Scavenger receptor structure and function in health and disease

Cells

Volumn 4, Issue 2, 2015, Pages 178-201

  Zani, Izma Abdul ^a   Stephen, Sam L ^a   Mughal, Nadeem A ^a,b   Russell, David ^b   Homer Vanniasinkam, Shervanthi ^b   Wheatcroft, Stephen B ^c   Ponnambalam, Sreenivasan ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b LEEDS GENERAL INFIRMARY   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Atherosclerosis; Oxidized LDL particle; Scavenger receptor; Signal transduction

Indexed keywords

CXCL16 CHEMOKINE; HEAT SHOCK PROTEIN 70; LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; REACTIVE OXYGEN METABOLITE; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR A; SCAVENGER RECEPTOR B; SCAVENGER RECEPTOR C; SCAVENGER RECEPTOR D; SCAVENGER RECEPTOR F;

AMINO ACID SEQUENCE; ATHEROSCLEROSIS; CELL FUNCTION; CELL MIGRATION; GENE; GENETIC TRANSCRIPTION; HUMAN; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; REVIEW; SCARA1 GENE; SCARB GENE; SIGNAL TRANSDUCTION; SRCL GENE; THROMBOCYTE ACTIVATION; VASCULAR SMOOTH MUSCLE;

EUKARYOTA;

EID: 85050577595     PISSN: None     EISSN: 20734409     Source Type: Journal    
DOI: 10.3390/cells4020178     Document Type: Review

References (155)

1. Prabhudas, M.; Bowdish, D.; Drickamer, K.; Febbraio, M.; Herz, J.; Kobzik, L.; Krieger, M.; Loike, J.; Means, T.K.; Moestrup, S.K.; et al. Standardizing scavenger receptor nomenclature. J. Immunol. 2014, 192, 1997-2006.
2. Kang, J.Y.; Lee, J.O. Structural biology of the Toll-like receptor family. Annu Rev. Biochem. 2011, 80, 917-941.
3. Gowen, B.B.; Borg, T.K.; Ghaffar, A.; Mayer, E.P. The collagenous domain of class A scavenger receptors is involved in macrophage adhesion to collagens. J. Leukoc. Biol. 2001, 69, 575-582.
4. Mietus-Snyder, M.; Friera, A.; Glass, C.K.; Pitas, R.E. Regulation of scavenger receptor expression in smooth muscle cells by protein kinase C: a role for oxidative stress. Arterioscler Thromb. Vasc. Biol. 1997, 17, 969-978.
5. Pitas, R.E. Expression of the acetyl low density lipoprotein receptor by rabbit fibroblasts and smooth muscle cells. Up-regulation by phorbol esters. J. Biol. Chem. 1990, 265, 12722-12727.
6. Han, H.J.; Tokino, T.; Nakamura, Y. CSR, a scavenger receptor-like protein with a protective role against cellular damage causedby UV irradiation and oxidative stress. Hum. Mol. Genet. 1998, 7, 1039-1046.
7. Li, J.Y.; Paragas, N.; Ned, R.M.; Qiu, A.; Viltard, M.; Leete, T.; Drexler, I.R.; Chen, X.; Sanna- Cherchi, S.; Mohammed, F.; et al. Scara5 is a ferritin receptor mediating non-transferrin iron delivery. Dev. Cell. 2009, 16, 35-46.
8. Kangas, M.; Brannstrom, A.; Elomaa, O.; Matsuda, Y.; Eddy, R.; Shows, T.B.; Tryggvason, K. Structure and chromosomal localization of the human and murine genes for the macrophage MARCO receptor. Genomics 1999, 58, 82-89.
9. Ojala, J.R.; Pikkarainen, T.; Tuuttila, A.; Sandalova, T.; Tryggvason, K. Crystal structure of the cysteine-rich domain of scavenger receptor MARCO reveals the presence of a basic and an acidic cluster that both contribute to ligand recognition. J. Biol. Chem. 2007, 282, 16654-16666.
10. Kraal, G.; van der Laan, L.J.; Elomaa, O.; Tryggvason, K. The macrophage receptor MARCO. Microbes Infect. 2000, 2, 313-316.
11. Thelen, T.; Hao, Y.; Medeiros, A.I.; Curtis, J.L.; Serezani, C.H.; Kobzik, L.; Harris, L.H.; Aronoff, D.M. The class A scavenger receptor, macrophage receptor with collagenous structure, is the major phagocytic receptor for Clostridium sordellii expressed by human decidual macrophages. J. Immunol. 2010, 185, 4328-4335.
12. Chen, Y.; Wang, X.; Ben, J.; Yue, S.; Bai, H.; Guan, X.; Bai, X.; Jiang, L.; Ji, Y.; Fan, L.; et al. The di-leucine motif contributes to class a scavenger receptor-mediated internalization of acetylated lipoproteins. Arterioscler. Thromb. Vasc. Biol. 2006, 26, 1317-1322.
13. Zhu, X.D.; Zhuang, Y.; Ben, J.J.; Qian, L.L.; Huang, H.P.; Bai, H.; Sha, J.H.; He, Z.G.; Chen, Q. Caveolae-dependent endocytosis is required for class A macrophage scavenger receptor-mediated apoptosis in macrophages. J. Biol. Chem. 2011, 286, 8231-8239.
14. Amiel, E.; Nicholson-Dykstra, S.; Walters, J.J.; Higgs, H.; Berwin, B. Scavenger receptor-A functions in phagocytosis of E. coli by bone marrow dendritic cells. Exp. Cell. Res. 2007, 313, 1438-1448.
