Immunomodulation by IVIg and the role of Fc-gamma receptors: Classic mechanisms of action after all?

Frontiers in Immunology

Volumn 6, Issue JAN, 2015, Pages

  Nagelkerke, Sietse Q ^a   Kuijpers, Taco W ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Fc gamma receptors; IgG; Immunomodulation; IVIg; Mechanisms of action

Indexed keywords

EID: 84926642136     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00674     Document Type: Review

References (113)

1. Gelfand EW. Intravenous immune globulin in autoimmune and inflammatory diseases. N Engl J Med (2012) 367:2015-25. doi:10.1056/NEJMra1009433
2. Imbach P, Barandun S, d'Apuzzo V, Baumgartner C, Hirt A, Morell A, et al. High-dose intravenous gammaglobulin for idiopathic thrombocytopenic purpura in childhood. Lancet (1981) 1(8232):1228-31. doi:10.1016/S0140-6736(81)92400-4
3. Bruhns P. Properties of mouse and human IgG receptors and their contribution to disease models. Blood (2012) 119:5640-9. doi:10.1182/blood-2012-01-380121
4. 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) 188:1318-24. doi:10.4049/jimmunol.1003945
5. Breunis WB, van Mirre E, Bruin M, Geissler J, de Boer M, Peters M, et al. Copy number variation of the activating FCGR2C gene predisposes to idiopathic thrombocytopenic purpura. Blood (2008) 111:1029-38. doi:10.1182/blood-2007-03-079913
6. Teeling JL, Jansen-Hendriks T, Kuijpers TW, de Haas M, van de Winkel JG, Hack CE, et al. Therapeutic efficacy of intravenous immunoglobulin preparations depends on the immunoglobulin G dimers: studies in experimental immune thrombocytopenia. Blood (2001) 98:1095-9. doi:10.1182/blood.V98.4.1095
7. Tackenberg B, Jelcic I, Baerenwaldt A, Oertel WH, Sommer N, Nimmerjahn F, et al. Impaired inhibitory Fcgamma receptor IIB expression on B cells in chronic inflammatory demyelinating polyneuropathy. Proc Natl Acad Sci U S A (2009) 106:4788-92. doi:10.1073/pnas.0807319106
8. Hartnell A, Kay AB, Wardlaw AJ. IFN-gamma induces expression of Fc gamma RIII (CD16) on human eosinophils. J Immunol (1992) 148(5):1471-8.
9. Davoine F, Lavigne S, Chakir J, Ferland C, Boulay ME, Laviolette M. Expression of FcgammaRIII (CD16) on human peripheral blood eosinophils increases in allergic conditions. J Allergy Clin Immunol (2002) 109:463-9. doi:10.1067/mai.2002.121952
10. Mocsai A, Ruland J, Tybulewicz VL. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol (2010) 10:387-402. doi:10.1038/nri2765
11. Bezbradica JS, Medzhitov R. Role of ITAM signaling module in signal integration. Curr Opin Immunol (2012) 24(1):58-66. doi:10.1016/j.coi.2011.12.010
12. van Vugt MJ, Heijnen AF, Capel PJ, Park SY, Ra C, Saito T, et al. FcR gamma-chain is essential for both surface expression and function of human Fc gamma RI (CD64) in vivo. Blood (1996) 87:3593-9.
13. Cohen DM, Bhalla SC, Anaissie EJ, Hester JP, Savary CA, Rex JH. Effects of in vitro and in vivo cytokine treatment, leucapheresis and irradiation on the function of human neutrophils: implications for white blood cell transfusion therapy. Clin Lab Haematol (1997) 19:39-47. doi:10.1046/j.1365-2257.1997.00207.x
14. Gericke GH, Ericson SG, Pan L, Mills LE, Guyre PM, Ely P. Mature polymorphonuclear leukocytes express high-affinity receptors for IgG (Fc gamma RI) after stimulation with granulocyte colony-stimulating factor (G-CSF). J Leukoc Biol (1995) 57:455-61.
