T-cell-intrinsic Tif1α/Trim24 regulates IL-1R expression on TH2 cells and TH2 cell-mediated airway allergy

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

Volumn 113, Issue 5, 2016, Pages E568-E576

  Perez Lloret, Jimena ^a   Okoye, Isobel S ^a   Guidi, Riccardo ^a   Kannan, Yashaswini ^a   Coomes, Stephanie M ^a   Czieso, Stephanie ^a   Mengus, Gabrielle ^b   Davidson, Irwin ^b   Wilson, Mark S ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Allergy; Asthma; Inflammation; Th2; Trim24

Indexed keywords

INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; TRANSCRIPTION FACTOR; TRANSCRIPTION INTERMEDIARY FACTOR 1 REGULATOR ALPHA; TRIPARTITE MOTIF CONTAINING 24; UNCLASSIFIED DRUG; NUCLEAR PROTEIN; TRANSCRIPTIONAL INTERMEDIARY FACTOR 1;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CHIMERA; COMPUTER MODEL; CONTROLLED STUDY; DERMATOPHAGOIDES; HELMINTH; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; ANIMAL; C57BL MOUSE; GENETICS; HYPERSENSITIVITY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; HELMINTHS; HYPERSENSITIVITY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NUCLEAR PROTEINS; RECEPTORS, INTERLEUKIN-1; TH2 CELLS; TRANSCRIPTION FACTORS;

EID: 84956630653     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1522287113     Document Type: Article

References (75)

