IL-10 transcription is negatively regulated by BAF180, a component of the SWI/SNF chromatin remodeling enzyme

BMC Immunology

Volumn 13, Issue , 2012, Pages

  Wurster, Andrea L ^a,d   Precht, Patricia ^a   Becker, Kevin G ^a   Wood III, William H ^a   Zhang, Yongqing ^a   Wang, Zhong ^b   Pazin, Michael J ^a,c  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARRIER TO AUTOINTEGRATION FACTOR; CHROMATIN REMODELING ENZYME; ENZYME; HISTONE; INTERLEUKIN 10; TRANSCRIPTION FACTOR SNF; UNCLASSIFIED DRUG; CYTOKINE; HELICASE; HIGH MOBILITY GROUP B PROTEIN; NONHISTONE PROTEIN; NUCLEAR PROTEIN; PBRM1 PROTEIN, MOUSE; SMARCA4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CHROMATIN; CONTROLLED STUDY; EXPERIMENTAL MOUSE; GENE DELETION; GENE EXPRESSION; GENE LOCUS; HISTONE ACETYLATION; LYMPHOID TISSUE; MOUSE; NONHUMAN; T LYMPHOCYTE; THYMUS; TRANSCRIPTION REGULATION; ANIMAL; CELL DIFFERENTIATION; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; TH2 CELL; THYMOCYTE;

ANIMALS; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; CYTOKINES; DNA HELICASES; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC LOCI; HMGB PROTEINS; INTERLEUKIN-10; MICE; NUCLEAR PROTEINS; T-LYMPHOCYTES; TH2 CELLS; THYMOCYTES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84862815386     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-13-9     Document Type: Article

References (87)

1. Lee GR, Kim ST, Spilianakis CG, Fields PE, Flavell RA. T helper cell differentiation: regulation by cis elements and epigenetics. Immunity 2006, 24(4):369-379. 10.1016/j.immuni.2006.03.007, 16618596.
2. Ansel KM, Djuretic I, Tanasa B, Rao A. Regulation of Th2 differentiation and Il4 locus accessibility. Annu Rev Immunol 2006, 24:607-656. 10.1146/annurev.immunol.23.021704.115821, 16551261.
3. Wilson CB, Rowell E, Sekimata M. Epigenetic control of T-helper-cell differentiation. Nat Rev Immunol 2009, 9(2):91-105. 10.1038/nri2487, 19151746.
4. Wurster AL, Pazin MJ. ATP-dependent chromatin remodeling in T cells. Biochemistry and cell biology = Biochimie et biologie cellulaire 2011, 10.1139/o11-042.
5. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010, 10(3):170-181. 10.1038/nri2711, 20154735.
6. Jones EA, Flavell RA. Distal enhancer elements transcribe intergenic RNA in the IL-10 family gene cluster. J Immunol 2005, 175(11):7437-7446.
7. Kang KH, Im SH. Differential regulation of the IL-10 gene in Th1 and Th2 T cells. Ann N Y Acad Sci 2005, 1050:97-107. 10.1196/annals.1313.011, 16014524.
8. Im SH, Hueber A, Monticelli S, Kang KH, Rao A. Chromatin-level regulation of the IL10 gene in T cells. J Biol Chem 2004, 279(45):46818-46825. 10.1074/jbc.M401722200, 15319439.
9. Vieira P, O'Garra A. Regula'ten' the gut. Nat Immunol 2007, 8(9):905-907. 10.1038/ni0907-905, 17712340.
10. Veldhoen M, Uyttenhove C, van Snick J, Helmby H, Westendorf A, Buer J, Martin B, Wilhelm C, Stockinger B. Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat Immunol 2008, 9(12):1341-1346. 10.1038/ni.1659, 18931678.
