Haemoglobin scavenger receptor: Function in relation to disease

Acta Biochimica Polonica

Volumn 53, Issue 2, 2006, Pages 257-268

  Zuwała Jagiełło, Jolanta ^a  

^a WROCLAW MEDICAL UNIVERSITY   (Poland)

Author keywords

Atherosclerotic lesions; CD163; Haem oxygenase; Haemoglobin scavenger receptor; Inflammation

Indexed keywords

EID: 33745847148     PISSN: 0001527X     EISSN: 1734154X     Source Type: Journal    
DOI: 10.18388/abp.2006_3338     Document Type: Review

References (99)

1. Abraham NG, da Silva JL, Lavrovsky Y, Stoltz RA, Kappas A, Dunn MW, Schwartzman ML (1995) Adenovirus-mediated haem oxygenase-1 gene transfer into rabbit ocular tissues. Invest Ophthalmol Vis Sci 36: 2202-2210.
2. Alcaraz MJ, Fernandez P, Guillen MI (2003) Anti-inflammatory actions of the haem oxygenase-1 pathway. Curr Pharm Des 9: 2541-2551.
3. Amersi F, Buelow R, Kato H, Ke B, Coito AJ, Shen XD, Zhao D, Zaky J, Melinek J, Lassman CR et al. (1999) Up-regulation of haem oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J Clin Invest 104: 1631-1639.
4. Aristoteli LP, Möller HJ, Bailey B, Moestrup SK, Kritharides L (2006) The monocytic lineage specific soluble CD163 is a plasma marker of coronary atherosclerosis. Atherosclerosis 184: 342-347.
5. Aronson D, Rayfield EJ (2002) How hyperglycemia promotes atherosclerosis?: molecular mechanisms. Cardiovasc Diabetol 1: 1-10.
6. Aruffo A, Melnick MB, Linsley PS, Seed B (1991) The lymphocyte glycoprotein CD6 contains a repeated domain structure characteristic of a new family of cell surface and secreted proteins. J Exp Med 174: 949-952.
7. Asleh R, Marsh S, Shilkrut M, Binah O, Guetta J, Lejbkowicz F, Enav B, Shehadeh N, Kanter Y, Lache O, Cohen O, Levy NS, Levy AP (2003) Genetically determined heterogeneity in haemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ Res 92: 1193-1200.
8. Baeten D, Möller HJ, Delanghe J, Veys EM, Moestrup SK, De Keyser F (2004) Association of CD163+ macrophages and local production of soluble CD163 with decreased lymphocyte activation in spondyloarthropathy synovitis. Arthritis Rheum 50: 1611-1623.
9. Basta G, Schmidt AM, De Caterina R (2004) Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes. Cardiovasc Res 63: 582-592.
10. Brouard S, Berberat PO, Tobiasch E, Seldon MP, Bach FH, Soares MP (2002) Haem oxygenase-1 derived carbon monoxide requires the activation of the transcription factor NF-kB to protect endothelial cells from TNF-alpha mediated apoptosis. J Biol Chem 277: 17950-17961.
11. Brown MS, Goldstein JL (1983) Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis. Annu Rev Biochem 52: 223-261.
12. Buechler C, Ritter M, Orso E, Langmann T, Klucken J, Schmitz G (2000) Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and anti-inflammatory stimuli. J Leukoc Biol 67: 97-103.
13. Burton JL, Kehrli ME (1996) Effects of dexamethasone on bovine circulating T lymphocyte populations. J Leukoc Biol 59: 90-99.
14. Cheng H, Bjerknes M, Chen H (1996) CRP-ductin: a gene expressed in intestinal crypts and in pancreas and hepatic ducts. Anat Rec 244: 327-334.
15. Christensen EI, Birn H (2002) Megalin and cubilin: multifunctional endocytic receptors. Nat Rev Mol Cell Biol 3: 256-266.
