Genome-wide analysis of STAT3 binding in vivo predicts effectors of the anti-inflammatory response in macrophages

Blood

Volumn 119, Issue 13, 2012, Pages

  Hutchins, Andrew Paul ^a   Poulain, Stéphane ^a   Miranda Saavedra, Diego ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; STAT3 PROTEIN; TRANSCRIPTOME;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE TARGETING; GENETIC ANALYSIS; GENETIC ASSOCIATION; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERITONEUM MACROPHAGE; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RNA SEQUENCE; TRANSCRIPTION REGULATION;

EID: 84859324848     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-09-381483     Document Type: Article

References (54)

1. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140(6):805-820.
2. Medzhitov R. Origin and physiological roles of inflammation. Nature. 2008;454(7203):428-435.
3. Riley JK, Takeda K, Akira S, Schreiber RD. Interleukin-10 receptor signaling through the JAKSTAT pathway. Requirement for two distinct receptor-derived signals for anti-inflammatory action. J Biol Chem. 1999;274(23):16513-16521.
4. Murray PJ. Understanding and exploiting the endogenous interleukin-10/STAT3-mediated antiinflammatory response. Curr Opin Pharmacol. 2006;6(4):379-386.
5. Kuwata H, Watanabe Y, Miyoshi H, et al. IL-10-inducible Bcl-3 negatively regulates LPS-induced TNF-alpha production in macrophages. Blood. 2003;102(12):4123-4129. (Pubitemid 37486997)
6. El Kasmi KC, Smith AM, Williams L, et al. Cutting edge: A transcriptional repressor and corepressor induced by the STAT3-regulated anti-inflammatory signaling pathway. J Immunol. 2007;179(11):7215-7219.
7. Lee TS, Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med. 2002;8(3):240-246.
8. Weaver BK, Bohn E, Judd BA, Gil MP, Schreiber RD. ABIN-3: a molecular basis for species divergence in interleukin-10-induced anti-inflammatory actions. Mol Cell Biol. 2007;27(13):4603-4616. (Pubitemid 47016116)
9. Hirotani T, Lee PY, Kuwata H, et al. The nuclear IkappaB protein IkappaBNS selectively inhibits lipopolysaccharide-induced IL-6 production in macrophages of the colonic lamina propria. J Immunol. 2005;174(6):3650-3657. (Pubitemid 40354075)
10. Kuwata H, Matsumoto M, Atarashi K, et al. IkappaBNS inhibits induction of a subset of Toll-like receptor-dependent genes and limits inflammation. Immunity. 2006;24(1):41-51. (Pubitemid 43077199)
11. Schaljo B, Kratochvill F, Gratz N, et al. Tristetraprolin is required for full anti-inflammatory response of murine macrophages to IL-10. J Immunol. 2009;183(2):1197-1206.
12. McCoy CE, Sheedy FJ, Qualls JE, et al. IL-10 inhibits miR-155 induction by toll-like receptors. J Biol Chem. 2010;285(27):20492-20498.
13. Northrup DL, Zhao K. Application of ChIP-Seq and related techniques to the study of immune function. Immunity. 2011;34(6):830-842.
14. Lang R, Patel D, Morris JJ, Rutschman RL, Murray PJ. Shaping gene expression in activated and resting primary macrophages by IL-10. J Immunol. 2002;169(5):2253-2263. (Pubitemid 34920965)
15. Wederell ED, Bilenky M, Cullum R, et al. Global analysis of in vivo Foxa2-binding sites in mouse adult liver using massively parallel sequencing. Nucleic Acids Res. 2008;36(14):4549-4564.
16. Chen X, Xu H, Yuan P, et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell. 2008;133(6):1106-1117. (Pubitemid 351787745)
17. Matys V, Kel-Margoulis OV, Fricke E, et al. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 2006;34(Database issue):D108-D110.
18. Thomas-Chollier M, Sand O, Turatsinze JV, et al. RSAT: regulatory sequence analysis tools. Nucleic Acids Res. 2008;36(Web issue):W119-W127.
19. Stephanou A, Latchman DS. Opposing actions of STAT-1 and STAT-3. Growth Factors. 2005;23(3):177-182. (Pubitemid 43203048)
20. Heinz S, Benner C, Spann N, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38(4):576-589.
21. Kwon H, Thierry-Mieg D, Thierry-Mieg J, et al. Analysis of interleukin-21-induced Prdm1 gene regulation reveals functional cooperation of STAT3 and IRF4 transcription factors. Immunity. 2009;31(6):941-952.
22. Conlon EM, Liu XS, Lieb JD, Liu JS. Integrating regulatory motif discovery and genome-wide expression analysis. Proc Natl Acad Sci U S A. 2003;100(6):3339-3344. (Pubitemid 36356585)
23. Siepel A, Bejerano G, Pedersen JS, et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 2005;15(8):1034-1050. (Pubitemid 41126859)
24. Schmidt D, Wilson MD, Ballester B, et al. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science. 2010;328(5981):1036-1040.
25. McLean CY, Bristor D, Hiller M, et al. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol. 2010;28(5):495-501.
26. Trapnell C, Williams BA, Pertea G, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-515.
27. Dewilde S, Vercelli A, Chiarle R, Poli V. Of alphas and betas: distinct and overlapping functions of STAT3 isoforms. Front Biosci. 2008;13:6501-6514.
