Type 2 scavenger receptor CD36 in platelet activation: The role of hyperlipemia and oxidative stress

Clinical Lipidology

Volumn 4, Issue 6, 2009, Pages 767-779

  Silverstein, Roy L ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CD36; Microparticles; Oxidized LDL; Platelets; Thrombosis

Indexed keywords

CD36 ANTIGEN; LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN; SCAVENGER RECEPTOR;

ANGIOGENESIS; ANTIGEN BINDING; ANTIGEN EXPRESSION; ANTIGEN FUNCTION; ANTIGEN STRUCTURE; ATHEROSCLEROSIS; DISEASE ASSOCIATION; GENE DELETION; HUMAN; HYPERLIPIDEMIA; IN VIVO STUDY; LIPID METABOLISM; NONHUMAN; OXIDATIVE STRESS; PLATELET MICROPARTICLE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOSIS;

MUS;

EID: 77649105407     PISSN: 17460875     EISSN: None     Source Type: Journal    
DOI: 10.2217/clp.09.57     Document Type: Review

References (149)

1. Kabbani SS, Watkins MW, Ashikaga T et al.: Platelet reactivity characterized prospectively: a determinant of outcome 90 days after percutaneous coronary intervention. Circulation 104, 181-186 (2001).
2. Everett CJ, Mainous AG 3rd, Koopman RJ, Diaz VA: Predicting coronary heart disease risk using multiple lipid measures. Am. J. Cardiol. 95, 986-988 (2005).
3. Carvalho AC, Colman RW, Lees RS: Platelet function in hyperlipoproteinemia. N. Engl. J. Med. 290(8), 434-438 (1974).
4. Shattil SJ, Anaya-Galindo R, Bennett J, Colman RW, Cooper RA: Platelet hypersensitivity induced by cholesterol incorporation. J. Clin. Invest. 55(3), 636-643 (1975).
5. Shattil SJ, Cooper RA: Membrane microviscosity and human platelet function. Biochemistry. 15, 4832-4837 (1976).
6. Plump AS, Smith JD, Hayek T et al.: Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71, 343-353 (1992).
7. Eitzman DT, Westrick RJ, Xu Z, Tyson J, Ginsburg D: Hyperlipidemia promotes thrombosis after injury to atherosclerotic vessels in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 20, 1831-1834 (2000). n Demonstrates the value of mouse hyperlipidemia and in vivo thrombosis models to study platelet hyper-reactivity.
8. Schafer K, Müller K, Hecke A et al.: Enhanced thrombosis in atherosclerosis-prone mice is associated with increased arterial expression of plasminogen activator inhibitor-1. Arterioscler. Thromb. Vasc. Biol. 23, 2097-2103 (2003).
9. Rother E, Brandl R, Baker DL et al.: Subtype-selective antagonists of lysophosphatidic acid receptors inhibit platelet activation triggered by the lipid core of atherosclerotic plaques. Circulation 108, 741-747 (2003).
10. Siess W, Tigyi G: Thrombogenic and atherogenic activities of lysophosphatidic acid. J. Cell Biochem. 92, 1086-1094 (2004).
11. Williams JR, Khandoga AL, Goyal P et al.: Unique ligand selectivity of the GPR92/LPA5 lysophosphatidate receptor indicates role in human platelet activation. J. Biol. Chem. 284, 17304-17319 (2009).
12. Zhang G, Han J, Welch EJ et al.: Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/ MyD88 and the cGMP-dependent protein kinase pathway. J. Immunol. 182, 7997-8004 (2009).
13. Imachi H, Murao K, Cao W et al.: Expression of human scavenger receptor B1 on and in human platelets. Arterioscler. Thromb. Vasc. Biol. 23, 898-904 (2003).
14. Clemetson KJ, Pfueller ST, Luscher EF, Jenkins CSP: Isolation of the membrane glycoproteins of human blood platelets by lection affinity chromatography. Biochim. Biophys. Acta 464, 493-508 (1977).
