High plasma thiocyanate levels modulate protein damage induced by myeloperoxidase and perturb measurement of 3-chlorotyrosine

Free Radical Biology and Medicine

Volumn 53, Issue 1, 2012, Pages 20-29

  Talib, Jihan ^a   Pattison, David I ^a,b   Harmer, Jason A ^a,c   Celermajer, David S ^a,c   Davies, Michael J ^a,b  

^a HEART RESEARCH INSTITUTE   (Australia)

^b University of Sydney   (Australia)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

Author keywords

3 Chlorotyrosine; Free radicals; Hypochlorous acid; Hypothiocyanous acid; Myeloperoxidase; Protein oxidation; Smoking; Thiocyanate

Indexed keywords

3 CHLOROTYROSINE; HISTIDINE; LYSINE; METHIONINE; MYELOPEROXIDASE; PROTEIN; THIOCYANATE; TRYPTOPHAN; TYROSINE;

AMINO ACID ANALYSIS; AMINO ACID BLOOD LEVEL; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; RISK FACTOR; SMOKING;

BIOLOGICAL MARKERS; BLOOD PROTEINS; CASE-CONTROL STUDIES; FEMALE; HUMANS; MALE; OXIDANTS; OXIDATION-REDUCTION; PEROXIDASE; SMOKING; SULFHYDRYL COMPOUNDS; THIOCYANATES; TYROSINE;

EID: 84861541509     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.04.018     Document Type: Article

References (71)

