Inhibition of myeloperoxidase- and neutrophil-mediated oxidant production by tetraethyl and tetramethyl nitroxides

Free Radical Biology and Medicine

Volumn 70, Issue , 2014, Pages 96-105

  Kajer, Tracey B ^a,b   Fairfull Smith, Kathryn E ^c   Yamasaki, Toshihide ^d   Yamada, Ken Ichi ^d   Fu, Shanlin ^e   Bottle, Steven E ^c   Hawkins, Clare L ^a,b   Davies, Michael J ^a,b  

^a HEART RESEARCH INSTITUTE   (Australia)

^b University of Sydney   (Australia)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^d KYUSHU UNIVERSITY   (Japan)

^e UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

Free radicals; Hypochlorous acid; Myeloperoxidase; Neutrophil; Nitroxide; Protein oxidation; Superoxide radicals

Indexed keywords

HYPOCHLOROUS ACID; MYELOPEROXIDASE; NITROXIDE; OXIDIZING AGENT; TAURINE; TETRAETHYL NITROXIDE; TOSYLCHLORAMIDE SODIUM; UNCLASSIFIED DRUG; 4-AMINO-2,2,6,6-TETRAMETHYLPIPERIDINE OXIDE; AMINE OXIDE; ANTIOXIDANT; HYDROGEN PEROXIDE; PEROXIDASE; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ARTICLE; CELL ISOLATION; CELL VIABILITY; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME INHIBITION; HUMAN; HUMAN CELL; IC 50; LEUKOCYTE ACTIVATION; NEUTROPHIL; NORMAL HUMAN; OXIDATION; PLASMA; PRIORITY JOURNAL; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DRUG EFFECTS; INFLAMMATION; METABOLISM; PATHOLOGY;

ANIMALS; ANTIOXIDANTS; CYCLIC N-OXIDES; HUMANS; HYDROGEN PEROXIDE; HYPOCHLOROUS ACID; INFLAMMATION; NEUTROPHIL ACTIVATION; NEUTROPHILS; PEROXIDASE; SUPEROXIDE DISMUTASE; SUPEROXIDES;

EID: 84896503124     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.02.011     Document Type: Article

References (67)

