Scavenger receptors: A key player in cardiovascular diseases

Biomolecular Concepts

Volumn 3, Issue 4, 2012, Pages 371-380

  Ashraf, Mohammad Z ^a   Sahu, Anita ^a  

^a DEFENCE INSTITUTE OF PHYSIOLOGY AND ALLIED SCIENCES   (India)

Author keywords

atherosclerosis; lipoproteins; oxidized phospholipids; scavenger receptors; thrombosis

Indexed keywords

EID: 85016609585     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/bmc-2012-0003     Document Type: Article

References (80)

1. 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.
2. Murphy JE, Tedbury PR, Homer-Vanniasinkam S, Walker JH, Ponnambalam S. Biochemistry and cell biology of mammalian scavenger receptors. Atherosclerosis 2005; 182: 1–15.
3. Plüddemann A, Neyen C, Gordon S. Macrophage scavenger receptors and host-derived ligands. Methods 2007; 43: 207–217.
4. Krieger M. The other side of scavenger receptors: pattern recognition for host defense. Curr Opin Lipidol 1997; 8: 275–280.
5. Platt N, Haworth R, Darley L, Gordon S. The many roles of the class A macrophage scavenger receptor. Int Rev Cytol 2002; 212: 1–40.
6. Gough PJ, Greaves DR, Gordon S. A naturally occurring isoform of the human macrophage scavenger receptor (SR-A) gene generated by alternative splicing blocks modifi ed LDL uptake. J Lipid Res 1998; 39: 531–543.
7. Jiang Y, Oliver P, Davies KE, Platt N. Identification and characterization of murine SCARA5, a novel class A scavenger receptor that is expressed by populations of epithelial cells. J Biol Chem 2006; 281: 11834–11845.
8. 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.
9. Kunjathoor VV, Febbraio M, Podrez EA, Moore KJ, Andersson L, Koehn S, Rhee JS, Silverstein R, Hoff HF, Freeman MW. 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.
10. 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.
11. Suzuki H, Kurihara Y, Takeya M, Kamada N, Kataoka M, Jishage K, Ueda O, Sakaguchi H, Higashi T, Suzuki T, Takashima Y, Kawabe Y, Cynshi O, Wada Y, Honda M, Kurihara H, Aburatani H, Doi T, Matsumoto A, Azuma S, Noda T, Toyoda Y, Itakura H, Yazaki Y, Horiuchi S, Takahashi K, Kruijt JK, Van Berkel TJC, Steinbrecher UP, Ishibashi S, Maeda N, Gordon S, Kodama T. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 1997; 386: 292–296.
12. Korporaal SJ, Van Eck M, Adelmeijer J, Ijsseldijk M, Out R, Listman T, Lenting PJ, Van Berkel TJ, Akkerman JW. Platelet activation by oxidized low density lipoprotein is mediated by CD36 and scavenger receptor-A. Arterioscler Thromb Vasc Biol 2007; 27: 2476–2483.
13. Korporaal SJ, Relou IA, van Eck M, Strasser V, Bezemer M, Gorter G, van Berkel TJ, Nimpf J, Akkerman JW, Lenting P.J. Binding of low density lipoprotein to platelet apolipoprotein E receptor 2 results in phosphorylation of p38 MAPK. J Biol Chem 2004; 279: 52526–52534.
14. Mäkinen PI, Lappalainen JP, Heinonen SE, Leppänen P, Lähteenvuo MT, Aarnio JV, Heikkilä J, Turunen MP, Ylä-Herttuala S. Silencing of either SR-A or CD36 reduces arthrosclerosis in hyperlipidaemic mice and reveals reciprocal upregulation of these receptors. Cardiovasc Res 2010; 88: 530–538.
15. Kraal G, van der Laan LJ, Elomaa O, Tryggvason K. The macrophage receptor MARCO. Microbes Infect 2000; 2: 313–316.
