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
-
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
-
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
-
An extensive network of coupling among gene expression machines.
Nature. 2002 Apr 4;416(6880):499-506
PMID: 11932736
-
Control of inducible gene expression by signal-dependent transcriptional elongation.
Cell. 2009 Jul 10;138(1):129-45
PMID: 19596240
-
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
-
Elongation by RNA polymerase II: the short and long of it.
Genes Dev. 2004 Oct 15;18(20):2437-68
PMID: 15489290
-
Multivalent engagement of chromatin modifications by linked binding modules.
Nat Rev Mol Cell Biol. 2007 Dec;8(12):983-94
PMID: 18037899
-
Transcriptional control of the inflammatory response.
Nat Rev Immunol. 2009 Oct;9(10):692-703
PMID: 19859064
-
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
-
Control of NF-kappaB-dependent transcriptional responses by chromatin organization.
Cold Spring Harb Perspect Biol. 2009 Oct;1(4):a000224
PMID: 20066094
-
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
-
Translating the histone code.
Science. 2001 Aug 10;293(5532):1074-80
PMID: 11498575
-
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
-
Selective transcription in response to an inflammatory stimulus.
Cell. 2010 Mar 19;140(6):833-44
PMID: 20303874
-
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
-
How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers.
Nat Struct Mol Biol. 2007 Nov;14(11):1025-1040
PMID: 17984965
-
Chromatin immunoprecipitation and microarray-based analysis of protein location.
Nat Protoc. 2006;1(2):729-48
PMID: 17406303
-
Brd4 coactivates transcriptional activation of NF-kappaB via specific binding to acetylated RelA.
Mol Cell Biol. 2009 Mar;29(5):1375-87
PMID: 19103749
-
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
-
The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription.
Mol Cell. 2008 Apr 11;30(1):51-60
PMID: 18406326
-
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
-
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
-
Immunodesign of experimental sepsis by cecal ligation and puncture.
Nat Protoc. 2009;4(1):31-6
PMID: 19131954
-
Pyrin critical to macrophage IL-1beta response to Francisella challenge.
J Immunol. 2009 Jun 15;182(12):7982-9
PMID: 19494323
-
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
-
Distinct factors control histone variant H3.3 localization at specific genomic regions.
Cell. 2010 Mar 5;140(5):678-91
PMID: 20211137
-
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