LPS and poly I:C induce chromatin modifications at a novel upstream region of the IL-23 p19 promoter

Inflammation

Volumn 31, Issue 4, 2008, Pages 235-246

  Garrett, Stacey ^a   Fitzgerald, Michael C ^a   Sullivan, Kathleen E ^a  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

CBP; Chromatin; Cytokines; Gene regulation; Histones; Human; Molecular biology; Monocyte macrophages

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; ENZYME PRECURSOR; FLAGELLIN; HISTONE H3; HISTONE H4; INTERLEUKIN 23P19; LIPOPEPTIDE; LOXORIBINE; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINE; POLYINOSINIC POLYCYTIDYLIC ACID;

ACETYLATION; ARTICLE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIMETHYLATION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; METHYLATION; MONOCYTE; PROMOTER REGION; PROTEIN MODIFICATION; REGULATORY MECHANISM; SPECIES DIFFERENCE; TRIMETHYLATION;

BASE SEQUENCE; CELLS, CULTURED; CHROMATIN; DNA PRIMERS; GENE EXPRESSION; HUMANS; INTERLEUKIN-23 SUBUNIT P19; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; MONOCYTES; POLY I-C; PROMOTER REGIONS (GENETICS); SEQUENCE HOMOLOGY, NUCLEIC ACID; TOLL-LIKE RECEPTORS;

EID: 47549116348     PISSN: 03603997     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10753-008-9070-6     Document Type: Article

References (66)

