CD32 ligation promotes the activation of CD4+T cells

Frontiers in Immunology

Volumn 9, Issue NOV, 2018, Pages

  Holgado, María Pía ^a   Sananez, Inés ^a   Raiden, Silvina ^a,b   Geffner, Jorge R ^a   Arruvito, Lourdes ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b HOSPITAL GENERAL DE NIÑOS PEDRO DE ELIZALDE   (Argentina)

Author keywords

Activation; Cytokines; Fc R; IgG; Proliferation; T cells

Indexed keywords

BASILIXIMAB; CALCIUM; CD14 ANTIGEN; CD19 ANTIBODY; CD32 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; HEPATITIS A VIRUS CELLULAR RECEPTOR 2; HLA DR ANTIGEN; IMMUNOGLOBULIN BINDING FACTOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 5; MEMBRANE ANTIGEN; MESSENGER RNA; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD3; NEUTRALIZING ANTIBODY; OKT 4; STAT5 PROTEIN; STAT6 PROTEIN; TUMOR NECROSIS FACTOR; FC RECEPTOR; FCGR2A PROTEIN, HUMAN; FCGR2B PROTEIN, HUMAN;

ADULT; ANTIGEN EXPRESSION; ARTICLE; BLOOD BUFFY COAT; CD4+ T LYMPHOCYTE; CELL AGGREGATION; CELL ISOLATION; CELL PROLIFERATION; CELL SELECTION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INFLAMMATION; LIGATION; MONOCYTE; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION; CAPPING PHENOMENON; CYTOLOGY; FEMALE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE;

ADULT; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; HUMANS; IMMUNOLOGIC CAPPING; LYMPHOCYTE ACTIVATION; MALE; RECEPTORS, IGG;

EID: 85057719462     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2018.02814     Document Type: Article

References (58)