16. Grolleau A, Misek DE, Kuick R, Hanash S, Mulé 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.
17. Arredouani M, Yang Z, Ning YY, Qin G, Soininen R, Tryggvason K, Kobzik L. The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles. J Exp Med 2004; 200: 267–272.
18. Arredouani MS, Palecanda A, Koziel H, Huang YC, Imrich A, Sulahian TH, Ning YY, Yang Z, Pikkarainen T, Sankala M, Vargas SO, Takeya M, Tryggvason K, Kobzik L. MARCO is the major binding receptor for unopsonized particles and bacteria on human alveolar macrophages. J Immunol 2005; 175: 6058–6064.
19. Ohtani K, Suzuki Y, Eda S, Kawai T, Kase T, Keshi H, Sakai Y, Fukuoh A, Sakamoto T, Itabe H, Suzutani T, Ogasawara M, Yoshida I, Wakamiya N. The membrane type collectin CL-P1 is a scavenger receptor on vascular endothelial cells. J Biol Chem 2001; 276: 44222–44228.
20. Jang SJ, Ohtani K, Fukuoh A, Yoshizaki T, Fukuda M, Motomura W, Mori K, Fukuzawa J, Kitamoto N, Yoshida I, Suzuki Y, Wakamiya N. Scavenger receptor collectin placenta 1 (CL-P1) predominantly mediates zymosan phagocytosis by human vascular endothelial cells. J Biol Chem 2009; 284: 3956–3965.
21. Auclair S, Milenkovic D, Besson C, Chauvet S, Gueux E, Morand C, Mazur A, Scalbert A. Catechin reduces atherosclerotic lesion development in apo E-deficient mice: a transcriptomic study. Atherosclerosis 2009; 204: 21–27.
22. Knowles DM 2nd, Tolidijian B, Marboe C, D'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 1984; 132: 2170–2173.
23. Tao N, Wagner SJ, Lublin DM. CD36 is palmitoylated on both N-and C-terminal cytoplasmic tails. J Biol Chem 1996; 271: 22315–22320.
24. Febbraio M, Hajjar DP, Silverstein RL. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, infl ammation, and lipid metabolism. J Clin Invest 2001; 108: 785–791.
25. Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, Crozat K, Sovath S, Shamel L, Hartung T, Zähringer U, Beutler B. CD36 is a sensor of diacylglycerides. Nature 2005; 433: 523–527.
26. Podrez EA, Febbraio M, Sheibani N, Schmitt D, Silverstein RL, Hajjar DP, Cohen PA, Frazier WA, Hoff HF, Hazen SL. Macrophage scavenger receptor CD36 is the major receptor for LDL modifi ed by monocyte-generated reactive nitrogen species. J Clin Invest 2000; 105: 1095–1108.
27. Febbraio M, Guy E, Silverstein RL. Stem cell transplantation reveals that absence of macrophage CD36 is protective against atherosclerosis. Arterioscler Thromb Vasc Biol 2004; 24: 2333–2338.
28. Guy E, Kuchibhotla S, Silverstein RL, Febbraio M. Continued inhibition of atherosclerotic lesion development in long term Western diet fed CD36° /apoE° mice. Atherosclerosis 2007; 192: 123–130.
29. Rahaman SO, Lennon DJ, Febbraio M, Podrez EA, Hazen SL, Silverstein RL. A CD36-dependent signalling cascade is necessary for macrophage foam cell formation. Cell Metab 2006; 4: 211–221.
30. Febbraio M, Podrez EA, Smith JD, Hajjar DP, Hazen SL, Hoff HF, Sharma K, Silverstein RL. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J Clin Invest 2000; 105: 1049–1056.
31. Silverstein RL. Type 2 scavenger receptor CD36 in platelet activation: the role of hyperlipemia and oxidative stress. Clin Lipidol 2009; 4: 767.
