The Emerging Role of Epigenetics in Inflammation and Immunometabolism

Trends in Endocrinology and Metabolism

Volumn 27, Issue 11, 2016, Pages 782-795

  Raghuraman, Sukanya ^a   Donkin, Ida ^b   Versteyhe, Soetkin ^b   Barrès, Romain ^a,b   Simar, David ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b Capital Region   (Denmark)

Author keywords

epigenetics; immune system; inflammation; metabolic diseases; obesity

Indexed keywords

UNTRANSLATED RNA;

CELL FUNCTION; DNA METHYLATION; EPIGENETICS; GENE TARGETING; GENETIC IDENTIFICATION; HISTONE MODIFICATION; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOCOMPETENT CELL; INFLAMMATION; METABOLIC DISORDER; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; ANIMAL; GENETIC EPIGENESIS; GENETICS;

ANIMALS; DIABETES MELLITUS, TYPE 2; EPIGENESIS, GENETIC; HUMANS; INFLAMMATION; METABOLIC DISEASES; OBESITY;

EID: 84994491866     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2016.06.008     Document Type: Review

References (93)

1. 1 Williamson, R.T., On the treatment of glycosuria and diabetes mellitus with sodium salicylate. Brit. Med. J. 1 (1901), 760–762.
2. 2 Hotamisligil, G.S., et al. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259 (1993), 87–91.
3. 3 Sell, H., et al. Adaptive immunity in obesity and insulin resistance. Nat. Rev. Endocrinol. 8 (2012), 709–716.
4. 4 Stienstra, R., et al. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab. 12 (2010), 593–605.
5. 5 Vandanmagsar, B., et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17 (2011), 179–188.
6. 6 Winer, D.A., et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 17 (2011), 610–617.
7. 7 Feuerer, M., et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 15 (2009), 930–939.
8. + effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 15 (2009), 914–920.
9. 9 Barrès, R., et al. Weight loss after gastric bypass surgery in human obesity remodels promoter methylation. Cell Rep. 3 (2013), 1020–1027.
10. 10 Lawson, B.R., et al. Transmethylation in immunity and autoimmunity. Clin. Immunol. 143 (2012), 8–21.
11. 11 Floess, S., et al. Epigenetic control of the Foxp3 locus in regulatory T cells. PLoS Biol., 5, 2007, e38.
12. 12 Lee, D.U., et al. Th2 lineage commitment and efficient IL-4 production involves extended demethylation of the IL-4 gene. Immunity 16 (2002), 649–660.
13. 13 Mullen, A.C., et al. Hlx is induced by and genetically interacts with T-bet to promote heritable TH1 gene induction. Nat. Immunol. 3 (2002), 652–658.
14. 14 Scharer, C.D., et al. Global DNA methylation remodeling accompanies CD8 T cell effector function. J. Immunol. 191 (2013), 3419–3429.
15. 15 Shaknovich, R., et al. DNA methyltransferase 1 and DNA methylation patterning contribute to germinal center B-cell differentiation. Blood 118 (2011), 3559–3569.
16. 16 Yang, X., et al. Epigenetic regulation of macrophage polarization by DNA methyltransferase 3b. Mol. Endocrinol. 28 (2014), 565–574.
17. 17 Wierda, R.J., et al. Epigenetic control of CCR5 transcript levels in immune cells and modulation by small molecules inhibitors. J. Cell. Mol. Med. 16 (2012), 1866–1877.
18. 18 Schoenborn, J.R., et al. Comprehensive epigenetic profiling identifies multiple distal regulatory elements directing transcription of the gene encoding interferon-γ. Nat. Immunol. 8 (2007), 732–742.
19. + T Cell differentiation and functionality. J. Immunol. 184 (2010), 4631–4636.
20. 20 Waibel, M., et al. Manipulation of B-cell responses with histone deacetylase inhibitors. Nat. Commun., 6, 2015, 6838.
