Epigenetic Mechanisms in Inflammation

Epigenetic modifications occur in response to environmental changes and play a fundamental role in gene expression following environmental stimuli. Major epigenetic events include methylation and acetylation of histones and regulatory factors, DNA methylation, and small non-coding RNAs. Diet, pollution, infections, and other environmental factors have profound effects on epigenetic modifications and trigger susceptibility to diseases. Despite a growing body of literature addressing the role of the environment on gene expression, very little is known about the epigenetic pathways involved in the modulation of inflammatory and anti-inflammatory genes. This review summarizes the current knowledge about epigenetic control mechanisms during the inflammatory response.

[1]  P. Vertino DNA methylation in cancer , 2011 .

[2]  S. Offenbacher,et al.  Altered gene expression in murine placentas in an infection-induced intrauterine growth restriction model: a microarray analysis. , 2010, Journal of reproductive immunology.

[3]  K. Helin,et al.  Polycomb group protein-mediated repression of transcription. , 2010, Trends in biochemical sciences.

[4]  Luca Mazzarella,et al.  Jarid2 is a PRC2 component in embryonic stem cells required for multi-lineage differentiation and recruitment of PRC1 and RNA Polymerase II to developmental regulators , 2010, Nature Cell Biology.

[5]  J. Goldberg,et al.  Helicobacter pylori infection, oncogenic pathways and epigenetic mechanisms in gastric carcinogenesis. , 2010, Future oncology.

[6]  J. Pers,et al.  Epigenetics and autoimmunity. , 2010, Journal of autoimmunity.

[7]  C. McCall,et al.  MicroRNAs Distinguish Translational from Transcriptional Silencing during Endotoxin Tolerance* , 2010, The Journal of Biological Chemistry.

[8]  R. Blumenthal,et al.  Coordinated chromatin control: structural and functional linkage of DNA and histone methylation. , 2010, Biochemistry.

[9]  I. Morita,et al.  Transcriptome Remodeling in Hypoxic Inflammation , 2010, Journal of dentistry research.

[10]  Reid F. Thompson,et al.  Epigenetic basis for fetal origins of age-related disease. , 2010, Journal of women's health.

[11]  Juri Rappsilber,et al.  JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells , 2010, Nature.

[12]  Takeshi Toyoda,et al.  Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells. , 2010, Cancer research.

[13]  H. Tsukamoto,et al.  MeCP2 controls an epigenetic pathway that promotes myofibroblast transdifferentiation and fibrosis. , 2010, Gastroenterology.

[14]  Gang Li,et al.  Jarid2 and PRC2, partners in regulating gene expression. , 2010, Genes & development.

[15]  S. Offenbacher,et al.  Alteration of PTGS2 Promoter Methylation in Chronic Periodontitis , 2010, Journal of dental research.

[16]  J. Jukema,et al.  Epigenetics in atherosclerosis and inflammation , 2010, Journal of cellular and molecular medicine.

[17]  J. Tay,et al.  Age-associated epigenetic modifications in human DNA increase its immunogenicity , 2010, Aging.

[18]  E. Seto,et al.  Histone deacetylases and the immunological network: implications in cancer and inflammation , 2010, Oncogene.

[19]  William Stedman,et al.  Epigenetic Regulation of Kaposi's Sarcoma-Associated Herpesvirus Latency by Virus-Encoded MicroRNAs That Target Rta and the Cellular Rbl2-DNMT Pathway , 2010, Journal of Virology.

[20]  Jialei Hu,et al.  The N-terminus of histone H3 is required for de novo DNA methylation in chromatin , 2009, Proceedings of the National Academy of Sciences.

[21]  S. Orkin,et al.  Jumonji Modulates Polycomb Activity and Self-Renewal versus Differentiation of Stem Cells , 2009, Cell.

[22]  Arend Sidow,et al.  Jarid2/Jumonji Coordinates Control of PRC2 Enzymatic Activity and Target Gene Occupancy in Pluripotent Cells , 2009, Cell.

[23]  H. Leonhardt,et al.  The multi-domain protein Np95 connects DNA methylation and histone modification , 2009, Nucleic acids research.

