Subendothelial lipoprotein retention as the initiating process in atherosclerosis: Update and therapeutic implications

Circulation

Volumn 116, Issue 16, 2007, Pages 1832-1844

  Tabas, Ira ^a,d   Williams, Kevin Jon ^b   Borén, Jan ^c  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d NewYork Presbyterian Hospital   (United States)

Author keywords

Atherosclerosis; Cardiovascular diseases; Extracellular matrix; Lipoproteins; Prevention; Proteoglycans; Statins

Indexed keywords

APOLIPOPROTEIN B; ATORVASTATIN; LIPOPROTEIN; LIPOPROTEIN LIPASE; LOW DENSITY LIPOPROTEIN; PHOSPHOLIPASE A2; PRAVASTATIN; SPHINGOMYELIN PHOSPHODIESTERASE;

ACUTE CORONARY SYNDROME; ATHEROGENESIS; ATHEROSCLEROSIS; CLINICAL TRIAL; HUMAN; INFLAMMATION; LIPOPROTEIN BLOOD LEVEL; MACROPHAGE; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; SUBENDOTHELIUM; T LYMPHOCYTE;

ANIMALS; APOLIPOPROTEINS B; ATHEROSCLEROSIS; ENDOTHELIUM, VASCULAR; HUMANS; LIPOPROTEIN(A);

EID: 37349021003     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.106.676890     Document Type: Review

References (133)

1. Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol. 1995;15:551-561.
2. Williams KJ, Tabas I. Lipoprotein retention-and clues for atheroma regression. Arterioscler Thromb Vasc Biol. 2005;25:1536-1540.
3. Williams KJ. Arterial wall chondroitin sulfate proteoglycans: diverse molecules with distinct roles in lipoprotein retention and atherogenesis. Curr Opin Lipidol. 2001;12:477-487.
4. Khalil MF, Wagner WD, Goldberg IJ. Molecular interactions leading to lipoprotein retention and the initiation of atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:2211-2218.
5. Chait A, Wight TN. Interaction of native and modified low-density lipoproteins with extracellular matrix. Curr Opin Lipidol. 2000;11:457-463.
6. Tabas I. Secretory sphingomyelinase. Chem Phys Lipids. 1999;102:123-130.
7. Pentikainen MO, Oksjoki R, Oorni K, Kovanen PT. Lipoprotein lipase in the arterial wall: linking LDL to the arterial extracellular matrix and much more. Arterioscler Thromb Vasc Biol. 2002;22:211-217.
8. Rosengren B, Jonsson-Rylander AC, Peilot H, Camejo G, Hurt-Camejo E. Distinctiveness of secretory phospholipase A2 group IIA and V suggesting unique roles in atherosclerosis. Biochim Biophys Acta. 2006;1761:1301-1308.
9. Skålén K, Gustafsson M, Rydberg EK, Hulten LM, Wiklund O, Innerarity TL, Borén J. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature. 2002;417:750-754.
10. Vikramadithyan RK, Kako Y, Chen G, Hu Y, Rikawa-Hirasawa E, Yamada Y, Goldberg IJ. Atherosclerosis in perlecan heterozygous mice. J Lipid Res. 2004;45:1806-1812.
11. Nakashima Y, Fujii H, Sumiyoshi S, Wight TN, Sueishi K. Early human atherosclerosis: accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler Thromb Vasc Biol. 2007;27:986-989.
12. Nakashima Y, Chen YX, Kinukawa N, Sueishi K. Distributions of diffuse intimal thickening in human arteries: preferential expression in atherosclerosis-prone arteries from an early age. Virchows Arch. 2002;441:279-288.
13. Napoli C, D'Armiento FP, Mancini FP, Postiglione A, Witztum JL, Palumbo G, Palinski W. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia: intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J Clin Invest. 1997;100:2680-2690.
14. Gotto AM Jr, LaRosa JC. The benefits of statin therapy: what questions remain? Clin Cardiol. 2005;28:499-503.
15. Hackam DG. Intensive reduction of low-density lipoprotein-cholesterol: implications of recent trials. Am J Cardiovasc Drugs. 2006;6:367-371.
