Histone deacetylase inhibitors decrease Toll-like receptor-mediated activation of proinflammatory gene expression by impairing transcription factor recruitment

Immunology

Volumn 122, Issue 4, 2007, Pages 596-606

  Bode, Konrad A ^a   Schroder, Kate ^b   Hume, David A ^b   Ravasi, Timothy ^c   Heeg, Klaus ^a   Sweet, Matthew J ^b   Dalpke, Alexander H ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Chromatin modifications; Dendritic cells; Histone deacetylases; Interleukin 12; Toll like receptors

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; MESSENGER RNA; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA; TRICHOSTATIN A; TUMOR NECROSIS FACTOR ALPHA; VORINOSTAT;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DENDRITIC CELL; DRUG INHIBITION; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; HUMAN; HUMAN CELL; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CHROMATIN; CYTOKINES; DENDRITIC CELLS; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HYDROXAMIC ACIDS; INFLAMMATION MEDIATORS; INTERLEUKIN-12 SUBUNIT P40; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTORS; TRANSCRIPTION, GENETIC;

EID: 35948983828     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2007.02678.x     Document Type: Article

References (52)

1. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006 124: 783 801.
2. Honda K, Taniguchi T. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 2006 6: 644 58.
3. O'Neill LA. How Toll-like receptors signal: what we know and what we don't know. Curr Opin Immunol 2006 18: 3 9.
4. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol 2005 17: 1 14.
5. Albrecht I, Tapmeier T, Zimmermann S, Frey M, Heeg K, Dalpke A. Toll-like receptors differentially induce nucleosome remodelling at the IL-12p40 promoter. EMBO Report 2004 5: 172 7.
6. Weinmann AS, Plevy SE, Smale ST. Rapid and selective remodeling of a positioned nucleosome during the induction of IL-12 p40 transcription. Immunity 1999 11: 665 75.
7. Chan HM, La Thangue NB. p300/CBP proteins. HATs for transcriptional bridges and scaffolds. J Cell Sci 2001 114: 2363 73.
8. Avots A, Buttmann M, Chuvpilo S et al. CBP/p300 integrates Raf/Rac-signaling pathways in the transcriptional induction of NF-ATc during T cell activation. Immunity 1999 10: 515 24.
9. Bannert N, Avots A, Baier M, Serfling E, Kurth R. GA-binding protein factors, in concert with the coactivator CREB binding protein/p300, control the induction of the interleukin 16 promoter in T lymphocytes. Proc Natl Acad Sci USA 1999 96: 1541 6.
10. Lu J, Sun H, Wang X, Liu C, Xu X, Li F, Huang B. Interleukin-12 p40 promoter activity is regulated by the reversible acetylation mediated by HDAC1 and p300. Cytokine 2005 31: 46 51.
11. Sisk TJ, Gourley T, Roys S, Chang CH. MHC class II transactivator inhibits IL-4 gene transcription by competing with NF-AT to bind the coactivator CREB binding protein (CBP)/p300. J Immunol 2000 165: 2511 17.
12. Vanden Berghe W, De Bosscher K, Boone E, Plaisance S, Haegeman G. The nuclear factor-kappaB engages CBP/p300 and histone acetyltransferase activity for transcriptional activation of the interleukin-6 gene promoter. J Biol Chem 1999 274: 32091 8.
13. Sengupta N, Seto E. Regulation of histone deacetylase activities. J Cell Biochem 2004 93: 57 67.
14. Marks P, Rifkind RA, Richon VM, Breslow R, Miller T, Kelly WK. Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer 2001 1: 194 202.
