Human macrophages induce CD4 + Foxp3 + regulatory T cells via binding and re-release of TGF-β

Immunology and Cell Biology

Volumn 94, Issue 8, 2016, Pages 747-762

  Schmidt, Angelika ^a   Zhang, Xing Mei ^a   Joshi, Rubin N ^a   Iqbal, Shasina ^a,b   Wahlund, Casper ^a   Gabrielsson, Susanne ^a   Harris, Robert A ^a   Tegnér, Jesper ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b BIONTECH AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; IKZF4 PROTEIN; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; LYMPHOID ENHANCER FACTOR 1; MESSENGER RNA; PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; AUTACOID; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN;

ADOPTIVE TRANSFER; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EXOSOME; HUMAN; HUMAN CELL; IMMUNOTHERAPY; IN VIVO STUDY; MACROPHAGE; MACROPHAGE CULTURE; PROTEIN EXPRESSION; PROTEIN STABILITY; REGULATORY T LYMPHOCYTE; CELL POLARITY; DNA DEMETHYLATION; IMMUNOLOGY; METABOLISM;

CELL DIFFERENTIATION; CELL POLARITY; CYTOKINES; DNA DEMETHYLATION; EXOSOMES; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INFLAMMATION MEDIATORS; MACROPHAGES; PROTEIN STABILITY; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84966470659     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2016.34     Document Type: Article

References (66)

