CD163: a regulated hemoglobin scavenger receptor with a role in the anti‐inflammatory response

References

• Bunn HF, Rosse W. Hemolytic anemias and acute blood loss. In: Braunwald E, Fauci AS, Kasper DL, Hauser SL, Longo JL, Jameson JL, editors. Harrison's Principles of Internal Medi-cine, 15th Edn. New York: McGraw-Hill; 2003:681–91.
   Google Scholar
• Kristiansen M, Graversen JH, Jacobsen C, Sonne 0, Hoffman HJ, Law SK, et al. Identification of the haemoglobin scavenger receptor. Nature 2001;409:198–201.
   Google Scholar
• Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 2003;24:449–55.
   PubMed Web of Science ®Google Scholar
• Bowman BH, Barnett DR, Lum JB, Yang FM. Haptoglobin. Methods Enzymol 1988;163:452–74.
   Google Scholar
• Wejman JC, Hovsepian D, Wall JS, Hainfeld JF, Greer J. Structure and Assembly of Haptoglobin Polymers by Electron-Microscopy. J Mol Biol 1984;174:343–68.
   Google Scholar
• Wejman JC, Hovsepian D, Wall JS, Hainfeld JF, Greer J. Structure of Haptoglobin and the Haptoglobin Hemoglobin Complex by Electron-Microscopy. J Mol Biol 1984;174:319–41.
   Google Scholar
• Law SKA, Micklem KJ, Shaw JM, Zhang XP, Dong Y, Willis AC, et al. A New Macrophage Differentiation Antigen Which Is A Member of the Scavenger Receptor Superfamily. Eur J Immunol 1993;23:2320–5.
   PubMed Web of Science ®Google Scholar
• Pulford K, Micklem K, McCarthy S, Cordell J, Jones M, Mason DY. A Monocyte Macrophage Antigen Recognized by the 4 Antibodies Ghi/61, Ber-Mac3, Ki-M8 and 5m4. Immunology 1992;75:588–95.
   Google Scholar
• Mosser DM. The many faces of macrophage activation. J Leukoc Biol 2003;73:209–12.
   PubMed Web of Science ®Google Scholar
• Gronlund J, Vitved L, Lausen M, Skjodt K, Holmskov U. Cloning of a novel scavenger receptor cysteine-rich type I transmembrane molecule (M160) expressed by human macro-phages. J Immunol 2000;165: 6406–15.
   Google Scholar
• Bowen MA, Aruffo AA, Bajorath J. Cell surface receptors and their ligands: In vitro analysis of CD6-CD166 interactions. Proteins 2000;40: 420–8.
   Google Scholar
• Horn IR, Nielsen MJ, Madsen M, Jacobsen C, Graversen JH, Moestrup SK. Generation of a haptoglobin-hemoglobin complex-specific Fab antibody blocking the binding of the complex to CD163. Eur J Haematol 2003;71:289–93.
   Google Scholar
• Fass D, Blacklow S, Kim PS, Berger JM. Molecular basis of familial hypercholesterolaemia from structure of LDL recep-tor module. Nature 1997;388:691–3.
   PubMed Web of Science ®Google Scholar
• Pratt DS, Kaplan MM. Jaundice. In: Braunwald E, Fauci AS, Kasper DL, Hauser SL, Longo JL, Jameson JL, editors. Harrison's Principles of Internal Medicine. 15th edn. New York: McGraw-Hill; 2001:255–9.
   Google Scholar
• Levy AP, Jablonski K, Resnick HE, Lee ET, Best LT, Howard BV. Haptoglobin phenotype and the risk of cardiovascular disease in individuals with diabetes: The Strong Heart Study. Circulation 2001;104:3.
   Google Scholar
• Langlois MR, Delanghe JR. Biological and clinical signifi- cance of haptoglobin polymorphism in humans. Clin Chem 1996;42:1589–600.
   PubMed Web of Science ®Google Scholar
• Delanghe JR, Langlois MR. Haptoglobin polymorphism and body iron stores. Clin Chem Lab Med 2002;40:212–6.
   PubMedGoogle Scholar
• Asleh R, Marsh S, Shilkrut M, Binah 0, Guetta J, Lejbkowicz F, et al. Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ Res 2003;92:1193–200.
   Google Scholar
• Ritter M, Buechler C, Kapinsky M, Schmitz G. Interaction of CD163 with the regulatory subunit of casein kinase II (CKII) and dependence of CD163 signaling on CKII and protein kinase C. Eur J Immunol 2001;31:999–1009.
