A Distal Conserved Sequence Element Controls Ifng Gene Expression by T Cells and NK Cells

Immunity

Volumn 25, Issue 5, 2006, Pages 717-729

  Hatton, Robin D ^a   Harrington, Laurie E ^a   Luther, Rita J ^b   Wakefield, Therese ^a   Janowski, Karen M ^a   Oliver, James R ^a   Lallone, Roger L ^c   Murphy, Kenneth M ^d   Weaver, Casey T ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c Brookwood Biomedical   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CELLIMMUNO; DNA

Indexed keywords

GAMMA INTERFERON; HISTONE; T BOX TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL LINEAGE; CELLULAR IMMUNITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EXON; GENE; GENE DELETION; GENE EXPRESSION; GENE LOCATION; GENE SEQUENCE; INNATE IMMUNITY; INTERFERON GAMMA GENE; LYMPHOCYTE DIFFERENTIATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MODIFICATION; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

ANIMALS; BASE SEQUENCE; CATTLE; CELL DIFFERENTIATION; CHICKENS; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CONSERVED SEQUENCE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HISTONES; INTERFERON TYPE II; KILLER CELLS, NATURAL; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; OPOSSUMS; POLYMERASE CHAIN REACTION; RATS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; T-LYMPHOCYTES;

EID: 33846208370     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2006.09.007     Document Type: Article

References (61)

