Human CD4+ T-cells: A role for low-affinity Fc receptors

Frontiers in Immunology

Volumn 7, Issue JUN, 2016, Pages

  Chauhan, Anil K ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmunity; Epigenetics; Fc receptors; T lymphocytes; Toll like receptors

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FC RECEPTOR; GAMMA INTERFERON; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 6; MYELOID DIFFERENTIATION FACTOR 88; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PROTEIN KINASE SYK; RETINOBLASTOMA BINDING PROTEIN 7; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR RUNX1; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANTIGEN ANTIBODY COMPLEX; ANTIGEN PRESENTATION; AUTOIMMUNITY; BINDING AFFINITY; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CYTOKINE PRODUCTION; EFFECTOR CELL; EPIGENETICS; GENE EXPRESSION REGULATION; HUMAN; IMMUNOREGULATION; INTERNALIZATION; LYMPHOCYTE DIFFERENTIATION; MOLECULAR INTERACTION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION;

EID: 84977578814     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00215     Document Type: Review

References (75)

1. Sandor M, Lynch RG. Lymphocyte Fc receptors: the special case of T cells. Immunol Today (1993) 14:227-31. doi:10.1016/0167-5699(93)90168-K
2. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol (2008) 8:34-47. doi:10.1038/nri2206
3. Qian D, Sperling AI, Lancki DW, Tatsumi Y, Barrett TA, Bluestone JA, et al. The gamma chain of the high-affinity receptor for IgE is a major functional subunit of the T-cell antigen receptor complex in gamma delta T lymphocytes. Proc Natl Acad Sci U S A (1993) 90:11875-9. doi:10.1073/pnas.90.24.11875
4. Shores E, Flamand V, Tran T, Grinberg A, Kinet JP, Love PE. Fc epsilonRI gamma can support T cell development and function in mice lacking endogenous TCR zeta-chain. J Immunol (1997) 159:222-30.
5. Liu CP, Lin WJ, Huang M, Kappler JW, Marrack P. Development and function of T cells in T cell antigen receptor/CD3 zeta knockout mice reconstituted with Fc epsilon RI gamma. Proc Natl Acad Sci U S A (1997) 94:616-21. doi:10.1073/pnas.94.2.616
6. Chauhan AK, Moore TL. Immune complexes and late complement proteins trigger activation of Syk tyrosine kinase in human CD4(+) T cells. Clin Exp Immunol (2012) 167:235-45. doi:10.1111/j.1365-2249.2011.04505.x
7. Latour S, Chow LM, Veillette A. Differential intrinsic enzymatic activity of Syk and Zap-70 protein-tyrosine kinases. J Biol Chem (1996) 271:22782-90. doi:10.1074/jbc.271.37.22782
8. Kurosaki T, Gander I, Ravetch JV. A subunit common to an IgG Fc receptor and the T-cell receptor mediates assembly through different interactions. Proc Natl Acad Sci U S A (1991) 88:3837-41. doi:10.1073/pnas.88.9.3837
9. Arase H, Suenaga T, Arase N, Kimura Y, Ito K, Shiina R, et al. Negative regulation of expression and function of Fc gamma RIII by CD3 zeta in murine NK cells. J Immunol (2001) 166:21-5. doi:10.4049/jimmunol.166.1.21
10. 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
11. 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
12. Toong C, Adelstein S, Phan TG. Clearing the complexity: immune complexes and their treatment in lupus nephritis. Int J Nephrol Renovasc Dis (2011) 4:17-28. doi:10.2147/IJNRD.S10233
13. Moore T, Ekworomadu CO, Eko FO, MacMillan L, Ramey K, Ananaba GA, et al. Fc receptor-mediated antibody regulation of T cell immunity against intracellular pathogens. J Infect Dis (2003) 188:617-24. doi:10.1086/377134
14. Bergtold A, Desai DD, Gavhane A, Clynes R. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity (2005) 23:503-14. doi:10.1016/j.immuni.2005.09.013