15. Robertson JO, Li W, Silverstein RL, Topol EJ, Smith JD: Deficiency of LRP8 in mice is associated with altered platelet function and prolonged time for in vivo thrombosis. Thromb. Res. 123, 644-652 (2009).
16. Podrez EA, Byzova TV, Febbraio M et al.: Platelet CD36 links hyperlipidemia, oxidant stress and a pro-thrombotic phenotype. Nat. Med. 13, 1086-1095 (2007).
17. Endemann G, Stanton LW, Madden KS, Bryant CM, White RT, Protter AA: CD36 is a receptor for oxidised low density lipoprotein. J. Biol. Chem. 268, 11811-11816 (1993).
18. Podrez EA, Febbraio M, Sheibani N et al.: The macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species. J. Clin. Invest. 105, 1095-1108 (2000).
19. Podrez EA, Batyreva E, Shen Z et al.: A novel family of atherogenic oxidized phospholipids promotes macrophage foam cell formation via the scavenger receptor CD36 and is enriched in atherosclerotic lesions. J. Biol. Chem. 277, 38517-38523 (2002).
20. Kunjathoor VV, Febbraio M, Podrez EA et al.: Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J. Biol. Chem. 277, 49982-49988 (2002).
21. Park YM, Febbraio M, Silverstein RL: CD36 modulates migration of mouse and human macrophages in response to oxidized LDL and contributes to macrophage trapping in the arterial intima. J. Clin. Invest. 119, 136-145 (2009).
22. Rahaman SO, Lennon DJ, Febbraio M, Podrez EA, Hazen SL, Silverstein RL: CD36-dependent activation of c-Jun N-terminal kinase by oxidized LDL is required for macrophage foam cell formation. Cell Metabol. 4, 211-221 (2006).
23. Moore KJ, El Khoury J, Medeiros LA et al.: A CD36-initiated signaling cascade mediates inflammatory effects of b-amyloid. J. Biol. Chem. 277, 47373-47379 (2002).
24. Janabi M, Yamashita S, Hirano K et al.: Oxidized LDL-induced NF-kB activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. Arterio. Thromb. Vasc. Biol. 20, 1953-1960 (2000).
25. Febbraio M, Podrez EA, Smith JD et al.: Targeted disruption of the class B scavenger receptor, CD36, protects against atherosclerotic lesion development in mice. J. Clin. Invest. 105, 1049-1056 (2000). n Defines a critical role for CD36 in atherogenesis.
26. Febbraio M, Guy E, Silverstein RL: Stem cell transplantation reveals that absence of macrophage CD36 is protective against atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 24, 2333-2338 (2004).
27. Guy E, Kuchibhotla S, Silverstein RL, Febbraio M: Continued inhibition of atherosclerotic lesion development in long term Western diet fed CD36o/apoEo mice. Atherosclerosis 192, 123-130 (2007).
28. Kuchibhotla S, Vanegas D, Kennedy EJ et al.: Absence of CD36 protects against atherosclerosis in ApoE knock-out mice with no additional protection provided by absence of scavenger receptor A I/II. Cardiovasc. Res. 78, 185-196 (2008).
29. Knowles DM, Tolidijian B, Marboe C, Agati VD, Grimes M, Chess L: Monoclonal anti-human monocyte antibodies OKM1 and OKM5 possess distinctive tissue distributions including differential reactivity with vascular endothelium. J. Immunol. 132, 2170-2173 (1984).
30. Oquendo P, Hundt E, Lawler J, Seed B: CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell 58, 95-101 (1994).
31. Calvo D, Dopazo J, Vega MA: The CD36, CLA-1 (CD36L1), and LIMPII (CD36L2) gene family: cellular distribution, chromosomal location, and genetic evolution. Genomics 25, 100-106 (1995).
32. Hart K, Wilcox MA: Drosophila gene encoding an epithelial membrane protein with homology to CD36/LIMP II. J. Mol. Biol. 234, 249-253 (1993).
33. Nichols Z, Vogt RG: The SNMP/CD36 gene family in Diptera, Hymenoptera and Coleoptera: Drosophila melanogaster, D. pseudoobscura, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum. Insect Biochem. Mol. Biol. 38, 398-415 (2008).
