” Journal of Nutritional Biochemistry, vol. 19, no. 5, pp. 320–327, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Pieri, R. Recchioni, F. Moroni et al., “Melatonin regulates the respiratory burst of human neutrophils and their depolarization,” Journal of Pineal Research, vol. 24, no. 1, pp. 43–49, 1998. View at Publisher · View at Google Scholar · View at Scopus
  42. C. H. E. Homburg, M. De Haas, A. E. G. K. Von dem Borne, A. J. Verhoeven, C. P. M. Reutelingsperger, and D. Roos, “Human neutrophils lose their surface FcγRIII and acquire Annexin V binding sites during apoptosis in vitro,” Blood, vol. 85, no. 2, pp. 532–540, 1995. View at Google Scholar · View at Scopus
  43. B. C. Dickinson and C. J. Chang, “Chemistry and biology of reactive oxygen species in signaling or stress responses,” Nature Chemical Biology, vol. 7, no. 8, pp. 504–511, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Sakai, J. Li, K. K. Subramanian et al., “Reactive oxygen species-induced actin glutathionylation controls actin dynamics in neutrophils,” Immunity, vol. 37, no. 6, pp. 1037–1049, 2012. View at Publisher · View at Google Scholar
  45. K. D. Metzler, T. A. Fuchs, W. M. Nauseef et al., “Myeloperoxidase is required for neutrophil extracellular trap formation: implications for innate immunity,” Blood, vol. 117, no. 3, pp. 953–959, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Ciz, P. Denev, M. Kratchanova et al., “Flavonoids inhibit the respiratory burst of neutrophils in mammals,” Oxidative Medicine and Cellular Longevity, vol. 2012, Article ID 181295, 6 pages, 2012. View at Publisher · View at Google Scholar
  47. M. Suzuki, K. Yoshino, M. Maeda-Yamamoto, T. Miyase, and M. Sano, “Inhibitory effects of tea catechins and O-methylated derivatives of (-)-epigallocatechin-3-O-gallate on mouse type IV allergy,” Journal of Agricultural and Food Chemistry, vol. 48, no. 11, pp. 5649–5653, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Kawai, Y. Matsui, H. Kondo et al., “Galloylated catechins as potent inhibitors of hypochlorous acid-induced DNA damage,” Chemical Research in Toxicology, vol. 21, no. 7, pp. 1407–1414, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. A. I. Tauber, J. R. Fay, and M. A. Marletta, “Flavonoid inhibition of the human neutrophil NADPH-oxidase,” Biochemical Pharmacology, vol. 33, no. 8, pp. 1367–1369, 1984. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Nishikawa, K. Wakano, and S. Kitani, “Inhibition of NADPH oxidase subunits translocation by tea catechin EGCG in mast cell,” Biochemical and Biophysical Research Communications, vol. 362, no. 2, pp. 504–509, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. P. C. Vasconcelos, L. N. Seito, L. C. Di Stasi et al., “Epicatechin used in the treatment of intestinal inflammatory disease: an analysis by experimental models,” Evidence-Based Complementary and Alternative Medicine, vol. 2012, Article ID 508902, 12 pages, 2012. View at Publisher · View at Google Scholar
  52. L. Selloum, S. Reichl, M. Müller, L. Sebihi, and J. Arnhold, “Effects of flavonols on the generation of superoxide anion radicals by xanthine oxidase and stimulated neutrophils,” Archives of Biochemistry and Biophysics, vol. 395, no. 1, pp. 49–56, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. M. G. Traber and J. F. Stevens, “Vitamins C and E: beneficial effects from a mechanistic perspective,” Free Radical Biology and Medicine, vol. 51, no. 5, pp. 1000–1013, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. E. Niki, “Action of ascorbic acid as a scavenger of active and stable oxygen radicals,” American Journal of Clinical Nutrition, vol. 54, supplement 6, p. 1119S, 1991. View at Google Scholar · View at Scopus