15. Maresco DL, Chang E, Theil KS, Francke U, Anderson CL. The three genes of the human FCGR1 gene family encoding Fc gamma RI flank the centromere of chromosome 1 at 1p12 and 1q21. Cytogenet Cell Genet (1996) 73:157-63. doi:10.1159/000134330
16. Ernst LK, Duchemin AM, Miller KL, Anderson CL. Molecular characterization of six variant Fcgamma receptor class I (CD64) transcripts. Mol Immunol (1998) 35:943-54. doi:10.1016/S0161-5890(98)00079-0
17. Van den Herik-Oudijk IE, Capel PJ, van der Bruggen T, van de Winkel JG. Identification of signaling motifs within human Fc gamma RIIa and Fc gamma RIIb isoforms. Blood (1995) 85:2202-11.
18. Smith KG, Clatworthy MR. FcgammaRIIB in autoimmunity and infection: evolutionary and therapeutic implications. Nat Rev Immunol (2010) 10:328-43. doi:10.1038/nri2762
19. Brooks DG, Qiu WQ, Luster AD, Ravetch JV. Structure and expression of human IgG FcRII(CD32). Functional heterogeneity is encoded by the alternatively spliced products of multiple genes. J Exp Med (1989) 170:1369-85. doi:10.1084/jem.170.4.1369
20. Warmerdam PA, Nabben NM, van de Graaf SA, van de Winkel JG, Capel PJ. The human low affinity immunoglobulin G Fc receptor IIC gene is a result of an unequal crossover event. J Biol Chem (1993) 268:7346-9.
21. Metes D, Ernst LK, Chambers WH, Sulica A, Herberman RB, Morel PA. Expression of functional CD32 molecules on human NK cells is determined by an allelic polymorphism of the FcgammaRIIC gene. Blood (1998) 91:2369-80.
22. Li X, Wu J, Ptacek T, Redden DT, Brown EE, Alarcon GS, et al. Allelic dependent expression of an activating Fc receptor n B cells enhances humoral immune responses. Sci Transl Med (2013) 5(216):216ra175. doi:10.1126/scitranslmed.3007097
23. Bussel J. Fc receptor blockade and immune thrombocytopenic purpura. Semin Hematol (2000) 37:261-6. doi:10.1053/shem.2000.8957
24. Breunis WB, van Mirre E, Geissler J, Laddach N, Wolbink G, van der Schoot E, et al. Copy number variation at the FCGR locus includes FCGR3A, FCGR2C and FCGR3B but not FCGR2A and FCGR2B. Hum Mutat (2009) 30:E640-50. doi:10.1002/humu.20997
25. van der Heijden J, Geissler J, van Mirre E, van Deuren M, van der Meer JW, Salama A, et al. A novel splice variant of FcγRIIα: a risk factor for anaphylaxis in patients with hypogammaglobulinemia. J Allergy Clin Immunol (2013) 131(5):1408-16. doi:10.1016/j.jaci.2013.02.009
26. Masuda M, Roos D. Association of all three types of Fc gamma R (CD64, CD32, and CD16) with a gamma-chain homodimer in cultured human monocytes. J Immunol (1993) 151:7188-95.
27. Trinchieri G, Valiante N. Receptors for the Fc fragment of IgG on natural killer cells. Nat Immunol (1993) 12(4-5):218-34.