1. Olin JT, Wechsler ME (2014) Asthma: Pathogenesis and novel drugs for treatment. BMJ 349:g5517.
2. Lloyd CM, Hessel EM (2010) Functions of T cells in asthma: More than just T (H) 2 cells. Nat Rev Immunol 10(12):838-848.
3. Busse WW, et al. (2013) Randomized, double-blind, placebo-controlled study of brodalumab, a human anti-IL-17 receptor monoclonal antibody, in moderate to severe asthma. Am J Respir Crit Care Med 188(11):1294-1302.
4. Corren J, et al. (2010) A randomized, controlled, phase 2 study of AMG 317, an IL-4Ralpha antagonist, in patients with asthma. Am J Respir Crit Care Med 181(8):788-796.
5. Ortega HG, et al.; MENSA Investigators (2014) Mepolizumab treatment in patients with severe eosinophilic asthma. N Engl J Med 371(13):1198-1207.
6. Arron JR, Scheerens H, Matthews JG (2013) Redefining approaches to asthma: Developing targeted biologic therapies. Adv Pharmacol 66:1-49.
7. Zheng W, Flavell RA (1997) The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89(4):587-596.
8. Stritesky GL, et al. (2011) The transcription factor STAT3 is required for T helper 2 cell development. Immunity 34(1):39-49.
9. Kaplan MH, Schindler U, Smiley ST, Grusby MJ (1996) Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4(3):313-319.
10. Ho IC, Hodge MR, Rooney JW, Glimcher LH (1996) The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85(7):973-983.
11. Okoye IS, Wilson MS (2011) CD4+ T helper 2 cells-microbial triggers, differentiation requirements and effector functions. Immunology 134(4):368-377.
12. Sims JE, Smith DE (2010) The IL-1 family: Regulators of immunity. Nat Rev Immunol 10(2):89-102.
13. Ben-Sasson SZ, et al. (2009) IL-1 acts directly on CD4 T cells to enhance their antigendriven expansion and differentiation. Proc Natl Acad Sci USA 106(17):7119-7124.
14. Papazian D, Hansen S, Wurtzen PA (2015) Airway responses towards allergens - from the airway epithelium to T cells. Clin Exp Allergy 45(8):1268-1287.
15. Kim W, etal. (2011) Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 44(2):325-340.
16. Wagner SA, et al. (2011) A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 10(10):M111.013284.
17. Danielsen JM, et al. (2011) Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol Cell Proteomics 10(3):M110.003590.
18. Brissoni B, et al. (2006) Intracellular trafficking of interleukin-1 receptor I requires Tollip. Curr Biol 16(22):2265-2270.
19. Teague TK, et al. (1999) Activation changes the spectrum but not the diversity of genes expressed by T cells. Proc Natl Acad Sci USA 96(22):12691-12696.
20. Ozato K, Shin DM, Chang TH, Morse HC, 3rd (2008) TRIM family proteins and their emerging roles in innate immunity. Nat Rev Immunol 8(11):849-860.
21. Cammas F, Khetchoumian K, Chambon P, Losson R (2012) TRIM involvement in transcriptional regulation. Adv Exp Med Biol 770:59-76.
22. Herquel B, Ouararhni K, Davidson I (2011) The TIF1α-related TRIM cofactors couple chromatin modifications to transcriptional regulation, signaling and tumor suppression. Transcription 2(5):231-236.
23. Zhou XF, etal. (2012) TRIM28 mediates chromatin modifications at the TCRα enhancer and regulates the development of T and natural killer T cells. Proc Natl Acad Sci USA 109(49):20083-20088.
24. Cambiaghi V, et al. (2012) TRIM proteins in cancer. Adv Exp Med Biol 770:77-91.
25. Versteeg GA, Benke S, García-Sastre A, Rajsbaum R (2014) InTRIMsic immunity: Positive and negative regulation of immune signaling by tripartite motif proteins. Cytokine Growth Factor Rev 25(5):563-576.
26. Chikuma S, Suita N, Okazaki IM, Shibayama S, Honjo T (2012) TRIM28 prevents autoinflammatory T cell development in vivo. Nat Immunol 13(6):596-603.
27. Jiang S, et al. (2015) TRIM24 suppresses development of spontaneous hepatic lipid accumulation and hepatocellular carcinoma in mice. J Hepatol 62(2):371-379.
28. Khetchoumian K, et al. (2007) Loss of Trim24(Tif1alpha) gene function confers oncogenic activity to retinoic acid receptor alpha. Nat Genet 39(12):1500-1506.
29. Herquel B, et al. (2013) Trim24-repressed VL30 retrotransposons regulate gene expression by producing noncoding RNA. Nat Struct Mol Biol 20(3):339-346.
30. Tisserand J, et al. (2011) Tripartite motif 24(Trim24/Tif1a) tumor suppressor protein is a novel negative regulator of interferon (IFN)/signal transducers and activators of transcription (STAT) signaling pathway acting through retinoic acid receptor α (Rarα) inhibition. J Biol Chem 286(38):33369-33379.
31. Khetchoumian K, et al. (2008) Trim24(Tif1 alpha): An essential 'brake' for retinoic acid-induced transcription to prevent liver cancer. Cell Cycle 7(23):3647-3652.
32. Lambrecht BN, Hammad H (2015) The immunology of asthma. Nat Immunol 16(1):45-56.
33. Okoye IS, et al. (2014) Transcriptomics identified a critical role for Th2 cell-intrinsic miR-155 in mediating allergy and antihelminth immunity. Proc Natl Acad Sci USA 111(30):E3081-E3090.
34. Krämer A, Green J, Pollard J, Jr, Tugendreich S (2014) Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics 30(4):523-530.
35. Reynolds LA, Filbey KJ, Maizels RM (2012) Immunity to the model intestinal helminth parasite Heligmosomoides polygyrus. Semin Immunopathol 34(6):829-846.
36. Humphreys NE, Grencis RK (2009) IL-1-dependent, IL-1R1-independent resistance to gastrointestinal nematodes. Eur J Immunol 39(4):1036-1045.
37. Helmby H, Grencis RK (2004) Interleukin 1 plays a major role in the development of Th2-mediated immunity. Eur J Immunol 34(12):3674-3681.
38. Ritter M, et al. (2014) Functional relevance of NLRP3 inflammasome-mediated interleukin (IL)-1β during acute allergic airway inflammation. Clin Exp Immunol 178(2):212-223.
