Dynamic changes in chromatin conformation at the TNF transcription start site in T helper lymphocyte subsets

European Journal of Immunology

Volumn 44, Issue 1, 2014, Pages 251-264

  Shebzukhov, Yury V ^a   Horn, Katharina ^a   Brazhnik, Kristina I ^a,b   Drutskaya, Marina S ^b,c   Kuchmiy, Anna A ^a,b   Kuprash, Dmitry V ^b,c   Nedospasov, Sergei A ^a,b,c  

^a Leibniz Institute   (Germany)

^b ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Chromatin conformation; T lymphocyte; Th cells; TNF; Transcription start site

Indexed keywords

BINDING PROTEIN; MICROCOCCAL NUCLEASE; PROTEIN C JUN; RESTRICTION ENDONUCLEASE; TRANSCRIPTION FACTOR NFAT; TUMOR NECROSIS FACTOR; CHROMATIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONFORMATION; CONTROLLED STUDY; GENE EXPRESSION; HELPER CELL; IMMUNE SYSTEM; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROMOTER REGION; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; TRANSCRIPTION INITIATION SITE; ANIMAL; C57BL MOUSE; CELL LINE; CHROMATIN; GENETICS; IMMUNOLOGY; METABOLISM; PROTEIN CONFORMATION; T LYMPHOCYTE SUBPOPULATION; TUMOR MICROENVIRONMENT;

ANIMALS; CELL LINE; CELLULAR MICROENVIRONMENT; CHROMATIN; MICE; MICE, INBRED C57BL; MICROCOCCAL NUCLEASE; PROMOTER REGIONS, GENETIC; PROTEIN CONFORMATION; PROTO-ONCOGENE PROTEINS C-JUN; T-LYMPHOCYTE SUBSETS; TH1 CELLS; TH17 CELLS; TRANSCRIPTION INITIATION SITE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84892456099     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201243297     Document Type: Article

References (108)

1. Shebzukhov, Y. and Kuprash, D., Transcriptional regulation of TNF/LT locus in immune cells. Mol. Biol. (Mosk.) 2011. 45: 47-57.
2. Falvo, J. V., Tsytsykova, A. V. and Goldfeld, A. E., Transcriptional control of the TNF gene. Curr. Dir. Autoimmun. 2010. 11: 27-60.
3. Anolik, J. H., Ravikumar, R., Barnard, J., Owen, T., Almudevar, A., Milner, E. C. B., Miller, C. H. et al., Cutting edge: anti-tumor necrosis factor therapy in rheumatoid arthritis inhibits memory B lymphocytes via effects on lymphoid germinal centers and follicular dendritic cell networks. J. Immunol. 2008. 180: 688-692.
4. Körner, H., Cook, M., Riminton, D. S., Lemckert, F. A., Hoek, R. M., Ledermann, B., Köntgen, F. et al., Distinct roles for lymphotoxin-α and tumor necrosis factor in organogenesis and spatial organization of lymphoid tissue. Eur. J. Immunol. 1997. 27: 2600-2609.
5. Kruglov, A. A., Kuchmiy, A., Grivennikov, S. I., Tumanov, A. V., Kuprash, D. V. and Nedospasov, S. A., Physiological functions of tumor necrosis factor and the consequences of its pathologic overexpression or blockade: Mouse models. Cytokine Growth Factor Rev. 2008. 19: 231-244.
6. Kuprash, D. V., Tumanov, A. V., Liepinsh, D. J., Koroleva, E. P., Drutskaya, M. S., Kruglov, A. A., Shakhov, A. N. et al., Novel tumor necrosis factor-knockout mice that lack Peyer's patches. Eur. J. Immunol. 2005. 35: 1592-1600.
7. Marino, M. W., Dunn, A., Grail, D., Inglese, M., Noguchi, Y., Richards, E., Jungbluth, A. et al., Characterization of tumor necrosis factor-deficient mice. Proc. Natl. Acad. Sci. USA 1997. 94: 8093-8098.