15. Suzuki, H.; Kurihara, Y.; Takeya, M.; Kamada, N.; Kataoka, M.; Jishage, K.; Ueda, O.; Sakaguchi, H.; Higashi, T.; Suzuki, T.; et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 1997, 386, 292-296.
16. 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, doi:10.5551/jat1994.8.1.
17. Manning-Tobin, J.J.; Moore, K.J.; Seimon, T.A.; Bell, S.A.; Sharuk, M.; Alvarez-Leite, J.I.; de Winther, M.P.; Tabas, I.; Freeman, M.W. Loss of SR-A and CD36 activity reduces atherosclerotic lesion complexity without abrogating foam cell formation in hyperlipidemic mice. Arterioscler. Thromb. Vasc. Biol. 2009, 29, 19-26.
18. Makinen, P.I.; Lappalainen, J.P.; Heinonen, S.E.; Leppanen, P.; Lahteenvuo, M.T.; Aarnio, J.V.; Heikkila, J.; Turunen, M.P.; Yla-Herttuala, S. Silencing of either SR-A or CD36 reduces atherosclerosis in hyperlipidaemic mice and reveals reciprocal upregulation of these receptors. Cardiovasc. Res. 2010, 88, 530-538.
19. Jalkanen, J.; Leppanen, P.; Narvanen, O.; Greaves, D.R.; Yla-Herttuala, S. Adenovirus-mediated gene transfer of a secreted decoy human macrophage scavenger receptor (SR-AI) in LDL receptor knock-out mice. Atherosclerosis 2003, 169, 95-103.
20. Ricci, R.; Sumara, G.; Sumara, I.; Rozenberg, I.; Kurrer, M.; Akhmedov, A.; Hersberger, M.; Eriksson, U.; Eberli, F.R.; Becher, B.; et al. Requirement of JNK2 for scavenger receptor A-mediated foam cell formation in atherogenesis. Science 2004, 306, 1558-1561.
21. Ohnishi, K.; Komohara, Y.; Fujiwara, Y.; Takemura, K.; Lei, X.; Nakagawa, T.; Sakashita, N.; Takeya, M. Suppression of TLR4-mediated inflammatory response by macrophage class A scavenger receptor (CD204). Biochem. Biophys. Res. Commun. 2011, 411, 516-522.
22. Dahl, M.; Bauer, A.K.; Arredouani, M.; Soininen, R.; Tryggvason, K.; Kleeberger, S.R.; Kobzik, L. Protection against inhaled oxidants through scavenging of oxidized lipids by macrophage receptors MARCO and SR-AI/II. J. Clin. Invest. 2007, 117, 757-764.
23. Mukhopadhyay, S.; Varin, A.; Chen, Y.; Liu, B.; Tryggvason, K.; Gordon, S. SR-A/MARCOmediated ligand delivery enhances intracellular TLR and NLR function, but ligand scavenging from cell surface limits TLR4 response to pathogens. Blood 2011, 117, 1319-1328.
24. Jozefowski, S.; Arredouani, M.; Sulahian, T.; Kobzik, L. Disparate regulation and function of the class A scavenger receptors SR-AI/II and MARCO. J. Immunol. 2005, 175, 8032-8041.
25. 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.
26. Chen, Y.; Pikkarainen, T.; Elomaa, O.; Soininen, R.; Kodama, T.; Kraal, G.; Tryggvason, K. Defective microarchitecture of the spleen marginal zone and impaired response to a thymusindependent type 2 antigen in mice lacking scavenger receptors MARCO and SR-A. J. Immunol. 2005, 175, 8173-8180.
27. Berwin, B.; Hart, J.P.; Rice, S.; Gass, C.; Pizzo, S.V.; Post, S.R.; Nicchitta, C.V. Scavenger receptor-A mediates gp96/GRP94 and calreticulin internalization by antigen-presenting cells. EMBO J. 2003, 22, 6127-6136.
28. Fischer, N.; Haug, M.; Kwok, W.W.; Kalbacher, H.; Wernet, D.; Dannecker, G.E.; Holzer, U. Involvement of CD91 and scavenger receptors in Hsp70-facilitated activation of human antigen-specific CD4+ memory T cells. Eur J. Immunol. 2010, 40, 986-997.
29. Graham, S.A.; Antonopoulos, A.; Hitchen, P.G.; Haslam, S.M.; Dell, A.; Drickamer, K.; Taylor, M.E. Identification of neutrophil granule glycoproteins as Lewis(x)-containing ligands cleared by the scavenger receptor C-type lectin. J. Biol. Chem. 2011, 286, 24336-24349.
30. Yoshida, T.; Tsuruta, Y.; Iwasaki, M.; Yamane, S.; Ochi, T.; Suzuki, R. SRCL/CL-P1 recognizes GalNAc and a carcinoma-associated antigen, Tn antigen. J. Biochem. 2003, 133, 271-277.
31. Jang, S.; Ohtani, K.; Fukuoh, A.; Yoshizaki, T.; Fukuda, M.; Motomura, W.; Mori, K.; Fukuzawa, J.; Kitamoto, N.; Yoshida, I.; et al. Scavenger receptor collectin placenta 1 (CL-P1) predominantly mediates zymosan phagocytosis by human vascular endothelial cells. J. Biol. Chem. 2009, 284, 3956-3965.
32. Ohtani, K.; Suzuki, Y.; Eda, S.; Kawai, T.; Kase, T.; Keshi, H.; Sakai, Y.; Fukuoh, A.; Sakamoto, T.; Itabe, H.; et al. The membrane-type collectin CL-P1 is a scavenger receptor on vascular endothelial cells. J. Biol. Chem. 2001, 276, 44222-44228.