[24]  H. Soreq,et al.  MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesterase. , 2009, Immunity.

[25]  Sascha Karberg Switching on Epigenetic Therapy , 2009, Cell.

[26]  P. Barnes Targeting the epigenome in the treatment of asthma and chronic obstructive pulmonary disease. , 2009, Proceedings of the American Thoracic Society.

[27]  W. Liu,et al.  A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. , 2009, The Journal of clinical investigation.

[28]  Tin-Lap Lee,et al.  DNA methylation of cancer genome. , 2009, Birth defects research. Part C, Embryo today : reviews.

[29]  T. Kerppola Polycomb group complexes--many combinations, many functions. , 2009, Trends in cell biology.

[30]  Danny Reinberg,et al.  Histones: annotating chromatin. , 2009, Annual review of genetics.

[31]  Kyoko Takahashi,et al.  Epigenetic Regulation of TLR4 Gene Expression in Intestinal Epithelial Cells for the Maintenance of Intestinal Homeostasis1 , 2009, The Journal of Immunology.

[32]  Kevin Struhl,et al.  An Epigenetic Switch Involving NF-κB, Lin28, Let-7 MicroRNA, and IL6 Links Inflammation to Cell Transformation , 2009, Cell.

[33]  A. Pivarcsi,et al.  microRNAs in Inflammation , 2009, International reviews of immunology.

[34]  R. Gay,et al.  Innate immunity, epigenetics and autoimmunity in rheumatoid arthritis. , 2009, Molecular immunology.

[35]  Peter A. Jones,et al.  Rethinking how DNA methylation patterns are maintained , 2009, Nature Reviews Genetics.

[36]  H. Kuwayama,et al.  Helicobacter pylori causes runx3 gene methylation and its loss of expression in gastric epithelial cells, which is mediated by nitric oxide produced by macrophages. , 2009, Biochemical and biophysical research communications.

[37]  Y. Dou,et al.  Epigenetic regulation of the alternatively activated macrophage phenotype. , 2009, Blood.

[38]  Ruslan Medzhitov,et al.  Transcriptional control of the inflammatory response , 2009, Nature Reviews Immunology.

[39]  Robert E. Kingston,et al.  Mechanisms of Polycomb gene silencing: knowns and unknowns , 2009, Nature Reviews Molecular Cell Biology.

[40]  R. Young,et al.  Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells. , 2009, Molecular cell.

[41]  M. El Gazzar,et al.  Aging‐dependent upregulation of IL‐23p19 gene expression in dendritic cells is associated with differential transcription factor binding and histone modifications , 2009, Aging cell.

[42]  Giuseppe Testa,et al.  Jmjd3 contributes to the control of gene expression in LPS-activated macrophages , 2009, The EMBO journal.

[43]  E. Abraham,et al.  miR-147, a microRNA that is induced upon Toll-like receptor stimulation, regulates murine macrophage inflammatory responses , 2009, Proceedings of the National Academy of Sciences.

[44]  M. Fabbri,et al.  Epigenetics, miRNAs, and human cancer: a new chapter in human gene regulation , 2009, Mammalian Genome.

[45]  Xiaoping Chen,et al.  The NF-κB Factor RelB and Histone H3 Lysine Methyltransferase G9a Directly Interact to Generate Epigenetic Silencing in Endotoxin Tolerance* , 2009, The Journal of Biological Chemistry.

[46]  I. Rahman,et al.  Current concepts on the role of inflammation in COPD and lung cancer. , 2009, Current opinion in pharmacology.

[47]  Peter A. Jones,et al.  The tumor suppressor microRNA-101 becomes an epigenetic player by targeting the Polycomb group protein EZH2 in cancer , 2009, Cell cycle.

[48]  Jun Yu,et al.  MicroRNA-143 targets DNA methyltransferases 3A in colorectal cancer , 2009, British Journal of Cancer.

[49]  J. Rinn,et al.  Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression , 2009, Proceedings of the National Academy of Sciences.

[50]  J. Stenvang,et al.  Silencing of microRNA-155 in mice during acute inflammatory response leads to derepression of c/ebp Beta and down-regulation of G-CSF , 2009, Nucleic acids research.