1. Bournazos S, Chow SK, Abboud N, Casadevall A, Ravetch JV. Human IgG Fc domain engineering enhances antitoxin neutralizing antibody activity. J Clin Invest. (2014) 124:725-9. doi: 10.1172/JCI72676 PubMed Abstract | CrossRef Full Text | Google Scholar
2. 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 PubMed Abstract | CrossRef Full Text | Google Scholar
3. Amigorena S, Bonnerot C, Drake JR, Choquet D, Hunziker W, Guillet JG, et al. Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. Science (1992) 256:1808-12. PubMed Abstract | Google Scholar
4. Swanson JA, Hoppe AD. The coordination of signaling during Fc receptor-mediated phagocytosis. J Leukoc Biol. (2004) 76:1093-103. doi: 10.1189/jlb.0804439 PubMed Abstract | CrossRef Full Text | Google Scholar
5. Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV. A 13-amino-acid motif in the cytoplasmic domain of Fc gamma RIIB modulates B-cell receptor signalling. Nature (1994) 369:340. doi: 10.1038/369340a0 PubMed Abstract | CrossRef Full Text | Google Scholar
6. Ono M, Bolland S, Tempst P, Ravetch JV. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc(gamma)RIIB. Nature (1996) 383:263-6. doi: 10.1038/383263a0 PubMed Abstract | CrossRef Full Text | Google Scholar
7. Ravetch JV, Lanier LL. Immune inhibitory receptors. Science (2000) 290:84-9. doi: 10.1126/science.290.5489.84 PubMed Abstract | CrossRef Full Text | Google Scholar
8. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol. (2008) 8:34-47. doi: 10.1038/nri2206 PubMed Abstract | CrossRef Full Text | Google Scholar
9. 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 PubMed Abstract | CrossRef Full Text | Google Scholar
10. Ravetch JV, Bolland S. IgG Fc receptors. Annu Rev Immunol. (2001) 19:275-90. doi: 10.1146/annurev.immunol.19.1.275 PubMed Abstract | CrossRef Full Text | Google Scholar
11. 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 PubMed Abstract | CrossRef Full Text | Google Scholar
12. Sandor M, Lynch RG. Lymphocyte Fc receptors: The special case of T cells. Immunol Today (1993) 14:227-31. PubMed Abstract | Google Scholar
13. Chauhan AK. Human CD4(+) T-cells: A role for low-affinity fc receptors. Front Immunol. (2016) 7:215. doi: 10.3389/fimmu.2016.00215 PubMed Abstract | CrossRef Full Text | Google Scholar
14. 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) 543:564-7. doi: 10.1038/nature21710 PubMed Abstract | CrossRef Full Text | Google Scholar
15. Mantzioris BX, Berger MF, Sewell W, Zola H. Expression of the Fc receptor for IgG (Fc gamma RII/CDw32) by human circulating T and B lymphocytes. J Immunol. (1993) 150:5175-84. PubMed Abstract | Google Scholar
16. Martin GE, Pace M, Thornhill JP, Phetsouphanh C, Meyerowitz J, Gossez M, et al. CD32-expressing CD4 T cells are phenotypically diverse and can contain proviral HIV DNA. Front Immunol. (2018) 9:928. doi: 10.3389/fimmu.2018.00928 PubMed Abstract | CrossRef Full Text | Google Scholar
17. Engelhardt W, Matzke J, Schmidt RE. Activation-dependent expression of low affinity IgG receptors Fc gamma RII(CD32) and Fc gamma RIII(CD16) in subpopulations of human T lymphocytes. Immunobiology (1995) 192:297-320. PubMed Abstract | Google Scholar
18. Sandilands GP, MacPherson SA, Burnett ER, Russell AJ, Downie I, MacSween RN. Differential expression of CD32 isoforms following alloactivation of human T cells. Immunology (1997) 91:204-11. PubMed Abstract | Google Scholar
19. Sandilands GP, McLaren AP, Howie D, MacSween RN. Occult expression of CD32 (Fc gamma RII) in normal human peripheral blood mononuclear cells. Immunology (1995) 86:525-32. PubMed Abstract | Google Scholar
20. Sandilands GP, Burnett ER, MacPherson SA, Downie I, More IA, MacSween RN. Demonstration of cytoplasmic CD32 (Fc gamma RII) within human lymphocytes following microwave treatment. Immunology (1997) 90:427-34. PubMed Abstract | Google Scholar
21. 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 CrossRef Full Text | Google Scholar
22. Theofilopoulos AN, Dixon FJ. Immune complexes in human diseases: A review. Am J Pathol. (1980) 100:529-94. PubMed Abstract | Google Scholar
23. Celis E, Chang TW. HBsAg-serum protein complexes stimulate immune T lymphocytes more efficiently than do pure HBsAg. Hepatology (1984) 4:1116-23. PubMed Abstract | Google Scholar