34. Jin X, Ha TS, Smith DP: SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc. Natl Acad. Sci. USA 105, 10996-11001 (2008).
35. Benton R, Vannice KS, Vosshall LB: An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450, 289-293 (2007).
36. Müller WEG, Thakur NL, Ushijima H et al.: Matrix-mediated canal formation in primmorphs from the sponge Suberites domuncula involves the expression of a CD36 receptor-ligand system. J. Cell. Sci. 117, 2579-2590 (2004).
37. Silverstein RL, Febbraio M: CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci. Signal. 2(72), re3 (2009).
38. Rac ME, Safranow K, Poncyljusz W: Molecular basis of human CD36 gene mutations. Mol. Med. 13, 288-296 (2007).
39. Hoosdally SJ, Andress EJ, Wooding C, Martin CA, Linton KJ: The human scavenger receptor CD36: glycosylation status and its role in trafficking and function. J. Biol. Chem. 284(24), 16277-16288 (2009).
40. Asch AS, Liu I, Briccetti FM et al.: Analysis of CD36 binding domains: ligand specificity controlled by dephosphorylation of an ectodomain. Science 262, 1436-1440 (1993). n Demonstrates that platelet CD36 function may be regulated by post-translational modification.
41. Ho M, Hoang HL, Lee KM et al.: Ectophosphorylation of CD36 regulates cytoadherence of Plasmodium falciparum to microvascular endothelium under flow conditions. Infect. Immun. 73, 8179-8187 (2005). (Pubitemid 41740306)
42. Tao N, Wagner SJ, Lublin DM: CD36 is palmitoylated on both N- and C-terminal cytoplasmic tails. J. Biol. Chem. 271, 22315-22320 (1996).
43. Smith J, Su X, El-Maghrabi R, Stahl PD, Abumrad NA: Opposite regulation of CD36 ubiquitination by fatty acids and insulin: effects on fatty acid uptake. J. Biol. Chem. 283, 13578-13585 (2008).
44. Sun M, Finnemann SC, Febbraio M et al.: Light-induced oxidation of photoreceptor outer segment phospholipids generates ligands for CD36-mediated phagocytosis by retinal pigment epithelium: a potential mechanism for modulating outer segment phagocytosis under oxidant stress condition. J. Biol. Chem. 281, 4222-4230 (2006).
45. Asch AS, Barnwell J, Silverstein RL, Nachman RL: Isolation of the thrombospondin membrane receptor. J. Clin. Invest. 79, 1054-1061 (1987).
46. Silverstein RL, Baird M, Yesner L: Sense and anti-sense cDNA transfection of glycoprotein IV (CD36) in melanoma cells: role of CD36 as a thrombospondin receptor. J. Biol. Chem. 267, 16607-16612 (1992).
47. Abumrad NA, el-Maghrabi MA, Amri EZ, Lopez E, Grimaldi PA: Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J. Biol. Chem. 268, 17665-17668 (1993).
48. Baillie AG, Coburn CT, Abumrad NA: Reversible binding of long-chain fatty acids to purified FAT, the adipose CD36 homolog. J. Membr. Biol. 153, 75-81 (1996).
49. Pearce SFA, Wu J, Silverstein RL: Recombinant fusion proteins define a thrombospondin binding domain: evidence for a single calcium-dependent binding site on CD36. J. Biol. Chem. 270, 2981-2986 (1995).
50. Leung LL, Li WX, McGregor JL, Albrecht G, Howard RJ: CD36 peptides enhance or inhibit CD36-thrombospondin binding. A two-step process of ligand-receptor interaction. J. Biol. Chem. 267, 18244-18250 (1992).
51. Crombie AR, Silverstein RL: Lysosomal integral membrane protein II binds thrombospondin1: evidence of functional homology with the cell adhesion molecule CD36. J. Biol. Chem. 273, 4855-4864 (1998).
