Inhibition of FcγR-mediated phagocytosis by IVIg is independent of IgG-Fc sialylation and FcγRIIb in human macrophages

Blood

Volumn 124, Issue 25, 2014, Pages 3709-3718

  Nagelkerke, Sietse Q ^a   Dekkers, Gillian ^a   Kustiawan, Iwan ^a   Van De Bovenkamp, Fleur S ^a   Geissler, Judy ^a   Plomp, Rosina ^b   Wuhrer, Manfred ^b   Vidarsson, Gestur ^a   Rispens, Theo ^a   Van Den Berg, Timo K ^a   Kuijpers, Taco W ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; COLONY STIMULATING FACTOR 1; FC RECEPTOR; FC RECEPTOR I; FC RECEPTOR IIA; FC RECEPTOR IIB; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN; IMMUNOGLOBULIN G; SIALIC ACID; UNCLASSIFIED DRUG; FCGR2B PROTEIN, HUMAN; IMMUNOGLOBULIN FC FRAGMENT; N ACETYLNEURAMINIC ACID;

ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; HUMAN; HUMAN CELL; MACROPHAGE; OPSONIZATION; PHAGOCYTOSIS; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIALYLATION; CELL CULTURE; DOSE RESPONSE; DRUG EFFECTS; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM;

CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ERYTHROCYTES; FLOW CYTOMETRY; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; IMMUNOGLOBULINS, INTRAVENOUS; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; N-ACETYLNEURAMINIC ACID; PHAGOCYTOSIS; RECEPTORS, IGG;

EID: 84919723220     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-05-576835     Document Type: Article

References (46)