33. Huang, J.; Zheng, D.L.; Qin, F.S.; Cheng, N.; Chen, H.; Wan, B.B.; Wang, Y.P.; Xiao, H.S.; Han, Z.G. Genetic and epigenetic silencing of SCARA5 may contribute to human hepatocellular carcinoma by activating FAK signaling. J. Clin. Invest. 2010, 120, 223-241.
34. Yan, N.; Zhang, S.; Yang, Y.; Cheng, L.; Li, C.; Dai, L.; Zhang, X.; Fan, P.; Tian, H.; Wang, R.; et al. Therapeutic upregulation of SCARA5 inhibits tumor growth and metastasis. Cancer Sci. 2012, 103, 1631-1639.
35. Jiang, Y.; Oliver, P.; Davies, K.E.; 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.
36. Guo, L.; Chen, M.; Song, Z.; Daugherty, A.; Li, X.A. C323 of SR-BI is required for SR-BImediated HDL binding and cholesteryl ester uptake. J. Lipid Res. 2011, 52, 2272-2278.
37. Scarselli, E.; Ansuini, H.; Cerino, R.; Roccasecca, R.M.; Acali, S.; Filocamo, G.; Traboni, C.; Nicosia, A.; Cortese, R.; Vitelli, A. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 2002, 21, 5017-5025.
38. Yates, M.; Kolmakova, A.; Zhao, Y.; Rodriguez, A. Clinical impact of scavenger receptor class B type I gene polymorphisms on human female fertility. Hum. Reprod 2011, 26, 1910-1916.
39. Ishikawa, Y.; Kimura-Matsumoto, M.; Murakami, M.; Yamamoto, K.; Akasaka, Y.; Uzuki, M.; Yuri, Y.; Inomata, N.; Yokoo, T.; Ishii, T. Distribution of smooth muscle cells and macrophages expressing scavenger receptor BI/II in atherosclerosis. J. Atheroscler. Thromb. 2009, 16, 829-839.
40. Eckhardt, E.R.; Cai, L.; Sun, B.; Webb, N.R.; van der Westhuyzen, D.R. High density lipoprotein uptake by scavenger receptor SR-BII. J. Biol. Chem. 2004, 279, 14372-14381.
41. Silverstein, R.L.; Li, W.; Park, Y.M.; Rahaman, S.O. Mechanisms of cell signaling by the scavenger receptor CD36: Implications in atherosclerosis and thrombosis. Trans. Am. Clin. Climatol. Assoc. 2010, 121, 206-220.
42. Liani, R.; Halvorsen, B.; Sestili, S.; Handberg, A.; Santilli, F.; Vazzana, N.; Formoso, G.; Aukrust, P.; Davi, G. Plasma levels of soluble CD36, platelet activation, inflammation, and oxidative stress are increased in type 2 diabetic patients. Free Radic. Biol. Med. 2012, 52, 1318-1324.
43. Nishikawa, S.; Sugimoto, J.; Okada, M.; Sakairi, T.; Takagi, S. Gene expression in livers of BALB/C and C57BL/6J mice fed a high-fat diet. Toxicol. Pathol. 2012, 40, 71-82.
44. Silverstein, R.L.; Febbraio, M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci. Signal. 2009, 2, re3.
45. Park, Y.M.; Drazba, J.A.; Vasanji, A.; Egelhoff, T.; Febbraio, M.; Silverstein, R.L. Oxidized LDL/CD36 interaction induces loss of cell polarity and inhibits macrophage locomotion. Mol. Biol. Cell. 2012, 23, 3057-3068.
46. Stewart, C.R.; Stuart, L.M.; Wilkinson, K.; van Gils, J.M.; Deng, J.; Halle, A.; Rayner, K.J.; Boyer, L.; Zhong, R.; Frazier, W.A.; et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 2010, 11, 155-161.
47. Kumar, S.; Gowda, N.M.; Wu, X.; Gowda, R.N.; Gowda, D.C. CD36 modulates proinflammatory cytokine responses to Plasmodium falciparum glycosylphosphatidylinositols and merozoites by dendritic cells. Parasite Immunol. 2012, 34, 372-382.
48. Acton, S.L.; Scherer, P.E.; Lodish, H.F.; Krieger, M. Expression cloning of SR-BI, a CD36- related class B scavenger receptor. J. Biol. Chem. 1994, 269, 21003-21009.
49. Nieland, T.J.; Ehrlich, M.; Krieger, M.; Kirchhausen, T. Endocytosis is not required for the selective lipid uptake mediated by murine SR-BI. Biochim Biophys Acta 2005, 1734, 44-51.
50. Sun, B.; Boyanovsky, B.B.; Connelly, M.A.; Shridas, P.; van der Westhuyzen, D.R.; Webb, N.R. Distinct mechanisms for OxLDL uptake and cellular trafficking by class B scavenger receptors CD36 and SR-BI. J. Lipid Res. 2007, 48, 2560-2570.
51. Tancevski, I.; Frank, S.; Massoner, P.; Stanzl, U.; Schgoer, W.; Wehinger, A.; Fievet, C.; Eller, P.; Patsch, J.R.; Ritsch, A. Increased plasma levels of LDL cholesterol in rabbits after adenoviral overexpression of human scavenger receptor class B type I. J. Mol. Med. (Berl) 2005, 83, 927-932.
52. Peng, Y.; Akmentin, W.; Connelly, M.A.; Lund-Katz, S.; Phillips, M.C.; Williams, D.L. 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.
53. Yamayoshi, S.; Fujii, K.; Koike, S. Scavenger receptor b2 as a receptor for hand, foot, and mouth disease and severe neurological diseases. Front. Microbiol. 2012, 3, 32.
