Scavenger receptors bind free extracellular ligands as the initial step in clearance of the ligands from the body (reviewed in Ascenzi et al. 2005, Areschoug and Gordon 2009, Nielsen et al. 2010). Some scavenger receptors, such as the CD163-haptoglobin system, are specific for only one ligand. Others, such as the SCARA receptors (SR-A receptors) are less specific, binding several ligands which share a common property, such as polyanionic charges. Brown and Goldstein originated the idea of receptors dedicated to scavenging aberrant molecules such as modified low density lipoprotein particles (Goldstein et al. 1979) and such receptors have been shown to participate in pathological processes such as atherosclerosis. Based on homology, scavenger receptors have been categorized into classes A-H (reviewed in Murphy et al. 2005).
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Apostolov EO, Shah SV, Ray D, Basnakian AG.; ''Scavenger receptors of endothelial cells mediate the uptake and cellular proatherogenic effects of carbamylated LDL.''; PubMedEurope PMCScholia
Facciponte JG, Wang XY, Subjeck JR.; ''Hsp110 and Grp170, members of the Hsp70 superfamily, bind to scavenger receptor-A and scavenger receptor expressed by endothelial cells-I.''; PubMedEurope PMCScholia
Sakai M, Miyazaki A, Hakamata H, Kobori S, Shichiri M, Horiuchi S.; ''Endocytic uptake of lysophosphatidylcholine mediated by macrophage scavenger receptor plays a major role in oxidized low density lipoprotein-induced macrophage growth.''; PubMedEurope PMCScholia
Adams PA, Berman MC.; ''Kinetics and mechanism of the interaction between human serum albumin and monomeric haemin.''; PubMedEurope PMCScholia
Smith A, Farooqui SM, Morgan WT.; ''The murine haemopexin receptor. Evidence that the haemopexin-binding site resides on a 20 kDa subunit and that receptor recycling is regulated by protein kinase C.''; PubMedEurope PMCScholia
Morgan WT, Liem HH, Sutor RP, Muller-Ebergard U.; ''Transfer of heme from heme-albumin to hemopexin.''; PubMedEurope PMCScholia
Santiago-García J, Kodama T, Pitas RE.; ''The class A scavenger receptor binds to proteoglycans and mediates adhesion of macrophages to the extracellular matrix.''; PubMedEurope PMCScholia
Widener J, Nielsen MJ, Shiflett A, Moestrup SK, Hajduk S.; ''Hemoglobin is a co-factor of human trypanosome lytic factor.''; PubMedEurope PMCScholia
Resnick D, Chatterton JE, Schwartz K, Slayter H, Krieger M.; ''Structures of class A macrophage scavenger receptors. Electron microscopic study of flexible, multidomain, fibrous proteins and determination of the disulfide bond pattern of the scavenger receptor cysteine-rich domain.''; PubMedEurope PMCScholia
Dunne DW, Resnick D, Greenberg J, Krieger M, Joiner KA.; ''The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid.''; PubMedEurope PMCScholia
Shiflett AM, Bishop JR, Pahwa A, Hajduk SL.; ''Human high density lipoproteins are platforms for the assembly of multi-component innate immune complexes.''; PubMedEurope PMCScholia
Keshi H, Sakamoto T, Kawai T, Ohtani K, Katoh T, Jang SJ, Motomura W, Yoshizaki T, Fukuda M, Koyama S, Fukuzawa J, Fukuoh A, Yoshida I, Suzuki Y, Wakamiya N.; ''Identification and characterization of a novel human collectin CL-K1.''; PubMedEurope PMCScholia
Berwin B, Hart JP, Rice S, Gass C, Pizzo SV, Post SR, Nicchitta CV.; ''Scavenger receptor-A mediates gp96/GRP94 and calreticulin internalization by antigen-presenting cells.''; PubMedEurope PMCScholia