16. Ford ES, Ajani UA, Croft JB, Critchley JA, Labarthe DR, Kottke TE, Giles WH, Capewell S. Explaining the decrease in U.S. deaths from coronary disease, 1980-2000. N Engl J Med. 2007;356:2388-2398.
17. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med. 1999;340:115-126.
18. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
19. Perez RL, Rivera-Marrero CA, Roman J. Pulmonary granulomatous inflammation: from sarcoidosis to tuberculosis. Semin Respir Infect. 2003;18:23-32.
20. Blankenberg S, Yusuf S. The inflammatory hypothesis: any progress in risk stratification and therapeutic targets? Circulation. 2006;114:1557-1560.
21. Hajra L, Evans AI, Chen M, Hyduk SJ, Collins T, Cybulsky MI. The NF-kappa B signal transduction pathway in aortic endothelial cells is primed for activation in regions predisposed to atherosclerotic lesion formation. Proc Natl Acad Sci U S A. 2000;97:9052-9057.
22. Orr AW, Sanders JM, Bevard M, Coleman E, Sarembock IJ, Schwartz MA. The subendothelial extracellular matrix modulates NF-kappaB activation by flow: a potential role in atherosclerosis. J Cell Biol. 2005;169:191-202.
23. Schonbeck U, Libby P Inflammation, immunity, and HMG-CoA reductase inhibitors: statins as antiinflammatory agents? Circulation. 2004;109(suppl II):II-18-II-26.
24. Sirtori CR, Calabresi L, Marchioli R, Rubins HB. Cardiovascular risk changes after lipid lowering medications: are they predictable? Atherosclerosis. 2000;152:1-8.
25. Cohen JC, Boerwinkle E, Mosley TH Jr, Hobbs HH. Sequence variations in PCSK9, low LDL, and protection against coronary heart disease. N Engl J Med. 2006;354:1264-1272.
26. Ray KK, Cannon CP, Ganz P. Beyond lipid lowering: what have we learned about the benefits of statins from the acute coronary syndromes trials? Am J Cardiol. 2006;98:18P-25P.
27. Williams KJ, Feig JE, Fisher EA. Rapid regression of atherosclerosis: insights from the clinical and experimental literature. Nat Clin Pract Cardiovasc Med. In press.
28. Glass CK, Witztum JL. Atherosclerosis. the road ahead. Cell. 2001;104:503-516.
29. Lusis AJ. Atherosclerosis Nature. 2000;407:233-241.
30. Rader DJ. Molecular regulation of HDL metabolism and function: implications for novel therapies. J Clin Invest. 2006;116:3090-3100.
31. Williams KJ, Tabas I. The response-to-retention hypothesis of atherogenesis, reinforced. Curr Opin Lipidol. 1998;9:471-474.
32. Gustafsson M, Flood C, Jirholt P, Borén J. Retention of atherogenic lipoproteins in atherogenesis. Cell Mol Life Sci. 2004;61:4-9.
33. Camejo G, Hurt-Camejo E, Wiklund O, Bondjers G. Association of apo B lipoproteins with arterial proteoglycans: pathological significance and molecular basis. Atherosclerosis. 1998;139:205-222.
34. Kanter JE, Johansson F, LeBoeuf RC, Bornfeldt KE. Do glucose and lipids exert independent effects on atherosclerotic lesion initiation or progression to advanced plaques? Circ Res. 2007;100:769-781.
35. Camejo G, Olsson U, Hurt-Camejo E, Baharamian N, Bondjers G. The extracellular matrix on atherogenesis and diabetes-associated vascular disease. Atheroscler Suppl. 2002;3:3-9.
36. Tannock LR, Chait A. Lipoprotein-matrix interactions in macrovascular disease in diabetes. Front Biosci. 2004;9:1728-1742.
37. MRC/BHF Heart Protection Study of cholesterol lowering with simvastatin in 20,536 high-risk individuals: a randomised placebo-controlled trial. Lancet. 2002;360:7-22.