52. Crombie AR, Silverstein RL, MacLow C, Pearce SFA, Nachman RL, Laurence J: Identification of a CD36-related thrombospondin-1 binding domain in HIV-1 envelope glycoprotein gp120: relationship to HIV-specific inhibitory factors in human saliva. J. Exp. Med. 187, 25-35 (1998).
53. Kar NS, Ashraf MS, Valiyaveettil M, Podrez EA: Mapping and characterization of the binding site for specific oxidized phospholipids and oxidized low density lipoprotein of scavenger receptor CD36. J. Biol. Chem. 283, 8765-8771 (2008).
54. Pearce SFA, Roy P, Febbraio M, Nicholson AC, Hajjar DP, Silverstein RL: Recombinant GST/ CD36 fusion proteins define an oxidized LDL binding domain. J. Biol. Chem. 273, 34875-34881 (1998).
55. Febbraio M, Hajjar DP, Silverstein RL: CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation and lipid metabolism. J. Clin. Inv. 108, 785-791 (2001).
56. Yesner LM, Huh HY, Pearce SFA, Silverstein RL: Regulation of thrombospondin and CD36 expression in human monocytes by soluble mediators. Arterioscler. Thromb. Vasc. Biol. 16, 1019-1025 (1996).
57. Huh HY, Pearce SF, Yesner LM, Schindler JL, Silverstein RL: Regulated expression of CD36 during monocyte to macrophage differentiation: Potential role of CD36 in foam cell formation. Blood 87, 2020-2028 (1996).
58. Albert ML, Pearce SFA, Francisco L, Sauter B, Silverstein RL, Bhardwaj N: Immature dendritic cells phagocytose apoptotic cells via avb5 and CD36, and cross-present antigens to CTLs. J. Exp. Med. 188, 1359-1368 (1998).
59. Tontonoz P, Nagy L, Alvarez JG, Thomazy VA, Evans RM: PPARg promotes monocyte/ macrophage differentiation and uptake of oxidized LDL. Cell 93, 241-252 (1998).
60. Han J, Hajjar DP, Febbraio M, Nicholson AC: Native and modified low density lipoproteins increase the functional expression of the macrophage class B scavenger receptor, CD36. J. Biol. Chem. 272, 21654-21659 (1997).
61. Han J, Hajjar DP, Tauras JM, Feng J, Gotto AM Jr, Nicholson AC: Transforming growth factor-b1 (TGF-b1) and TGF-b2 decrease expression of CD36, the type B scavenger receptor, through mitogen-activated protein kinase phosphorylation of peroxisome proliferator-activated receptor-g. J. Biol. Chem. 275, 1241-1246 (2000).
62. Kashyap SR, Ioachimescu A, Gornik HL et al.: Lipid induced insulin resistance is associated with increased monocyte expression of scavenger receptor CD36 and internalization of oxidized LDL. Obesity DOI: 10.1038/ oby.2009.179 (2009) (Epub ahead of print).
63. Griffin E, Re A, Hamel N et al.: A link between diabetes and atherosclerosis: glucose regulates expression of CD36 at the level of translation. Nat. Med. 7, 840-846 (2001).
64. Liang CP, Han S, Okamoto H et al.: Increased CD36 protein as a response to defective insulin signaling in macrophages. J. Clin. Invest. 113, 764-773 (2004).
65. Dressman J, Kincer J, Matveev SV et al.: HIV protease inhibitors promote atherosclerotic lesion formation independent of dyslipidemia by increasing CD36-dependent cholesteryl ester accumulation in macrophages. J. Clin. Invest. 111, 389-397 (2003).
66. Zhou J, Febbraio M, Zhai Y et al.: LXR, PXR, and PPARg cooperate in regulating fatty acid transporter CD36 and promoting hepatic lipogenesis. Gastroenter. 134, 556-567 (2008).
67. Bonen A, Dyck DJ, Ibrahimi A, Abumrad NA: Muscle contractile activity increases fatty acid metabolism and transport and FAT/CD36. Am. J. Physiol. 276, E642-E649 (1999).
68. Nickerson JG, Momken I, Benton CR et al.: Protein-mediated fatty acid uptake: regulation by contraction, AMP-activated protein kinase, and endocrine signals. Appl. Physiol. Nutr. Metab. 32, 865-873 (2007).
