Understanding Fc receptor involvement in inflammatory diseases: From mechanisms to new therapeutic tools

Frontiers in Immunology

Volumn 10, Issue APR, 2019, Pages

  Mkaddem, Sanae Ben ^a,b,c,d   Benhamou, Marc ^a,b,c,d   Monteiro, Renato C ^b,c,d,e  

^a CENTRE DE RECHERCHE SUR L INFLAMMATION   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Laboratory of Excellence Labex INFLAMEX   (France)

^e BICHAT HOSPITAL   (France)

Author keywords

Antibody treatment; Fc receptor; Immunoglobilins; Inflammatory diseases; Signaling signaling pathways

Indexed keywords

CD23 ANTIGEN; FC RECEPTOR; FC RECEPTOR AGONIST; IMMUNOGLOBULIN; IMMUNOGLOBULIN M; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ALLERGY; ANTIINFLAMMATORY ACTIVITY; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CELL MIGRATION; COPY NUMBER VARIATION; CYTOTOXICITY; DISEASE EXACERBATION; DOWN REGULATION; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC VARIABILITY; GLYCOSYLATION; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; IMMUNOTHERAPY; INFLAMMATORY DISEASE; KIDNEY INJURY; KIDNEY TRANSPLANTATION; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; UPREGULATION; ANIMAL; ANTIGEN ANTIBODY COMPLEX; IMMUNOLOGY; INFLAMMATION; INNATE IMMUNITY;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; AUTOIMMUNE DISEASES; HUMANS; IMMUNITY, INNATE; INFLAMMATION; RECEPTORS, FC; SIGNAL TRANSDUCTION;

EID: 85065659351     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2019.00811     Document Type: Review

References (130)

1. 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
2. Bruhns P, Jonsson F. Mouse and human FcR effector functions. Immunol Rev. (2015) 268:25-51. doi: 10.1111/imr.12350
3. Kubagawa H, Kubagawa Y, Jones D, Nasti TH, Walter MR, Honjo K. The old but new IgM Fc receptor (FcmuR). Curr Top Microbiol Immunol. (2014) 382:3-28. doi: 10.1007/978-3-319-07911-0-1
4. Mkaddem SB, Murua A, Flament H, Titeca-Beauport D, Bounaix C, Danelli L, et al. Lyn and Fyn function as molecular switches that control immunoreceptors to direct homeostasis or inflammation. Nat Commun. (2017) 8:246. doi: 10.1038/s41467-017-00294-0
5. Malbec O, Fong DC, Turner M, Tybulewicz VL, Cambier JC, Fridman WH, et al. Fc epsilon receptor I-associated lyn-dependent phosphorylation of Fc gamma receptor IIB during negative regulation of mast cell activation. J Immunol. (1998) 160:1647-58.
6. Bolland S, Ravetch JV. Inhibitory pathways triggered by ITIM-containing receptors. Adv Immunol. (1999) 72:149-77. doi: 10.1016/S0065-2776(08)60019-X
7. Pasquier B, Launay P, Kanamaru Y, Moura IC, Pfirsch S, Ruffie C, et al. Identification of FcalphaRI as an inhibitory receptor that controls inflammation: dual role of FcRgamma ITAM. Immunity. (2005) 22:31-42. doi: 10.1016/j.immuni.2004.11.017
8. Pinheiro da Silva F, Aloulou M, Skurnik D, Benhamou M, Andremont A, Velasco IT, et al. CD16 promotes Escherichia coli sepsis through an FcR gamma inhibitory pathway that prevents phagocytosis and facilitates inflammation. Nat Med. (2007) 13:1368-74. doi: 10.1038/nm1665
9. Kanamaru Y, Pfirsch S, Aloulou M, Vrtovsnik F, Essig M, Loirat C, et al. Inhibitory ITAM signaling by Fc alpha RI-FcR gamma chain controls multiple activating responses and prevents renal inflammation. J Immunol. (2008) 180:2669-78. doi: 10.4049/jimmunol.180.4.2669
10. Aloulou M, Ben Mkaddem S, Biarnes-Pelicot M, Boussetta T, Souchet H, Rossato E, et al. IgG1 and IVIg induce inhibitory ITAM signaling through FcgammaRIII controlling inflammatory responses. Blood. (2012) 119:3084-96. doi: 10.1182/blood-2011-08-376046
11. Ben Mkaddem S, Hayem G, Jonsson F, Rossato E, Boedec E, Boussetta T, et al. Shifting FcgammaRIIA-ITAM from activation to inhibitory configuration ameliorates arthritis. J Clin Invest. (2014) 124:3945-59. doi: 10.1172/JCI74572
