Critical role of all-trans retinoic acid in stabilizing human natural regulatory T cells under inflammatory conditions

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 33, 2014, Pages

  Lu, Ling ^a,b   Lan, Qin ^b,c   Li, Zhiyuan ^d   Zhou, Xiaohui ^b,c   Gu, Jian ^a,b   Li, Qiang ^b   Wang, Julie ^b   Chen, Maogen ^b   Liu, Ya ^b   Shen, Yi ^c   Brand, David D ^e   Ryffel, Bernhard ^f   Horwitz, David A ^b   Quismorio, Francisco P ^b   Liu, Zhongmin ^c   Li, Bin ^d   Olsen, Nancy J ^g   Zheng, Song Guo ^b,c,g  

^a NANJING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c First Affiliated Hospital of Fourth Military Medical University   (China)

^d INSTITUTE PASTEUR OF SHANGHAI   (China)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f UNIVERSITÉ D'ORLÉANS   (France)

^g PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

Epigenetic regulation; Epigenetics; Inflammation; Treg cells; X GVHD

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; RAPAMYCIN; RETINOIC ACID; STIP1 HOMOLOGY AND U BOX CONTAINING PROTEIN 1; TRANSCRIPTION FACTOR FOXP3; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL TRANSFORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CPG ISLAND; DRUG EFFECT; GENE LOCUS; GRAFT VERSUS HOST REACTION; HISTONE ACETYLATION; HISTONE DEMETHYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; XENOGRAFT;

EPIGENETIC REGULATION; EPIGENETICS; INFLAMMATION; TREG CELLS; X-GVHD;

BASE SEQUENCE; CYTOKINES; DNA PRIMERS; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INFLAMMATION; INTERLEUKIN-1; INTERLEUKIN-6; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, INTERLEUKIN-1; RECEPTORS, INTERLEUKIN-6; T-LYMPHOCYTES, REGULATORY; TRETINOIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84906308941     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1408780111     Document Type: Article

References (45)