16. de la Llera-Moya M, Connelly MA, Drazul D (2001) Scavenger receptor class B type I affects cholesterol homeostasis by magnifying cholesterol flux between cells and HDL. J Lipid Res 42: 1969-1978.
17. Deiss A (1999) Destruction of erythrocytes. In Wintrobe's Clinical Hematology (Lee RG, Foerster J, Lukens J, Paraskevas F, Greer JP, Rodgers GM, eds) pp 267-299, Williams and Wilkins, Baltimore.
18. Delanghe JR, Langlois MR, De Buyzere ML (1998) Congenital anhaptoglobinemia versus acquired hypohaptoglobinemia [Letter]. Blood 91: 3524.
19. Demetter P, De Vos M, Van Huysse JA, Baeten D, Ferdinande L, Peeters H, Mielants H, Veys EM, De Keyser F, Cuvelier CA (2005) Colon mucosa of patients both with spondyloarthritis and Crohn's disease is enriched with macrophages expressing the scavenger receptor CD163. Ann Rheum Dis 64: 321-324.
20. Djemadji-Oudjiel N, Goerdt S, Kodelja V, Schmuth M, Orfanos CE (1996) Immunohistochemical identification of type II alternatively activated dendritic macrophages (RM 3/1+3, MS-1+/-, 25F9-) in psoriatic dermis. Arch Dermatol Res 288: 757-764.
21. Droste A, Sorg C, Hogger P (1999) Shedding of CD163, a novel regulatory mechanism for a member of the scavenger receptor cysteine-rich family. Biochem Biophys Res Commun 256: 110-113.
22. Dulak J, Jozkowicz A (2003) Carbon monoxide - a "new" gaseous modulator of gene expression. Acta Biochim Polon 50: 31-47.
23. Elbirt KK, Bonkovsky HL (1999) Heme oxygenase: recent advances in understanding its regulation and role. Proc Assoc Am Physicians 111: 438-447.
24. Fabriek BO, Van Haastert ES, Galea I, Polfliet MM, Dopp ED, Van Den Heuvel MM, Van Den Berg TK, De Groot CJ, Van Der Valk P, Dijkstra CD (2005) CD163-positive perivascular macrophages in the human CNS express molecules for antigen recognition and presentation. Glia 51: 297-305.
25. Fagoonee S, Gburek J, Hirsch E, Marro S, Moestrup SK, Laurberg JM, Christensen EI, Silengo L, Altruda F, Tolosano E (2005) Plasma protein haptoglobin modulates renal iron loading. Am J Pathol 166: 973-983.
26. Fernandez AZ, Lopez F, Tablante A, Romano E, Hurt-Camejo E, Camejo G, Apitz-Castro R (2001) Intravascular haemolysis increases atherogenicity of diet-induced hypercholesterolemia in rabbits in spite of haem oxygenase-1 gene and protein induction. Atherosclerosis 158: 103-111.
27. Funding M, Vorum H, Nexo E, Moestrup SK, Ehlers N, Möller HJ (2005) Soluble CD163 and interleukin-6 are increased in aqueous humour from patients with endothelial rejection of corneal grafts. Acta Ophthalmol Scand 83: 234-239.
28. Gburek J, Osada J (2000) Haemoglobin binding sites on renal brush-border membranes. Biochemie 82: 1135-1142.
29. Gburek J, Verroust PJ, Willnow TE, Fyfe JC, Nowacki W, Jacobsen C, Moestrup SK, Christensen EI (2002) Megalin and cubilin are endocytic receptors involved in renal clearance of haemoglobin. J Am Soc Nephrol 13: 423-430.
30. Gebe JA, Kiener PA, Ring HZ, Li X, Francke U, Aruffo A (1997) Molecular cloning, mapping to human chromosome 1 q21-q23, and cell binding characteristics of Spα, a new member of the scavenger receptor cysteine-rich (SRCR) family of proteins. J Biol Chem 272: 6151- 6158.