12. Iborra S, Martinez-Lopez M, Cueto FJ, Conde-Garrosa R, Del Fresno C, Izquierdo HM, et al. Leishmania uses mincle to target an inhibitory ITAM signaling pathway in dendritic cells that dampens adaptive immunity to infection. Immunity. (2016) 45:788-801. doi: 10.1016/j.immuni.2016.09.012
13. Getahun A, Cambier JC. Of ITIMs, ITAMs, and ITAMis: revisiting immunoglobulin Fc receptor signaling. Immunol Rev. (2015) 268:66-73. doi: 10.1111/imr.12336
14. Blank U, Launay P, Benhamou M, Monteiro RC. Inhibitory ITAMs as novel regulators of immunity. Immunol Rev. (2009) 232:59-71. doi: 10.1111/j.1600-065X.2009.00832.x
15. Stefanova I, Hemmer B, Vergelli M, Martin R, Biddison WE, Germain RN. TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways. Nat Immunol. (2003) 4:248-54. doi: 10.1038/ni895
16. Getahun A, Beavers NA, Larson SR, Shlomchik MJ, Cambier JC. Continuous inhibitory signaling by both SHP-1 and SHIP-1 pathways is required to maintain unresponsiveness of anergic B cells. J Exp Med. (2016) 213:751-69. doi: 10.1084/jem.20150537
17. Abram CL, Roberge GL, Pao LI, Neel BG, Lowell CA. Distinct roles for neutrophils and dendritic cells in inflammation and autoimmunity in motheaten mice. Immunity. (2013) 38:489-501. doi: 10.1016/j.immuni.2013.02.018
18. Chan VW, Lowell CA, DeFranco AL. Defective negative regulation of antigen receptor signaling in Lyn-deficient B lymphocytes. Curr Biol. (1998) 8:545-53. doi: 10.1016/S0960-9822(98)70223-4
19. Lowell CA. Src-family kinases: rheostats of immune cell signaling. Mol Immunol. (2004) 41:631-43. doi: 10.1016/j.molimm.2004.04.010
20. Apodaca G, Bomsel M, Arden J, Breitfeld PP, Tang K, Mostov KE. The polymeric immunoglobulin receptor. a model protein to study transcytosis. J Clin Invest. (1991) 87:1877-82. doi: 10.1172/JCI115211
21. Donaldson GP, Ladinsky MS, Yu KB, Sanders JG, Yoo BB, Chou WC, et al. Gut microbiota utilize immunoglobulin A for mucosal colonization. Science. (2018) 360:795-800. doi: 10.1126/science.aaq0926
22. Kikuno K, Kang DW, Tahara K, Torii I, Kubagawa HM, Ho KJ, et al. Unusual biochemical features and follicular dendritic cell expression of human Fcalpha/mu receptor. Eur J Immunol. (2007) 37:3540-50. doi: 10.1002/eji.200737655
23. Ahmed AA, Giddens J, Pincetic A, Lomino JV, Ravetch JV, Wang LX, et al. Structural characterization of anti-inflammatory immunoglobulin G Fc proteins. J Mol Biol. (2014) 426:3166-3179. doi: 10.1016/j.jmb.2014.07.006
24. Pennington LF, Tarchevskaya S, Brigger D, Sathiyamoorthy K, Graham MT, Nadeau KC, et al. Structural basis of omalizumab therapy and omalizumab-mediated IgE exchange. Nat Commun. (2016) 7:11610. doi: 10.1038/ncomms11610
25. Hogarth PM. Fc receptors are major mediators of antibody based inflammation in autoimmunity. Curr Opin Immunol. (2002) 14:798-802. doi: 10.1016/S0952-7915(02)00409-0
26. Monteiro RC, Van De Winkel JG. IgA Fc receptors. Annu Rev Immunol. (2003) 21:177-204. doi:10.1146/annurev.immunol.21.120601.141011
27. Kubagawa H, Oka S, Kubagawa Y, Torii I, Takayama E, Kang DW, et al. Identity of the elusive IgM Fc receptor (FcmuR) in humans. J Exp Med. (2009) 206:2779-93. doi: 10.1084/jem.20091107
28. Shibuya A, Sakamoto N, Shimizu Y, Shibuya K, Osawa M, Hiroyama T, et al. Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat Immunol. (2000) 1:441-6. doi: 10.1038/80886
29. Daeron M. Fc receptors as adaptive immunoreceptors. Curr Top Microbiol Immunol. (2014) 382:131-64. doi: 10.1007/978-3-319-07911-0-7
30. Diana J, Moura IC, Vaugier C, Gestin A, Tissandie E, Beaudoin L, et al. Secretory IgA induces tolerogenic dendritic cells through SIGNR1 dampening autoimmunity in mice. J Immunol. (2013) 191:2335-43. doi: 10.4049/jimmunol.1300864
31. Paul-Eugene N, Kolb JP, Abadie A, Gordon J, Delespesse G, Sarfati M, et al. Ligation of CD23 triggers cAMP generation and release of inflammatory mediators in human monocytes. J Immunol. (1992) 149:3066-71.