39. Broide DH, Campbell K, Gifford T, Sriramarao P (2000) Inhibition of eosinophilic inflammation in allergen-challenged, IL-1 receptor type 1-deficient mice is associated with reduced eosinophil rolling and adhesion on vascular endothelium. Blood 95(1):263-269.
40. Nakae S, et al. (2003) IL-1 is required for allergen-specific Th2 cell activation and the development of airway hypersensitivity response. Int Immunol 15(4):483-490.
41. Kopf M, et al. (1993) Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature 362(6417):245-248.
42. Torres-Padilla ME, Zernicka-Goetz M (2006) Role of TIF1alpha as a modulator of embryonic transcription in the mouse zygote. J Cell Biol 174(3):329-338.
43. Niederreither K, Remboutsika E, Gansmuller A, Losson R, Dollé P (1999) Expression of the transcriptional intermediary factor TIF1alpha during mouse development and in the reproductive organs. Mech Dev 88(1):111-117.
44. Liu X, et al. (2014) Overexpression of TRIM24 is associated with the onset and progress of human hepatocellular carcinoma. PLoS One 9(1):e85462.
45. Miao ZF, et al. (2015) TRIM24 is upregulated in human gastric cancer and promotes gastric cancer cell growth and chemoresistance. Virchows Archive: European Journal of Pathology 466(5):525-532.
46. Li H, et al. (2012) Overexpression of TRIM24 correlates with tumor progression in nonsmall cell lung cancer. PLoS One 7(5):e37657.
47. Freilich RW, Woodbury ME, Ikezu T (2013) Integrated expression profiles of mRNA and miRNA in polarized primary murine microglia. PLoS One 8(11):e79416.
48. Doisne JM, et al. (2009) iNKT cell development is orchestrated by different branches of TGF-beta signaling. J Exp Med 206(6):1365-1378.
49. Ravasi T, et al. (2010) An atlas of combinatorial transcriptional regulation in mouse and man. Cell 140(5):744-752.
50. Xue D, et al. (2015) Clinical significance and biological roles of TRIM24 in human bladder carcinoma. Tumour Biol 36(9):6849-6855.
51. Cui Z, et al. (2013) TRIM24 overexpression is common in locally advanced head and neck squamous cell carcinoma and correlates with aggressive malignant phenotypes. PLoS One 8(5):e63887.
52. Tsai WW, et al. (2010) TRIM24 links a non-canonical histone signature to breast cancer. Nature 468(7326):927-932.
53. Guiter C, et al. (2004) Constitutive STAT6 activation in primary mediastinal large B-cell lymphoma. Blood 104(2):543-549.
54. Ni Z, et al. (2002) Selective activation of members of the signal transducers and activators of transcription family in prostate carcinoma. J Urol 167(4):1859-1862.
55. Skinnider BF, et al. (2002) Signal transducer and activator of transcription 6 is frequently activated in Hodgkin and Reed-Sternberg cells of Hodgkin lymphoma. Blood 99(2):618-626.
56. Qin JZ, et al. (2001) Constitutive and interleukin-7- and interleukin-15-stimulated DNA binding of STAT and novel factors in cutaneous T cell lymphoma cells. J Invest Dermatol 117(3):583-589.
57. Pathiraja TN, et al. (2015) TRIM24 links glucose metabolism with transformation of human mammary epithelial cells. Oncogene 34(22):2836-2845.
58. Michalek RD, et al. (2011) Cutting edge: Distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol 186(6):3299-3303.
59. Thénot S, Henriquet C, Rochefort H, Cavaillès V (1997) Differential interaction of nuclear receptors with the putative human transcriptional coactivator hTIF1. J Biol Chem 272(18):12062-12068.
60. Bonds RS, Midoro-Horiuti T (2013) Estrogen effects in allergy and asthma. Curr Opin Allergy Clin Immunol 13(1):92-99.
61. Hall JA, Grainger JR, Spencer SP, Belkaid Y (2011) The role of retinoic acid in tolerance and immunity. Immunity 35(1):13-22.
62. Bishop B, Lloyd CM (2003) CC chemokine ligand 1 promotes recruitment of eosinophils but not Th2 cells during the development of allergic airways disease. J Immunol 170(9):4810-4817.
63. Schuh JM, Blease K, Hogaboam CM (2002) The role of CC chemokine receptor 5(CCR5) and RANTES/CCL5 during chronic fungal asthma in mice. FASEB J 16(2):228-230.
64. Lajoie S, et al. (2014) IL-21 receptor signalling partially mediates Th2-mediated allergic airway responses. Clin Exp Allergy 44(7):976-985.
65. Müller KM, Jaunin F, Masouyé I, Saurat JH, Hauser C (1993) Th2 cells mediate IL-4-dependent local tissue inflammation. J Immunol 150(12):5576-5584.
66. Xanthou G, et al. (2007) Osteopontin has a crucial role in allergic airway disease through regulation of dendritic cell subsets. Nat Med 13(5):570-578.
67. Corrigan CJ, et al. (2011) T-helper cell type 2(Th2) memory T cell-potentiating cytokine IL-25 has the potential to promote angiogenesis in asthma. Proc Natl Acad Sci USA 108(4):1579-1584.
68. Tamachi T, et al. (2006) IL-25 enhances allergic airway inflammation by amplifying a TH2 cell-dependent pathway in mice. J Allergy Clin Immunol 118(3):606-614.
69. Löhning M, et al. (1998) T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function. Proc Natl Acad Sci USA 95(12):6930-6935.
70. Stylianou E, et al. (1992) Interleukin 1 induces NF-kappa B through its type I but not its type II receptor in lymphocytes. J Biol Chem 267(22):15836-15841.
71. Tomar D, Singh R (2015) TRIM family proteins: Emerging class of RING E3 ligases as regulator of NF-kappaB pathway. Biol Cell 107(1):22-40.
72. Wang D, Li Y, Liu Y, Shi G (2014) The use of biologic therapies in the treatment of rheumatoid arthritis. Curr Pharm Biotechnol 15(6):542-548.
73. Palmer WS, et al. (2015) Structure-guided design of IACS-9571, a selective high-affinity dual TRIM24-BRPF1 bromodomain inhibitor. J Med Chem, 10.1021/acs.jmedchem.5b00405.
74. Bennett J, et al. (2015) Discovery of a chemical tool inhibitor targeting the bromodomains of TRIM24 and BRPF. J Med Chem, 10.1021/acs.jmedchem.5b00458.
75. Wilson MS, et al. (2005) Suppression of allergic airway inflammation by helminthinduced regulatory T cells. J Exp Med 202(9):1199-1212.