1. Crow AR, Lazarus AH. Role of Fcgamma receptors in the pathogenesis and treatment of idiopathic thrombocytopenic purpura. J Pediatr Hematol Oncol. 2003;25(Suppl 1):S14-S18.
2. Bruhns P, Iannascoli B, England P, et al. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood. 2009;113(16):3716-3725.
3. Lux A, Yu X, Scanlan CN, Nimmerjahn F. Impact of immune complex size and glycosylation on IgG binding to human FcgRs. J Immunol. 2013;190(8):4315-4323.
4. Anderson CL, Shen L, Eicher DM, Wewers MD, Gill JK. Phagocytosis mediated by three distinct Fc gamma receptor classes on human leukocytes. J Exp Med. 1990;171(4):1333-1345.
5. Breunis WB, van Mirre E, Bruin M, et al. Copy number variation of the activating FCGR2C gene predisposes to idiopathic thrombocytopenic purpura. Blood. 2008;111(3):1029-1038.
6. Hunter S, Indik ZK, Kim MK, Cauley MD, Park JG, Schreiber AD. Inhibition of Fcgamma receptormediated phagocytosis by a nonphagocytic Fcgamma receptor. Blood. 1998;91(5):1762-1768.
7. Imbach P, Barandun S, d'Apuzzo V, et al. Highdose intravenous gammaglobulin for idiopathic thrombocytopenic purpura in childhood. Lancet. 1981;1(8232):1228-1231.
8. Provan D, Stasi R, Newland AC, et al. International consensus report on the investigation and management of primary immune thrombocytopenia. Blood. 2010;115(2):168-186.
9. Flores G, Cunningham-Rundles C, Newland AC, Bussel JB. Efficacy of intravenous immunoglobulin in the treatment of autoimmune hemolytic anemia: results in 73 patients. Am J Hematol. 1993;44(4):237-242.
10. Debré M, Bonnet MC, Fridman WH, et al. Infusion of Fc gamma fragments for treatment of children with acute immune thrombocytopenic purpura. Lancet. 1993;342(8877):945-949.
11. Burdach SE, Evers KG, Geursen RG. Treatment of acute idiopathic thrombocytopenic purpura of childhood with intravenous immunoglobulin G: comparative efficacy of 7S and 5S preparations. J Pediatr. 1986;109(5):770-775.
12. Bussel JB. Fc receptor blockade and immune thrombocytopenic purpura. Semin Hematol. 2000; 37(3):261-266.
13. Teeling JL, Jansen-Hendriks T, Kuijpers TW, et al. Therapeutic efficacy of intravenous immunoglobulin preparations depends on the immunoglobulin G dimers: studies in experimental immune thrombocytopenia. Blood. 2001;98(4):1095-1099.
14. Bazin R, Lemieux R, Tremblay T, St-Amour I. Tetramolecular immune complexes are more efficient than IVIg to prevent antibody-dependent in vitro and in vivo phagocytosis of blood cells. Br J Haematol. 2004;127(1):90-96.
15. Machino Y, Suzuki E, Higurashi S, et al. Chemically dimerized intravenous immunoglobulin has potent ameliorating activity in a mouse immune thrombocytopenic purpura model. Biochem Biophys Res Commun. 2012;418(4):748-753.
16. Bazin R, Lemieux R, Tremblay T. Reversal of immune thrombocytopenia in mice by cross-linking human immunoglobulin G with a high-affinity monoclonal antibody. Br J Haematol. 2006;135(1):97-100.
17. Tremblay T, Paré I, Bazin R. Immunoglobulin G dimers and immune complexes are dispensable for the therapeutic efficacy of intravenous immune globulin in murine immune thrombocytopenia. Transfusion. 2013;53(2):261-269.
18. Samuelsson A, Towers TL, Ravetch JV. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science. 2001;291(5503):484-486.
19. Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science. 2006;313(5787):670-673.
20. Anthony RM, Kobayashi T, Wermeling F, Ravetch JV. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature. 2011;475(7354):110-113.
21. Anthony RM, Wermeling F, Karlsson MC, Ravetch JV. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci USA. 2008;105(50):19571-19578.
22. Schwab I, Biburger M, Krönke G, Schett G, Nimmerjahn F. IVIg-mediated amelioration of ITP in mice is dependent on sialic acid and SIGNR1. Eur J Immunol. 2012;42(4):826-830.
23. Schwab I, Nimmerjahn F. Intravenous immunoglobulin therapy: how does IgG modulate the immune system? Nat Rev Immunol. 2013;13(3):176-189.
24. Schwab I, Mihai S, Seeling M, Kasperkiewicz M, Ludwig RJ, Nimmerjahn F. Broad requirement for terminal sialic acid residues and FcgRIIB for the preventive and therapeutic activity of intravenous immunoglobulins in vivo. Eur J Immunol. 2014;44(5):1444-1453.
25. Guhr T, Bloem J, Derksen NI, et al. Enrichment of sialylated IgG by lectin fractionation does not enhance the efficacy of immunoglobulin G in a murine model of immune thrombocytopenia. PLoS ONE. 2011;6(6):e21246.