Dahl M, Bauer AK, Arredouani M, Soininen R, Tryggvason K, Kleeberger SR, Kobzik L.; ''Protection against inhaled oxidants through scavenging of oxidized lipids by macrophage receptors MARCO and SR-AI/II.''; PubMedEurope PMCScholia
Janabi M, Yamashita S, Hirano K, Sakai N, Hiraoka H, Matsumoto K, Zhang Z, Nozaki S, Matsuzawa Y.; ''Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients.''; PubMedEurope PMCScholia
Podrez EA, Poliakov E, Shen Z, Zhang R, Deng Y, Sun M, Finton PJ, Shan L, Gugiu B, Fox PL, Hoff HF, Salomon RG, Hazen SL.; ''Identification of a novel family of oxidized phospholipids that serve as ligands for the macrophage scavenger receptor CD36.''; PubMedEurope PMCScholia
Park SY, Jung MY, Lee SJ, Kang KB, Gratchev A, Riabov V, Kzhyshkowska J, Kim IS.; ''Stabilin-1 mediates phosphatidylserine-dependent clearance of cell corpses in alternatively activated macrophages.''; PubMedEurope PMCScholia
Yokota T, Ehlin-Henriksson B, Hansson GK.; ''Scavenger receptors mediate adhesion of activated B lymphocytes.''; PubMedEurope PMCScholia
Tao N, Wagner SJ, Lublin DM.; ''CD36 is palmitoylated on both N- and C-terminal cytoplasmic tails.''; PubMedEurope PMCScholia
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.''; PubMedEurope PMCScholia
Nielsen MJ, Petersen SV, Jacobsen C, Thirup S, Enghild JJ, Graversen JH, Graversen JH, Moestrup SK.; ''A unique loop extension in the serine protease domain of haptoglobin is essential for CD163 recognition of the haptoglobin-hemoglobin complex.''; PubMedEurope PMCScholia
Hansen B, Longati P, Elvevold K, Nedredal GI, Schledzewski K, Olsen R, Falkowski M, Kzhyshkowska J, Carlsson F, Johansson S, Smedsrød B, Goerdt S, Johansson S, McCourt P.; ''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.''; PubMedEurope PMCScholia
Vishnyakova TG, Bocharov AV, Baranova IN, Chen Z, Remaley AT, Csako G, Eggerman TL, Patterson AP.; ''Binding and internalization of lipopolysaccharide by Cla-1, a human orthologue of rodent scavenger receptor B1.''; PubMedEurope PMCScholia
Smith A, Morgan WT.; ''Haem transport to the liver by haemopexin. Receptor-mediated uptake with recycling of the protein.''; PubMedEurope PMCScholia
Gowen BB, Borg TK, Ghaffar A, Mayer EP.; ''Selective adhesion of macrophages to denatured forms of type I collagen is mediated by scavenger receptors.''; PubMedEurope PMCScholia
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.''; PubMedEurope PMCScholia
Endemann G, Stanton LW, Madden KS, Bryant CM, White RT, Protter AA.; ''CD36 is a receptor for oxidized low density lipoprotein.''; PubMedEurope PMCScholia
Truncated Alpha-1-Microglobulin binds heme b and then degrades heme b by an unknown mechanism (Allhorn et al. 2002). The crystal structure of the untruncated Alpha1-Microglobulin:heme complex indicates that each Alpha1-Microglobulin molecule binds 2 heme molecules and the Alpha1-Microglobulin molecules trimerize (Siebel et al. 2012).
The CD163 receptor binds the haptoglobin:hemoglobin complex (Kristiansen et al. 2001, Madsen et al. 2004, Nielsen et al. 2007). After binding, the CD163:haptoglobin:hemoglobin complex is internalized by endocytosis and is degraded in the lysosome. CD163 is found on the membranes of monocytes and macrophages.
When haptoglobin capacity to buffer hemoglobin is overwhelmed, hemoglobin undergoes a rapid conversion to methemoglobin. Ferriheme is transferred directly from methemoglobin to hemopexin (Miller et al. 1996, Mauk and Mauk 2010).