8. Pasparakis, M., Alexopoulou, L., Episkopou, V. and Kollias, G., Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J. Exp. Med. 1996. 184: 1397-1411.
9. Grivennikov, S. I., Tumanov, A. V., Liepinsh, D. J., Kruglov, A. A., Marakusha, B. I., Shakhov, A. N., Murakami, T. et al., Distinct and nonredundant in vivo functions of TNF produced by t cells and macrophages/neutrophils: protective and deleterious effects. Immunity 2005. 22: 93-104.
10. Kruglov, A. A., Lampropoulou, V., Fillatreau, S. and Nedospasov, S. A., Pathogenic and protective functions of TNF in neuroinflammation are defined by its expression in T lymphocytes and myeloid cells. J. Immunol. 2011. 187: 5660-5670.
11. Tumanov, A. V., Grivennikov, S. I., Kruglov, A. A., Shebzukhov, Y. V., Koroleva, E. P., Piao, Y., Cui, C. Y. et al., Cellular source and molecular form of TNF specify its distinct functions in organization of secondary lymphoid organs. Blood 2010. 116: 3456-3464.
12. Hargreaves, D. C., Horng, T. and Medzhitov, R., Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 2009. 138: 129-145.
13. Ramirez-Carrozzi, V. R., Braas, D., Bhatt, D. M., Cheng, C. S., Hong, C., Doty, K. R., Black, J. C. et al., A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 2009. 138: 114-128.
14. Tumanov, A. V., Nedospasov, S. A. and Turetskaia, R. L., Chromatin organization in the tumor necrosis factor/lymphotoxin gene locus: correlation with tissue-specific expression. Mol. Biol. (Mosk.) 1998. 32: 98-102.
15. Barthel, R. and Goldfeld, A. E., T cell-specific expression of the human TNF-alpha gene involves a functional and highly conserved chromatin signature in intron 3. J. Immunol. 2003. 171: 3612-3619.
16. Espel, E., Garcia-Sanz, J. A., Aubert, V., Menoud, V., Sperisen, P., Fernández, N. and Spertini, F., Transcriptional and translational control of TNF-α gene expression in human monocytes by major histocompatibility complex class II ligands. Eur. J. Immunol. 1996. 26: 2417-2424.
17. Kuhnert, P., Peterhans, E. and Pauli, U., Chromatin structure and DNase I hypersensitivity in the transcriptionally active and inactive porcine tumor necrosis factor gene locus. Nucleic Acids Res. 1992. 20: 1943-1948.
18. Ramirez-Carrozzi, V. R., Nazarian, A. A., Li, C. C., Gore, S. L., Sridharan, R., Imbalzano, A. N. and Smale, S. T., Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev. 2006. 20: 282-296.
19. Skoog, T., Hamsten, A. and Eriksson, P., Allele-specific chromatin remodeling of the tumor necrosis factor-α promoter. Biochem. Biophys. Res. Commun. 2006. 351: 777-783.
20. Sung, S. J., Walters, J. A., Hudson, J. and Gimble, J. M., Tumor necrosis factor-alpha mRNA accumulation in human myelomonocytic cell lines. Role of transcriptional regulation by DNA sequence motifs and mRNA stabilization. J. Immunol. 1991. 147: 2047-2054.
21. Taylor, J. M., Wicks, K., Vandiedonck, C. and Knight, J. C., Chromatin profiling across the human tumour necrosis factor gene locus reveals a complex, cell type-specific landscape with novel regulatory elements. Nucleic Acids Res. 2008. 36: 4845-4862.
22. Biglione, S., Tsytsykova, A. V. and Goldfeld, A. E., Monocyte-specific accessibility of a matrix attachment region in the tumor necrosis factor locus. J. Biol. Chem. 2011. 286: 44126-44133.