1. Harris RA. Spatial, temporal, and functional aspects of macrophages during "the good, the bad, and the ugly" phases of inflammation. Front Immunol 2014; 5: 612.
2. Sakaguchi S. Regulatory T cells: history and perspective. Methods Mol Biol 2011; 707: 3-17.
3. Pere H, Tanchot C, Bayry J, Terme M, Taieb J, Badoual C et al. Comprehensive analysis of current approaches to inhibit regulatory T cells in cancer. Oncoimmunology 2012; 1: 326-333.
4. Pillai V, Ortega SB, Wang CK, Karandikar NJ. Transient regulatory T-cells: a state attained by all activated human T-cells. Clin Immunol 2007; 123: 18-29.
5. Wang J, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Toes RE. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol 2007; 37: 129-138.
6. Miyao T, Floess S, Setoguchi R, Luche H, Fehling HJ, Waldmann H et al. Plasticity of Foxp3(+) T cells reflects promiscuous Foxp3 expression in conventional T cells but not reprogramming of regulatory T cells. Immunity 2012; 36: 262-275.
7. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 2005; 22: 329-341.
8. Fu W, Ergun A, Lu T, Hill JA, Haxhinasto S, Fassett MS et al. A multiply redundant genetic switch 'locks in' the transcriptional signature of regulatory T cells. Nat Immunol 2012; 13: 972-980.
9. Delacher M, Schreiber L, Richards DM, Farah C, Feuerer M, Huehn J. Transcriptional control of regulatory T cells. Curr Top Microbiol Immunol 2014; 381: 83-124.
10. Ohkura N, Hamaguchi M, Morikawa H, Sugimura K, Tanaka A, Ito Y et al. T cell receptor stimulation-induced epigenetic changes and Foxp3 expression are independent and complementary events required for Treg cell development. Immunity 2012; 37: 785-799.
11. Morikawa H, Ohkura N, Vandenbon A, Itoh M, Nagao-Sato S, Kawaji H et al. Differential roles of epigenetic changes and Foxp3 expression in regulatory T cell-specific transcriptional regulation. Proc Natl Acad Sci USA 2014; 111: 5289-5294.
12. Floess S, Freyer J, Siewert C, Baron U, Olek S, Polansky J et al. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol 2007; 5: e38.
13. Huehn J, Polansky JK, Hamann A. Epigenetic control of FOXP3 expression: the key to a stable regulatory T-cell lineage? Nat Rev Immunol 2009; 9: 83-89.
14. Kitagawa Y, Ohkura N, Sakaguchi S. Molecular determinants of regulatory T cell development: the essential roles of epigenetic changes. Front Immunol 2013; 4: 106.
15. Abbas AK, Benoist C, Bluestone JA, Campbell DJ, Ghosh S, Hori S et al. Regulatory T cells: recommendations to simplify the nomenclature. Nat Immunol 2013; 14: 307-308.
16. Yadav M, Stephan S, Bluestone JA. Peripherally induced tregs - role in immune homeostasis and autoimmunity. Front Immunol 2013; 4: 232.
17. Haribhai D, Lin W, Edwards B, Ziegelbauer J, Salzman NH, Carlson MR et al. A central role for induced regulatory T cells in tolerance induction in experimental colitis. J Immunol 2009; 182: 3461-3468.
18. Haribhai D, Williams JB, Jia S, Nickerson D, Schmitt EG, Edwards B et al. A requisite role for induced regulatory T cells in tolerance based on expanding antigen receptor diversity. Immunity 2011; 35: 109-122.
19. Josefowicz SZ, Niec RE, Kim HY, Treuting P, Chinen T, Zheng Y et al. Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature 2012; 482: 395-399.
20. Samstein RM, Josefowicz SZ, Arvey A, Treuting PM, Rudensky AY. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 2012; 150: 29-38.
21. Trzonkowski P, Bieniaszewska M, Juscinska J, Dobyszuk A, Krzystyniak A, Marek N et al. First-in-man clinical results of the treatment of patients with graft versus host disease with human ex vivo expanded CD4+CD25+C. Clin Immunol 2009; 133: 22-26.
22. Brunstein CG, Miller JS, Cao Q, McKenna DH, Hippen KL, Curtsinger J et al. Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: safety profile and detection kinetics. Blood 2011; 117: 1061-1070.
23. Di Ianni M, Falzetti F, Carotti A, Terenzi A, Castellino F, Bonifacio E et al. Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood 2011; 117: 3921-3928.
24. Lan Q, Fan H, Quesniaux V, Ryffel B, Liu Z, Zheng SG. Induced Foxp3(+) regulatory T cells: a potential new weapon to treat autoimmune and inflammatory diseases? J Mol Cell Biol 2012; 4: 22-28.
25. Baron U, Floess S, Wieczorek G, Baumann K, Grutzkau A, Dong J et al. DNA demethylation in the human FOXP3 locus discriminates regulatory T cells from activated FOXP3(+) conventional T cells. Eur J Immunol 2007; 37: 2378-2389.
26. Schmitt EG, Williams CB. Generation and function of induced regulatory T cells. Front Immunol 2013; 4: 152.
27. Chen Q, Kim YC, Laurence A, Punkosdy GA, Shevach EM. IL-2 controls the stability of Foxp3 expression in TGF-beta-induced Foxp3+ T cells in vivo. J Immunol 2011; 186: 6329-6337.
28. Wallberg M, Harris RA. Co-infection with Trypanosoma brucei brucei prevents experimental autoimmune encephalomyelitis in DBA/1 mice through induction of suppressor APCs. Int Immunol 2005; 17: 721-728.
29. Weber MS, Prod'homme T, Youssef S, Dunn SE, Rundle CD, Lee L et al. Type II monocytes modulate T cell-mediated central nervous system autoimmune disease. Nat Med 2007; 13: 935-943.
30. Wang Y, Wang YP, Zheng G, Lee VW, Ouyang L, Chang DH et al. Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease. Kidney Int 2007; 72: 290-299.
31. Haribhai D, Ziegelbauer J, Jia S, Upchurch K, Yan K, Schmitt EG et al. Alternatively activated macrophages boost induced regulatory T and Th17 cell responses during immunotherapy for colitis. J Immunol 2016; 196: 3305-3317.
32. Parsa R, Andresen P, Gillett A, Mia S, Zhang XM, Mayans S et al. Adoptive transfer of immunomodulatory M2 macrophages prevents type 1 diabetes in NOD mice. Diabetes 2012; 61: 2881-2892.
33. Zhang XM, Lund H, Mia S, Parsa R, Harris RA. Adoptive transfer of cytokine-induced immunomodulatory adult microglia attenuates experimental autoimmune encephalomyelitis in DBA/1 mice. Glia 2014; 62: 804-817.