   PubMed Web of Science ®Google Scholar
• Buechler C, Ritter M, Orso E, Langmann T, Klucken J, Schmitz G. Regulation of scavenger receptor CD163 expres-sion in human monocytes and macrophages by pro- and antiinflammatory stimuli. J Leukoc Biol 2000;67:97–103.
   PubMed Web of Science ®Google Scholar
• Van den Heuvel MM, Tensen CP, van As JH, Van den Berg TK, Fluitsma DM, Dijkstra CD, et al. Regulation of CD163 on human macrophages: cross-linking of CD163 induces signaling and activation. J Leukoc Biol 1999;66:858–66.
   PubMed Web of Science ®Google Scholar
• Schaer DJ, Boretti FS, Schoedon G, Schaffner A. Induction of the CD163-dependent haemoglobin uptake by macrophages as a novel anti-inflammatory action of glucocorticoids. Br J Haematol 2002;119:239–43.
   Google Scholar
• Ratcliffe NR, Kennedy SM, Morganelli PM. Immunocyto-chemical detection of Fc gamma receptors in human athero-sclerotic lesions. Immunol Lett 2001;77:169–74.
   Google Scholar
• Fonseca JE, Edwards JCW, Blades S, Gouldin NJ. Macro-phage subpopulations in rheumatoid synovium - Reduced CD163 expression in CD4+ T lymphocyte-rich microenviro-ments. Arthritis Rheum 2002;46:1210–6.
   PubMedGoogle Scholar
• Baeten D, Demetter P, Cuvelier CA, Kruithof E, Van Damme N, De Vos M, et al. Macrophages expressing the scavenger receptor CD163: a link between immune alterations of the gut and synovial inflammation in spondyloarthropathy. J Pathol 2002;196: 343–50.
   Google Scholar
• Philippidis P, Mason JC, Evans B, Nadra I, Taylor KM, Haskard DO, et al. The hemoglobin scavenger receptor CD163 on human macrophages is linked to athero-protective IL-10 and HO-1 effector pathways. Atherosclerosis 2003;170: S14.
   Google Scholar
• Zwadlo G, Voegeli R, Osthoff KS, Sorg C. A Monoclonal-Antibody to A Novel Differentiation Antigen on Human Macrophages Associated with the Down-Regulatory Phase of the Inflammatory Process. Exp Cell Biol 1987;55:295–304.
   PubMedGoogle Scholar
• Hogger P, Dreier J, Droste A, Buck F, Sorg C. Identification of the integral membrane protein RM3/1 on human monocytes as a glucocorticoid-inducible member of the scavenger receptor cysteine-rich family (CD163). J Immunol 1998; 161: 1883–90.
   Google Scholar
• Sulahian TH, Hogger P, Wardwell K, Wardwell K, Goulding NJ, Sorg C, et al. Human monocytes express CD163, which is upregulated by IL-10 and identical to p155. FASEB J 2000;14: A1143.
   Google Scholar
• Zwadloklarwasser G, Bent S, Hauheck HD, Sorg C, Schmutzler W. Glucocorticoid-Induced Appearance of the Macrophage Subtype Rm 3/1 in Peripheral-Blood of Man. Int Arch Allergy Immunol 1990;91: 175–80.
   Google Scholar
• Williams L, Jaral G, Smith A, Finan P. IL-10 expression profiling in human monocytes. J Leukoc Biol 2002;72:800–9.
   PubMed Web of Science ®Google Scholar
• Gratchev A, Guillot P, Hakiy N, Politz 0, Orfanos CE, Schledzewski K, et al. Alternatively activated macrophages differentially express fihronectin and its splice variants and the extracellular matrix protein beta IG-H3. Scand J Immunol 2001;53: 386–92.
   Google Scholar
• Song EW, Ouyang N, Horbelt M, Antus B, Wang MH, Exton MS. Influence of alternatively and classically activated macrophages on fibrogemc activities of human fibroblasts. Cell Immunol 2000;204:19–28.
   PubMed Web of Science ®Google Scholar
• Topoll HH, Zwadlo G, Lange DE, Sorg C. Phenotypic Dynamics of Macrophage Subsets During Human Gingivitis. J Dent Res 1988;67:685.
   Google Scholar
• Mitani K, Fujita H, Kappas A, Sass a S. Heme Oxygenase Is A Positive Acute-Phase Reactant in Human Hep3B Hepatoma-Cells. Blood 1992;79: 1255–9.
