Differential Expression of CD163 on Monocyte Subsets in Healthy and HIV-1 Infected Individuals

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Tippett, Emma ^a,b   Cheng, Wan Jung ^a   Westhorpe, Clare ^a   Cameron, Paul U ^a,b,c   Brew, Bruce J ^d   Lewin, Sharon R ^a,b,c   Jaworowski, Anthony ^a,b   Crowe, Suzanne M ^a,b  

^a MACFARLANE BURNET INSTITUTE FOR MEDICAL RESEARCH AND PUBLIC HEALTH   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c ALFRED HOSPITAL   (Australia)

^d ST VINCENT S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD16 ANTIGEN; CD163 ANTIGEN; COLONY STIMULATING FACTOR 1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR; CELL SURFACE RECEPTOR; DIFFERENTIATION ANTIGEN; LEUKOCYTE ANTIGEN;

ADULT; ARTICLE; CD4 LYMPHOCYTE COUNT; CELL DIFFERENTIATION; CELL MATURATION; CELL SURFACE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOPHENOTYPING; INFLAMMATION; MACROPHAGE; MONOCYTE; PROTEIN EXPRESSION; VIRUS LOAD; CASE CONTROL STUDY; FLOW CYTOMETRY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; CASE-CONTROL STUDIES; FLOW CYTOMETRY; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOPHENOTYPING; MONOCYTES; RECEPTORS, CELL SURFACE;

EID: 79956305447     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019968     Document Type: Article

References (75)