Haptoglobin is an acute phase protein. It is produced by the liver and secreted into the plasma where it binds alpha-beta dimers of hemoglobin (Hamaguchi et al. 1971, Nagel and Gibson 1971, Tsapis et al. 1978, reviewed in Chiabrando et al. 2011). Haptoglobin monomers contain alpha and beta chains cleaved from a single proprotein and bonded by cystine disulfide bonds. The monomers further associate into dimers by disulfide-bonding and beta strand swapping (Andersen et al. 2012). Each haptoglobin dimer can bind two hemoglobin dimers, each containing hemoglobin alpha and hemoglobin beta.
Hemopexin binds either ferriheme b or ferroheme b, however the stability of the complex containing ferriheme b is greater than the stability of the complex containing ferroheme b (Morgan 1976, Pasternack et al. 1983, Solar et al. 1989, Miller and Shaklai 1999, Rosell et al. 2005, Mauk and Mauk 2010).
Despite the lower affinity of ferriheme for albumin than for hemopexin, ferriheme initially associates with albumin, presumably because the molar concentration of albumin in plasma is considerably greater than that of hemopexin. Ferriheme is transferred directly from serum albumin to hemopexin (Morgan et al. 1976, Pasternack et al. 1983, Pasternack et al. 1985).
Alpha-1-Microglobulin binds heme b (Allhorn et al. 2002, Larsson et al. 2004). The crystal structure of the complex indicates that each microglobulin molecule binds 2 heme molecules and the microglobulin:heme complex trimerizes (Siebel et al. 2012).
Haptoglobin-related protein (HRP) is present in human serum in a complex known as trypanosome lytic factor-1 (TLF-1) that contains APOL1, APOA1, and HDL3. The HPR subunit of the complex binds hemoglobin with an unknown stoichiometry (Shiflett et al. 2005, Nielsen et al. 2006, Widener et al. 2007, Harrington et al. 2009).
Once formed in the plasma, the hemopexin:heme complex is rapidly cleared from circulation and it is taken up by the liver (Smith and Morgan 1984, Smith and Morgan 1985, Tolosano et al. 2010, Vinchi et al. 2008), where heme is degraded by heme oxygenases. In mouse, rat and rabbit several experimental evidences led to the postulation of a specific receptor on hepatocytes with high affinity for the hemopexin:heme complex (Smith and Morgan 1981, Smith and Morgan 1984, Smith et al, 1988, Smith et al., 1991), but such a receptor has not been identified to date. The only known hemopexin:heme receptor is LRP1 (CD91) that is ubiquitously expressed and has a low affinity for the complex. LRP1 is a multi-ligand scavenger receptor, involved in endocytosis in some cells types, for example macrophages, and in signaling in other cell types (reviewed in Boucher and Herz 2011). LRP1 is known to act in the metabolism of lipoprotein and it is expressed in several cell types including macrophages, hepatocytes and neurons. Among several ligands, LRP1 (CD91) can bind the hemopexin:heme complex (Hvidberg et al. 2005).