21. 21 Saeed, S., et al. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science, 345, 2014, 1251086.
22. 22 Takeuch, O., et al. Epigenetic control of macrophage polarization. Eur. J. Immunol. 41 (2011), 2490–2493.
23. 23 Chen, X., et al. Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 2865–2874.
24. 24 Zhang, Q., et al. Tet2 is required to resolve inflammation by recruiting Hdac2 to specifically repress IL-6. Nature 525 (2015), 389–393.
25. 25 Iglesias, M.J., et al. Combined chromatin and expression analysis reveals specific regulatory mechanisms within cytokine genes in the macrophage early immune response. PLoS ONE, 7, 2012, e32306.
26. 26 Mullican, S.E., et al. Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev. 25 (2011), 2480–2488.
27. 27 Foster, S.L., et al. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447 (2007), 972–978.
28. 28 Schmidt, S.V., et al. The transcriptional regulator network of human inflammatory macrophages is defined by open chromatin. Cell Res. 26 (2016), 151–170.
29. 29 Kiguchi, N., et al. Epigenetic augmentation of the macrophage inflammatory protein 2/C-X-C chemokine receptor type 2 axis through histone H3 acetylation in injured peripheral nerves elicits neuropathic pain. J. Pharmacol. Exp. Ther. 340 (2012), 577–587.
30. 30 Kiguchi, N., et al. Epigenetic upregulation of CCL2 and CCL3 via histone modifications in infiltrating macrophages after peripheral nerve injury. Cytokine 64 (2013), 666–672.
31. 31 Bannister, A.J., et al. Regulation of chromatin by histone modifications. Cell Res. 21 (2011), 381–395.
32. 32 Wellen, K.E., et al. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324 (2009), 1076–1080.
33. +-dependent SIRT1 deacetylase participates in epigenetic reprogramming during endotoxin tolerance. J. Biol. Chem. 286 (2011), 9856–9864.
34. 34 Zhao, K., et al. Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95 (1998), 625–636.
35. 35 Chen, C-Z., et al. Regulation of immune responses and tolerance: the microRNA perspective. Immunol. Rev. 253 (2013), 112–128.
36. 36 Lee, H-M., et al. Progress and challenge of microRNA research in immunity. Front. Genet., 5, 2014, 178.
37. 37 Heward, J.A., et al. Long non-coding RNAs in the regulation of the immune response. Trends Immunol. 35 (2014), 408–419.
38. 38 Chen, C-Z., et al. MicroRNAs modulate hematopoietic lineage differentiation. Science 303 (2004), 83–86.
39. 39 Luo, S., et al. The role of microRNA-1246 in the regulation of B cell activation and the pathogenesis of systemic lupus erythematosus. Clin. Epigenetics, 7, 2015, 24.
40. 40 Marcais, A., et al. microRNA-mediated regulation of mTOR complex components facilitates discrimination between activation and anergy in CD4 T cells. J. Exp. Med. 211 (2014), 2281–2295.
41. + T cell subsets cytokine exposure alone drives miR-146a expression. J. Transl. Med. 12 (2014), 292–303.
42. 42 Kelada, S., et al. miR-182 and miR-10a are key regulators of Treg specialisation and stability during schistosome and leishmania-associated inflammation. PLoS Pathog., 9, 2013, e1003451.
43. + T lymphocytes by targeting PRKCɛ. Eur. J. Immunol. 45 (2014), 260–272.
44. 44 Okoye, I.S., et al. Transcriptomics identified a critical role for Th2 cell-intrinsic miR-155 in mediating allergy and antihelminth immunity. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 3081–3090.
45. 45 Ceppi, M., et al. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 106 (2009), 2735–2740.
46. + neonatal monocytes via post-transcriptional regulation. J. Leukoc. Biol. 92 (2012), 171–182.
