High-density lipoproteins, platelets and the pathogenesis of atherosclerosis: Frontiers in research review: Physiological and pathological functions of high-density lipoprotein

Clinical and Experimental Pharmacology and Physiology

Volumn 37, Issue 7, 2010, Pages 726-735

  Nofer, Jerzy Roch ^a,b   Brodde, Martin F ^a   Kehrel, Beate E ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

atherosclerosis; high density lipoprotein; platelets

Indexed keywords

APOLIPOPROTEIN E; FIBRIC ACID DERIVATIVE; FIBRINOGEN; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; NICOTINIC ACID; NITRIC OXIDE; OXIDIZED HIGH DENSITY LIPOPROTEIN; PROTEIN KINASE C; SCAVENGER RECEPTOR BI; THROMBOXANE A2; UNCLASSIFIED DRUG; CHOLESTEROL;

ANTIOXIDANT ACTIVITY; ATHEROSCLEROTIC PLAQUE; CELL FUNCTION; CELL INTERACTION; CHOLESTEROL TRANSPORT; CORONARY ARTERY ATHEROSCLEROSIS; CORONARY ARTERY OBSTRUCTION; CORONARY ARTERY THROMBOSIS; DRUG MECHANISM; HUMAN; NONHUMAN; PATHOGENESIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; RECURRENT DISEASE; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOGENESIS; VENOUS THROMBOEMBOLISM; ANIMAL; ATHEROSCLEROSIS; BLOOD; CORONARY ARTERY DISEASE; CORONARY OCCLUSION; FEMALE; MALE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; RABBIT; RAT; TRANSPORT AT THE CELLULAR LEVEL; VASCULAR ENDOTHELIUM;

ANIMALS; ATHEROSCLEROSIS; BIOLOGICAL TRANSPORT; BLOOD PLATELETS; CHOLESTEROL; CORONARY ARTERY DISEASE; CORONARY OCCLUSION; ENDOTHELIUM, VASCULAR; FEMALE; FIBRINOGEN; HUMANS; LIPOPROTEINS, HDL; MALE; MICE; PLATELET AGGREGATION; RABBITS; RATS; VENOUS THROMBOEMBOLISM;

EID: 77953865873     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2010.05377.x     Document Type: Review

References (116)