15. Hoshikawa Y, Kwon HJ, Yoshida M, Horinouchi S, Beppu T. Trichostatin A induces morphological changes and gelsolin expression by inhibiting histone deacetylase in human carcinoma cell lines. Exp Cell Res 1994 214: 189 97.
16. Miyashita T, Yamamoto H, Nishimune Y, Nozaki M, Morita T, Matsushiro A. Activation of the mouse cytokeratin A (endo A) gene in teratocarcinoma F9 cells by the histone deacetylase inhibitor Trichostatin A. FEBS Lett 1994 353: 225 9.
17. Futamura M, Monden Y, Okabe T, Fujita-Yoshigaki J, Yokoyama S, Nishimura S. Trichostatin A inhibits both ras-induced neurite outgrowth of PC12 cells and morphological transformation of NIH3T3 cells. Oncogene 1995 10: 1119 23.
18. Kim YB, Ki SW, Yoshida M, Horinouchi S. Mechanism of cell cycle arrest caused by histone deacetylase inhibitors in human carcinoma cells. J Antibiot (Tokyo) 2000 53: 1191 200.
19. Reilly CM, Mishra N, Miller JM et al. Modulation of renal disease in MRL/lpr mice by suberoylanilide hydroxamic acid. J Immunol 2004 173: 4171 8.
20. Leoni F, Zaliani A, Bertolini G et al. The antitumor histone deacetylase inhibitor suberoylanilide hydroxamic acid exhibits antiinflammatory properties via suppression of cytokines. Proc Natl Acad Sci USA 2002 99: 2995 3000.
21. Choi JH, Oh SW, Kang MS, Kwon HJ, Oh GT, Kim DY. Trichostatin A attenuates airway inflammation in mouse asthma model. Clin Exp Allergy 2005 35: 89 96.
22. Camelo S, Iglesias AH, Hwang D et al. Transcriptional therapy with the histone deacetylase inhibitor trichostatin A ameliorates experimental autoimmune encephalomyelitis. J Neuroimmunol 2005 164: 10 21.
23. Aung HT, Schroder K, Himes SR et al. LPS regulates proinflammatory gene expression in macrophages by altering histone deacetylase expression. FASEB J 2006 20: 1315 27.
24. Brogdon J, Xu Y, Szabo S, An S, Buxton F, Cohen D, Huang Q. Histone deacetylase activities are required for innate immune cell control of Th1 but not Th2 effector cell function. Blood 2007 109: 1123 30.
25. Inaba K, Inaba M, Romani N et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992 176: 1693 702.
26. Murray PJ. The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proc Natl Acad Sci USA 2005 102: 8686 91.
27. Saccani S, Pantano S, Natoli G. p38-dependent marking of inflammatory genes for increased NF-kappa B recruitment. Nat Immunol 2002 3: 69 75.
28. Bosisio D, Marazzi I, Agresti A, Shimizu N, Bianchi ME, Natoli G. A hyper-dynamic equilibrium between promoter-bound and nucleoplasmic dimers controls NF-kappaB-dependent gene activity. EMBO J 2006 25: 798 810.
29. Andrews NC, Faller DV. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucl Acids Res 1991 19: 2499.
30. Rao S, Procko E, Shannon MF. 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 503.
31. Dai Y, Rahmani M, Dent P, Grant S. Blockade of histone deacetylase inhibitor-induced RelA/p65 acetylation and NF-κB activation potentiates apoptosis in leukemia cells through a process mediated by oxidative damage, XIAP downregulation, and c-Jun N-terminal kinase 1 activation. Mol Cell Biol 2005 25: 5429 44.
32. Sweet MJ, Campbell CC, Sester DP et al. Colony-stimulating factor-1 suppresses responses to CpG DNA and expression of Toll-like receptor 9 but enhances responses to lipopolysaccharide in murine macrophages. J Immunol 2002 168: 392 9.
33. Plevy SE, Gemberling JH, Hsu S, Dorner AJ, Smale ST. Multiple control elements mediate activation of the murine and human interleukin 12 p40 promoters. Evidence of functional synergy between C/EBP and Rel proteins. Mol Cell Biol 1997 17: 4572 88.