32. Kolb JP, Abadie A, Paul-Eugene N, Capron M, Sarfati M, Dugas B, et al. Ligation of CD23 triggers cyclic AMP generation in human B lymphocytes. J Immunol. (1993) 150:4798-809.
33. Chan MA, Gigliotti NM, Matangkasombut P, Gauld SB, Cambier JC, Rosenwasser LJ. CD23-mediated cell signaling in human B cells differs from signaling in cells of the monocytic lineage. Clin Immunol. (2010) 137:330-6. doi: 10.1016/j.clim.2010.08.005
34. Hargreaves CE, Rose-Zerilli MJ, Machado LR, Iriyama C, Hollox EJ, Cragg MS, et al. Fcgamma receptors: genetic variation, function, and disease. Immunol Rev. (2015) 268:6-24. doi: 10.1111/imr.12341
35. Gillis C, Gouel-Cheron A, Jonsson F, Bruhns P. Contribution of human fcgammars to disease with evidence from human polymorphisms and transgenic animal studies. Front Immunol. (2014) 5:254. doi: 10.3389/fimmu.2014.00254
36. Li X, Gibson AW, Kimberly RP. Human FcR polymorphism and disease. Curr Top Microbiol Immunol. (2014) 382:275-302 doi: 10.1007/978-3-319-07911-0-13
37. 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
38. 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
39. Takai T. Roles of Fc receptors in autoimmunity. Nat Rev Immunol. (2002) 2:580-92. doi:10.1038/nri856
40. 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
41. Sanders LA, Feldman RG, Voorhorst-Ogink MM, de Haas M, Rijkers GT, Capel PJ, et al. Human immunoglobulin G (IgG) Fc receptor IIA (CD32) polymorphism and IgG2-mediated bacterial phagocytosis by neutrophils. Infect Immun. (1995) 63:73-81.
42. 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
43. Onouchi Y, Ozaki K, Burns JC, Shimizu C, Terai M, Hamada H, et al. Japan kawasaki disease genome U. S. K. Consortium DG. A genome-wide association study identifies three new risk loci for Kawasaki disease. Nat Genet. (2012) 44:517-21. doi: 10.1038/ng.2220
44. Asano K, Matsushita T, Umeno J, Hosono N, Takahashi A, Kawaguchi T, et al. A genome-wide association study identifies three new susceptibility loci for ulcerative colitis in the Japanese population. Nat Genet. (2009) 41:1325-9. doi: 10.1038/ng.482
45. van der Pol WL, van den Berg LH, Scheepers RH, van der Bom JG, van Doorn PA, van Koningsveld R, et al. IgG receptor IIa alleles determine susceptibility and severity of Guillain-Barre syndrome. Neurology. (2000) 54:1661-5. doi: 10.1212/WNL.54.8.1661
46. Tsang ASMW, Nagelkerke SQ, Bultink IE, Geissler J, Tanck MW, Tacke CE, et al. Fc-gamma receptor polymorphisms differentially influence susceptibility to systemic lupus erythematosus and lupus nephritis. Rheumatology (Oxford). (2016) 55:939-48. doi: 10.1093/rheumatology/kev433
47. Qiao J, Al-Tamimi M, Baker RI, Andrews RK, Gardiner EE. The platelet Fc receptor, FcgammaRIIa. Immunol Rev. (2015) 268:241-52. doi: 10.1111/imr.12370
48. Tanaka Y, Suzuki Y, Tsuge T, Kanamaru Y, Horikoshi S, Monteiro RC, et al. FcgammaRIIa-131R allele and FcgammaRIIIa-176V/V genotype are risk factors for progression of IgA nephropathy. Nephrol Dial Transplant. (2005) 20:2439-45. doi: 10.1093/ndt/gfi043
49. McKenzie SE, Taylor SM, Malladi P, Yuhan H, Cassel DL, Chien P, et al. The role of the human Fc receptor Fc gamma RIIA in the immune clearance of platelets: a transgenic mouse model. J Immunol. (1999) 162:4311-8.