28. Park JG, Isaacs RE, Chien P, Schreiber AD. In the absence of other Fc receptors, Fc gamma RIIIA transmits a phagocytic signal that requires the cytoplasmic domain of its gamma subunit. J Clin Invest (1993) 92:1967-73. doi:10.1172/JCI116790
29. Edberg JC, Moon JJ, Chang DJ, Kimberly RP. Differential regulation of human neutrophil FcgammaRIIa (CD32) and FcgammaRIIIb (CD16)-induced Ca2+ transients. J Biol Chem (1998) 273:8071-9. doi:10.1074/jbc.273.14.8071
30. Fernandes MJ, Lachance G, Pare G, Rollet-Labelle E, Naccache PH. Signaling through CD16b in human neutrophils involves the Tec family of tyrosine kinases. J Leukoc Biol (2005) 78:524-32. doi:10.1189/jlb.0804479
31. Guilliams M, Bruhns P, Saeys Y, Hammad H, Lambrecht BN. The function of Fcgamma receptors in dendritic cells and macrophages. Nat Rev Immunol (2014) 14:94-108. doi:10.1038/nri3582
32. Pincetic A, Bournazos S, DiLillo DJ, Maamary J, Wang TT, Dahan R, et al. Type I and type II Fc receptors regulate innate and adaptive immunity. Nat Immunol (2014) 15:707-16. doi:10.1038/ni.2939
33. Yu XJ, 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) 425:1253-8. doi:10.1016/j.jmb.2013.02.006
34. Warmerdam PA, van de Winkel JG, Gosselin EJ, Capel PJ. Molecular basis for a polymorphism of human Fc gamma receptor II (CD32). J Exp Med (1990) 172:19-25. doi:10.1084/jem.172.1.19
35. Li X, Wu J, Carter RH, Edberg JC, Su K, Cooper GS, et al. A novel polymorphism in the Fcgamma receptor IIB (CD32B) transmembrane region alters receptor signaling. Arthritis Rheum (2003) 48:3242-52. doi:10.1002/art.11313
36. Nicu EA, van der Velden U, Everts V, van Winkelhoff AJ, Roos D, Loos BG. Hyper-reactive PMNs in FcgammaRIIa 131 H/H genotype periodontitis patients. J Clin Periodontol (2007) 34:938-45. doi:10.1111/j.1600-051X.2007.01136.x
37. Yamamoto K, Sugita N, Kobayashi T, Okuda K, van de Winkel JG, Yoshie H. Evidence for a novel polymorphism affecting both N-linked glycosylation and ligand binding of the IgG receptor IIIB (CD16). Tissue Antigens (2001) 57:363-6. doi:10.1034/j.1399-0039.2001.057004363.x
38. Bruhns P, Iannascoli B, England P, Mancardi DA, Fernandez N, Jorieux S, et al. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood (2009) 113:3716-25. doi:10.1182/blood-2008-09-179754
39. Yamamoto K, Kobayashi T, Sugita N, Tai H, Yoshie H. The FcgammaRIIa polymorphism influences production of interleukin-1 by mononuclear cells. Int J Immunogenet (2007) 34:369-72. doi:10.1111/j.1744-313X.2007.00701.x
40. Bredius RG, Fijen CA, de Haas M, Kuijper EJ, Weening RS, van de Winkel JG, et al. Role of neutrophil Fc gamma RIIa (CD32) and Fc gamma RIIIb (CD16) polymorphic forms in phagocytosis of human IgG1-and IgG3-opsonized bacteria and erythrocytes. Immunology (1994) 83:624-30.
