Interaction of Ets-1 with HDAC1 represses IL-10 expression in Th1 cells

Journal of Immunology

Volumn 188, Issue 5, 2012, Pages 2244-2253

  Lee, Choong Gu ^a   Kwon, Ho Keun ^a   Sahoo, Anupama ^a   Hwang, Won ^a   So, Jae Seon ^a   Hwang, Ji Sun ^a   Chae, Chang Suk ^a   Kim, Gi Cheon ^a   Kim, Jung Eun ^a   So, Hong Seob ^b   Hwang, Eun Sook ^c   Grenningloh, Roland ^d,e   Ho, I Cheng ^d,e   Im, Sin Hyeog ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

^b Wonkwang University   (South Korea)

^c Ewha Womans University   (South Korea)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE 1; HISTONE H3; INTERLEUKIN 10; TRANSCRIPTION FACTOR ETS 1; TRICHOSTATIN A;

ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; INTERLEUKIN 10 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; TH1 CELL; TH2 CELL; UPREGULATION; WILD TYPE;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DOWN-REGULATION; GENE EXPRESSION REGULATION; HEK293 CELLS; HISTONE DEACETYLASE 1; HUMANS; INTERLEUKIN-10; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEIN C-ETS-1; TH1 CELLS; UP-REGULATION;

EID: 84863184174     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101614     Document Type: Article

References (62)

1. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765. (Pubitemid 32368050)
2. O'Garra, A., and P. Vieira. 2007. T(H)1 cells control themselves by producing interleukin-10. Nat. Rev. Immunol. 7: 425-428. (Pubitemid 46834852)
3. Murphy, K. M., and S. L. Reiner. 2002. The lineage decisions of helper T cells. Nat. Rev. Immunol. 2: 933-944. (Pubitemid 37323214)
4. Wilson, C. B., E. Rowell, and M. Sekimata. 2009. Epigenetic control of T-helper-cell differentiation. Nat. Rev. Immunol. 9: 91-105.
5. Trinchieri, G. 2007. Interleukin-10 production by effector T cells: Th1 cells show self control. J. Exp. Med. 204: 239-243. (Pubitemid 46294539)
6. Anderson, C. F., M. Oukka, V. J. Kuchroo, and D. Sacks. 2007. CD4(+)CD25(-) Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204: 285-297. (Pubitemid 46294545)
7. Jankovic, D., M. C. Kullberg, C. G. Feng, R. S. Goldszmid, C. M. Collazo, M. Wilson, T. A. Wynn, M. Kamanaka, R. A. Flavell, and A. Sher. 2007. Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204: 273-283. (Pubitemid 46294544)
8. Batten, M., N. M. Kljavin, J. Li, M. J. Walter, F. J. de Sauvage, and N. Ghilardi. 2008. Cutting edge: IL-27 is a potent inducer of IL-10 but not FoxP3 in murine T cells. J. Immunol. 180: 2752-2756.
9. Rutz, S., M. Janke, N. Kassner, T. Hohnstein, M. Krueger, and A. Scheffold. 2008. Notch regulates IL-10 production by T helper 1 cells. Proc. Natl. Acad. Sci. USA 105: 3497-3502. (Pubitemid 351723581)
10. Saraiva, M., J. R. Christensen, M. Veldhoen, T. L. Murphy, K. M. Murphy, and A. O'Garra. 2009. Interleukin-10 production by Th1 cells requires interleukin-12-induced STAT4 transcription factor and ERK MAP kinase activation by high antigen dose. Immunity 31: 209-219.
11. Im, S. H., A. Hueber, S. Monticelli, K. H. Kang, and A. Rao. 2004. Chromatin-level regulation of the IL10 gene in T cells. J. Biol. Chem. 279: 46818-46825. (Pubitemid 39518332)
12. Jones, E. A., and R. A. Flavell. 2005. Distal enhancer elements transcribe intergenic RNA in the IL-10 family gene cluster. J. Immunol. 175: 7437-7446. (Pubitemid 41713441)
13. Chang, H. D., C. Helbig, L. Tykocinski, S. Kreher, J. Koeck, U. Niesner, and A. Radbruch. 2007. Expression of IL-10 in Th memory lymphocytes is conditional on IL-12 or IL-4, unless the IL-10 gene is imprinted by GATA-3. Eur. J. Immunol. 37: 807-817. (Pubitemid 46916947)
14. Shoemaker, J., M. Saraiva, and A. O'Garra. 2006. GATA-3 directly remodels the IL-10 locus independently of IL-4 in CD4+ T cells. J. Immunol. 176: 3470-3479. (Pubitemid 43363994)
15. Wang, Z. Y., H. Sato, S. Kusam, S. Sehra, L. M. Toney, and A. L. Dent. 2005. Regulation of IL-10 gene expression in Th2 cells by Jun proteins. J. Immunol. 174: 2098-2105. (Pubitemid 40223953)
16. Sharrocks, A. D. 2001. The ETS-domain transcription factor family. Nat. Rev. Mol. Cell Biol. 2: 827-837. (Pubitemid 33674083)
17. Dittmer, J. 2003. The biology of the Ets1 proto-oncogene. Mol. Cancer 2: 29.
18. Barton, K., N. Muthusamy, C. Fischer, C. N. Ting, T. L. Walunas, L. L. Lanier, and J. M. Leiden. 1998. The Ets-1 transcription factor is required for the development of natural killer cells in mice. Immunity 9: 555-563. (Pubitemid 28499206)
19. Bories, J. C., D. M. Willerford, D. Grévin, L. Davidson, A. Camus, P. Martin, D. Stéhelin, and F. W. Alt. 1995. Increased T-cell apoptosis and terminal B-cell differentiation induced by inactivation of the Ets-1 proto-oncogene. Nature 377: 635-638.
20. Muthusamy, N., K. Barton, and J. M. Leiden. 1995. Defective activation and survival of T cells lacking the Ets-1 transcription factor. Nature 377: 639-642.
21. Grenningloh, R., B. Y. Kang, and I. C. Ho. 2005. Ets-1, a functional cofactor of T-bet, is essential for Th1 inflammatory responses. J. Exp. Med. 201: 615-626. (Pubitemid 40289551)
22. Moisan, J., R. Grenningloh, E. Bettelli, M. Oukka, and I. C. Ho. 2007. Ets-1 is a negative regulator of Th17 differentiation. J. Exp. Med. 204: 2825-2835. (Pubitemid 350179553)