23. Chiang, E. Y., Kolumam, G. A., Yu, X., Francesco, M., Ivelja, S., Peng, I., Gribling, P. et al., Targeted depletion of lymphotoxin-alpha-expressing TH1 and TH17 cells inhibits autoimmune disease. Nat. Med. 2009. 15: 766-773.
24. Tsytsykova, A. V., Rajsbaum, R., Falvo, J. V., Ligeiro, F., Neely, S. R. and Goldfeld, A. E., Activation-dependent intrachromosomal interactions formed by the TNF gene promoter and two distal enhancers. Proc. Natl. Acad. Sci. USA 2007. 104: 16850-16855.
25. Goldfeld, A. E., McCaffrey, P. G., Strominger, J. L. and Rao, A., Identification of a novel cyclosporin-sensitive element in the human tumor necrosis factor alpha gene promoter. J. Exp. Med. 1993. 178: 1365-1379.
26. Goldfeld, A. E., Tsai, E., Kincaid, R., Belshaw, P. J., Schrieber, S. L., Strominger, J. L. and Rao, A., Calcineurin mediates human tumor necrosis factor alpha gene induction in stimulated T and B cells. J. Exp. Med. 1994. 180: 763-768.
27. McCaffrey, P. G., Goldfeld, A. E. and Rao, A., The role of NFATp in cyclosporin A-sensitive tumor necrosis factor-alpha gene transcription. J. Biol. Chem. 1994. 269: 30445-30450.
28. Tsai, E. Y., Jain, J., Pesavento, P. A., Rao, A. and Goldfeld, A. E., Tumor necrosis factor alpha gene regulation in activated T cells involves ATF-2/Jun and NFATp. Mol. Cell. Biol. 1996. 16: 459-467.
29. Tsai, E. Y., Yie, J., Thanos, D. and Goldfeld, A. E., Cell-type-specific regulation of the human tumor necrosis factor alpha gene in B cells and T cells by NFATp and ATF-2/JUN. Mol. Cell. Biol. 1996. 16: 5232-5244.
30. Oum, J. H., Han, J., Myung, H., Hleb, M., Sharma, S. and Park, J., Molecular mechanism of NFAT family proteins for differential regulation of the IL-2 and TNF-alpha promoters. Mol. Cell 2002. 13: 77-84.
31. Kaminuma, O., Kitamura, F., Kitamura, N., Hiroi, T., Miyoshi, H., Miyawaki, A. and Miyatake, S., Differential contribution of NFATc2 and NFATc1 to TNF-alpha gene expression in T cells. J. Immunol. 2008. 180: 319-326.
32. Shakhov, A. N., Collart, M. A., Vassalli, P., Nedospasov, S. A. and Jongeneel, C. V., Kappa B-type enhancers are involved in lipopolysaccharide-mediated transcriptional activation of the tumor necrosis factor alpha gene in primary macrophages. J. Exp. Med. 1990. 171: 35-47.
33. Collart, M. A., Baeuerle, P. and Vassalli, P., Regulation of tumor necrosis factor alpha transcription in macrophages: involvement of four kappa B-like motifs and of constitutive and inducible forms of NF-kappa B. Mol. Cell. Biol. 1990. 10: 1498-1506.
34. Yao, J., Mackman, N., Edgington, T. S. and Fan, S. T., Lipopolysaccharide induction of the tumor necrosis factor-alpha promoter in human monocytic cells. Regulation by Egr-1, c-Jun, and NF-kappaB transcription factors. J. Biol. Chem. 1997. 272: 17795-17801.
35. Drouet, C., Shakhov, A. N. and Jongeneel, C. V., Enhancers and transcription factors controlling the inducibility of the tumor necrosis factor-alpha promoter in primary macrophages. J. Immunol. 1991. 147: 1694-1700.
36. Krausgruber, T., Saliba, D., Ryzhakov, G., Lanfrancotti, A., Blazek, K. and Udalova, I. A., IRF5 is required for late-phase TNF secretion by human dendritic cells. Blood 2010. 115: 4421-4430.