38. Roberts WC. Preventing and arresting coronary atherosclerosis. Am Heart J. 1995;130:580-600.
39. Linton MF, Farese RV Jr, Young SG. Familial hypobetalipoproteinemia. J Lipid Res. 1993;34:521-541.
40. Genser B, Marz W. Low density lipoprotein cholesterol, statins and cardiovascular events: a meta-analysis. Clin Res Cardiol. 2006;95:393-404.
41. LaRosa JC. Means and ends of statins and low-density lipoprotein cholesterol lowering. J Am Coll Cardiol. 2007;50:419-420.
42. Wiviott SD, Cannon CP, Morrow DA, Ray KK, Pfeffer MA, Braunwald E. Can low-density lipoprotein be too low? The safety and efficacy of achieving very low low-density lipoprotein with intensive statin therapy: a PROVE IT-TIMI 22 substudy. J Am Coll Cardiol. 2005;46:1411-1416.
43. Leeper NJ, Ardehali R, Degoma EM, Heidenreich PA. Statin use in patients with extremely low low-density lipoprotein levels is associated with improved survival. Circulation. 2007;116:613-618.
44. Kuvin JT, Patel AR, Sliney KA, Pandian NG, Karas RH. Comparison of flow-mediated dilatation of the brachial artery in coronary patients with low-density lipoprotein cholesterol levels <80 mg/dl versus patients with levels 80 to 100 mg/dl. Am J Cardiol. 2005;95:93-95.
45. Angeli V, Llodra J, Rong JX, Satoh K, Ishii S, Shimizu T, Fisher EA, Randolph GJ. Dyslipidemia associated with atherosclerotic disease systemically alters dendritic cell mobilization. Immunity. 2004;21:561-574.
46. McCrindle BW, Urbina EM, Dennison BA, Jacobson MS, Steinberger J, Rocchini AP, Hayman LL, Daniels SR. Drug therapy of high-risk lipid abnormalities in children and adolescents: a scientific statement from the American Heart Association Atherosclerosis, Hypertension, and Obesity in Youth Committee, Council of Cardiovascular Disease in the Young, with the Council on Cardiovascular Nursing. Circulation. 2007;115:1948-1967.
47. Thavendiranathan P, Bagai A, Brookhart MA, Choudhry NK. Primary prevention of cardiovascular diseases with statin therapy: a meta-analysis of randomized controlled trials. Arch Intern Med. 2006;166:2307-2313.
48. Lauer MS. Primary prevention of atherosclerotic cardiovascular disease: the high public burden of low individual risk. JAMA. 2007;297:1376-1378.
49. Lloyd-Jones DM, Leip EP, Larson MG, D'Agostino RB, Beiser A, Wilson PW, Wolf PA, Levy D. Prediction of lifetime risk for cardiovascular disease by risk factor burden at 50 years of age. Circulation. 2006;113:791-798.
50. Loria CM, Liu K, Lewis CE, Hulley SB, Sidney S, Schreiner PJ, Williams OD, Bild DE, Detrano R. Early adult risk factor levels and subsequent coronary artery calcification. J Am Coll Cardiol. 2007;49:2013-2020.
51. Avis HJ, Vissers MN, Stein EA, Wijburg FA, Trip MD, Kastelein JJ, Hutten BA. A systematic review and meta-analysis of statin therapy in children with familial hypercholesterolemia. Arterioscler Thromb Vasc Biol. 2007;27:1803-1810.
52. Rodenburg J, Vissers MN, Wiegman A, van Trotsenburg AS, van der GA, de GE, Wijburg FA, Kastelein JJ, Hutten BA. Statin treatment in children with familial hypercholesterolemia: the younger, the better. Circulation. 2007;116:664-668.
53. Twickler T, Dallinga-Thie GM, Chapman MJ, Cohn JS. Remnant lipoproteins and atherosclerosis. Curr Atheroscler Rep. 2005;7:140-147.
54. Anuurad E, Boffa MB, Koschinsky ML, Berglund L. Lipoprotein(a): a unique risk factor for cardiovascular disease. Clin Lab Med. 2006;26:751-772.
