Humans with atherosclerosis have impaired ABCA1 cholesterol efflux and enhanced high-density lipoprotein oxidation by myeloperoxidase

Circulation Research

Volumn 114, Issue 11, 2014, Pages 1733-1742

  Shao, Baohai ^a,c   Tang, Chongren ^a,c   Sinha, Abhishek ^a   Mayer, Philip S ^a,c   Davenport, George D ^a   Brot, Nathan ^b,c   Oda, Michael N ^d   Zhao, Xue Qiao ^a   Heinecke, Jay W ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c FLORIDA ATLANTIC UNIVERSITY   (United States)

^d CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

acute coronary syndrome; cardiovascular diseases; chlorotyrosine; mass spectrometry; peroxidase

Indexed keywords

3 CHLOROTYROSINE; ABC TRANSPORTER A1; APOLIPOPROTEIN A1; C REACTIVE PROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; METHIONINE; MYELOPEROXIDASE; TRIACYLGLYCEROL; TYROSINE;

ACUTE CORONARY SYNDROME; ADULT; ARTICLE; CARDIOVASCULAR RISK; CLINICAL ARTICLE; CONTROLLED STUDY; CORONARY ARTERY DISEASE; ENZYME BLOOD LEVEL; FEMALE; HUMAN; LIPOPROTEIN BLOOD LEVEL; MACROPHAGE; MALE; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; TANDEM MASS SPECTROMETRY;

3-CHLOROTYROSINE; ACUTE CORONARY SYNDROME; CARDIOVASCULAR DISEASES; MASS SPECTROMETRY; PEROXIDASE;

ACUTE CORONARY SYNDROME; AGED; APOLIPOPROTEIN A-I; ATHEROSCLEROSIS; ATP BINDING CASSETTE TRANSPORTER 1; BIOLOGICAL MARKERS; C-REACTIVE PROTEIN; CASE-CONTROL STUDIES; CELLS, CULTURED; CHOLESTEROL; CORONARY ARTERY DISEASE; FEMALE; HUMANS; LIPOPROTEINS, HDL; MALE; METHIONINE; MIDDLE AGED; OXIDATION-REDUCTION; PEROXIDASE; SIGNAL TRANSDUCTION;

EID: 84901637810     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.114.303454     Document Type: Article

References (47)