1. World Health Organisation Report of the global tobacco epidemic 2011 WHO Geneva
2. C.J. ODonnell, and W.B. Kannel Epidemiology of atherosclerotic vascular disease P.T. Lanzer, E.J. Topel, Panvascular Medicine 2003 Springer-Verlag Berlin
3. K. Yamagishi, H. Iso, A. Kitamura, T. Sankai, T. Tanigawa, Y. Naito, S. Sato, H. Imano, T. Ohira, and T. Shimamoto Smoking raises the risk of total and ischemic strokes in hypertensive men Hypertens. Res. 26 2003 209 217
4. S. Chelland Campbell, R.J. Moffatt, and B.A. Stamford Smoking and smoking cessation - the relationship between cardiovascular disease and lipoprotein metabolism: a review Atherosclerosis 201 2008 225 235
5. P. Libby, P.M. Ridker, and A. Maseri Inflammation and atherosclerosis Circulation 105 2002 1135 1143
6. T.S. Perlstein, and R.T. Lee Smoking, metalloproteinases, and vascular disease Arterioscler. Thromb. Vasc. Biol. 26 2006 250 256
7. E.A. Bermudez, N. Rifai, J.E. Buring, J.E. Manson, and P.M. Ridker Relation between markers of systemic vascular inflammation and smoking in women Am. J. Cardiol. 89 2002 1117 1119
8. M. Reilly, N. Delanty, J.A. Lawson, and G.A. FitzGerald Modulation of oxidant stress in vivo in chronic cigarette smokers Circulation 94 1996 19 25
9. E.A. Jaimes, E.G. DeMaster, R.X. Tian, and L. Raij Stable compounds of cigarette smoke induce endothelial superoxide anion production via NADPH oxidase activation Arterioscler. Thromb. Vasc. Biol. 24 2004 1031 1036
10. Z. Wang, S.J. Nicholls, E.R. Rodriguez, O. Kummu, S. Horkko, J. Barnard, W.F. Reynolds, E.J. Topol, J.A. DiDonato, and S.L. Hazen Protein carbamylation links inflammation, smoking, uremia and atherogenesis Nat. Med 13 2007 1176 1184
11. A. Spagnolo, S. Torsello, G. Morisi, E. Petrozzi, R. Antonini, G. Ricci, G.C. Urbinati, and A. Menotti Serum thiocyanate levels as an objective measure of smoking habits in epidemiological studies Eur. J. Epidemiol. 4 1988 206 211
12. P.E. Morgan, D.I. Pattison, J. Talib, F.A. Summers, J.A. Harmer, D.S. Celermajer, C.L. Hawkins, and M.J. Davies High plasma thiocyanate levels in smokers are a key determinant of thiol oxidation induced by myeloperoxidase Free Radic. Biol. Med. 51 2011 1815 1822
13. A. Daugherty, J.L. Dunn, D.L. Rateri, and J.W. Heinecke Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions J. Clin. Invest. 94 1994 437 444
14. T.K. Rudolph, V. Rudolph, and S. Baldus Contribution of myeloperoxidase to smoking-dependent vascular inflammation Proc. Am. Thorac. Soc 5 2008 820 823
15. 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
16. 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
17. S.J. Nicholls, and S.L. Hazen Myeloperoxidase and cardiovascular disease Arterioscler. Thromb. Vasc. Biol. 25 2005 1102 1111
18. C.J. van Dalen, M.W. Whitehouse, C.C. Winterbourn, and A.J. Kettle Thiocyanate and chloride as competing substrates for myeloperoxidase Biochem. J. 327 1997 487 492
19. S.L. Hazen, and J.W. Heinecke 3-Chlorotyrosine, a specific marker of myeloperoxidase-catalysed oxidation, is markedly elevated in low density lipoprotein isolated from human atherosclerotic intima J. Clin. Invest 99 1997 2075 2081
20. S.L. Hazen, 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 1996 23080 23088
21. H. Buss, R. Senthilmohan, B.A. Darlow, N. Mogridge, A.J. Kettle, and C.C. Winterbourn 3-Chlorotyrosine as a marker of protein damage by myeloperoxidase in traceal aspirates from preterm infants: association with adverse respiratory outcome Pediatr. Res. 53 2003 455 462
22. C.C. Winterbourn, and A.J. Kettle Biomarkers of myeloperoxidase-derived hypochlorous acid Free Radic. Biol. Med. 29 2000 403 409
23. B. Shao, C. Bergt, X. Fu, P. Green, J.C. Voss, M.N. Oda, J.F. Oram, and J.W. Heinecke Tyrosine 192 in apolipoprotein A-I is the major site of nitration and chlorination by myeloperoxidase, but only chlorination markedly impairs ABCA1-dependent cholesterol transport J. Biol. Chem. 280 2005 5983 5993
24. C.L. Hawkins The role of hypothiocyanous acid (HOSCN) in biological systems Free Radic. Res. 43 2009 1147 1158
25. T.P. Botti, H. Amin, L. Hiltscher, and R.W. Wissler A comparison of the quantitation of macrophage foam cell populations and the extent of apolipoprotein E deposition in developing atherosclerotic lesions in young people: high and low serum thiocyanate groups as an indication of smoking Atherosclerosis 124 1996 191 202