69. Bruni F, Pasqui AL, Pastorelli M et al.: Different effect of statins on platelet oxidized- LDL receptor (CD36 and LOX-1) expression in hypercholesterolemic subjects. Clin. Appl. Thromb. Hemost. 11, 417-428 (2005).
70. Kajihara S, Hisatomi A, Ogawa Y et al.: Association of the Pro90Ser CD36 mutation with elevated free fatty acid concentrations but not with insulin resistance syndrome in Japanese. Clin. Chim. Acta 314, 125-130 (2001).
71. Furuhashi M, Ura N, Nakata T, Shimamoto K: Insulin sensitivity and lipid metabolism in human CD36 deficiency. Diabetes Care 26, 471-474 (2003).
72. Yanai H, Chiba H, Morimoto M, Jamieson GA, Matsuno K: Type I CD36 deficiency in humans is not associated with insulin resistance syndrome. Thromb. Haemost. 83, 786 (2000).
73. Love-Gregory L, Sherva R, Sun L et al.: Variants in the CD36 gene associate with the metabolic syndrome and high-density lipoprotein cholesterol. Hum. Mol. Genet. 17, 1695-1704 (2008).
74. Silverstein RL, Febbraio M: CD36-TSPHRGP interactions in the regulation of angiogenesis. Curr. Pharm. Des. 13, 3559-3567 (2007).
75. Kaur B, Sandberg EM, Devi NS et al.: Vasculostatin inhibits intracranial glioma growth and negatively regulates in vivo angiogenesis through a CD36-dependent mechanism. Canc. Res. 69(3), 1212-1220 (2009).
76. Dawson DW, Pearce SFA, Zhong R, Silverstein RL, Frazier WA, Bouck NP: CD36 mediates the inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol. 138, 707-717 (1997).
77. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck NP: Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat. Med. 6, 41-48 (2000).
78. Volpert OV, Zaichuk T, Zhou W et al.: Inducer-stimulated Fas targets activated endothelium for destruction by anti-angiogenic thrombospondin-1 and pigment epitheliumderived factor. Nat. Med. 8, 349-357 (2002).
79. Rege TA, Stewart J Jr, Dranka B, Benveniste EN, Silverstein RL, Gladson CL: Thrombospondin-1-induced apoptosis of brain microvascular endothelial cells can be mediated by TNF-R1. J. Cell Phys. 218, 94-103 (2009).
80. Coburn CT, Knapp FF Jr, Febbraio M, Beets AL, Silverstein RL, Abumrad NA: Defective uptake and utilization of long-chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J. Biol. Chem. 275, 32523-32529 (2000).
81. Drover VA, Nguyen DV, Bastie CC et al.: CD36 mediates both cellular uptake of very long chain fatty acids and their intestinal absorption in mice. J. Biol. Chem. 283, 13108-13115 (2008).
82. Nassir F, Wilson B, Han X, Gross RW, Abumrad NA: CD36 is important for fatty acid and cholesterol uptake by the proximal but not distal intestine. J. Biol. Chem. 282, 19493-19501 (2007).
83. van Bennekum A, Werder M, Thuahnai ST et al.: Class B scavenger receptor-mediated intestinal absorption of dietary b-carotene and cholesterol. Biochem. 44, 4517-4525 (2005).
84. Febbraio M, Abumrad NA, Hajjar DP et al.: A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J. Biol. Chem. 274, 19055-19062 (1999).
85. Glazier AM, Scott, J, Aitman TJ: Molecular basis of the CD36 chromosomal deletion underlying SHR defects in insulin action and fatty acid metabolism. Mamm. Genome 13, 108-113 (2002).
86. Miyaoka K, Kuwasako T, Hirano K, Nozaki S, Yamashita S, Matsuzawa Y: CD36 deficiency associated with insulin resistance. Lancet 357, 686-687 (2001). (Pubitemid 32206428)
87. Corpeleijn E, van der Kallen CJ, Kruijshoop M et al.: Direct association of a promoter polymorphism in the CD36/FAT fatty acid transporter gene with Type 2 diabetes mellitus and insulin resistance. Diabet. Med. 23, 907-911 (2006).