  55. M. Chatterjee, R. Saluja, V. Kumar et al., “Ascorbate sustains neutrophil NOS expression, catalysis, and oxidative burst,” Free Radical Biology and Medicine, vol. 45, no. 8, pp. 1084–1093, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. I. L. Chapple et al., “Ascorbate and alpha-tocopherol differentially modulate reactive oxygen species generation by neutrophils in response to FcgammaR and TLR agonists,” Innate Immunity, vol. 19, no. 2, pp. 152–159, 2012. View at Google Scholar
  57. A. V. Peskin and C. C. Winterbourn, “Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine, and ascorbate,” Free Radical Biology and Medicine, vol. 30, no. 5, pp. 572–579, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. A. C. Carr, M. R. McCall, and B. Frei, “Oxidation of LDL by myeloperoxidase and reactive nitrogen species: reaction pathways and antioxidant protection,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 20, no. 7, pp. 1716–1723, 2000. View at Google Scholar · View at Scopus
  59. L. A. Marquez, H. B. Dunford, and H. Van Wart, “Kinetic studies on the reaction of compound II of myeloperoxidase with ascorbic acid. Role of ascorbic acid in myeloperoxidase function,” The Journal of Biological Chemistry, vol. 265, no. 10, pp. 5666–5670, 1990. View at Google Scholar · View at Scopus
  60. L. Harper, S. L. Nuttall, U. Martin, and C. O. S. Savage, “Adjuvant treatment of patients with antineutrophil cytoplasmic antibody-associated vasculitis with vitamins E and C reduces superoxide production by neutrophils,” Rheumatology, vol. 41, no. 3, pp. 274–278, 2002. View at Google Scholar · View at Scopus
  61. S. Z. Samsam Shariat, S. A. Mostafavi, and F. Khakpour, “Antioxidant effects of vitamins C and e on the low-density lipoprotein oxidation mediated by myeloperoxidase,” Iranian Biomedical Journal, vol. 17, no. 1, pp. 22–28, 2013. View at Google Scholar
  62. M. G. Traber and J. Atkinson, “Vitamin E, antioxidant and nothing more,” Free Radical Biology and Medicine, vol. 43, no. 1, pp. 4–15, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. S. B. Hanauer and D. H. Present, “The state of the art in the management of inflammatory bowel disease,” Reviews in Gastroenterological Disorders, vol. 3, no. 2, pp. 81–92, 2003. View at Google Scholar · View at Scopus
  64. B. M. Fournier and C. A. Parkos, “The role of neutrophils during intestinal inflammation,” Mucosal Immunology, vol. 5, no. 4, pp. 354–366, 2012. View at Google Scholar
  65. S. Yousefi, J. A. Gold, N. Andina et al., “Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense,” Nature Medicine, vol. 14, no. 9, pp. 949–953, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. A. S. Savchenko, A. Inoue, R. Ohashi et al., “Long pentraxin 3 (PTX3) expression and release by neutrophils in vitro and in ulcerative colitis,” Pathology International, vol. 61, no. 5, pp. 290–297, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. T. Magrone and E. Jirillo, “Mechanisms of neutrophil-mediated disease: innovative therapeutic interventions,” Current Pharmaceutical Design, vol. 18, no. 12, pp. 1609–1619, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. H. Allgayer, S. Rang, U. Klotz et al., “Superoxide inhibition following different stimuli of respiratory burst and metabolism of aminosalicylates in neutrophils,” Digestive Diseases and Sciences, vol. 39, no. 1, pp. 145–151, 1994. View at Google Scholar · View at Scopus
  69. N. A. Punchard, S. M. Greenfield, and R. P. Thompson, “Mechanism of action of 5-arninosalicylic acid,” Mediators of Inflammation, vol. 1, no. 3, pp. 151–165, 1992. View at Google Scholar
  70. C. Von Ritter, M. B. Grisham, and D. N. Granger, “Sulfasalazine metabolites and dapsone attenuate formyl-methionyl-leucyl-phenylalanine-induced mucosal injury in rat ileum,” Gastroenterology, vol. 96, no. 3, pp. 811–816, 1989. View at Google Scholar · View at Scopus
  71. J. G. Williams and M. B. Hallett, “Effect of sulphasalazine and its active metabolite, 5-amino-salicylic acid, on toxic oxygen metabolite production by neutrophils,” Gut, vol. 30, no. 11, pp. 1581–1587, 1989. View at Google Scholar · View at Scopus