1. Assmann G, Nofer JR. Atheroprotective effects of high-density lipoproteins. Annu. Rev. Med. 2003 54: 321 341.
2. Genest Jr. JJ, Martin-Munley SS, McNamara JR et al. Familial lipoprotein disorders in patients with premature coronary artery disease. Circulation 1992 85: 2025 2033.
3. Remaley AT, Amar M, Sviridov D. HDL-replacement therapy: Mechanism of action, types of agents and potential clinical indications. Expert Rev. Cardiovasc. Ther. 2008 6: 1203 1215.
4. Duffy D, Rader DJ. Update on strategies to increase HDL quantity and function. Nat. Rev. Cardiol. 2009 6: 455 463.
5. Marcil M, Bissonnette R, Vincent J, Krimbou L, Genest J. Cellular phospholipid and cholesterol efflux in high-density lipoprotein deficiency. Circulation 2003 107: 1366 1371.
6. von Eckardstein A, Nofer JR, Assmann G. High density lipoproteins and arteriosclerosis. Role of cholesterol efflux and reverse cholesterol transport. Arterioscler. Thromb. Vasc. Biol. 2001 21: 13 27.
7. von Rokitansky C. A Manual of Pathological Anatomy. Sydeham Society
8. Carstairs KC, Woolf N. The identification of platelets and platelet antigens in histological sections. J. Pathol. Bacteriol. 1965 90: 225 231.
9. Craig HI, Bell EP, Goldsmith CH, Schwartz CJ. Thrombosis and atherosclerosis. The organization of pulmonary thrombi in pig. Atherosclerosis 1973 18: 277 300.
10. Craig HI, Schwartz CJ. Contribution of thrombus free and esterified cholesterol to atherosclerotic plaques. Pathology 1972 4: 303 306.
11. Friedman RJ, Stemernman MD, Wenz B et al. The effect of thrombocytopenia on experimental atherosclerotic lesion formation in rabbits. J. Clin. Invest. 1977 60: 1191 1201.
12. Fuster V, Bowie WJ, Lewis JC, Fass DN, Owen CA, Brown AL. Resistance to arteriosclerosis in pigs with von Willebrand disease. Spontaneus and high cholestarol-diet induced atherosclerosis. J. Clin. Invest. 1978 61: 722 730.
13. Theilmeier G, Michiels C, Spaepen E et al. Endothelial von Willebrand factor recruits platelets to atherosclerosis-prone sites in response to hypercholesterolemia. Blood 2002 99: 4486 4493.
14. Bombeli T, Schwartz BR, Harlan JM. Adhesion of activated platelets to endothelial cells. Evidence for a GPIIbIIIa-dependent bridging mechanism and novel roles for endothelial intercellular adhesion molecule 1 (ICAM-1), alphavbeta3 integrin, and GPIbalpha. J. Exp. Med. 1998 187: 329 339.
15. Frenette PS, Johnson RC, Hynes RO, Wagner DD. Platelets roll on stimulated endothelium in vivo: An interaction mediated by endothelial P-selectin. Proc. Natl Acad. Sci. USA 1995 92: 7450 7454.
16. Frenette PS, Denis CV, Weiss L et al. P-Selectin glycoprotein ligand 1 (PSGL-1) is expressed on platelets and can mediate platelet-endothelial interactions in vivo. J. Exp. Med. 2000 191: 1413 1422.
17. Gawaz M, Neumann FJ, Dickfeld T et al. Vitronectin receptor (alpha (v) beta3) mediates platelet adhesion to the luminal aspect of endothelial cells: Implications for reperfusion in acute myocardial infarction. Circulation 1997 96: 1809 1818.
18. Lindemann S, Tolley ND, Dixon DA et al. Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis. J. Cell Biol. 2001 154: 485 490.
19. Henn V, Slupsky JR, Gräfe M et al. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 1998 391: 591 594.
20. May AE, Kälsch T, Massberg S, Herouy Y, Schmidt R, Gawaz M. Engagement of glycoprotein IIb/IIIa (alpha (IIb) beta3) on platelets upregulates CD40L and triggers CD40L-dependent matrix degradation by endothelial cells. Circulation 2002 106: 2111 2117.
21. von Hundelshausen P, Koenen RR, Sack M et al. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005 105: 924 930.
22. von Hundelshausen P, Weber KS, Huo Y et al. RANTES deposition by platelets triggers monocyte arrest on inflamed and atherosclerotic endothelium. Circulation 2001 103: 1772 1777. (Pubitemid 32291415)
23. Schober A, Manka D, von Hundelshausen P et al. Deposition of platelet RANTES triggering monocyte recruitment requires P-selectin and is involved in neointima formation after arterial injury. Circulation 2002 106: 1523 1529.
24. Baltus T, von Hundelshausen P, Mause SF, Buhre W, Rossaint R, Weber C. Differential and additive effects of platelet-derived chemokines on monocyte arrest on inflamed endothelium under flow conditions. J. Leukoc. Biol. 2005 78: 435 441.