88. Greco D, Kotronen A, Westerbacka J et al.: Gene expression in human NAFLD. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G1281-G12817 (2008).
89. Laugerette F, Passilly-Degrace P, Patris B et al.: CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J. Clin. Invest. 115, 3177-3184 (2005).
90. van Berkel TJ, Out R, Hoekstra M, Kuiper J, Biessen E, van Eck M: Scavenger receptors: friend or foe in atherosclerosis? Curr. Opin. Lipidol. 16, 525-535 (2005).
91. Akira A, Takeda S: Toll-like receptor signaling. Nat. Rev. Immunol. 4, 499-511 (2004).
92. Hoebe K, Georgel P, Rutschmann S et al.: CD36 is a sensor of diacylglycerides. Nature 433, 523-527 (2005).
93. Philips JA, Rubin EJ, Perrimon N: Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 309, 1251-1253 (2005).
94. Means TK, Mylonakis E, Tampakakis E et al.: Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J. Exp. Med. 206, 637-653 (2009).
95. Smith TG, Serghides L, Patel S, Febbraio M, Silverstein RL, Kain KC: CD36-mediated non-opsonic phagocytosis of erythrocytes infected with stage I and IIA gametocyes of Plasmodium falciparum. Infect. Immun. 71, 393-400 (2003).
96. Savill J, Hogg N: Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90, 1513-1522 (1992).
97. Ren Y, Silverstein RL, Allen J, Savill J: CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J. Exp. Med. 181, 1857-1862 (1995).
98. Ghosh A, Li W, Febbraio M, Espinola RG, McCrae K, Silverstein RL: Platelet CD36 mediates interactions with endothelial cell-derived microparticles and contributes to thrombosis in vivo. J. Clin. Invest. 118, 1934-1943 (2008).
99. Ryeom S, Sparrow J, Silverstein RL: CD36 Participates in the phagocytosis of rod outer segments on retinal pigment epithelium. J. Cell Sci. 109, 387-395 (1996).
100. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE: A cell surface receptor complex for fibrillar b-amyloid mediates microglial activation. J. Neurosci. 23, 2665-7264. 2003.
101. El Khoury JB, Moore KJ, Means TK et al.: CD36 mediates the innate host response to b-amyloid. J. Exp. Med. 197, 1657-1666 (2003).
102. Greenberg ME, Li XM, Gugiu BG et al.: The lipid whisker model of the structure of oxidized cell membranes. J. Biol. Chem. 283, 2385-2396 (2008). n This elegant paper uses sophisticated structural biology tools to characterize the oxidized phospholipid ligands for CD36.
103. Cho S, Park EM, Febbraio M et al.: The class B scavenger receptor CD36 mediates free radical production and tissue injury in cerebral ischemia. J. Neurosci. 25, 2504-2512 (2005).
104. Moore KJ, Kunjathoor VV, Koehn SL et al.: Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J Clin Invest. 115, 2192-2201 (2005).
105. Moore KJ, Freeman MW: Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler. Thromb. Vasc. Biol. 26, 1702-1711 (2006).
106. Manning-Tobin JJ, Moore KJ, Seimon TA et al.: Loss of SR-A and CD36 activity reduces atherosclerotic lesion complexity without abrogating foam cell formation in hyperlipidemic mice. Arterioscler. Thromb. Vasc. Biol. 29, 19-26 (2009).
107. Volf I, Moeslinger T, Cooper J, Schmid W, Koller E: Human platelets exclusively bind oxidized low density lipoprotein showing no specificity for acetylated low density lipoprotein. FEBS Lett. 449, 141-145 (1999).
108. Volf I, Roth A, Cooper J, Moeslinger T, Koller E: Hypochlorite modified LDL are a stronger agonist for platelets than copper oxidized LDL. FEBS Lett. 483, 155-159 (2000).