   Google Scholar
• Wagener FADT, van Beurden HE, den Hoff JW, Adema GJ, Figdor CG. The heme-heme oxygenase system: a molecular switch in wound healing. Blood 2003;102:521–8.
   PubMed Web of Science ®Google Scholar
• Lee TS, Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 20028: 240–6.
   Google Scholar
• Lee TS, Tsai HL, Chau LY. Induction of heme oxygenase-1 expression in murine macrophages is essential for the anti-inflammatory effect of low dose 15-deoxy-Delta(12,14)-pros-taglandin J(2). J Biol Chem 2003;278: 19325–30.
   Google Scholar
• Moller HJ, Peterslund NA, Graversen JH, Moestrup SK. Identification of the hemoglobin scavenger receptor/CD 163 as a natural soluble protein in plasma. Blood 2002;99:378-80. the monocyte hemoglobin scavenger receptor CD163. J Leukoc Biol 2002;72: 711–7.
   Google Scholar
• Moestrup SK, Gliemann J. Binding of Alpha-2-Macro-globulin-Proteinase to the Purified Receptor - Evidence That High Functional AFFinity Is Achieved by Binding to Adjacent Receptors. Biol Chem Hoppe-Seyler 1991;372:142.
   Google Scholar
• Frings W, Dreier J, Sorg C. Only the soluble form of the scavenger receptor CD163 acts inhibitory on phorbol ester-activated T-lymphocytes, whereas membrane-bound protein has no effect. FEBS Lett 2002;526: 93–6.
   Google Scholar
• Hogger P, Sorg C. Soluble CD163 inhibits phorbol ester-induced lymphocyte proliferation. Biochem Biophys Res Commun 2001;288:841–3.
   PubMed Web of Science ®Google Scholar
• Matsushita N, Kashiwagi M, Wait R, Nagayoshi R, Naka-mura M, Matsuda T, et al. Elevated levels of soluble CD163 in sera and fluids from rheumatoid arthritis patients and inhibition of the shedding of CD163 by TIMP-3. Clin Exp Immunol 2002;130: 156–61.
   Google Scholar
• Matsuyama T. Elevated levels of functional soluble CD163 in sera and fluids from rheumatoid arthritis patients and inhibition of the shedding of CD163 by TIMP-3. Arthritis Rheum 2002;46:5422–5423.
   Google Scholar
• Goldstein JI, Goldstein KA, Wardwell K, Fahrner SL, Goonan KE, Cheney MD, et al. Increase in plasma and surface CD163 levels in patients undergoing coronary artery bypass graft surgery. FASEB J 2003;17:C48.
   Google Scholar
• Moller HJ, de Fost M, Aerts H, Hollak C, Moestrup SK. Plasma level of the macrophage-derived soluble CD163 is increased and positively correlates with severity in Gaucher's disease. Eur J Haematol 2004;72:135–9.
   PubMed Web of Science ®Google Scholar
• Baeten D, Moller HJ, Delanghe JR, Veys EM, Moestrup SK, De Keyser F. CD163+ macrophages and local production of soluble CD163 are associated with lower lymphocyte acti-vation in spondyloarthropathy synovitis. Arthritis Rheum 2004:In press.
   Google Scholar
• Moller HJ, Petersen PH, Rejnmark L, Moestrup SK. Biological variation of soluble CD163. Scand J Clin Lab Invest 2003;63:15–21.
   PubMed Web of Science ®Google Scholar
• Walter RB, Bachli EB, Schaer DJ, Ruegg R, Schoedon G. Expression of the hemoglobin scavenger receptor (CD163/ HbSR) as immunophenotypic marker of monocytic lineage in acute myeloid leukemia. Blood 2003;101: 3755–6.
   Google Scholar
• Hotchkiss RS, Karl IE. Medical progress: The pathophysi-ology and treatment of sepsis. New Engl J Med 2003;348:138–50.
   PubMed Web of Science ®Google Scholar
• Moller HJ, Petersen PH, Rejnmark L, Moestrup SK. Biological variation of soluble CD163. Scand J Clin Lab Invest 2003;63:15–21.
   PubMed Web of Science ®Google Scholar
• Walter RB, Bachli EB, Schaer DJ, Ruegg R, Schoedon G. Expression of the hemoglobin scavenger receptor (CD 163/ HbSR) as immunophenotypic marker of monocytic lineage in acute myeloid leukemia. Blood 2003;101: 3755–6.
   Google Scholar
• Hotchkiss RS, Karl IE. Medical progress: The pathophysi-ology and treatment of sepsis. New Engl J Med 2003;348:138–50.
   PubMed Web of Science ®Google Scholar