55. Lundstam U, Hurt-Camejo E, Olsson G, Sartipy P, Camejo G, Wiklund O. Proteoglycans contribution to association of Lp (a) and LDL with smooth muscle cell extracellular matrix. Arterioscler Thromb Vasc Biol. 1999;19:1162-1167.
56. Edelstein C, Yousef M, Scanu AM. Elements in the C terminus of apolipoprotein [a] responsible for the binding to the tenth type III module of human fibronectin. J Lipid Res. 2005;46:2673-2680.
57. Tsimikas S, Brilakis ES, Miller ER, McConnell JP, Lennon RJ, Kornman KS, Witztum JL, Berger PB. Oxidized phospholipids, Lp (a) lipoprotein, and coronary artery disease. N Engl J Med. 2005;353:46-57.
58. Tsimikas S, Kiechl S, Willeit J, Mayr M, Miller ER, Kronenberg F, Xu Q, Bergmark C, Weger S, Oberhollenzer F, Witztum JL. Oxidized phospholipids predict the presence and progression of carotid and femoral atherosclerosis and symptomatic cardiovascular disease: five-year prospective results from the Bruneck study. J Am Coll Cardiol. 2006;47:2219-2228.
59. Angelin B. Therapy for lowering lipoprotein (a) levels. Curr Opin Lipidol. 1997;8:337-341.
60. Moreton JR. Atherosclerosis and alimentary hyperlipidemia. Science. 1947;106:190-191.
61. Zilversmit DB. Atherogenesis: a postprandial phenomenon. Circulation. 1979;60:473-485.
62. Rapp JH, Lespine A, Hamilton RL, Colyvas N, Chaumeton AH, Tweedie-Hardman J, Kotite L, Kunitake ST, Havel RJ, Kane JP. Triglyceride-rich lipoproteins isolated by selected-affinity antiapolipoprotein B immunosorption from human atherosclerotic plaque. Arterioscler Thromb. 1994;14:1767-1774.
63. Chung BH, Tallis G, Yalamoori V, Anantharamaiah GM, Segrest JP. Liposome-like particles isolated from human atherosclerotic plaques are structurally and compositionally similar to surface remnants of triglyceride-rich lipoproteins. Arterioscler Thromb. 1994;14:622-635.
64. Xi H, Akishita M, Nagai K, Yu W, Hasegawa H, Eto M, Kozaki K, Toba K. Potent free radical scavenger, edaravone, suppresses oxidative stress-induced endothelial damage and early atherosclerosis. Atherosclerosis. 2007;191:281-289.
65. Tso C, Martinic G, Fan WH, Rogers C, Rye KA, Barter PJ. High-density lipoproteins enhance progenitor-mediated endothelium repair in mice. Arterioscler Thromb Vasc Biol. 2006;26:1144-1149.
66. Kolovou GD, Anagnostopoulou KK, Salpea KD, Daskalopoulou SS, Mikhailidis DP. The effect of statins on postprandial lipemia. Curr Drug Targets. 2007;8:551-560.
67. Bays HE, Ose L, Fraser N, Tribble DL, Quinto K, Reyes R, Johnson-Levonas AO, Sapre A, Donahue SR. A multicenter, randomized, double-blind, placebo-controlled, factorial design study to evaluate the lipid-altering efficacy and safety profile of the ezetimibe/simvastatin tablet compared with ezetimibe and simvastatin monotherapy in patients with primary hypercholesterolemia. Clin Ther. 2004;26:1758-1773.
68. Abbasi F, Chu JW, McLaughlin T, Lamendola C, Leary ET, Reaven GM. Effect of metformin treatment on multiple cardiovascular disease risk factors in patients with type 2 diabetes mellitus. Metabolism. 2004;53:159-164.
69. MacArthur JM, Bishop JR, Stanford KI, Wang L, Bensadoun A, Witztum JL, Esko JD. Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J Clin Invest. 2007;117:153-164.