24. Xu DZ, Huang KL, Zhao K, Xu LF, Shi N, Yuan ZH, et al. Vaccination with recombinant HBsAg-HBIG complex in healthy adults. Vaccine (2005) 23:2658-64. doi: 10.1016/j.vaccine.2004.10.040 PubMed Abstract | CrossRef Full Text | Google Scholar
25. Heyman B. Antibodies as natural adjuvants. Curr Top Microbiol Immunol. (2014) 382:201-19. doi: 10.1007/978-3-319-07911-0_9 PubMed Abstract | CrossRef Full Text | Google Scholar
26. Pelegrin M, Naranjo-Gomez M, Piechaczyk M. Antiviral monoclonal antibodies: Can they be more than simple neutralizing agents?. Trends Microbiol. (2015) 23:653-65. doi: 10.1016/j.tim.2015.07.005 PubMed Abstract | CrossRef Full Text | Google Scholar
27. Lambour J, Naranjo-Gomez M, Piechaczyk M, Pelegrin M. Converting monoclonal antibody-based immunotherapies from passive to active: Bringing immune complexes into play. Emerg Microbes Infect. (2016) 5:e92. doi: 10.1038/emi.2016.97 PubMed Abstract | CrossRef Full Text | Google Scholar
28. Wen YM, Mu L, Shi Y. Immunoregulatory functions of immune complexes in vaccine and therapy. EMBO Mol Med. (2016) 8:1120-33. doi: 10.15252/emmm.201606593 PubMed Abstract | CrossRef Full Text | Google Scholar
29. Bournazos S, Wang TT, Dahan R, Maamary J, Ravetch JV. Signaling by antibodies: Recent progress. Annu Rev Immunol. (2017) 35:285-311. doi: 10.1146/annurev-immunol-051116-052433 PubMed Abstract | CrossRef Full Text | Google Scholar
30. Maamary J, Wang TT, Tan GS, Palese P, Ravetch JV. Increasing the breadth and potency of response to the seasonal influenza virus vaccine by immune complex immunization. Proc Natl Acad Sci USA. (2017) 114:10172-7. doi: 10.1073/pnas.1707950114 PubMed Abstract | CrossRef Full Text | Google Scholar
31. van Mirre E, Breunis WB, Geissler J, Hack CE, de Boer M, Roos D, et al. Neutrophil responsiveness to IgG, as determined by fixed ratios of mRNA levels for activating and inhibitory FcgammaRII (CD32), is stable over time and unaffected by cytokines. Blood (2006) 108:584-90. doi: 10.1182/blood-2005-12-4997 PubMed Abstract | CrossRef Full Text | Google Scholar
32. Banki Z, Kacani L, Mullauer B, Wilflingseder D, Obermoser G, Niederegger H, et al. Cross-linking of CD32 induces maturation of human monocyte-derived dendritic cells via NF-kappa B signaling pathway. J Immunol. (2003) 170:3963-70. doi: 10.4049/jimmunol.170.8.3963 PubMed Abstract | CrossRef Full Text | Google Scholar
33. 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. PubMed Abstract | Google Scholar
34. de Andres B, Mueller AL, Verbeek S, Sandor M, Lynch RG. A regulatory role for Fcgamma receptors CD16 and CD32 in the development of murine B cells. Blood (1998) 92:2823-9. PubMed Abstract | Google Scholar
35. Boruchov AM, Heller G, Veri MC, Bonvini E, Ravetch JV, Young JW. Activating and inhibitory IgG Fc receptors on human DCs mediate opposing functions. J Clin Invest. (2005) 115:2914-23. doi: 10.1172/JCI24772 PubMed Abstract | CrossRef Full Text | Google Scholar
36. Avery L, Filderman J, Szymczak-Workman AL, Kane LP. Tim-3 co-stimulation promotes short-lived effector T cells, restricts memory precursors, and is dispensable for T cell exhaustion. Proc Natl Acad Sci USA. (2018) 115:2455-60. doi: 10.1073/pnas.1712107115 PubMed Abstract | CrossRef Full Text | Google Scholar
37. Roberts GM, Davies EV, Pettit EJ, Hallett MB. The timing and magnitude of Ca2+ signaling by CD32 depends on its redistribution on the cell surface. Exp Cell Res. (1997) 230:303-9. doi: 10.1006/excr.1996.3416 PubMed Abstract | CrossRef Full Text | Google Scholar
38. Arman M, Krauel K. Human platelet IgG Fc receptor FcgammaRIIA in immunity and thrombosis. J Thromb Haemost. (2015) 13:893-908. doi: 10.1111/jth.12905 PubMed Abstract | CrossRef Full Text | Google Scholar
39. Ghazizadeh S, Bolen JB, Fleit HB. Tyrosine phosphorylation and association of Syk with Fc gamma RII in monocytic THP-1 cells. Biochem J. (1995) 305(Pt 2):669-74. PubMed Abstract | Google Scholar
40. Burchill MA, Yang J, Vogtenhuber C, Blazar BR, Farrar MA. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells. J Immunol. (2007) 178:280-90. doi: 10.4049/jimmunol.178.1.280 PubMed Abstract | CrossRef Full Text | Google Scholar
41. O'Shea JJ, Paul WE. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science (2010) 327:1098-02. doi: 10.1126/science.1178334 PubMed Abstract | CrossRef Full Text | Google Scholar