25. Zernecke A, Schober A, Bot I et al. SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ. Res. 2005 96: 784 791.
26. + cells to endothelial progenitor cells. Circulation 2008 117: 206 215.
27. + progenitor cells into foam cells and endothelial cells. FASEB J. 2006 20: 2559 2561.
28. Kruth HS. Platelet-mediated cholesterol accumulation in cultured aortic smooth muscle cells. Science 1985 227: 1243 1245.
29. Curtiss LK, Black AS, Takagi Y, Plow EF. New mechanism for foam cell generation in atherosclerotic lesions. J. Clin. Invest. 1987 80: 367 373.
30. Burger PC, Wagner DD. Platelet P-selectin facilitates atherosclerotic lesion development. Blood 2003 101: 2661 2666.
31. Manka D, Forlow SB, Sanders JM et al. Critical role of platelet P-selectin in the response to arterial injury in apolipoprotein-E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2004 24: 1124 1129.
32. Huo Y, Schober A, Forlow SB et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat. Med. 2003 9: 61 7.
33. Dong ZM, Chapman SM, Brown AA, Frenette PS, Hynes RO, Wagner DD. The combined role of P-and E-selectins in atherosclerosis. J. Clin. Invest. 1998 102: 145 152.
34. Massberg S, Schürzinger K, Lorenz M et al. Platelet adhesion via glycoprotein IIb integrin is critical for atheroprogression and focal cerebral ischemia: An in vivo study in mice lacking glycoprotein IIb. Circulation 2005 112: 1180 1188.
35. Massberg S, Brand K, Grüner S et al. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J. Exp. Med. 2002 196: 887 896.
36. Koenen RR, von Hundelshausen P, Nesmelova IV et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat. Med. 2009 15: 97 103.
37. Naqvi TZ, Shah PK, Ivey PA et al. Evidence that high-density lipoprotein cholesterol is an independent predictor of acute platelet-dependent thrombus formation. Am. J. Cardiol. 1999 84: 1011 1017.
38. Lerch PG, Spycher MO, Doran JE. Reconstituted high density lipoprotein (rHDL) modulates platelet activity in vitro and ex vivo. Thromb. Haemost. 1998 80: 316 320.
39. Calkin AC, Drew BG, Ono A et al. Reconstituted high-density lipoprotein attenuates platelet function in individuals with type 2 diabetes mellitus by promoting cholesterol efflux. Circulation 2009 120: 2095 2104.
40. Li D, Weng S, Yang B et al. Inhibition of arterial thrombus formation by ApoA1 Milano. Arterioscler. Thromb. Vasc. Biol. 1999 19: 378 383.
41. Doggen CJ, Smith NL, Lemaitre RN, Heckbert SR, Rosendaal FR, Psaty BM. Serum lipid levels and the risk of venous thrombosis. Arterioscler. Thromb. Vasc. Biol. 2004 24: 1970 1975.
42. Deguchi H, Pecheniuk NM, Elias DJ, Averell PM, Griffin JH. High-density lipoprotein deficiency and dyslipoproteinemia associated with venous thrombosis in men. Circulation 2005 112: 893 899.
43. Eichinger S, Pecheniuk NM, Hron G et al. High-density lipoprotein and the risk of recurrent venous thromboembolism. Circulation 2007 115: 1609 1614. (Pubitemid 46648646)
44. Jang MJ, Choi WI, Bang SM et al. Metabolic syndrome is associated with venous thromboembolism in the Korean population. Arterioscler. Thromb. Vasc. Biol. 2009 29: 311 315.
45. Ageno W, Becattini C, Brighton T, Selby R, Kamphuisen PW. Cardiovascular risk factors and venous thromboembolism: A meta-analysis. Circulation 2008 117: 93 102.
46. Chamberlain AM, Folsom AR, Heckbert SR, Rosamond WD, Cushman M. High-density lipoprotein cholesterol and venous thromboembolism in the Longitudinal Investigation of Thromboembolism Etiology (LITE). Blood 2008 112: 2675 2680.
47. Harmon JT, Tandon NN, Hoeg JM, Jamieson GA. Thrombin binding and response in platelets from patients with dyslipoproteinemias: Increased stimulus-response coupling in type II hyperlipoproteinemia. Blood 1986 68: 498 505.
48. Nofer JR, Herminghaus G, Brodde M et al. Impaired platelet activation in familial high density lipoprotein deficiency (Tangier disease). J. Biol. Chem. 2004 279: 34.
49. Nofer JR, Walter M, Kehrel B et al. HDL3-mediated inhibition of thrombin-induced platelet aggregation and fibrinogen binding occurs via decreased production of phosphoinositide-derived second messengers 1,2-diacylglycerol and inositol 1,4,5-tris-phosphate. Arterioscler. Thromb. Vasc. Biol. 1998 18: 861 869.