1. Agarwal S., and Rao A. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 9 (1998) 765-775
2. Ansel K.M., Lee D.U., and Rao A. An epigenetic view of helper T cell differentiation. Nat. Immunol. 4 (2003) 616-623
3. Ansel K.M., Greenwald R.J., Agarwal S., Bassing C.H., Monticelli S., Interlandi J., Djuretic I.M., Lee D.U., Sharpe A.H., Alt F.W., and Rao A. Deletion of a conserved Il4 silencer impairs T helper type 1-mediated immunity. Nat. Immunol. 5 (2004) 1251-1259
4. Ansel K.M., Djuretic I., Tanasa B., and Rao A. Regulation of Th2 differentiation and Il4 locus accessibility. Annu. Rev. Immunol. 24 (2006) 607-656
5. Avni O., Lee D., Macian F., Szabo S.J., Glimcher L.H., and Rao A. T(H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat. Immunol. 3 (2002) 643-651
6. Berenson L.S., Ota N., and Murphy K.M. Issues in T-helper 1 development-resolved and unresolved. Immunol. Rev. 202 (2004) 157-174
7. Bird J.J., Brown D.R., Mullen A.C., Moskowitz N.H., Mahowald M.A., Sider J.R., Gajewski T.F., Wang C.R., and Reiner S.L. Helper T cell differentiation is controlled by the cell cycle. Immunity 9 (1998) 229-237
8. Cartharius K., Frech K., Grote K., Klocke B., Haltmeier M., Klingenhoff A., Frisch M., Bayerlein M., and Werner T. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21 (2005) 2933-2942
9. Chang S., and Aune T.M. Histone hyperacetylated domains across the Ifng gene region in natural killer cells and T cells. Proc. Natl. Acad. Sci. USA 102 (2005) 17095-17100
10. Cho J.Y., Grigura V., Murphy T.L., and Murphy K. Identification of cooperative monomeric Brachyury sites conferring T-bet responsiveness to the proximal IFN-gamma promoter. Int. Immunol. 15 (2003) 1149-1160
11. Dermitzakis E.T., Reymond A., and Antonarakis S.E. Conserved non-genic sequences-an unexpected feature of mammalian genomes. Nat. Rev. Genet. 6 (2005) 151-157
12. Fields P.E., Kim S.T., and Flavell R.A. Cutting edge: changes in histone acetylation at the IL-4 and IFN-gamma loci accompany Th1/Th2 differentiation. J. Immunol. 169 (2002) 647-650
13. Frazer K.A., Pachter L., Poliakov A., Rubin E.M., and Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 32 (2004) W273-W279
14. Grogan J.L., Mohrs M., Harmon B., Lacy D.A., Sedat J.W., and Locksley R.M. Early transcription and silencing of cytokine genes underlie polarization of T helper cell subsets. Immunity 14 (2001) 205-215
15. Gu X., and Su Z. Web-based resources for comparative genomics. Hum. Genomics 2 (2005) 187-190
16. Guo L., Hu-Li J., Zhu J., Watson C.J., Difilippantonio M.J., Pannetier C., and Paul W.E. In TH2 cells the Il4 gene has a series of accessibility states associated with distinctive probabilities of IL-4 production. Proc. Natl. Acad. Sci. USA 99 (2002) 10623-10628
17. Henkel G., Weiss D.L., McCoy R., Deloughery T., Tara D., and Brown M.A. A DNase I-hypersensitive site in the second intron of the murine IL-4 gene defines a mast cell-specific enhancer. J. Immunol. 149 (1992) 3239-3246
18. Hsieh S., Chen N., Tarbell K., Liao N., Lai Y., Lee K., Wu S., Sytwu H., Han S., and McDevitt H. Transgenic mice expressing surface markers for IFN-gamma and IL-4 producing cells. Mol. Immunol. 37 (2000) 281-293
19. Hsu L.Y., Lauring J., Liang H.E., Greenbaum S., Cado D., Zhuang Y., and Schlissel M.S. A conserved transcriptional enhancer regulates RAG gene expression in developing B cells. Immunity 19 (2003) 105-117
20. Hwang E.S., Hong J.H., and Glimcher L.H. IL-2 production in developing Th1 cells is regulated by heterodimerization of RelA and T-bet and requires T-bet serine residue 508. J. Exp. Med. 202 (2005) 1289-1300
21. Hwang E.S., Szabo S.J., Schwartzberg P.L., and Glimcher L.H. T helper cell fate specified by kinase-mediated interaction of T-bet with GATA-3. Science 307 (2005) 430-433
22. Jones E.A., and Flavell R.A. Distal enhancer elements transcribe intergenic RNA in the IL-10 family gene cluster. J. Immunol. 175 (2005) 7437-7446
23. Kaplan M.H., Sun Y.L., Hoey T., and Grusby M.J. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382 (1996) 174-177
24. Kelly B.L., and Locksley R.M. Coordinate regulation of the IL-4, IL-13, and IL-5 cytokine cluster in Th2 clones revealed by allelic expression patterns. J. Immunol. 165 (2000) 2982-2986
25. Kubo M., Ransom J., Webb D., Hashimoto Y., Tada T., and Nakayama T. T-cell subset-specific expression of the IL-4 gene is regulated by a silencer element and STAT6. EMBO J. 16 (1997) 4007-4020
26. Lakso M., Pichel J.G., Gorman J.R., Sauer B., Okamoto Y., Lee E., Alt F.W., and Westphal H. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. USA 93 (1996) 5860-5865
27. Lee E.C., Yu D., Martinez de Velasco J., Tessarollo L., Swing D.A., Court D.L., Jenkins N.A., and Copeland N.G. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73 (2001) 56-65
28. Lee D.U., Agarwal S., and Rao A. Th2 lineage commitment and efficient IL-4 production involves extended demethylation of the IL-4 gene. Immunity 16 (2002) 649-660
29. Lee D.U., Avni O., Chen L., and Rao A. A distal enhancer in the interferon-gamma (IFN-gamma) locus revealed by genome sequence comparison. J. Biol. Chem. 279 (2004) 4802-4810
30. Lee G.R., Spilianakis C.G., and Flavell R.A. Hypersensitive site 7 of the TH2 locus control region is essential for expressing TH2 cytokine genes and for long-range intrachromosomal interactions. Nat. Immunol. 6 (2005) 42-48
31. Lee G.R., Kim S.T., Spilianakis C.G., Fields P.E., and Flavell R.A. T helper cell differentiation: regulation by cis elements and epigenetics. Immunity 24 (2006) 369-379