54. Yamayoshi, S.; Iizuka, S.; Yamashita, T.; Minagawa, H.; Mizuta, K.; Okamoto, M.; Nishimura, H.; Sanjoh, K.; Katsushima, N.; Itagaki, T.; et al. Human SCARB2-dependent infection by coxsackievirus A7, A14, and A16 and enterovirus 71. J. Virol. 2012, 86, 5686-5696.
55. Eckhardt, E.R.; Cai, L.; Shetty, S.; Zhao, Z.; Szanto, A.; Webb, N.R.; Van der Westhuyzen, D.R. High density lipoprotein endocytosis by scavenger receptor SR-BII is clathrin-dependent and requires a carboxyl-terminal dileucine motif. J. Biol. Chem. 2006, 281, 4348-4353.
56. Carrasco-Marin, E.; Fernandez-Prieto, L.; Rodriguez-Del Rio, E.; Madrazo-Toca, F.; Reinheckel, T.; Saftig, P.; Alvarez-Dominguez, C. LIMP-2 links late phagosomal trafficking with the onset of the innate immune response to Listeria monocytogenes: A role in macrophage activation. J. Biol. Chem. 2011, 286, 3332-3341.
57. Innate Immunity; Ezekowitz, R.A.B., Hoffman, J.A., Eds.; Humana press: Totowa, NJ, USA, 2003.
58. Ramet, M.; Pearson, A.; Manfruelli, P.; Li, X.; Koziel, H.; Gobel, V.; Chung, E.; Krieger, M.; Ezekowitz, R.A. Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 2001, 15, 1027-1038.
59. Li, A.C.; Guidez, F.R.; Collier, J.G.; Glass, C.K. 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.
60. 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.
61. Holness, C.L.; Simmons, D.L. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 1993, 81, 1607-1613.
62. Ramprasad, M.P.; 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.
63. Da Silva, R.P.; Gordon, S. Phagocytosis stimulates alternative glycosylation of macrosialin (mouse CD68), a macrophage-specific endosomal protein. Biochem. J. 1999, 338, 687-694.
64. Zeibig, S.; Li, Z.; Wagner, S.; Holthoff, H.P.; Ungerer, M.; Bultmann, A.; Uhland, K.; Vogelmann, J.; Simmet, T.; Gawaz, M.; et al. Effect of the oxLDL binding protein Fc-CD68 on plaque extension and vulnerability in atherosclerosis. Circ. Res. 2011, 108, 695-703.
65. De Beer, M.C.; Zhao, Z.; Webb, N.R.; van der Westhuyzen, D.R.; de Villiers, W.J. Lack of a direct role for macrosialin in oxidized LDL metabolism. J. Lipid Res. 2003, 44, 674-685.
66. Song, L.; Lee, C.; Schindler, C. Deletion of the murine scavenger receptor CD68. J. Lipid Res. 2011, 52, 1542-1550.
67. Mitra, S.; Goyal, T.; Mehta, J.L. Oxidized LDL, LOX-1 and atherosclerosis. Cardiovasc. Drugs Ther. 2011, 25, 419-429.
68. Wu, Z.; Sawamura, T.; Kurdowska, A.K.; Ji, H.L.; Idell, S.; Fu, J. LOX-1 deletion improves neutrophil responses, enhances bacterial clearance, and reduces lung injury in a murine polymicrobial sepsis model. Infect. Immun. 2011, 79, 2865-2870.
69. Mehta, J.L.; Sanada, N.; Hu, C.P.; Chen, J.; Dandapat, A.; Sugawara, F.; Satoh, H.; Inoue, K.; Kawase, Y.; Jishage, K.; et al. Deletion of LOX-1 reduces atherogenesis in LDLR knockout mice fed high cholesterol diet. Circ. Res. 2007, 100, 1634-1642.
70. Li, D.; Liu, L.; Chen, H.; Sawamura, T.; Ranganathan, S.; Mehta, J.L. LOX-1 mediates oxidized low-density lipoprotein-induced expression of matrix metalloproteinases in human coronary artery endothelial cells. Circulation 2003, 107, 612-617.
71. Inoue, K.; Arai, Y.; Kurihara, H.; Kita, T.; Sawamura, T. Overexpression of lectin-like oxidized low-density lipoprotein receptor-1 induces intramyocardial vasculopathy in apolipoprotein E-null mice. Circ. Res. 2005, 97, 176-184.
72. Ishigaki, Y.; Katagiri, H.; Gao, J.; Yamada, T.; Imai, J.; Uno, K.; Hasegawa, Y.; Kaneko, K.; Ogihara, T.; Ishihara, H.; et al. Impact of plasma oxidized low-density lipoprotein removal on atherosclerosis. Circulation 2008, 118, 75-83.
73. Kume, N.; Kita, T. Lectin-like oxidized low-density lipoprotein receptor-1 (LOX-1) in atherogenesis. Trends Cardiovasc Med. 2001, 11, 22-25.
74. Kataoka, H.; Kume, N.; Miyamoto, S.; Minami, M.; Morimoto, M.; Hayashida, K.; Hashimoto, N.; Kita, T. 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.
75. Biocca, S.; Falconi, M.; Filesi, I.; Baldini, F.; Vecchione, L.; Mango, R.; Romeo, F.; Federici, G.; Desideri, A.; Novelli, G. Functional analysis and molecular dynamics simulation of LOX-1 K167N polymorphism reveal alteration of receptor activity. PLoS ONE 2009, 4, e4648.
76. Khaidakov, M.; Wang, X.; Mehta, J.L. Potential involvement of LOX-1 in functional consequences of endothelial senescence. PLoS ONE 2011, 6, e20964.
77. Shimaoka, T.; Kume, N.; Minami, M.; Hayashida, K.; Sawamura, T.; Kita, T.; Yonehara, S. LOX-1 supports adhesion of Gram-positive and Gram-negative bacteria. J. Immunol. 2001, 166, 5108-5114.