MSR1 (SCARA1, SR-A) binds oxidized and acetylated low density lipid (LDL) particles ((Brown et al. 1980), Haberland et al 1984, Gough et al. 1998, Yang et al. 2011), apolipoproteins A-I and E (human and mouse, Neyen et al. 2009), lysophosphatidylcholine from apoptotic cells (mouse, Sakai et al. 1996), phosphatidylinositol and phosphatidylserine (mouse, Nishikawa et al. 1990). MSR1 binds activated B-lymphocytes (human, Yokota et al. 1998), calreticulin and gp96 (mouse, Berwin et al. 2003). MSR1 binds bacterial products (E.coli, Neisseria meningitides, Staphylococcus aureus) (mouse, Peiser et al. 2006), Lipopolysaccharide (LPS) (mouse and bovine, Hampton et al. 1991), Lipoteichoic acid (LTA) and Gram-positive bacteria (bovine, Dunne et al. 1994), Adenovirus 5 (Haisma et al. 2009). MSR1 binds polysaccharides (carrageenan, dextran sulphate, fucoidan) (Brown et al. 1980, Krieger et al. 1992), extracellular matrix proteoglycans, biglycan and decorin (mouse, Santiago-Garcia et al. 2003). MSR1 binds extracellular matrix molecules, including denatured type I and III collagen, as well as glycated collagen IV (human and mouse and bovine, el Khoury et al. 1994, Gowen et al. 2000, Gowen et al. 2001), beta-amyloid fibrils (human and mouse, El Khoury et al. 1996), maleyl-BSA and advanced glycation end-product modified (AGE)-BSA (bovine, Brown et al. 1980, Araki et al. 1995). MSR1 binds polynucleotides (polyI, polyG) (bovine, Brown et al. 1980, Pearson et al. 1993, Mielewczyk et al. 1996), double-stranded RNA (Limmon et al. 2008, DeWitte-Orr et al. 2010). MSR1 interacts with the modified apoB-100 component of LDL (Parthasarathy et al. 1987) and with the lipid part of LDL (Terpstra et al. 1998). MSR1 is expressed most strongly on macrophages and can also be detected on endothelial cells and smooth muscle cells.
Unlike MSR1, MARCO uses the SRCR domain and more particularly the arginine-rich region within this domain for binding. (Brannstrom et al. 2002). MARCO binds lipopolysaccharide and lipoteichoic acid, both found on the surfaces of bacteria (Elomaa et al. 1998, Elshourbagy et al. 2000). MARCO binds and phagocytoses Streptococcus pneumoniae (mouse, Dorrington et al. 2013), Escherichia coli and Staphylococcus aureus (Elshourbagy, Li et al. 2000), Neisseria meningitidis (Mukhopadhyay et al. 2006), Clostridium sordellii (Thelen et al. 2010). MARCO binds proinflammatory oxidized lipids (mouse, Dahl et al. 2007). MARCO binds CpG oligonucleotide sequences (CpG-ODN) in microbial DNA (mouse, Jozefowski et al. 2006), uteroglobin-related protein 1 (Bin et al. 2003), unopsonized particles (TiO2, Fe2O3, and latex beads) (Palecanda et al. 1999) and silica particles (Hamilton et al. 2006). MARCO is most strongly expressed on subgroups of macrophages and can also be detected on splenic dendritic cells.
COLEC12 (SCARA4) binds beta-glucan (Jang et al. 2009), N-acetylgalactosamine (Yoshida et al. 2003), oxidized LDL (Ohtani et al. 2001), and double-stranded RNA (DeWitte-Orr et al. 2010). COLEC12 is expressed on endothelial cells
CD36 (Platelet glycoprotein IV) binds oxidized LDL (Janabi et al. 2000, Endemann et al. 1993) through both the lipid and the protein moieties of LDL (Boullier et al. 2000), oxidized phospholipids (Podrez et al. 2002), long-chain fatty acids (inferred from rat and mouse, Abumrad et al. 1993, Laugerette et al. 2005), hexarelin (a hexapeptide member of the growth hormone-releasing peptide family) (inferred from rat and mouse, Bodart et al. 2002), betaglucan (Means et al. 2009), oxidized and native phosphatidylserine (Greenberg et al. 2006) and apoptotic cells (Ren et al. 1995; Fadok et al. 1998), lipopeptide from Staphylococcus aureus as well as lipoteichoic acid from Gram-positive bacteria, both in cooperation with TLR2 (inferred from mouse, Hoebe et al. 2005). As inferred from mouse, CD36 also binds phosphatidylinositol, and HDL.
