Monomeric immunoglobulin A from plasma inhibits human Th17 responses in vitro independent of FcαRI and DC-SIGN

Frontiers in Immunology

Volumn 8, Issue MAR, 2017, Pages

  Saha, Chaitrali ^a   Das, Mrinmoy ^a,b   Patil, Veerupaxagouda ^a   Stephen Victor, Emmanuel ^a,b   Sharma, Meenu ^a   Wymann, Sandra ^c   Jordi, Monika ^c   Vonarburg, Cédric ^c   Kaveri, Srini V ^a,b,d   Bayry, Jagadeesh ^a,b,d  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c ZLB Behring AG   (Switzerland)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

CD89; DC SIGN; FcaRI; IL 17; IVIG; Monomeric IgA; Natural antibodies; Th17; Treg

Indexed keywords

CD45RA ANTIGEN; CD45RO ANTIGEN; FC RECEPTOR; GAMMA INTERFERON; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTERLEUKIN 1BETA; INTERLEUKIN 21; INTERLEUKIN 6; RETINOID RELATED ORPHAN RECEPTOR GAMMA; STAT3 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; BINDING ASSAY; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; PHOSPHORYLATION; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH17 CELL;

EID: 85017231611     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00275     Document Type: Article

References (71)

1. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 cells. Annu Rev Immunol (2009) 27:485-517. doi: 10.1146/annurev.immunol.021908.132710
2. Maddur MS, Miossec P, Kaveri SV, Bayry J. Th17 cells: biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies. Am J Pathol (2012) 181:8-18. doi:10.1016/j.ajpath.2012.03.044
3. Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P. The immune geography of IgA induction and function. Mucosal Immunol (2008) 1:11-22. doi:10.1038/mi.2007.6
4. Slack E, Balmer ML, Fritz JH, Hapfelmeier S. Functional flexibility of intestinal IgA-broadening the fine line. Front Immunol (2012) 3:100. doi:10.3389/fimmu.2012.00100
5. Oortwijn BD, Roos A, van der Boog PJ, Klar-Mohamad N, van Remoortere A, Deelder AM, et al. Monomeric and polymeric IgA show a similar association with the myeloid FcalphaRI/CD89. Mol Immunol (2007) 44:966-73. doi:10.1016/j.molimm.2006.03.014
6. Monteiro R, Van De Winkel JG. IgA Fc receptors. Annu Rev Immunol (2003) 21:177-204. doi:10.1146/annurev.immunol.21.120601.141011
7. Pasquier B, Lepelletier Y, Baude C, Hermine O, Monteiro RC. Differential expression and function of IgA receptors (CD89 and CD71) during maturation of dendritic cells. J Leukoc Biol (2004) 76:1134-41. doi:10.1189/jlb.0204101
8. Geissmann F, Launay P, Pasquier B, Lepelletier Y, Leborgne M, Lehuen A, et al. A subset of human dendritic cells expresses IgA Fc receptor (CD89), which mediates internalization and activation upon cross-linking by IgA complexes. J Immunol (2001) 166:346-52. doi:10.4049/jimmunol.166.1.346
9. 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
10. 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
11. 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
12. 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
13. Watanabe T, Kanamaru Y, Liu C, Suzuki Y, Tada N, Okumura K, et al. Negative regulation of inflammatory responses by immunoglobulin A receptor (FcalphaRI) inhibits the development of toll-like receptor-9 signalling-accelerated glomerulonephritis. Clin Exp Immunol (2011) 166:235-50. doi:10.1111/j.1365-2249.2011.04452.x
14. Wehrli M, Cortinas-Elizondo F, Hlushchuk R, Daudel F, Villiger PM, Miescher S, et al. Human IgA Fc receptor FcalphaRI (CD89) triggers different forms of neutrophil death depending on the inflammatory microenvironment. J Immunol (2014) 193:5649-59. doi:10.4049/jimmunol.1400028
15. Sudo M, Miyaji K, Spath PJ, Morita-Matsumoto K, Yamaguchi Y, Yuki N. Polyclonal IgM and IgA block in vitro complement deposition mediated by anti-ganglioside antibodies in autoimmune neuropathies. Int Immunopharmacol (2016) 40:11-5. doi:10.1016/j.intimp.2016.08.019