1. M.J. Davies Myeloperoxidase-derived oxidation: mechanisms of biological damage and its prevention J. Clin. Biochem. Nutr. 48 2011 8 19
2. M.J. Davies, C.L. Hawkins, D.I. Pattison, and M.D. Rees Mammalian heme peroxidases: from molecular mechanisms to health implications Antioxid. Redox Signaling 10 2008 1199 1234 (Pubitemid 351634397)
3. B.S. van der Veen, M.P. de Winther, and P. Heeringa Myeloperoxidase: molecular mechanisms of action and their relevance to human health and disease Antioxid. Redox Signaling 11 2009 2899 2937
4. S.J. Klebanoff, A.J. Kettle, H. Rosen, C.C. Winterbourn, and W.M. Nauseef Myeloperoxidase: a front-line defender against phagocytosed microorganisms J. Leukocyte Biol. 93 2013 185 198
5. C.C. Winterbourn, and A.J. Kettle Redox reactions and microbial killing in the neutrophil phagosome Antioxid. Redox Signaling 18 2013 642 660
6. A. Slungaard Thiocyanate mediates eosinophil peroxidase toxicity through formation of a sulfhydryl-reactive oxidant Clin. Res. 40 1992 (A715-A715)
7. A. Slungaard, and J.R. Mahoney Thiocyanate is the major substrate for eosinophil peroxidase in physiological fluids - implications for cytotoxicity J. Biol. Chem. 266 1991 4903 4910 (Pubitemid 21909440)
8. J.D. Chandler, and B.J. Day Thiocyanate: a potentially useful therapeutic agent with host defense and antioxidant properties Biochem. Pharmacol. 84 2012 1381 1387
9. D. Das, P.K. De, and R.K. Banerjee Thiocyanate, a plausible physiological electron donor of gastric peroxidase Biochem. J. 305 1995 59 64
10. M.T. Ashby Inorganic chemistry of defensive peroxidases in the human oral cavity J. Dent. Res. 87 2008 900 914
11. T.M. Aune, and E.L. Thomas Oxidation of protein sulfhydryls by products of peroxidase-catalyzed oxidation of thiocyanate ion Biochemistry 17 1978 1005 1010 (Pubitemid 8310752)
12. S.J. Nicholls, and S.L. Hazen Myeloperoxidase and cardiovascular disease Arterioscler. Thromb. Vasc. Biol. 25 2005 1102 1111 (Pubitemid 40776595)
13. E. Malle, P.G. Furtmuller, W. Sattler, and C. Obinger Myeloperoxidase: a target for new drug development? Br. J. Pharmacol. 152 2007 838 854 (Pubitemid 350100486)
14. I. Aldib, J. Soubhye, K. Zouaoui Boudjeltia, M. Vanhaeverbeek, A. Rousseau, P.G. Furtmuller, C. Obinger, F. Dufrasne, J. Neve, P. Van Antwerpen, and M. Prevost Evaluation of new scaffolds of myeloperoxidase inhibitors by rational design combined with high-throughput virtual screening J. Med. Chem. 55 2012 7208 7218
15. A.J. Kettle, C.A. Gedye, M.B. Hampton, and C.C. Winterbourn Inhibition of myeloperoxidase by benzoic acid hydrazides Biochem. J. 308 1995 559 563
16. A.J. Kettle, and C.C. Winterbourn Mechanism of inhibition of myeloperoxidase by anti-inflammatory drugs Biochem. Pharmacol. 41 1991 1485 1492
17. A.K. Tiden, T. Sjogren, M. Svensson, A. Bernlind, R. Senthilmohan, F. Auchere, H. Norman, P.O. Markgren, S. Gustavsson, S. Schmidt, S. Lundquist, L.V. Forbes, N.J. Magon, L.N. Paton, G.N. Jameson, H. Eriksson, and A.J. Kettle 2-Thioxanthines are mechanism-based inactivators of myeloperoxidase that block oxidative stress during inflammation J. Biol. Chem. 286 2011 37578 37589
18. I. Sliskovic, I. Abdulhamid, M. Sharma, and H.M. Abu-Soud Analysis of the mechanism by which tryptophan analogs inhibit human myeloperoxidase Free Radic. Biol. Med. 47 2009 1005 1013