11. Saraiva M, Christensen JR, Veldhoen M, Murphy TL, Murphy KM, O'Garra A. Interleukin-10 production by Th1 cells requires interleukin-12-induced STAT4 transcription factor and ERK MAP kinase activation by high antigen dose. Immunity 2009, 31(2):209-219. 10.1016/j.immuni.2009.05.012, 2791889, 19646904.
12. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993, 75(2):263-274. 10.1016/0092-8674(93)80068-P, 8402911.
13. Hawrylowicz CM, O'Garra A. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat Rev Immunol 2005, 5(4):271-283. 10.1038/nri1589, 15775993.
14. Shevach EM. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 2009, 30(5):636-645. 10.1016/j.immuni.2009.04.010, 19464986.
15. Barrett JC, Clayton DG, Concannon P, Akolkar B, Cooper JD, Erlich HA, Julier C, Morahan G, Nerup J, Nierras C, et al. Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat Genet 2009, 41(6):703-707. 10.1038/ng.381, 2889014, 19430480.
16. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, Lees CW, Balschun T, Lee J, Roberts R, et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 2010, 42(12):1118-1125. 10.1038/ng.717, 21102463.
17. McGovern DP, Gardet A, Torkvist L, Goyette P, Essers J, Taylor KD, Neale BM, Ong RT, Lagace C, Li C, et al. Genome-wide association identifies multiple ulcerative colitis susceptibility loci. Nat Genet 2010, 42(4):332-337. 10.1038/ng.549, 3087600, 20228799.
18. Mizuki N, Meguro A, Ota M, Ohno S, Shiota T, Kawagoe T, Ito N, Kera J, Okada E, Yatsu K, et al. Genome-wide association studies identify IL23R-IL12RB2 and IL10 as Behcet's disease susceptibility loci. Nat Genet 2010, 42(8):703-706. 10.1038/ng.624, 20622879.
19. Flaus A, Martin DM, Barton GJ, Owen-Hughes T. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res 2006, 34(10):2887-2905. 10.1093/nar/gkl295, 1474054, 16738128.
20. Saha A, Wittmeyer J, Cairns BR. Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 2006, 7(6):437-447. 10.1038/nrm1945, 16723979.
21. Precht P, Wurster AL, Pazin MJ. The SNF2H chromatin remodeling enzyme has opposing effects on cytokine gene expression. Mol Immunol 2010, 47(11-12):2038-2046. 10.1016/j.molimm.2010.04.009, 2891439, 20471682.
22. Landry JW, Banerjee S, Taylor B, Aplan PD, Singer A, Wu C. Chromatin remodeling complex NURF regulates thymocyte maturation. Genes Dev 2011, 25(3):275-286. 10.1101/gad.2007311, 3034902, 21289071.
23. Ramirez J, Hagman J. The Mi-2/NuRD complex: a critical epigenetic regulator of hematopoietic development, differentiation and cancer. Epigenetics 2009, 4(8):532-536. 10.4161/epi.4.8.10108, 19923891.
24. Wurster AL, Pazin MJ. BRG1-mediated chromatin remodeling regulates differentiation and gene expression of T helper cells. Mol Cell Biol 2008, 28(24):7274-7285. 10.1128/MCB.00835-08, 2593447, 18852284.
25. Kaeser MD, Aslanian A, Dong MQ, Yates JR, Emerson BM. BRD7, a novel PBAF-specific SWI/SNF subunit, is required for target gene activation and repression in embryonic stem cells. J Biol Chem 2008, 283(47):32254-32263. 10.1074/jbc.M806061200, 2583284, 18809673.
26. Chi T. A BAF-centred view of the immune system. Nat Rev Immunol 2004, 4(12):965-977. 10.1038/nri1501, 15573131.
27. Wang W, Cote J, Xue Y, Zhou S, Khavari PA, Biggar SR, Muchardt C, Kalpana GV, Goff SP, Yaniv M, et al. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J 1996, 15(19):5370-5382. 452280, 8895581.