1. Crowe SM, Westhorpe CL, Mukhamedova N, Jaworowski A, Sviridov D, et al. (2010) The macrophage: the intersection between HIV infection and atherosclerosis. J Leukoc Biol 87: 589-598.
2. Glass JD, Fedor H, Wesselingh SL, McArthur JC, (1995) Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 38: 755-762.
3. Roberts ES, Zandonatti MA, Watry DD, Madden LJ, Henriksen SJ, et al. (2003) Induction of pathogenic sets of genes in macrophages and neurons in NeuroAIDS. Am J Pathol 162: 2041-2057.
4. Roberts ES, Masliah E, Fox HS, (2004) CD163 identifies a unique population of ramified microglia in HIV encephalitis (HIVE). J Neuropathol Exp Neurol 63: 1255-1264.
5. Knudsen TB, Larsen K, Kristiansen TB, Moller HJ, Tvede M, et al. (2007) Diagnostic value of soluble CD163 serum levels in patients suspected of meningitis: Comparison with CRP and procalcitonin. Scand J Infect Dis 39: 542-553.
6. Schaer DJ, Schleiffenbaum B, Kurrer M, Imhof A, Bachli E, et al. (2005) Soluble hemoglobin-haptoglobin scavenger receptor CD163 as a lineage-specific marker in the reactive hemophagocytic syndrome. Eur J Haematol 74: 6-10.
7. Bleesing J, Prada A, Siegel DM, Villanueva J, Olson J, et al. (2007) The diagnostic significance of soluble CD163 and soluble interleukin-2 receptor alpha-chain in macrophage activation syndrome and untreated new-onset systemic juvenile idiopathic arthritis. Arthritis Rheum 56: 965-971.
8. Moller HJ, Aerts H, Gronbaek H, Peterslund NA, Hyltoft Petersen P, et al. (2002) Soluble CD163: a marker molecule for monocyte/macrophage activity in disease. Scand J Clin Lab Invest (Suppl 237): 29-33.
9. Kristiansen M, Graversen JH, Jacobsen C, Sonne O, Hoffman HJ, et al. (2001) Identification of the haemoglobin scavenger receptor. Nature 409: 198-201.
10. Schaer CA, Vallelian F, Imhof A, Schoedon G, Schaer DJ, (2007) CD163-expressing monocytes constitute an endotoxin-sensitive Hb clearance compartment within the vascular system. J Leukoc Biol 82: 106-110.
11. Schaer DJ, Alayash AI, Buehler PW, (2007) Gating the radical hemoglobin to macrophages: the anti-inflammatory role of CD163, a scavenger receptor. Antioxid Redox Signal 9: 991-999.
12. Bover LC, Cardo-Vila M, Kuniyasu A, Sun J, Rangel R, et al. (2007) A previously unrecognized protein-protein interaction between TWEAK and CD163: potential biological implications. J Immunol 178: 8183-8194.
13. Fabriek BO, Polfliet MM, Vloet RP, van der Schors RC, Ligtenberg AJ, et al. (2007) The macrophage CD163 surface glycoprotein is an erythroblast adhesion receptor. Blood 109: 5223-5229.
14. Fabriek BO, van Bruggen R, Deng DM, Ligtenberg AJ, Nazmi K, et al. (2009) The macrophage scavenger receptor CD163 functions as an innate immune sensor for bacteria. Blood 113: 887-892.
15. Philippidis P, Mason JC, Evans BJ, Nadra I, Taylor KM, et al. (2004) Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme 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.
16. Hamann W, Floter A, Schmutzler W, Zwadlo-Klarwasser G, (1995) Characterization of a novel anti-inflammatory factor produced by RM3/1 macrophages derived from glucocorticoid treated human monocytes. Inflamm Res 44: 535-540.
17. Polfliet MM, Fabriek BO, Daniels WP, Dijkstra CD, van den Berg TK, (2006) The rat macrophage scavenger receptor CD163: expression, regulation and role in inflammatory mediator production. Immunobiology 211: 419-425.
18. Hogger P, Sorg C, (2001) Soluble CD163 inhibits phorbol ester-induced lymphocyte proliferation. Biochem Biophys Res Commun 288: 841-843.
19. Frings W, Dreier J, Sorg C, (2002) 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 526: 93-96.
20. Moniuszko M, Bodzenta-Lukaszyk A, Kowal K, Lenczewska D, Dabrowska M, (2009) Enhanced frequencies of CD14++CD16+, but not CD14+CD16+, peripheral blood monocytes in severe asthmatic patients. Clin Immunol 130: 338-346.
21. Goodale D, Phay C, Brown W, Gray-Statchuk L, Furlong P, et al. (2009) Flow cytometric assessment of monocyte activation markers and circulating endothelial cells in patients with localized or metastatic breast cancer. Cytometry B Clin Cytom 76: 107-117.
22. Goldstein JI, Goldstein KA, Wardwell K, Fahrner SL, Goonan KE, et al. (2003) Increase in plasma and surface CD163 levels in patients undergoing coronary artery bypass graft surgery. Atherosclerosis 170: 325-332.
23. Zwadlo-Klarwasser G, Bent S, Haubeck HD, Sorg C, Schmutzler W, (1990) Glucocorticoid-induced appearance of the macrophage subtype RM 3/1 in peripheral blood of man. Int Arch Allergy Appl Immunol 91: 175-180.
24. Wenzel I, Roth J, Sorg C, (1996) Identification of a novel surface molecule, RM3/1, that contributes to the adhesion of glucocorticoid-induced human monocytes to endothelial cells. Eur J Immunol 26: 2758-2763.
25. Buechler C, Ritter M, Orso E, Langmann T, Klucken J, et al. (2000) Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and antiinflammatory stimuli. J Leukoc Biol 67: 97-103.