16. Ben Mkaddem S, Rossato E, Heming N, Monteiro RC. Anti-inflammatory role of the IgA Fc receptor (CD89): from autoimmunity to therapeutic perspectives. Autoimmun Rev (2013) 12:666-9. doi:10.1016/j.autrev.2012.10.011
17. Maddur MS, Sharma M, Hegde P, Stephen-Victor E, Pulendran B, Kaveri SV, et al. Human B cells induce dendritic cell maturation and favour Th2 polarization by inducing OX-40 ligand. Nat Commun (2014) 5:4092. doi:10.1038/ncomms5092
18. Yang L, Anderson DE, Baecher-Allan C, Hastings WD, Bettelli E, Oukka M, et al. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature (2008) 454:350-2. doi:10.1038/nature07021
19. Gilardin L, Bayry J, Kaveri SV. Intravenous immunoglobulin as clinical immune-modulating therapy. CMAJ (2015) 187:257-64. doi:10.1503/cmaj.130375
20. Arnson Y, Shoenfeld Y, Amital H. Intravenous immunoglobulin therapy for autoimmune diseases. Autoimmunity (2009) 42:553-60. doi:10.1080/08916930902785363
21. Gelfand EW. Intravenous immune globulin in autoimmune and inflammatory diseases. N Engl J Med (2012) 367:2015-25. doi:10.1056/NEJMra1009433
22. Shopsin B, Kaveri SV, Bayry J. Tackling difficult Staphylococcus aureus infections: antibodies show the way. Cell Host Microbe (2016) 20:555-7. doi:10.1016/j.chom.2016.10.018
23. Seite JF, Shoenfeld Y, Youinou P, Hillion S. What is the contents of the magic draft IVIg? Autoimmun Rev (2008) 7:435-9. doi:10.1016/j.autrev.2008.04.012
24. Maddur MS, Vani J, Hegde P, Lacroix-Desmazes S, Kaveri SV, Bayry J. Inhibition of differentiation, amplification, and function of human TH17 cells by intravenous immunoglobulin. J Allergy Clin Immunol (2011) 127:823-30. doi:10.1016/j.jaci.2010.12.1102
25. Maddur MS, Kaveri SV, Bayry J. Comparison of different IVIg preparations on IL-17 production by human Th17 cells. Autoimmun Rev (2011) 10:809-10. doi:10.1016/j.autrev.2011.02.007
26. Othy S, Hegde P, Topçu S, Sharma M, Maddur MS, Lacroix-Desmazes S, et al. Intravenous gammaglobulin inhibits encephalitogenic potential of pathogenic T cells and interferes with their trafficking to the central nervous system, implicating sphingosine-1 phosphate receptor 1-mammalian target of rapamycin axis. J Immunol (2013) 190:4535-41. doi:10.4049/jimmunol.1201965
27. Lee SY, Jung YO, Ryu JG, Kang CM, Kim EK, Son HJ, et al. Intravenous immunoglobulin attenuates experimental autoimmune arthritis by inducing reciprocal regulation of Th17 and Treg cells in an interleukin-10-dependent manner. Arthritis Rheumatol (2014) 66:1768-78. doi:10.1002/art.38627
28. Maddur MS, Rabin M, Hegde P, Bolgert F, Guy M, Vallat JM, et al. Intravenous immunoglobulin exerts reciprocal regulation of Th1/Th17 cells and regulatory T cells in Guillain-Barre syndrome patients. Immunol Res (2014) 60:320-9. doi:10.1007/s12026-014-8580-6
29. Guo MM, Tseng WN, Ko CH, Pan HM, Hsieh KS, Kuo HC. Th17-and Treg-related cytokine and mRNA expression are associated with acute and resolving Kawasaki disease. Allergy (2015) 70:310-8. doi:10.1111/all.12558
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. Schwartz-Albiez R, Monteiro R, Rodriguez M, Binder C, Shoenfeld Y. Natural antibodies, intravenous immunoglobulin and their role in autoimmunity, cancer and inflammation. Clin Exp Immunol (2009) 158:43-50. doi:10.1111/j.1365-2249.2009.04026.x
32. Le Pottier L, Bendaoud B, Dueymes M, Daridon C, Youinou P, Shoenfeld Y, et al. BAFF, a new target for intravenous immunoglobulin in autoimmunity and cancer. J Clin Immunol (2007) 27:257-65. doi:10.1007/s10875-007-9082-2
33. von Gunten S, Simon HU. Natural anti-Siglec autoantibodies mediate potential immunoregulatory mechanisms: implications for the clinical use of intravenous immunoglobulins (IVIg). Autoimmun Rev (2008) 7:453-6. doi:10.1016/j.autrev.2008.03.015
34. Bouhlal H, Martinvalet D, Teillaud JL, Fridman C, Kazatchkine MD, Bayry J, et al. Natural autoantibodies to Fcgamma receptors in intravenous immunoglobulins. J Clin Immunol (2014) 34(Suppl 1):S4-11. doi:10.1007/s10875-014-0019-2