50. Assinger A, Schmid W, Eder S, Schmid D, Koller E, Volf I. Oxidation by hypochlorite converts protective HDL into a potent platelet agonist. FEBS Lett. 2008 582: 778 784.
51. Surya II, Gorter G, Akkerman JW. Arachidonate transfer between platelets and lipoproteins. Thromb. Haemost. 1992 68: 719 726.
52. Higashihara M, Kinoshita M, Kume S, Teramoto T, Kurokawa K. Inhibition of platelet function by high-density lipoprotein from a patient with apolipoprotein E deficiency. Biochem. Biophys. Res. Commun. 1991 181: 1331 1336.
53. Fujimoto Y, Tsunomori M, Muta E et al. High density lipoprotein inhibits platelet 12-lipoxygenase activity. Res. Commun. Mol. Pathol. Pharmacol. 1994 85: 355 358.
54. Beitz J, Beitz A, Müller G, Giessler C, Mest HJ. Influence of HDL on the formation of 6-keto-PGF1 alpha and TXB2 in vitro: The importance of the source of HDL. Eicosanoids 1992 5: 53 6.
55. Aviram M, Brook JG. Platelet interaction with high and low density lipoproteins. Atherosclerosis 1983 46: 259 268.
56. Beitz A, Nikitina NA, Giessler C et al. Modulation of TXA2 generation of platelets by human lipoproteins. Prostaglandins Leukot. Essent. Fatty Acids 1990 40: 57 61.
57. Hassall DG, Owen JS, Bruckdorfer KR. The aggregation of isolated human platelets in the presence of lipoproteins and prostacyclin. Biochem. J. 1983 216: 43 9.
58. Valiyaveettil M, Kar N, Ashraf MZ, Byzova TV, Febbraio M, Podrez EA. Oxidized high-density lipoprotein inhibits platelet activation and aggregation via scavenger receptor BI. Blood 2008 111: 1962 1971.
59. 2) formation by washed human platelets under the influence of low and high density lipoproteins from healthy donors. Prostaglandins Leukot. Med. 1986 23: 303 309.
60. Desai K, Bruckdorfer KR, Hutton RA, Owen JS. Binding of apoE-rich high density lipoprotein particles by saturable sites on human blood platelets inhibits agonist-induced platelet aggregation. J. Lipid Res. 1989 30: 831 840.
61. Higashihara M, Kinoshita M, Teramoto T, Kume S, Kurokawa K. The role of apoE in inhibitory effects of apoE-rich HDL on platelet function. FEBS Lett. 1991 282: 82 6.
62. Koller E, Koller F, Binder BR. Purification and identification of the lipoprotein-binding proteins from human blood platelet membrane. J. Biol. Chem. 1989 264: 12.
63. Nofer JR, Walter M, Kehrel B, Seedorf U, Assmann G. HDL3 activates phospholipase D in normal but not in glycoprotein IIb/IIIa-deficient platelets. Biochem. Biophys. Res. Commun. 1995 207: 148 154.
64. Pedreño J, Vila M, Masana L. Mechanisms for regulating platelet high density lipoprotein type3 binding sites: Evidence that binding sites are downregulated by a protein kinase C-dependent mechanism. Thromb. Res. 1999 94: 33 44.
65. Pedreño J, de Castellarnau C, Masana L. Platelet HDL (3) binding sites are not related to integrin alpha (IIb) beta (3) (GPIIb-IIIa). Atherosclerosis 2001 154: 23 9.
66. Riddell DR, Vinogradov DV, Stannard AK, Chadwick N, Owen JS. Identification and characterization of LRP8 (apoER2) in human blood platelets. J. Lipid Res. 1999 40: 1925 1930.
67. Korporaal SJ, Relou IA, van Eck M et al. Binding of low density lipoprotein to platelet apolipoprotein E receptor 2′ results in phosphorylation of p38MAPK. J. Biol. Chem. 2004 279: 52.
68. Imachi H, Murao K, Cao W et al. Expression of human scavenger receptor B1 on and in human platelets. Arterioscler. Thromb. Vasc. Biol. 2003 23: 898 904.
69. Nofer JR, Brodde M, Korporaal SJ, Tietge UJ, van Eck M, Kehrel B. Native high density lipoproteins inhibit thrombin-induced platelet activation via scavenger receptor B1 (SR-B1). Clin. Chem. Lab. Med. 2009 47: A47.
70. + antiport in human platelets. Thromb. Haemost. 1996 75: 635 641.
71. Nazih H, Devred D, Martin-Nizard F, Fruchart JC, Delbart C. Phosphatidylcholine breakdown in HDL3 stimulated platelets. Thromb. Res. 1990 59: 913 920.
72. Nazih H, Devred D, Martin-Nizard F, Clavey V, Fruchart JC, Delbart C. Pertussis toxin sensitive G-protein coupling of HDL receptor to phospholipase C in human platelets. Thromb. Res. 1992 67: 559 567.
73. Riddell DR, Graham A, Owen JS. Apolipoprotein E inhibits platelet aggregation through the l-arginine-nitric oxide pathway. Implications for vascular disease. J. Biol. Chem. 1997 272: 89 95.