19. B.P. Soule, F. Hyodo, K. Matsumoto, N.L. Simone, J.A. Cook, M.C. Krishna, and J.B. Mitchell The chemistry and biology of nitroxide compounds Free Radic. Biol. Med. 42 2007 1632 1650 (Pubitemid 46617154)
20. J.B. Mitchell, S. Xavier, A.M. DeLuca, A.L. Sowers, J.A. Cook, M.C. Krishna, S.M. Hahn, and A. Russo A low molecular weight antioxidant decreases weight and lowers tumour incidence Free Radic. Biol. Med. 34 2003 93 102 (Pubitemid 36043890)
21. R.F. Queiroz, A.K. Jordao, A.C. Cunha, V.F. Ferreira, M.R. Brigagao, A. Malvezzi, A.T. Amaral, and O. Augusto Nitroxides attenuate carrageenan-induced inflammation in rat paws by reducing neutrophil infiltration and the resulting myeloperoxidase-mediated damage Free Radic. Biol. Med. 53 2012 1942 1953
22. F. Karmeli, R. Eliakim, E. Okon, A. Samuni, and D. Rachmilewitz A stable nitroxide radical effectively decreases mucosal damage in experimental colitis Gut 37 1995 386 393
23. S.F. Knight, J. Yuan, S. Roy, and J.D. Imig Simvastatin and tempol protect against endothelial dysfunction and renal injury in a model of obesity and hypertension Am. J. Physiol. Renal Physiol. 298 2010 F86 F94
24. C.S. Wilcox, and A. Pearlman Chemistry and antihypertensive effects of tempol and other nitroxides Pharmacol. Rev. 60 2008 418 469
25. A. Samuni, J.B. Mitchell, W. DeGraff, C.M. Krishna, U. Samuni, and A. Russo Nitroxide SOD-mimics: modes of action Free Radic. Res. Commun. 12-13 1991 187 194
26. C.M. Krishna, and A. Samuni Nitroxides as antioxidants Methods Enzymol. 234 1994 580 589 (Pubitemid 24330331)
27. J.B. Mitchell, A. Samuni, M.C. Krishna, W.G. DeGraff, M.S. Ahn, U. Samuni, and A. Russo Biologically active metal-independent superoxide dismutase mimics Biochemistry 29 1990 2802 2807 (Pubitemid 20122615)
28. M.A. Lam, D.I. Pattison, S.E. Bottle, D.J. Keddie, and M.J. Davies Nitric oxide and nitroxides can act as efficient scavengers of protein-derived free radicals Chem. Res. Toxicol. 21 2008 2111 2119
29. D.I. Pattison, M. Lam, S.S. Shinde, R.F. Anderson, and M.J. Davies The nitroxide TEMPO is an efficient scavenger of protein radicals: cellular and kinetic studies Free Radic. Biol. Med. 53 2012 1664 1674
30. E. Linares, S. Giorgio, and O. Augusto Inhibition of in vivo leishmanicidal mechanisms by tempol: nitric oxide down-regulation and oxidant scavenging Free Radic. Biol. Med. 44 2008 1668 1676
31. C.M. Krishna, A. Samuni, J. Taira, J.A. Goldstein, J.B. Mitchell, and A. Russo Stimulation by nitroxides of catalase-like activity of heme proteins; kinetics and mechanism J. Biol. Chem. 271 1996 26018 26025 (Pubitemid 26347440)
32. B.P. Soule, F. Hyodo, K. Matsumoto, N.L. Simone, J.A. Cook, M.C. Krishna, and J.B. Mitchell Therapeutic and clinical applications of nitroxide compounds Antioxid. Redox Signaling 9 2007 1731 1743 (Pubitemid 47462975)
33. S.M. Vaz, and O. Augusto Inhibition of myeloperoxidase-mediated protein nitration by tempol: kinetics, mechanism, and implications Proc. Natl. Acad. Sci. USA 105 2008 8191 8196 (Pubitemid 351904733)
34. M.D. Rees, S.E. Bottle, K.E. Fairfull-Smith, E. Malle, J.M. Whitelock, and M.J. Davies Inhibition of myeloperoxidase-mediated hypochlorous acid production by nitroxides Biochem. J. 421 2009 79 86
35. R.F. Queiroz, S.M. Vaz, and O. Augusto Inhibition of the chlorinating activity of myeloperoxidase by tempol: revisiting the kinetics and mechanisms Biochem. J. 439 2011 423 431