35. Stephen-Victor E, Sharma VK, Das M, Karnam A, Saha C, Lecerf M, et al. IL-1β, but not programed death-1 and programed death ligand pathway, is critical for the human Th17 response to Mycobacterium tuberculosis. Front Immunol (2016) 7:465. doi:10.3389/fimmu.2016.00465
36. Monteiro RC. The role of IgA and IgA Fc receptors as anti-inflammatory agents. J Clin Immunol (2010) 30(Suppl 1):S61-4. doi:10.1007/s10875-010-9397-2
37. Van Epps DE, Williams RC Jr. Suppression of leukocyte chemotaxis by human IgA myeloma components. J Exp Med (1976) 144:1227-42. doi:10.1084/jem.144.5.1227
38. Van Epps DE, Reed K, Williams RC Jr. Suppression of human PMN bactericidal activity by human IgA paraproteins. Cell Immunol (1978) 36:363-76. doi:10.1016/0008-8749(78)90280-0
39. Wilton JM. Suppression by IgA of IgG-mediated phagocytosis by human polymorphonuclear leucocytes. Clin Exp Immunol (1978) 34:423-8.
40. Wolf HM, Fischer MB, Puhringer H, Samstag A, Vogel E, Eibl MM. Human serum IgA downregulates the release of inflammatory cytokines (tumor necrosis factor-alpha, interleukin-6) in human monocytes. Blood (1994) 83:1278-88.
41. Nikolova EB, Russell MW. Dual function of human IgA antibodies: inhibition of phagocytosis in circulating neutrophils and enhancement of responses in IL-8-stimulated cells. J Leukoc Biol (1995) 57:875-82.
42. Wolf HM, Hauber I, Gulle H, Samstag A, Fischer MB, Ahmad RU, et al. Anti-inflammatory properties of human serum IgA: induction of IL-1 receptor antagonist and Fc alpha R (CD89)-mediated down-regulation of tumour necrosis factor-alpha (TNF-alpha) and IL-6 in human monocytes. Clin Exp Immunol (1996) 105:537-43. doi:10.1046/j.1365-2249.1996.d01-793.x
43. Olas K, Butterweck H, Teschner W, Schwarz HP, Reipert B. Immunomodulatory properties of human serum immunoglobulin A: anti-inflammatory and pro-inflammatory activities in human monocytes and peripheral blood mononuclear cells. Clin Exp Immunol (2005) 40:478-90. doi:10.1111/j.1365-2249.2005.02779.x
44. Pilette C, Detry B, Guisset A, Gabriels J, Sibille Y. Induction of interleukin-10 expression through Fcalpha receptor in human monocytes and monocyte-derived dendritic cells: role of p38 MAPKinase. Immunol Cell Biol (2010) 88:486-93. doi:10.1038/icb.2009.120
45. Heystek HC, Moulon C, Woltman AM, Garonne P, van Kooten C. Human immature dendritic cells efficiently bind and take up secretory IgA without the induction of maturation. J Immunol (2002) 168:102-7. doi:10.4049/jimmunol.168.1.102
46. Baumann J, Park CG, Mantis NJ. Recognition of secretory IgA by DC-SIGN: implications for immune surveillance in the intestine. Immunol Lett (2010) 131:59-66. doi:10.1016/j.imlet.2010.03.005
47. Yang J, Sundrud MS, Skepner J, Yamagata T. Targeting Th17 cells in autoimmune diseases. Trends Pharmacol Sci (2014) 35:493-500. doi:10.1016/j.tips.2014.07.006
48. Kim DJ, Lee SK, Kim JY, Na BJ, Hur SE, Lee M, et al. Intravenous immunoglobulin G modulates peripheral blood Th17 and Foxp3(+) regulatory T cells in pregnant women with recurrent pregnancy loss. Am J Reprod Immunol (2014) 71:441-50. doi:10.1111/aji.12208
49. Li S, Jin T, Zhang HL, Yu H, Meng F, Concha Quezada H, et al. Circulating Th17, Th22, and Th1 cells are elevated in the Guillain-Barre syndrome and downregulated by IVIg treatments. Mediators Inflamm (2014) 2014:740947. doi:10.1155/2014/740947
50. Figueiredo CA, Drohomyrecky PC, McCarthy SD, Leontyev D, Ma XZ, Branch DR, et al. Optimal attenuation of experimental autoimmune encephalomyelitis by intravenous immunoglobulin requires an intact interleukin-11 receptor. PLoS One (2014) 9:e101947. doi:10.1371/journal.pone.0101947
51. Hirota K, Turner JE, Villa M, Duarte JH, Demengeot J, Steinmetz OM, et al. Plasticity of Th17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses. Nat Immunol (2013) 14:372-9. doi:10.1038/ni.2552
