Atherosclerosis
Volume 182, Issue 1 , Pages 1-15 , September 2005

Biochemistry and cell biology of mammalian scavenger receptors

  • Jane E. Murphy

      Affiliations

    • School of Biochemistry and Microbiology, University of Leeds, Leeds LS2 9JT, UK
  • ,
  • Philip R. Tedbury

      Affiliations

    • School of Biochemistry and Microbiology, University of Leeds, Leeds LS2 9JT, UK
  • ,
  • Shervanthi Homer-Vanniasinkam

      Affiliations

    • Academic Unit of Vascular Surgery, Leeds General Infirmary, Great George Street, Leeds LS1 3EX, UK
  • ,
  • John H. Walker

      Affiliations

    • School of Biochemistry and Microbiology, University of Leeds, Leeds LS2 9JT, UK
  • ,
  • Sreenivasan Ponnambalam

      Affiliations

    • School of Biochemistry and Microbiology, University of Leeds, Leeds LS2 9JT, UK
    • Corresponding Author InformationCorresponding author. Tel.: +44 113 343 3007; fax: +44 113 343 3167.

Received 5 November 2004 ,Revised 10 March 2005 ,Accepted 24 March 2005.

References 

  1. World Health Organization. www.who.int/cardiovascular_diseases
  2. Brown MS, Goldstein JL. A receptor-mediated pathway for cholesterol homeostasis. Science. 1986;232:34–47
  3. Goldstein JL, Ho YK, Basu SK, Brown MS. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci USA. 1979;76:333–337
  4. Rice-Evans C, Leake D, Bruckdorfer KR, Diplock AT. Practical approaches to low density lipoprotein oxidation: whys, wherefores and pitfalls. Free Radic Res. 1996;25:285–311
  5. Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J Biol Chem. 1997;272:20963–20966
  6. Navab M, Ananthramaiah GM, Reddy ST, et al. The oxidation hypothesis of atherogenesis: the role of oxidized phospholipids and HDL. J Lipid Res. 2004;45:993–1007
  7. Abuja PM, Esterbauer H. Simulation of lipid peroxidation in low-density lipoprotein by a basic “skeleton” of reactions. Chem Res Toxicol. 1995;8:753–763
  8. Young IS, McEneny J. Lipoprotein oxidation and atherosclerosis. Biochem Soc Trans. 2001;29:358–362
  9. Fong LG, Parthasarathy S, Witztum JL, Steinberg D. Nonenzymatic oxidative cleavage of peptide bonds in apoprotein B-100. J Lipid Res. 1987;28:1466–1477
  10. Freeman M, Ashkenas J, Rees DJ, et al. An ancient, highly conserved family of cysteine-rich protein domains revealed by cloning type I and type II murine macrophage scavenger receptors. Proc Natl Acad Sci USA. 1990;87:8810–8814
  11. Gough PJ, Greaves DR, Gordon S. A naturally occurring isoform of the human macrophage scavenger receptor (SR-A) gene generated by alternative splicing blocks modified LDL uptake. J Lipid Res. 1998;39:531–543
  12. Elomaa O, Kangas M, Sahlberg C, et al. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell. 1995;80:603–609
  13. Nakamura K, Funakoshi H, Miyamoto K, Tokunaga F, Nakamura T. Molecular cloning and functional characterization of a human scavenger receptor with C-type lectin (SRCL), a novel member of a scavenger receptor family. Biochem Biophys Res Commun. 2001;280:1028–1035
  14. Emi M, Asaoka H, Matsumoto A, et al. Structure, organization, and chromosomal mapping of the human macrophage scavenger receptor gene. J Biol Chem. 1993;268:2120–2125
  15. Kangas M, Brannstrom A, Elomaa O, et al. Structure and chromosomal localization of the human and murine genes for the macrophage MARCO receptor. Genomics. 1999;58:82–89
  16. Mietus-Snyder M, Gowri MS, Pitas RE. Class A scavenger receptor up-regulation in smooth muscle cells by oxidized low density lipoprotein. Enhancement by calcium flux and concurrent cyclooxygenase-2 up-regulation. J Biol Chem. 2000;275:17661–17670
  17. Terpstra V, van Amersfoort ES, van Velzen AG, Kuiper J, van Berkel TJ. Hepatic and extrahepatic scavenger receptors: function in relation to disease. Arterioscler Thromb Vasc Biol. 2000;20:1860–1872
  18. Svensson L, Noren K, Wiklund O, et al. Inhibitory effects of N-acetylcysteine on scavenger receptor class A expression in human macrophages. J Intern Med. 2002;251:437–446
  19. de Villiers WJ, Fraser IP, Hughes DA, Doyle AG, Gordon S. Macrophage-colony-stimulating factor selectively enhances macrophage scavenger receptor expression and function. J Exp Med. 1994;180:705–709
  20. Via DP, Pons L, Dennison DK, Fanslow AE, Bernini F. Induction of acetyl-LDL receptor activity by phorbol ester in human monocyte cell line THP-1. J Lipid Res. 1989;30:1515–1524
  21. Hsu HY, Nicholson AC, Hajjar DP. Inhibition of macrophage scavenger receptor activity by tumor necrosis factor-alpha is transcriptionally and post-transcriptionally regulated. J Biol Chem. 1996;271:7767–7773
  22. Bottalico LA, Wager RE, Agellon LB, Assoian RK, Tabas I. Transforming growth factor-beta 1 inhibits scavenger receptor activity in THP-1 human macrophages. J Biol Chem. 1991;266:22866–22871
  23. Geng YJ, Hansson GK. Interferon-gamma inhibits scavenger receptor expression and foam cell formation in human monocyte-derived macrophages. J Clin Invest. 1992;89:1322–1330