31. Glassock RJ (1995) Hematuria and pigmenturia. In Textbook of Nephrology (Massry SG, Glasock RJ, eds) p 557, Williams and Wilkins, Baltimore.
32. Gough PJ, Greaves DR, Gordon S (1998) A naturally occurring isoform of the human macrophage scavenger receptor (SR-A) gene generated by alternative splicing blocks modified LDL uptake. J Lipid Res 39: 531-543.
33. Graversen JH, Madsen M, Moestrup SK (2002) CD163: a signal receptor scavenging haptoglobin-haemoglobin complexes from plasma. Int J Biochem Cell Biol 34: 309-314.
34. Gutteridge JMC (1987) The antioxidant activity of haptoglobin towards haemoglobin-stimulated lipid peroxidation. Biochim Biophys Acta 917: 219-223.
35. Hamann W, Floter A, Schmutzler W, Zwadlo-Klarwasser G (1995) Characterisation of a novel anti-inflammatory factor produced by RM3/1 macrophages derived from glucocorticoid treated human monocytes. Inflamm Res 44: 535-540.
36. Hintz KA, Rassias AJ, Wardwell K, Moss ML, Morganelli PM, Pioli PA, Givan AL, Wallace PK, Yeager MP, Guyre PM (2002) Endotoxin induces rapid metalloproteinase-mediated shedding followed by up-regulation of the monocyte haemoglobin scavenger receptor CD163. J Leukoc Biol 72: 711-717.
37. Hiraoka A, Horiike N, Akbar SM, Michitaka K, Matsuyama T, Onji M (2005) Soluble CD163 in patients with liver diseases: very high levels of soluble CD163 in patients with fulminant hepatic failure. J Gastroenterol 40: 52-56.
38. Holmskov JU, Mollenhauer J, Madsen J, Vitved L, Gronlund J, Tornoe I, Kliem A, Reid KB, Poustka A, Skjodt K (1999) Cloning of gp-340, a putative opsonin receptor for lung surfactant protein D. Proc Natl Acad Sci USA 96: 10794-10799.
39. Högger P, Dreier J, Droste A, Buck F, Sorg C (1998) 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 161: 1883-1890.
40. Hvidberg V, Maniecki MB, Jacobsen C, Hojrup P, Möller HJ, Moestrup SK (2005) Identification of the receptor scavenging hemopexin-heme complexes. Blood 106: 2572-2579.
41. Jones NH, Clabby ML, Dialynas DP, Huang HJ, Herzenberg LA, Strominger JL (1986) Isolation of complementary DNA clones encoding the human lymphocyte glycoprotein T1/Leu-1. Nature 323: 346-349.
42. Keene WR, Jandl JH (1965) The sites of hemoglobin catabolism. Blood 26: 705-719.
43. Kino K, Tsunoo H, Higa Y, Takami M, Nakajima H (1982) Kinetic aspects of haemoglobin-haptoglobin-receptor interaction in rat liver plasma membranes, isolated liver cells, and liver cells in primary culture. J Biol Chem 257: 4828-4833.
44. Knudsen TB, Gustafson P, Kronborg G, Kristiansen TB, Moestrup SK, Nielsen JO, Gomes V, Aaby P, Lisse I, Möller HJ, Eugen-Olsen J (2005) Predictive value of soluble haemoglobin scavenger receptor CD163 serum levels for survival in verified tuberculosis patients. Clin Microbiol Infect 11: 730-735.
45. Krieger M (2001) Scavenger receptor class B type I is a multiligand HDL receptor that influences diverse physiologic systems. J Clin Invest 108: 793-797.
46. Kristiansen M, Graversen JH, Jacobsen C, Sonne O, Hoffman HJ, Law SK, Moestrup SK (2001) Identification of the haemoglobin scavenger receptor. Nature 409: 198-201.
47. Langlois MR, Delanghe JR (1996) Biological and clinical significance of haptoglobin polymorphism in humans. Clin Chem 42: 1589-1600.
