The myeloperoxidase product hypochlorous acid generates irreversible high-density lipoprotein receptor inhibitors

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 5, 2013, Pages 1020-1027

  Binder, Veronika ^a   Ljubojevic, Senka ^a   Haybaeck, Johannes ^a   Holzer, Michael ^a   El Gamal, Dalia ^a   Schicho, Rudolf ^a   Pieske, Burkert ^a   Heinemann, Akos ^a   Marsche, Gunther ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

advanced oxidation protein products; atherosclerosis; end stage renal disease; high density lipoprotein metabolism; high density lipoprotein composition; myeloperoxidase; scavenger receptor class B, type 1

Indexed keywords

3 CHLOROTYROSINE; CHLORAMINE DERIVATIVE; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN RECEPTOR; HIGH DENSITY LIPOPROTEIN RECEPTOR INHIBITOR; HYPOCHLOROUS ACID; LIGAND; LYSINE; MYELOPEROXIDASE; RECEPTOR BLOCKING AGENT; SERUM ALBUMIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARDIOVASCULAR DISEASE; CHRONIC KIDNEY DISEASE; CONCENTRATION RESPONSE; CONTROLLED STUDY; LIPID COMPOSITION; NONHUMAN; OXIDATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTECTION; PROTEIN BINDING; PROTEIN MODIFICATION;

ANIMALS; ANTIGENS, CD36; CARDIOVASCULAR DISEASES; CHO CELLS; CRICETINAE; CRICETULUS; HUMANS; HYPOCHLOROUS ACID; KIDNEY FAILURE, CHRONIC; LIPOPROTEINS, HDL; MICE; MICE, INBRED BALB C; PEROXIDASE; RECEPTORS, LIPOPROTEIN; SERUM ALBUMIN;

EID: 84876295516     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.301235     Document Type: Article

References (47)