  24. Granucci F, Petralia F, Urbano M, et al. The scavenger receptor MARCO mediates cytoskeleton rearrangements in dendritic cells and microglia. Blood. 2003;102:2940–2947
  25. Grolleau A, Misek DE, Kuick R, Hanash S, Mule JJ. Inducible expression of macrophage receptor MARCO by dendritic cells following phagocytic uptake of dead cells uncovered by oligonucleotide arrays. J Immunol. 2003;171:2879–2888
  26. Kraal G, van der Laan LJ, Elomaa O, Tryggvason K. The macrophage receptor MARCO. Microbes Infect. 2000;2:313–316
  27. Ohtani K, Suzuki Y, Eda S, et al. The membrane-type collectin CL-P1 is a scavenger receptor on vascular endothelial cells. J Biol Chem. 2001;276:44222–44228
  28. Dhaliwal BS, Steinbrecher UP. Scavenger receptors and oxidized low density lipoproteins. Clin Chim Acta. 1999;286:191–205
  29. Matsumoto A, Naito M, Itakura H, et al. Human macrophage scavenger receptors: primary structure, expression, and localization in atherosclerotic lesions. Proc Natl Acad Sci USA. 1990;87:9133–9137
  30. Doi T, Higashino K, Kurihara Y, et al. Charged collagen structure mediates the recognition of negatively charged macromolecules by macrophage scavenger receptors. J Biol Chem. 1993;268:2126–2133
  31. Sankala M, Brannstrom A, Schulthess T, et al. Characterization of recombinant soluble macrophage scavenger receptor MARCO. J Biol Chem. 2002;277:33378–33385
  32. Brannstrom A, Sankala M, Tryggvason K, Pikkarainen T. Arginine residues in domain V have a central role for bacteria-binding activity of macrophage scavenger receptor MARCO. Biochem Biophys Res Commun. 2002;290:1462–1469
  33. Penman M, Lux A, Freedman NJ, et al. The type I and type II bovine scavenger receptors expressed in Chinese hamster ovary cells are trimeric proteins with collagenous triple helical domains comprising noncovalently associated monomers and Cys83-disulfide-linked dimers. J Biol Chem. 1991;266:23985–23993
  34. Mori T, Takahashi K, Naito M, et al. Endocytic pathway of scavenger receptors via trans-Golgi system in bovine alveolar macrophages. Lab Invest. 1994;71:409–416
  35. Hsu HY, Hajjar DP, Khan KM, Falcone DJ. Ligand binding to macrophage scavenger receptor-A induces urokinase-type plasminogen activator expression by a protein kinase-dependent signaling pathway. J Biol Chem. 1998;273:1240–1246
  36. Whitman SC, Daugherty A, Post SR. Regulation of acetylated low density lipoprotein uptake in macrophages by pertussis toxin-sensitive G proteins. J Lipid Res. 2000;41:807–813
  37. Hsu HY, Chiu SL, Wen MH, Chen KY, Hua KF. Ligands of macrophage scavenger receptor induce cytokine expression via differential modulation of protein kinase signaling pathways. J Biol Chem. 2001;276:28719–28730
  38. Coller SP, Paulnock DM. Signaling pathways initiated in macrophages after engagement of type A scavenger receptors. J Leukoc Biol. 2001;70:142–148
  39. Chao SK, Hamilton RF, Pfau JC, Holian A. Cell surface regulation of silica-induced apoptosis by the SR-A scavenger receptor in a murine lung macrophage cell line (MH-S). Toxicol Appl Pharmacol. 2001;174:10–16
  40. Kim WS, Ordija CM, Freeman MW. Activation of signaling pathways by putative scavenger receptor class A (SR-A) ligands requires CD14 but not SR-A. Biochem Biophys Res Commun. 2003;310:542–549
  41. Peiser L, Gough PJ, Kodama T, Gordon S. Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro. Infect Immun. 2000;68:1953–1963
  42. Thomas CA, Li Y, Kodama T, et al. Protection from lethal Gram-positive infection by macrophage scavenger receptor-dependent phagocytosis. J Exp Med. 2000;191:147–156
  43. Hampton RY, Golenbock DT, Penman M, Krieger M, Raetz CR. Recognition and plasma clearance of endotoxin by scavenger receptors. Nature. 1991;352:342–344
  44. Santiago Garcia J, Kodama T, Pitas RE. The class A scavenger receptor binds to proteoglycans and mediates adhesion of macrophages to the extracellular matrix. J Biol Chem. 2003;278:6942–6946
  45. Arredouani M, Yang Z, Ning Y, et al. The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles. J Exp Med. 2004;200:267–272
  46. Pikkarainen T, Brannstrom A, Tryggvason K. Expression of macrophage MARCO receptor induces formation of dendritic plasma membrane processes. J Biol Chem. 1999;274:10975–10982
  47. Lougheed M, Lum CM, Ling W, et al. High affinity saturable uptake of oxidized low density lipoprotein by macrophages from mice lacking the scavenger receptor class A type I/II. J Biol Chem. 1997;272:12938–12944
  48. Ling W, Lougheed M, Suzuki H, et al. Oxidized or acetylated low density lipoproteins are rapidly cleared by the liver in mice with disruption of the scavenger receptor class A type I/II gene. J Clin Invest. 1997;100:244–252
  49. 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. 2002;277:49982–49988
  50. Kamada N, Kodama T, Suzuki H. Macrophage scavenger receptor (SR-A I/II) deficiency reduced diet-induced atherosclerosis in C57BL/6J mice. J Atheroscler Thromb. 2001;8:1–6