  72. M. T. Baltazar, R. J. Dinis-Oliveira, J. A. Duarte, M. L. Bastos, and F. Carvalho, “Antioxidant properties and associated mechanisms of salicylates,” Current Medicinal Chemistry, vol. 18, no. 21, pp. 3252–3264, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. J. Milara, G. Juan, T. Peiró, A. Serrano, and J. Cortijo, “Neutrophil activation in severe, early-onset COPD patients versus healthy non-smoker subjects in vitro: effects of antioxidant therapy,” Respiration, vol. 83, no. 2, pp. 147–158, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. F. Vanderbist, P. Maes, and J. Nève, “In vitro comparative assessment of the antioxidant activity of nacystelyn against three reactive oxygen species,” Arzneimittel-Forschung, vol. 46, no. 8, pp. 783–788, 1996. View at Google Scholar · View at Scopus
  75. P. Van Antwerpen, K. Z. Boudjeltia, S. Babar et al., “Thiol-containing molecules interact with the myeloperoxidase/H2O2/chloride system to inhibit LDL oxidation,” Biochemical and Biophysical Research Communications, vol. 337, no. 1, pp. 82–88, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. O. I. Aruoma, B. Halliwell, B. M. Hoey, and J. Butler, “The antioxidant action of taurine, hypotaurine and their metabolic precursors,” Biochemical Journal, vol. 256, no. 1, pp. 251–255, 1988. View at Google Scholar · View at Scopus
  77. O. I. Aruoma, B. Halliwell, B. M. Hoey, and J. Butler, “The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid,” Free Radical Biology and Medicine, vol. 6, no. 6, pp. 593–597, 1989. View at Google Scholar · View at Scopus
  78. S. Tobwala and N. Ercal, “N-Acetylcysteine Amide (NACA), a novel GSH Prodrug: its metabolism and implication in health,” in Glutathione: Biochemistry, Mechanisms of Action and Biotechnological Implications, N. Labrou and E. Flemetakis, Eds., pp. 111–142, Nova Science, 2013. View at Google Scholar
  79. U. Burner, W. Jantschko, and C. Obinger, “Kinetics of oxidation of aliphatic and aromatic thiols by myeloperoxidase compounds I and II,” FEBS Letters, vol. 443, no. 3, pp. 290–296, 1999. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Umeki, “Effects of non-steroidal anti-inflammatory drugs on human neutrophil NADPH oxidase in both whole cell and cell-free systems,” Biochemical Pharmacology, vol. 40, no. 3, pp. 559–564, 1990. View at Publisher · View at Google Scholar · View at Scopus
  81. X. Shi, M. Ding, Z. Dong et al., “Antioxidant properties of aspirin: characterization of the ability of aspirin to inhibit silica-induced lipid peroxidation, DNA damage, NF-κB activation, and TNF-α production,” Molecular and Cellular Biochemistry, vol. 199, no. 1-2, pp. 93–102, 1999. View at Publisher · View at Google Scholar · View at Scopus
  82. A. L. Sagone Jr. and R. M. Husney, “Oxidation of salicylates by stimulated granulocytes: evidence that these drugs act as free radical scavengers in biological systems,” Journal of Immunology, vol. 138, no. 7, pp. 2177–2183, 1987. View at Google Scholar · View at Scopus
  83. K.-A. Marshall, R. J. Reiter, B. Poeggeler, O. I. Aruoma, and B. Halliwell, “Evaluation of the antioxidant activity of melatonin in vitro,” Free Radical Biology and Medicine, vol. 21, no. 3, pp. 307–315, 1996. View at Publisher · View at Google Scholar · View at Scopus
  84. V. F. Ximenes, S. O. De Silva, M. R. Rodrigues et al., “Superoxide-dependent oxidation of melatonin by myeloperoxidase,” The Journal of Biological Chemistry, vol. 280, no. 46, pp. 38160–38169, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Galijasevic, I. Abdulhamid, and H. M. Abu-Soud, “Melatonin is a potent inhibitor for myeloperoxidase,” Biochemistry, vol. 47, no. 8, pp. 2668–2677, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. C. Keithahn and A. Lerchl, “5-Hydroxytryptophan is a more potent in vitro hydroxyl radical scavenger than melatonin or vitamin C,” Journal of Pineal Research, vol. 38, no. 1, pp. 62–66, 2005. View at Publisher · View at Google Scholar · View at Scopus