26. C.E.O. Scanlon, B. Berger, G. Malcom, and R.W. Wissler Evidence for more extensive deposits of epitopes of oxidized low density lipoproteins in aortas of young people with elevated serum thiocyanate levels Atherosclerosis 121 1996 23 33
27. M. Holzer, M. Gauster, T. Pfeifer, C. Wadsack, G. Fauler, P. Stiegler, H. Koefeler, E. Beubler, R. Schuligoi, A. Heinemann, and G. Marsche Protein carbamylation renders high-density lipoprotein dysfunctional Antioxid. Redox Signaling 14 2011 2337 2346
28. D.I. Pattison, and M.J. Davies Reactions of myeloperoxidase-derived oxidants with biological substrates: gaining insight into human inflammatory diseases Curr. Med. Chem. 13 2006 3271 3290
29. 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
30. P. Nagy, G.N. Jameson, and C.C. Winterbourn Kinetics and mechanisms of the reaction of hypothiocyanous acid with 5-thio-2-nitrobenzoic acid and reduced glutathione Chem. Res. Toxicol 22 2009 1833 1840
31. O. Skaff, D.I. Pattison, P.E. Morgan, R. Bachana, V.K. Jain, K.I. Priyadarsini, and M.J. Davies Selenium-containing amino acids are major targets for myeloperoxidase-derived hypothiocyanous acid: determination of absolute rate constants and implications for biological damage Biochem. J. 441 2012 305 316
32. Pattison, D.I.; Davies, M.J.; Hawkins, C.L. Reactions and reactivity of myeloperoxidase-derived oxidants: differential biological effects of hypochlorous and hypothiocyanous acids. Free Radic. Res., 10.3109/10715762.2012. 667566, in press.
33. S.E. Moriarty-Craige, and D.P. Jones Extracellular thiols and thiol/disulfide redox in metabolism Annu. Rev. Nutr. 24 2004 481 509
34. S. Ashfaq, J.L. Abramson, D.P. Jones, S.D. Rhodes, W.S. Weintraub, W.C. Hooper, V. Vaccarino, D.G. Harrison, and A.A. Quyyumi The relationship between plasma levels of oxidized and reduced thiols and early atherosclerosis in healthy adults J. Am. Coll. Cardiol. 47 2006 1005 1111
35. J.P. Gaut, J. Byun, H.D. Tran, and J.W. Heinecke Artifact-free quantification of free 3-chlorotyrosine, 3-bromotyrosine, and 3-nitrotyrosine in human plasma by electron capture-negative chemical ionization gas chromatography mass spectrometry and liquid chromatography-electrospray ionization tandem mass spectrometry Anal. Biochem 300 2002 252 259
36. J.W. Heinecke, F.F. Hsu, J.R. Crowley, S.L. Hazen, C. Leeuwenburgh, D.M. Mueller, J.E. Rasmussen, and J. Turk Detecting oxidative modification of biomolecules with isotope dilution mass spectrometry: sensitive and quantitative assays for oxidized amino acids in proteins and tissues Methods Enzymol. 300 1999 124 144
37. C.L. Hawkins, P.E. Morgan, and M.J. Davies Quantification of protein modification by oxidants Free Radic. Biol. Med. 46 2009 965 988
38. A. Vivekanandan-Giri, J. Byun, and S. Pennathur Quantification analysis of amino acid oxidation markers by tandem mass spectrometry Methods Enzymol. 491 2011 75 87
39. D.I. Pattison, C.L. Hawkins, and M.J. Davies What are the plasma targets of the oxidant hypochlorous acid? A kinetic modeling approach Chem. Res. Toxicol. 22 2009 807 817
40. C.L. Hawkins, D.I. Pattison, N.R. Stanley, and M.J. Davies Tryptophan residues are targets in hypothiocyanous acid-mediated protein oxidation Biochem. J. 414 2008 271 280
41. A.J. Kettle Neutrophils convert tyrosyl residues in albumin to chlorotyrosine FEBS Lett 379 1996 103 106
42. A.A. Woods, S.M. Linton, and M.J. Davies Detection of HOCl-mediated protein oxidation products in the extracellular matrix of human atherosclerotic plaques Biochem. J. 370 2003 729 735
43. C.L. Hawkins, and M.J. Davies Hypochlorite-induced damage to proteins: formation of nitrogen-centred radicals from lysine residues and their role in protein fragmentation Biochem. J 332 1998 617 625
44. C.L. Hawkins, and M.J. Davies Hypochlorite-induced oxidation of proteins in plasma: formation of chloramines and nitrogen-centred radicals and their role in protein fragmentation Biochem. J 340 1999 539 548
45. M.J. Davies Myeloperoxidase-derived oxidation: mechanisms of biological damage and its prevention J. Clin. Biochem. Nutr. 48 2011 8 19
46. J. Wilson Cyanide in human disease: a review of clinical and laboratory evidence Fundam. Appl. Toxicol. 3 1983 397 399
47. P.G. Furtmuller, U. Burner, and C. Obinger Reaction of myeloperoxidase compound I with chloride, bromide, iodide, and thiocyanate Biochemistry 37 1998 17923 17930
48. 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
49. H.E. Roxborough, and I.S. Young Carbamylation of proteins and atherogenesis in renal failure Med. Hypotheses 45 1995 125 128