1. E. Birney 2007 Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project Nature 447 799 816
2. I. Albrecht T. Tapmeier S. Zimmermann M. Frey K. Heeg A. Dalpke 2004 Toll-like receptors differentially induce nucleosome remodelling at the IL-12p40 promoter EMBO Reports 5 172 177
3. F. Altare D. Lammas P. Revy E. Jouanguy R. Doffinger S. Lamhamedi P. Drysdale D. Scheel-Toellner J. Girdlestone P. Darbyshire M. Wadhwa H. Dockrell M. Salmon A. Fischer A. Durandy J. L. Casanova D. S. Kumararatne 1998 Inherited interleukin 12 deficiency in a child with bacille Calmette-Guerin and Salmonella enteritidis disseminated infection J. Clin. Invest 102 2035 2040
4. A. Andersson R. Kokkola J. Wefer H. Erlandsson-Harris R. A. Harris 2004 Differential macrophage expression of IL-12 and IL-23 upon innate immune activation defines rat autoimmune susceptibility J. Leukoc. Biol 76 1118 1124
5. M. L. Belladonna J. C. Renauld R. Bianchi C. Vacca F. Fallarino C. Orabona M. C. Fioretti U. Grohmann P. Puccetti 2002 IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells J. Immunol 168 5448 5454
6. B. E. Bernstein E. L. Humphrey R. L. Erlich R. Schneider P. Bouman J. S. Liu T. Kouzarides S. L. Schreiber 2002 Methylation of histone H3 Lys 4 in coding regions of active genes Proc. Natl. Acad. Sci. U. S. A. 99 8695 8700
7. B. E. Bernstein M. Kamal K. Lindblad-Toh S. Bekiranov D. K. Bailey D. J. Huebert S. McMahon E. K. Karlsson E. J. Kulbokas 3rd T. R. Gingeras S. L. Schreiber E. S. Lander 2005 Genomic maps and comparative analysis of histone modifications in human and mouse Cell 120 169 181
8. A. Billich 2007 Drug evaluation: apilimod, an oral IL-12/IL-23 inhibitor for the treatment of autoimmune diseases and common variable immunodeficiency IDrugs 10 53 59
9. J. P. Butchar M. V. Rajaram L. P. Ganesan K. V. Parsa C. D. Clay L. S. Schlesinger S. Tridandapani 2007 Francisella tularensis induces IL-23 production in human monocytes J. Immunol. 178 4445 4454
10. R. J. Carmody Q. Ruan H. C. Liou Y. H. Chen 2007 Essential roles of c-Rel in TLR-induced IL-23 p19 gene expression in dendritic cells J. Immunol. 178 186 191
11. O. Couronne A. Poliakov N. Bray T. Ishkhanov D. Ryaboy E. Rubin L. Pachter I. Dubchak 2003 Strategies and tools for whole-genome alignments Genome. Res 13 73 80
12. D. J. Cua J. Sherlock Y. Chen C. A. Murphy B. Joyce B. Seymour L. Lucian W. To S. Kwan T. Churakova S. Zurawski M. Wiekowski S. A. Lira D. Gorman R. A. Kastelein J. D. Sedgwick 2003 Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain Nature 421 744 748
13. R. de Jong F. Altare I. A. Haagen D. G. Elferink T. Boer P. J. van Breda Vriesman P. J. Kabel J. M. Draaisma J. T. van Dissel F. P. Kroon J. L. Casanova T. H. Ottenhoff 1998 Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients Science 280 1435 1438
14. K. Decken G. Kohler K. Palmer-Lehmann A. Wunderlin F. Mattner J. Magram M. K. Gately G. Alber 1998 Interleukin-12 is essential for a protective Th1 response in mice infected with Cryptococcus neoformans Infect. Immun. 66 4994 5000
15. R. P. Deering J. S. Orange 2006 Development of a clinical assay to evaluate toll-like receptor function Clin. Vaccine Immunol. 13 68 76
16. R. H. Duerr K. D. Taylor S. R. Brant J. D. Rioux M. S. Silverberg M. J. Daly A. H. Steinhart C. Abraham M. Regueiro A. Griffiths T. Dassopoulos A. Bitton H. Yang S. Targan L. W. Datta E. O. Kistner L. P. Schumm A. T. Lee P. K. Gregersen M. M. Barmada J. I. Rotter D. L. Nicolae J. H. Cho 2006 A genome-wide association study identifies IL23R as an inflammatory bowel disease gene Science 314 1461 1463