  51. Xu J, et al. Germline mutations and sequence variants of the macrophage scavenger receptor 1 gene are associated with prostate cancer risk. Nat Genet. 2002;32:321–325
  52. Wang L, McDonnell SK, Cunningham JM, et al. No association of germline alteration of MSR1 with prostate cancer risk. Nat Genet. 2003;35:128–129
  53. El Khoury J, Hickman SE, Thomas CA, et al. Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature. 1996;382:716–719
  54. Armesilla AL, Vega MA. Structural organization of the gene for human CD36 glycoprotein. J Biol Chem. 1994;269:18985–18991
  55. Cao G, Garcia CK, Wyne KL, et al. Structure and localization of the human gene encoding SR-BI/CLA-1. Evidence for transcriptional control by steroidogenic factor 1. J Biol Chem. 1997;272:33068–33076
  56. Webb NR, de Villiers WJ, Connell PM, de Beer FC, van der Westhuyzen DR. Alternative forms of the scavenger receptor BI (SR-BI). J Lipid Res. 1997;38:1490–1495
  57. Chinetti G, Gbaguidi FG, Griglio S, et al. CLA-1/SR-BI is expressed in atherosclerotic lesion macrophages and regulated by activators of peroxisome proliferator-activated receptors. Circulation. 2000;101:2411–2417
  58. Langer C, Gansz B, Goepfert C, et al. Testosterone up-regulates scavenger receptor BI and stimulates cholesterol efflux from macrophages. Biochem Biophys Res Commun. 2002;296:1051–1057
  59. Spady DK, Kearney DM, Hobbs HH. Polyunsaturated fatty acids up-regulate hepatic scavenger receptor B1 (SR-BI) expression and HDL cholesteryl ester uptake in the hamster. J Lipid Res. 1999;40:1384–1394
  60. Khovidhunkit W, Moser AH, Shigenaga JK, Grunfeld C, Feingold KR. Regulation of scavenger receptor class B type I in hamster liver and Hep3B cells by endotoxin and cytokines. J Lipid Res. 2001;42:1636–1644
  61. Han J, Nicholson AC, Zhou X, et al. Oxidized low density lipoprotein decreases macrophage expression of scavenger receptor B-I. J Biol Chem. 2001;276:16567–16572
  62. Matsumoto K, Hirano K, Nozaki S, et al. Expression of macrophage (Mphi) scavenger receptor, CD36, in cultured human aortic smooth muscle cells in association with expression of peroxisome proliferator activated receptor-gamma, which regulates gain of Mphi-like phenotype in vitro, and its implication in atherogenesis. Arterioscler Thromb Vasc Biol. 2000;20:1027–1032
  63. Calvo D, Dopazo J, Vega MA. The CD36, CLA-1 (CD36L1), and LIMPII (CD36L2) gene family: cellular distribution, chromosomal location, and genetic evolution. Genomics. 1995;25:100–106
  64. 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. 1997;272:21654–21659
  65. Yesner LM, Huh HY, Pearce SF, Silverstein RL. Regulation of monocyte CD36 and thrombospondin-1 expression by soluble mediators. Arterioscler Thromb Vasc Biol. 1996;16:1019–1025
  66. Nakagawa T, Nozaki S, Nishida M, et al. Oxidized LDL increases and interferon-gamma decreases expression of CD36 in human monocyte-derived macrophages. Arterioscler Thromb Vasc Biol. 1998;18:1350–1357
  67. Han J, Hajjar DP, Tauras JM, et al. Transforming growth factor-beta1 (TGF-beta1) and TGF-beta2 decrease expression of CD36, the type B scavenger receptor, through mitogen-activated protein kinase phosphorylation of peroxisome proliferator-activated receptor-gamma. J Biol Chem. 2000;275:1241–1246
  68. Nicholson AC. Expression of CD36 in macrophages and atherosclerosis the role of lipid regulation of PPARgamma signaling. Trends Cardiovasc Med. 2004;14:8–12
  69. Greenwalt DE, Lipsky RH, Ockenhouse CF, et al. Membrane glycoprotein CD36: a review of its roles in adherence, signal transduction, and transfusion medicine. Blood. 1992;80:1105–1115
  70. Gruarin P, Sitia R, Alessio M. Formation of one or more intrachain disulphide bonds is required for the intracellular processing and transport of CD36. Biochem J. 1997;328:635–642
  71. Calvo D, Gomez-Coronado D, Suarez Y, Lasuncion MA, Vega MA. Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL. J Lipid Res. 1998;39:777–788
  72. Rigotti A, Acton SL, Krieger M. The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J Biol Chem. 1995;270:16221–16224
  73. Podrez EA, Poliakov E, Shen Z, et al. Identification of a novel family of oxidized phospholipids that serve as ligands for the macrophage scavenger receptor CD36. J Biol Chem. 2002;277:38503–38516
  74. Puente Navazo MD, Daviet L, Ninio E, McGregor JL. Identification on human CD36 of a domain (155–183) implicated in binding oxidized low-density lipoproteins (Ox-LDL). Arterioscler Thromb Vasc Biol. 1996;16:1033–1039
  75. Thorne RF, Meldrum CJ, Harris SJ, et al. CD36 forms covalently associated dimers and multimers in platelets and transfected COS-7 cells. Biochem Biophys Res Commun. 1997;240:812–818
  76. Reaven E, Cortez Y, Leers-Sucheta S, Nomoto A, Azhar S. Dimerization of the scavenger receptor class B type I: formation, function, and localization in diverse cells and tissues. J Lipid Res. 2004;45:513–528
  77. Tao N, Wagner SJ, Lublin DM. CD36 is palmitoylated on both N- and C-terminal cytoplasmic tails. J Biol Chem. 1996;271:22315–22320