26. Leontyev D, Katsman Y, Ma XZ, Miescher S, Käsermann F, Branch DR. Sialylation-independent mechanism involved in the amelioration of murine immune thrombocytopenia using intravenous gammaglobulin. Transfusion. 2012;52(8):1799-1805.
27. von Gunten S, Shoenfeld Y, Blank M, et al. IVIG pluripotency and the concept of Fc-sialylation: challenges to the scientist. Nat Rev Immunol. 2014;14(5):349.
28. Rispens T, Ooijevaar-de Heer P, Derksen NI, et al. Nanomolar to sub-picomolar affinity measurements of antibody-antigen interactions and protein multimerizations: fluorescence-assisted high-performance liquid chromatography. Anal Biochem. 2013;437(2):118-122.
29. Verreck FA, de Boer T, Langenberg DM, et al. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci USA. 2004;101(13):4560-4565.
30. van der Heijden J, Breunis WB, Geissler J, de Boer M, van den Berg TK, Kuijpers TW. Phenotypic variation in IgG receptors by nonclassical FCGR2C alleles. J Immunol. 2012;188(3):1318-1324.
31. Ierino FL, Hulett MD, McKenzie IF, Hogarth PM. Mapping epitopes of human Fc gamma RII (CDw32) with monoclonal antibodies and recombinant receptors. J Immunol. 1993;150(5):1794-1803.
32. Fleit HB, Wright SD, Unkeless JC. Human neutrophil Fc gamma receptor distribution and structure. Proc Natl Acad Sci USA. 1982;79(10):3275-3279.
33. Veri MC, Gorlatov S, Li H, et al. Monoclonal antibodies capable of discriminating the human inhibitory Fcgamma-receptor IIB (CD32B) from the activating Fcgamma-receptor IIA (CD32A): biochemical, biological and functional characterization. Immunology. 2007;121(3):392-404.
34. Dougherty GJ, Selvendran Y, Murdoch S, Palmer DG, Hogg N. The human mononuclear phagocyte high-affinity Fc receptor, FcRI, defined by a monoclonal antibody, 10.1. Eur J Immunol. 1987;17(10):1453-1459.
35. Kurlander RJ. Blockade of Fc receptor-mediated binding to U-937 cells by murine monoclonal antibodies directed against a variety of surface antigens. J Immunol. 1983;131(1):140-147.
36. Foo AH, Ramkumar S, Helke S, Branch DR. Chemical treatment of anti-D results in improved efficacy for the inhibition of Fcgamma receptor-mediated phagocytosis. Transfusion. 2007;47(12):2250-2259.
37. Käsermann F, Boerema DJ, Rüegsegger M, et al. Analysis and functional consequences of increased Fab-sialylation of intravenous immunoglobulin (IVIG) after lectin fractionation. PLoS ONE. 2012;7(6):e37243.
38. Clarkson SB, Bussel JB, Kimberly RP, Valinsky JE, Nachman RL, Unkeless JC. Treatment of refractory immune thrombocytopenic purpura with an anti-Fc gamma-receptor antibody. N Engl J Med. 1986;314(19):1236-1239.
39. Leontyev D, Katsman Y, Branch DR. Mouse background and IVIG dosage are critical in establishing the role of inhibitory Fcg receptor for the amelioration of experimental ITP. Blood. 2012;119(22):5261-5264.
40. van Mirre E, Teeling JL, van der Meer JW, Bleeker WK, Hack CE. Monomeric IgG in intravenous Ig preparations is a functional antagonist of FcgammaRII and FcgammaRIIIb. J Immunol. 2004;173(1):332-339.
41. Miescher S, Spycher MO, Amstutz H, et al. A single recombinant anti-RhD IgG prevents RhD immunization: association of RhD-positive red blood cell clearance rate with polymorphisms in the FcgammaRIIA and FcgammaIIIA genes. Blood. 2004;103(11):4028-4035.
42. Bussel JB, Kimberly RP, Clarkson SB, et al. Infusion of a monoclonal anti-FcR III in patients with refractory ITP. Neo-Adjuvant Chemotherapy II. 1988;169:883-887.
43. Ericson SG, Coleman KD, Wardwell K, et al. Monoclonal antibody 197 (anti-Fc gamma RI) infusion in a patient with immune thrombocytopenia purpura (ITP) results in down-modulation of Fc gamma RI on circulating monocytes. Br J Haematol. 1996;92(3):718-724.
44. Campbell IK, Miescher S, Branch DR, et al. Therapeutic effect of IVIG on inflammatory arthritis in mice is dependent on the Fc portion and independent of sialylation or basophils. J Immunol. 2014;192(11):5031-5038.
45. Ogata S, Shimizu C, Franco A, et al. Treatment response in Kawasaki disease is associated with sialylation levels of endogenous but not therapeutic intravenous immunoglobulin G. PLoS ONE. 2013;8(12):e81448.
46. Yu X, Vasiljevic S, Mitchell DA, Crispin M, Scanlan CN. Dissecting the molecular mechanism of IVIg therapy: the interaction between serum IgG and DC-SIGN is independent of antibody glycoform or Fc domain. J Mol Biol. 2013;425(8):1253-1258.