70. Beigneux AP, Davies BS, Gin P, Weinstein MM, Farber E, Qiao X, Peale F, Bunting S, Walzem RL, Wong JS, Blaner WS, Ding ZM, Melford K, Wongsiriroj N, Shu X, de Sauvage F, Ryan RO, Fong LG, Bensadoun A, Young SG. Glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons. Cell Metab. 2007;5:279-291.
71. Williams KJ, Fuki IV. Cell-surface heparan sulfate proteoglycans: dynamic molecules mediating ligand catabolism. Curr Opin Lipidol. 1997;8:253-262.
72. Anisfeld AM, Kast-Woelbern HR, Meyer ME, Jones SA, Zhang Y, Williams KJ, Willson T, Edwards PA. Syndecan-1 expression is regulated in an isoform-specific manner by the farnesoid-X receptor. J Biol Chem. 2003;278:20420-20428.
73. Williams KJ, Liu ML, Zhu Y, Xu X, Davidson WR, McCue P, Sharma K. Loss of heparan N-sulfotransferase in diabetic liver: role of angiotensin II. Diabetes. 2005;54:1116-1122.
74. Berneis KK, Krauss RM. Metabolic origins and clinical significance of LDL heterogeneity. J Lipid Res. 2002;43:1363-1379.
75. Kuznetsov AS, Missyul BV. The charge and atherogenicity of low density lipoproteins. Ukr Biokhim Zh. 1992;64:3-19.
76. Orr AW, Stockton R, Simmers MB, Sanders JM, Sarembock IJ, Blackman BR, Schwartz MA. Matrix-specific p21-activated kinase activation regulates vascular permeability in atherogenesis. J Cell Biol. 2007;176:719-727.
77. Zilversmit DB. Atherogenic nature of triglycerides, postprandial lipidemia, and triglyceride-rich remnant lipoproteins. Clin Chem. 1995;41:153-158.
78. Proctor SD, Vine DF, Mamo JC. Arterial retention of apolipoprotein B(48)- and B(100)-containing lipoproteins in atherogenesis. Curr Opin Lipidol. 2002;13:461-470.
79. Hurt-Camejo E, Camejo G, Sartipy P. Phospholipase A2 and small, dense low-density lipoprotein. Curr Opin Lipidol. 2000;11:465-471.
80. Flood C, Gustafsson M, Pitas RE, Arnaboldi L, Walzem RL, Borén J. Molecular mechanism for changes in proteoglycan binding on compositional changes of the core and the surface of low-density lipoprotein-containing human apolipoprotein B100. Arterioscler Thromb Vasc Biol. 2004;24:564-570.
81. Schwenke DC, Carew TE. Initiation of atherosclerotic lesions in cholesterol-fed rabbits, II: selective retention of LDL vs. selective increases in LDL permeability in susceptible sites of arteries. Arteriosclerosis. 1989;9:908-918.
82. Nielsen LB, Nordestgaard BG, Stender S, Kjeldsen K. Aortic permeability to LDL as a predictor of aortic cholesterol accumulation in cholesterol-fed rabbits. Arterioscler Thromb. 1992;12:1402-1409.
83. Weinberg PD. Rate-limiting steps in the development of atherosclerosis: the response-to-influx theory. J Vasc Res. 2004;41:1-17.
84. Bretherton KN, Day AJ, Skinner SL. Effect of hypertension on the entry of 125 I-labelled low density lipoprotein into the aortic intima in normal-fed rabbits. Atherosclerosis. 1976;24:99-106.
85. Simionescu M. Implications of early structural-functional changes in the endothelium for vascular disease. Arterioscler Thromb Vasc Biol. 2007;27:266-274.
86. Chen YL, Jan KM, Lin HS, Chien S. Relationship between endothelial cell turnover and permeability to horseradish peroxidase. Atherosclerosis. 1997;133:7-14.
87. Goldschmidt-Clermont PJ, Creager MA, Losordo DW, Lam GK, Wassef M, Dzau VJ. Atherosclerosis 2005: recent discoveries and novel hypotheses. Circulation. 2005;112:3348-3353.
88. Galis ZS, Alavi MZ, Moore S. Co-localization of aortic apolipoprotein B and chondroitin sulfate in an injury model of atherosclerosis. Am J Pathol. 1993;142:1432-1438.