37. Kuprash, D. V., Udalova, I. A., Turetskaya, R. L., Rice, N. R. and Nedospasov, S. A., Conserved kappa B element located downstream of the tumor necrosis factor alpha gene: distinct NF-kappa B binding pattern and enhancer activity in LPS activated murine macrophages. Oncogene 1995. 11: 97-106.
38. Kuprash, D. V., Udalova, I. A., Turetskaya, R. L., Kwiatkowski, D., Rice, N. R. and Nedospasov, S. A., Similarities and differences between human and murine TNF promoters in their response to lipopolysaccharide. J. Immunol. 1999. 162: 4045-4052.
39. Udalova, I. A., Knight, J. C., Vidal, V., Nedospasov, S. A. and Kwiatkowski, D., Complex NF-kappaB interactions at the distal tumor necrosis factor promoter region in human monocytes. J. Biol. Chem. 1998. 273: 21178-21186.
40. Cheng, J., Phong, B., Wilson, D. C., Hirsch, R. and Kane, L. P., Akt fine-tunes NF-kB-dependent gene expression during T cell activation. J. Biol. Chem. 2011. 286: 36076-36085.
41. Schones, D. E., Cui, K., Cuddapah, S., Roh, T.-Y., Barski, A., Wang, Z., Wei, G. et al., Dynamic regulation of nucleosome positioning in the human genome. Cell 2008. 132: 887-898.
42. Cherwinski, H. M., Schumacher, J. H., Brown, K. D. and Mosmann, T. R., Two types of mouse helper T cell clone. III. Further differences in lymphokine synthesis between Th1 and Th2 clones revealed by RNA hybridization, functionally monospecific bioassays, and monoclonal antibodies. J. Exp. Med. 1987. 166: 1229-1244.
43. Ferreri, N. R., Askari, B., Mahboubi, K. and Ruddle, N. H., Tumor necrosis factor-α and lymphotoxin: regulation by PGE2 in T-cell subsets. Immunol. Methods 1993. 2: 245-254.
44. Ferreri, N. R., Millet, I., Askari, B., Magnani, P. and Ruddle, N. H., Lymphotoxin-beta and TNF regulation in T cell subsets: differential effects of PGE2. Cytokine 1997. 9: 157-165.
45. Ebinuma, H., Nakamoto, N., Li, Y., Price, D. A., Gostick, E., Levine, B. L., Tobias, J. et al., Identification and in vitro expansion of functional antigen-specific CD25+ FoxP3+ regulatory T cells in hepatitis C virus infection. J. Virol. 2008. 82: 5043-5053.
46. Stockis, J., Fink, W., François, V., Connerotte, T., de Smet, C., Knoops, L., van der Bruggen, P. et al., Comparison of stable human Treg and Th clones by transcriptional profiling. Eur. J. Immunol. 2009. 39: 869-882.
47. Ayyoub, M., Deknuydt, F., Raimbaud, I., Dousset, C., Leveque, L., Bioley, G. and Valmori, D., Human memory FOXP3 +Tregs secrete IL-17 ex vivo and constitutively express the TH17 lineage-specific transcription factor RORγt. Proc. Natl. Acad. Sci. USA 2009. 106: 8635-8640.
48. Wang, Y., Kissenpfennig, A., Mingueneau, M., Richelme, S., Perrin, P., Chevrier, S., Genton, C. et al., Th2 lymphoproliferative disorder of LatY136F mutant mice unfolds independently of TCR-MHC engagement and is insensitive to the action of Foxp3+ regulatory T cells. J. Immunol. 2008. 180: 1565-1575.
49. Tsytsykova, A. V. and Goldfeld, A. E., Nuclear factor of activated T cells transcription factor NFATp controls superantigen-induced lethal shock. J. Exp. Med. 2000. 192: 581-586.