[51]  Gina Lee,et al.  Chronic inflammation, chronic obstructive pulmonary disease, and lung cancer , 2009, Current opinion in pulmonary medicine.

[52]  M. T. McCabe,et al.  Cancer DNA Methylation: Molecular Mechanisms and Clinical Implications , 2009, Clinical Cancer Research.

[53]  A. Wells New Insights into the Molecular Basis of T Cell Anergy: Anergy Factors, Avoidance Sensors, and Epigenetic Imprinting , 2009, The Journal of Immunology.

[54]  Thomas B. Knudsen,et al.  Modulation of TLR2 Protein Expression by miR-105 in Human Oral Keratinocytes* , 2009, The Journal of Biological Chemistry.

[55]  Robert S Illingworth,et al.  CpG islands – ‘A rough guide’ , 2009, FEBS letters.

[56]  Yoonjung Park,et al.  Feed-forward signaling of TNF-alpha and NF-kappaB via IKK-beta pathway contributes to insulin resistance and coronary arteriolar dysfunction in type 2 diabetic mice. , 2009, American journal of physiology. Heart and circulatory physiology.

[57]  K. Fong,et al.  Epigenomic targets for the treatment of respiratory disease , 2009, Expert opinion on therapeutic targets.

[58]  R. Gomez,et al.  Epigenetics and periodontal disease: future perspectives , 2009, Inflammation Research.

[59]  S. Offenbacher,et al.  Epigenetics: Connecting Environment and Genotype to Phenotype and Disease , 2009, Journal of dental research.

[60]  R. Gay,et al.  Epigenetic control in rheumatoid arthritis synovial fibroblasts , 2009, Nature Reviews Rheumatology.

[61]  Ryan M. O’Connell,et al.  Inositol phosphatase SHIP1 is a primary target of miR-155 , 2009, Proceedings of the National Academy of Sciences.

[62]  Yang Shi,et al.  Epigenetic regulation: methylation of histone and non-histone proteins , 2009, Science in China Series C: Life Sciences.

[63]  R. Place,et al.  miR-449a targets HDAC-1 and induces growth arrest in prostate cancer , 2009, Oncogene.

[64]  G. Stein,et al.  Biological Functions of miR-29b Contribute to Positive Regulation of Osteoblast Differentiation* , 2009, The Journal of Biological Chemistry.

[65]  A. Visel,et al.  ChIP-seq accurately predicts tissue-specific activity of enhancers , 2009, Nature.

[66]  A. Urbaniak,et al.  Tyrosine kinases and inflammatory signalling. , 2009, Current molecular medicine.

[67]  D. Levy,et al.  Epigenetic Regulation of Foxp3 Expression in Regulatory T Cells by DNA Methylation1 , 2009, The Journal of Immunology.

[68]  A. Riggs,et al.  Methylation of polycomb target genes in intestinal cancer is mediated by inflammation. , 2008, Cancer research.

[69]  S. Varambally,et al.  Genomic Loss of microRNA-101 Leads to Overexpression of Histone Methyltransferase EZH2 in Cancer , 2008, Science.

[70]  G. Hawkins,et al.  G9a and HP1 Couple Histone and DNA Methylation to TNFα Transcription Silencing during Endotoxin Tolerance* , 2008, Journal of Biological Chemistry.

[71]  J. Pollack,et al.  MYC stimulates EZH2 expression by repression of its negative regulator miR-26a. , 2008, Blood.

[72]  Jennifer A. Erwin,et al.  Polycomb Proteins Targeted by a Short Repeat RNA to the Mouse X Chromosome , 2008, Science.

[73]  S. Gay,et al.  Epigenetic modifications in rheumatoid arthritis , 2008, Arthritis research & therapy.

[74]  R. Medzhitov Origin and physiological roles of inflammation , 2008, Nature.

[75]  Chung F. Wong,et al.  MicroRNA-26a Targets the Histone Methyltransferase Enhancer of Zeste homolog 2 during Myogenesis* , 2008, Journal of Biological Chemistry.