89. Cardoso LE, Mourao PA. Glycosaminoglycan fractions from human arteries presenting diverse susceptibilities to atherosclerosis have different binding affinities to plasma LDL. Arterioscler Thromb. 1994;14:115-124.
90. Talusan P, Bedri S, Yang S, Kattapuram T, Silva N, Roughley PJ, Stone JR. Analysis of intimal proteoglycans in atherosclerosis-prone and atherosclerosis-resistant human arteries by mass spectrometry. Mol Cell Proteomics. 2005;4:1350-1357.
91. Borén J, Olin K, Lee I, Chait A, Wight TN, Innerarity TL. Identification of the principal proteoglycan-binding site in LDL: a single-point mutation in apo-B100 severely affects proteoglycan interaction without affecting LDL receptor binding. J Clin Invest. 1998;101:2658-2664.
92. Flood C, Gustafsson M, Richardson PE, Harvey SC, Segrest JP, Borén J. Identification of the proteoglycan binding site in apolipoprotein B48. J Biol Chem. 2002;277:32228-32233.
93. Goldberg IJ, Wagner WD, Pang L, Paka L, Curtiss LK, DeLozier JA, Shelness GS, Young CS, Pillarisetti S. The NH2-terminal region of apolipoprotein B is sufficient for lipoprotein association with glycosaminoglycans. J Biol Chem. 1998;273:35355-35361.
94. 93a. 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. August 30, 2007. DOI: 10.1161/CIRCRESAHA.107.149666. Available at http://circres.ahajournals.org. Accessed September 18, 2007.
95. Schwenke DC, Carew TE. Initiation of atherosclerotic lesions in cholesterol-fed rabbits, I: focal increases in arterial LDL concentrations precede development of fatty streak lesions. Arteriosclerosis. 1989;9:895-907.
96. Chang MY, Olin KL, Tsoi C, Wight TN, Chait A. Human monocytederived macrophages secrete two forms of proteoglycan-macrophage colony-stimulating factor that differ in their ability to bind low density lipoproteins. J Biol Chem. 1998;273:15985-15992.
97. Maor I, Hayek T, Hirsh M, Iancu TC, Aviram M. Macrophage-released proteoglycans enhance LDL aggregation: studies in aorta from apolipoprotein E-deficient mice. Atherosclerosis. 2000;150:91-101.
98. Lees AM, Deconinck AE, Campbell BD, Lees RS. Atherin: a newly identified, lesion-specific, LDL-binding protein in human atherosclerosis. Atherosclerosis. 2005;182:219-230.
99. Auerbach BJ, Bisgaier CL, Wolle J, Saxena U. Oxidation of low density lipoproteins greatly enhances their association with lipoprotein lipase anchored to endothelial cell matrix. J Biol Chem. 1996;271:1329-1335.
100. Sneck M, Kovanen PT, Oorni K. Decrease in pH strongly enhances binding of native, proteolyzed, lipolyzed, and oxidized low density lipoprotein particles to human aortic proteoglycans. J Biol Chem. 2005;280:37449-37454.
101. Al Haj ZA, Caligiuri G, Sainz J, Lemitre M, Demerens C, Lafont A. Decorin overexpression reduces atherosclerosis development in apolipoprotein E-deficient mice. Atherosclerosis. 2006;187:31-39.
102. Little PJ, Tannock L, Olin KL, Chait A, Wight TN. Proteoglycans synthesized by arterial smooth muscle cells in the presence of transforming growth factor-beta1 exhibit increased binding to LDLs. Arterioscler Thromb Vasc Biol. 2002;22:55-60.
103. Kunjathoor VV, Chiu DS, O'Brien KD, LeBoeuf RC. Accumulation of biglycan and perlecan, but not versican, in lesions of murine models of atherosclerosis. Arterioscler Thromb Vasc Biol. 2002;22:462-468.
104. Saxena U, Auerbach BJ, Ferguson E, Wolle J, Marcel YL, Weisgraber KH, Hegele RA, Bisgaier CL. Apolipoprotein B and E basic amino acid clusters influence low-density lipoprotein association with lipoprotein lipase anchored to the subendothelial matrix. Arterioscler Thromb Vasc Biol. 1995;15:1240-1247.