  78. Babitt J, Trigatti B, Rigotti A, et al. Murine SR-BI, a high density lipoprotein receptor that mediates selective lipid uptake, is N-glycosylated and fatty acylated and colocalizes with plasma membrane caveolae. J Biol Chem. 1997;272:13242–13249
  79. Acton SL, Scherer PE, Lodish HF, Krieger M. Expression cloning of SR-BI, a CD36-related class B scavenger receptor. J Biol Chem. 1994;269:21003–21009
  80. Murao K, Terpstra V, Green SR, et al. Characterization of CLA-1, a human homologue of rodent scavenger receptor BI, as a receptor for high density lipoprotein and apoptotic thymocytes. J Biol Chem. 1997;272:17551–17557
  81. Webb NR, Connell PM, Graf GA, et al. SR-BII, an isoform of the scavenger receptor BI containing an alternate cytoplasmic tail, mediates lipid transfer between high density lipoprotein and cells. J Biol Chem. 1998;273:15241–15248
  82. 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. 2003;278:45931–45936
  83. Malaud E, Hourton D, Giroux LM, et al. The terminal six amino-acids of the carboxy cytoplasmic tail of CD36 contain a functional domain implicated in the binding and capture of oxidized low-density lipoprotein. Biochem J. 2002;364:507–515
  84. Peng Y, Akmentin W, Connelly MA, et al. Scavenger receptor BI (SR-BI) clustered on microvillar extensions suggests that this plasma membrane domain is a way station for cholesterol trafficking between cells and high-density lipoprotein. Mol Biol Cell. 2004;15:384–396
  85. Vinals M, Xu S, Vasile E, Krieger M. Identification of the N-linked glycosylation sites on the high density lipoprotein (HDL) receptor SR-BI and assessment of their effects on HDL binding and selective lipid uptake. J Biol Chem. 2003;278:5325–5332
  86. Rhainds D, Bourgeois P, Bourret G, et al. Localization and regulation of SR-BI in membrane rafts of HepG2 cells. J Cell Sci. 2004;117:3095–3105
  87. Silver DL, Wang N, Xiao X, Tall AR. High density lipoprotein (HDL) particle uptake mediated by scavenger receptor class B type 1 results in selective sorting of HDL cholesterol from protein and polarized cholesterol secretion. J Biol Chem. 2001;276:25287–25293
  88. Vishnyakova TG, Bocharov AV, Baranova IN, et al. Binding and internalization of lipopolysaccharide by Cla-1, a human orthologue of rodent scavenger receptor B1. J Biol Chem. 2003;278:22771–22780
  89. Eckhardt ER, Cai L, Sun B, Webb NR, van der Westhuyzen DR. High density lipoprotein uptake by scavenger receptor SR-BII. J Biol Chem. 2004;279:14372–14381
  90. Moore KJ, El Khoury J, Medeiros LA, et al. A CD36-initiated signaling cascade mediates inflammatory effects of beta-amyloid. J Biol Chem. 2002;277:47373–47379
  91. Medeiros LA, Khan T, El Khoury JB, et al. Fibrillar amyloid protein present in atheroma activates CD36 signal transduction. J Biol Chem. 2004;279:10643–10648
  92. Jimenez B, Volpert OV, Crawford SE, et al. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med. 2000;6:41–48
  93. Abumrad NA, el-Maghrabi MR, 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. 1993;268:17665–17668
  94. Acton S, Rigotti A, Landschulz KT, et al. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 1996;271:518–520
  95. Ji Y, Jian B, Wang N, et al. Scavenger receptor BI promotes high density lipoprotein-mediated cellular cholesterol efflux. J Biol Chem. 1997;272:20982–20985
  96. Ikemoto M, Arai H, Feng D, et al. Identification of a PDZ-domain-containing protein that interacts with the scavenger receptor class B type I. Proc Natl Acad Sci USA. 2000;97:6538–6543
  97. Mineo C, Shaul PW. HDL stimulation of endothelial nitric oxide synthase: a novel mechanism of HDL action. Trends Cardiovasc Med. 2003;13:226–231
  98. Mulcahy JV, Riddell DR, Owen JS. Human scavenger receptor class B type II (SR-BII) and cellular cholesterol efflux. Biochem J. 2004;377:741–747
  99. Tsukamoto K, Kinoshita M, Kojima K, et al. Synergically increased expression of CD36, CLA-1 and CD68, but not of SR-A and LOX-1, with the progression to foam cells from macrophages. J Atheroscler Thromb. 2002;9:57–64
  100. 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. 2000;105:1049–1056
  101. Coraci IS, Husemann J, Berman JW, et al. CD36, a class B scavenger receptor, is expressed on microglia in Alzheimer's disease brains and can mediate production of reactive oxygen species in response to beta-amyloid fibrils. Am J Pathol. 2002;160:101–112
  102. El Khoury JB, Moore KJ, Means TK, et al. CD36 mediates the innate host response to beta-amyloid. J Exp Med. 2003;197:1657–1666
  103. Ricciarelli R, D’Abramo C, Zingg JM, et al. CD36 overexpression in human brain correlates with beta-amyloid deposition but not with Alzheimer's disease. Free Radic Biol Med. 2004;36:1018–1024
  104. Lepretre F, Vasseur F, Vaxillaire M, et al. A CD36 nonsense mutation associated with insulin resistance and familial type 2 diabetes. Hum Mutat. 2004;24:104