32. Podrez EA, Byzova TV, Febbraio M, Salomon RG, Ma Y, Valiyaveettil M, Poliakov E, Sun M, Finton PJ, Curtis BR, Chen J, Zhang R, Silverstein RL, Hazen SL. Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype. Nat Med 2007; 13: 1086–1095.
33. Göpfert MS, Siedler F, Siess W, Sellmayer A. Structural identification of oxidized acylphosphatidylcholines that induce platelet activation. J Vasc Res 2005; 42: 120–132.
34. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP. CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 1997; 138: 707–717.
35. Li W, Febbraio M, Reddy SP, Yu DY, Yamamoto M, Silverstein RL. CD36 participates in a signaling pathway that regulates ROS formation in murine VSMCs. J Clin Invest 2010; 120: 3996–4006.
36. Silverstein RL, Li W, Park YM, Rahaman SO. Mechanisms of cell signaling by the scavenger receptor CD36: implications in atherosclerosis and thrombosis. Trans Am Clin Climatol Assoc 2010; 121: 206–220.
37. Medeiros LA, Khan T, El Khoury JB, Pham CL, Hatters DM, Howlett GJ, Lopez R, O'Brien KD, Moore KJ. Fibrillar amyloid protein present in atheroma activates CD36 signal transduction. J Biol Chem 2004; 279: 10643–10648.
38. De Meyer GR, De Cleen DM, Cooper S, Knaapen MW, Jans DM, Martinet W, Herman AG, Bult H, Kockx MM. Platelet phagocytosis and processing of β-amyloid precursor protein as a mechanism of macrophage activation in atherosclerosis. Circ Res 2002; 90: 1197–1204.
39. Silver DL. SR-BI and protein-protein interactions in hepatic high density lipoprotein metabolism. Rev Endocr Metab Disord 2004; 5: 327–333.
40. Krieger M. Charting the fate of the “ good cholesterol”: identification and characterization of high-density lipoprotein receptor SR-BI. Annu Rev Biochem 1999; 68: 523–558.
41. Kozarsky KF, Donahee MH, Rigotti A, Iqbal SN, Edelman E, Krieger M. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature 1997; 387: 414–417.
42. Ashraf MZ, Kar NS, Chen X, Choi J, Febbraio M, Podrez EA. Specific oxidized phospholipids inhibit scavenger receptors BI mediated selective uptake of cholesteryl esters. J Biol Chem 2008; 283: 10408–10414.
43. Hirano K, Yamashita S, Nakagawa Y, Ohya T, Matsuura F, Tsukamoto K, Okamoto Y, Matsuyama A, Matsumoto K, Miyagawa J, Matsuzawa Y. Expression of human scavenger receptor class B type I in cultured human monocyte-derived macrophages and atherosclerotic lesions. Circ Res 1999; 85: 108–116.
44. Stangl H, Cao G, Wyne KL, Hobbs HH. Scavenger receptor, class B, type I-dependent stimulation of cholesterol esterification by high density lipoproteins, low density lipoproteins, and nonlipoprotein cholesterol. J Biol Chem 1998; 273: 31002–31008.
45. Zhang W, Yancey PG, Su YR, Babaev VR, Zhang Y, Fazio S, Linton MF. Inactivation of macrophage scavenger receptor class B type I promotes atherosclerotic lesion development in apolipo-protein E deficient mice. Circulation 2003; 108: 2258–2263.
46. Van Eck M, Bos IS, Hildebrand RB, Van Rij BT, Van Berkel TJ. Dual role for scavenger receptor class B, type I on bone marrow-derived cells in atherosclerotic lesion development. Am J Pathol 2004; 165: 785–794.
47. Seetharam D, Mineo C, Gormley AK, Gibson LL, Vongpatanasin W, Chambliss KL, Hahner LD, Cummings ML, Kitchens RL, Marcel YL, Rader DJ, Shaul P.W. High-density lipoprotein promotes endothelial cell migration and reendothelialization via scavenger receptor-B type I. Circ Res 2006; 98: 63–72.