SCARA5 binds double-stranded RNA (DeWitte-Orr et al. 2010). As inferred from mouse SCARA5 also binds lipopolysaccharide and ferritin. SCARA5 is expressed on epithelial cells.
SCARF1 (SREC-I) binds low density lipoprotein (LDL), oxidized LDL, acetylated LDL (Adachi et al. 1997), carbamylated LDL (Apostolov et al. 2009), beta glucan (Means et al. 2009), and calreticulin (Berwin et al. 2004). SREC-I binds Hsp90 and Hsp90-chaperoned peptides (Murshid et al. 2010) as well as Heat shock protein 110 (hsp110) and glucose-regulated protein (grp170) (inferred from mouse, Facciponte, Wang et al. 2007). SREC-I interacts with PorB of Neisseria gonorrhoeae and mediates host cell entry (Rechner et al. 2007).
SCARB1 (SR-BI) binds low density lipoprotein (LDL), acetylated LDL, oxidized LDL, high density lipoprotein (HDL) (Calvo et al. 1997, Murao et al. 1997, Rhainds et al. 1999, inferred from hamster in Acton et al. 1994). SCARB1 binds HDL via its protein moiety, including apolipoproteins A-I, A-II, CII, CIII and E (Bultel-Brienne et al. 2002, inferred from mouse in Xu, Laccotripe et al. 1997, Li et al. 2002). SCARB1 also binds serum amyloid A protein (Baranova et al. 2005), and lipopolysaccharide (LPS) (Vishnyakova et al. 2003). SCARB1 is expressed on the extracellular face of the plasma membrane of several types of polarized epithelial cells.
STAB1 (FEEL-1) binds acetylated low density lipoprotein (LDL) (Adachi & Tsujimoto 2002, Palani et al. 2011), phosphatidylserine (exposed when cells are lysed) (Park et al. 2009), advanced glycation end products (AGE) (Tamura et al. 2003, Hansen et al. 2005), and Osteonectin (SPARC) (Kzhyshkowska et al. 2006).
Both hemoglobin and the cytosolic face of erythrocytes are able to catalyze the cleavage of Alpha-1-Microglobulin in the IgA:Alpha-1-Microglobulin complex present in serum (Allhorn et al. 2002). The reaction produces truncated Alpha-1-Microglobulin, which is able to bind and degrade heme. About half of the circulating Alpha-1-Microglobulin is covalently bound to IgA.
The CD163:haptoglobin:hemoglobin complex is endocytosed (Schaer et al. 2006, Kristiansen et al. 2001) by monocytes or macrophages. CD163 is constitutively endocytosed by monocytes independently of ligand binding (Schaer et al. 2006). Upon endocytosis, the receptor–ligand complex enters early endosomes where haptoglobin:hemoglobin complexes are released from CD163. The receptor then recycles to the cell surface while haptoglobin:hemoglobin complexes continue through the endocytic pathway to end up in lysosomes where the protein moieties and the ligand are degraded.
The LRP1:hemopexin:heme complex is endocytosed and the complex is dissociated in lysosomes, leading to heme uptake. Heme is then degraded by heme oxygenases. Whereas LRP1 is subsequently recycled to the plasma membrane, the destiny of hemopexin is controversial. Some studies have suggested that hemopexin can be recycled as an intact molecule to the extracellular milieu (Smith and Morgan, 1979). However, it has also been proposed that following hepatic uptake of heme from hemopexin:heme, varying proportions of the protein are either returned to the circulation or degraded in the liver (Potter et al., 1993). Recently, Hvidberg et al. have shown that most hemopexin is degraded in lysosomes (Hvidberg et al., 2005).
The MARCO:ligand complex is endocytosed (Arredouani et al. 2005, Thelen et al. 2010). In cases where the ligand is part of a bacterial cell the entire cell is phagocytosed.
The STAB2:ligand complex is endocytosed (Tamura et al. 2003, Li et al. 2011). Endocytosis of stabilin-1 or stabilin-2 can occur independently of ligand binding, via clathrin (Hansen et al. 2005).