28. Wang W, Xue Y, Zhou S, Kuo A, Cairns BR, Crabtree GR. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev 1996, 10(17):2117-2130. 10.1101/gad.10.17.2117, 8804307.
29. Lemon B, Inouye C, King DS, Tjian R. Selectivity of chromatin-remodelling cofactors for ligand-activated transcription. Nature 2001, 414(6866):924-928. 10.1038/414924a, 11780067.
30. Nie Z, Xue Y, Yang D, Zhou S, Deroo BJ, Archer TK, Wang W. A specificity and targeting subunit of a human SWI/SNF family-related chromatin-remodeling complex. Mol Cell Biol 2000, 20(23):8879-8888. 10.1128/MCB.20.23.8879-8888.2000, 86543, 11073988.
31. Yan Z, Cui K, Murray DM, Ling C, Xue Y, Gerstein A, Parsons R, Zhao K, Wang W. PBAF chromatin-remodeling complex requires a novel specificity subunit, BAF200, to regulate expression of selective interferon-responsive genes. Genes Dev 2005, 19(14):1662-1667. 10.1101/gad.1323805, 1176002, 15985610.
32. Moshkin YM, Mohrmann L, van Ijcken WF, Verrijzer CP. Functional differentiation of SWI/SNF remodelers in transcription and cell cycle control. Mol Cell Biol 2007, 27(2):651-661. 10.1128/MCB.01257-06, 1800805, 17101803.
33. Lessard J, Wu JI, Ranish JA, Wan M, Winslow MM, Staahl BT, Wu H, Aebersold R, Graef IA, Crabtree GR. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 2007, 55(2):201-215. 10.1016/j.neuron.2007.06.019, 2674110, 17640523.
34. Ho L, Ronan JL, Wu J, Staahl BT, Chen L, Kuo A, Lessard J, Nesvizhskii AI, Ranish J, Crabtree GR. An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc Natl Acad Sci USA 2009, 106(13):5181-5186. 10.1073/pnas.0812889106, 2654396, 19279220.
35. Wurster AL, Precht P, Pazin MJ. NF-kappaB and BRG1 bind a distal regulatory element in the IL-3/GM-CSF locus. Molecular immunology 2011, 48(15-15):2178-2188.
36. Gao X, Tate P, Hu P, Tjian R, Skarnes WC, Wang Z. ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc Natl Acad Sci USA 2008, 105(18):6656-6661. 10.1073/pnas.0801802105, 2373334, 18448678.
37. Yan Z, Wang Z, Sharova L, Sharov AA, Ling C, Piao Y, Aiba K, Matoba R, Wang W, Ko MS. BAF250B-associated SWI/SNF chromatin-remodeling complex is required to maintain undifferentiated mouse embryonic stem cells. Stem Cells 2008, 26(5):1155-1165. 10.1634/stemcells.2007-0846, 2409195, 18323406.
38. Nagl NG, Wang X, Patsialou A, Van Scoy M, Moran E. Distinct mammalian SWI/SNF chromatin remodeling complexes with opposing roles in cell-cycle control. EMBO J 2007, 26(3):752-763. 10.1038/sj.emboj.7601541, 1794396, 17255939.
39. Gui Y, Guo G, Huang Y, Hu X, Tang A, Gao S, Wu R, Chen C, Li X, Zhou L, et al. Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat Genet 2011, 43(9):875-878. 10.1038/ng.907, 21822268.
40. Wang Z, Zhai W, Richardson JA, Olson EN, Meneses JJ, Firpo MT, Kang C, Skarnes WC, Tjian R. Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev 2004, 18(24):3106-3116. 10.1101/gad.1238104, 535920, 15601824.
41. Huang X, Gao X, Diaz-Trelles R, Ruiz-Lozano P, Wang Z. Coronary development is regulated by ATP-dependent SWI/SNF chromatin remodeling component BAF180. Dev Biol 2008, 319(2):258-266. 10.1016/j.ydbio.2008.04.020, 18508041.