48. Law SK, Micklem KJ, Shaw JM, Zhang X-P, Dong Y, Willis AC, Mason DY (1993) A new macrophage differentiation antigen which is a member of the scavenger receptor superfamily. Eur J Immunol 23: 2320-2325.
49. Lee TS, Chau LY (2002) Haem oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 8: 240-246.
50. Levy AP, Hochber I, Jablonski K, Resnick HE, Lee ET, Best L, Howard BV (2002) Haptoglobin phenotype is an independent risk factor for cardiovascular disease in individuals with diabetes: the strong heart study. J Am Coll Cardinol 40: 1984-1990.
51. Li XJ, Snyder SH (1995) Molecular cloning of Ebnerin, a von Ebner's gland protein associated with taste buds. J Biol Chem 270: 17674-17681.
52. Li W, Xu LH, Yuan XM (2004) Macrophage haemoglobin scavenger receptor and ferritin accumulation in human atherosclerotic lesions. Ann N Y Acad Sci 1030: 196-201.
53. Lim SK, Ferraro B, Moore K, Halliwell B (2001) Role of haptoglobin in free haemoglobin metabolism. Redox Rep 6: 219-227.
54. Matsushita N, Kashiwagi M, Wait R, Nagayoshi R, Nakamura M, Matsuda T, Hogger P, Guyre PM, Nagase H, Matsuyama T (2002) 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 130: 156-161.
55. Melamed-Frank M, Lache O, Enav BI, Szafranek T, Levy NS, Ricklis RM, Levy AP (2001) Structure/function analysis of the anti-oxidant properties of haptoglobin. Blood 98: 3693-3698.
56. Miller Y, Altamentova S, Shaklai N (1997) Oxidation of low-density lipoprotein by haemoglobin stems from a haem-initiated globin radical: antioxidant role of haptoglobin. Biochemistry 36: 12189-12198.
57. Moestrup SK, Möller HJ (2004) CD163: a regulated haemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann Med 36: 347-354.
58. Mollenhauer J, Wiemann S, Scheurlen W, Korn B, Hayashi Y, Wilgenbus KK, von Deimling A, Poustka A (1997) DMBT1, a new member of the SRCR superfamily, on chromosome 10q25.3-26.1 is deleted in malignant brain tumours. Nat Genet 17: 32-39.
59. Möller HJ, Peterslund NA, Graversen JH, Moestrup SK (2002) Identification of the haemoglobin scavenger receptor/CD163 as a natural soluble protein in plasma. Blood 99: 378-380.
60. Möller HJ, de Fost M, Aerts H, Hollak C, Moestrup SK (2004) Plasma level of the macrophage-derived soluble CD163 is increased and positively correlates with severity in Gaucher's disease. Eur J Haematol 72: 135-139.
61. Nguyen TT, Schwartz EJ, West RB, Warnke RA, Arber DA, Natkunam Y (2005) Expression of CD163 (haemoglobin scavenger receptor) in normal tissues, lymphomas, carcinomas, and sarcomas is largely restricted to the monocyte/macrophage lineage. Am J Surg Pathol 29: 617-624.
62. Nielsen MJ, Madsen M, Möller HJ, Moestrup SK (2006) The macrophage scavenger receptor CD163: endocytic properties of cytoplasmic tail variants. J Leukoc Biol 79: 837-845.
63. Okuda M, Tokunaga R, Taketani S (1992) Expression of haptoglobin receptors in human hepatoma cells. Biochim Biophys Acta 1136: 143-149.
64. Osada J, Nowacki W (1989) Elimination of goat haemoglobin and its complexes with goat haptoglobin from goat and rat circulation. Acta Biochim Polon 36: 365-369.
65. Oshiro S, Nakajima H (1988) Intrahepatocellular site of the catabolism of heme and globin moiety of hemoglobin-haptoglobin after intravenous administration to rats. J Biol Chem 263: 16032-16038.