1. Klebanoff SJ. Myeloperoxidase-halide-hydrogen peroxide antibacterial system. J Bacteriol. 1968;95:2131-2138.
2. Klebanoff SJ. Myeloperoxidase: friend and foe. J Leukoc Biol. 2005;77:598-625.
3. Witko-Sarsat V, Friedlander M, Capeillère-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J, Jungers P, Descamps-Latscha B. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int. 1996;49:1304-1313.
4. Descamps-Latscha B, Witko-Sarsat V. Importance of oxidatively modifed proteins in chronic renal failure. Kidney Int Suppl. 2001;78:S108-S113.
5. Pattison DI, Hawkins CL, Davies MJ. What are the plasma targets of the oxidant hypochlorous acid? A kinetic modeling approach. Chem Res Toxicol. 2009;22:807-817.
6. Colombo G, Clerici M, Giustarini D, Rossi R, Milzani A, Dalle-Donne I. Redox albuminomics: oxidized albumin in human diseases. Antioxid Redox Signal. 2012;17:1515-1527.
7. Selmeci L. Advanced oxidation protein products (AOPP): novel uremic toxins, or components of the non-enzymatic antioxidant system of the plasma proteome? Free Radic Res. 2011;45:1115-1123.
8. Musante L, Bruschi M, Candiano G, Petretto A, Dimasi N, Del Boccio P, Urbani A, Rialdi G, Ghiggeri GM. Characterization of oxidation end product of plasma albumin 'in vivo'. Biochem Biophys Res Commun. 2006;349:668-673.
9. Musante L, Candiano G, Petretto A, Bruschi M, Dimasi N, Caridi G, Pavone B, Del Boccio P, Galliano M, Urbani A, Scolari F, Vincenti F, Ghiggeri GM. Active focal segmental glomerulosclerosis is associated with massive oxidation of plasma albumin. J Am Soc Nephrol. 2007;18:799-810.
10. Winterbourn CC. Comparative reactivities of various biological compounds with myeloperoxidase-hydrogen peroxide-chloride, and similarity of the oxidant to hypochlorite. Biochim Biophys Acta. 1985;840: 204-210.
11. Pattison DI, Davies MJ. Absolute rate constants for the reaction of hypo-chlorous acid with protein side chains and peptide bonds. Chem Res Toxicol. 2001;14:1453-1464.
12. Hazen SL, Hsu FF, d'Avignon A, Heinecke JW. Human neutrophils employ myeloperoxidase to convert alpha-amino acids to a battery of reactive aldehydes: a pathway for aldehyde generation at sites of infammation. Biochemistry. 1998;37:6864-6873.
13. Hazen SL, d'Avignon A, Anderson MM, Hsu FF, Heinecke JW. Human neutrophils employ the myeloperoxidase-hydrogen peroxide-chloride system to oxidize alpha-amino acids to a family of reactive aldehydes. Mechanistic studies identifying labile intermediates along the reaction pathway. J Biol Chem. 1998;273:4997-5005.
14. Marsche G, Frank S, Hrzenjak A, Holzer M, Dirnberger S, Wadsack C, Scharnagl H, Stojakovic T, Heinemann A, Oettl K. Plasma-advanced oxidation protein products are potent high-density lipoprotein receptor antagonists in vivo. Circ Res. 2009;104:750-757.
15. Acton SL, Scherer PE, Lodish HF, Krieger M. Expression cloning of SR-BI, a CD36-related class B scavenger receptor. J Biol Chem. 1994;269: 21003-21009.
16. Krieger M. Scavenger receptor class B type I is a multiligand HDL receptor that infuences diverse physiologic systems. J Clin Invest. 2001;108: 793-797.
17. Trigatti BL, Krieger M, Rigotti A. Infuence of the HDL receptor SR-BI on lipoprotein metabolism and atherosclerosis. Arterioscler Thromb Vasc Biol. 2003;23:1732-1738.
18. Rigotti A, Miettinen HE, Krieger M. The role of the high-density lipopro-tein receptor SR-BI in the lipid metabolism of endocrine and other tissues. Endocr Rev. 2003;24:357-387.
19. Kozarsky KF, Donahee MH, Rigotti A, Iqbal SN, Edelman ER, Krieger M. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature. 1997;387:414-417.
20. Mineo C, Shaul PW. Role of high-density lipoprotein and scavenger receptor B type I in the promotion of endothelial repair. Trends Cardiovasc Med. 2007;17:156-161.
21. Ma Y, Ashraf MZ, Podrez EA. Scavenger receptor BI modulates platelet reactivity and thrombosis in dyslipidemia. Blood. 2010;116: 1932-1941.
22. Capeillère-Blandin C, Gausson V, Descamps-Latscha B, Witko-Sarsat V. Biochemical and spectrophotometric signifcance of advanced oxidized protein products. Biochim Biophys Acta. 2004;1689:91-102.
23. Marsche G, Semlitsch M, Hammer A, Frank S, Weigle B, Demling N, Schmidt K, Windischhofer W, Waeg G, Sattler W, Malle E. Hypochlorite-modifed albumin colocalizes with RAGE in the artery wall and promotes MCP-1 expression via the RAGE-Erk1/2 MAP-kinase pathway. FASEB J. 2007;21:1145-1152.
24. Himmelfarb J, McMenamin ME, Loseto G, Heinecke JW. Myeloperoxidase- catalyzed 3-chlorotyrosine formation in dialysis patients. Free Radic Biol Med. 2001;31:1163-1169.
25. Marsche G, Furtmüller PG, Obinger C, Sattler W, Malle E. Hypochlorite-modifed high-density lipoprotein acts as a sink for myeloperoxidase in vitro. Cardiovasc Res. 2008;79:187-194.
26. Shur SA, Vulfson PL, Severin SE. The role of cysteinyl residues in the phosphorylase kinase activity as revealed by iodacetamide modifcation. Biochem Int. 1983;7:197-206.