78. Kielian, T.; Haney, A.; Mayes, P.M.; Garg, S.; Esen, N. Toll-like receptor 2 modulates the proinflammatory milieu in Staphylococcus aureus-induced brain abscess. Infect. Immun. 2005, 73, 7428-7435.
79. Jeannin, P.; Bottazzi, B.; Sironi, M.; Doni, A.; Rusnati, M.; Presta, M.; Maina, V.; Magistrelli, G.; Haeuw, J.F.; Hoeffel, G.; et al. Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors. Immunity 2005, 22, 551-560.
80. 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.
81. Ishii, J.; Adachi, H.; Aoki, J.; Koizumi, H.; Tomita, S.; Suzuki, T.; Tsujimoto, M.; Inoue, K.; Arai, H. 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.
82. Murshid, A.; Gong, J.; Calderwood, S.K. Heat shock protein 90 mediates efficient antigen cross presentation through the scavenger receptor expressed by endothelial cells-I. J. Immunol. 2010, 185, 2903-2917.
83. Sano, M.; Korekane, H.; Ohtsubo, K.; Yamaguchi, Y.; Kato, M.; Shibukawa, Y.; Tajiri, M.; Adachi, H.; Wada, Y.; Asahi, M.; et al. N-glycans of SREC-I (scavenger receptor expressed by endothelial cells): essential role for ligand binding, trafficking and stability. Glycobiology 2012, 22, 714-724.
84. Gutwein, P.; Abdel-Bakky, M.S.; Schramme, A.; Doberstein, K.; Kampfer-Kolb, N.; Amann, K.; Hauser, I.A.; Obermuller, N.; Bartel, C.; Abdel-Aziz, A.A.; et al. CXCL16 is expressed in podocytes and acts as a scavenger receptor for oxidized low-density lipoprotein. Am. J. Pathol 2009, 174, 2061-2072.
85. Gursel, M.; Gursel, I.; Mostowski, H.S.; Klinman, D.M. CXCL16 influences the nature and specificity of CpG-induced immune activation. J. Immunol. 2006, 177, 1575-1580.
86. Sheikine, Y.; Sirsjo, A. CXCL16/SR-PSOX-A friend or a foe in atherosclerosis? Atherosclerosis 2008, 197, 487-495.
87. Yamauchi, R.; Tanaka, M.; Kume, N.; Minami, M.; Kawamoto, T.; Togi, K.; Shimaoka, T.; Takahashi, S.; Yamaguchi, J.; Nishina, T.; 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.
88. Wagsater, D.; Olofsson, P.S.; Norgren, L.; Stenberg, B.; Sirsjo, A. The chemokine and scavenger receptor CXCL16/SR-PSOX is expressed in human vascular smooth muscle cells and is induced by interferon gamma. Biochem. Biophys. Res. Commun. 2004, 325, 1187-1193.
89. Wuttge, D.M.; Zhou, X.; Sheikine, Y.; Wagsater, D.; Stemme, V.; Hedin, U.; Stemme, S.; Hansson, G.K.; Sirsjo, A. CXCL16/SR-PSOX is an interferon-gamma-regulated chemokine and scavenger receptor expressed in atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 2004, 24, 750-755.
90. Zhang, L.; Liu, H.J.; Li, T.J.; Yang, Y.; Guo, X.L.; Wu, M.C.; Rui, Y.C.; Wei, L.X. Lentiviral vector-mediated siRNA knockdown of SR-PSOX inhibits foam cell formation in vitro. Acta Pharmacol. Sin. 2008, 29, 847-852.
91. Quan, Z.; Yang, H.; Yang, Y.; Yan, B.; Cao, R.; Wen, G.; Liu, C.; Xu, Y. Construction and functional analysis of a lentiviral expression vector containing a scavenger receptor (SR-PSOX) that binds uniquely phosphatidylserine and oxidized lipoprotein. Acta Biochim. Biophys. Sin. 2007, 39, 208-216.
92. Lundberg, G.A.; Kellin, A.; Samnegard, A.; Lundman, P.; Tornvall, P.; Dimmeler, S.; Zeiher, A.M.; Hamsten, A.; Hansson, G.K.; Eriksson, P. Severity of coronary artery stenosis is associated with a polymorphism in the CXCL16/SR-PSOX gene. J. Intern. Med. 2005, 257, 415-422.
93. Wu, T.; Xie, C.; Wang, H.W.; Zhou, X.J.; Schwartz, N.; Calixto, S.; Mackay, M.; Aranow, C.; Putterman, C.; Mohan, C. Elevated urinary VCAM-1, P-selectin, soluble TNF receptor-1, and CXC chemokine ligand 16 in multiple murine lupus strains and human lupus nephritis. J. Immunol. 2007, 179, 7166-7175.
94. Uza, N.; Nakase, H.; Yamamoto, S.; Yoshino, T.; Takeda, Y.; Ueno, S.; Inoue, S.; Mikami, S.; Matsuura, M.; Shimaoka, T.; et al. SR-PSOX/CXCL16 plays a critical role in the progression of colonic inflammation. Gut 2011, 60, 1494-1505.
95. Shimaoka, T.; Seino, K.; Kume, N.; Minami, M.; Nishime, C.; Suematsu, M.; Kita, T.; Taniguchi, M.; Matsushima, K.; Yonehara, S. Critical role for CXC chemokine ligand 16 (SRPSOX) in Th1 response mediated by NKT cells. J. Immunol. 2007, 179, 8172-8179.