  105. Pain A, Urban BC, Kai O, et al. A non-sense mutation in Cd36 gene is associated with protection from severe malaria. Lancet. 2001;357:1502–1503
  106. Rigotti A, Trigatti BL, Penman M, et al. A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc Natl Acad Sci USA. 1997;94:12610–12615
  107. Braun A, Trigatti BL, Post MJ, et al. Loss of SR-BI expression leads to the early onset of occlusive atherosclerotic coronary artery disease, spontaneous myocardial infarctions, severe cardiac dysfunction, and premature death in apolipoprotein E-deficient mice. Circ Res. 2002;90:270–276
  108. Osgood D, Corella D, Demissie S, et al. Genetic variation at the scavenger receptor class B type I gene locus determines plasma lipoprotein concentrations and particle size and interacts with type 2 diabetes: the framingham study. J Clin Endocrinol Metab. 2003;88:2869–2879
  109. Pearson A, Lux A, Krieger M. Expression cloning of dSR-CI, a class C macrophage-specific scavenger receptor from Drosophila melanogaster. Proc Natl Acad Sci USA. 1995;92:4056–4060
  110. Ramet M, Pearson A, Manfruelli P, et al. Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity. 2001;15:1027–1038
  111. Jiang Z, Shih DM, Xia YR, et al. Structure, organization, and chromosomal mapping of the gene encoding macrosialin, a macrophage-restricted protein. Genomics. 1998;50:199–205
  112. de Saint-Vis B, Vincent J, Vandenabeele S, et al. A novel lysosome-associated membrane glycoprotein, DC-LAMP, induced upon DC maturation, is transiently expressed in MHC class II compartment. Immunity. 1998;9:325–336
  113. Li AC, Guidez FR, Collier JG, Glass CK. The macrosialin promoter directs high levels of transcriptional activity in macrophages dependent on combinatorial interactions between PU.1 and c-Jun. J Biol Chem. 1998;273:5389–5399
  114. Yoshida H, Quehenberger O, Kondratenko N, Green S, Steinberg D. Minimally oxidized low-density lipoprotein increases expression of scavenger receptor A, CD36, and macrosialin in resident mouse peritoneal macrophages. Arterioscler Thromb Vasc Biol. 1998;18:794–802
  115. Holness CL, Simmons DL. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood. 1993;81:1607–1613
  116. Ramprasad MP, Terpstra V, Kondratenko N, Quehenberger O, Steinberg D. Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proc Natl Acad Sci USA. 1996;93:14833–14838
  117. Williams MA, Fukuda M. Accumulation of membrane glycoproteins in lysosomes requires a tyrosine residue at a particular position in the cytoplasmic tail. J Cell Biol. 1990;111:955–966
  118. da Silva RP, Gordon S. Phagocytosis stimulates alternative glycosylation of macrosialin (mouse CD68), a macrophage-specific endosomal protein. Biochem J. 1999;338(Pt 3):687–694
  119. Kurushima H, Ramprasad M, Kondratenko N, et al. Surface expression and rapid internalization of macrosialin (mouse CD68) on elicited mouse peritoneal macrophages. J Leukoc Biol. 2000;67:104–108
  120. de Villiers WJ, Smith JD, Miyata M, et al. Macrophage phenotype in mice deficient in both macrophage-colony-stimulating factor (op) and apolipoprotein E. Arterioscler Thromb Vasc Biol. 1998;18:631–640
  121. de Beer MC, Zhao Z, Webb NR, van der Westhuyzen DR, de Villiers WJ. Lack of a direct role for macrosialin in oxidized LDL metabolism. J Lipid Res. 2003;44:674–685
  122. Yamanaka S, Zhang XY, Miura K, Kim S, Iwao H. The human gene encoding the lectin-type oxidized LDL receptor (OLR1) is a novel member of the natural killer gene complex with a unique expression profile. Genomics. 1998;54:191–199
  123. Sobanov Y, Bernreiter A, Derdak S, et al. A novel cluster of lectin-like receptor genes expressed in monocytic, dendritic and endothelial cells maps close to the NK receptor genes in the human NK gene complex. Eur J Immunol. 2001;31:3493–3503
  124. Chen M, Masaki T, Sawamura T. LOX-1, the receptor for oxidized low-density lipoprotein identified from endothelial cells: implications in endothelial dysfunction and atherosclerosis. Pharmacol Ther. 2002;95:89–100
  125. Kume N, Murase T, Moriwaki H, et al. Inducible expression of lectin-like oxidized LDL receptor-1 in vascular endothelial cells. Circ Res. 1998;83:322–327
  126. Murase T, Kume N, Korenaga R, et al. Fluid shear stress transcriptionally induces lectin-like oxidized LDL receptor-1 in vascular endothelial cells. Circ Res. 1998;83:328–333
  127. Morawietz H, Duerrschmidt N, Niemann B, et al. Induction of the oxLDL receptor LOX-1 by endothelin-1 in human endothelial cells. Biochem Biophys Res Commun. 2001;284:961–965
  128. Morawietz H, Rueckschloss U, Niemann B, et al. Angiotensin II induces LOX-1, the human endothelial receptor for oxidized low-density lipoprotein. Circulation. 1999;100:899–902
  129. Li D, Mehta JL. Upregulation of endothelial receptor for oxidized LDL (LOX-1) by oxidized LDL and implications in apoptosis of human coronary artery endothelial cells: evidence from use of antisense LOX-1 mRNA and chemical inhibitors. Arterioscler Thromb Vasc Biol. 2000;20:1116–1122