[76]  I. Adcock,et al.  Epigenetic regulation of airway inflammation. , 2007, Current opinion in immunology.

[77]  C. Morrison,et al.  MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B , 2007, Proceedings of the National Academy of Sciences.

[78]  G. Natoli,et al.  The Histone H3 Lysine-27 Demethylase Jmjd3 Links Inflammation to Inhibition of Polycomb-Mediated Gene Silencing , 2007, Cell.

[79]  T. Mikkelsen,et al.  Genome-wide maps of chromatin state in pluripotent and lineage-committed cells , 2007, Nature.

[80]  Michael Weber,et al.  Genomic patterns of DNA methylation: targets and function of an epigenetic mark. , 2007, Current opinion in cell biology.

[81]  A. Feinberg Phenotypic plasticity and the epigenetics of human disease , 2007, Nature.

[82]  K. Sullivan,et al.  Epigenetic Regulation of Tumor Necrosis Factor Alpha , 2007, Molecular and Cellular Biology.

[83]  Dustin E. Schones,et al.  High-Resolution Profiling of Histone Methylations in the Human Genome , 2007, Cell.

[84]  Nathaniel D. Heintzman,et al.  Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome , 2007, Nature Genetics.

[85]  R. Jirtle,et al.  Bacterial Infection Promotes DNA Hypermethylation , 2007, Journal of dental research.

[86]  S. Barros,et al.  Exploring the relationship between periodontal disease and pregnancy complications. , 2006, Journal of the American Dental Association.

[87]  D. Baltimore,et al.  NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses , 2006, Proceedings of the National Academy of Sciences.

[88]  T. Dalmay,et al.  The cartilage specific microRNA‐140 targets histone deacetylase 4 in mouse cells , 2006, FEBS letters.

[89]  James A. Cuff,et al.  A Bivalent Chromatin Structure Marks Key Developmental Genes in Embryonic Stem Cells , 2006, Cell.

[90]  M. Suico,et al.  Promoter hypomethylation of Toll‐like receptor‐2 gene is associated with increased proinflammatory response towardbacterial peptidoglycan in cystic fibrosis bronchial epithelial cells , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[91]  Andreas Houben,et al.  Chromosomal histone modification patterns--from conservation to diversity. , 2006, Trends in plant science.

[92]  K. Lindblad-Toh,et al.  Systematic discovery of regulatory motifs in human promoters and 3′ UTRs by comparison of several mammals , 2005, Nature.

[93]  C. Burge,et al.  Conserved Seed Pairing, Often Flanked by Adenosines, Indicates that Thousands of Human Genes are MicroRNA Targets , 2005, Cell.

[94]  A. Jeltsch,et al.  Biochemistry and biology of mammalian DNA methyltransferases , 2004, Cellular and Molecular Life Sciences CMLS.

[95]  J. Herman,et al.  Gene silencing in cancer in association with promoter hypermethylation. , 2003, The New England journal of medicine.

[96]  R. Gaynor,et al.  Histone H3 phosphorylation by IKK-α is critical for cytokine-induced gene expression , 2003, Nature.

[97]  A. Harel-Bellan,et al.  Histone acetylation and disease , 2001, Cellular and Molecular Life Sciences CMLS.

[98]  Xiaofei Li,et al.  TRANSFORMATION , 2001, Human Rights: Universality and Diversity.

[99]  A. Wilber,et al.  Roles of inflammation in cancer initiation, progression, and metastasis. , 2010, Frontiers in bioscience.

[100]  T. Dunning Periodontal disease--the overlooked diabetes complication. , 2009, Nephrology nursing journal : journal of the American Nephrology Nurses' Association.

[101]  M. Mahmoudi,et al.  Chronic inflammation and oxidative stress as a major cause of age-related diseases and cancer. , 2009, Recent patents on inflammation & allergy drug discovery.

[102]  A. Jeltsch Molecular enzymology of mammalian DNA methyltransferases. , 2006, Current topics in microbiology and immunology.

[103]  R. Gaynor,et al.  Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. , 2003, Nature.

[104]  B. Strahl,et al.  A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. , 2003, Nature.

[105]  Biochemistry and Biology , 1933, Nature.