41. Floto RA, Clatworthy MR, Heilbronn KR, Rosner DR, MacAry PA, Rankin A, et al. Loss of function of a lupus-associated FcgammaRIIb polymorphism through exclusion from lipid rafts. Nat Med (2005) 11:1056-8. doi:10.1038/nm1288
42. Kono H, Kyogoku C, Suzuki T, Tsuchiya N, Honda H, Yamamoto K, et al. FcgammaRIIB Ile232Thr transmembrane polymorphism associated with human systemic lupus erythematosus decreases affinity to lipid rafts and attenuates inhibitory effects on B cell receptor signaling. Hum Mol Genet (2005) 14:2881-92. doi:10.1093/hmg/ddi320
43. Willcocks LC, Carr EJ, Niederer HA, Rayner TF, Williams TN, Yang W, et al. A defunctioning polymorphism in FCGR2B is associated with protection against malaria but susceptibility to systemic lupus erythematosus. Proc Natl Acad Sci U S A (2010) 107:7881-5. doi:10.1073/pnas.0915133107
44. Siriboonrit U, Tsuchiya N, Sirikong M, Kyogoku C, Bejrachandra S, Suthipinittharm P, et al. Association of Fcgamma receptor IIb and IIIb polymorphisms with susceptibility to systemic lupus erythematosus in Thais. Tissue Antigens (2003) 61:374-83. doi:10.1034/j.1399-0039.2003.00047.x
45. Kyogoku C, Dijstelbloem HM, Tsuchiya N, Hatta Y, Kato H, Yamaguchi A, et al. Fcgamma receptor gene polymorphisms in Japanese patients with systemic lupus erythematosus: contribution of FCGR2B to genetic susceptibility. Arthritis Rheum (2002) 46:1242-54. doi:10.1002/art.10257
46. Radstake TR, Franke B, Wenink MH, Nabbe KC, Coenen MJ, Welsing P, et al. The functional variant of the inhibitory Fcgamma receptor IIb (CD32B) is associated with the rate of radiologic joint damage and dendritic cell function in rheumatoid arthritis. Arthritis Rheum (2006) 54:3828-37. doi:10.1002/art.22275
47. Bruin M, Bierings M, Uiterwaal C, Revesz T, Bode L, Wiesman ME, et al. Platelet count, previous infection and FCGR2B genotype predict development of chronic disease in newly diagnosed idiopathic thrombocytopenia in childhood: results of a prospective study. Br J Haematol (2004) 127:561-7. doi:10.1111/j.1365-2141.2004.05235.x
48. Mackay M, Stanevsky A, Wang T, Aranow C, Li M, Koenig S, et al. Selective dysregulation of the FcgammaIIB receptor on memory B cells in SLE. J Exp Med (2006) 203:2157-64. doi:10.1084/jem.20051503
49. Carreno LJ, Pacheco R, Gutierrez MA, Jacobelli S, Kalergis AM. Disease activity in systemic lupus erythematosus is associated with an altered expression of low-affinity Fc gamma receptors and costimulatory molecules on dendritic cells. Immunology (2009) 128:334-41. doi:10.1111/j.1365-2567.2009.03138.x
50. Wenink MH, Santegoets KC, Roelofs MF, Huijbens R, Koenen HJ, van Beek R, et al. The inhibitory Fc gamma IIb receptor dampens TLR4-mediated immune responses and is selectively up-regulated on dendritic cells from rheumatoid arthritis patients with quiescent disease. J Immunol (2009) 183:4509-20. doi:10.4049/jimmunol.0900153
51. Su K, Wu J, Edberg JC, Li X, Ferguson L, Cooper GS, et al. A promoter haplotype of the immunoreceptor tyrosine-based inhibitory motif-bearing FcgammaRIIb alters receptor expression and associates with autoimmunity. I. Regulatory FCGR2B polymorphisms and their association with systemic lupus erythematosus. J Immunol (2004) 172:7186-91. doi:10.4049/jimmunol.172.11.7186
52. Wu J, Edberg JC, Redecha PB, Bansal V, Guyre PM, Coleman K, et al. A novel polymorphism of FcgammaRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J Clin Invest (1997) 100:1059-70. doi:10.1172/JCI119616
53. Dall'Ozzo S, Tartas S, Paintaud G, Cartron G, Colombat P, Bardos P, et al. Rituximab-dependent cytotoxicity by natural killer cells: influence of FCGR3A polymorphism on the concentration-effect relationship. Cancer Res (2004) 64:4664-9. doi:10.1158/0008-5472.CAN-03-2862
54. Ory PA, Clark MR, Kwoh EE, Clarkson SB, Goldstein IM. Sequences of complementary DNAs that encode the NA1 and NA2 forms of Fc receptor III on human neutrophils. J Clin Invest (1989) 84:1688-91. doi:10.1172/JCI114350
55. Bux J, Stein EL, Bierling P, Fromont P, Clay M, Stroncek D, et al. Characterization of a new alloantigen (SH) on the human neutrophil Fc gamma receptor IIIb. Blood (1997) 89:1027-34.