1. Xu L, Kitani A, Fuss I, Strober W (2007) Cutting edge: Regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol 178(11):6725-6729. (Pubitemid 46847395)
2. Zheng SG, Wang J, Horwitz DA (2008) Cutting edge: Foxp3+CD4+CD25+ regulatory T cells induced by IL-2 and TGF-beta are resistant to Th17 conversion by IL-6. J Immunol 180(11):7112-7116.
3. Lu L, et al. (2010) Role of SMAD and non-SMAD signals in the development of Th17 and regulatory T cells. J Immunol 184(8):4295-4306.
4. Wan YY, Flavell RA (2007) Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 445(7129):766-770. (Pubitemid 46279706)
5. Huter EN, Stummvoll GH, DiPaolo RJ, Glass DD, Shevach EM (2008) Cutting edge: Antigen-specific TGF beta-induced regulatory T cells suppress Th17-mediated autoimmune disease. J Immunol 181(12):8209-8213.
6. Zhou X, et al. (2009) Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat Immunol 10(9):1000-1007.
7. Koenen HJ, et al. (2008) Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 112(6):2340-2352.
8. Beriou G, et al. (2009) IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood 113(18):4240-4249.
9. Fontenot JD, Gavin MA, Rudensky AY (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4(4):330-336. (Pubitemid 36432314)
10. Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299(5609):1057-1061. (Pubitemid 36222930)
11. Khattri R, Cox T, Yasayko SA, Ramsdell F (2003) An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol 4(4):337-342. (Pubitemid 36432315)
12. Floess S, et al. (2007) Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol 5(2):e38.
13. Huehn J, Polansky JK, Hamann A (2009) Epigenetic control of FOXP3 expression: The key to a stable regulatory T-cell lineage? Nature Rev 9(2):83-89.
14. Polansky JK, et al. (2010) Methylation matters: Binding of Ets-1 to the demethylated Foxp3 gene contributes to the stabilization of Foxp3 expression in regulatory T cells. J Mol Med (Berl) 88(10):1029-1040.
15. Morikawa H, et al.; FANTOM Consortium (2014) Differential roles of epigenetic changes and Foxp3 expression in regulatory T cell-specific transcriptional regulation. Proc Natl Acad Sci USA 111(14):5289-5294.
16. Lal G, et al. (2009) Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J Immunol 182(1):259-273.
17. Zheng Y, et al. (2010) Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 463(7282):808-812.
18. Zhou X, et al. (2010) Cutting edge: All-trans retinoic acid sustains the stability and function of natural regulatory T cells in an inflammatory milieu. J Immunol 185(5):2675-2679.
19. Golovina TN, et al. (2011) Retinoic acid and rapamycin differentially affect and synergistically promote the ex vivo expansion of natural human T regulatory cells. PLoS ONE 6(1):e15868.
20. Lan Q, et al. (2012) Induced Foxp3(+) regulatory T cells: A potential new weapon to treat autoimmune and inflammatory diseases? J Mol Cell Biol 4(1):22-28.
21. Thornton AM, et al. (2010) Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J Immunol 184(7):3433-3441.
22. Yadav M, et al. (2012) Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J Exp Med 209(10):1713-1722.
23. Weiss JM, et al. (2012) Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J Exp Med 209(10):1723-1742, S1721.
24. Hoffmann P, et al. (2009) Loss of FOXP3 expression in natural human CD4+CD25+ regulatory T cells upon repetitive in vitro stimulation. Eur J Immunol 39(4):1088-1097.
25. Imaizumi M, Breitman TR (1986) A combination of a T cell-derived lymphokine differentiation-inducing activity and a physiologic concentration of retinoic acid induces HL-60 to differentiate to cells with functional chemotactic peptide receptors. Blood 67(5):1273-1280. (Pubitemid 16080593)
26. Ito R, et al. (2009) Highly sensitive model for xenogenic GVHD using severe immunodeficient NOG mice. Transplantation 87(11):1654-1658.
27. Tran DQ, et al. (2009) Selective expression of latency-associated peptide (LAP) and IL-1 receptor type I/II (CD121a/CD121b) on activated human FOXP3+ regulatory T cells allows for their purification from expansion cultures. Blood 113(21):5125-5133.
28. + Treg cells in the inflamed CNS are insensitive to IL-6-driven IL-17 production. Eur J Immunol 42(5):1174-1179.
29. Joshi VD, et al. (2006) A role for Stat1 in the regulation of lipopolysaccharide-induced interleukin-1beta expression. J Interferon Cytokine Res 26(10):739-747. (Pubitemid 44934113)
30. Sawa S, et al. (2006) Autoimmune arthritis associated with mutated interleukin (IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+ T cells. J Exp Med 203(6):1459-1470. (Pubitemid 43877608)
31. Nguyen H, et al. (2003) IRAK-dependent phosphorylation of Stat1 on serine 727 in response to interleukin-1 and effects on gene expression. J Interferon Cytokine Res 23(4):183-192. (Pubitemid 36528981)
32. Koziczak-Holbro M, et al. (2007) IRAK-4 kinase activity is required for interleukin-1 (IL-1) receptor- and toll-like receptor 7-mediated signaling and gene expression. J Biol Chem 282(18):13552-13560. (Pubitemid 47100553)
33. Goh KC, Haque SJ, Williams BR (1999) p38 MAP kinase is required for STAT1 serine phosphorylation and transcriptional activation induced by interferons. EMBO J 18(20):5601-5608. (Pubitemid 29486379)
34. Miyao T, et al. (2012) Plasticity of Foxp3(+) T cells reflects promiscuous Foxp3 expression in conventional T cells but not reprogramming of regulatory T cells. Immunity 36(2):262-275.
35. Chen Z, et al. (2013) The ubiquitin ligase Stub1 negatively modulates regulatory T cell suppressive activity by promoting degradation of the transcription factor Foxp3. Immunity 39(2):272-285.
36. Rubtsov YP, et al. (2010) Stability of the regulatory T cell lineage in vivo. Science 329(5999):1667-1671.
37. Valencia X, et al. (2006) TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood 108(1):253-261. (Pubitemid 43990636)
38. Miyara M, et al. (2009) Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 30(6):899-911.
39. Hibbert L, Pflanz S, De Waal Malefyt R, Kastelein RA (2003) IL-27 and IFN-alpha signal via Stat1 and Stat3 and induce T-Bet and IL-12Rbeta2 in naive T cells. J Interferon Cytokine Res 23(9):513-522. (Pubitemid 37130074)
40. Iwata M, Eshima Y, Kagechika H (2003) Retinoic acids exert direct effects on T cells to suppress Th1 development and enhance Th2 development via retinoic acid receptors. Int Immunol 15(8):1017-1025. (Pubitemid 36987299)
41. Mucida D, et al. (2007) Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317(5835):256-260. (Pubitemid 47076203)
42. Lu L, et al. (2011) All-trans retinoic acid promotes TGF-β-induced Tregs via histone modification but not DNA demethylation on Foxp3 gene locus. PLoS ONE 6(9):e24590.
43. Scottà C, et al. (2013) Differential effects of rapamycin and retinoic acid on expansion, stability and suppressive qualities of human CD4(+)CD25(+)FOXP3(+) T regulatory cell subpopulations. Haematologica 98(8):1291-1299.
44. Zhou X, et al. (2010) Isolation of purified and live Foxp3+ regulatory T cells using FACS sorting on scatter plot. J Mol Cell Biol 2(3):164-169.
45. Dahl JA, Collas P (2008) A rapid micro chromatin immunoprecipitation assay (microChIP). Nat Protoc 3(6):1032-1045. (Pubitemid 351818692)