34. Negishi H, Fujita Y, Yanai H et al. Evidence for licensing of IFN-gamma-induced IFN regulatory factor 1 transcription factor by MyD88 in Toll-like receptor-dependent gene induction program. Proc Natl Acad Sci USA 2006 103: 15136 41.
35. Takaoka A, Yanai H, Kondo S et al. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 2005 434: 243 9.
36. Salkowski CA, Kopydlowski K, Blanco J, Cody MJ, McNally R, Vogel SN. IL-12 is dysregulated in macrophages from IRF-1 and IRF-2 knockout mice. J Immunol 1999 163: 1529 36.
37. Zhou L, Nazarian AA, Smale ST. Interleukin-10 inhibits interleukin-12 p40 gene transcription by targeting a late event in the activation pathway. Mol Cell Biol 2004 24: 2385 96.
38. Schmitz F, Heit A, Guggemoos S et al. Interferon-regulatory-factor 1 controls Toll-like receptor 9-mediated IFN-beta production in myeloid dendritic cells. Eur J Immunol 2007 37: 315 27.
39. Hoebe K, Janssen EM, Kim SO, Alexopoulou L, Flavell RA, Han J, Beutler B. Upregulation of costimulatory molecules induced by lipopolysaccharide and double-stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat Immunol 2003 4: 1223 9.
40. Klampfer L, Huang J, Swaby LA, Augenlicht L. Requirement of histone deacetylase activity for signaling by STAT1. J Biol Chem 2004 279: 30358 68.
41. Nusinzon I, Horvath CM. Positive and negative regulation of the innate antiviral response and beta interferon gene expression by deacetylation. Mol Cell Biol 2006 26: 3106 13.
42. Sakamoto S, Potla R, Larner AC. Histone deacetylase activity is required to recruit RNA polymerase II to the promoters of selected interferon-stimulated early response genes. J Biol Chem 2004 279: 40362 7.
43. Iwata K, Tomita K, Sano H, Fujii Y, Yamasaki A, Shimizu E. Trichostatin A, a histone deacetylase inhibitor, down-regulates interleukin-12 transcription in SV-40-transformed lung epithelial cells. Cell Immunol 2002 218: 26 33.
44. Sun H, Lu J, Wei L, Wang X, Xu X, Dong M, Huang B. Histone acetyltransferase activity of p300 enhances the activation of IL-12 p40 promoter. Mol Immunol 2004 41: 1241 6.
45. Weinmann AS, Mitchell DM, Sanjabi S, Bradley MN, Hoffmann A, Liou HC, Smale ST. Nucleosome remodeling at the IL-12 p40 promoter is a TLR-dependent, Rel-independent event. Nat Immunol 2001 2: 51 7.
46. Yamaguchi K, Lantowski A, Dannenberg AJ, Subbaramaiah K. Histone deacetylase inhibitors suppress the induction of c-Jun and its target genes including COX-2. J Biol Chem 2005 280: 32569 77.
47. Chen LF, Greene WC. Regulation of distinct biological activities of the NF-kappaB transcription factor complex by acetylation. J Mol Med 2003 81: 549 57.
48. 2 and activated carbon fibers. J Colloid Interface Sci 2005 282: 87 91.
49. Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 2001 293: 1653 7.
50. Nusinzon I, Horvath CM. Interferon-stimulated transcription and innate antiviral immunity require deacetylase activity and histone deacetylase. Proc Natl Acad Sci USA 2003 100: 14742 7.
51. Liang MD, Zhang Y, McDevit D, Marecki S, Nikolajczyk BS. The interleukin-1beta gene is transcribed from a poised promoter architecture in monocytes. J Biol Chem 2006 281: 9227 37.
52. Murphy TL, Cleveland MG, Kulesza P, Magram J, Murphy KM. Regulation of interleukin 12 p40 expression through an NF-kappa B half-site. Mol Cell Biol 1995 15: 5258 67.