56. Matsuo K, Procter J, Stroncek D. Variations in genes encoding neutrophil antigens NA1 and NA2. Transfusion (2000) 40:645-53. doi:10.1046/j.1537-2995.2000.40060645.x
57. Salmon JE, Edberg JC, Kimberly RP. Fc gamma receptor III on human neutrophils. Allelic variants have functionally distinct capacities. J Clin Invest (1990) 85:1287-95. doi:10.1172/JCI114566
58. de Smith AJ, Tsalenko A, Sampas N, Scheffer A, Yamada NA, Tsang P, et al. Array CGH analysis of copy number variation identifies 1284 new genes variant in healthy white males: implications for association studies of complex diseases. Hum Mol Genet (2007) 16:2783-94. doi:10.1093/hmg/ddm208
59. Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, et al. Global variation in copy number in the human genome. Nature (2006) 444:444-54. doi:10.1038/nature05329
60. Wong KK, de Leeuw RJ, Dosanjh NS, Kimm LR, Cheng Z, Horsman DE, et al. A comprehensive analysis of common copy-number variations in the human genome. Am J Hum Genet (2007) 80:91-104. doi:10.1086/510560
61. Iafrate AJ, Feuk L, Rivera MN, Listewnik ML, Donahoe PK, Qi Y, et al. Detection of large-scale variation in the human genome. Nat Genet (2004) 36:949-51. doi:10.1038/ng1416
62. Koene HR, Kleijer M, Roos D, de Haas M, von dem Borne AE. Fc gamma RIIIB gene duplication: evidence for presence and expression of three distinct Fc gamma RIIIB genes in NA(1+,2+)SH(+) individuals. Blood (1998) 91:673-9.
63. de Haas M, Kleijer M, van Zwieten R, Roos D, von dem Borne AE. Neutrophil Fc gamma RIIIb deficiency, nature, and clinical consequences: a study of 21 individuals from 14 families. Blood (1995) 86:2403-13.
64. Willcocks LC, Lyons PA, Clatworthy MR, Robinson JI, Yang W, Newland SA, et al. Copy number of FCGR3B, which is associated with systemic lupus erythematosus, correlates with protein expression and immune complex uptake. J Exp Med (2008) 205:1573-82. doi:10.1084/jem.20072413
65. Zhou XJ, Lv JC, Bu DF, Yu L, Yang YR, Zhao J, et al. Copy number variation of FCGR3A rather than FCGR3B and FCGR2B is associated with susceptibility to anti-GBM disease. Int Immunol (2010) 22:45-51. doi:10.1093/intimm/dxp113
66. Fanciulli M, Norsworthy PJ, Petretto E, Dong R, Harper L, Kamesh L, et al. FCGR3B copy number variation is associated with susceptibility to systemic, but not organ-specific, autoimmunity. Nat Genet (2007) 39:721-3. doi:10.1038/ng2046
67. Mamtani M, Anaya JM, He W, Ahuja SK. Association of copy number variation in the FCGR3B gene with risk of autoimmune diseases. Genes Immun (2010) 11:155-60. doi:10.1038/gene.2009.71
68. Morris DL, Roberts AL, Witherden AS, Tarzi R, Barros P, Whittaker JC, et al. Evidence for both copy number and allelic (NA1/NA2) risk at the FCGR3B locus in systemic lupus erythematosus. Eur J Hum Genet (2010) 18:1027-31. doi:10.1038/ejhg.2010.56
69. Niederer HA, Willcocks LC, Rayner TF, Yang W, Lau YL, Williams TN, et al. Copy number, linkage disequilibrium and disease association in the FCGR locus. Hum Mol Genet (2010) 19:3282-94. doi:10.1093/hmg/ddq216
70. Aitman TJ, Dong R, Vyse TJ, Norsworthy PJ, Johnson MD, Smith J, et al. Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature (2006) 439:851-5. doi:10.1038/nature04489