50. Tsai, E. Y., Falvo, J. V., Tsytsykova, A. V., Barczak, A. K., Reimold, A. M., Glimcher, L. H., Fenton, M. J. et al., A lipopolysaccharide-specific enhancer complex involving Ets, Elk-1, Sp1, and CREB binding protein and p300 is recruited to the tumor necrosis factor alpha promoter in vivo. Mol. Cell. Biol. 2000. 20: 6084-6094.
51. Falvo, J. V., Uglialoro, A. M., Brinkman, B. M., Merika, M., Parekh, B. S., Tsai, E. Y., King, H. C. et al., Stimulus-specific assembly of enhancer complexes on the tumor necrosis factor alpha gene promoter. Mol. Cell. Biol. 2000. 20: 2239-2247.
52. Becker, C., Barbulescu, K., Wirtz, S., Meyer zum Buschenfelde, K. H., Pettersson, S. and Neurath, M. F., Constitutive and inducible in vivo protein-DNA interactions at the tumor necrosis factor-alpha promoter in primary human T lymphocytes. Gene Expr. 1999. 8: 115-127.
53. Cockerill, P. N., Identification of DNaseI Hypersensitive Sites within Nuclei. In Tymms, M. J. (Ed.) Transcription factor protocols, Humana Press Inc., Totowa, NJ 1999, pp. 29-46.
54. Cockerill, P. N., Structure and function of active chromatin and DNase I hypersensitive sites. FEBS J. 2011. 278: 2182-2210.
55. Ranjbar, S., Rajsbaum, R. and Goldfeld, A. E., Transactivator of transcription from HIV type 1 subtype E selectively inhibits TNF gene expression via interference with chromatin remodeling of the TNF locus. J. Immunol. 2006. 176: 4182-4190.
56. El Gazzar, M., Liu, T., Yoza, B. K. and McCall, C. E., Dynamic and selective nucleosome repositioning during endotoxin tolerance. J. Biol. Chem. 2010. 285: 1259-1271.
57. Lee, J. Y., Kim, N. A., Sanford, A. and Sullivan, K. E., Histone acetylation and chromatin conformation are regulated separately at the TNF-alpha promoter in monocytes and macrophages. J. Leukoc. Biol. 2003. 73: 862-871.
58. Leddin, M., Perrod, C., Hoogenkamp, M., Ghani, S., Assi, S., Heinz, S., Wilson, N. K. et al., Two distinct auto-regulatory loops operate at the PU.1 locus in B cells and myeloid cells. Blood 2011. 117: 2827-2838.
59. Falvo, J. V., Jasenosky, L. D., Kruidenier, L. and Goldfeld, A. E., Epigenetic control of cytokine gene expression: regulation of the TNF/LT locus and T helper cell differentiation. Adv. Immunol. 2013. 118: 37-128.
60. Samstein, R. M., Arvey, A., Josefowicz, S. Z., Peng, X., Reynolds, A., Sandstrom, R., Neph, S. et al., Foxp3 exploits a pre-existent enhancer landscape for regulatory T cell lineage specification. Cell 2012. 151: 153-166.
61. Nakayamada, S., Kanno, Y., Takahashi, H., Jankovic, D., Lu, K. T., Johnson, T. A., Sun, H.-W. et al., Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 2011. 35: 919-931.
62. Tomaras, G. D., Foster, D. A., Burrer, C. M. and Taffet, S. M., ETS transcription factors regulate an enhancer activity in the third intron of TNF-alpha. J. Leukoc. Biol. 1999. 66: 183-193.
63. Wicks, K. and Knight, J. C., Transcriptional repression and DNA looping associated with a novel regulatory element in the final exon of the lymphotoxin-beta gene. Genes Immun. 2011. 12: 126-135.
64. Watanabe, T., Ishihara, K., Hirosue, A., Watanabe, S., Hino, S., Ojima, H., Kanai, Y. et al., Higher-order chromatin regulation and differential gene expression in the human tumor necrosis factor/lymphotoxin locus in hepatocellular carcinoma cells. Mol. Cell. Biol. 2012. 32: 1529-1541.