23. Russell, L., and L. A. Garrett-Sinha. 2010. Transcription factor Ets-1 in cytokine and chemokine gene regulation. Cytokine 51: 217-226.
24. Blumenthal, S. G., G. Aichele, T. Wirth, A. P. Czernilofsky, A. Nordheim, and J. Dittmer. 1999. Regulation of the human interleukin-5 promoter by Ets transcription factors. Ets1 and Ets2, but not Elf-1, cooperate with GATA3 and HTLV-I Tax1. J. Biol. Chem. 274: 12910-12916.
25. Romano-Spica, V., P. Georgiou, H. Suzuki, T. S. Papas, and N. K. Bhat. 1995. Role of ETS1 in IL-2 gene expression. J. Immunol. 154: 2724-2732.
26. Thomas, R. S., M. J. Tymms, L. H. McKinlay, M. F. Shannon, A. Seth, and I. Kola. 1997. ETS1, NFkappaB and AP1 synergistically transactivate the human GM-CSF promoter. Oncogene 14: 2845-2855. (Pubitemid 27313417)
27. Wang, D., S. A. John, J. L. Clements, D. H. Percy, K. P. Barton, and L. A. Garrett-Sinha. 2005. Ets-1 deficiency leads to altered B cell differentiation, hyperresponsiveness to TLR9 and autoimmune disease. Int. Immunol. 17: 1179-1191. (Pubitemid 41236075)
28. Szabo, S. J., B. M. Sullivan, C. Stemmann, A. R. Satoskar, B. P. Sleckman, and L. H. Glimcher. 2002. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 295: 338-342. (Pubitemid 34074366)
29. Kaplan, M. H., Y. L. Sun, T. Hoey, and M. J. Grusby. 1996. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382: 174-177. (Pubitemid 26242885)
30. Lee, C. G., K. H. Kang, J. S. So, H. K. Kwon, J. S. Son, M. K. Song, A. Sahoo, H. J. Yi, K. C. Hwang, T. Matsuyama, et al. 2009. A distal cis-regulatory element, CNS-9, controls NFAT1 and IRF4-mediated IL-10 gene activation in T helper cells. Mol. Immunol. 46: 613-621.
31. Nelson, J. D., O. Denisenko, and K. Bomsztyk. 2006. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 1: 179-185.
32. Rao, S., E. Procko, and M. F. Shannon. 2001. Chromatin remodeling, measured by a novel real-time polymerase chain reaction assay, across the proximal promoter region of the IL-2 gene. J. Immunol. 167: 4494-4503. (Pubitemid 32954327)
33. Mayor, C., M. Brudno, J. R. Schwartz, A. Poliakov, E. M. Rubin, K. A. Frazer, L. S. Pachter, and I. Dubchak. 2000. VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16: 1046-1047. (Pubitemid 32051021)
34. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128: 693-705. (Pubitemid 46273577)
35. Berger, S. L. 2007. The complex language of chromatin regulation during transcription. Nature 447: 407-412. (Pubitemid 46816746)
36. Koipally, J., A. Renold, J. Kim, and K. Georgopoulos. 1999. Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J. 18: 3090-3100. (Pubitemid 29255617)
37. Cowley, S. M., B. M. Iritani, S. M. Mendrysa, T. Xu, P. F. Cheng, J. Yada, H. D. Liggitt, and R. N. Eisenman. 2005. The mSin3A chromatin-modifying complex is essential for embryogenesis and T-cell development. Mol. Cell. Biol. 25: 6990-7004. (Pubitemid 41105899)
38. Fredriksson, S., M. Gullberg, J. Jarvius, C. Olsson, K. Pietras, S. M. Gústafsdóttir, A. Ostman, and U. Landegren. 2002. Protein detection using proximity-dependent DNA ligation assays. Nat. Biotechnol. 20: 473-477. (Pubitemid 34495933)
39. Sahoo, A., C. G. Lee, A. Jash, J. S. Son, G. Kim, H. K. Kwon, J. S. So, and S. H. Im. 2011. Stat6 and c-Jun mediate Th2 cell-specific IL-24 gene expression. J. Immunol. 186: 4098-4109.
40. Soler, D., T. R. Chapman, L. R. Poisson, L. Wang, J. Cote-Sierra, M. Ryan, A. McDonald, S. Badola, E. Fedyk, A. J. Coyle, et al. 2006. CCR8 expression identifies CD4 memory T cells enriched for FOXP3+ regulatory and Th2 effector lymphocytes. J. Immunol. 177: 6940-6951. (Pubitemid 44715060)
41. Hollenhorst, P. C., A. A. Shah, C. Hopkins, and B. J. Graves. 2007. Genomewide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev. 21: 1882-1894. (Pubitemid 47204928)
42. Oikawa, T., and T. Yamada. 2003. Molecular biology of the Ets family of transcription factors. Gene 303: 11-34. (Pubitemid 36151767)
