Function and distribution of apolipoprotein A1 in the artery wall are markedly distinct from those in plasma

Circulation

Volumn 128, Issue 15, 2013, Pages 1644-1655

  DiDonato, Joseph A ^a   Huang, Ying ^a   Aulak, Kulwant S ^a   Even Or, Orli ^b   Gerstenecker, Gary ^a,c   Gogonea, Valentin ^a,c   Wu, Yuping ^c   Fox, Paul L ^a   Tang, W H Wilson ^a   Plow, Edward F ^a   Smith, Jonathan D ^a   Fisher, Edward A ^b   Hazen, Stanley L ^a,c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

Apolipoproteins; Arteriosclerosis; Cardiovascular diseases; Plaque, atherosclerotic

Indexed keywords

APOLIPOPROTEIN A1; HIGH DENSITY LIPOPROTEIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 10G1.5; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; UNCLASSIFIED DRUG;

AORTA; ARTERY WALL; ARTICLE; ATHEROSCLEROTIC PLAQUE; CONTROLLED STUDY; DENSITY; ENZYME ACTIVITY; FRACTIONATION; FUNCTIONAL ASSESSMENT; HUMAN; HUMAN TISSUE; LIPOPROTEIN BLOOD LEVEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; TISSUE HOMOGENATE;

APOLIPOPROTEINS; ARTERIOSCLEROSIS; CARDIOVASCULAR DISEASES; PLAQUE, ATHEROSCLEROTIC;

ACYLTRANSFERASES; ANIMALS; ANTIBODIES, MONOCLONAL; AORTA; APOLIPOPROTEIN A-I; ATHEROSCLEROSIS; CELL LINE; HUMANS; LIPOPROTEINS, HDL; LIPOPROTEINS, LDL; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; OXIDATION-REDUCTION; PLAQUE, ATHEROSCLEROTIC;

EID: 84885860263     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.002624     Document Type: Article

References (50)