65. Kwon, J., Lee, S. J. and Benveniste, E. N., A 3′ cis-acting element is involved in tumor necrosis factor-alpha gene expression in astrocytes. J. Biol. Chem. 1996. 271: 22383-22390.
66. Sullivan, K. E., Reddy, A. B., Dietzmann, K., Suriano, A. R., Kocieda, V. P., Stewart, M. and Bhatia, M., Epigenetic regulation of tumor necrosis factor alpha. Mol. Cell. Biol. 2007. 27: 5147-5160.
67. Boyle, A. P., Davis, S., Shulha, H. P., Meltzer, P., Margulies, E. H., Weng, Z., Furey, T. S. et al., High-resolution mapping and characterization of open chromatin across the genome. Cell 2008. 132: 311-322.
68. Kochanek, S., Toth, M., Dehmel, A., Renz, D. and Doerfler, W., Interindividual concordance of methylation profiles in human genes for tumor necrosis factors alpha and beta. Proc. Natl. Acad. Sci. USA 1990. 87: 8830-8834.
69. Kochanek, S., Radbruch, A., Tesch, H., Renz, D. and Doerfler, W., DNA methylation profiles in the human genes for tumor necrosis factors alpha and beta in subpopulations of leukocytes and in leukemias. Proc. Natl. Acad. Sci. USA 1991. 88: 5759-5763.
70. Tsytsykova, A. V. and Goldfeld, A. E., Inducer-specific enhanceosome formation controls tumor necrosis factor alpha gene expression in T lymphocytes. Mol. Cell. Biol. 2002. 22: 2620-2631.
71. Kulaeva, O. I., Gaykalova, D. A. and Studitsky, V. M., Transcription through chromatin by RNA polymerase II: histone displacement and exchange. Mutat. Res. 2007. 618: 116-129.
72. Martens, J. H. A., Verlaan, M., Kalkhoven, E. and Zantema, A., Cascade of distinct histone modifications during collagenase gene activation. Mol. Cell. Biol. 2003. 23: 1808-1816.
73. Chang, Q., Zhang, Y., Beezhold, K. J., Bhatia, D., Zhao, H., Chen, J., Castranova, V. et al., Sustained JNK1 activation is associated with altered histone H3 methylations in human liver cancer. J. Hepatol. 2009. 50: 323-333.
74. Wolter, S., Doerrie, A., Weber, A., Schneider, H., Hoffmann, E., von der Ohe, J., Bakiri, L. et al., c-Jun controls histone modifications, NF-κB recruitment, and RNA polymerase II function to activate the ccl2 gene. Mol. Cell. Biol. 2008. 28: 4407-4423.
75. Goldfeld, A. E., Doyle, C. and Maniatis, T., Human tumor necrosis factor alpha gene regulation by virus and lipopolysaccharide. Proc. Nat. Acad. Sci. USA 1990. 87: 9769-9773.
76. Goldfeld, A. E., Strominger, J. L. and Doyle, C., Human tumor necrosis factor alpha gene regulation in phorbol ester stimulated T and B cell lines. J. Exp. Med. 1991. 174: 73-81.
77. Tsytsykova, A. V., Falvo, J. V., Schmidt-Supprian, M., Courtois, G., Thanos, D. and Goldfeld, A. E., Post-induction, stimulus-specific regulation of tumor necrosis factor mRNA expression. J. Biol. Chem. 2007. 282: 11629-11638.
78. Ziegler-Heitbrock, H. W., Sternsdorf, T., Liese, J., Belohradsky, B., Weber, C., Wedel, A., Schreck, R. et al., Pyrrolidine dithiocarbamate inhibits NF-kappa B mobilization and TNF production in human monocytes. J. Immunol. 1993. 151: 6986-6993.