The Platelet glycoprotein IV (CD36):ligand complex is endocytosed (Zeng et al. 2003, McDermott_Roe et al. 2008, Nilsen et al. 2008, Collins et al. 2009). The endocytosis of CD36:oxidized LDL is independent of caveolin (Zeng et al. 2003) and dependent on actin (Collins et al. 2009). As inferred from mouse, endocytosis of CD36:oxidized LDL is independent of caveolae, microtubules, and actin cytoskeleton, but dependent on dynamin (Sun et al. 2007).
The STAB1:ligand complex is endocytosed (Tamura et al. 2003, Kzhyshkowska et al. 2004, Li et al. 2011, Prevo et al. 2004; Kzhyshkowska et al. 2005). Endocytosis of stabilin-1 or stabilin-2 can occur independently of ligand binding, via clathrin (Hansen et al. 2005).
The SCARF1:ligand complex is endocytosed (Adachi et al. 1997, Berwin et al. 2004) and cross-presented on MHC class II (Murshid et al. 2010). SREC-I mediates host cell entry of Neisseria gonorrhoeae (Rechner et al. 2007)
The MSR1:ligand complex (SCARA1:ligand, SR-A:ligand) is endocytosed (Matsumoto et al. 1990, Gough et al. 1998, Peiser et al. 2000, Aguilar-Gaytan and Mas-Oliva 2003, Wang and Chandawarkar 2010, Orr et al. 2011). In the cases in which the ligands are located on bacteria or yeast cells the entire cell is phagocytosed (Aguilar-Gaytan and Mas-Oliva 2003, Wang and Chandawarkar 2010). Uptake of modified LDL by macrophages via MSR1 appears to contribute to foam cell formation during atherosclerosis (Matsumoto et al. 1990).
The SCARB1 (SR-BI, SR-BII):ligand complex is endocytosed (Calvo et al. 1997, Murao et al. 1997, Rhainds et al. 1999, Vishnyakova et al. 2003, Baranova et al. 2005, Eckhardt et al. 2004) but selective lipid uptake from lipoprotein particles does not require SR-BI endocytosis in mouse (Nieland et al. 2005) but is partly dependent on endocytosis in human (Zhang et al. 2007). HDL particles are resecreted after lipid unloading in the endocytic pathway (Pagler et al. 2006; Zhang et al. 2007). SR-BI colocalizes with caveolae (inferred from mouse, Babitt et al. 1997) while SR-BII, an alternatively spliced form of SCARB1, localizes to clathrin-coated pits due to a dileucine motif in the cytosolic tail (inferred from mouse, Eckhardt et al. 2006). Endocytosis of oxidized LDL by SR-BI is independent of caveolae, microtubules, and actin cytoskeleton (inferred from mouse, Sun et al. 2007).
COLEC12 (CL-P1, SCARA4, SRCL, NSR2) bound to yeast or bacteria is phagocytosed (Jang et al. 2009, Ohtani et al. 2012). Endocytosis of other ligands bound to COLEC12 is inferred.
SSC5D is a secreted member of group B of the SRCR superfamily. Human SSC5D binds surfaces of whole bacteria and is able to discriminate pathogenic strains from non-pathogenic strains (Bessa Pereira et al. 2016). Mouse Ssc5d (S5D-SRCRB) binds bacterial surface polymers (peptidoglycan, lipopolysaccharide), yeast surface polymers (beta-glucan), and glycoproteins (Galectin-1, Galectin-3, Laminin). Human SSC5D may bind similar ligands but this has not yet been demonstrated. Mouse Ssc5d is expressed in the urogenital tract (Miró-Julià et al. 2014).
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glycoprotein
IV:Ligandglycoprotein
IV:LigandAnnotated Interactions
glycoprotein
IV:Ligandglycoprotein
IV:Ligandglycoprotein
IV:Ligand