32. Loots G.G., Locksley R.M., Blankespoor C.M., Wang Z.E., Miller W., Rubin E.M., and Frazer K.A. Identification of a coordinate regulator of interleukins 4, 13, and 5 by cross-species sequence comparisons. Science 288 (2000) 136-140
33. McKenzie B.S., Kastelein R.A., and Cua D.J. Understanding the IL-23-IL-17 immune pathway. Trends Immunol. 27 (2006) 17-23
34. Mohrs M., Blankespoor C.M., Wang Z.E., Loots G.G., Afzal V., Hadeiba H., Shinkai K., Rubin E.M., and Locksley R.M. Deletion of a coordinate regulator of type 2 cytokine expression in mice. Nat. Immunol. 2 (2001) 842-847
35. H2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7 (1989) 145-173
36. Mostoslavsky R., Alt F.W., and Bassing C.H. Chromatin dynamics and locus accessibility in the immune system. Nat. Immunol. 4 (2003) 603-606
37. Muljo S.A., Ansel K.M., Kanellopoulou C., Livingston D.M., Rao A., and Rajewsky K. Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 202 (2005) 261-269
38. Mullen A.C., High F.A., Hutchins A.S., Lee H.W., Villarino A.V., Livingston D.M., Kung A.L., Cereb N., Yao T.P., Yang S.Y., and Reiner S.L. Role of T-bet in commitment of TH1 cells before IL-12-dependent selection. Science 292 (2001) 1907-1910
39. Mullen A.C., Hutchins A.S., High F.A., Lee H.W., Sykes K.J., Chodosh L.A., and Reiner S.L. Hlx is induced by and genetically interacts with T-bet to promote heritable T(H)1 gene induction. Nat. Immunol. 3 (2002) 652-658
40. Murali-Krishna K., Altman J.D., Suresh M., Sourdive D.J., Zajac A.J., Miller J.D., Slansky J., and Ahmed R. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8 (1998) 177-187
41. Murphy K.M., and Reiner S.L. The lineage decisions of helper T cells. Nat. Rev. Immunol. 2 (2002) 933-944
42. Pearce E.L., Mullen A.C., Martins G.A., Krawczyk C.M., Hutchins A.S., Zediak V.P., Banica M., DiCioccio C.B., Gross D.A., Mao C.A., et al. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302 (2003) 1041-1043
43. Ptacek T., and Sell S.M. A tiered approach to comparative genomics. Brief Funct. Genomic Proteomic 4 (2005) 178-185
44. Robinson D., Shibuya K., Mui A., Zonin F., Murphy E., Sana T., Hartley S.B., Menon S., Kastelein R., Bazan F., and O'Garra A. IGIF does not drive Th1 development but synergizes with IL-12 for interferon-gamma production and activates IRAK and NFkappaB. Immunity 7 (1997) 571-581
45. Santangelo S., Cousins D.J., Winkelmann N.E., and Staynov D.Z. DNA methylation changes at human Th2 cytokine genes coincide with DNase I hypersensitive site formation during CD4(+) T cell differentiation. J. Immunol. 169 (2002) 1893-1903
46. Shnyreva M., Weaver W.M., Blanchette M., Taylor S.L., Tompa M., Fitzpatrick D.R., and Wilson C.B. Evolutionarily conserved sequence elements that positively regulate IFN-gamma expression in T cells. Proc. Natl. Acad. Sci. USA 101 (2004) 12622-12627
47. Smale S.T., and Fisher A.G. Chromatin structure and gene regulation in the immune system. Annu. Rev. Immunol. 20 (2002) 427-462
48. Soutto M., Zhou W., and Aune T.M. Cutting edge: distal regulatory elements are required to achieve selective expression of IFN-gamma in Th1/Tc1 effector cells. J. Immunol. 169 (2002) 6664-6667
49. Spilianakis C.G., and Flavell R.A. Long-range intrachromosomal interactions in the T helper type 2 cytokine locus. Nat. Immunol. 5 (2004) 1017-1027
50. Spilianakis C.G., Lalioti M.D., Town T., Lee G.R., and Flavell R.A. Interchromosomal associations between alternatively expressed loci. Nature 435 (2005) 637-645
51. Szabo S.J., Gold J.S., Murphy T.L., and Murphy K.M. Identification of cis-acting regulatory elements controlling interleukin-4 gene expression in T cells: roles for NF-Y and NF-ATc. Mol. Cell. Biol. 13 (1993) 4793-4805
52. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., and Glimcher L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100 (2000) 655-669
53. Takemoto N., Koyano-Nakagawa N., Yokota T., Arai N., Miyatake S., and Arai K. Th2-specific DNase I-hypersensitive sites in the murine IL-13 and IL-4 intergenic region. Int. Immunol. 10 (1998) 1981-1985
54. Thierfelder W.E., van Deursen J.M., Yamamoto K., Tripp R.A., Sarawar S.R., Carson R.T., Sangster M.Y., Vignali D.A., Doherty P.C., Grosveld G.C., and Ihle J.N. Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature 382 (1996) 171-174
55. Weaver C.T., Harrington L.E., Mangan P.R., Gavrieli M., and Murphy K.M. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24 (2006) 677-688
56. West A.G., and Fraser P. Remote control of gene transcription. Hum. Mol. Genet. 14 Spec No 1 (2005) R101-R111
57. Yang J., Murphy T.L., Ouyang W., and Murphy K.M. Induction of interferon-gamma production in Th1 CD4+ T cells: evidence for two distinct pathways for promoter activation. Eur. J. Immunol. 29 (1999) 548-555
58. Yang J., Zhu H., Murphy T.L., Ouyang W., and Murphy K.M. IL-18-stimulated GADD45 beta required in cytokine-induced, but not TCR-induced, IFN-gamma production. Nat. Immunol. 2 (2001) 157-164
59. Young H.A., Ghosh P., Ye J., Lederer J., Lichtman A., Gerard J.R., Penix L., Wilson C.B., Melvin A.J., McGurn M.E., et al. Differentiation of the T helper phenotypes by analysis of the methylation state of the IFN-γ gene. J. Immunol. 153 (1994) 3603-3610
60. Zheng W.-P., and Flavell R.A. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89 (1997) 587-596
61. Zhu H., Yang J., Murphy T.L., Ouyang W., Wagner F., Saparov A., Weaver C.T., and Murphy K.M. Unexpected characteristics of the IFN-gamma reporters in nontransformed T cells. J. Immunol. 167 (2001) 855-865