  130. Nagase M, Hirose S, Fujita T. Unique repetitive sequence and unexpected regulation of expression of rat endothelial receptor for oxidized low-density lipoprotein (LOX-1). Biochem J. 1998;330:1417–1422
  131. Hoshikawa H, Sawamura T, Kakutani M, et al. High affinity binding of oxidized LDL to mouse lectin-like oxidized LDL receptor (LOX-1). Biochem Biophys Res Commun. 1998;245:841–846
  132. Xie Q, Matsunaga S, Niimi S, et al. Human lectin-like oxidized low-density lipoprotein receptor-1 functions as a dimer in living cells. DNA Cell Biol. 2004;23:111–117
  133. Murase T, Kume N, Kataoka H, et al. Identification of soluble forms of lectin-like oxidized LDL receptor-1. Arterioscler Thromb Vasc Biol. 2000;20:715–720
  134. Jono T, Miyazaki A, Nagai R, et al. Lectin-like oxidized low density lipoprotein receptor-1 (LOX-1) serves as an endothelial receptor for advanced glycation end products (AGE). FEBS Lett. 2002;511:170–174
  135. Moriwaki H, Kume N, Sawamura T, et al. Ligand specificity of LOX-1, a novel endothelial receptor for oxidized low density lipoprotein. Arterioscler Thromb Vasc Biol. 1998;18:1541–1547
  136. Kakutani M, Masaki T, Sawamura T. A platelet-endothelium interaction mediated by lectin-like oxidized low-density lipoprotein receptor-1. Proc Natl Acad Sci USA. 2000;97:360–364
  137. Oka K, Sawamura T, Kikuta K, et al. Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc Natl Acad Sci USA. 1998;95:9535–9540
  138. Shimaoka T, Kume N, Minami M, et al. LOX-1 supports adhesion of Gram-positive and Gram-negative bacteria. J Immunol. 2001;166:5108–5114
  139. Marsche G, Levak-Frank S, Quehenberger O, et al. Identification of the human analog of SR-BI and LOX-1 as receptors for hypochlorite-modified high density lipoprotein on human umbilical venous endothelial cells. FASEB J. 2001;15:1095–1097
  140. Shi X, Niimi S, Ohtani T, Machida S. Characterization of residues and sequences of the carbohydrate recognition domain required for cell surface localization and ligand binding of human lectin-like oxidized LDL receptor. J Cell Sci. 2001;114:1273–1282
  141. Chen M, Inoue K, Narumiya S, Masaki T, Sawamura T. Requirements of basic amino acid residues within the lectin-like domain of LOX-1 for the binding of oxidized low-density lipoprotein. FEBS Lett. 2001;499:215–219
  142. Chen M, Narumiya S, Masaki T, Sawamura T. Conserved C-terminal residues within the lectin-like domain of LOX-1 are essential for oxidized low-density-lipoprotein binding. Biochem J. 2001;355:289–296
  143. Kataoka H, Kume N, Miyamoto S, et al. Biosynthesis and post-translational processing of lectin-like oxidized low density lipoprotein receptor-1 (LOX-1). N-linked glycosylation affects cell-surface expression and ligand binding. J Biol Chem. 2000;275:6573–6579
  144. Bruneau N, Richard S, Silvy F, Verine A, Lombardo D. Lectin-like Ox-LDL receptor is expressed in human INT-407 intestinal cells: involvement in the transcytosis of pancreatic bile salt-dependent lipase. Mol Biol Cell. 2003;14:2861–2875
  145. Nishimura S, Akagi M, Yoshida K, et al. Oxidized low-density lipoprotein (ox-LDL) binding to lectin-like ox-LDL receptor-1 (LOX-1) in cultured bovine articular chondrocytes increases production of intracellular reactive oxygen species (ROS) resulting in the activation of NF-kappaB. Osteoarthritis Cartilage. 2004;12:568–576
  146. Kuhlmann CR, Schafer M, Li F, et al. Modulation of endothelial Ca(2+)-activated K(+) channels by oxidized LDL and its contribution to endothelial proliferation. Cardiovasc Res. 2003;60:626–634
  147. Cominacini L, Pasini AF, Garbin U, et al. Oxidized low density lipoprotein (ox-LDL) binding to ox-LDL receptor-1 in endothelial cells induces the activation of NF-kappaB through an increased production of intracellular reactive oxygen species. J Biol Chem. 2000;275:12633–12638
  148. Matsunaga T, Hokari S, Koyama I, Harada T, Komoda T. NF-kappa B activation in endothelial cells treated with oxidized high-density lipoprotein. Biochem Biophys Res Commun. 2003;303:313–319
  149. Li D, Mehta JL. Antisense to LOX-1 inhibits oxidized LDL-mediated upregulation of monocyte chemoattractant protein-1 and monocyte adhesion to human coronary artery endothelial cells. Circulation. 2000;101:2889–2895
  150. Li D, Singh RM, Liu L, et al. Oxidized-LDL through LOX-1 increases the expression of angiotensin converting enzyme in human coronary artery endothelial cells. Cardiovasc Res. 2003;57:238–243
  151. Li D, Liu L, Chen H, Sawamura T, Mehta JL. LOX-1, an oxidized LDL endothelial receptor, induces CD40/CD40L signaling in human coronary artery endothelial cells. Arterioscler Thromb Vasc Biol. 2003;23:816–821
  152. Li D, Liu L, Chen H, et al. LOX-1 mediates oxidized low-density lipoprotein-induced expression of matrix metalloproteinases in human coronary artery endothelial cells. Circulation. 2003;107:612–617
  153. Kataoka H, Kume N, Miyamoto S, et al. Oxidized LDL modulates Bax/Bcl-2 through the lectinlike Ox-LDL receptor-1 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2001;21:955–960