42. Takai T. Roles of Fc receptors in autoimmunity. Nat Rev Immunol. (2002) 2:580-92. doi: 10.1038/nri856 PubMed Abstract | CrossRef Full Text | Google Scholar
43. Muta T, Kurosaki T, Misulovin Z, Sanchez M, Nussenzweig MC, Ravetch JV. A 13-amino-acid motif in the cytoplasmic domain of Fc gamma RIIB modulates B-cell receptor signalling. Nature (1994) 368:70-3. doi: 10.1038/368070a0 PubMed Abstract | CrossRef Full Text | Google Scholar
44. 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 PubMed Abstract | CrossRef Full Text | Google Scholar
45. Kliks S. Antibody-enhanced infection of monocytes as the pathogenetic mechanism for severe dengue illness. AIDS Res Hum Retroviruses (1990) 6:993-8. doi: 10.1089/aid.1990.6.993 PubMed Abstract | CrossRef Full Text | Google Scholar
46. Hessell AJ, Hangartner L, Hunter M, Havenith CE, Beurskens FJ, Bakker JM, et al. Fc receptor but not complement binding is important in antibody protection against HIV. Nature (2007) 449:101-4. doi: 10.1038/nature06106 CrossRef Full Text | Google Scholar
47. Monsalvo AC, Batalle JP, Lopez MF, Krause JC, Klemenc J, Hernandez JZ, et al. Severe pandemic 2009 H1N1 influenza disease due to pathogenic immune complexes. Nat Med. (2011) 17:195-9. doi: 10.1038/nm.2262 PubMed Abstract | CrossRef Full Text | Google Scholar
48. Ohyama K, Ueki Y, Kawakami A, Kishikawa N, Tamai M, Osaki M, et al. Immune complexome analysis of serum and its application in screening for immune complex antigens in rheumatoid arthritis. Clin Chem. (2011) 57:905-9. doi: 10.1373/clinchem.2010.157776 PubMed Abstract | CrossRef Full Text | Google Scholar
49. Moore TL. Immune complexes in juvenile idiopathic arthritis. Front Immunol. (2016) 7:177. doi: 10.3389/fimmu.2016.00177 PubMed Abstract | CrossRef Full Text | Google Scholar
50. Mancini I, Ferrari B, Valsecchi C, Pontiggia S, Fornili M, Biganzoli E, et al. ADAMTS13-specific circulating immune complexes as potential predictors of relapse in patients with acquired thrombotic thrombocytopenic purpura. Eur J Intern Med. (2017) 39:79-83. doi: 10.1016/j.ejim.2016.11.003 PubMed Abstract | CrossRef Full Text | Google Scholar
51. Olaru F, Dobel T, Lonsdorf AS, Oehrl S, Maas M, Enk AH, et al. Intracapillary immune complexes recruit and activate slan-expressing CD16+ monocytes in human lupus nephritis. JCI Insight (2018) 3:96492. doi: 10.1172/jci.insight.96492 PubMed Abstract | CrossRef Full Text | Google Scholar
52. Gamberale R, Geffner JR, Giordano M. Immune complexes and apoptosis in B-cell chronic lymphocytic leukemia. Leuk Lymphoma (2002) 43:251-5. doi: 10.1080/10428190290006008 PubMed Abstract | CrossRef Full Text | Google Scholar
53. Dhodapkar KM, Kaufman JL, Ehlers M, Banerjee DK, Bonvini E, Koenig S, et al. Selective blockade of inhibitory Fcgamma receptor enables human dendritic cell maturation with IL-12p70 production and immunity to antibody-coated tumor cells. Proc Natl Acad Sci USA. (2005) 102:2910-5. doi: 10.1073/pnas.0500014102 PubMed Abstract | CrossRef Full Text | Google Scholar
54. Cramer DW, O'Rourke DJ, Vitonis AF, Matulonis UA, Dijohnson DA, Sluss PM, et al. CA125 immune complexes in ovarian cancer patients with low CA125 concentrations. Clin Chem. (2010) 56:1889-92. doi: 10.1373/clinchem.2010.153122 PubMed Abstract | CrossRef Full Text | Google Scholar
55. Lanier LL, Kipps TJ, Phillips JH. Functional properties of a unique subset of cytotoxic CD3+ T lymphocytes that express Fc receptors for IgG (CD16/Leu-11 antigen). J Exp Med. (1985) 162:2089-106. PubMed Abstract | Google Scholar
56. Chauhan AK, Chen C, Moore TL, DiPaolo RJ. Induced expression of FcgammaRIIIa (CD16a) on CD4+ T cells triggers generation of IFN-gammahigh subset. J Biol Chem. (2015) 290:5127-40. doi: 10.1074/jbc.M114.599266 PubMed Abstract | CrossRef Full Text | Google Scholar
57. Chauhan AK, Moore TL, Bi Y, Chen C. FcgammaRIIIa-Syk Co-signal modulates CD4+ T-cell response and up-regulates Toll-like Receptor (TLR) expression. J Biol Chem. (2016) 291:1368-86. doi: 10.1074/jbc.M115.684795 PubMed Abstract | CrossRef Full Text | Google Scholar
58. Chauhan AK. A contribution of FcγRIIIa cosignaling in TFH subset development in Systemic Lupus Erythematosus. bioRxiv (2018) 256198:1-31. doi: 10.1101/256198 CrossRef Full Text | Google Scholar