109. Göpfert MS, Siedler F, Siess W, Sellmayer A: Structural identification of oxidized acyl-phosphatidylcholines that induce platelet activation. J. Vasc. Res. 42, 120-132 (2005).
110. Chen K, Febbraio M, Li W, Silverstein RL: A specific CD36-dependent signaling pathway is required for platelet activation by oxidized LDL. Circ. Res. 102, 1512-1519 (2008).
111. Siess W, Zangl KJ, Essler M et al.: Lysophosphatidic acid mediates the rapid activation of platelets and endothelial cells by mildly oxidized low density lipoprotein and accumulates in human atherosclerotic lesions. Proc. Natl Acad. Sci. USA 96, 6931-6936 (1999).
112. Haserück N, Erl W, Pandey D et al.: The plaque lipid lysophosphatidic acid stimulates platelet activation and platelet-monocyte aggregate formation in whole blood: involvement of P2Y1 and P2Y12 receptors. Blood 103, 2585-2592 (2004).
113. Retzer M, Essler M: Lysophosphatidic acid-induced platelet shape change proceeds via Rho/Rho kinase-mediated myosin light-chain and moesin phosphorylation. Cell Signal. 12, 645-648 (2000). (Pubitemid 30844837)
114. 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. 30, 831-840 (1989).
115. Pedreño J, de Castellarnau C, Masana L: Platelet HDL(3) binding sites are not related to integrin a(IIb)b(3) (GPIIb-IIIa). Atherosclerosis 154, 23-29 (2001).
116. 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. 582, 778-784 (2008).
117. Chen LY, Mehta JL: Inhibitory effect of high-density lipoprotein on platelet function is mediated by increase in nitric oxide synthase activity in platelets. Life Sci. 55, 1815-1821 (1994).
118. Mehta JL, Chen LY: Reversal by high-density lipoprotein of the effect of oxidized low-density lipoprotein on nitric oxide synthase protein expression in human platelets. J. Lab. Clin. Med. 127, 287-295 (1996).
119. 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-trisphosphate. Arterioscler. Thromb. Vasc. Biol. 18, 861-869 (1998).
120. 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. 279, 52526-52534 (2004).
121. Korporaal SJ, Akkerman JW: Platelet signaling induced by lipoproteins. Cardiovasc. Hematol. Agents Med. Chem. 4, 93-109 (2006).
122. 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 111, 1962-1971 (2008). n Identifies roles for oxidized HDL and scavenger receptor BI in platelet function.
123. Combes V, Simon AC, Grau GE et al.: In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J. Clin. Invest. 104, 93-102 (1999).
124. Falati S, Liu Q, Gross P et al.: Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J. Exp. Med. 197, 1585-1598 (2003).
125. Bernal-Mizrachi L, Jy W, Jimenez JJ et al.: High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am. Heart J. 145, 962-970 (2003).
126. Shet AS, Aras O, Gupta K et al.: Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood 102, 2678-2683 (2003).
127. Davi G, Ferroni P: Microparticles in Type 2 diabetes mellitus. J. Thromb. Haemost. 3, 1166-1167 (2005).
128. Koga H, Sugiyama S, Kugiyama K et al.: Elevated levels of VE-cadherin-positive endothelial microparticles in patients with Type 2 diabetes mellitus and coronary artery disease. J. Am. Coll. Cardiol. 45, 1622-1630 (2005).
129. Jimenez JJ, Jy W, Mauro LM, Horstman LL, Ahn YS: Elevated endothelial microparticles in thrombotic thrombocytopenic purpura: findings from brain and renal microvascular cell culture and patients with active disease. Br. J. Haematol. 112, 81-90 (2001).
130. Dignat-George F, Camoin-Jau L, Sabatier F et al.: Endothelial microparticles: a potential contribution to the thrombotic complications of the antiphospholipid syndrome. Thromb. Haemost. 91, 667-673 (2004).
131. Gonzalez-Quintero VH, Smarkusky LP, Jimenez JJ et al.: Elevated plasma endothelial microparticles: preeclampsia versus gestational hypertension. Am. J. Obstet. Gynecol. 191, 1418-1424 (2004).