15. Heesters BA, Chatterjee P, Kim YA, Gonzalez SF, Kuligowski MP, Kirchhausen T, et al. Endocytosis and recycling of immune complexes by follicular dendritic cells enhances B cell antigen binding and activation. Immunity (2013) 38:1164-75. doi:10.1016/j.immuni.2013.02.023
16. Phan TG, Green JA, Gray EE, Xu Y, Cyster JG. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat Immunol (2009) 10:786-93. doi:10.1038/ni.1745
17. 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
18. Shrivastav M, Niewold TB. Nucleic acid sensors and type I interferon production in systemic lupus erythematosus. Front Immunol (2013) 4:319. doi:10.3389/fimmu.2013.00319
19. Mills KH. TLR-dependent T cell activation in autoimmunity. Nat Rev Immunol (2011) 11:807-22. doi:10.1038/nri3095
20. Pelka K, Shibata T, Miyake K, Latz E. Nucleic acid-sensing TLRs and autoimmunity: novel insights from structural and cell biology. Immunol Rev (2016) 269:60-75. doi:10.1111/imr.12375
21. Desmet CJ, Ishii KJ. Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat Rev Immunol (2012) 12:479-91. doi:10.1038/nri3247
22. Hornung V, Latz E. Intracellular DNA recognition. Nat Rev Immunol (2010) 10:123-30. doi:10.1038/nri2690
23. Reynolds JM, Dong C. Toll-like receptor regulation of effector T lymphocyte function. Trends Immunol (2013) 34:511-9. doi:10.1016/j.it.2013.06.003
24. Bruhns P, Jonsson F. Mouse and human FcR effector functions. Immunol Rev (2015) 268:25-51. doi:10.1111/imr.12350
25. 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. doi:10.1084/jem.162.6.2089
26. Moretta L, Webb SR, Grossi CE, Lydyard PM, Cooper MD. Functional analysis of two human T-cell subpopulations: help and suppression of B-cell responses by T cells bearing receptors for IgM or IgG. J Exp Med (1977) 146:184-200. doi:10.1084/jem.146.1.184
27. Moretta L, Mingari MC, Moretta A, Fauci AS. Human lymphocyte surface markers. Semin Hematol (1982) 19:273-84.
28. Sandor M, Gajewski T, Thorson J, Kemp JD, Fitch FW, Lynch RG. CD4+ murine T cell clones that express high levels of immunoglobulin binding belong to the interleukin 4-producing T helper cell type 2 subset. J Exp Med (1990) 171:2171-6. doi:10.1084/jem.171.6.2171
29. Fridman WH, Golstein P. Immunoglobulin-binding factor present on and produced by thymus-processed lymphocytes (T cells). Cell Immunol (1974) 11:442-55. doi:10.1016/0008-8749(74)90042-2
30. Kinet JP. The gamma-zeta dimers of Fc receptors as connectors to signal transduction. Curr Opin Immunol (1992) 4:43-8. doi:10.1016/0952-7915(92)90122-U
31. Sandor M, Houlden B, Bluestone J, Hedrick SM, Weinstock J, Lynch RG. In vitro and in vivo activation of murine gamma/delta T cells induces the expression of IgA, IgM, and IgG Fc receptors. J Immunol (1992) 148:2363-9.
32. Hudrisier D, Clemenceau B, Balor S, Daubeuf S, Magdeleine E, Daeron M, et al. Ligand binding but undetected functional response of FcR after their capture by T cells via trogocytosis. J Immunol (2009) 183:6102-13. doi:10.4049/jimmunol.0900821
33. Uciechowski P, Gessner JE, Schindler R, Schmidt RE. Fc gamma RIII activation is different in CD16+ cytotoxic T lymphocytes and natural killer cells. Eur J Immunol (1992) 22:1635-8. doi:10.1002/eji.1830220643
34. Noraz N, Schwarz K, Steinberg M, Dardalhon V, Rebouissou C, Hipskind R, et al. Alternative antigen receptor (TCR) signaling in T cells derived from ZAP-70-deficient patients expressing high levels of Syk. J Biol Chem (2000) 275:15832-8. doi:10.1074/jbc. M908568199
35. Grammatikos AP, Ghosh D, Devlin A, Kyttaris VC, Tsokos GC. Spleen tyrosine kinase (Syk) regulates systemic lupus erythematosus (SLE) T cell signaling. PLoS One (2013) 8:e74550. doi:10.1371/journal.pone.0074550
36. Tan SL, Liao C, Lucas MC, Stevenson C, DeMartino JA. Targeting the SYK-BTK axis for the treatment of immunological and hematological disorders: recent progress and therapeutic perspectives. Pharmacol Ther (2013) 138:294-309. doi:10.1016/j.pharmthera.2013.02.001