28. Smith AM, Qualls JE, O'Brien K, et al. A distal enhancer in Il12b is the target of transcriptional repression by the STAT3 pathway and requires the basic leucine zipper (B-ZIP) protein NFIL3. J Biol Chem. 2011;286(26):23582-23590.
29. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57.
30. Murray PJ. The primary mechanism of the IL-10-regulated anti-inflammatory response is to selectively inhibit transcription. Proc Natl Acad Sci U S A. 2005;102(24):8686-8691. (Pubitemid 40862796)
31. Fulton DL, Sundararajan S, Badis G, et al. TFCat: the curated catalog of mouse and human transcription factors. Genome Biol. 2009;10(3):R29.
32. Wilson D, Charoensawan V, Kummerfeld SK, Teichmann SA. DBD-taxonomically broad transcription factor predictions: new content and functionality. Nucleic Acids Res. 2008;36(Database issue):D88-D92. (Pubitemid 351149701)
33. John LB, Ward AC. The Ikaros gene family: transcriptional regulators of hematopoiesis and immunity. Mol Immunol. 2011;48(9-10):1272-1278.
34. Cho SJ, Huh JE, Song J, Rhee DK, Pyo S. Ikaros negatively regulates inducible nitric oxide synthase expression in macrophages: involvement of Ikaros phosphorylation by casein kinase 2. Cell Mol Life Sci. 2008;65(20):3290-3303.
35. Welch JS, Ricote M, Akiyama TE, Gonzalez FJ, Glass CK. PPARgamma and PPARdelta negatively regulate specific subsets of lipopolysaccharide and IFN-gamma target genes in macrophages. Proc Natl Acad Sci U S A. 2003;100(11):6712-6717. (Pubitemid 36666645)
36. Han S, Lu J, Zhang Y, et al. Recruitment of histone deacetylase 4 by transcription factors represses interleukin-5 transcription. Biochem J. 2006;400(3):439-448. (Pubitemid 44974455)
37. Pascual G, Glass CK. Nuclear receptors versus inflammation: mechanisms of transrepression. Trends Endocrinol Metab. 2006;17(8):321-327. (Pubitemid 44397567)
38. Yamamoto M, Yamazaki S, Uematsu S, et al. Regulation of Toll/IL-1-receptor-mediated gene expression by the inducible nuclear protein IkappaBzeta. Nature. 2004;430(6996):218-222. (Pubitemid 38902431)
39. Kayama H, Ramirez-Carrozzi VR, Yamamoto M, et al. Class-specific regulation of proinflammatory genes by MyD88 pathways and IkappaBzeta. J Biol Chem. 2008;283(18):12468-12477.
40. Mestre JR, Rivadeneira DE, Mackrell PJ, et al. Overlapping CRE and E-box promoter elements can independently regulate COX-2 gene transcription in macrophages. FEBS Lett. 2001;496(2-3):147-151. (Pubitemid 32441816)
41. Childs KS, Goodbourn S. Identification of novel co-repressor molecules for Interferon Regulatory Factor-2. Nucleic Acids Res. 2003;31(12):3016-3026. (Pubitemid 37441759)
42. Carneiro FR, Ramalho-Oliveira R, Mognol GP, Viola JP. Interferon regulatory factor 2 binding protein 2 is a new NFAT1 partner and represses its transcriptional activity. Mol Cell Biol. 2011;31(14):2889-2901.
43. Atkey MR, Lachance JF, Walczak M, Rebello T, Nilson LA. Capicua regulates follicle cell fate in the Drosophila ovary through repression of mirror. Development. 2006;133(11):2115-2123. (Pubitemid 43986122)
44. Houlard M, Arudchandran R, Regnier-Ricard F, et al. Vav1 is a component of transcriptionally active complexes. J Exp Med. 2002;195(9):1115-1127. (Pubitemid 34517138)
45. Akazawa H, Kudoh S, Mochizuki N, et al. A novel LIM protein Cal promotes cardiac differentiation by association with CSX/NKX2-5. J Cell Biol. 2004;164(3):395-405. (Pubitemid 38174767)
46. Wang F, Liu H, Blanton WP, Belkina A, Lebrasseur NK, Denis GV. Brd2 disruption in mice causes severe obesity without Type 2 diabetes. Biochem J. 2010;425(1):71-83.
47. Gazzinelli RT, Wysocka M, Hieny S, et al. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J Immunol. 1996;157(2):798-805. (Pubitemid 26231385)
48. Hunter CA, Ellis-Neyes LA, Slifer T, et al. IL-10 is required to prevent immune hyperactivity during infection with Trypanosoma cruzi. J Immunol. 1997;158(7):3311-3316. (Pubitemid 127484048)
49. Vallania F, Schiavone D, Dewilde S, et al. Genome-wide discovery of functional transcription factor binding sites by comparative genomics: the case of Stat3. Proc Natl Acad Sci U S A. 2009;106(13):5117-5122.
50. Kobayashi T, Matsuoka K, Sheikh SZ, et al. NFIL3 is a regulator of IL-12 p40 in macrophages and mucosal immunity. J Immunol. 2011;186(8):4649-4655.
51. Pranda AL, Metz S, Hermann, A, Heinrich PC, Muller-Newman G. Real time analysis of STAT3 nucleocytoplasmic shutting. J. Biol Chem. 2004;279(15):15114- 15123. (Pubitemid 38618906)
52. Williams L, Bradley L, Smith A, Foxwell B. Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J Immunol. 2004;172(1):567-576. (Pubitemid 38020514)
53. Rossato M, Cencig S, Gasperini S, Cassatella MA, Bazzoni F. IL-10 modulates cytokine gene transcription by protein synthesis-independent and dependent mechanisms in lipopolysaccharide-treated neutrophils. Eur J Immunol. 2007;37(11):3176-3189. (Pubitemid 350131296)
54. Nathan C, Ding A. Nonresolving inflammation. Cell. 2010;140(6):871-882.