79. Siggers, T., Chang, A. B., Teixeira, A., Wong, D., Williams, K. J., Ahmed, B., Ragoussis, J. et al., Principles of dimer-specific gene regulation revealed by a comprehensive characterization of NFκB family DNA binding. Nat. Immunol. 2011. 13: 95-102.
80. Trede, N. S., Tsytsykova, A. V., Chatila, T., Goldfeld, A. E. and Geha, R. S., Transcriptional activation of the human TNF-alpha promoter by superantigen in human monocytic cells: role of NF-kappa B. J. Immunol. 1995. 155: 902-908.
81. El Gazzar, M., Yoza, B. K., Hu, J. Y.-Q., Cousart, S. L. and McCall, C. E., Epigenetic silencing of tumor necrosis factor α during endotoxin tolerance. J. Biol. Chem. 2007. 282: 26857-26864.
82. Garber, M., Yosef, N., Goren, A., Raychowdhury, R., Thielke, A., Guttman, M., Robinson, J. et al., A high-throughput chromatin immunoprecipitation approach reveals principles of dynamic gene regulation in mammals. Mol. Cell 2012. 47: 810-822.
83. Barish, G. D., Yu, R. T., Karunasiri, M., Ocampo, C. B., Dixon, J., Benner, C., Dent, A. L. et al., Bcl-6 and NF-kappaB cistromes mediate opposing regulation of the innate immune response. Genes Dev. 2010. 24: 2760-2765.
84. Rao, P., Hayden, M. S., Long, M., Scott, M. L., West, A. P., Zhang, D., Oeckinghaus, A. et al., IkappaBbeta acts to inhibit and activate gene expression during the inflammatory response. Nature 2010. 466: 1115-1119.
85. Smallie, T., Ricchetti, G., Horwood, N. J., Feldmann, M., Clark, A. R. and Williams, L. M., IL-10 inhibits transcription elongation of the human TNF gene in primary macrophages. J. Exp. Med. 2010. 207: 2081-2088.
86. Mirabella, F., Baxter, E. W., Boissinot, M., James, S. R. and Cockerill, P. N., The human IL-3/granulocyte-macrophage colony-stimulating factor locus is epigenetically silent in immature thymocytes and is progressively activated during T cell development. J. Immunol. 2010. 184: 3043-3054.
87. Hawwari, A., Burrows, J., Vadas, M. A. and Cockerill, P. N., The human IL-3 locus is regulated cooperatively by two NFAT-dependent enhancers that have distinct tissue-specific activities. J. Immunol. 2002. 169: 1876-1886.
88. Duncliffe, K. N., Bert, A. G., Vadas, M. A. and Cockerill, P. N., A T cell-specific enhancer in the interleukin-3 locus is activated cooperatively by Oct and NFAT elements within a DNase I-hypersensitive site. Immunity 1997. 6: 175-185.
89. Solymar, D. C., Agarwal, S., Bassing, C. H., Alt, F. W. and Rao, A., A 3′ enhancer in the IL-4 gene regulates cytokine production by Th2 cells and mast cells. Immunity 2002. 17: 41-50.
90. Lee, D. U., Avni, O., Chen, L. and Rao, A., A distal enhancer in the interferon-γ (IFN-γ) locus revealed by genome sequence comparison. J. Biol. Chem. 2004. 279: 4802-4810.
91. Rao, S., Procko, E. and Shannon, M. F., Chromatin remodeling, measured by a novel real-time polymerase chain reaction assay, across the proximal promoter region of the IL-2 gene. J. Immunol. 2001. 167: 4494-4503.
92. Johnson, B. V., Bert, A. G., Ryan, G. R., Condina, A. and Cockerill, P. N., Granulocyte-macrophage colony-stimulating factor enhancer activation requires cooperation between NFAT and AP-1 elements and is associated with extensive nucleosome reorganization. Mol. Cell. Biol. 2004. 24: 7914-7930.
93. Ishihara, S. and Schwartz, R. H., Two-Step binding of transcription factors causes sequential chromatin structural changes at the activated IL-2 promoter. J. Immunol. 2011. 187: 3292-3299.