17. K. L. Elkins A. Cooper S. M. Colombini S. C. Cowley T. L. Kieffer 2002 In vivo clearance of an intracellular bacterium, Francisella tularensis LVS, is dependent on the p40 subunit of interleukin-12 (IL-12) but not on IL-12 p70 Infect. Immun. 70 1936 1948
18. V. Gafa R. Lande M. C. Gagliardi M. Severa E. Giacomini M. E. Remoli R. Nisini C. Ramoni P. Di Francesco D. Aldebert R. Grillot E. M. Coccia 2006 Human dendritic cells following Aspergillus fumigatus infection express the CCR7 receptor and a differential pattern of interleukin-12 (IL-12), IL-23, and IL-27 cytokines, which lead to a Th1 response Infect. Immun. 74 1480 1489
19. H. S. Goodridge W. Harnett F. Y. Liew M. M. Harnett 2003 Differential regulation of interleukin-12 p40 and p35 induction via Erk mitogen-activated protein kinase-dependent and -independent mechanisms and the implications for bioactive IL-12 and IL-23 responses Immunology 109 415 425
20. S. Goriely D. Demonte S. Nizet D. De Wit F. Willems M. Goldman C. Van Lint 2003 Human IL-12(p35) gene activation involves selective remodeling of a single nucleosome within a region of the promoter containing critical Sp1-binding sites Blood 101 4894 4902
21. R. Grumont H. Hochrein M. O'Keeffe R. Gugasyan C. White I. Caminschi W. Cook S. Gerondakis 2001 c-Rel regulates interleukin 12 p70 expression in CD8(+) dendritic cells by specifically inducing p35 gene transcription J. Exp. Med. 194 1021 1032
22. N. D. Heintzman R. K. Stuart G. Hon Y. Fu C. W. Ching R. D. Hawkins L. O. Barrera S. Van Calcar C. Qu K. A. Ching W. Wang Z. Weng R. D. Green G. E. Crawford B. Ren 2007 Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome Nat. Genet. 39 311 318
23. C. Holscher R. A. Atkinson B. Arendse N. Brown E. Myburgh G. Alber F. Brombacher 2001 A protective and agonistic function of IL-12p40 in mycobacterial infection J. Immunol. 167 6957 6966
24. N. Kadowaki S. Ho S. Antonenko R. W. Malefyt R. A. Kastelein F. Bazan Y. J. Liu 2001 Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens J. Exp. Med. 194 863 869
25. R. A. Kastelein C. A. Hunter D. J. Cua 2007 Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation Annu. Rev. Immunol. 25 221 242
26. S. A. Khader G. K. Bell J. E. Pearl J. J. Fountain J. Rangel-Moreno G. E. Cilley F. Shen S. M. Eaton S. L. Gaffen S. L. Swain R. M. Locksley L. Haynes T. D. Randall A. M. Cooper 2007 IL-23 and IL-17 in the establishment of protective pulmonary CD4+T cell responses after vaccination and during Mycobacterium tuberculosis challenge Nat. Immunol. 8 369 377
27. M. A. Kleinschek U. Muller S. J. Brodie W. Stenzel G. Kohler W. M. Blumenschein R. K. Straubinger T. McClanahan R. A. Kastelein G. Alber 2006 IL-23 enhances the inflammatory cell response in Cryptococcus neoformans infection and induces a cytokine pattern distinct from IL-12 J. Immunol. 176 1098 1106
28. T. Kopp P. Lenz C. Bello-Fernandez R. A. Kastelein T. S. Kupper G. Stingl 2003 IL-23 production by cosecretion of endogenous p19 and transgenic p40 in keratin 14/p40 transgenic mice: evidence for enhanced cutaneous immunity J. Immunol. 170 5438 5444
29. T. Kouzarides 2007 Chromatin modifications and their function Cell 128 693 705
30. C. L. Langrish Y. Chen W. M. Blumenschein J. Mattson B. Basham J. D. Sedgwick T. McClanahan R. A. Kastelein D. J. Cua 2005 IL-23 drives a pathogenic T cell population that induces autoimmune inflammation J. Exp. Med. 201 233 240
31. C. Lapenta S. M. Santini M. Spada S. Donati F. Urbani D. Accapezzato D. Franceschini M. Andreotti V. Barnaba F. Belardelli 2006 IFN-alpha-conditioned dendritic cells are highly efficient in inducing cross-priming CD8(+) T cells against exogenous viral antigens Eur. J. Immunol. 36 2046 2060