1. Barter PJ, Caulfield M, Eriksson M, Grundy SM, Kastelein JJ, Komajda M, Lopez-Sendon J, Mosca L, Tardif JC, Waters DD, Shear CL, Revkin JH, Buhr KA, Fisher MR, Tall AR, Brewer B; ILLUMINATE Investigators. Effects of torcetrapib in patients at high risk for coronary events. N Engl J Med. 2007;357:2109-2122
2. Boden WE, Probstfield JL, Anderson T, Chaitman BR, Desvignes-Nickens P, Koprowicz K, McBride R, Teo K, Weintraub W. Niacin in patients with low HDL cholesterol levels receiving intensive statin therapy. N Engl J Med. 2011;365:2255-2267
3. Schwartz GG, Olsson AG, Abt M, Ballantyne CM, Barter PJ, Brumm J, Chaitman BR, Holme IM, Kallend D, Leiter LA, Leitersdorf E, McMurray JJ, Mundl H, Nicholls SJ, Shah PK, Tardif JC, Wright RS; dal-OUTCOMES Investigators. Effects of dalcetrapib in patients with a recent acute coronary syndrome. N Engl J Med. 2012;367:2089-2099
4. Voight BF, Peloso GM, Orho-Melander M, Frikke-Schmidt R, Barbalic M, Jensen MK, Hindy G, Hólm H, Ding EL, Johnson T, Schunkert H, Samani NJ, Clarke R, Hopewell JC, Thompson JF, Li M, Thorleifsson G, Newton-Cheh C, Musunuru K, Pirruccello JP, Saleheen D, Chen L, Stewart A, Schillert A, Thorsteinsdottir U, Thorgeirsson G, Anand S, Engert JC, Morgan T, Spertus J, Stoll M, Berger K, Martinelli N, Girelli D, McKeown PP, Patterson CC, Epstein SE, Devaney J, Burnett MS, Mooser V, Ripatti S, Surakka I, Nieminen MS, Sinisalo J, Lokki ML, Perola M, Havulinna A, De Faire U, Gigante B, Ingelsson E, Zeller T, Wild P, De Bakker PI, Klungel OH, Maitland-Van Der Zee AH, Peters BJ, De Boer A, Grobbee DE, Kamphuisen PW, Deneer VH, Elbers CC, Onland-Moret NC, Hofker MH, Wijmenga C, Verschuren WM, Boer JM, van Der Schouw YT, Rasheed A, Frossard P, Demissie S, Willer C, Do R, Ordovas JM, Abecasis GR, Boehnke M, Mohlke KL, Daly MJ, Guiducci C, Burtt NP, Surti A, Gonzalez E, Purcell S, Gabriel S, Marrugat J, Peden J, Erdmann J, Diemert P, Willenborg C, König IR, Fischer M, Hengstenberg C, Ziegler A, Buysschaert I, Lambrechts D, Van De Werf F, Fox KA, El Mokhtari NE, Rubin D, Schrezenmeir J, Schreiber S, Schäfer A, Danesh J, Blankenberg S, Roberts R, McPherson R, Watkins H, Hall AS, Overvad K, Rimm E, Boerwinkle E, Tybjaerg-Hansen A, Cupples LA, Reilly MP, Melander O, Mannucci PM, Ardissino D, Siscovick D, Elosua R, Stefansson K, O'Donnell CJ, Salomaa V, Rader DJ, Peltonen L, Schwartz SM, Altshuler D, Kathiresan S. Plasma HDL cholesterol and risk of myocardial infarction: A Mendelian randomisation study. Lancet. 2012;380:572-580
5. Rye KA, Barter PJ. Formation and metabolism of prebeta-migrating, lipidpoor apolipoprotein A-I. Arterioscler Thromb Vasc Biol. 2004;24:421-428
6. Chao FF, Amende LM, Blanchette-Mackie EJ, Skarlatos SI, Gamble W, Resau JH, Mergner WT, Kruth HS. Unesterified cholesterol-rich lipid particles in atherosclerotic lesions of human and rabbit aortas. Am J Pathol. 1988;131:73-83
7. Tîrziu D, Dobrian A, Tasca C, Simionescu M, Simionescu N. Intimal thickenings of human aorta contain modified reassembled lipoproteins. Atherosclerosis. 1995;112:101-114
8. 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
9. Wu Z, Wagner MA, Zheng L, Parks JS, Shy JM III, Smith JD, Gogonea V, Hazen SL. The refined structure of nascent HDL reveals a key functional domain for particle maturation and dysfunction. Nat Struct Mol Biol. 2007;14:861-868
10. Undurti A, Huang Y, Lupica JA, Smith JD, DiDonato JA, Hazen SL. Modification of high density lipoprotein by myeloperoxidase generates a pro-inflammatory particle. J Biol Chem. 2009;284:30825-30835
11. Pennathur S, Bergt C, Shao B, Byun J, Kassim SY, Singh P, Green PS, McDonald TO, Brunzell J, Chait A, Oram JF, Obrien K, Geary RL, Heinecke JW. Human atherosclerotic intima and blood of patients with established coronary artery disease contain high density lipoprotein damaged by reactive nitrogen species. J Biol Chem. 2004;279:42977-42983
12. Hadfield KA, Pattison DI, Brown BE, Hou L, Rye KA, Davies MJ, Hawkins CL. Myeloperoxidase-Derived oxidants modify apolipoprotein A-I and generate dysfunctional high-Density lipoproteins: Comparison of hypothiocyanous acid (HOSCN) with hypochlorous acid (HOCl). Biochem J. 2013;449:531-542