96. Shimaoka, T.; Nakayama, T.; Fukumoto, N.; Kume, N.; Takahashi, S.; Yamaguchi, J.; Minami, M.; Hayashida, K.; Kita, T.; Ohsumi, J.; et al. Cell surface-anchored SR-PSOX/CXC chemokine ligand 16 mediates firm adhesion of CXC chemokine receptor 6-expressing cells. J. Leukoc. Biol. 2004, 75, 267-274.
97. Gratchev, A.; Sobenin, I.; Orekhov, A.; Kzhyshkowska, J. Monocytes as a diagnostic marker of cardiovascular diseases. Immunobiology 2012, 217, 476-482.
98. 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.
99. Shetty, S.; Weston, C.J.; Oo, Y.H.; Westerlund, N.; Stamataki, Z.; Youster, J.; Hubscher, S.G.; Salmi, M.; Jalkanen, S.; Lalor, P.F.; et al. Common lymphatic endothelial and vascular endothelial receptor-1 mediates the transmigration of regulatory T cells across human hepatic sinusoidal endothelium. J. Immunol. 2011, 186, 4147-4155.
100. Palani, S.; Maksimow, M.; Miiluniemi, M.; Auvinen, K.; Jalkanen, S.; Salmi, M. Stabilin- 1/CLEVER-1, a type 2 macrophage marker, is an adhesion and scavenging molecule on human placental macrophages. Eur. J. Immunol. 2011, 41, 2052-2063.
101. Adachi, H.; Tsujimoto, M. Adaptor protein sorting nexin 17 interacts with the scavenger receptor FEEL-1/stabilin-1 and modulates its expression on the cell surface. Biochim. Biophys. Acta 2010, 1803, 553-563.
102. Kzhyshkowska, J.; Workman, G.; Cardo-Vila, M.; Arap, W.; Pasqualini, R.; Gratchev, A.; Krusell, L.; Goerdt, S.; Sage, E.H. Novel function of alternatively activated macrophages: stabilin-1-mediated clearance of SPARC. J. Immunol. 2006, 176, 5825-5832.
103. Park, S.Y.; Kim, S.Y.; Kang, K.B.; Kim, I.S. Adaptor protein GULP is involved in stabilin-1- mediated phagocytosis. Biochem. Biophys. Res. Commun. 2010, 398, 467-472.
104. Kim, S.; Park, S.Y.; Kim, S.Y.; Bae, D.J.; Pyo, J.H.; Hong, M.; Kim, I.S. Cross Talk between Engulfment Receptors Stabilin-2 and Integrin alphavbeta5 Orchestrates Engulfment of Phosphatidylserine-Exposed Erythrocytes. Mol. Cell. Biol. 2012, 32, 2698-2708.
105. Moeller, J.B.; Nielsen, M.J.; Reichhardt, M.P.; Schlosser, A.; Sorensen, G.L.; Nielsen, O.; Tornoe, I.; Gronlund, J.; Nielsen, M.E.; Jorgensen, J.S.; et al. CD163-L1 is an endocytic macrophage protein strongly regulated by mediators in the inflammatory response. J. Immunol. 2012, 188, 2399-2409.
106. Nielsen, M.J.; Madsen, M.; Moller, H.J.; Moestrup, S.K. The macrophage scavenger receptor CD163: Endocytic properties of cytoplasmic tail variants. J. Leukoc. Biol. 2006, 79, 837-845.
107. Kristiansen, M.; Graversen, J.H.; Jacobsen, C.; Sonne, O.; Hoffman, H.J.; Law, S.K.; Moestrup, S.K. Identification of the haemoglobin scavenger receptor. Nature 2001, 409, 198-201.
108. Thomsen, J.H.; Etzerodt, A.; Svendsen, P.; Moestrup, S.K. The haptoglobin-CD163-heme oxygenase-1 pathway for hemoglobin scavenging. Oxid Med. Cell. Longev. 2013, 2013, doi:10.1155/2013/523652.
109. Canton, J.; Neculai, D.; Grinstein, S. Scavenger receptors in homeostasis and immunity. Nat. Rev. Immunol. 2013, 13, 621-634.
110. Alonso, R.; Buors, C.; Le Dantec, C.; Hillion, S.; Pers, J.O.; Saraux, A.; Montero, E.; Marianowski, R.; Loisel, S.; Devauchelle, V.; et al. Aberrant expression of CD6 on B-cell subsets from patients with Sjogren's syndrome. J. Autoimmun. 2010, 35, 336-341.
111. Burdo, T.H.; Lentz, M.R.; Autissier, P.; Krishnan, A.; Halpern, E.; Letendre, S.; Rosenberg, E.S.; Ellis, R.J.; Williams, K.C. Soluble CD163 made by monocyte/macrophages is a novel marker of HIV activity in early and chronic infection prior to and after anti-retroviral therapy. J. Infect. Dis. 2011, 204, 154-163.
112. Etzerodt, A.; Moestrup, S.K. CD163 and inflammation: biological, diagnostic, and therapeutic aspects. Antioxid. Redox Signal. 2013, 18, 2352-2363.
113. Fabriek, B.O.; Polfliet, M.M.; Vloet, R.P.; van der Schors, R.C.; Ligtenberg, A.J.; Weaver, L.K.; Geest, C.; Matsuno, K.; Moestrup, S.K.; Dijkstra, C.D.; et al. The macrophage CD163 surface glycoprotein is an erythroblast adhesion receptor. Blood 2007, 109, 5223-5229.
114. Ramasamy, R.; Yan, S.F.; Schmidt, A.M. RAGE: therapeutic target and biomarker of the inflammatory response--the evidence mounts. J. Leukoc. Biol. 2009, 86, 505-512.