26. Weaver LK, Pioli PA, Wardwell K, Vogel SN, Guyre PM, (2007) Up-regulation of human monocyte CD163 upon activation of cell-surface Toll-like receptors. J Leukoc Biol 81: 663-671.
27. Xu W, Schlagwein N, Roos A, van den Berg TK, Daha MR, et al. (2007) Human peritoneal macrophages show functional characteristics of M-CSF-driven anti-inflammatory type 2 macrophages. Eur J Immunol 37: 1594-1599.
28. Williams L, Jarai G, Smith A, Finan P, (2002) IL-10 expression profiling in human monocytes. J Leukoc Biol 72: 800-809.
29. Gleissner CA, Shaked I, Erbel C, Bockler D, Katus HA, et al. (2010) CXCL4 downregulates the atheroprotective hemoglobin receptor CD163 in human macrophages. Circ Res 106: 203-211.
30. Sulahian TH, Pioli PA, Wardwell K, Guyre PM, (2004) Cross-linking of FcgammaR triggers shedding of the hemoglobin-haptoglobin scavenger receptor CD163. J Leukoc Biol 76: 271-277.
31. 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.
32. Matsushita N, Kashiwagi M, Wait R, Nagayoshi R, Nakamura M, et al. (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.
33. Hintz KA, Rassias AJ, Wardwell K, Moss ML, Morganelli PM, et al. (2002) Endotoxin induces rapid metalloproteinase-mediated shedding followed by up-regulation of the monocyte hemoglobin scavenger receptor CD163. J Leukoc Biol 72: 711-717.
34. Weaver LK, Hintz-Goldstein KA, Pioli PA, Wardwell K, Qureshi N, et al. (2006) Pivotal advance: activation of cell surface Toll-like receptors causes shedding of the hemoglobin scavenger receptor CD163. J Leukoc Biol 80: 26-35.
35. Fabriek BO, Moller HJ, Vloet RP, van Winsen LM, Hanemaaijer R, et al. (2007) Proteolytic shedding of the macrophage scavenger receptor CD163 in multiple sclerosis. J Neuroimmunol 187: 179-186.
36. Daly A, Walsh C, Feighery C, O'Shea U, Jackson J, et al. (2006) Serum levels of soluble CD163 correlate with the inflammatory process in coeliac disease. Aliment Pharmacol Ther 24: 553-559.
37. Moller HJ, Peterslund NA, Graversen JH, Moestrup SK, (2002) Identification of the hemoglobin scavenger receptor/CD163 as a natural soluble protein in plasma. Blood 99: 378-380.
38. Kusi KA, Gyan BA, Goka BQ, Dodoo D, Obeng-Adjei G, et al. (2008) Levels of soluble CD163 and severity of malaria in children in Ghana. Clin Vaccine Immunol 15: 1456-1460.
39. Davis BH, Zarev PV, (2005) Human monocyte CD163 expression inversely correlates with soluble CD163 plasma levels. Cytometry B Clin Cytom 63: 16-22.
40. Fischer-Smith T, Bell C, Croul S, Lewis M, Rappaport J, (2008) Monocyte/macrophage trafficking in acquired immunodeficiency syndrome encephalitis: lessons from human and nonhuman primate studies. J Neurovirol 14: 318-326.
41. Kim WK, Alvarez X, Fisher J, Bronfin B, Westmoreland S, et al. (2006) CD163 identifies perivascular macrophages in normal and viral encephalitic brains and potential precursors to perivascular macrophages in blood. Am J Pathol 168: 822-834.
42. Burdo TH, Soulas C, Orzechowski K, Button J, Krishnan A, et al. (2010) Increased monocyte turnover from bone marrow correlates with severity of SIV encephalitis and CD163 levels in plasma. PLoS Pathog 6: e1000842.
43. Yearley JH, Pearson C, Shannon RP, Mansfield KG, (2007) Phenotypic variation in myocardial macrophage populations suggests a role for macrophage activation in SIV-associated cardiac disease. AIDS Res Hum Retroviruses 23: 515-524.
44. Sanchez C, Domenech N, Vazquez J, Alonso F, Ezquerra A, et al. (1999) The porcine 2A10 antigen is homologous to human CD163 and related to macrophage differentiation. J Immunol 162: 5230-5237.
45. Moniuszko M, Kowal K, Rusak M, Pietruczuk M, Dabrowska M, et al. (2006) Monocyte CD163 and CD36 expression in human whole blood and isolated mononuclear cell samples: influence of different anticoagulants. Clin Vaccine Immunol 13: 704-707.
46. Maniecki MB, Etzerodt A, Moestrup SK, Moller HJ, Graversen JH, (2011) Comparative assessment of the recognition of domain-specific CD163 monoclonal antibodies in human monocytes explains wide discrepancy in reported levels of cellular surface CD163 expression. Immunobiology In press.
47. Ziegler-Heitbrock L, Ancuta P, Crowe S, Dalod M, Grau V, et al. (2010) Nomenclature of monocytes and dendritic cells in blood. Blood 116: e74-80.
48. Musson RA, (1984) Human monocyte maturation/differentiation during in vitro culture. Surv Immunol Res 3: 138-141.
49. Souques F, Duperray C, Pene J, Bousquet J, Arnoux B, (1997) Modification of surface marker expression on CD14 monocytes of allergic patients after lysis or Ficoll purification. J Immunol Methods 204: 153-160.
50. Shepherd VL, Campbell EJ, Senior RM, Stahl PD, (1982) Characterization of the mannose/fucose receptor on human mononuclear phagocytes. J Reticuloendothel Soc 32: 423-431.
51. Etzerodt A, Maniecki MB, Moller K, Moller HJ, Moestrup SK, (2010) Tumor necrosis factor alpha-converting enzyme (TACE/ADAM17) mediates ectodomain shedding of the scavenger receptor CD163. J Leukoc Biol 88: 1201-1205.