66. Oshiro S, Yajima Y, Kawamura K, Kubota M, Yokofujita J, Nishibe Y, Takahama M, Nakajima H (1992) Catabolism of haemoglobin-haptoglobin complex in microsome subfractions. Chem Pharm Bull 40: 1847-1851.
67. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM (2000) Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6: 422-428.
68. Panter SS, Sadrzadeh SMH, Hallaway PE, Haines JL, Andersen VE, Eaton JW (1985) Hypohaptoglobinemia associated with familial epilepsy. J Exp Med 161: 748-754.
69. Philippidis P, Mason JC, Evans BJ, Nadra I, Taylor KM, Haskard DO, Landis RC (2004) Haemoglobin scavenger receptor CD163 mediates interleukin-10 release and haem oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ Res 94: 119-126.
70. Platt N, Suzuki H, Kurihara Y, Kodama T, Gordon S (1996) Role for the class-A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro. Proc Natl Acad Sci USA 93: 12456-12460.
71. Resnick D, Pearson A, Krieger M (1994) The SRCR superfamily: a family reminiscent of the Ig superfamily. Trends Biochem Sci 19: 5-8.
72. Ritter M, Buechler C, Langmann T, Schmitz G (1999) Genomic organization and chromosomal localization of the human CD163 (M130) gene: a member of the scavenger receptor cysteine-rich superfamily. Biochem Biophys Res Commun 260: 466-474.
73. Ritter M, Buechler C, Kapinsky M, Schmitz G (2001) Interaction of CD163 with the regulatory subunit of casein kinase II (CKII) and dependence of CD163 signalling on CKII and protein kinase C. Eur J Immunol 31: 999-1009.
74. Sanchez C, Domenech N, Vazquez J, Alonso F, Ezquerra A, Dominguez A (1999) The porcine 2A10 antigen is homologous to human CD163 and related to macrophage differentiation. J Immunol 162: 5230-5237.
75. Sarady JK, Otterbein SL, Liu F, Otterbein LE, Choi AM (2002) Carbon monoxide modulates endotoxin-induced production of granulocyte macrophage colony stimulating factor in macrophages. Am J Respir Cell Mol Biol 27: 739-745.
76. Schaer DJ, Boretti FS, Hongegger A, Poehler D, Linnscheid P, Staege H, Muller C, Schoedon G, Schaffner A (2001) Molecular cloning and characterization of the mouse CD163 homologue, a highly glucocorticoid-inducible member of the scavenger receptor cysteine-rich family. Immunogentics 53: 170-177.
77. Schaer DJ, Schleiffenbaum B, Kurrer M, Imhof A, Bachli E, Fehr J, Möller HJ, Moestrup SK, Schaffner A (2005) Soluble haemoglobin-haptoglobin scavenger receptor CD163 as a lineage-specific marker in the reactive hemophagocytic syndrome. Eur J Haematol 74: 6-10.
78. Schaer DJ, Schaer CA, Buehler PW, Boykins RA, Schoedon G, Alayash AI, Schaffner A (2006) CD163 is the macrophage scavenger receptor for native and chemically modified haemoglobins in the absence of haptoglobin. Blood 107: 373-380.
79. Song R, Ning W, Liu F, Ameredes BT, Calhoun WJ, Otterbein LE, Choi AM (2003) Regulation of IL-1beta-induced GM-CSF production in human airway smooth muscle cells by carbon monoxide. Am J Physiol Lung Cell Mol Physiol 284: L50-L56.
80. Spits H, de Waal Malefyt R (1992) Functional characterization of human IL-10. Int Arch Allergy Immunol 99: 8-15.
81. Sulahian TH, Hintz KA, Wardwell K, Guyre PM (2001) Development of an ELISA to measure soluble CD163 in biological fluids. J Immunol Methods 252: 25-31.
82. Sulahian TH, Pioli PA, Wardwell K, Guyre PM (2004) Cross-linking of Fc gamma R triggers shedding of the haemoglobin-haptoglobin scavenger receptor CD163. J Leukoc Biol 76: 271-277.