13. Zheng L, Settle M, Brubaker G, Schmitt D, Hazen SL, Smith JD, Kinter M. Localization of nitration and chlorination sites on apolipoprotein A-I catalyzed by myeloperoxidase in human atheroma and associated oxidative impairment in ABCA1-Dependent cholesterol efflux from macrophages. J Biol Chem. 2005;280:38-47
14. Peng DQ, Wu Z, Brubaker G, Zheng L, Settle M, Gross E, Kinter M, Hazen SL, Smith JD. Tyrosine modification is not required for myeloperoxidase- induced loss of apolipoprotein A-I functional activities. J Biol Chem. 2005;280:33775-33784
15. 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
16. 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
17. Ståhlman M, Davidsson P, Kanmert I, Rosengren B, Borén J, Fagerberg B, Camejo G. Proteomics and lipids of lipoproteins isolated at low salt concentrations in D2O/sucrose or in KBr. J Lipid Res. 2008;49:481-490
18. Wu Z, Gogonea V, Lee X, Wagner MA, Li XM, Huang Y, Undurti A, May RP, Haertlein M, Moulin M, Gutsche I, Zaccai G, Didonato JA, Hazen SL. Double superhelix model of high density lipoprotein. J Biol Chem. 2009;284:36605-36619
19. Matz CE, Jonas A. Micellar complexes of human apolipoprotein A-I with phosphatidylcholines and cholesterol prepared from cholate-lipid dispersions. J Biol Chem. 1982;257:4535-4540
20. Nelson DP, Kiesow LA. Enthalpy of decomposition of hydrogen peroxide by catalase at 25 degrees C (with molar extinction coefficients of H2O2 solutions in the UV). Anal Biochem. 1972;49:474-478
21. Chisholm JW, Gebre AK, Parks JS. Characterization of C-terminal histidine- tagged human recombinant lecithin:cholesterol acyltransferase. J Lipid Res. 1999;40:1512-1519
22. Parks JS, Gebre AK, Furbee JW. Lecithin-cholesterol acyltransferase: Assay of cholesterol esterification and phospholipase A2 activities. Methods Mol Biol. 1999;109:123-131
23. Smith JD, Le Goff W, Settle M, Brubaker G, Waelde C, Horwitz A, Oda MN. ABCA1 mediates concurrent cholesterol and phospholipid efflux to apolipoprotein A-I. J Lipid Res. 2004;45:635-644
24. Piao ZH, Kim MS, Jeong M, Yun S, Lee SH, Sun HN, Song HY, Suh HW, Jung H, Yoon SR, Kim TD, Lee YH, Choi I. VDUP1 exacerbates bacteremic shock in mice infected with Pseudomonas aeruginosa. Cell Immunol. 2012;280:1-9
25. Wang N, Silver DL, Costet P, Tall AR. Specific binding of ApoA-I, enhanced cholesterol efflux, and altered plasma membrane morphology in cells expressing ABC1. J Biol Chem. 2000;275:33053-33058
26. Mulya A, Lee JY, Gebre AK, Thomas MJ, Colvin PL, Parks JS. Minimal lipidation of pre-beta HDL by ABCA1 results in reduced ability to interact with ABCA1. Arterioscler Thromb Vasc Biol. 2007;27:1828-1836
27. Duong PT, Weibel GL, Lund-Katz S, Rothblat GH, Phillips MC. Characterization and properties of pre beta-HDL particles formed by ABCA1-mediated cellular lipid efflux to apoA-I. J Lipid Res. 2008;49:1006-1014
28. Liu L, Bortnick AE, Nickel M, Dhanasekaran P, Subbaiah PV, Lund-Katz S, Rothblat GH, Phillips MC. Effects of apolipoprotein A-I on ATPbinding cassette transporter A1-mediated efflux of macrophage phospholipid and cholesterol: Formation of nascent high density lipoprotein particles. J Biol Chem. 2003;278:42976-42984
29. Eriksson M, Schönland S, Yumlu S, Hegenbart U, von Hutten H, Gioeva Z, Lohse P, Büttner J, Schmidt H, Röcken C. Hereditary apolipoprotein AI-associated amyloidosis in surgical pathology specimens: Identification of three novel mutations in the APOA1 gene. J Mol Diagn. 2009;11:257-262
30. Tabas I, Williams KJ, Borén J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: Update and therapeutic implications. Circulation. 2007;116:1832-1844
31. Gustafsson M, Levin M, Skålén K, Perman J, Fridén V, Jirholt P, Olofsson SO, Fazio S, Linton MF, Semenkovich CF, Olivecrona G, Borén J. Retention of low-Density lipoprotein in atherosclerotic lesions of the mouse: Evidence for a role of lipoprotein lipase. Circ Res. 2007;101:777-783
32. Devlin CM, Leventhal AR, Kuriakose G, Schuchman EH, Williams KJ, Tabas I. Acid sphingomyelinase promotes lipoprotein retention within early atheromata and accelerates lesion progression. Arterioscler Thromb Vasc Biol. 2008;28:1723-1730