52. Cao AT, Yao S, Gong B, Nurieva RI, Elson CO, Cong Y. Interleukin (IL)-21 promotes intestinal IgA response to microbiota. Mucosal Immunol (2015) 8:1072-82. doi:10.1038/mi.2014.134
53. Christensen D, Mortensen R, Rosenkrands I, Dietrich J, Andersen P. Vaccine-induced Th17 cells are established as resident memory cells in the lung and promote local IgA responses. Mucosal Immunol (2017) 10:260-70. doi:10.1038/mi.2016.28
54. Mitsdoerffer M, Lee Y, Jager A, Kim HJ, Korn T, Kolls JK, et al. Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc Natl Acad Sci U S A (2010) 107:14292-7. doi:10.1073/pnas.1009234107
55. Schwartz-Albiez R, Laban S, Eichmuller S, Kirschfink M. Cytotoxic natural antibodies against human tumours: an option for anti-cancer immunotherapy? Autoimmun Rev (2008) 7:491-5. doi:10.1016/j.autrev.2008.03.012
56. Ehrenstein MR, Notley CA. The importance of natural IgM: scavenger, protector and regulator. Nat Rev Immunol (2010) 10:778-86. doi:10.1038/nri2849
57. Kaveri SV, Silverman GJ, Bayry J. Natural IgM in immune equilibrium and harnessing their therapeutic potential. J Immunol (2012) 188:939-45. doi:10.4049/jimmunol.1102107
58. Grönwall C, Vas J, Silverman G. Protective roles of natural IgM antibodies. Front Immunol (2012) 3:66. doi:10.3389/fimmu.2012.00066
59. Tsiantoulas D, Gruber S, Binder C. B-1 cell immunoglobulin directed against oxidation-specific epitopes. Front Immunol (2013) 3:415. doi:10.3389/fimmu.2012.00415
60. Kohler H, Bayry J, Kaveri SV. The homophilic domain-an immunological archetype. Front Immunol (2016) 7:106. doi:10.3389/fimmu.2016.00106
61. Rothstein T. Natural antibodies as rheostats for susceptibility to chronic diseases in the aged. Front Immunol (2016) 7:127. doi:10.3389/fimmu.2016.00127
62. Baumgarth N. B-1 cell heterogeneity and the regulation of natural and antigen-induced IgM production. Front Immunol (2016) 7:324. doi:10.3389/fimmu.2016.00324
63. Lobo PI. Role of natural autoantibodies and natural IgM anti-leucocyte autoantibodies in health and disease. Front Immunol (2016) 7:198. doi:10.3389/fimmu.2016.00198
64. Gunti S, Messer RJ, Xu C, Yan M, Coleman WG Jr, Peterson KE, et al. Stimulation of toll-like receptors profoundly influences the titer of polyreactive antibodies in the circulation. Sci Rep (2015) 5:15066. doi:10.1038/srep15066
65. Kaveri SV. Intravenous immunoglobulin: exploiting the potential of natural antibodies. Autoimmun Rev (2012) 11:792-4. doi:10.1016/j.autrev.2012.02.006
66. Holland M, Yagi H, Takahashi N, Kato K, Savage CO, Goodall DM, et al. Differential glycosylation of polyclonal IgG, IgG-Fc and IgG-Fab isolated from the sera of patients with ANCA-associated systemic vasculitis. Biochim Biophys Acta (2006) 1760:669-77. doi:10.1016/j.bbagen.2005.11.021
67. Monteiro RC. Role of IgA and IgA fc receptors in inflammation. J Clin Immunol (2010) 30:1-9. doi:10.1007/s10875-009-9338-0
68. Mestecky J, Tomana M, Moldoveanu Z, Julian BA, Suzuki H, Matousovic K, et al. Role of aberrant glycosylation of IgA1 molecules in the pathogenesis of IgA nephropathy. Kidney Blood Press Res (2008) 31:29-37. doi:10.1159/000112922
69. Mattu TS, Pleass RJ, Willis AC, Kilian M, Wormald MR, Lellouch AC, et al. The glycosylation and structure of human serum IgA1, Fab, and Fc regions and the role of N-glycosylation on Fca receptor interactions. J Biol Chem (1998) 273:2260-72. doi:10.1074/jbc.273.4.2260
70. Othy S, Topcu S, Saha C, Kothapalli P, Lacroix-Desmazes S, Kasermann F, et al. Sialylation may be dispensable for reciprocal modulation of helper T cells by intravenous immunoglobulin. Eur J Immunol (2014) 44:2059-63. doi:10.1002/eji.201444440
71. Engert A, Balduini C, Brand A, Coiffier B, Cordonnier C, Dohner H, et al. The European hematology association roadmap for european hematology research: a consensus document. Haematologica (2016) 101:115-208. doi:10.3324/haematol.2015.136739