1. Gordon DJ, Rifkind BM. High-density lipoprotein-the clinical implications of recent studies. N Engl J Med. 1989;321:1311-1316.
2. Tall AR, Yvan-Charvet L, Terasaka N, Pagler T, Wang N. HDL, ABC transporters, and cholesterol efflux: implications for the treatment of atherosclerosis. Cell Metab. 2008;7:365-375.
3. Wang X, Rader DJ. Molecular regulation of macrophage reverse cholesterol transport. Curr Opin Cardiol. 2007;22:368-372.
4. Davidson WS, Thompson TB. The structure of apolipoprotein A-I in high density lipoproteins. J Biol Chem. 2007;282:22249-22253.
5. Freeman MW. Effluxed lipids: Tangier Island's latest export. Proc Natl Acad Sci USA. 1999;96:10950-10952.
6. Oram JF, Heinecke JW. ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol Rev. 2005;85:1343-1372.
7. Lawn RM, Wade DP, Garvin MR, Wang X, Schwartz K, Porter JG, Seilhamer JJ, Vaughan AM, Oram JF. The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. J Clin Invest. 1999;104:R25-R31.
8. Assmann G, von Eckardstein, A. and Brewer, H.B. Familial high density lipoprotein deficiency: Tangier disease. In: Scriver CR, Beaudet, A.L., Sly, W.S. and Valle, D., eds. The Metabolic and Molecular Basis of Inherited Disease. New York: McGraw-Hill; 1995:2053-2072.
9. Ferrans VJ, Fredrickson DS. The pathology of Tangier disease. A light and electron microscopic study. Am J Pathol. 1975;78:101-158.
10. Aiello RJ, Brees D, Francone OL. ABCA1-deficient mice: insights into the role of monocyte lipid efflux in HDL formation and inflammation. Arterioscler Thromb Vasc Biol. 2003;23:972-980.
11. van Eck M, Bos IS, Kaminski WE, Orsó E, Rothe G, Twisk J, Böttcher A, Van Amersfoort ES, Christiansen-Weber TA, Fung-Leung WP, Van Berkel TJ, Schmitz G. Leukocyte ABCA1 controls susceptibility to atherosclerosis and macrophage recruitment into tissues. Proc Natl Acad Sci USA. 2002;99:6298-6303.
12. Barter PJ, Nicholls S, Rye KA, Anantharamaiah GM, Navab M, Fogelman AM. Antiinflammatory properties of HDL. Circ Res. 2004;95:764-772.
13. McGillicuddy FC, de la Llera Moya M, Hinkle CC, Joshi MR, Chiquoine EH, Billheimer JT, Rothblat GH, Reilly MP. Inflammation impairs reverse cholesterol transport in vivo. Circulation 2009;119:1135-1145.
14. Shao B, Oda MN, Oram JF, Heinecke JW. Myeloperoxidase: an oxidative pathway for generating dysfunctional high-density lipoprotein. Chem Res Toxicol. 2010;23:447-454.
15. Berliner JA, Heinecke JW. The role of oxidized lipoproteins in atherogenesis. Free Radic Biol Med. 1996;20:707-727.
16. Stocker R, Keaney JF Jr. Role of oxidative modifications in atherosclerosis. Physiol Rev. 2004;84:1381-1478.
17. Daugherty A, Dunn JL, Rateri DL, Heinecke JW. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J Clin Invest. 1994;94:437-444.
18. Hazen SL, Hsu FF, Mueller DM, Crowley JR, Heinecke JW. Human neutrophils employ chlorine gas as an oxidant during phagocytosis. J Clin Invest. 1996;98:1283-1289.
19. Hurst JK, Barrette WC Jr. Leukocytic oxygen activation and microbicidal oxidative toxins. Crit Rev Biochem Mol Biol. 1989;24:271-328.
20. Domigan NM, Charlton TS, Duncan MW, Winterbourn CC, Kettle AJ. Chlorination of tyrosyl residues in peptides by myeloperoxidase and human neutrophils. J Biol Chem. 1995;270:16542-16548.
21. 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.
22. Bergt C, Pennathur S, Fu X, Byun J, O'Brien K, McDonald TO, Singh P, Anantharamaiah GM, Chait A, Brunzell J, Geary RL, Oram JF, Heinecke JW. The myeloperoxidase product hypochlorous acid oxidizes HDL in the human artery wall and impairs ABCA1-dependent cholesterol transport. Proc Natl Acad Sci USA. 2004;101:13032-13037.
23. Shao B, Bergt C, Fu X, Green P, Voss JC, Oda MN, Oram JF, Heinecke JW. 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. 2005;280:5983-5993.
24. Zheng L, Nukuna B, Brennan ML, Sun M, Goormastic M, Settle M, Schmitt D, Fu X, Thomson L, Fox PL, Ischiropoulos H, Smith JD, Kinter M, Hazen SL. Apolipoprotein A-I is a selective target for myeloperoxidase-catalyzed oxidation and functional impairment in subjects with cardiovascular disease. J Clin Invest. 2004;114:529-541.
25. Shao B, Oda MN, Bergt C, Fu X, Green PS, Brot N, Oram JF, Heinecke JW. Myeloperoxidase impairs ABCA1-dependent cholesterol efflux through methionine oxidation and site-specific tyrosine chlorination of apolipoprotein A-I. J Biol Chem. 2006;281:9001-9004.
26. Shao B, Cavigiolio G, Brot N, Oda MN, Heinecke JW. Methionine oxidation impairs reverse cholesterol transport by apolipoprotein A-I. Proc Natl Acad Sci USA. 2008;105:12224-12229.