27. Van Eck M, Twisk J, Hoekstra M, Van Rij BT, Van der Lans CA, Bos IS, Kruijt JK, Kuipers F, Va n Berkel TJ. Differential effects of scavenger receptor BI defciency on lipid metabolism in cells of the arterial wall and in the liver. J Biol Chem. 2003;278:23699-23705.
28. Baldus S, Eiserich JP, Mani A, Castro L, Figueroa M, Chumley P, Ma W, Tousson A, White CR, Bullard DC, Brennan ML, Lusis AJ, Moore KP, Freeman BA. Endothelial transcytosis of myeloperoxidase confers specifcity to vascular ECM proteins as targets of tyrosine nitration. J Clin Invest. 2001;108:1759-1770.
29. Raftery MJ, Yang Z, Valenzuela SM, Geczy CL. Novel intra-and inter-molecular sulfnamide bonds in S100A8 produced by hypochlorite oxidation. J Biol Chem. 2001;276:33393-33401.
30. Fu X, Mueller DM, Heinecke JW. Generation of intramolecular and intermolecular sulfenamides, sulfnamides, and sulfonamides by hypochlorous acid: a potential pathway for oxidative cross-linking of low-density lipoprotein by myeloperoxidase. Biochemistry. 2002;41: 1293-1301.
31. Yu M, Romer KA, Nieland TJ, Xu S, Saenz-Vash V, Penman M, Yesilaltay A, Carr SA, Krieger M. Exoplasmic cysteine Cys384 of the HDL receptor SR-BI is critical for its sensitivity to a small-molecule inhibitor and normal lipid transport activity. Proc Natl Acad Sci USA. 2011;108:12243-12248.
32. Carr AC, Hawkins CL, Thomas SR, Stocker R, Frei B. Relative reactivities of N-chloramines and hypochlorous acid with human plasma constituents. Free Radic Biol Med. 2001;30:526-536.
33. Chapman AL, Winterbourn CC, Brennan SO, Jordan TW, Kettle AJ. Characterization of non-covalent oligomers of proteins treated with hypo-chlorous acid. Biochem J. 2003;375(pt 1):33-40.
34. Hazell LJ, van den Berg JJ, Stocker R. Oxidation of low-density lipoprotein by hypochlorite causes aggregation that is mediated by modifcation of lysine residues rather than lipid oxidation. Biochem J. 1994;302 (pt 1):297-304.
35. Folkes LK, Candeias LP, Wardman P. Kinetics and mechanisms of hypo-chlorous acid reactions. Arch Biochem Biophys. 1995;323:120-126.
36. Holzer M, Gauster M, Pfeifer T, Wadsack C, Fauler G, Stiegler P, Koefeler H, Beubler E, Schuligoi R, Heinemann A, Marsche G. Protein carba-mylation renders high-density lipoprotein dysfunctional. Antioxid Redox Signal. 2011;14:2337-2346.
37. Holzer M, Zangger K, El-Gamal D, Binder V, Curcic S, Konya V, Schuligoi R, Heinemann A, Marsche G. Myeloperoxidase-derived chlorinating species induce protein carbamylation through decomposition of thiocyanate and urea: novel pathways generating dysfunctional high-density lipopro-tein. Antioxid Redox Signal. 2012;17:1043-1052.
38. El-Gamal D, Holzer M, Gauster M, Schicho R, Binder V, Konya V, Wadsack C, Schuligoi R, Heinemann A, Marsche G. Cyanate is a novel inducer of endothelial icam-1 expression. Antioxid Redox Signal. 2012;16:129-137.
39. Talib J, Pattison DI, Harmer JA, Celermajer DS, Davies MJ. High plasma thiocyanate levels modulate protein damage induced by myeloperoxidase and perturb measurement of 3-chlorotyrosine. Free Radic Biol Med. 2012;53:20-29.
40. Anderson MM, Requena JR, Crowley JR, Thorpe SR, Heinecke JW. The myeloperoxidase system of human phagocytes generates Nepsilon-(carboxymethyl) lysine on proteins: a mechanism for producing advanced glycation end products at sites of infammation. J Clin Invest. 1999;104:103-113.
41. Cao W, Xu J, Zhou ZM, Wang GB, Hou FF, Nie J. Advanced oxidation protein products activate intrarenal renin-angiotensin system via a CD36-mediated, redox-dependent pathway. Antioxid Redox Signal. 2013;18:19-35.
42. Zhou LL, Cao W, Xie C, Tian J, Zhou Z, Zhou Q, Zhu P, Li A, Liu Y, Miyata T, Hou FF, Nie J. The receptor of advanced glycation end products plays a central role in advanced oxidation protein products-induced podo-cyte apoptosis. Kidney Int. 2012;82:759-770.
43. Zhang Y, Da Silva JR, Reilly M, Billheimer JT, Rothblat GH, Rader DJ. Hepatic expression of scavenger receptor class B type I (SR-BI) is a positive regulator of macrophage reverse cholesterol transport in vivo. J Clin Invest. 2005;115:2870-2874.
44. Holzer M, Birner-Gruenberger R, Stojakovic T, El-Gamal D, Binder V, Wadsack C, Heinemann A, Marsche G. Uremia alters HDL composition and function. J Am Soc Nephrol. 2011;22:1631-1641.
45. Marsche G, Saemann MD, Heinemann A, Holzer M. Infammation alters HDL composition and function: implications for HDL-raising therapies. Pharmacol Ther. 2013;137:341-351.
46. Hirano K, Yamashita S, Nakagawa Y, Ohya T, Matsuura F, Tsukamoto K, Okamoto Y, Matsuyama A, Matsumoto K, Miyagawa J, Matsuzawa Y. Expression of human scavenger receptor class B type I in cultured human monocyte-derived macrophages and atherosclerotic lesions. Circ Res. 1999;85:108-116.
47. Liu SX, Hou FF, Guo ZJ, Nagai R, Zhang WR, Liu ZQ, Zhou ZM, Zhou M, Xie D, Wang GB, Zhang X. Advanced oxidation protein products accelerate atherosclerosis through promoting oxidative stress and infam-mation. Arterioscler Thromb Vasc Biol. 2006;26:1156-1162.