37. Harding FA, McArthur JG, Gross JA, Raulet DH, Allison JP. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature (1992) 356:607-9. doi:10.1038/356607a0
38. Bour-Jordan H, Esensten JH, Martinez-Llordella M, Penaranda C, Stumpf M, Bluestone JA. Intrinsic and extrinsic control of peripheral T-cell tolerance by costimulatory molecules of the CD28/B7 family. Immunol Rev (2011) 241:180-205. doi:10.1111/j.1600-065X.2011.01011.x
39. den Braber I, Mugwagwa T, Vrisekoop N, Westera L, Mogling R, de Boer AB, et al. Maintenance of peripheral naive T cells is sustained by thymus output in mice but not humans. Immunity (2012) 36:288-97. doi:10.1016/j.immuni.2012.02.006
40. Zastepa E, Fitz-Gerald L, Hallett M, Antel J, Bar-Or A, Baranzini S, et al. Naive CD4 T-cell activation identifies MS patients having rapid transition to progressive MS. Neurology (2014) 82:681-90. doi:10.1212/WNL.0000000000000146
41. Chauhan AK, Moore TL. T cell activation by terminal complex of complement and immune complexes. J Biol Chem (2011) 286:38627-37. doi:10.1074/jbc. M111.266809
42. Bluestone JA. Mechanisms of tolerance. Immunol Rev (2011) 241:5-19. doi:10.1111/j.1600-065X.2011.01019.x
43. Chauhan AK, DiPaolo RJ, Moore TL. Generation of CD4+ follicular helper T cells by complement and immune complexes. Arthritis Rheum (2012) 64:978. doi:10.1002/art.37735
44. Cao X. Self-regulation and cross-regulation of pattern-recognition receptor signalling in health and disease. Nat Rev Immunol (2015) 16:35-50. doi:10.1038/nri.2015.8
45. Bakema JE, Tuk CW, van Vliet SJ, Bruijns SC, Vos JB, Letsiou S, et al. Antibody-opsonized bacteria evoke an inflammatory dendritic cell phenotype and polyfunctional Th cells by cross-talk between TLRs and FcRs. J Immunol (2015) 194:1856-66. doi:10.4049/jimmunol.1303126
46. 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 FcgammaRIIa in human dendritic cells. Blood (2012) 120:112-21. doi:10.1182/blood-2011-12-399931
47. van Egmond M, Vidarsson G, Bakema JE. Cross-talk between pathogen recognizing Toll-like receptors and immunoglobulin Fc receptors in immunity. Immunol Rev (2015) 268:311-27. doi:10.1111/imr.12333
48. Blasius AL, Beutler B. Intracellular toll-like receptors. Immunity (2010) 32:305-15. doi:10.1016/j.immuni.2010.03.012
49. Barton GM, Kagan JC, Medzhitov R. Intracellular localization of Toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat Immunol (2006) 7:49-56. doi:10.1038/ni1280
50. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol (2007) 8:487-96. doi:10.1038/ni1457
51. Landrigan A, Wong MT, Utz PJ. CpG and non-CpG oligodeoxynucleotides directly costimulate mouse and human CD4+ T cells through a TLR9-and MyD88-independent mechanism. J Immunol (2011) 187:3033-43. doi:10.4049/jimmunol.1003414
52. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat Rev Immunol (2006) 6:823-35. doi:10.1038/nri1957
53. Qiao Y, Giannopoulou EG, Chan CH, Park SH, Gong S, Chen J, et al. Synergistic activation of inflammatory cytokine genes by interferon-gamma-induced chromatin remodeling and toll-like receptor signaling. Immunity (2013) 39:454-69. doi:10.1016/j.immuni.2013.08.009
54. Foster SL, Hargreaves DC, Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature (2007) 447:972-8. doi:10.1038/nature05836
55. Merad M, Sathe P, Helft J, Miller J, Mortha A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol (2013) 31:563-604. doi:10.1146/annurev-immunol-020711-074950
56. Junt T, Barchet W. Translating nucleic acid-sensing pathways into therapies. Nat Rev Immunol (2015) 15:529-44. doi:10.1038/nri3875