50. Tan Sardjono C, Mottram PL, van de Velde NC, Powell MS, Power D, Slocombe RF, et al. Development of spontaneous multisystem autoimmune disease and hypersensitivity to antibody-induced inflammation in Fcgamma receptor IIa-transgenic mice. Arthritis Rheum. (2005) 52:3220-9. doi: 10.1002/art.21344
51. Reilly AF, Norris CF, Surrey S, Bruchak FJ, Rappaport EF, Schwartz E, et al. Genetic diversity in human Fc receptor II for immunoglobulin G: Fc gamma receptor IIA ligand-binding polymorphism. Clin Diagn Lab Immunol. (1994) 1:640-4.
52. Pfirsch-Maisonnas S, Aloulou M, Xu T, Claver J, Kanamaru Y, Tiwari M, et al. Inhibitory ITAM signaling traps activating receptors with the phosphatase SHP-1 to form polarized "inhibisome" clusters. Sci Signal. (2011) 4:ra24. doi: 10.1126/scisignal.2001309
53. Pietersz GA, Mottram PL, van de Velde NC, Sardjono CT, Esparon S, Ramsland PA, et al. Inhibition of destructive autoimmune arthritis in FcgammaRIIa transgenic mice by small chemical entities. Immunol Cell Biol. (2009) 87:3-12. doi: 10.1038/icb.2008.82
54. White AL, Beers SA, Cragg MS. FcgammaRIIB as a key determinant of agonistic antibody efficacy. Curr Top Microbiol Immunol. (2014) 382:355-72. doi: 10.1007/978-3-319-07911-0-16
55. 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
56. Espeli M, Smith KG, Clatworthy MR. FcgammaRIIB and autoimmunity. Immunol Rev. (2016) 269:194-211. doi: 10.1111/imr.12368
57. McGaha TL, Sorrentino B, Ravetch JV. Restoration of tolerance in lupus by targeted inhibitory receptor expression. Science. (2005) 307:590-3. doi: 10.1126/science.1105160
58. Morgan AW, Griffiths B, Ponchel F, Montague BM, Ali M, Gardner PP, et al. Fcgamma receptor type IIIA is associated with rheumatoid arthritis in two distinct ethnic groups. Arthritis Rheum. (2000) 43:2328-34. doi: 10.1002/1529-0131(200010)43:10<2328::AID-ANR21>3.0.CO;2-Z
59. Nieto A, Pascual M, Caliz R, Mataran L, Martin J. Association of Fcgamma receptor IIIA polymorphism with rheumatoid arthritis: comment on the article by Morgan et al. Arthritis Rheum. (2002) 46:556-9. doi: 10.1002/art.10122
60. Tsuge T, Shimokawa T, Horikoshi S, Tomino Y, Ra C. Polymorphism in promoter region of Fcalpha receptor gene in patients with IgA nephropathy. Hum Genet. (2001) 108:128-33. doi: 10.1007/s004390100458
61. Wu J, Ji C, Xie F, Langefeld CD, Qian K, Gibson AW, et al. FcalphaRI (CD89) alleles determine the proinflammatory potential of serum IgA. J Immunol. (2007) 178:3973-82. doi: 10.4049/jimmunol.178.6.3973
62. Broen JC, Coenen MJ, Rueda B, Witte T, Padyukov L, Klareskog L, et al. The functional polymorphism 844 A>G in FcalphaRI (CD89) does not contribute to systemic sclerosis or rheumatoid arthritis susceptibility. J Rheumatol. (2011) 38:446-9. doi: 10.3899/jrheum.100427
63. Maillard N, Thibaudin L, Abadja F, Masson I, Garraud O, Berthoux F, et al. Single nucleotidic polymorphism 844 A->G of FCAR is not associated with IgA nephropathy in Caucasians. Nephrol Dial Transplant. (2012) 27:656-60. doi: 10.1093/ndt/gfr246
64. Kaneko S, Kobayashi T, Yamamoto K, Jansen MD, van de Winkel JG, Yoshie H. A novel polymorphism of FcalphaRI (CD89) associated with aggressive periodontitis. Tissue Antigens. (2004) 63:572-7. doi: 10.1111/j.0001-2815.2004.0228.x
65. Hirunsatit R, Kongruttanachok N, Shotelersuk K, Supiyaphun P, Voravud N, Sakuntabhai A, et al. Polymeric immunoglobulin receptor polymorphisms and risk of nasopharyngeal cancer. BMC Genet. (2003) 4:3. doi: 10.1186/1471-2156-4-3
66. Hasegawa M, Nishiyama C, Nishiyama M, Akizawa Y, Mitsuishi K, Ito T, et al. A novel-66T/C polymorphism in Fc epsilon RI alpha-chain promoter affecting the transcription activity: possible relationship to allergic diseases. J Immunol. (2003) 171:1927-33. doi: 10.4049/jimmunol.171.4.1927
67. Potaczek DP, Sanak M, Mastalerz L, Setkowicz M, Kaczor M, Nizankowska E, et al. The alpha-chain of high-affinity receptor for IgE (FcepsilonRIalpha) gene polymorphisms and serum IgE levels. Allergy. (2006) 61:1230-3. doi: 10.1111/j.1398-9995.2006.01195.x