43. Verger, A., and M. Duterque-Coquillaud. 2002. When Ets transcription factors meet their partners. Bioessays 24: 362-370.
44. Li, R., H. Pei, D. K. Watson, and T. S. Papas. 2000. EAP1/Daxx interacts with ETS1 and represses transcriptional activation of ETS1 target genes. Oncogene 19: 745-753. (Pubitemid 30107705)
45. Hollenhorst, P. C., K. J. Chandler, R. L. Poulsen, W. E. Johnson, N. A. Speck, and B. J. Graves. 2009. DNA specificity determinants associate with distinct transcription factor functions. PLoS Genet. 5: e1000778.
46. Narlikar, G. J., H. Y. Fan, and R. E. Kingston. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108: 475-487. (Pubitemid 34260873)
47. Schübeler, D., D. M. MacAlpine, D. Scalzo, C. Wirbelauer, C. Kooperberg, F. van Leeuwen, D. E. Gottschling, L. P. O'Neill, B. M. Turner, J. Delrow, et al. 2004. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18: 1263-1271. (Pubitemid 38720594)
48. Villagra, A., F. Cheng, H. W. Wang, I. Suarez, M. Glozak, M. Maurin, D. Nguyen, K. L. Wright, P. W. Atadja, K. Bhalla, et al. 2009. The histone deacetylase HDAC11 regulates the expression of interleukin 10 and immune tolerance. Nat. Immunol. 10: 92-100.
49. Grant, L. R., Z. J. Yao, C. M. Hedrich, F. Wang, A. Moorthy, K. Wilson, D. Ranatunga, and J. H. Bream. 2008. Stat4-dependent, T-bet-independent regulation of IL-10 in NK cells. Genes Immun. 9: 316-327. (Pubitemid 351791487)
50. Wasylyk, B., S. L. Hahn, and A. Giovane. 1993. The Ets family of transcription factors. Eur. J. Biochem. 211: 7-18. (Pubitemid 23039491)
51. Yang, C., L. H. Shapiro, M. Rivera, A. Kumar, and P. K. Brindle. 1998. A role for CREB binding protein and p300 transcriptional coactivators in Ets-1 transactivation functions. Mol. Cell. Biol. 18: 2218-2229. (Pubitemid 28152670)
52. Aalfs, J. D., and R. E. Kingston. 2000. What does 'chromatin remodeling' mean? Trends Biochem. Sci. 25: 548-555.
53. Ng, H. H., and A. Bird. 2000. Histone deacetylases: silencers for hire. Trends Biochem. Sci. 25: 121-126. (Pubitemid 30122423)
54. Cowley, D. O., and B. J. Graves. 2000. Phosphorylation represses Ets-1 DNA binding by reinforcing autoinhibition. Genes Dev. 14: 366-376. (Pubitemid 30106491)
55. Pufall, M. A., G. M. Lee, M. L. Nelson, H. S. Kang, A. Velyvis, L. E. Kay, L. P. McIntosh, and B. J. Graves. 2005. Variable control of Ets-1 DNA binding by multiple phosphates in an unstructured region. Science 309: 142-145. (Pubitemid 40934995)
56. Nelson, M. L., H. S. Kang, G. M. Lee, A. G. Blaszczak, D. K. Lau, L. P. McIntosh, and B. J. Graves. 2010. Ras signaling requires dynamic properties of Ets1 for phosphorylation-enhanced binding to coactivator CBP. Proc. Natl. Acad. Sci. USA 107: 10026-10031.
57. Grenningloh, R., S. C. Miaw, J. Moisan, B. J. Graves, and I. C. Ho. 2008. Role of Ets-1 phosphorylation in the effector function of Th cells. Eur. J. Immunol. 38: 1700-1705.
58. Czuwara-Ladykowska, J., V. I. Sementchenko, D. K. Watson, and M. Trojanowska. 2002. Ets1 is an effector of the transforming growth factor beta (TGF-beta) signaling pathway and an antagonist of the profibrotic effects of TGF-beta. J. Biol. Chem. 277: 20399-20408. (Pubitemid 34967335)
59. Han, J. W., H. F. Zheng, Y. Cui, L. D. Sun, D. Q. Ye, Z. Hu, J. H. Xu, Z. M. Cai, W. Huang, G. P. Zhao, et al. 2009. Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat. Genet. 41: 1234-1237.
60. Yang, W., N. Shen, D. Q. Ye, Q. Liu, Y. Zhang, X. X. Qian, N. Hirankarn, D. Ying, H. F. Pan, C. C. Mok, et al Asian Lupus Genetics Consortium. 2010. Genome-wide association study in Asian populations identifies variants in ETS1 and WDFY4 associated with systemic lupus erythematosus. PLoS Genet. 6: e1000841.
61. Llorente, L., and Y. Richaud-Patin. 2003. The role of interleukin-10 in systemic lupus erythematosus. J. Autoimmun. 20: 287-289. (Pubitemid 36677520)
62. Houssiau, F. A., C. Lefebvre, M. Vanden Berghe, M. Lambert, J. P. Devogelaer, and J. C. Renauld. 1995. Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus 4: 393-395.