52. Fischer-Smith T, Tedaldi E, Rappaport J, (2008) CD163/CD16 Coexpression by Circulating Monocytes/Macrophages in HIV: Potential Biomarkers for HIV Infection and AIDS Progression. AIDS Research and Human Retroviruses 24: 417-421.
53. Bissel SJ, Wang G, Trichel AM, Murphey-Corb M, Wiley CA, (2006) Longitudinal analysis of activation markers on monocyte subsets during the development of simian immunodeficiency virus encephalitis. J Neuroimmunol 177: 85-98.
54. Sulahian TH, Hogger P, Wahner AE, Wardwell K, Goulding NJ, et al. (2000) Human monocytes express CD163, which is upregulated by IL-10 and identical to p155. Cytokine 12: 1312-1321.
55. Van den Heuvel MM, Tensen CP, van As JH, Van den Berg TK, Fluitsma DM, et al. (1999) Regulation of CD163 on human macrophages: cross-linking of CD163 induces signalling and activation. J Leukoc Biol 66: 858-866.
56. Belge KU, Dayyani F, Horelt A, Siedlar M, Frankenberger M, et al. (2002) The proinflammatory CD14+CD16+DR++ monocytes are a major source of TNF. J Immunol 168: 3536-3542.
57. Ziegler-Heitbrock L, (2007) The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J Leukoc Biol 81: 584-592.
58. Boyle JJ, Harrington HA, Piper E, Elderfield K, Stark J, et al. (2009) Coronary intraplaque hemorrhage evokes a novel atheroprotective macrophage phenotype. Am J Pathol 174: 1097-1108.
59. Pilling D, Fan T, Huang D, Kaul B, Gomer RH, (2009) Identification of markers that distinguish monocyte-derived fibrocytes from monocytes, macrophages, and fibroblasts. PLoS One 4: e7475.
60. Stec M, Weglarczyk K, Baran J, Zuba E, Mytar B, et al. (2007) Expansion and differentiation of CD14+CD16(-) and CD14+ +CD16+ human monocyte subsets from cord blood CD34+ hematopoietic progenitors. J Leukoc Biol 82: 594-602.
61. Ancuta P, Wang J, Gabuzda D, (2006) CD16+ monocytes produce IL-6, CCL2, and matrix metalloproteinase-9 upon interaction with CX3CL1-expressing endothelial cells. J Leukoc Biol 80: 1156-1164.
62. Richens J, Fairclough L, Ghaemmaghami AM, Mahdavi J, Shakib F, et al. (2007) The detection of ADAM8 protein on cells of the human immune system and the demonstration of its expression on peripheral blood B cells, dendritic cells and monocyte subsets. Immunobiology 212: 29-38.
63. Schaer CA, Schoedon G, Imhof A, Kurrer MO, Schaer DJ, (2006) Constitutive endocytosis of CD163 mediates hemoglobin-heme uptake and determines the noninflammatory and protective transcriptional response of macrophages to hemoglobin. Circ Res 99: 943-950.
64. Verreck FA, de Boer T, Langenberg DM, Hoeve MA, Kramer M, et al. (2004) Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci U S A 101: 4560-4565.
65. Verreck FA, de Boer T, Langenberg DM, van der Zanden L, Ottenhoff TH, (2006) Phenotypic and functional profiling of human proinflammatory type-1 and anti-inflammatory type-2 macrophages in response to microbial antigens and IFN-gamma- and CD40L-mediated costimulation. J Leukoc Biol 79: 285-293.
66. Kruger M, Coorevits L, De Wit TP, Casteels-Van Daele M, Van De Winkel JG, et al. (1996) Granulocyte-macrophage colony-stimulating factor antagonizes the transforming growth factor-beta-induced expression of Fc gamma RIII (CD16) on human monocytes. Immunology 87: 162-167.
67. Ancuta P, Weiss L, Haeffner-Cavaillon N, (2000) CD14+CD16++ cells derived in vitro from peripheral blood monocytes exhibit phenotypic and functional dendritic cell-like characteristics. Eur J Immunol 30: 1872-1883.
68. Jaworowski A, Ellery P, Maslin CL, Naim E, Heinlein AC, et al. (2006) Normal CD16 Expression and Phagocytosis of Mycobacterium avium Complex by Monocytes from a Current Cohort of HIV-1-Infected Patients. J Infect Dis 193: 693-697.
69. Morganelli PM, Guyre PM, (1988) IFN-gamma plus glucocorticoids stimulate the expression of a newly identified human mononuclear phagocyte-specific antigen. J Immunol 140: 2296-2304.
70. Hogger 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.
71. Clerici M, Galli M, Bosis S, Gervasoni C, Moroni M, et al. (2000) Immunoendocrinologic abnormalities in human immunodeficiency virus infection. Ann N Y Acad Sci 917: 956-961.
72. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
73. Rajasuriar R, Booth D, Solomon A, Chua K, Spelman T, et al. (2010) Biological determinants of immune reconstitution in HIV-infected patients receiving antiretroviral therapy: the role of interleukin 7 and interleukin 7 receptor alpha and microbial translocation. J Infect Dis 202: 1254-1264.
74. Moller HJ, Moestrup SK, Weis N, Wejse C, Nielsen H, et al. (2006) Macrophage serum markers in pneumococcal bacteremia: Prediction of survival by soluble CD163. Crit Care Med 34: 2561-2566.
75. Rempel H, Sun B, Calosing C, Pillai SK, Pulliam L, (2010) Interferon-alpha drives monocyte gene expression in chronic unsuppressed HIV-1 infection. AIDS 24: 1415-1423.