Home LiteratureArticle Details
PMID: 21068722 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Suppression of inflammation by a synthetic histone mimic.

Nature ·Vol. 468 ·No. 7327 ·2010-12-23 ·Pages 1119-23

Nicodeme E, Jeffrey KL, Schaefer U, Beinke S, Dewell S, Chung CW, Chandwani R, Marazzi I, Wilson P, Coste H, White J, Kirilovsky J, Rice CM, Lora JM, Prinjha RK, Lee K, Tarakhovsky A

Abstract

Interaction of pathogens with cells of the immune system results in activation of inflammatory gene expression. This response, although vital for immune defence, is frequently deleterious to the host due to the exaggerated production of inflammatory proteins. The scope of inflammatory responses reflects the activation state of signalling proteins upstream of inflammatory genes as well as signal-induced assembly of nuclear chromatin complexes that support mRNA expression. Recognition of post-translationally modified histones by nuclear proteins that initiate mRNA transcription and support mRNA elongation is a critical step in the regulation of gene expression. Here we present a novel pharmacological approach that targets inflammatory gene expression by interfering with the recognition of acetylated histones by the bromodomain and extra terminal domain (BET) family of proteins. We describe a synthetic compound (I-BET) that by 'mimicking' acetylated histones disrupts chromatin complexes responsible for the expression of key inflammatory genes in activated macrophages, and confers protection against lipopolysaccharide-induced endotoxic shock and bacteria-induced sepsis. Our findings suggest that synthetic compounds specifically targeting proteins that recognize post-translationally modified histones can serve as a new generation of immunomodulatory drugs.