115. Yan, S.D.; Chen, X.; Fu, J.; Chen, M.; Zhu, H.; Roher, A.; Slattery, T.; Zhao, L.; Nagashima, M.; Morser, J.; et al. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 1996, 382, 685-691.
116. Hofmann, M.A.; Drury, S.; Fu, C.; Qu, W.; Taguchi, A.; Lu, Y.; Avila, C.; Kambham, N.; Bierhaus, A.; Nawroth, P.; et al. RAGE mediates a novel proinflammatory axis: A central cell surface receptor for S100/calgranulin polypeptides. Cell 1999, 97, 889-901.
117. He, M.; Kubo, H.; Morimoto, K.; Fujino, N.; Suzuki, T.; Takahasi, T.; Yamada, M.; Yamaya, M.; Maekawa, T.; Yamamoto, Y.; et al. Receptor for advanced glycation end products binds to phosphatidylserine and assists in the clearance of apoptotic cells. EMBO Rep. 2011, 12, 358-364.
118. Hori, O.; Brett, J.; Slattery, T.; Cao, R.; Zhang, J.; Chen, J.X.; Nagashima, M.; Lundh, E.R.; Vijay, S.; Nitecki, D.; et al. The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system. J. Biol. Chem. 1995, 270, 25752-25761.
119. Li, J.; Schmidt, A.M. Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J. Biol. Chem. 1997, 272, 16498-16506.
120. Yao, D.; Brownlee, M. Hyperglycemia-induced reactive oxygen species increase expression of the receptor for advanced glycation end products (RAGE) and RAGE ligands. Diabetes 2010, 59, 249-255.
121. Xie, J.; Mendez, J.D.; Mendez-Valenzuela, V.; Aguilar-Hernandez, M.M. Cellular signalling of the receptor for advanced glycation end products (RAGE). Cell. Signal. 2013, 25, 2185-2197.
122. Yeh, C.H.; Sturgis, L.; Haidacher, J.; Zhang, X.N.; Sherwood, S.J.; Bjercke, R.J.; Juhasz, O.; Crow, M.T.; Tilton, R.G.; Denner, L. Requirement for p38 and p44/p42 mitogen-activated protein kinases in RAGE-mediated nuclear factor-kappaB transcriptional activation and cytokine secretion. Diabetes 2001, 50, 1495-1504.
123. Harja, E.; Bu, D.X.; Hudson, B.I.; Chang, J.S.; Shen, X.; Hallam, K.; Kalea, A.Z.; Lu, Y.; Rosario, R.H.; Oruganti, S.; et al. Vascular and inflammatory stresses mediate atherosclerosis via RAGE and its ligands in apoE-/- mice. J. Clin. Invest. 2008, 118, 183-194.
124. Sun, Y.; Chen, X. Ox-LDL-induced LOX-1 expression in vascular smooth muscle cells: role of reactive oxygen species. Fundam. Clin. Pharmacol. 2011, 25, 572-579.
125. Cominacini, L.; Fratta Pasini, A.; Garbin, U.; Pastorino, A.; Rigoni, A.; Nava, C.; Davoli, A.; Lo Cascio, V.; Sawamura, T. 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.
126. Hu, C.; Dandapat, A.; Chen, J.; Fujita, Y.; Inoue, N.; Kawase, Y.; Jishage, K.; Suzuki, H.; Sawamura, T.; Mehta, J.L. LOX-1 deletion alters signals of myocardial remodeling immediately after ischemia-reperfusion. Cardiovasc. Res. 2007, 76, 292-302.
127. 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.
128. Aguilar-Gaytan, R.; Mas-Oliva, J. Oxidative stress impairs endocytosis of the scavenger receptor class A. Biochem. Biophys. Res. Commun. 2003, 305, 510-517.
129. Li, W.; Febbraio, M.; Reddy, S.P.; Yu, D.Y.; Yamamoto, M.; Silverstein, R.L. CD36 participates in a signaling pathway that regulates ROS formation in murine VSMCs. J. Clin. Invest. 2010, 120, 3996-4006.
130. Cho, S.; Park, E.M.; Febbraio, M.; Anrather, J.; Park, L.; Racchumi, G.; Silverstein, R.L.; Iadecola, C. The class B scavenger receptor CD36 mediates free radical production and tissue injury in cerebral ischemia. J. Neurosci. 2005, 25, 2504-2512.
131. Boullier, A.; Bird, D.A.; Chang, M.K.; Dennis, E.A.; Friedman, P.; Gillotre-Taylor, K.; Horkko, S.; Palinski, W.; Quehenberger, O.; Shaw, P.; et al. Scavenger receptors, oxidized LDL, and atherosclerosis. Ann. N. Y. Acad. Sci. 2001, 947, 214-223.
132. Lehtolainen, P.; Takeya, M.; Yla-Herttuala, S. Retrovirus-mediated, stable scavenger-receptor gene transfer leads to functional endocytotic receptor expression, foam cell formation, and increased susceptibility to apoptosis in rabbit aortic smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 2000, 20, 52-60.
133. Hamilton, R.F., Jr.; Thakur, S.A.; Mayfair, J.K.; Holian, A. MARCO mediates silica uptake and toxicity in alveolar macrophages from C57BL/6 mice. J. Biol. Chem. 2006, 281, 34218-34226.
134. Zhu, Z.H.; Yu, Y.P.; Shi, Y.K.; Nelson, J.B.; Luo, J.H. CSR1 induces cell death through inactivation of CPSF3. Oncogene 2009, 28, 41-51.
135. Nishiuchi, T.; Murao, K.; Imachi, H.; Yu, X.; Dobashi, H.; Haba, R.; Ishida, T. Scavenger receptor class BI mediates the anti-apoptotic effect of erythropoietin. Ann. Med. 2010, 42, 151-160.