34. Ma SF, Chen YJ, Zhang JX, Shen L, Wang R, Zhou JS et al. Adoptive transfer of M2 macrophages promotes locomotor recovery in adult rats after spinal cord injury. Brain Behav Immun 2015; 45: 157-170.
35. Mia S, Warnecke A, Zhang XM, Malmstrom V, Harris RA. An optimized protocol for human M2 macrophages using M-CSF and IL-4/IL-10/TGF-beta yields a dominant immunosuppressive phenotype. Scand J Immunol 2014; 79: 305-314.
36. Mahnke K, Ring S, Bedke T, Karakhanova S, Enk AH. Interaction of regulatory T cells with antigen-presenting cells in health and disease. Chem Immunol Allergy 2008; 94: 29-39.
37. Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJ, John S, Taams LS. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci USA 2007; 104: 19446-19451.
38. Pan F, Yu H, Dang EV, Barbi J, Pan X, Grosso JF et al. Eos mediates Foxp3-dependent gene silencing in CD4+ regulatory T cells. Science 2009; 325: 1142-1146.
39. Sharma MD, Huang L, Choi JH, Lee EJ, Wilson JM, Lemos H et al. An inherently bifunctional subset of Foxp3+ T helper cells is controlled by the transcription factor eos. Immunity 2013; 38: 998-1012.
40. Beyer M, Thabet Y, Muller RU, Sadlon T, Classen S, Lahl K et al. Repression of the genome organizer SATB1 in regulatory T cells is required for suppressive function and inhibition of effector differentiation. Nat Immunol 2011; 12: 898-907.
41. Lee YK, Mukasa R, Hatton RD, Weaver CT. Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol 2009; 21: 274-280.
42. Lee Y, Awasthi A, Yosef N, Quintana FJ, Xiao S, Peters A et al. Induction and molecular signature of pathogenic TH17 cells. Nat Immunol 2012; 13: 991-999.
43. Rubtsov YP, Rudensky AY. TGFbeta signalling in control of T-cell-mediated self-reactivity. Nat Rev Immunol 2007; 7: 443-453.
44. ten Dijke P, Arthur HM. Extracellular control of TGFbeta signalling in vascular development and disease. Nat Rev Mol Cell Biol 2007; 8: 857-869.
45. Travis MA, Sheppard D. TGF-beta activation and function in immunity. Annu Rev Immunol 2014; 32: 51-82.
46. Baumgartner RA, Deramo VA, Beaven MA. Constitutive and inducible mechanisms for synthesis and release of cytokines in immune cell lines. J Immunol 1996; 157: 4087-4093.
47. Cai Z, Zhang W, Li M, Yue Y, Yang F, Yu L et al. TGF-beta1 gene-modified, immature dendritic cells delay the development of inflammatory bowel disease by inducing CD4(+)Foxp3(+) regulatory T cells. Cell Mol Immunol 2010; 7: 35-43.
48. Yu L, Yang F, Jiang L, Chen Y, Wang K, Xu F et al. Exosomes with membrane-associated TGF-beta1 from gene-modified dendritic cells inhibit murine EAE independently of MHC restriction. Eur J Immunol 2013; 43: 2461-2472.
49. Wang GJ, Liu Y, Qin A, Shah SV, Deng ZB, Xiang X et al. Thymus exosomes-like particles induce regulatory T cells. J Immunol 2008; 181: 5242-5248.
50. Nguyen DG, Booth A, Gould SJ, Hildreth JE. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J Biol Chem 2003; 278: 52347-52354.
51. Gorelik L, Flavell RA. Transforming growth factor-beta in T-cell biology. Nat Rev Immunol 2002; 2: 46-53.
52. Lin JT, Martin SL, Xia L, Gorham JD. TGF-beta 1 uses distinct mechanisms to inhibit IFN-gamma expression in CD4+ T cells at priming and at recall: differential involvement of Stat4 and T-bet. J Immunol 2005; 174: 5950-5958.
53. Walker MR, Kasprowicz DJ, Gersuk VH, Benard A, Van Landeghen M, Buckner JH et al. Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+. J Clin Invest 2003; 112: 1437-1443.
54. Gavin MA, Torgerson TR, Houston E, DeRoos P, Ho WY, Stray-Pedersen A et al. Singlecell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development. Proc Natl Acad Sci USA 2006; 103: 6659-6664.
55. Allan SE, Crome SQ, Crellin NK, Passerini L, Steiner TS, Bacchetta R et al. Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol 2007; 19: 345-354.
56. Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood 2007; 110: 2983-2990.
57. Yang R, Qu C, Zhou Y, Konkel JE, Shi S, Liu Y et al. Hydrogen sulfide promotes Tet1- and Tet2-mediated Foxp3 demethylation to drive regulatory T cell differentiation and maintain immune homeostasis. Immunity 2015; 43: 251-263.
58. Yue X, Trifari S, Aijo T, Tsagaratou A, Pastor WA, Zepeda-Martinez JA et al. Control of Foxp3 stability through modulation of TET activity. J Exp Med 2016; 213: 377-397.
59. Sasidharan NV, Song MH, Oh KI. Vitamin C facilitates demethylation of the Foxp3 enhancer in a Tet-dependent manner. J Immunol 2016; 196: 2119-2131.
60. Schmitt EG, Haribhai D, Williams JB, Aggarwal P, Jia S, Charbonnier LM et al. IL-10 produced by induced regulatory T cells (iTregs) controls colitis and pathogenic ex-iTregs during immunotherapy. J Immunol 2012; 189: 5638-5648.
61. Sela U, Olds P, Park A, Schlesinger SJ, Steinman RM. Dendritic cells induce antigen-specific regulatory T cells that prevent graft versus host disease and persist in mice. J Exp Med 2011; 208: 2489-2496.
62. Komatsu N, Okamoto K, Sawa S, Nakashima T, Oh-Hora M, Kodama T et al. Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nat Med 2014; 20: 62-68.
63. Clayton A, Mitchell JP, Court J, Mason MD, Tabi Z. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res 2007; 67: 7458-7466.
64. Graner MW, Alzate O, Dechkovskaia AM, Keene JD, Sampson JH, Mitchell DA et al. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J 2009; 23: 1541-1557.
65. Wada J, Onishi H, Suzuki H, Yamasaki A, Nagai S, Morisaki T et al. Surface-bound TGF-beta1 on effusion-derived exosomes participates in maintenance of number and suppressive function of regulatory T-cells in malignant effusions. Anticancer Res 2010; 30: 3747-3757.
66. Schmidt A, Oberle N, Weiss EM, Vobis D, Frischbutter S, Baumgrass R et al. Human regulatory T cells rapidly suppress T cell receptor-induced Ca(2+), NF-kappaB, and NFAT signaling in conventional T cells. Sci Signal 2011; 4: ra90.