83. 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 (1997) A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 386: 292-296.
84. Timmermann M, Hogger P (2005) Oxidative stress and 8-iso-prostaglandin F(2alpha) induce ectodomain shedding of CD163 and release of tumor necrosis factor-alpha from human monocytes. Free Radic Biol Med 39: 98-107.
85. Torres SH, De Sanctis JB, de L Briceno M, Hernandez N, Finol HJ (2004) Inflammation and nitric oxide production in skeletal muscle of type 2 diabetic patients. J Endocrinol 181: 419-427.
86. Tosaki A, Das DK (2002) The role of haem oxygenase signaling in various disorders. Mol Cell Biochem 232: 49-57.
87. Van den Heuvel MM, Tensen CP, van As JH, Van den Berg TK, Fluitsma DM, Dijkstra CD, Dopp EA, Droste A, Van Gaalen FA, Sorg C, Hogger P, Beelen RH (1999) Regulation of CD 163 on human macrophages: cross-linking of CD163 induces signaling and activation. J Leukoc Biol 66: 858-866.
88. Vogel I, Grove J, Thorsen P, Moestrup SK, Uldbjerg N, Möller HJ (2005) Preterm delivery predicted by soluble CD163 and CRP in women with symptoms of preterm delivery. BJOG 112: 737-742.
89. Vos JA, Abbondanzo SL, Barekman CL, Andriko JW, Miettinen M, Aguilera NS (2005) Histiocytic sarcoma: a study of five cases including the histiocyte CD163. Mod Pathol 18: 693-704.
90. Wada T, Oara H, Watanabe K, Kinoshita H, Yachi A (1970) Autoradiographic study on the site of uptake of the haptoglobin-haemoglobin complex. J Reticuloendothel Soc 8: 185-193.
91. Wagener FA, Van Beurden HE, Von Den Hoff JW, Adema GJ, Figdor CG (2003) The haem-haem oxygenase system: a molecular switch in wound healing. Blood 102: 521-528.
92. Walter RB, Bachli EB, Schaer DJ, Ruegg R, Schoedon G (2003) Expression of the haemoglobin scavenger receptor (CD163/HbSR) as immunophenotypic marker of monocytic lineage in acute myeloid leukemia. Blood 101: 3755-3756.
93. Weinstein MB, Segal HL (1984) Uptake of free hemoglobin by rat liver parenchymal cells. Biochem Biophys Res Commun 123: 489-496.
94. Wijngaard PL, Metzelaar MJ, MacHugh ND, Morrison WI, Clevers HC (1992) Molecular characterization of the WC1 antigen expressed specifically on bovine CD42 CD82 g dT lymphocytes. J Immunol 149: 3273-3277.
95. Willis D, Moore AR, Frederick R, Willoughby DA (1996) Haem oxygenase: a novel target for the modulation of the inflammatory response. Nat Med 2: 87-90.
96. Woodward J, Sisley K, Reeves G, Nichols C, Parsons MA, Mudhar H, Rennie I (2004) Evidence of macrophage and lymphocyte, but not dendritic cell, infiltration in Posterior uveal melanomas, whilst cultured uveal melanomas demonstrate pluripotency by expressing CD68 and CD163. Int J Exp Pathol 85: 35-43.
97. Yu B, Hailman E, Wright SD (1997) Lipopolysaccharide binding protein and soluble CD14 catalyze exchange of phospholipids. J Clin Invest 99: 315-324.
98. Zuwała-Jagiełło J, Osada J (1998) Internalization study using EDTA-prepared hepatocytes for receptor-mediated endocytosis of haemoglobin-haptoglobin complex. Int J Biochem Cell Biol 30: 923-931.
99. Zwadlo G, Voegeli R, Osthoff KS, Sorg C (1987) A monoclonal antibody to a novel differentiation antigen on human macrophages associated with the down-regulatory phase of the inflammatory process. Exp Cell Biol 55: 295-304.