32. J. Lehmann S. Bellmann C. Werner R. Schroder N. Schutze G. Alber 2001 IL-12p40-dependent agonistic effects on the development of protective innate and adaptive immunity against Salmonella enteritidis J. Immunol. 167 5304 5315
33. M. Lehner P. Morhart A. Stilper D. Petermann P. Weller D. Stachel W. Holter 2007 Efficient chemokine-dependent migration and primary and secondary IL-12 secretion by human dendritic cells stimulated through Toll-like receptors J. Immunother. (1997) 30 312 322
34. S. Leibundgut-Landmann O. Gross M. J. Robinson F. Osorio E. C. Slack S. V. Tsoni E. Schweighoffer V. Tybulewicz G. D. Brown J. Ruland E. S. C. Reis 2007 Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17 Nat. Immunol. 8 630 638
35. B. Li M. Carey J. L. Workman 2007 The role of chromatin during transcription Cell 128 707 719
36. L. A. Lieberman F. Cardillo A. M. Owyang D. M. Rennick D. J. Cua R. A. Kastelein C. A. Hunter 2004 IL-23 provides a limited mechanism of resistance to acute toxoplasmosis in the absence of IL-12 J. Immunol. 173 1887 1893
37. F. L. Liu C. H. Chen S. J. Chu J. H. Chen J. H. Lai H. K. Sytwu D. M. Chang 2007 Interleukin (IL)-23 p19 expression induced by IL-1{beta} in human fibroblast-like synoviocytes with rheumatoid arthritis via active nuclear factor-{kappa}B and AP-1 dependent pathway Rheumatology 46 8 1266 1273
38. M. Martin K. Rehani R. S. Jope S. M. Michalek 2005 Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3 Nat. Immunol. 6 777 784
39. D. McGovern F. Powrie 2007 The IL23 axis plays a key role in the pathogenesis of IBD Gut 56 1333 1336
40. B. S. McKenzie R. A. Kastelein D. J. Cua 2006 Understanding the IL-23-IL-17 immune pathway Trends. Immunol. 27 17 23
41. S. Mise-Omata E. Kuroda J. Niikura U. Yamashita Y. Obata T. S. Doi 2007 A proximal kappaB site in the IL-23 p19 promoter is responsible for RelA- and c-Rel-dependent transcription J. Immunol. 179 6596 6603
42. K. V. Morris S. W. Chan S. E. Jacobsen D. J. Looney 2004 Small interfering RNA-induced transcriptional gene silencing in human cells Science 305 1289 1292
43. C. A. Murphy C. L. Langrish Y. Chen W. Blumenschein T. McClanahan R. A. Kastelein J. D. Sedgwick D. J. Cua 2003 Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation J. Exp. Med. 198 1951 1957
44. N. Nakano C. Nishiyama S. Kanada Y. Niwa N. Shimokawa H. Ushio M. Nishiyama K. Okumura H. Ogawa 2007 Involvement of mast cells in IL-12/23 p40 production is essential for survival from polymicrobial infections Blood 109 4846 4855
45. L. P. O'Neill B. M. Turner 1995 Histone H4 acetylation distinguishes coding regions of the human genome from heterochromatin in a differentiation-dependent but transcription-independent manner EMBO. J. 14 3946 3957
46. C. Picard C. Fieschi F. Altare S. Al-Jumaah S. Al-Hajjar J. Feinberg S. Dupuis C. Soudais I. Z. Al-Mohsen E. Genin D. Lammas D. S. Kumararatne T. Leclerc A. Rafii H. Frayha B. Murugasu L. B. Wah R. Sinniah M. Loubser E. Okamoto A. Al-Ghonaium H. Tufenkeji L. Abel J. L. Casanova 2002 Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients from six kindreds Am. J. Hum. Genet. 70 336 348
47. J. Pirhonen S. Matikainen I. Julkunen 2002 Regulation of virus-induced IL-12 and IL-23 expression in human macrophages J. Immunol. 169 5673 5678
48. X. L. Rudner K. I. Happel E. A. Young J. E. Shellito 2007 Interleukin-23 (IL-23)-IL-17 cytokine axis in murine Pneumocystis carinii infection Infect. Immun. 75 3055 3061
49. R. Schneider A. J. Bannister F. A. Myers A. W. Thorne C. Crane-Robinson T. Kouzarides 2004 Histone H3 lysine 4 methylation patterns in higher eukaryotic genes Nat. Cell Biol. 6 73 77
50. N. Schuetze S. Schoeneberger U. Mueller M. A. Freudenberg G. Alber R. K. Straubinger 2005 IL-12 family members: differential kinetics of their TLR4-mediated induction by Salmonella enteritidis and the impact of IL-10 in bone marrow-derived macrophages Intern. Immunol. 17 649 659