50. S. Horkko, M.J. Savolainen, K. Kervinen, and Y.A. Kesaniemi Carbamylation-induced alterations in low-density lipoprotein metabolism Kidney Int. 41 1992 1175 1181
51. E. Ok, A.G. Basnakian, E.O. Apostolov, Y.M. Barri, and S.V. Shah Carbamylated low-density lipoprotein induces death of endothelial cells: a link to atherosclerosis in patients with kidney disease Kidney Int. 68 2005 173 178
52. G.R. Stark Reactions of cyanate with functional groups of proteins. III. Reactions with amino and carboxyl groups Biochemistry 4 1965 1030 1036
53. M.T. Ashby, A.C. Carlson, and M.J. Scott Redox buffering of hypochlorous acid by thiocyanate in physiologic fluids J. Am. Chem. Soc. 126 2004 15976 15977
54. P. Nagy, J.L. Beal, and M.T. Ashby Thiocyanate is an efficient endogenous scavenger of the phagocytic killing agent hypobromous acid Chem. Res. Toxicol 19 2006 587 593
55. Y. Xu, S. Szep, and Z. Lu The antioxidant role of thiocyanate in the pathogenesis of cystic fibrosis and other inflammation-related diseases Proc. Natl. Acad. Sci. USA 106 2009 20515 20519
56. P.N. Okafor, C.O. Okorowkwo, and E.N. Maduagwu Occupational and dietary exposures of humans to cyanide poisoning from large-scale cassava processing and ingestion of cassava foods Food Chem. Toxicol 40 2002 1001 1005
57. C.J. Vesey, and P.V. Cole Blood cyanide and thiocyanate concentrations produced by long-term therapy with sodium nitroprusside Br. J. Anaesth. 57 1985 148 155
58. D. Das, P.K. De, and R.K. Banerjee Thiocyanate, a plausible physiological electron donor of gastric peroxidase Biochem. J. 305 1995 59 64
59. M.T. Ashby Inorganic chemistry of defensive peroxidases in the human oral cavity J. Dent. Res. 87 2008 900 914
60. C. Bergt, S. Pennathur, X. Fu, J. Byun, K. OBrien, T.O. McDonald, P. Singh, G.M. Anantharamaiah, A. Chait, J. Brunzell, R.L. Geary, J.F. Oram, and J.W. Heinecke The myeloperoxidase product hypochlorous acid oxidizes HDL in the human artery wall and impairs ABCA1-dependent cholesterol transport Proc. Natl. Acad. Sci. USA 101 2004 13032 13037
61. D.K. Choi, S. Pennathur, C. Perier, K. Tieu, P. Teismann, D.C. Wu, V. Jackson-Lewis, M. Vila, J.P. Vonsattel, J.W. Heinecke, and S. Przedborski Ablation of the inflammatory enzyme myeloperoxidase mitigates features of Parkinsons disease in mice J. Neurosci. 25 2005 6594 6600
62. J. Himmelfarb, M.E. McMenamin, G. Loseto, and J.W. Heinecke Myeloperoxidase-catalyzed 3-chlorotyrosine formation in dialysis patients Free Radic. Biol. Med. 31 2001 1163 1169
63. A.J. Kettle, T. Chan, I. Osberg, R. Senthilmohan, A.L.P. Chapman, T.J. Mocatta, and J.S. Wagener Myeloperoxidase and protein oxidation in the airways of young children with cystic fibrosis Am. J. Respir. Crit. Care Med. 170 2004 1317 1323
64. A. Van Der Vliet, M.N. Nguyen, M.K. Shigenaga, J.P. Eiserich, G.P. Marelich, and C.E. Cross Myeloperoxidase and protein oxidation in cystic fibrosis Am. J. Physiol. Lung Cell. Mol. Physiol 279 2000 L537 L546
65. H. Mita, N. Higashi, M. Taniguchi, A. Higashi, Y. Kawagishi, and K. Akiyama Urinary 3-bromotyrosine and 3-chlorotyrosine concentrations in asthmatic patients: lack of increase in 3-bromotyrosine concentration in urine and plasma proteins in aspirin-induced asthma after intravenous aspirin challenge Clin. Exp. Allergy 34 2004 931 938
66. A.L. Chapman, M.B. Hampton, R. Senthilmohan, C.C. Winterbourn, and A.J. Kettle Chlorination of bacterial and neutrophil proteins during phagocytosis and killing of Staphylococcus aureus J. Biol. Chem. 277 2002 9757 9762
67. S.M. Bozonet, A.P. Scott-Thomas, P. Nagy, and M.C. Vissers Hypothiocyanous acid is a potent inhibitor of apoptosis and caspase 3 activation in endothelial cells Free Radic. Biol. Med. 49 2010 1054 1063
68. M.M. Lloyd, D.M. van Reyk, M.J. Davies, and C.L. Hawkins Hypothiocyanous acid is a more potent inducer of apoptosis and protein thiol depletion in murine macrophage cells than hypochlorous acid or hypobromous acid Biochem. J 414 2008 271 280
69. A.E. Lane, J.T. Tan, C.L. Hawkins, A.K. Heather, and M.J. Davies The myeloperoxidase-derived oxidant HOSCN inhibits protein tyrosine phosphatases and modulates cell signalling via the mitogen-activated protein kinase (MAPK) pathway in macrophages Biochem. J. 430 2010 161 169
70. R.T. Dean, S. Fu, R. Stocker, and M.J. Davies Biochemistry and pathology of radical-mediated protein oxidation Biochem. J. 324 1997 1 18
71. M.J. Davies The oxidative environment and protein damage Biochim. Biophys. Acta 1703 2005 93 109