68. Kim SH, Ye YM, Lee SK, Park HS. Genetic mechanism of aspirin-induced urticaria/angioedema. Curr Opin Allergy Clin Immunol. (2006) 6:266-70. doi: 10.1097/01.all.0000235899.57182.d4
69. Zhou J, Zhou Y, Lin LH, Wang J, Peng X, Li J, et al. Association of polymorphisms in the promoter region of FCER1A gene with atopic dermatitis, chronic uticaria, asthma, and serum immunoglobulin E levels in a Han Chinese population. Hum Immunol. (2012) 73:301-5. doi: 10.1016/j.humimm.2011.12.001
70. Zhang X, Zhang W, Qiu D, Sandford A, Tan WC. The E237G polymorphism of the high-affinity IgE receptor beta chain and asthma. Ann Allergy Asthma Immunol. (2004) 93:499-503. doi: 10.1016/S1081-1206(10)61419-6
71. Yang HJ, Zheng L, Zhang XF, Yang M, Huang X. Association of the MS4A2 gene promoter C-109T or the 7th exon E237G polymorphisms with asthma risk: a meta-analysis. Clin Biochem. (2014) 47:605-11. doi: 10.1016/j.clinbiochem.2014.01.022
72. Wu J, Lin R, Huang J, Guan W, Oetting WS, Sriramarao P, et al. Functional Fcgamma receptor polymorphisms are associated with human allergy. PLoS ONE. (2014) 9:e89196. doi: 10.1371/journal.pone.0089196
73. 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
74. Lee YH, Ji JD, Song GG. Associations between FCGR3A polymorphisms and susceptibility to rheumatoid arthritis: a metaanalysis. J Rheumatol. (2008) 35:2129-35. doi: 10.3899/jrheum.080186
75. Carcao MD, Blanchette VS, Wakefield CD, Stephens D, Ellis J, Matheson K, et al. Fcgamma receptor IIa and IIIa polymorphisms in childhood immune thrombocytopenic purpura. Br J Haematol. (2003) 120:135-41. doi: 10.1046/j.1365-2141.2003.04033.x
76. Koene HR, Kleijer M, Swaak AJ, Sullivan KE, Bijl M, Petri MA, et al. The Fc gammaRIIIA-158F allele is a risk factor for systemic lupus erythematosus. Arthritis Rheum. (1998) 41:1813-8. doi: 10.1002/1529-0131(199810)41:10<1813::AID-ART13>3.0.CO;2-6
77. Moroi R, Endo K, Kinouchi Y, Shiga H, Kakuta Y, Kuroha M, et al. FCGR3A-158 polymorphism influences the biological response to infliximab in Crohn's disease through affecting the ADCC activity. Immunogenetics. (2013) 65:265-71. doi: 10.1007/s00251-013-0679-8
78. Kelley JM, Monach PA, Ji C, Zhou Y, Wu J, Tanaka S, et al. IgA and IgG antineutrophil cytoplasmic antibody engagement of Fc receptor genetic variants influences granulomatosis with polyangiitis. Proc Natl Acad Sci U.S.A. (2011) 108:20736-41. doi: 10.1073/pnas.1109227109
79. van Egmond M, van Garderen E, van Spriel AB, Damen CA, van Amersfoort ES, van Zandbergen G, et al. FcalphaRI-positive liver Kupffer cells: reappraisal of the function of immunoglobulin A in immunity. Nat Med. (2000) 6:680-5. doi: 10.1038/76261
80. Pallasch CP, Schulz A, Kutsch N, Schwamb J, Hagist S, Kashkar H, et al. Overexpression of TOSO in CLL is triggered by B-cell receptor signaling and associated with progressive disease. Blood. (2008) 112:4213-9. doi: 10.1182/blood-2008-05-157255
81. Hitoshi Y, Lorens J, Kitada SI, Fisher J, LaBarge M, Ring HZ, et al. Toso, a cell surface, specific regulator of Fas-induced apoptosis in T cells. Immunity. (1998) 8:461-71. doi: 10.1016/S1074-7613(00)80551-8
82. Miller LS, Atabai K, Nowakowski M, Chan A, Bluth MH, Minkoff H, et al. Increased expression of CD23 (Fc(epsilon) receptor II) by peripheral blood monocytes of aids patients. AIDS Res Hum Retroviruses. (2001) 17:443-52. doi: 10.1089/088922201750102544
83. Morgan AW, Keyte VH, Babbage SJ, Robinson JI, Ponchel F, Barrett JH, et al. FcgammaRIIIA-158V and rheumatoid arthritis: a confirmation study. Rheumatology (Oxford). (2003) 42:528-33. doi: 10.1093/rheumatology/keg169
84. Descours B, Petitjean G, Lopez-Zaragoza JL, Bruel T, Raffel R, Psomas C, et al. CD32a is a marker of a CD4 T-cell HIV reservoir harbouring replication-competent proviruses. Nature. (2017) 543:564-567. doi: 10.1038/nature21710
85. Abdel-Mohsen M, Kuri-Cervantes L, Grau-Exposito J, Spivak AM, Nell RA, Tomescu C, et al. CD32 is expressed on cells with transcriptionally active HIV but does not enrich for HIV DNA in resting T cells. Sci Transl Med. (2018) 10:eaar6759. doi: 10.1126/scitranslmed.aar6759.