47. 47 Jennewein, C., et al. MicroRNA-27b contributes to lipopolysaccharide-mediated peroxisome proliferator-activated receptor (PPAR) mRNA Destabilization. J. Biol. Chem. 285 (2010), 11846–11853.
48. 48 Sheedy, F.J., et al. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat. Immunol. 11 (2009), 141–147.
49. 49 Cheng, N-L., et al. MicroRNA-125b modulates inflammatory chemokine CCL4 expression in immune cells and its reduction causes CCL4 increase with age. Aging Cell 14 (2015), 200–208.
50. 50 van Dijk, S.J., et al. Epigenetics and human obesity. Int. J. Obes. 39 (2014), 85–97.
51. 51 Ng, S-F., et al. Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 467 (2010), 963–966.
52. 52 Wang, X., et al. Obesity related methylation changes in DNA of peripheral blood leukocytes. BMC Med., 8, 2010, 87.
53. 53 Hermsdorff, H.H., et al. TNF-alpha promoter methylation in peripheral white blood cells: relationship with circulating TNFα, truncal fat and n-6 PUFA intake in young women. Cytokine 64 (2013), 265–271.
54. 54 Zhao, J., et al. Global DNA methylation is associated with insulin resistance: a monozygotic twin study. Diabetes 61 (2012), 542–546.
55. 55 Simar, D., et al. DNA methylation is altered in B and NK lymphocytes in obese and type 2 diabetic human. Metabolism 63 (2014), 1188–1197.
56. 56 Abu-Farha, M., et al. Proteomics analysis of human obesity reveals the epigenetic factor HDAC4 as a potential Target for obesity. PLoS ONE, 8, 2013, e75342.
57. 57 Miao, F., et al. In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions. J. Biol. Chem. 279 (2004), 18091–18097.
58. 58 Li, Y., et al. Role of the histone H3 lysine 4 methyltransferase, SET7/9, in the regulation of NF-κB-dependent inflammatory genes: relevance to diabetes and inflammation. J. Biol. Chem. 283 (2008), 26771–26781.
59. 59 Tian, W., et al. Brahma-related gene 1 bridges epigenetic regulation of proinflammatory cytokine production to steatohepatitis in mice. Hepatology 58 (2013), 576–588.
60. 60 Mikula, M., et al. Obesity increases histone H3 lysine 9 and 18 acetylation at Tnfa and Ccl2 genes in mouse liver. Int. J. Mol. Med. 34 (2014), 1647–1654.
61. 61 Gillum, M.P., et al. SirT1 regulates adipose tissue inflammation. Diabetes 60 (2011), 3235–3245.
62. 62 Christensen, D.P., et al. Histone deacetylase (HDAC) inhibition as a novel treatment for diabetes mellitus. Mol. Med. 17 (2011), 378–390.
63. 63 Tao, R., et al. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat. Med. 13 (2007), 1299–1307.
64. 64 Hulsmans, M., et al. Decrease of miR-146b-5p in monocytes during obesity is associated with loss of the anti-inflammatory but not insulin signaling action of adiponectin. PLoS ONE, 7, 2012, e32794.
65. 65 Balasubramanyam, M., et al. Impaired miR-146a expression links subclinical inflammation and insulin resistance in Type 2 diabetes. Mol. Cell. Bioch. 351 (2011), 197–205.
66. 66 Foley, N.H., et al. miR-107: a Toll-like receptor-regulated miRNA dysregulated in obesity and type II diabetes. J. Leukoc. Biol. 92 (2012), 521–527.
67. 67 Vatandoost, N., et al. Dysregulated miR-103 and miR-143 expression in peripheral blood mononuclear cells from induced prediabetes and type 2 diabetes rats. Gene 572 (2015), 95–100.
68. 68 Xie, H., et al. MicroRNAs induced during adipogenesis that accelerate fat cell development are downregulated in obesity. Diabetes 58 (2009), 1050–1057.
69. 69 Arner, E., et al. Adipose tissue microRNAs as regulators of CCL2 production in human obesity. Diabetes 61 (2012), 1986–1993.