105. Zeng X, Chen J, Miller YI, Javaherian K, Moulton KS. Endostatin binds biglycan and LDL and interferes with LDL retention to the subendothelial matrix during atherosclerosis. J Lipid Res. 2005;46:1849-1859.
106. Fredrikson GN, Soderberg I, Lindholm M, Dimayuga P, Chyu KY, Shah PK, Nilsson J. Inhibition of atherosclerosis in apoE-null mice by immunization with apoB-100 peptide sequences. Arterioscler Thromb Vasc Biol. 2003;23:879-884.
107. Little PJ, Ballinger ML, Osman N. Vascular wall proteoglycan synthesis and structure as a target for the prevention of atherosclerosis. Vasc Health Risk Manag. 2007;3:117-124.
108. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12:1075-1080.
109. Olsson U, Bondjers G, Camejo G. Fatty acids modulate the composition of extracellular matrix in cultured human arterial smooth muscle cells by altering the expression of genes for proteoglycan core proteins. Diabetes. 1999;48:616-622.
110. Rodriguez-Lee M, Ostergren-Lunden G, Wallin B, Moses J, Bondjers G, Camejo G. Fatty acids cause alterations of human arterial smooth muscle cell proteoglycans that increase the affinity for low-density lipoprotein. Arterioscler Thromb Vasc Biol. 2006;26:130-135.
111. Merrilees M, Beaumont B, Scott L, Hermanutz V, Fennessy P. Effect of TGF-beta(1) antisense S-oligonucleotide on synthesis and accumulation of matrix proteoglycans in balloon catheter-injured neointima of rabbit carotid arteries. J Vasc Res. 2000;37:50-60.
112. Goldberg IJ. Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J Lipid Res. 1996;37:693-707.
113. Williams KJ, Fless GM, Petrie KA, Snyder ML, Brocia RW, Swenson TL. Mechanisms by which lipoprotein lipase alters cellular metabolism of lipoprotein(a), low density lipoprotein, and nascent lipoproteins: roles for low density lipoprotein receptors and heparan sulfate proteoglycans. J Biol Chem. 1992;267:13284-13292.
114. Oorni K, Pentikainen MO, Annila A, Kovanen PT. Oxidation of low density lipoprotein particles decreases their ability to bind to human aortic proteoglycans: dependence on oxidative modification of the lysine residues. J Biol Chem. 1997;272:21303-21311.
115. Tabas I, Li Y, Brocia RW, Wu SW, Swenson TL, Williams KJ. Lipoprotein lipase and sphingomyelinase synergistically enhance the association of atherogenic lipoproteins with smooth muscle cells and extracellular matrix: a possible mechanism for low density lipoprotein and lipoprotein(a) retention and macrophage foam cell formation. J Biol Chem. 1993;268:20419-20432.
116. Clee SM, Bissada N, Miao F, Miao L, Marais AD, Henderson HE, Steures P, McManus J, McManus B, LeBoeuf RC, Kastelein JJ, Hayden MR. Plasma and vessel wall lipoprotein lipase have different roles in atherosclerosis. J Lipid Res. 2000;41:521-531.
117. Semenkovich CF, Coleman T, Daugherty A. Effects of heterozygous lipoprotein lipase deficiency on diet-induced atherosclerosis in mice. J Lipid Res. 1998;39:1141-1151.
118. Babaev VR, Patel MB, Semenkovich CF, Fazio S, Linton MF. Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in low density lipoprotein receptor-deficient mice. J Biol Chem. 2000;275:26293-26299.
119. Wu X, Wang J, Fan J, Chen M, Chen L, Huang W, Liu G. Localized vessel expression of lipoprotein lipase in rabbits leads to rapid lipid deposition in the balloon-injured arterial wall. Atherosclerosis. 2006;187:65-73.