136. Li, K.; Yang, M.; Yuen, P.M.; Chik, K.W.; Li, C.K.; Shing, M.M.; Lam, H.K.; Fok, T.F. Thrombospondin-1 induces apoptosis in primary leukemia and cell lines mediated by CD36 and Caspase-3. Int. J. Mol. Med. 2003, 12, 995-1001.
137. Lu, J.; Yang, J.H.; Burns, A.R.; Chen, H.H.; Tang, D.; Walterscheid, J.P.; Suzuki, S.; Yang, C.Y.; Sawamura, T.; Chen, C.H. Mediation of electronegative low-density lipoprotein signaling by LOX-1: a possible mechanism of endothelial apoptosis. Circ. Res. 2009, 104, 619-627.
138. Chen, J.; Mehta, J.L.; Haider, N.; Zhang, X.; Narula, J.; Li, D. Role of caspases in Ox-LDLinduced apoptotic cascade in human coronary artery endothelial cells. Circ. Res. 2004, 94, 370-376.
139. Murphy, J.E.; Tacon, D.; Tedbury, P.R.; Hadden, J.M.; Knowling, S.; Sawamura, T.; Peckham, M.; Phillips, S.E.; Walker, J.H.; Ponnambalam, S. LOX-1 scavenger receptor mediates calciumdependent recognition of phosphatidylserine and apoptotic cells. Biochem. J. 2006, 393, 107-115.
140. Oka, K.; Sawamura, T.; Kikuta, K.; Itokawa, S.; Kume, N.; Kita, T.; Masaki, T. 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.
141. Park, S.Y.; Jung, M.Y.; Kim, H.J.; Lee, S.J.; Kim, S.Y.; Lee, B.H.; Kwon, T.H.; Park, R.W.; Kim, I.S. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell. Death Differ. 2008, 15, 192-201.
142. Park, S.Y.; Jung, M.Y.; Lee, S.J.; Kang, K.B.; Gratchev, A.; Riabov, V.; Kzhyshkowska, J.; Kim, I.S. Stabilin-1 mediates phosphatidylserine-dependent clearance of cell corpses in alternatively activated macrophages. J. Cell. Sci. 2009, 122, 3365-3373.
143. Bak, S.P.; Walters, J.J.; Takeya, M.; Conejo-Garcia, J.R.; Berwin, B.L. Scavenger receptor-Atargeted leukocyte depletion inhibits peritoneal ovarian tumor progression. Cancer Res. 2007, 67, 4783-4789.
144. Neyen, C.; Pluddemann, A.; Mukhopadhyay, S.; Maniati, E.; Bossard, M.; Gordon, S.; Hagemann, T. Macrophage scavenger receptor a promotes tumor progression in murine models of ovarian and pancreatic cancer. J. Immunol. 2013, 190, 3798-3805.
145. Bock, A.J.; Nymoen, D.A.; Brenne, K.; Kaern, J.; Davidson, B. SCARA3 mRNA is overexpressed in ovarian carcinoma compared with breast carcinoma effusions. Hum. Pathol. 2012, 43, 669-674.
146. Yu, G.; Tseng, G.C.; Yu, Y.P.; Gavel, T.; Nelson, J.; Wells, A.; Michalopoulos, G.; Kokkinakis, D.; Luo, J.H. CSR1 suppresses tumor growth and metastasis of prostate cancer. Am. J. Pathol 2006, 168, 597-607.
147. Shabo, I.; Stal, O.; Olsson, H.; Dore, S.; Svanvik, J. Breast cancer expression of CD163, a macrophage scavenger receptor, is related to early distant recurrence and reduced patient survival. Int. J. Cancer 2008, 123, 780-786.
148. Shabo, I.; Olsson, H.; Sun, X.F.; Svanvik, J. Expression of the macrophage antigen CD163 in rectal cancer cells is associated with early local recurrence and reduced survival time. Int. J. Cancer 2009, 125, 1826-1831.
149. Llaverias, G.; Danilo, C.; Wang, Y.; Witkiewicz, A.K.; Daumer, K.; Lisanti, M.P.; Frank, P.G. A Western-type diet accelerates tumor progression in an autochthonous mouse model of prostate cancer. Am. J. Pathol. 2010, 177, 3180-3191.
150. Hale, J.S.; Li, M.; Sinyuk, M.; Jahnen-Dechent, W.; Lathia, J.D.; Silverstein, R.L. Context dependent role of the CD36--thrombospondin--histidine-rich glycoprotein axis in tumor angiogenesis and growth. PLoS ONE 2012, 7, e40033.
151. Jiang, J.; Yan, M.; Mehta, J.L.; Hu, C. Angiogenesis is a link between atherosclerosis and tumorigenesis: role of LOX-1. Cardiovasc Drugs Ther. 2011, 25, 461-468.
152. Khaidakov, M.; Mehta, J.L. Oxidized LDL triggers pro-oncogenic signaling in human breast mammary epithelial cells partly via stimulation of MiR-21. PLoS ONE 2012, 7, e46973.
153. Liang, M.; Zhang, P.; Fu, J. Up-regulation of LOX-1 expression by TNF-alpha promotes transendothelial migration of MDA-MB-231 breast cancer cells. Cancer Lett. 2007, 258, 31-37.
154. Irjala, H.; Alanen, K.; Grenman, R.; Heikkila, P.; Joensuu, H.; Jalkanen, S. 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.
155. Facciponte, J.G.; Wang, X.Y.; Subjeck, J.R. Hsp110 and Grp170, members of the Hsp70 superfamily, bind to scavenger receptor-A and scavenger receptor expressed by endothelial cells-I. Eur. J. Immunol. 2007, 37, 2268-2279.