57. Yanai H, Ban T, Wang Z, Choi MK, Kawamura T, Negishi H, et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature (2009) 462:99-103. doi:10.1038/nature08512
58. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim JY, Strassheim D, et al. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol (2006) 290:C917-24. doi:10.1152/ajpcell.00401.2005
59. Ishii KJ, Coban C, Kato H, Takahashi K, Torii Y, Takeshita F, et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol (2006) 7:40-8. doi:10.1038/ni1282
60. Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol (2015) 16:343-53. doi:10.1038/ni.3123
61. Sano H, Morimoto C. Dna isolated from DNA/anti-DNA antibody immune complexes in systemic lupus erythematosus is rich in guanine-cytosine content. J Immunol (1982) 128:1341-5.
62. Mi XB, Zeng FQ. Hypomethylation of interleukin-4 and-6 promoters in T cells from systemic lupus erythematosus patients. Acta Pharmacol Sin (2008) 29:105-12. doi:10.1111/j.1745-7254.2008.00739.x
63. Chauhan AK. Immune complexes and complement mediate epigenetic changes and trigger TLR signaling in CD4+ T cells. Ann Rheum Dis (2015) 74:194-5. doi:10.1136/annrhemdis-2015-eular.4958
64. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature (2009) 459:108-12. doi:10.1038/nature07829
65. Miao CG, Yang JT, Yang YY, Du CL, Huang C, Huang Y, et al. Critical role of DNA methylation in the pathogenesis of systemic lupus erythematosus: new advances and future challenges. Lupus (2014) 23:730-42. doi:10.1177/0961203314527365
66. Schoenborn JR, Dorschner MO, Sekimata M, Santer DM, Shnyreva M, Fitzpatrick DR, et al. Comprehensive epigenetic profiling identifies multiple distal regulatory elements directing transcription of the gene encoding interferon-gamma. Nat Immunol (2007) 8:732-42. doi:10.1038/ni1474
67. Jeffries MA, Sawalha AH. Epigenetics in systemic lupus erythematosus: leading the way for specific therapeutic agents. Int J Clin Rheumtol (2011) 6:423-39. doi:10.2217/ijr.11.32
68. Absher DM, Li X, Waite LL, Gibson A, Roberts K, Edberg J, et al. Genome-wide DNA methylation analysis of systemic lupus erythematosus reveals persistent hypomethylation of interferon genes and compositional changes to CD4+ T-cell populations. PLoS Genet (2013) 9:e1003678. doi:10.1371/journal.pgen.1003678
69. Jones B, Chen J. Inhibition of IFN-gamma transcription by site-specific methylation during T helper cell development. EMBO J (2006) 25:2443-52. doi:10.1038/sj.emboj.7601148
70. Liu CC, Ou TT, Wu CC, Li RN, Lin YC, Lin CH, et al. Global DNA methylation, DNMT1, and MBD2 in patients with systemic lupus erythematosus. Lupus (2011) 20:131-6. doi:10.1177/0961203310381517
71. Balada E, Ordi-Ros J, Serrano-Acedo S, Martinez-Lostao L, Vilardell-Tarres M. Transcript overexpression of the MBD2 and MBD4 genes in CD4+ T cells from systemic lupus erythematosus patients. J Leukoc Biol (2007) 81:1609-16. doi:10.1189/jlb.0107064
72. Boi SK, Elsawa SF. Epigentic regulation of Toll-like receptor signaling. Med Epigenet (2013) 1:19-30. doi:10.1159/000353684
73. Sullivan KE, Reddy AB, Dietzmann K, Suriano AR, Kocieda VP, Stewart M, et al. Epigenetic regulation of tumor necrosis factor alpha. Mol Cell Biol (2007) 27:5147-60. doi:10.1128/MCB.02429-06
74. Song W, Tai YT, Tian Z, Hideshima T, Chauhan D, Nanjappa P, et al. HDAC inhibition by LBH589 affects the phenotype and function of human myeloid dendritic cells. Leukemia (2011) 25:161-8. doi:10.1038/leu.2010.244
75. Quddus J, Johnson KJ, Gavalchin J, Amento EP, Chrisp CE, Yung RL, et al. Treating activated CD4+ T cells with either of two distinct DNA methyltransferase inhibitors, 5-azacytidine or procainamide, is sufficient to cause a lupus-like disease in syngeneic mice. J Clin Invest (1993) 92:38-53. doi:10.1172/JCI116576