86. Badia R, Ballana E, Castellvi M, Garcia-Vidal E, Pujantell M, Clotet B, et al. CD32 expression is associated to T-cell activation and is not a marker of the HIV-1 reservoir. Nat Commun. (2018) 9:2739. doi: 10.1038/s41467-018-05157-w
87. Su K, Yang H, Li X, Li X, Gibson AW, Cafardi JM, et al. Expression profile of FcgammaRIIb on leukocytes and its dysregulation in systemic lupus erythematosus. J Immunol. (2007) 178:3272-80. doi: 10.4049/jimmunol.178.5.3272
88. Liu Y, Gong Y, Qu C, Zhang Y, You R, Yu N, et al. CD32b expression is down-regulated on double-negative memory B cells in patients with Hashimoto's thyroiditis. Mol Cell Endocrinol. (2017) 440:1-7. doi: 10.1016/j.mce.2016.11.004
89. Wong KL, Yeap WH, Tai JJ, Ong SM, Dang TM, Wong SC. The three human monocyte subsets: implications for health and disease. Immunol Res. (2012) 53:41-57. doi: 10.1007/s12026-012-8297-3
90. Grossetete B, Launay P, Lehuen A, Jungers P, Bach JF, Monteiro RC. Down-regulation of Fc alpha receptors on blood cells of IgA nephropathy patients: evidence for a negative regulatory role of serum IgA. Kidney Int. (1998) 53:1321-35.
91. Grossetete B, Viard JP, Lehuen A, Bach JF, Monteiro RC. Impaired Fc alpha receptor expression is linked to increased immunoglobulin A levels and disease progression in HIV-1-infected patients. AIDS. (1995) 9:229-34. doi: 10.1097/00002030-199509030-00003
92. Silvain C, Patry C, Launay P, Lehuen A, Monteiro RC. Altered expression of monocyte IgA Fc receptors is associated with defective endocytosis in patients with alcoholic cirrhosis. Potential role for IFN-gamma. J Immunol. (1995) 155:1606-18.