51. H. H. Smits A. J. van Beelen C. Hessle R. Westland E. de Jong E. Soeteman A. Wold E. A. Wierenga M. L. Kapsenberg 2004 Commensal Gram-negative bacteria prime human dendritic cells for enhanced IL-23 and IL-27 expression and enhanced Th1 development Eur. J. Immunol. 34 1371 1380
52. W. Suhara M. Yoneyama I. Kitabayashi T. Fujita 2002 Direct involvement of CREB-binding protein/p300 in sequence-specific DNA binding of virus-activated interferon regulatory factor-3 holocomplex J. Biol. Chem. 277 22304 22313
53. K. E. Sullivan A. B. Reddy K. Dietzmann A. R. Suriano V. P. Kocieda M. Stewart M. Bhatia 2007 Epigenetic regulation of tumor necrosis factor alpha Mol. Cell. Biol. 27 5147 5160
54. C. Sutton C. Brereton B. Keogh K. H. Mills E. C. Lavelle 2006 A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis J. Exp. Med. 203 1685 1691
55. K. Takeda S. Akira 2004 TLR signaling pathways Semin. Immunol. 16 3 9
56. H. H. Uhlig B. S. McKenzie S. Hue C. Thompson B. Joyce-Shaikh R. Stepankova N. Robinson S. Buonocore H. Tlaskalova-Hogenova D. J. Cua F. Powrie 2006 Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology Immunity 25 309 318
57. M. Utsugi K. Dobashi T. Ishizuka T. Kawata T. Hisada Y. Shimizu A. Ono M. Mori 2006 Rac1 negatively regulates lipopolysaccharide-induced IL-23 p19 expression in human macrophages and dendritic cells and NF-kappaB p65 trans activation plays a novel role J. Immunol. 177 4550 4557
58. S. Vanden Eijnden S. Goriely D. De Wit M. Goldman F. Willems 2006 Preferential production of the IL-12(p40)/IL-23(p19) heterodimer by dendritic cells from human newborns Eur. J. Immunol. 36 21 26
59. M. Veldhoen R. J. Hocking C. J. Atkins R. M. Locksley B. Stockinger 2006 TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells Immunity 24 179 189
60. Y. Wada R. Lu D. Zhou J. Chu T. Przewloka S. Zhang L. Li Y. Wu J. Qin V. Balasubramanyam J. Barsoum M. Ono 2007 Selective abrogation of Th1 response by STA-5326, a potent IL-12/IL-23 inhibitor Blood 109 1156 1164
61. S. M. Wahl I. M. Katona B. M. Stadler R. L. Wilder W. E. Helsel L. M. Wahl 1984 Isolation of human mononuclear cell subsets by counterflow centrifugal elutriation (CCE). II. Functional properties of B-lymphocyte-, T-lymphocyte-, and monocyte-enriched fractions Cell. Imunol. 85 384 395
62. Z. Waibler U. Kalinke J. Will M. H. Juan J. M. Pfeilschifter H. H. Radeke 2007 TLR-ligand stimulated interleukin-23 subunit expression and assembly is regulated differentially in murine plasmacytoid and myeloid dendritic cells Mol. Immunol. 44 1483 1489
63. A. S. Weinmann S. E. Plevy S. T. Smale 1999 Rapid and selective remodeling of a positioned nucleosome during the induction of IL-12 p40 transcription Immunity 11 665 675
64. C. S. Yang C. H. Song J. S. Lee S. B. Jung J. H. Oh J. Park H. J. Kim J. K. Park T. H. Paik E. K. Jo 2006 Intracellular network of phosphatidylinositol 3-kinase, mammalian target of the rapamycin/70 kDa ribosomal S6 kinase 1, and mitogen-activated protein kinases pathways for regulating mycobacteria-induced IL-23 expression in human macrophages Cell. Microbiol. 8 1158 1171
65. T. Zelante A. De Luca P. Bonifazi C. Montagnoli S. Bozza S. Moretti M. L. Belladonna C. Vacca C. Conte P. Mosci F. Bistoni P. Puccetti R. A. Kastelein M. Kopf L. Romani 2007 IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance Eur. J. Immunol. 37 2695 2706
66. L. Zhou A. A. Nazarian J. Xu D. Tantin L. M. Corcoran S. T. Smale 2007 An inducible enhancer required for IL-12b promoter activity in an insulated chromatin environment Mol. Cell. Biol. 27 2698 2712