36. G.G. Borisenko, I. Martin, Q. Zhao, A.A. Amoscato, and V.E. Kagan Nitroxides scavenge myeloperoxidase-catalyzed thiyl radicals in model systems and in cells J. Am. Chem. Soc. 126 2004 9221 9232 (Pubitemid 38989438)
37. T. Goffman, D. Cuscela, J. Glass, S. Hahn, C.M. Krishna, G. Lupton, and J.B. Mitchell Topical application of nitroxide protects radiation-induced alopecia in guinea pigs Int. J. Radiat. Oncol. Biol. Phys. 22 1992 803 806
38. D. Cuscela, D. Coffin, G.P. Lupton, J.A. Cook, M.C. Krishna, R.F. Bonner, and J.B. Mitchell Protection from radiation-induced alopecia with topical application of nitroxides: fractionated studies Cancer J. Sci. Am. 2 1996 273 278
39. J.F. Keana, S. Pou, and G.M. Rosen Nitroxides as potential contrast enhancing agents for MRI application: influence of structure on the rate of reduction by rat hepatocytes, whole liver homogenate, subcellular fractions, and ascorbate Magn. Reson. Med 5 1987 525 536
40. W.R. Couet, R.C. Brasch, G. Sosnovsky, and T.N. Tozer Factors affecting nitroxide reduction in ascorbate solution and tissue homogenates Magn. Reson. Imaging 3 1985 83 88 (Pubitemid 15075066)
41. I.A. Kirilyuk, A.A. Bobko, I.A. Grigorev, and V.V. Khramtsov Synthesis of the tetraethyl substituted pH-sensitive nitroxides of imidazole series with enhanced stability towards reduction Org. Biomol. Chem. 2 2004 1025 1030
42. Y. Kinoshita, K. Yamada, T. Yamasaki, F. Mito, M. Yamato, N. Kosem, H. Deguchi, C. Shirahama, Y. Ito, K. Kitagawa, N. Okukado, K. Sakai, and H. Utsumi In vivo evaluation of novel nitroxyl radicals with reduction stability Free Radic. Biol. Med. 49 2010 1703 1709
43. Y. Kinoshita, K. Yamada, T. Yamasaki, H. Sadasue, K. Sakai, and H. Utsumi Development of novel nitroxyl radicals for controlling reactivity with ascorbic acid Free Radic. Res. 43 2009 565 571
44. T. Yamasaki, F. Mito, Y. Ito, S. Pandian, Y. Kinoshita, K. Nakano, R. Murugesan, K. Sakai, H. Utsumi, and K. Yamada Structure-reactivity relationship of piperidine nitroxide: electrochemical, ESR and computational studies J. Org. Chem. 76 2011 435 440
45. J.T. Paletta, M. Pink, B. Foley, S. Rajca, and A. Rajca Synthesis and reduction kinetics of sterically shielded pyrrolidine nitroxides Org. Lett. 14 2012 5322 5325
46. P. Schattling, F.D. Jochum, and P. Theato Multi-responsive copolymers: using thermo-, light- and redox stimuli as three independent inputs towards polymeric information processing Chem. Commun. (Cambridge) 47 2011 8859 8861
47. K. Sakai, K. Yamada, T. Yamasaki, Y. Kinoshita, F. Mito, and H. Utsumi Effective 2,6-substitution of piperidine nitroxyl radical by carbonyl compound Tetrahedron 66 2010 2311 2315
48. E.L. Thomas, M.B. Grisham, and M.M. Jefferson Preparation and characterization of chloramines Methods Enzymol. 132 1986 569 585 (Pubitemid 17233604)
49. O. Skaff, D.I. Pattison, and M.J. Davies Hypothiocyanous acid reactivity with low-molecular-mass and protein thiols: absolute rate constants and assessment of biological relevance Biochem. J. 422 2009 111 117
50. P. Eyer, F. Worek, D. Kiderlen, G. Sinko, A. Stuglin, V. Simeon-Rudolf, and E. Reiner Molar absorption coefficients for the reduced Ellman reagent: reassessment Anal. Biochem. 312 2003 224 227 (Pubitemid 36151135)