74. Relou AM, Gorter G, van Rijn HJ, Akkerman JW. Platelet activation by the apoB/E receptor-binding domain of LDL. Thromb. Haemost. 2002 87: 880 887.
75. Shao B, Oda MN, Vaisar T, Oram JF, Heinecke JW. Pathways for oxidation of high-density lipoprotein in human cardiovascular disease. Curr. Opin. Mol. Ther. 2006 8: 198 205.
76. Navab M, Hama SY, Anantharamaiah GM et al. Normal high density lipoprotein inhibits three steps in the formation of mildly oxidized low density lipoprotein: Steps 2 and 3. J. Lipid Res. 2000 41: 1495 1508.
77. Pennathur S, Bergt C, Shao B et al. 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: 42.
78. Bergt C, Pennathur S, Fu X et al. 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: 13.
79. Ardlie NG, Selley ML, Simons LA. Platelet activation by oxidatively modified low density lipoproteins. Atherosclerosis 1989 76: 117 124.
80. Takahashi Y, Chiba H, Matsuno K et al. Native lipoproteins inhibit platelet activation induced by oxidized lipoproteins. Biochem. Biophys. Res. Commun. 1996 222: 453 459.
81. Mallat Z, Benamer H, Hugel B et al. Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 2000 101: 841 843.
82. Martinez MC, Tesse A, Zobairi F, Andriantsitohaina R. Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am. J. Physiol. Heart Circ. Physiol. 2005 288: H1004 9.
83. Bombeli T, Schwartz BR, Harlan JM. Endothelial cells undergoing apoptosis become proadhesive for nonactivated platelets. Blood 1999 93: 3831 3838.
84. Uittenbogaard A, Shaul PW, Yuhanna IS, Blair A, Smart EJ. High density lipoprotein prevents oxidized low density lipoprotein-induced inhibition of endothelial nitric-oxide synthase localization and activation in caveolae. J. Biol. Chem. 2000 275: 11.
85. Yuhanna IS, Zhu Y, Cox BE et al. High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat. Med. 2001 7: 853 857.
86. Drew BG, Fidge NH, Gallon-Beaumier G, Kemp BE, Kingwell BA. High-density lipoprotein and apolipoprotein AI increase endothelial NO synthase activity by protein association and multisite phosphorylation. Proc. Natl Acad. Sci. USA 2004 101: 6999 7004.
87. Mineo C, Yuhanna IS, Quon MJ, Shaul PW. High density lipoprotein-induced endothelial nitric-oxide synthase activation is mediated by Akt and MAP kinases. J. Biol. Chem. 2003 278: 9142 9149.
88. Nofer JR, Tolle M, Wolinska I et al. HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3. J. Clin. Invest. 2004 113: 569 581.
89. Kimura T, Tomura H, Sato K et al. Mechanism and role of high-density lipoprotein-induced activation of AMP-activated protein kinase in endothelial cells. J. Biol. Chem. 2010 285: 4387 4397.
90. Ramet ME, Ramet M, Lu Q et al. High-density lipoprotein increases the abundance of eNOS protein in human vascular endothelial cells by increasing its half-life. J. Am. Coll. Cardiol. 2003 41: 2288 2297.
91. Kuvin JT, Ramet ME, Patel AR, Pandian NG, Mendelsohn ME, Karas RH. A novel mechanism for the beneficial vascular effects of high-density lipoprotein cholesterol: Enhanced vasorelaxation and increased endothelial nitric oxide synthase expression. Am. Heart J. 2002 144: 165 172.
92. Kuvin JT, Patel AR, Sidhu M et al. Relation between high-density lipoprotein cholesterol and peripheral vasomotor function. Am. J. Cardiol. 2003 92: 275 279.
93. Warnholtz A, Wild P, Ostad MA et al. Effects of oral niacin on endothelial dysfunction in patients with coronary artery disease: Results of the randomized, double-blind, placebo-controlled INEF study. Atherosclerosis 2009 204: 216 221.
94. Bisoendial RJ, Hovingh GK, Levels JH et al. Restoration of endothelial function by increasing high-density lipoprotein in subjects with isolated low high-density lipoprotein. Circulation 2003 107: 2944 2948.
95. Fleisher LN, Tall AR, Witte LD, Miller RW, Cannon PJ. Stimulation of arterial endothelial cell prostacyclin synthesis by high density lipoproteins. J. Biol. Chem. 1982 257: 6653 6655.
96. Spector AA, Scanu AM, Kaduce TL, Figard PH, Fless GM, Czervionke RL. Effect of human plasma lipoproteins on prostacyclin production by cultured endothelial cells. J. Lipid Res. 1985 26: 288 297.