42. Thompson M. Polybromo-1: the chromatin targeting subunit of the PBAF complex. Biochimie 2009, 91(3):309-319. 10.1016/j.biochi.2008.10.019, 2646799, 19084573.
43. Burrows AE, Smogorzewska A, Elledge SJ. Polybromo-associated BRG1-associated factor components BRD7 and BAF180 are critical regulators of p53 required for induction of replicative senescence. Proc Natl Acad Sci USA 2010, 107(32):14280-14285. 10.1073/pnas.1009559107, 2922604, 20660729.
44. Xia W, Nagase S, Montia AG, Kalachikov SM, Keniry M, Su T, Memeo L, Hibshoosh H, Parsons R. BAF180 is a critical regulator of p21 induction and a tumor suppressor mutated in breast cancer. Cancer Res 2008, 68(6):1667-1674. 10.1158/0008-5472.CAN-07-5276, 2915562, 18339845.
45. Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P, Davies H, Jones D, Lin ML, Teague J, et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 2011, 469(7331):539-542. 10.1038/nature09639, 3030920, 21248752.
46. Li M, Zhao H, Zhang X, Wood LD, Anders RA, Choti MA, Pawlik TM, Daniel HD, Kannangai R, Offerhaus GJ, et al. Inactivating mutations of the chromatin remodeling gene ARID2 in hepatocellular carcinoma. Nat Genet 2011, 43(9):828-829. 10.1038/ng.903, 3163746, 21822264.
47. De S, Wurster AL, Precht P, Wood WH, Becker KG, Pazin MJ. Dynamic BRG1 recruitment during T helper differentiation and activation reveals distal regulatory elements. Mol Cell Biol 2011, 31(7):1512-1527. 10.1128/MCB.00920-10, 3135292, 21262765.
48. Jung M, Ramankulov A, Roigas J, Johannsen M, Ringsdorf M, Kristiansen G, Jung K. In search of suitable reference genes for gene expression studies of human renal cell carcinoma by real-time PCR. BMC Mol Biol 2007, 8:47. 10.1186/1471-2199-8-47, 1913536, 17559644.
49. Potts RC, Zhang P, Wurster AL, Precht P, Mughal MR, Wood WH, Zhang Y, Becker KG, Mattson MP, Pazin MJ. CHD5, a Brain-Specific Paralog of Mi2 Chromatin Remodeling Enzymes, Regulates Expression of Neuronal Genes. PLoS One 2011, 6(9):e24515. 10.1371/journal.pone.0024515, 3172237, 21931736.
50. Cheadle C, Vawter MP, Freed WJ, Becker KG. Analysis of microarray data using Z score transformation. J Mol Diagn 2003, 5(2):73-81. 10.1016/S1525-1578(10)60455-2, 1907322, 12707371.
51. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98(9):5116-5121. 10.1073/pnas.091062498, 33173, 11309499.
52. Kim SY, Volsky DJ. PAGE: parametric analysis of gene set enrichment. BMC Bioinforma 2005, 6:144.
53. De S, Zhang Y, Garner JR, Wang SA, Becker KG. Disease and phenotype gene set analysis of disease-based gene expression in mouse and human. Physiol Genomics 2010, 42A(2):162-167. 10.1152/physiolgenomics.00008.2010, 2957794, 20682848.
54. Lu J, Pazin MJ, Ravid K. Properties of ets-1 binding to chromatin and its effect on platelet factor 4 gene expression. Mol Cell Biol 2004, 24(1):428-441. 10.1128/MCB.24.1.428-441.2004, 303331, 14673175.
55. Lee PP, Fitzpatrick DR, Beard C, Jessup HK, Lehar S, Makar KW, Perez-Melgosa M, Sweetser MT, Schlissel MS, Nguyen S, et al. A critical role for dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 2001, 15(5):763-774. 10.1016/S1074-7613(01)00227-8, 11728338.