33. Vasile E, Antohe F, Simionescu M, Simionescu N. Transport pathways of beta-VLDL by aortic endothelium of normal and hypercholesterolemic rabbits. Atherosclerosis. 1989;75:195-210
34. Truskey GA, Roberts WL, Herrmann RA, Malinauskas RA. Measurement of endothelial permeability to 125I-low density lipoproteins in rabbit arteries by use of en face preparations. Circ Res. 1992;71:883-897
35. Rozenberg I, Sluka SH, Rohrer L, Hofmann J, Becher B, Akhmedov A, Soliz J, Mocharla P, Borén J, Johansen P, Steffel J, Watanabe T, Lüscher TF, Tanner FC. Histamine H1 receptor promotes atherosclerotic lesion formation by increasing vascular permeability for low-Density lipoproteins. Arterioscler Thromb Vasc Biol. 2010;30:923-930
36. 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
37. Vaisar T, Pennathur S, Green PS, Gharib SA, Hoofnagle AN, Cheung MC, Byun J, Vuletic S, Kassim S, Singh P, Chea H, Knopp RH, Brunzell J, Geary R, Chait A, Zhao XQ, Elkon K, Marcovina S, Ridker P, Oram JF, Heinecke JW. Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL. J Clin Invest. 2007;117:746-756
38. Davidson WS, Silva RA, Chantepie S, Lagor WR, Chapman MJ, Kontush A. Proteomic analysis of defined HDL subpopulations reveals particlespecific protein clusters: Relevance to antioxidative function. Arterioscler Thromb Vasc Biol. 2009;29:870-876
39. Holzer M, Wolf P, Curcic S, Birner-Gruenberger R, Weger W, Inzinger M, El-Gamal D, Wadsack C, Heinemann A, Marsche G. Psoriasis alters HDL composition and cholesterol efflux capacity. J Lipid Res. 2012;53:1618-1624
40. Tölle M, Huang T, Schuchardt M, Jankowski V, Prüfer N, Jankowski J, Tietge UJ, Zidek W, van Der Giet M. High-Density lipoprotein loses its anti-inflammatory capacity by accumulation of pro-inflammatory-serum amyloid A. Cardiovasc Res. 2012;94:154-162.
41. Riwanto M, Rohrer L, Roschitzki B, Besler C, Mocharla P, Mueller M, Perisa D, Heinrich K, Altwegg L, von Eckardstein A, Lüscher TF, Landmesser U. Altered activation of endothelial anti- and proapoptotic pathways by high-Density lipoprotein from patients with coronary artery disease: Role of high-Density lipoprotein-proteome remodeling. Circulation. 2013;127:891-904
42. Taylor AJ, Sullenberger LE, Lee HJ, Lee JK, Grace KA. Arterial Biology for the Investigation of the Treatment Effects of Reducing Cholesterol (ARBITER) 2: A double-blind, placebo-controlled study of extendedrelease niacin on atherosclerosis progression in secondary prevention patients treated with statins. Circulation. 2004;110:3512-3517
43. Vogt A, Kassner U, Hostalek U, Peiter A, Steinhagen-Thiessen E. Safety and tolerability of nicotinic acid: Results of the multicenter, open, prospective NAUTILUS study [in German]. MMW Fortschr Med. 2006;148:41
44. Schwartz GG, Olsson AG, Ballantyne CM, Barter PJ, Holme IM, Kallend D, Leiter LA, Leitersdorf E, McMurray JJ, Shah PK, Tardif JC, Chaitman BR, Duttlinger-Maddux R, Mathieson J; dal-OUTCOMES Committees and Investigators. Rationale and design of the dal-OUTCOMES trial: Efficacy and safety of dalcetrapib in patients with recent acute coronary syndrome. Am Heart J. 2009;158:896-901.e3
45. McKenney J, Bays H, Koren M, Ballantyne CM, Paolini JF, Mitchel Y, Betteridge A, Kuznetsova O, Sapre A, Sisk CM, Maccubbin D. Safety of extended-release niacin/laropiprant in patients with dyslipidemia. J Clin Lipidol. 2010;4:105-112.e1
46. Nicholls SJ. Is niacin ineffective? Or did AIM-HIGH miss its target? Cleve Clin J Med. 2012;79:38-43
47. Rader DJ, Tall AR. The not-so-simple HDL story: Is it time to revise the HDL cholesterol hypothesis? Nat Med. 2012;18:1344-1346
48. 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
49. Li XM, Tang WH, Mosior MK, Huang Y, Wu Y, Matter W, Gao V, Schmitt D, Didonato JA, Fisher EA, Smith JD, Hazen SL. Paradoxical association of enhanced cholesterol efflux with increased incident cardiovascular risks. Arterioscler Thromb Vasc Biol. 2013;33:1696-1705
50. Macheboeuf M. Recherches sur les phosphoaminolipides et les sterids du serum et du plasma sanguins: Ii etude physiochimique De la fraction proteidique la plus riche en phospholipids et in sterides: Proteidique la plus riche en phospholipids et in steridesproteidique la plus riche en phospholipids et in sterides. Bull Soc Chim Biol. 1929;11:485-503