27. Shao B, Pennathur S, Heinecke JW. Myeloperoxidase targets apolipoprotein A-I, the major high density lipoprotein protein, for site-specific oxidation in human atherosclerotic lesions. J Biol Chem. 2012;287:6375-6386.
28. Feingold KR, Grunfeld C. The acute phase response inhibits reverse cholesterol transport. J Lipid Res. 2010;51:682-684.
29. de la Llera-Moya M, Drazul-Schrader D, Asztalos BF, Cuchel M, Rader DJ, Rothblat GH. The ability to promote efflux via ABCA1 determines the capacity of serum specimens with similar high-density lipoprotein cholesterol to remove cholesterol from macrophages. Arterioscler Thromb Vasc Biol. 2010;30:796-801
30. Khera AV, Cuchel M, de la Llera-Moya M, Rodrigues A, Burke MF, Jafri K, French BC, Phillips JA, Mucksavage ML, Wilensky RL, Mohler ER, Rothblat GH, Rader DJ. Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N Engl J Med. 2011;364:127-135.
31. Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991;43:109-142.
32. Szapacs ME, Kim HY, Porter NA, Liebler DC. Identification of proteins adducted by lipid peroxidation products in plasma and modifications of apolipoprotein A1 with a novel biotinylated phospholipid probe. J Proteome Res. 2008;7:4237-4246.
33. Li S, Schöneich C, Borchardt RT. Chemical instability of protein pharmaceuticals: Mechanisms of oxidation and strategies for stabilization. Biotechnol Bioeng. 1995;48:490-500.
34. Ryan RO, Forte TM, Oda MN. Optimized bacterial expression of human apolipoprotein A-I. Protein Expr Purif. 2003;27:98-103.
35. Anderson L, Hunter CL. Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins. Mol Cell Proteomics. 2006;5:573-588.
36. Panzenböck U, Kritharides L, Raftery M, Rye KA, Stocker R. Oxidation of methionine residues to methionine sulfoxides does not decrease potential antiatherogenic properties of apolipoprotein A-I. J Biol Chem. 2000;275:19536-19544.
37. Shao B, Tang C, Heinecke JW, Oram JF. Oxidation of apolipoprotein A-I by myeloperoxidase impairs the initial interactions with ABCA1 required for signaling and cholesterol export. J Lipid Res. 2010;51:1849-1858.
38. Gaut JP, Yeh GC, Tran HD, Byun J, Henderson JP, Richter GM, Brennan ML, Lusis AJ, Belaaouaj A, Hotchkiss RS, Heinecke JW. Neutrophils employ the myeloperoxidase system to generate antimicrobial brominating and chlorinating oxidants during sepsis. Proc Natl Acad Sci USA. 2001;98:11961-11966.
39. Lowther WT, Brot N, Weissbach H, Honek JF, Matthews BW. Thiol-disulfide exchange is involved in the catalytic mechanism of peptide methionine sulfoxide reductase. Proc Natl Acad Sci USA. 2000;97:6463-6468.
40. Atger V, de la Llera Moya M, Bamberger M, Francone O, Cosgrove P, Tall A, Walsh A, Moatti N, Rothblat G. Cholesterol efflux potential of sera from mice expressing human cholesteryl ester transfer protein and/or human apolipoprotein AI. J Clin Invest. 1995;96:2613-2622.
41. Peng DQ, Brubaker G, Wu Z, Zheng L, Willard B, Kinter M, Hazen SL, Smith JD. Apolipoprotein A-I tryptophan substitution leads to resistance to myeloperoxidase-mediated loss of function. Arterioscler Thromb Vasc Biol. 2008;28:2063-2070.
42. Garner B, Waldeck AR, Witting PK, Rye KA, Stocker R. Oxidation of high density lipoproteins. II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins AI and AII. J Biol Chem. 1998;273:6088-6095.
43. Cascio G, Schiera G, Di Liegro I. Dietary fatty acids in metabolic syndrome, diabetes and cardiovascular diseases. Curr Diabetes Rev. 2012;8:2-17.
44. Brock JW, Jenkins AJ, Lyons TJ, Klein RL, Yim E, Lopes-Virella M, Carter RE, Thorpe SR, Baynes JW; DCCT/EDIC Research Group. Increased methionine sulfoxide content of apoA-I in type 1 diabetes. J Lipid Res. 2008;49:847-855.
45. Lindahl B, Toss H, Siegbahn A, Venge P, Wallentin L. Markers of myocardial damage and inflammation in relation to long-term mortality in unstable coronary artery disease. FRISC Study Group. Fragmin during Instability in Coronary Artery Disease. N Engl J Med. 2000;343:1139-1147.
46. Alwaili K, Bailey D, Awan Z, Bailey SD, Ruel I, Hafiane A, Krimbou L, Laboissiere S, Genest J. The HDL proteome in acute coronary syndromes shifts to an inflammatory profile. Biochim Biophys Acta. 2012;1821:405-415.
47. Van Lenten BJ, Hama SY, de Beer FC, Stafforini DM, McIntyre TM, Prescott SM, La Du BN, Fogelman AM, Navab M. Anti-inflammatory HDL becomes pro-inflammatory during the acute phase response. Loss of protective effect of HDL against LDL oxidation in aortic wall cell cocultures. J Clin Invest. 1995;96:2758-2767.