71. McKinney C, Broen JC, Vonk MC, Beretta L, Hesselstrand R, Hunzelmann N, et al. Evidence that deletion at FCGR3B is a risk factor for systemic sclerosis. Genes Immun (2012) 13:458-60. doi:10.1038/gene.2012.15
72. McKinney C, Fanciulli M, Merriman ME, Phipps-Green A, Alizadeh BZ, Koeleman BP, et al. Association of variation in Fcgamma receptor 3B gene copy number with rheumatoid arthritis in Caucasian samples. Ann Rheum Dis (2010) 69:1711-6. doi:10.1136/ard.2009.123588
73. Graf SW, Lester S, Nossent JC, Hill CL, Proudman SM, Lee A, et al. Low copy number of the FCGR3B gene and rheumatoid arthritis: a case-control study and meta-analysis. Arthritis Res Ther (2012) 14:R28. doi:10.1186/ar3731
74. Marques RB, Thabet MM, White SJ, Houwing-Duistermaat JJ, Bakker AM, Hendriks GJ, et al. Genetic variation of the Fc gamma receptor 3B gene and association with rheumatoid arthritis. PLoS One (2010) 5(10):ii:e13173. doi:10.1371/journal.pone.0013173
75. 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) 109:770-5. doi:10.1016/S0022-3476(86)80691-6
76. Debré M, Bonnet MC, Fridman WH, Carosella E, Philippe N, Reinert P, et al. Infusion of Fc gamma fragments for treatment of children with acute immune thrombocytopenic purpura. Lancet (1993) 342:945-9. doi:10.1016/0140-6736(93)92000-J
77. 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) 173:332-9. doi:10.4049/jimmunol.173.1.332
78. 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):S14-8. doi:10.1097/00043426-200312001-00004
79. Nagelkerke SQ, Dekkers G, Kustiawan I, van de Bovenkamp FS, Geissler J, Plomp R, et al. Inhibition of FcγR-mediated phagocytosis by IVIg is independent of IgG-Fc sialylation and FcγRIIb in human macrophages. Blood (2014) 124:3709-18. doi:10.1182/blood-2014-05-576835
80. Schwab I, Nimmerjahn F. Intravenous immunoglobulin therapy: how does IgG modulate the immune system? Nat Rev Immunol (2013) 13:176-89. doi:10.1038/nri3401
81. Leontyev D, Katsman Y, Branch DR. Mouse background and IVIG dosage are critical in establishing the role of inhibitory Fc gamma receptor for the amelioration of experimental ITP. Blood (2012) 119:5261-4. doi:10.1182/blood-2012-03-415695
82. Guhr T, Bloem J, Derksen NI, Wuhrer M, Koenderman AH, Aalberse RC, 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) 2011(6):e21246. doi:10.1371/journal.pone.0021246
83. 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) 52:1799-805. doi:10.1111/j.1537-2995.2011.03517.x
84. Campbell IK, Miescher S, Branch DR, Mott PJ, Lazarus AH, Han D, 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) 192:5031-8. doi:10.4049/jimmunol.1301611
85. Kasermann F, Boerema DJ, Ruegsegger M, Hofmann A, Wymann S, Zuercher AW, et al. Analysis and functional consequences of increased Fab-sialylation of intravenous immunoglobulin (IVIG) after lectin fractionation. PLoS One (2012) 7:e37243. doi:10.1371/journal.pone.0037243
86. Maksymowych WP, Aviña-Zubieta A, Luong M, Russell AS. High dose intravenous immunoglobulin (IVIg) in severe refractory rheumatoid arthritis: no evidence for efficacy. Clin Exp Rheumatol (1996) 14(6):657-60.