93. Berthelot L, Jamin A, Viglietti D, Chemouny JM, Ayari H, Pierre M, et al. Value of biomarkers for predicting immunoglobulin A vasculitis nephritis outcome in an adult prospective cohort. Nephrol Dial Transplant. (2017) 33:1579-90. doi: 10.1093/ndt/gfx300
94. Xue J, Zhao Q, Zhu L, Zhang W. Deglycosylation of FcalphaR at N58 increases its binding to IgA. Glycobiology. (2010) 20:905-15. doi: 10.1093/glycob/cwq048
95. Monteiro RC. Recent advances in the physiopathology of IgA nephropathy. Nephrol Ther. (2018) 14(Suppl 1):S1-8. doi: 10.1016/j.nephro.2018.02.004
96. Vuong MT, Hahn-Zoric M, Lundberg S, Gunnarsson I, van Kooten C, Wramner L, et al. Association of soluble CD89 levels with disease progression but not susceptibility in IgA nephropathy. Kidney Int. (2010) 78:1281-7. doi: 10.1038/ki.2010.314
97. Berthelot L, Robert T, Vuiblet V, Tabary T, Braconnier A, Drame M, et al. Recurrent IgA nephropathy is predicted by altered glycosylated IgA, autoantibodies and soluble CD89 complexes. Kidney Int. (2015) 88:815-22. doi: 10.1038/ki.2015.158
98. Berthelot L, Papista C, Maciel TT, Biarnes-Pelicot M, Tissandie E, Wang PH, et al. Transglutaminase is essential for IgA nephropathy development acting through IgA receptors. J Exp Med. (2012) 209:793-806. doi: 10.1084/jem.20112005
99. Moura IC, Centelles MN, Arcos-Fajardo M, Malheiros DM, Collawn JF, Cooper MD, et al. Identification of the transferrin receptor as a novel immunoglobulin (Ig)A1 receptor and its enhanced expression on mesangial cells in IgA nephropathy. J Exp Med. (2001) 194:417-25. doi: 10.1084/jem.194.4.417
100. Tamouza H, Chemouny JM, Raskova Kafkova L, Berthelot L, Flamant M, Demion M, et al. The IgA1 immune complex-mediated activation of the MAPK/ERK kinase pathway in mesangial cells is associated with glomerular damage in IgA nephropathy. Kidney Int. (2012) 82:1284-96. doi: 10.1038/ki.2012.192
101. Coulon S, Dussiot M, Grapton D, Maciel TT, Wang PH, Callens C, et al. Polymeric IgA1 controls erythroblast proliferation and accelerates erythropoiesis recovery in anemia. Nat Med. (2011) 17:1456-65. doi: 10.1038/nm.2462
102. Kanamaru Y, Arcos-Fajardo M, Moura IC, Tsuge T, Cohen H, Essig M, et al. Fc alpha receptor I activation induces leukocyte recruitment and promotes aggravation of glomerulonephritis through the FcR gamma adaptor. Eur J Immunol. (2007) 37:1116-28. doi: 10.1002/eji.200636826
103. Launay P, Patry C, Lehuen A, Pasquier B, Blank U, Monteiro RC. Alternative endocytic pathway for immunoglobulin A Fc receptors (CD89) depends on the lack of FcRgamma association and protects against degradation of bound ligand. J Biol Chem. (1999) 274:7216-25. doi: 10.1074/jbc.274.11.7216
104. Honjo K, Kubagawa Y, Suzuki Y, Takagi M, Ohno H, Bucy RP, et al. Enhanced auto-antibody production and Mott cell formation in FcmuR-deficient autoimmune mice. Int Immunol. (2014) 26:659-72. doi: 10.1093/intimm/dxu070
105. Ouchida R, Mori H, Hase K, Takatsu H, Kurosaki T, Tokuhisa T, et al. Critical role of the IgM Fc receptor in IgM homeostasis, B-cell survival, and humoral immune responses. Proc Natl Acad Sci USA. (2012) 109:E2699-706. doi: 10.1073/pnas.1210706109
106. Li FJ, Kubagawa Y, McCollum MK, Wilson L, Motohashi T, Bertoli LF, et al. Enhanced levels of both the membrane-bound and soluble forms of IgM Fc receptor (FcmuR) in patients with chronic lymphocytic leukemia. Blood. (2011) 118:4902-9. doi: 10.1182/blood-2011-04-350793
107. Madarova M, Mucha R, Hresko S, Makarova Z, Gdovinova Z, Szilasiova J, et al. Identification of new phosphorylation sites of CD23 in B-cells of patients with chronic lymphocytic leukemia. Leuk Res. (2018) 70:25-33. doi: 10.1016/j.leukres.2018.05.002
108. Tsuboi N, Asano K, Lauterbach M, Mayadas TN. Human neutrophil Fcgamma receptors initiate and play specialized nonredundant roles in antibody-mediated inflammatory diseases. Immunity. (2008) 28:833-46. doi: 10.1016/j.immuni.2008.04.013
109. Rossato E, Ben Mkaddem S, Kanamaru Y, Hurtado-Nedelec M, Hayem G, Descatoire V, et al. Reversal of arthritis by human monomeric IgA through the receptor-mediated SH2 domain-containing phosphatase 1 Inhibitory pathway. Arthritis Rheumatol. (2015) 67:1766-77. doi: 10.1002/art.39142