94. Berth-Jones, J., The use of ciclosporin in psoriasis. J. Dermatolog. Treat. 2005. 16: 258-277.
95. Cohen, D. J., Loertscher, R., Rubin, M. F., Tilney, N. L., Carpenter, C. B. and Strom, T. B., Cyclosporine: a new immunosuppressive agent for organ transplantation. Ann. Intern. Med. 1984. 101: 667-682.
96. Faulds, D., Goa, K. L. and Benfield, P., Cyclosporin. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic use in immunoregulatory disorders. Drugs 1993. 45: 953-1040.
97. Galeazzi, M., Bellisai, F., Manganelli, S., Morozzi, G. and Sebastiani, G. D., Cyclosporine A for the treatment of autoimmune disorders in HCV infected patients. Autoimmun. Rev. 2006. 5: 493-498.
98. Tedesco, D. and Haragsim, L., Cyclosporine: a review. J. Transplant. 2012. DOI 10.115/2012/230386.
99. Han, Z., Boyle, D. L., Chang, L., Bennett, B., Karin, M., Yang, L., Manning, A. M. et al., c-Jun N-terminal kinase is required for metalloproteinase expression and joint destruction in inflammatory arthritis. J. Clin. Invest. 2001. 108: 73-81.
100. Assi, K., Pillai, R., Gómez-Muñoz, A., Owen, D. and Salh, B., The specific JNK inhibitor SP600125 targets tumour necrosis factor-α production and epithelial cell apoptosis in acute murine colitis. Immunology 2006. 118: 112-121.
101. Crocker, C. E., Khan, S., Cameron, M. D., Robertson, H. A., Robertson, G. S. and LoGrasso, P., JNK inhibition protects dopamine neurons and provides behavioral improvement in a Rat 6-hydroxydopamine model of Parkinson's disease. ACS Chem. Neurosci. 2011. 2: 207-212.
102. Kuan, C. Y. and Burke, R. E., Targeting the JNK signaling pathway for stroke and Parkinson's diseases therapy. Curr. Drug. Targets CNS Neurol. Disord. 2005. 4: 63-67.
103. Mingo-Sion, A. M., Marietta, P. M., Koller, E., Wolf, D. M. and Van Den Berg, C. L., Inhibition of JNK reduces G2/M transit independent of p53, leading to endoreduplication, decreased proliferation, and apoptosis in breast cancer cells. Oncogene 2003. 23: 596-604.
104. Mucha, S. R., Rizzani, A., Gerbes, A. L., Camaj, P., Thasler, W. E., Bruns, C. J., Eichhorst, S. T. et al., JNK inhibition sensitises hepatocellular carcinoma cells but not normal hepatocytes to the TNF-related apoptosis-inducing ligand. Gut 2009. 58: 688-698.
105. Bogoyevitch, M. A., Ngoei, K. R. W., Zhao, T. T., Yeap, Y. Y. C. and Ng, D. C. H., c-Jun N-terminal kinase (JNK) signaling: recent advances and challenges. Biochim. Biophys. Acta 2010. 1804: 463-475.
106. Sweeney, S. E. and Firestein, G. S., Mitogen activated protein kinase inhibitors: where are we now and where are we going? Ann. Rheum. Dis. 2006. 65(Suppl 3): iii83-iii88.
107. Muller, M., Eugster, H. P., Le Hir, M., Shakhov, A., Di Padova, F., Maurer, C., Quesniaux, V. F. et al., Correction or transfer of immunodeficiency due to TNF-LT alpha deletion by bone marrow transplantation. Mol. Med. 1996. 2: 247-255.
108. Wang, T., Lafuse, W. P., Takeda, K., Akira, S. and Zwilling, B. S., Rapid chromatin remodeling of Toll-like receptor 2 promoter during infection of macrophages with Mycobacterium avium. J. Immunol. 2002. 169: 795-801.