87. Kanik KS, Yarboro CH, Naparstek Y, Plotz PH, Wilder RL. Failure of low-dose intravenous immunoglobulin therapy to suppress disease activity in patients with treatment-refractory rheumatoid arthritis. Arthritis Rheum (1996) 39(6):1027-9. doi:10.1002/art.1780390621
88. De Vita S, Ferraccioli GF, Di Poi E, Bartoli E, Bombardieri S. High dose intravenous immunoglobulin therapy for rheumatic diseases: clinical relevance and personal experience. Clin Exp Rheumatol (1996) 14(Suppl 15):S85-92.
89. Ferrara C, Grau S, Jäger C, Sondermann P, Brünker P, Waldhauer I, et al. Unique carbhydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Natl Acad Sci U S A (2011) 108(31):12669-74. doi:10.1073/pnas.1108455108
90. Peipp M, Lammerts van Bueren JJ, Schneider-Merck T, Bleeker WW, Dechant M, Beyer T, et al. Antibody fucosylation differentially impacts cytotoxicity mediated by NK and PMN effector cells. Blood (2008) 112(6):2390-9. doi:10.1182/blood-2008-03-144600
91. Roopenian DC, Akilesh S. FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol (2007) 7(9):715-25. doi:10.1038/nri2155
92. Chaudhury C, Mehnaz S, Robinson JM, Hayton WL, Pearl DK, Roopenian DC, et al. The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J Exp Med (2003) 197(3):315-22. doi:10.1084/jem.20021829
93. Raphael JC, Chevret S, Hughes RA, Annane D. Plasma exchange for Guillain-Barré syndrome. Cochrane Database Syst Rev (2012) 7:CD001798. doi:10.1002/14651858.CD001798.pub2
94. Hughes RA, Swan AV, van Doorn PA. Intravenous immunoglobulin for Guillain-Barré syndrome. Cochrane Database Syst Rev (2014) 9:CD002063. doi:10.1002/14651858.CD002063.pub5
95. Provan D, Stasi R, Newland AC, Blanchette VS, Bolton-Maggs P, Bussel JB, et al. International consensus report on the investigation and management of primary immune thrombocytopenia. Blood (2010) 115:168-86. doi:10.1182/blood-2009-06-225565
96. Masseau A, Guitton C, Bretonnière C, Renard B, Villers D, Hamidou M. Plasma exchanges as treatment of severe acute immune thrombocytopenic purpura. Rev Med Interne (2005) 26(10):824-6. doi:10.1016/j.revmed.2005.06.009
97. Tjon AS, van Gent R, Jaadar H, van Hagen MP, Mancham S, van der Laan LJ, et al. Intravenous immunoglobulin treatment in humans suppresses dendritic cell function via stimulation of IL-4 and IL-13 production. J Immunol (2014) 192(12):5625-34. doi:10.4049/jimmunol.1301260
98. den Dunnen J, Vogelpoel LT, Wypych T, Muller FJ, de Boer L, Kuijpers TW, et al. IgG opsonization of bacteria promotes Th17 responses via synergy between TLRs and FcγRIIα in human dendritic cells. Blood (2012) 120(1):112-21. doi:10.1182/blood-2011-12-399931
99. Massoud AH, Yona M, Xue D, Chouiali F, Alturaihi H, Ablona A, et al. Dendritic cell immunoreceptor: a novel receptor for intravenous immunoglobulin mediates induction of regulatory T cells. J Allergy Clin Immunol (2013) 133(3):853-63. doi:10.1016/j.jaci.2013.09.029
100. Sehgal K, Guo X, Koduru S, Shah A, Lin A, Yan X, et al. Plasmacytoid dendritic cells, interferon signaling, and FcgammaR contribute to pathogenesis and therapeutic response in childhood immune thrombocytopenia. Sci Transl Med (2013) 5(193):193ra89. doi:10.1126/scitranslmed.3006277