  154. Chen J, Mehta JL, Haider N, et al. Role of caspases in Ox-LDL-induced apoptotic cascade in human coronary artery endothelial cells. Circ Res. 2004;94:370–376
  155. Shin HK, Kim YK, Kim KY, Lee JH, Hong KW. Remnant lipoprotein particles induce apoptosis in endothelial cells by NAD(P)H oxidase-mediated production of superoxide and cytokines via lectin-like oxidized low-density lipoprotein receptor-1 activation: prevention by cilostazol. Circulation. 2004;109:1022–1028
  156. Nakagawa T, Yasuda T, Hoshikawa H, et al. LOX-1 expressed in cultured rat chondrocytes mediates oxidized LDL-induced cell death-possible role of dephosphorylation of Akt. Biochem Biophys Res Commun. 2002;299:91–97
  157. Cominacini L, Fratta Pasini A, Garbin U, et al. The platelet-endothelium interaction mediated by lectin-like oxidized low-density lipoprotein receptor-1 reduces the intracellular concentration of nitric oxide in endothelial cells. J Am Coll Cardiol. 2003;41:499–507
  158. Honjo M, Nakamura K, Yamashiro K, et al. Lectin-like oxidized LDL receptor-1 is a cell-adhesion molecule involved in endotoxin-induced inflammation. Proc Natl Acad Sci USA. 2003;100:1274–1279
  159. Shimaoka T, Kume N, Minami M, et al. Lectin-like oxidized low density lipoprotein receptor-1 (LOX-1) supports cell adhesion to fibronectin. FEBS Lett. 2001;504:65–68
  160. Hu B, Li D, Sawamura T, Mehta JL. Oxidized LDL through LOX-1 modulates LDL-receptor expression in human coronary artery endothelial cells. Biochem Biophys Res Commun. 2003;307:1008–1012
  161. Tatsuguchi M, Furutani M, Hinagata J, et al. Oxidized LDL receptor gene (OLR1) is associated with the risk of myocardial infarction. Biochem Biophys Res Commun. 2003;303:247–250
  162. Mango R, Clementi F, Borgiani P, et al. Association of single nucleotide polymorphisms in the oxidised LDL receptor 1 (OLR1) gene in patients with acute myocardial infarction. J Med Genet. 2003;40:933–936
  163. Chen M, Kakutani M, Minami M, et al. Increased expression of lectin-like oxidized low density lipoprotein receptor-1 in initial atherosclerotic lesions of Watanabe heritable hyperlipidemic rabbits. Arterioscler Thromb Vasc Biol. 2000;20:1107–1115
  164. Kataoka H, Kume N, Miyamoto S, et al. Expression of lectinlike oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation. 1999;99:3110–3117
  165. Nakagawa T, Akagi M, Hoshikawa H, et al. Lectin-like oxidized low-density lipoprotein receptor 1 mediates leukocyte infiltration and articular cartilage destruction in rat zymosan-induced arthritis. Arthritis Rheum. 2002;46:2486–2494
  166. Li D, Williams V, Liu L, et al. Expression of lectin-like oxidized low-density lipoprotein receptors during ischemia-reperfusion and its role in determination of apoptosis and left ventricular dysfunction. J Am Coll Cardiol. 2003;41:1048–1055
  167. Li D, Williams V, Liu L, et al. LOX-1 inhibition in myocardial ischemia–reperfusion injury: modulation of MMP-1 and inflammation. Am J Physiol Heart Circ Physiol. 2002;283:1795–1801
  168. Nagase M, Kaname S, Nagase T, et al. Expression of LOX-1, an oxidized low-density lipoprotein receptor, in experimental hypertensive glomerulosclerosis. J Am Soc Nephrol. 2000;11:1826–1836
  169. Adachi H, Tsujimoto M, Arai H, Inoue K. Expression cloning of a novel scavenger receptor from human endothelial cells. J Biol Chem. 1997;272:31217–31220
  170. Adachi H, Tsujimoto M. Characterization of the human gene encoding the scavenger receptor expressed by endothelial cell and its regulation by a novel transcription factor, endothelial zinc finger protein-2. J Biol Chem. 2002;277:24014–24021
  171. Ishii J, Adachi H, Aoki J, et al. SREC-II, a new member of the scavenger receptor type F family, trans-interacts with SREC-I through its extracellular domain. J Biol Chem. 2002;277:39696–39702
  172. Zhou Z, Hartwieg E, Horvitz HR. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell. 2001;104:43–56
  173. Tamura Y, et al. Scavenger receptor expressed by endothelial cells I (SREC-I) mediates the uptake of acetylated low density lipoproteins by macrophages stimulated with lipopolysaccharide. J Biol Chem. 2004;279:30938–30944
  174. Shibata M, Ishii J, Koizumi H, et al. Type F scavenger receptor SREC-I interacts with advillin, a member of the gelsolin/villin family, and induces neurite-like outgrowth. J Biol Chem 2004.
  175. Shimaoka T, Kume N, Minami M, et al. Molecular cloning of a novel scavenger receptor for oxidized low density lipoprotein, SR-PSOX, on macrophages. J Biol Chem. 2000;275:40663–40666
  176. Abel S, Hundhausen C, Mentlein R, et al. The transmembrane CXC-chemokine ligand 16 is induced by IFN-gamma and TNF-alpha and shed by the activity of the disintegrin-like metalloproteinase ADAM10. J Immunol. 2004;172:6362–6372
  177. Shimaoka T, Nakayama T, Kume N, et al. Cutting edge: SR-PSOX/CXC chemokine ligand 16 mediates bacterial phagocytosis by APCs through its chemokine domain. J Immunol. 2003;171:1647–1651