48. Imachi H, Murao K, Cao W, Tada S, Taminato T, Wong NC, Takahara J, Ishida T. Expression of human scavenger receptor B1 on and in human platelets. Arterioscler Thromb Vasc Biol 2003; 23: 898–904.
49. Dole VS, Matuskova J, Vasile E, Yesilaltay A, Bergmeier W, Bernimoulin M, Wagner DD, Krieger M. Thrombocytopenia and platelet abnormalities in high-density lipoprotein receptor deficient mice. Arterioscler Thromb Vasc Biol 2008; 28: 1111–1116.
50. Korporaal SJ, Meurs I, Hauer AD, Hildebrand RB, Hoekstra M, Ten Cate HT, Prati$ o D, Akkerman JW, Van Berkel TJ, Kuiper J, Van Eck M. Deletion of the high-density lipoprotein receptor scavenger receptor BI in mice modulates thrombosis susceptibility and indirectly affects platelet function by elevation of plasma free cholesterol. Arterioscler Thromb Vasc Biol 2011; 31: 34–42.
51. Ma Y, Ashraf MZ, Podrez EA. Scavenger receptor BI modulates platelet reactivity and thrombosis in dyslipidemia. Blood 2010; 116: 1932–1941.
52. 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.
53. Sun B, Boyanovsky BB, Connelly MA, Shridas P, van der Westhuyzen DR, Webb NR. Distinct mechanisms for OxLDL uptake and cellular trafficking by class B scavenger receptors CD36 and SR-BI. J Lipid Res 2007; 48: 2560–2570.
54. Moestrup SK, Moller HJ. CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann Med 2004; 36: 347–354.
55. Gleissner CA, Shaked I, Erbel C, Böckler D, Katus HA, Ley K. CXCL4 downregulates the atheroprotective hemoglobin receptor CD163 in human macrophages. Circ Res 2010; 106: 203–211.
56. Ramprasad MP, Fischer W, Witztum JL, Sambrano GR, Quehenberger O, Steinberg D. The 94-to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc Natl Acad Sci USA 1995; 92: 9580–9584.
57. 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.
58. 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.
59. Sawamura T, Kume N, Aoyama T, Moriwaki H, Hoshikawa H, Aiba Y, Tanaka T, Miwa S, Katsura Y, Kita T, Masaki T. An endothelial receptor for oxidized low-density lipoprotein. Nature 1997; 386: 73–77.
60. Kataoka H, Kume N, Miyamoto S, Minami M, Moriwaki H, Murase T, Sawamura T, Masaki T, Hashimoto N, Kita T. Expression of lectin-like oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation 1999; 99: 3110–3117.
61. 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.
62. Nagase M, Hirose S, Sawamura T, Masaki T, Fujita T. Enhanced expression of endothelial oxidized low-density lipoprotein receptor (LOX-1) in hypertensive rats. Biochem Biophys Res Commun 1997; 237: 496–498.
63. Mehta JL, Chen J, Hermonat PL, Romeo F, Novelli G. Lectin-like, oxidized low-density lipoprotein receptor-1 (LOX-1): a critical player in the development of atherosclerosis and related disorders. Cardiovasc Res 2006; 69: 36–45.
64. 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.
65. Chen M, Kakutani M, Naruko T, Ueda M, Narumiya S, Masaki T, Sawamura T. Activation-dependent surface expression of LOX-1 in human platelets. Biochem Biophys Res Commun 2001; 282: 153–158.
66. Takahashi Y, Fuda H, Yanai H, Akita H, Shuping H, Chiba H, Matsuno K. Significance of membrane glycoproteins in platelet interaction with oxidized low-density lipoprotein. Semin Thromb Hemost 1998; 24: 251–253.