51. A. Ferrante, and Y.H. Thong Optimal conditions for simultaneous purification of mononuclear and polymorphonuclear leucocytes from human blood by the Hypaque-Ficoll method J. Immunol. Methods 36 1980 109 117 (Pubitemid 10056419)
52. A.A. Bobko, I.A. Kirilyuk, I.A. Grigorev, J.L. Zweier, and V.V. Khramtsov Reversible reduction of nitroxides to hydroxylamines: roles for ascorbate and glutathione Free Radic. Biol. Med. 42 2007 404 412 (Pubitemid 46038046)
53. N. Kocherginsky, and H.M. Swartz Nitroxide Spin Labels: Reactions in Biology and Chemistry 1995 CRC Press Boca Raton
54. B.M. Babior The respiratory burst oxidase Trends Biochem. Sci. 12 1987 241 243
55. A. Samuni, C.M. Krishna, J.B. Mitchell, C.R. Collins, and A. Russo Superoxide reaction with nitroxides Free Radic. Res. Commun. 9 1990 241 249 (Pubitemid 20376777)
56. J. Fuchs, N. Groth, T. Herrling, and G. Zimmer Electron paramagnetic resonance studies on nitroxide radical 2,2,5,5-tetramethyl-4-piperidin-1-oxyl (TEMPO) redox reactions in human skin Free Radic. Biol. Med. 22 1997 967 976 (Pubitemid 27084133)
57. H. Deguchi, K. Yasukawa, T. Yamasaki, F. Mito, Y. Kinoshita, T. Naganuma, S. Sato, M. Yamato, K. Ichikawa, K. Sakai, H. Utsumi, and K. Yamada Nitroxides prevent exacerbation of indomethacin-induced gastric damage in adjuvant arthritis rats Free Radic. Biol. Med. 51 2011 1799 1805
58. K. Takeshita, A. Hamada, and H. Utsumi Mechanisms related to reduction of radical in mouse lung using an L-band ESR spectrometer Free Radic. Biol. Med 26 1999 951 960 (Pubitemid 29198367)
59. P.G. Furtmuller, M. Zederbauer, W. Jantschko, J. Helm, M. Bogner, C. Jakopitsch, and C. Obinger Active site structure and catalytic mechanisms of human peroxidases Arch. Biochem. Biophys. 445 2006 199 213 (Pubitemid 43082213)
60. A.J. Kettle, C.A. Gedye, and C.C. Winterbourn Superoxide is an antagonist of antiinflammatory drugs that inhibit hypochlorous acid production by myeloperoxidase Biochem. Pharmacol. 45 1993 2003 2010 (Pubitemid 23162595)
61. I. Fridovich Superoxide dismutases Annu. Rev. Biochem. 44 1975 147 159
62. M.C. Krishna, D.A. Grahame, A. Samuni, J.B. Mitchell, and A. Russo Oxoammonium cation intermediate in the nitroxide-catalyzed dismutation of superoxide Proc. Natl. Acad. Sci. USA 89 1992 5537 5541
63. P.G. Furtmuller, U. Burner, G. Regelsberger, and C. Obinger Spectral and kinetic studies on the formation of eosinophil peroxidase compound I and its reaction with halides and thiocyanate Biochemistry 39 2000 15578 15584 (Pubitemid 32002786)
64. G.J. Dever, R. Benson, C.L. Wainwright, S. Kennedy, and C.M. Spickett Phospholipid chlorohydrin induces leukocyte adhesion to ApoE-/- mouse arteries via upregulation of P-selectin Free Radic. Biol. Med. 44 2008 452 463
65. J.M. Pullar, C.C. Winterbourn, and M.C. Vissers The effect of hypochlorous acid on the expression of adhesion molecules and activation of NF-kappaB in cultured human endothelial cells Antioxid. Redox Signaling 4 2002 5 15 (Pubitemid 34260681)
66. J.L. Hodgson, M. Namazian, S.E. Bottle, and M.L. Coote One-electron oxidation and reduction potentials of nitroxide antioxidants: a theoretical study J. Phys. Chem. A 111 2007 13595 13605
67. J.P. Blinco, J.L. Hodgson, B.J. Morrow, J.R. Walker, G.D. Will, M.L. Coote, and S.E. Bottle Experimental and theoretical studies of the redox potentials of cyclic nitroxides J. Org. Chem. 73 2008 6763 6771