97. Vinals M, Martinez-Gonzalez J, Badimon JJ, Badimon L. HDL-induced prostacyclin release in smooth muscle cells is dependent on cyclooxygenase-2 (Cox-2). Arterioscler. Thromb. Vasc. Biol. 1997 17: 3481 3488.
98. Van SickleWA, Wilcox HG, Malik KU, Nasjletti A. High density lipoprotein-induced cardiac prostacyclin synthesis in vitro: Relationship to cardiac arachidonate mobilization. J. Lipid Res. 1986 27: 517 522.
99. Calabresi L, Rossoni G, Gomaraschi M, Sisto F, Berti F, Franceschini G. High-density lipoproteins protect isolated rat hearts from ischemia-reperfusion injury by reducing cardiac tumor necrosis factor-alpha content and enhancing prostaglandin release. Circ. Res. 2003 92: 330 337.
100. Pomerantz KB, Fleisher LN, Tall AR, Cannon PJ. Enrichment of endothelial cell arachidonate by lipid transfer from high density lipoproteins: Relationship to prostaglandin I2 synthesis. J. Lipid Res. 1985 26: 1269 1276.
101. Cockerill GW, Saklatvala J, Ridley SH et al. High-density lipoproteins differentially modulate cytokine-induced expression of E-selectin and cyclooxygenase-2. Arterioscler. Thromb. Vasc. Biol. 1999 19: 910 917.
102. Norata GD, Callegari E, Inoue H, Catapano AL. HDL3 induces cyclooxygenase-2 expression and prostacyclin release in human endothelial cells via a p38 MAPK/CRE-dependent pathway. Effects on COX-2/PGI-synthase coupling. Arterioscler. Thromb. Vasc. Biol. 2004 24: 871 877.
103. Symons JD. Longitudinal and cross-sectional studies of the relationship between 6-keto PGF1 alpha and high density lipoproteins. Prostaglandins Leukot. Essent. Fatty Acids 1990 39: 159 165.
104. Viswambharan H, Ming XF, Zhu S et al. Reconstituted high-density lipoprotein inhibits thrombin-induced endothelial tissue factor expression through inhibition of RhoA and stimulation of phosphatidylinositol 3-kinase but not Akt/endothelial nitric oxide synthase. Circ. Res. 2004 94: 918 925.
105. Sugano M, Tsuchida K, Makino N. High-density lipoproteins protect endothelial cells from tumor necrosis factor-alpha-induced apoptosis. Biochem. Biophys. Res. Commun. 2000 272: 872 876.
106. Nofer JR, Levkau B, Wolinska I et al. Suppression of endothelial cell apoptosis by high density lipoproteins (HDL) and HDL-associated lysosphingolipids. J. Biol. Chem. 2001 276: 34.
107. Li XA, Guo L, Dressman JL, Asmis R, Smart EJ. A novel ligand-independent apoptotic pathway induced by scavenger receptor class B, type I and suppressed by endothelial nitric-oxide synthase and high density lipoprotein. J. Biol. Chem. 2005 280: 19087 19096.
108. Seetharam S, Mineo C, Gormley AK et al. HDL promotes endothelial cell migration and reendothelialization via scavenger receptor-B type I. Circ. Res. 2006 98: 63 72.
109. de Souza JA, Vindis C, Nègre-Salvayre A et al. Small, dense HDL3 particles attenuates apoptosis in endothelial cells. Pivotal role of apolipoprotein A-I. J. Cell Mol. Med. 2009 13: Epub 20 February 2009; doi
110. Assanasen C, Mineo C, Seetharam D et al. Cholesterol binding, efflux, and a PDZ-interacting domain of scavenger receptor-BI mediate HDL-initiated signaling. J. Clin. Invest. 2005 115: 969 977.
111. Zhu W, Saddar S, Seetharam D et al. The scavenger receptor class B type I adaptor protein PDZK1 maintains endothelial monolayer integrity. Circ. Res. 2008 102: 480 487.
112. Kimura T, Sato K, Malchinkhuu E et al. High-density lipoprotein stimulates endothelial cell migration and survival through sphingosine 1-phosphate and its receptors. Arterioscler. Thromb. Vasc. Biol. 2003 23: 1283 1288.
113. González-Díez M, Rodríguez C, Badimon L, Martínez-González J. Prostacyclin induction by high-density lipoprotein (HDL) in vascular smooth muscle cells depends on sphingosine 1-phosphate receptors: Effect of simvastatin. Thromb. Haemost. 2008 100: 119 126.
114. Podrez EA, Byzova TV, Febbraio M et al. Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype. Nat. Med. 2007 13: 1086 1095.
115. Barter PJ, Caulfield M, Eriksson M et al. Effects of torcetrapib in patients at high risk for coronary events. N. Engl. J. Med. 2007 357: 2109 2122.
116. Williamson R, Lee D, Hagman J, Maeda N. Marked reduction of high density lipoprotein cholesterol in mice genetically modified to lack apolipoprotein A-I. Proc. Natl Acad. Sci. USA 1992 89: 7134 7138.