110. van der Steen LP, Bakema JE, Sesarman A, Florea F, Tuk CW, Kirtschig G, et al. Blocking Fcalpha receptor I on granulocytes prevents tissue damage induced by IgA autoantibodies. J Immunol. (2012) 189:1594-601. doi: 10.4049/jimmunol.1101763
111. Heineke MH, van der Steen LPE, Korthouwer RM, Hage JJ, Langedijk JPM, Benschop JJ, et al. Peptide mimetics of immunoglobulin A (IgA) and FcalphaRI block IgA-induced human neutrophil activation and migration. Eur J Immunol. (2017) 47:1835-45. doi: 10.1002/eji.201646782
112. Jardieu PM, Fick RB Jr. IgE inhibition as a therapy for allergic disease. Int Arch Allergy Immunol. (1999) 118:112-5 (1999) doi: 10.1159/000024043
113. Milgrom H, Fick RB Jr, Su JQ, Reimann JD, Bush RK, Watrous ML, et al. Treatment of allergic asthma with monoclonal anti-IgE antibody. rhuMAb-E25 Study Group. N Engl J Med. (1999) 341:1966-73. doi: 10.1056/NEJM199912233412603
114. Kazatchkine MD, Kaveri SV. Immunomodulation of autoimmune and inflammatory diseases with intravenous immune globulin. N Engl J Med. (2001) 345:747-55. doi: 10.1056/NEJMra993360
115. Pecoraro A, Crescenzi L, Granata F, Genovese A, Spadaro G. Immunoglobulin replacement therapy in primary and secondary antibody deficiency: the correct clinical approach. Int Immunopharmacol. (2017). 52:136-42. doi: 10.1016/j.intimp.2017.09.005
116. Jin F, Balthasar JP. Mechanisms of intravenous immunoglobulin action in immune thrombocytopenic purpura. Hum Immunol. (2005) 66:403-10. doi: 10.1016/j.humimm.2005.01.029
117. Debre 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
118. Nimmerjahn F, Ravetch JV. Anti-inflammatory actions of intravenous immunoglobulin. Annu Rev Immunol. (2008) 26:513-33. doi: 10.1146/annurev.immunol.26.021607.090232
119. Siragam V, Crow AR, Brinc D, Song S, Freedman J, Lazarus AH. Intravenous immunoglobulin ameliorates ITP via activating Fc gamma receptors on dendritic cells. Nat Med. (2006) 12:688-92. doi: 10.1038/nm1416
120. Epstein JS, Zoon KC. Important drug warning: immune globulin intravenous (human) (IGIV) products. Neonatal Netw. (2000) 19:60-2.
121. Bolland S, Ravetch JV. Spontaneous autoimmune disease in Fc(gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity. (2000) 13:277-85. doi: 10.1016/S1074-7613(00)00027-3
122. van Mirre E, van Royen A, Hack CE. IVIg-mediated amelioration of murine ITP via FcgammaRIIb is not necessarily independent of SHIP-1 and SHP-1 activity. Blood. (2004) 103:1973. doi: 10.1182/blood-2003-11-3933
123. Veri MC, Gorlatov S, Li H, Burke S, Johnson S, Stavenhagen J, 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) 121:392-404. doi: 10.1111/j.1365-2567.2007.02588.x
124. Xiang Z, Cutler AJ, Brownlie RJ, Fairfax K, Lawlor KE, Severinson E, et al. FcgammaRIIb controls bone marrow plasma cell persistence and apoptosis. Nat Immunol. (2007) 8:419-29. doi: 10.1038/ni1440
125. Vaccaro C, Zhou J, Ober RJ, Ward ES. Engineering the Fc region of immunoglobulin G to modulate in vivo antibody levels. Nat Biotechnol. (2005) 23:1283-8. doi: 10.1038/nbt1143
126. Liu L, Garcia AM, Santoro H, Zhang Y, McDonnell K, Dumont J, et al. Amelioration of experimental autoimmune myasthenia gravis in rats by neonatal FcR blockade. J Immunol. (2007) 178:5390-8. doi: 10.4049/jimmunol.178.8.5390
127. Zhang Z, Shen K, Lu W, Cole PA. The role of C-terminal tyrosine phosphorylation in the regulation of SHP-1 explored via expressed protein ligation. J Biol Chem. (2003) 278:4668-74. doi: 10.1074/jbc.M210028200
128. Jones ML, Craik JD, Gibbins JM, Poole AW. Regulation of SHP-1 tyrosine phosphatase in human platelets by serine phosphorylation at its C terminus. J Biol Chem. (2004) 279:40475-83. doi: 10.1074/jbc.M402970200
129. Camps M, Ruckle T, Ji H, Ardissone V, Rintelen F, Shaw J, et al. Blockade of PI3Kgamma suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat Med. (2005) 11:936-43. doi: 10.1038/nm1284
130. Huang Y, Li G, An L, Fan Y, Cheng X, Li X, et al. Fyn regulates multipolar-bipolar transition and neurite morphogenesis of migrating neurons in the developing neocortex. Neuroscience. (2017) 352:39-51. doi: 10.1016/j.neuroscience.2017.03.032