56. Strobeck MW, DeCristofaro MF, Banine F, Weissman BE, Sherman LS, Knudsen ES. The BRG-1 subunit of the SWI/SNF complex regulates CD44 expression. J Biol Chem 2001, 276(12):9273-9278. 10.1074/jbc.M009747200, 11108719.
57. Wei L, Vahedi G, Sun HW, Watford WT, Takatori H, Ramos HL, Takahashi H, Liang J, Gutierrez-Cruz G, Zang C, et al. Discrete roles of STAT4 and STAT6 transcription factors in tuning epigenetic modifications and transcription during T helper cell differentiation. Immunity 2010, 32(6):840-851. 10.1016/j.immuni.2010.06.003, 2904651, 20620946.
58. Liao W, Schones DE, Oh J, Cui Y, Cui K, Roh TY, Zhao K, Leonard WJ. Priming for T helper type 2 differentiation by interleukin 2-mediated induction of interleukin 4 receptor alpha-chain expression. Nat Immunol 2008, 9(11):1288-1296. 10.1038/ni.1656, 2762127, 18820682.
59. Ernst J, Kellis M. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat Biotechnol 2010, 28(8):817-825. 10.1038/nbt.1662, 2919626, 20657582.
60. Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V, Zlobin A, Diaz MO, Scacheri PC, Harte PJ. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 2009, 136(18):3131-3141. 10.1242/dev.037127, 2730368, 19700617.
61. Jin Q, Yu LR, Wang L, Zhang Z, Kasper LH, Lee JE, Wang C, Brindle PK, Dent SY, Ge K. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27 ac in nuclear receptor transactivation. EMBO J 2011, 30(2):249-262. 10.1038/emboj.2010.318, 3025463, 21131905.
62. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci USA 2010, 107(50):21931-21936. 10.1073/pnas.1016071107, 3003124, 21106759.
63. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 2011, 470(7333):279-283. 10.1038/nature09692, 21160473.
64. Zentner GE, Tesar PJ, Scacheri PC. Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome research 2011,
65. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 2008, 40(7):897-903. 10.1038/ng.154, 2769248, 18552846.
66. Ramos YF, Hestand MS, Verlaan M, Krabbendam E, Ariyurek Y, van Galen M, van Dam H, van Ommen GJ, den Dunnen JT, Zantema A, et al. Genome-wide assessment of differential roles for p300 and CBP in transcription regulation. Nucleic Acids Res 2010, 38(16):5396-5408. 10.1093/nar/gkq184, 2938195, 20435671.
67. Sahoo A, Lee CG, Jash A, Son JS, Kim G, Kwon HK, So JS, Im SH. Stat6 and c-Jun mediate Th2 cell-specific IL-24 gene expression. J Immunol 2011, 186(7):4098-4109. 10.4049/jimmunol.1002620, 21357535.
68. Northrup DL, Zhao K. Application of ChIP-Seq and related techniques to the study of immune function. Immunity 2011, 34(6):830-842. 10.1016/j.immuni.2011.06.002, 21703538.
69. Memedula S, Belmont AS. Sequential Recruitment of HAT and SWI/SNF Components to Condensed Chromatin by VP16. Curr Biol 2003, 13(3):241-246. 10.1016/S0960-9822(03)00048-4, 12573221.
70. Hargreaves DC, Crabtree GR. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell research 2011, 21(3):396-420. 10.1038/cr.2011.32, 3110148, 21358755.
71. Ryme J, Asp P, Bohm S, Cavellan E, Farrants AK. Variations in the composition of mammalian SWI/SNF chromatin remodelling complexes. J Cell Biochem 2009, 108(3):565-576. 10.1002/jcb.22288, 19650111.
72. Biddie SC, Hager GL. Glucocorticoid receptor dynamics and gene regulation. Stress 2009, 12(3):193-205. 10.1080/10253890802506409, 19051126.
73. Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem 2009, 78:273-304. 10.1146/annurev.biochem.77.062706.153223, 19355820.
74. Ho L, Crabtree GR. Chromatin remodelling during development. Nature 2010, 463(7280):474-484. 10.1038/nature08911, 3060774, 20110991.
75. Tarakhovsky A. Tools and landscapes of epigenetics. Nat Immunol 2010, 11(7):565-568. 10.1038/ni0710-565, 20562839.
76. Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006, 442(7098):86-90.
77. Mendel I, Shevach EM. The IL-10-producing competence of Th2 cells generated in vitro is IL-4 dependent. Eur J Immunol 2002, 32(11):3216-3224. 10.1002/1521-4141(200211)32:11<3216::AID-IMMU3216>3.0.CO;2-H, 12555667.
78. Zamisch M, Tian L, Grenningloh R, Xiong Y, Wildt KF, Ehlers M, Ho IC, Bosselut R. The transcription factor Ets1 is important for CD4 repression and Runx3 up-regulation during CD8 T cell differentiation in the thymus. J Exp Med 2009, 206(12):2685-2699. 10.1084/jem.20092024, 2806616, 19917777.
79. Grenningloh R, Miaw SC, Moisan J, Graves BJ, Ho IC. Role of Ets-1 phosphorylation in the effector function of Th cells. Eur J Immunol 2008, 38(6):1700-1705. 10.1002/eji.200738112, 18465773.
80. Flowers S, Nagl NG, Beck GR, Moran E. Antagonistic roles for BRM and BRG1 SWI/SNF complexes in differentiation. J Biol Chem 2009, 284(15):10067-10075. 10.1074/jbc.M808782200, 2665061, 19144648.
81. Hendriks RW, Nawijn MC, Engel JD, van Doorninck H, Grosveld F, Karis A. Expression of the transcription factor GATA-3 is required for the development of the earliest T cell progenitors and correlates with stages of cellular proliferation in the thymus. Eur J Immunol 1999, 29(6):1912-1918. 10.1002/(SICI)1521-4141(199906)29:06<1912::AID-IMMU1912>3.0.CO;2-D, 10382753.
82. Pai SY, Truitt ML, Ting CN, Leiden JM, Glimcher LH, Ho IC. Critical roles for transcription factor GATA-3 in thymocyte development. Immunity 2003, 19(6):863-875. 10.1016/S1074-7613(03)00328-5, 14670303.
83. Prlic M, Bevan MJ. Cutting Edge: {beta}-Catenin Is Dispensable for T Cell Effector Differentiation, Memory Formation, and Recall Responses. J Immunol 2011, 187(4):1542-1546. 10.4049/jimmunol.1100907, 3150307, 21724993.
84. Weber BN, Chi AW, Chavez A, Yashiro-Ohtani Y, Yang Q, Shestova O, Bhandoola A. A critical role for TCF-1 in T-lineage specification and differentiation. Nature 2011, 476(7358):63-68. 10.1038/nature10279, 3156435, 21814277.
85. Chi TH, Wan M, Lee PP, Akashi K, Metzger D, Chambon P, Wilson CB, Crabtree GR. Sequential roles of Brg, the ATPase subunit of BAF chromatin remodeling complexes, in thymocyte development. Immunity 2003, 19(2):169-182. 10.1016/S1074-7613(03)00199-7, 12932351.
86. Ji H, Jiang H, Ma W, Johnson DS, Myers RM, Wong WH. An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat Biotechnol 2008, 26(11):1293-1300. 10.1038/nbt.1505, 2596672, 18978777.
87. Wei G, Wei L, Zhu J, Zang C, Hu-Li J, Yao Z, Cui K, Kanno Y, Roh TY, Watford WT, et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 2009, 30(1):155-167. 10.1016/j.immuni.2008.12.009, 2722509, 19144320.