70. 70 Zheng, L., et al. Effect of miRNA-10b in regulating cellular steatosis level by targeting PPAR-α expression, a novel mechanism for the pathogenesis of NAFLD. J. Gastroenterol. Hepatol. 25 (2010), 156–163.
71. 71 Abente, E.J., et al. MicroRNAs in obesity-associated disorders. Arch. Biochem. Biophys. 589 (2016), 108–119.
72. 72 Feng, Y.Y., et al. Aberrant hepatic microRNA expression in nonalcoholic fatty liver disease. Cell. Physiol. Biochem. 34 (2014), 1983–1997.
73. 73 Hur, W., et al. Downregulation of microRNA-451 in non-alcoholic steatohepatitis inhibits fatty acid-induced proinflammatory cytokine production through the AMPK/AKT pathway. Int. J. Biochem. Cell Biol. 64 (2015), 265–276.
74. 74 Reddy, M.A., et al. Regulation of inflammatory phenotype in macrophages by a diabetes-induced long noncoding RNA. Diabetes 63 (2014), 4249–4261.
75. 75 Puthanveetil, P., et al. Long non-coding RNA MALAT1 regulates hyperglycaemia induced inflammatory process in the endothelial cells. J. Cell. Mol. Med. 19 (2015), 1418–1425.
76. 76 Deiuliis, J.A., MicroRNAs as regulators of metabolic disease: Pathophysiologic significance and emerging role as biomarkers and therapeutics. Int. J. Obes. 40 (2016), 88–101.
77. 77 Shakespear, M.R., et al. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol. 32 (2011), 335–343.
78. 78 Archin, N.M., et al. Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature 487 (2012), 482–485.
79. 79 Wang, G., et al. HDAC inhibition prevents white matter injury by modulating microglia/macrophage polarization through the GSK3β/PTEN/Akt axis. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), 2853–2858.
80. 80 Lewis, E.C., et al. The oral histone deacetylase inhibitor ITF2357 reduces cytokines and protects islet β cells in vivo and in vitro. Mol. Med. 17 (2011), 369–377.
81. + T-cells and monocytes and is superior to valproic acid for latent HIV-1 expression in vitro. JAIDS 54 (2010), 1–9.
82. 82 Kruidenier, L., et al. A selective jumonji H3K27 demethylase inhibitor modulates the proinflammatory macrophage response. Nature 488 (2012), 404–408.
83. 83 Choi, J-H., et al. Trichostatin A exacerbates atherosclerosis in low density lipoprotein receptor-deficient mice. Arterioscler. Throm. Vasc. Biol. 25 (2005), 2404–2409.
84. 84 Roger, T., et al. Histone deacetylase inhibitors impair innate immune responses to Toll-like receptor agonists and to infection. Blood 117 (2011), 1205–1217.
85. 85 Falkenberg, K.J., et al. Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nat. Rev. Drug Discov. 13 (2014), 673–691.
86. 86 Needham, L.A., et al. Drug targeting to monocytes and macrophages using esterase-sensitive chemical motifs. J. Pharmacol. Exp. Ther. 339 (2011), 132–142.
87. 87 Janssen, H.L.A., et al. Treatment of HCV infection by targeting microRNA. N. Engl. J. Med. 368 (2013), 1685–1694.
88. 88 Kota, J., et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137 (2009), 1005–1017.
89. 89 Luck, M.E., et al. Prospects for therapeutic targeting of microRNAs in human immunological diseases. J. Immunol. 194 (2015), 5047–5052.
90. 90 Ebert, M.S., et al. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 4 (2007), 721–726.
91. 91 Momen-Heravi, F., et al. Exosome-mediated delivery of functionally active miRNA-155 inhibitor to macrophages. Nanomedicine 10 (2014), 1517–1527.
92. 92 Newton, R., et al. Immunometabolism of regulatory T cells. Nat. Immunol. 17 (2016), 618–625.
93. 93 Lesourd, B.M., et al. Immune responses during recovery from protein-energy malnutrition. Clin. Nutr. 16:Suppl. 1 (1997), 37–46.