  178. Chandrasekar B, Bysani S, Mummidi S. CXCL16 signals via Gi, phosphatidylinositol 3-kinase, Akt, I kappa B kinase, and nuclear factor-kappa B and induces cell-cell adhesion and aortic smooth muscle cell proliferation. J Biol Chem. 2004;279:3188–3196
  179. Minami M, Kume N, Shimaoka T, et al. Expression of SR-PSOX, a novel cell-surface scavenger receptor for phosphatidylserine and oxidized LDL in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2001;21:1796–1800
  180. Fukumoto N, Shimaoka T, Fujimura H, et al. Critical roles of CXC chemokine ligand 16/scavenger receptor that binds phosphatidylserine and oxidized lipoprotein in the pathogenesis of both acute and adoptive transfer experimental autoimmune encephalomyelitis. J Immunol. 2004;173:1620–1627
  181. Yamauchi R, Tanaka M, Kume N, et al. Upregulation of SR-PSOX/CXCL16 and recruitment of CD8+ T cells in cardiac valves during inflammatory valvular heart disease. Arterioscler Thromb Vasc Biol. 2004;24:282–287
  182. Adachi H, Tsujimoto M. FEEL-1, a novel scavenger receptor with in vitro bacteria-binding and angiogenesis-modulating activities. J Biol Chem. 2002;277:34264–34270
  183. Politz O, Gratchev A, McCourt PA, et al. Stabilin-1 and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues. Biochem J. 2002;362:155–164
  184. Irjala H, Elima K, Johansson E, et al. The same endothelial receptor controls lymphocyte traffic both in vascular and lymphatic vessels. Eur J Immunol. 2003;33:815–824
  185. Tamura Y, Adachi H, Osuga J, et al. FEEL-1 and FEEL-2 are endocytic receptors for advanced glycation end products. J Biol Chem. 2003;278:12613–12617
  186. Prevo R, Banerji S, Ni J, Jackson DG. Rapid plasma membrane–endosomal trafficking of the lymph node sinus and high endothelial venule scavenger receptor/homing receptor stabilin-1 (FEEL-1/CLEVER-1). J Biol Chem. 2004;279:52580–52592
  187. McCourt PA, Smedsrod BH, Melkko J, Johansson S. Characterization of a hyaluronan receptor on rat sinusoidal liver endothelial cells and its functional relationship to scavenger receptors. Hepatology. 1999;30:1276–1286
  188. Kzhyshkowska J, Gratchev A, Martens JH, et al. Stabilin-1 localizes to endosomes and the trans-Golgi network in human macrophages and interacts with GGA adaptors. J Leukoc Biol. 2004;76:1151–1161
  189. Hansen B, Longati P, Elvevold K, et al. Stabilin-1 and stabilin-2 are both directed into the early endocytic pathway in hepatic sinusoidal endothelium via interactions with clathrin/AP-2, independent of ligand binding. Exp Cell Res. 2005;303:160–173
  190. Irjala H, Alanen K, Grenman R, et al. Mannose receptor (MR) and common lymphatic endothelial and vascular endothelial receptor (CLEVER)-1 direct the binding of cancer cells to the lymph vessel endothelium. Cancer Res. 2003;63:4671–4676
  191. Salmi M, Koskinen K, Henttinen T, Elima K, Jalkanen S. CLEVER-1 mediates lymphocyte transmigration through vascular and lymphatic endothelium. Blood. 2004;104:3849–3857
  192. Horiuchi S, Sakamoto Y, Sakai M. Scavenger receptors for oxidized and glycated proteins. Amino Acids. 2003;25:283–292
  193. Ahmed N. Advanced glycation endproducts—role in pathology of diabetic complications. Diabetes Res Clin Pract. 2005;67:3–21
  194. Araki N, Higashi T, Mori T, et al. Macrophage scavenger receptor mediates the endocytic uptake and degradation of advanced glycation end products of the Maillard reaction. Eur J Biochem. 1995;230:408–415
  195. Ohgami N, Nagai R, Ikemoto M, et al. Cd36, a member of the class b scavenger receptor family, as a receptor for advanced glycation end products. J Biol Chem. 2001;276:3195–3202
  196. Ohgami N, Nagai R, Miyazaki A, et al. Scavenger receptor class B type I-mediated reverse cholesterol transport is inhibited by advanced glycation end products. J Biol Chem. 2001;276:13348–13355
  197. Neeper M, Schmidt AM, Brett J, et al. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem. 1992;267:14998–15004
  198. Kislinger T, Fu C, Huber B, et al. N(epsilon)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J Biol Chem. 1999;274:31740–31749
  199. Park L, Raman KG, Lee KJ, et al. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med. 1998;4:1025–1031
  200. Gugliucci A. Glycation as the glucose link to diabetic complications. J Am Osteopath Assoc. 2000;100:621–634
  201. Basta G, Schmidt AM, De Caterina R. Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes. Cardiovasc Res. 2004;63:582–592
  202. Sorkin A, Von Zastrow M. Signal transduction and endocytosis: close encounters of many kinds. Nat Rev Mol Cell Biol. 2002;3:600–614
  203. Aoyama T, Fujiwara H, Masaki T, Sawamura T. Induction of lectin-like oxidized LDL receptor by oxidized LDL and lysophosphatidylcholine in cultured endothelial cells. J Mol Cell Cardiol. 1999;31:2101–2114

PII: S0021-9150(05)00250-9

doi: 10.1016/j.atherosclerosis.2005.03.036

Atherosclerosis
Volume 182, Issue 1 , Pages 1-15 , September 2005