120. Wang J, Xian X, Huang W, Chen L, Wu L, Zhu Y, Fan J, Ross C, Hayden MR, Liu G. Expression of LPL in endothelial-intact artery results in lipid deposition and vascular cell adhesion molecule-1 upregulation in both LPL and ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 2007;27:197-203.
121. Oorni K, Pentikainen MO, Ala-Korpela M, Kovanen PT. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J Lipid Res. 2000;41:1703-1714.
122. Schissel SL, Jiang XC, Tweedie-Hardman J, Jeong TS, Camejo EH, Najib J, Rapp JH, Williams KJ, Tabas I. Secretory sphingomyelinase, a product of the acid sphingomyelinase gene, can hydrolyze atherogenic lipoproteins at neutral pH: implications for atherosclerotic lesion development. J Biol Chem. 1998;273:2738-2746.
123. Jiang XC, Paultre F, Pearson TA, Reed RG, Francis CK, Lin M, Berglund L, Tall AR. Plasma sphingomyelin level as a risk factor for coronary artery disease. Arterioscler Thromb Vasc Biol. 2000;20:2614-2618.
124. Boyanovsky BB, van der Westhuyzen DR, Webb NR. Group V secretory phospholipase A2-modified low density lipoprotein promotes foam cell formation by a SR-A- and CD36-independent process that involves cellular proteoglycans. J Biol Chem. 2005;280:32746-32752.
125. Bostrom MA, Boyanovsky BB, Jordan CT, Wadsworth MP, Taatjes DJ, de Beer FC, Webb NR. Group V secretory phospholipase A2 promotes atherosclerosis: evidence from genetically altered mice. Arterioscler Thromb Vasc Biol. 2007;27:600-606.
126. Marathe S, Miranda SR, Devlin C, Johns A, Kuriakose G, Williams KJ, Schuchman EH, Tabas I. Creation of a mouse model for non-neurological (type B) Niemann-Pick disease by stable, low level expression of lysosomal sphingomyelinase in the absence of secretory sphingomyelinase: relationship between brain intra-lysosomal enzyme activity and central nervous system function. Hum Mol Genet. 2000;9:1967-1976.
127. Issandou M. Pharmacological regulation of low density lipoprotein receptor expression: current status and future developments. Pharmacol Ther. 2006;111:424-433.
128. Williams KJ, Fisher EA. Atherosclerosis: cell biology and lipoproteins: three distinct processes that control apolipoprotein-B secretion. Curr Opin Lipidol. 2001;12:235-237.
129. Zimmermann TS, Lee AC, Akinc A, Bramlage B, Bumcrot D, Fedoruk MN, Harborth J, Heyes JA, Jeffs LB, John M, Judge AD, Lam K, McClintock K, Nechev LV, Palmer LR, Racie T, Rohl I, Seiffert S, Shanmugam S, Sood V, Soutschek J, Toudjarska I, Wheat AJ, Yaworski E, Zedalis W, Koteliansky V, Manoharan M, Vornlocher HP, MacLachlan I. RNAi-mediated gene silencing in non-human primates. Nature. 2006;441:111-114.
130. Data demonstrate in vivo activity with systemic RNAi therapeutics targeting PCSK9 for hypercholesterolemia: advancements with antagomirs, potential RNAi therapeutics that target microRNAs. Alnylam Pharmaceuticals. Available at: http://phx.corporate-ir.net/phoenix.zhtml?c=148005&pirol-news Article&ID=919540&highlight=. Accessed June 2007.
131. Wyler von Ballmoos M, Dubler D, Mirlacher M, Cathomas G, Muser J, Biedermann BC. Increased apolipoprotein deposits in early atherosclerotic lesions distinguish symptomatic from asymptomatic patients. Arterioscler Thromb Vasc Biol. 2006;26:359-364.
132. Bragdon JH, Boyle E, Havel RJ. Human serum lipoproteins, II: some effects of their intravenous injection in rats. J Lab Clin Med. 1956;48:43-50.
133. Nievelstein PFEM, Fogelman AM, Mottino G, Frank JS. Lipid accumulation in rabbit aortic intima 2 hours after bolus infusion of low density lipoprotein. Arterioscler Thromb. 1991;11:1795-1805.