101. Crow YJ. Type I interferonopathies: a novel set of inborn errors of immunity. Ann N Y Acad Sci (2011) 1238:91-8. doi:10.1111/j.1749-6632.2011.06220.x
102. Rice GI, Kasher PR, Forte GM, Mannion NM, Greenwood SM, Szynkiewicz M, et al. Mutations in ADAR1 cause Aicardi-Goutières syndrome associated with a type I interferon signature. Nat Genet (2012) 44:1243-8. doi:10.1038/ng.2414
103. Basta M, Dalakas MC. High-dose intravenous immunoglobulin exerts its beneficial effect in patients with dermatomyositis by blocking endomysial deposition of activated complement fragments. J Clin Invest (1994) 94(5):1729-35. doi:10.1172/JCI117520
104. Diebolder CA, Beurskens FJ, de Jong RN, Koning RI, Strumane K, Lindorfer MA, et al. Complement is activated by IgG hexamers assembled at the cell surface. Science (2014) 343(6176):1260-3. doi:10.1126/science.1248943
105. Sultan Y, Kazatchkine MD, Nydegger U, Rossi F, Dietrich G, Algiman M. Intravenous immunoglobulin in the treatment of spontaneously acquired factor VIII:C inhibitors. Am J Med (1991) 91(5A):35S-9S. doi:10.1016/S0002-9343(91)80147-E
106. Abe Y, Horiuchi A, Miyake M, Kimura S. Anti-cytokine nature of natural human immunoglobulin: one possible mechanism of the clinical effect of intravenous immunoglobulin therapy. Immunol Rev (1994) 139:5-19. doi:10.1111/j.1600-065X.1994.tb00854.x
107. Ross C, Svenson M, Hansen MB, Vejlsgaard GL, Bendtzen K. High avidity IFN-neutralizing antibodies in pharmaceutically prepared human IgG. J Clin Invest (1995) 95(5):1974-8. doi:10.1172/JCI117881
108. Svenson M, Hansen MB, Ross C, Diamant M, Rieneck K, Nielsen H, et al. Antibody to granulocyte-macrophage colony-stimulating factor is a dominant anti-cytokine activity in human IgG preparations. Blood (1998) 91(6):2054-61.
109. Reipert BM, Stellamor MT, Poell M, Ilas J, Sasgary M, Reipert S, et al. Variation of anti-Fas antibodies in different lots of intravenous immunoglobulin. Vox Sang (2008) 94(4):334-41. doi:10.1111/j.1423-0410.2008.001036.x
110. Viard I, Wehrli P, Bullani R, Schneider P, Holler N, Salomon D, et al. Inhibition of toxic epidermal necrolysis by blockade of CD95 with human intravenous immunoglobulin. Science (1998) 282(5388):490-3. doi:10.1126/science.282.5388.490
111. Shrestha S, Wiener HW, Olson AK, Edberg JC, Bowles NE, Patel H, et al. Functional FCGR2B gene variants influence intravenous immunoglobulin response in patients with Kawasaki disease. J Allergy Clin Immunol (2011) 128(3):677-80. doi:10.1016/j.jaci.2011.04.027
112. Shrestha S, Wiener H, Shendre A, Kaslow RA, Wu J, Olson A, et al. Role of activating FcgammaR gene polymorphisms in Kawasaki disease susceptibility and intravenous immunoglobulin response. Circ Cardiovasc Genet (2012) 5(3):309-16. doi:10.1161/CIRCGENETICS.111.962464
113. Lewkowicz N, Klink M, Mycko MP, Lewkowicz P. Neutrophil-CD4+CD25+ T regulatory cell interactions: a possible new mechanism of infectious tolerance. Immunobiology (2013) 218(4):455-64. doi:10.1016/j.imbio.2012.05.029