132. Pihusch V, Rank A, Steber R et al.: Endothelial cell-derived microparticles in allogeneic hematopoietic stem cell recipients. Transplant. 81, 1405-1409 (2006). (Pubitemid 43847150)
133. Sims PJ, Wiedmer T, Esmon CT, Weiss HJ, Shattil SJ: Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane. Studies in Scott syndrome: an isolated defect in platelet procoagulant activity. J. Biol. Chem. 264, 17049-17057 (1989).
134. Sabatier F, Roux V, Anfosso F, Camoin L, Sampol J, Dignat-George F: Interaction of endothelial microparticles with monocytic cells in vitro induces tissue factor-dependent procoagulant activity. Blood 99, 3962-3970 (2002).
135. Korporaal SJ, van Eck M, Adelmeijer J et al.: Platelet activation by oxidized low density lipoprotein is mediated by CD36 and scavenger receptor-A. Arterioscler. Thromb. Vasc. Biol. 27, 2476-2483 (2007). n This paper suggests that CD36 and scavenger receptor-A may cooperate in platelet signaling in response to oxidized LDL.
136. Stuart LM, Deng J, Silver JM et al.: Response to Staphylococcus aureus requires CD36- mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J. Cell Biol. 170, 477-485 (2005).
137. Lisanti MP, Scherer PE, Vidugiriene J: Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J. Cell Biol. 126, 111-126 (1994).
138. Pohl J, Ring A, Korkmaz U, Ehehalt R, Stremmel W: FAT/CD36-mediated long-chain fatty acid uptake in adipocytes requires plasma membrane rafts. Mol. Biol. Cell 16, 24-31 (2005).
139. Zeng Y, Tao N, Chung KN, Heuser JE, Lublin DM: Endocytosis of oxidized low density lipoprotein through scavenger receptor CD36 utilizes a lipid raft pathway that does not require caveolin-1. J Biol. Chem. 278, 45931-45936 (2003).
140. Kincer JF, Uittenbogaard A, Dressman J et al.: Hypercholesterolemia promotes a CD36-dependent and endothelial nitric-oxide synthase-mediated vascular dysfunction. J. Biol. Chem. 277, 23525-23533 (2002).
141. Miao WM, Vasile E, Lane WS, Lawler J: CD36 associates with CD9 and integrins on human blood platelets. Blood 97, 1689-1696 (2001).
142. Triantafilou M, Gamper FG, Haston RM et al.: Membrane sorting of Toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281, 31002-31011 (2006).
143. Nilsen NJ, Deininger S, Nonstad U et al.: Cellular trafficking of lipoteichoic acid and Toll-like receptor 2 in relation to signaling: role of CD14 and CD36. J. Leukoc. Biol. 84, 280-291 (2008).
144. Hashimoto M, Tawaratsumida K, Kariya H et al.: Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus. J. Immunol. 177, 3162-3169 (2006).
145. Baranova IN, Kurlander R, Bocharov AV et al.: Role of human CD36 in bacterial recognition, phagocytosis, and pathogen-induced JNK-mediated signaling. J. Immunol. 181, 7147-7156 (2008).
146. Wilkinson B, Koenigsknecht-Talboo J, Grommes C, Lee CY, Landreth G: Fibrillar b-amyloid-stimulated intracellular signaling cascades require Vav for induction of respiratory burst and phagocytosis in monocytes and microglia. J. Biol. Chem. 281, 20842-20850 (2006).
147. Finnemann SC, Silverstein RL: Differential roles of CD36 and avb5 integrin in photoreceptor phagocytosis by the retinal pigment epithelium. J. Exp. Med. 194, 1289-1298 (2001).
148. Pijuan-Thompson V, Grammar JR, Stewart J et al.: Retenoic acid alters the mechanism of attachment of malignant astrocytoma and neuroblatoma cells to TSP-1. Exp. Cell Res. 249, 86-101 (1999).
149. Stuart LM, Bell SA, Stewart CR et al.: CD36 signals to the actin cytoskeleton and regulates microglial migration via a p130Cas complex. J. Biol. Chem. 282, 27392-127301 (2007).