MeSH Terms
Acetylation/drug effects Animals Anti-Inflammatory Agents/chemistry,pharmacology,therapeutic use Benzodiazepines Cells, Cultured Epigenomics Gene Expression Regulation/drug effects Genome-Wide Association Study Heterocyclic Compounds, 4 or More Rings/chemistry,pharmacology,therapeutic use Histone Deacetylase Inhibitors/pharmacology Hydroxamic Acids/pharmacology Inflammation/drug therapy,prevention & control Kaplan-Meier Estimate Lipopolysaccharides/pharmacology Macrophages/drug effects Mice Mice, Inbred C57BL Models, Molecular Protein Serine-Threonine Kinases/metabolism Protein Structure, Tertiary Salmonella Infections/drug therapy,immunology,physiopathology,prevention & control Salmonella typhimurium Sepsis/drug therapy,prevention & control Shock, Septic/drug therapy,prevention & control
Chemicals
Anti-Inflammatory Agents Heterocyclic Compounds, 4 or More Rings Histone Deacetylase Inhibitors Hydroxamic Acids Lipopolysaccharides Benzodiazepines trichostatin A molibresib Protein Serine-Threonine Kinases
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Nicodeme Edwige
Centre de Recherche GSK, 27 Avenue du Québec, 91140 Villebon Sur Yvette, France.
Jeffrey Kate L
Schaefer Uwe
Beinke Soren
Dewell Scott
Chung Chun-Wa
Chandwani Rohit
Marazzi Ivan
Wilson Paul
Coste Hervé
White Julia
Kirilovsky Jorge
Rice Charles M
Lora Jose M
Prinjha Rab K
Lee Kevin
Tarakhovsky Alexander
References (27)
27 references, click to expand
  1. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4.
    Mol Cell. 2005 Aug 19;19(4):535-45 PMID: 16109377
  2. Solution structure of the second bromodomain of Brd2 and its specific interaction with acetylated histone tails.
    BMC Struct Biol. 2007 Sep 12;7:57 PMID: 17848202
  3. An extensive network of coupling among gene expression machines.
    Nature. 2002 Apr 4;416(6880):499-506 PMID: 11932736
  4. Control of inducible gene expression by signal-dependent transcriptional elongation.
    Cell. 2009 Jul 10;138(1):129-45 PMID: 19596240
  5. Mammalian mediator of transcriptional regulation and its possible role as an end-point of signal transduction pathways.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8538-43 PMID: 9671713
  6. Elongation by RNA polymerase II: the short and long of it.
    Genes Dev. 2004 Oct 15;18(20):2437-68 PMID: 15489290
  7. Multivalent engagement of chromatin modifications by linked binding modules.
    Nat Rev Mol Cell Biol. 2007 Dec;8(12):983-94 PMID: 18037899
  8. Transcriptional control of the inflammatory response.
    Nat Rev Immunol. 2009 Oct;9(10):692-703 PMID: 19859064
  9. Structures of the dual bromodomains of the P-TEFb-activating protein Brd4 at atomic resolution.
    J Biol Chem. 2009 Dec 25;284(52):36547-36556 PMID: 19828451
  10. Control of NF-kappaB-dependent transcriptional responses by chromatin organization.
    Cold Spring Harb Perspect Biol. 2009 Oct;1(4):a000224 PMID: 20066094
  11. Expression and characterization of recombinant human acyloxyacyl hydrolase, a leukocyte enzyme that deacylates bacterial lipopolysaccharides.
    Biochemistry. 1991 Aug 27;30(34):8415-23 PMID: 1883828
  12. Translating the histone code.
    Science. 2001 Aug 10;293(5532):1074-80 PMID: 11498575
  13. Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response.
    Genes Dev. 2006 Feb 1;20(3):282-96 PMID: 16452502
  14. Selective transcription in response to an inflammatory stimulus.
    Cell. 2010 Mar 19;140(6):833-44 PMID: 20303874
  15. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription.
    Mol Cell. 2005 Aug 19;19(4):523-34 PMID: 16109376
  16. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers.
    Nat Struct Mol Biol. 2007 Nov;14(11):1025-1040 PMID: 17984965
  17. Chromatin immunoprecipitation and microarray-based analysis of protein location.
    Nat Protoc. 2006;1(2):729-48 PMID: 17406303
  18. Brd4 coactivates transcriptional activation of NF-kappaB via specific binding to acetylated RelA.
    Mol Cell Biol. 2009 Mar;29(5):1375-87 PMID: 19103749
  19. Identification of transcription complexes that contain the double bromodomain protein Brd2 and chromatin remodeling machines.
    J Proteome Res. 2006 Mar;5(3):502-11 PMID: 16512664
  20. The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription.
    Mol Cell. 2008 Apr 11;30(1):51-60 PMID: 18406326
  21. Brd4 is required for recovery from antimicrotubule drug-induced mitotic arrest: preservation of acetylated chromatin.
    Mol Biol Cell. 2006 Feb;17(2):814-23 PMID: 16339075
  22. Structural basis and binding properties of the second bromodomain of Brd4 with acetylated histone tails.
    Biochemistry. 2008 Jun 17;47(24):6403-17 PMID: 18500820
  23. Immunodesign of experimental sepsis by cecal ligation and puncture.
    Nat Protoc. 2009;4(1):31-6 PMID: 19131954
  24. Pyrin critical to macrophage IL-1beta response to Francisella challenge.
    J Immunol. 2009 Jun 15;182(12):7982-9 PMID: 19494323
  25. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase.
    J Biol Chem. 1996 Oct 25;271(43):27176-83 PMID: 8900211
  26. Distinct factors control histone variant H3.3 localization at specific genomic regions.
    Cell. 2010 Mar 5;140(5):678-91 PMID: 20211137
  27. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling.
    Cell. 2009 Jul 10;138(1):114-28 PMID: 19596239
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2010-12-23
Epub
2010-00-10
Pages
1119-23
Language
English
Region
England
NLM ID
0410462
PMCID
PMC5415086
Subset
IM
Grants
NIAID NIH HHS · R21 AI077018 · United States
Databases
PDB
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com