67. Tamura Y, Osuga J, Adachi H, Tozawa R, Takanezawa Y, Ohashi K, Yahagi N, Sekiya M, Okazaki H, Tomita S, Iizuka Y, Koizumi H, Inaba T, Yagyu H, Kamada N, Suzuki H, Shimano H, Kadowaki T, Tsujimoto M, Arai H, Yamada N, Ishibashi S. 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.
68. Greaves DR, Gordon S. Thematic review series: the immune system and atherogenesis. Recent insights into the biology of macrophage scavenger receptors. J Lipid Res 2005; 46: 11–20.
69. Shimaoka T, Nakayama T, Kume N, Takahashi S, Yamaguchi J, Minami M, Hayashida K, Kita T, Ohsumi J, Yoshie O, Yonehara S. Cutting edge: SR-PSOX/CXC chemokine ligand 16 mediates bacterial phagocytosis by APCs through its chemokine domain. J Immunol 2003; 171: 1647–1651.
70. Minami M, Kume N, Shimaoka T, Kataoka H, Hayashida K, Akiyama Y, Nagata I, Ando K, Nobuyoshi M, Hanyuu M, Komeda M, Yonehara S, Kita T. 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.
71. Aslanian AM, Charo IF. Targeted disruption of the scavenger receptor and chemokine CXCL16 accelerates atherosclerosis. Circulation 2006; 114: 583–590.
72. Yamauchi R, Tanaka M, Kume N, Minami M, Kawamoto T, Togi K, Shimaoka T, Takahashi S, Yamaguchi J, Nishina T, Kitaichi M, Komeda M, Manabe T, Yonehara S, Kita T. Up-regulation of SR-PSOX/CXCL16 and recruitment of CD4+ T cells in cardiac valves during inflammatory valvular heart disease. Arterioscler Thromb Vasc Biol 2004; 24: 282–287.
73. Siegel-Axel D, Daub K, Seizer P, Lindemann S, Gawaz M. Platelet lipoprotein interplay: trigger of foam cell formation and driver of atherosclerosis. Cardiovasc Res 2008; 78: 8–17.
74. Hildebrand RB, Lammers B, Meurs I, Korporaal SJ, De Haan W, Zhao Y, Kruijt JK, Pratic o D, Schimmel AW, Holleboom AG, Hoekstra M, Kuivenhoven JA, Van Berkel TJ, Rensen PC, Van Eck M. Restoration of high-density lipoprotein levels by cholesteryl ester transfer protein expression in scavenger receptor class B type I (SR-BI) knockout mice does not normalize pathologies associated with SR-BI deficiency. Arterioscler Thromb Vasc Biol 2010; 30: 1439–1445.
75. Stephen SL, Freestone K, Dunn S, Twigg MW, Homer-Vanniasinkam S, Walker JH, Wheatcroft SB, Ponnambalam S. Scavenger receptors and their potential as therapeutic targets in the treatment of cardiovascular disease. Int J Hypertens 2010; 2010: 646929.
76. Ockenhouse CF, Tandon NN, Magowan C, Jamieson GA, Chulay JD. Identification of a platelet membrane glycoprotein as a Falciparum malaria sequestration receptor. Science 1989; 243: 1469–1471.
77. Ren Y, Silverstein RL, Allen J, Savill J. CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J Exp Med 1995; 181: 1857–1862.
78. Greenberg ME, Sun M, Zhang R, Febbraio M, Silverstein R, Hazen SL. Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. Cell Metab 2006; 4: 211–221.
79. Kennedy DJ, Kuchibhotla S, Westfall KM, Silverstein RL, Morton RE, Febbraio M. A CD36-dependent pathway enhances macrophage and adipose tissue inflammation and impairs insulin signalling. Cardiovasc Res 2011; 89: 604–613.
80. Braun A, Trigatti BL, Post MJ, Sato K, Simons M, Edelberg JM, Rosenberg RD, Schrenzel M, Krieger M. 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.