Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Inflammopharmacology
Published in: Inflammopharmacology 2/2020

01-04-2020 | Insulins | Review

The inflammatory effect of epigenetic factors and modifications in type 2 diabetes

Authors: Mohamad Akbari, Vahideh Hassan-Zadeh

Published in: Inflammopharmacology | Issue 2/2020

Login to get access

Abstract

Inflammation has a central role in the etiology of type 2 diabetes (T2D) and its complications. Both genetic and epigenetic factors have been implicated in the development of T2D-associated inflammation. Epigenetic mechanisms regulate the function of several components of the immune system. Diabetic conditions trigger aberrant epigenetic alterations that contribute to the progression of insulin resistance and β-cell dysfunction by induction of inflammatory responses. Thus, targeting epigenetic factors and modifications, as one of the underlying causes of inflammation, could lead to the development of novel immune-based strategies for the treatment of T2D. The aim of this review is to provide an overview of the epigenetic mechanisms involved in the propagation and perpetuation of chronic inflammation in T2D. We also discuss the possible anti-inflammatory approaches that target epigenetic factors for the treatment of T2D.
Appendix
Available only for authorised users
Literature
Akbari M, Hassan-Zadeh V (2018) Hyperglycemia affects the expression of inflammatory genes in peripheral blood mononuclear cells of patients with type 2 diabetes. Immunol Invest 47:654–665PubMed
Arab Sadeghabadi Z, Nourbakhsh M, Pasalar P, Emamgholipour S, Golestani A, Larijani B, Razzaghy-Azar M (2018) Reduced gene expression of sirtuins and active AMPK levels in children and adolescents with obesity and insulin resistance. Obes Res Clin Pract 12:167–173PubMed
Babu M, Devi TD, Mäkinen P, Kaikkonen M, Lesch HP, Junttila S, Laiho A, Ghimire B, Gyenesei A, Ylä-Herttuala S (2015) Differential promoter methylation of macrophage genes is associated with impaired vascular growth in ischemic muscles of hyperlipidemic and type 2 diabetic micenovelty and significance: genome-wide promoter methylation study. Circ Res 117:289–299PubMed
Bae EJ (2017) Sirtuin 6, a possible therapeutic target for type 2 diabetes. Arch Pharm Res 40:1380–1389PubMed
Balasubramanyam K, Varier RA, Altaf M, Swaminathan V, Siddappa NB, Ranga U, Kundu TK (2004) Curcumin, a novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. J Biol Chem 279:51163–51171PubMed
Balasubramanyam M, Aravind S, Gokulakrishnan K, Prabu P, Sathishkumar C, Ranjani H, Mohan V (2011) Impaired miR-146a expression links subclinical inflammation and insulin resistance in Type 2 diabetes. Mol Cell Biochem 351:197–205PubMed
Batista PJ, Chang HY (2013) Long noncoding RNAs: cellular address codes in development and disease. Cell 152:1298–1307PubMedPubMedCentral
Biswas S, Thomas AA, Chen S, Aref-Eshghi E, Feng B, Gonder J, Sadikovic B, Chakrabarti S (2018) MALAT1: an epigenetic regulator of inflammation in diabetic retinopathy. Sci Rep 8:6526PubMedPubMedCentral
Boldin MP, Taganov KD, Rao DS, Yang L, Zhao JL, Kalwani M, Garcia-Flores Y, Luong M, Devrekanli A, Xu J, Sun G, Tay J, Linsley PS, Baltimore D (2011) miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J Exp Med 208:1189–1201PubMedPubMedCentral
Bowers EM, Yan G, Mukherjee C, Orry A, Wang L, Holbert MA, Crump NT, Hazzalin CA, Liszczak G, Yuan H, Larocca C, Saldanha SA, Abagyan R, Sun Y, Meyers DJ, Marmorstein R, Mahadevan LC, Alani RM, Cole PA (2010) Virtual ligand screening of the p300/CBP histone acetyltransferase: identification of a selective small molecule inhibitor. Chem Biol 17:471–482PubMedPubMedCentral
Brasacchio D, Okabe J, Tikellis C, Balcerczyk A, George P, Baker EK, Calkin AC, Brownlee M, Cooper ME, El-Osta A (2009) Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail. Diabetes 58:1229–1236PubMedPubMedCentral
Buerki C, Rothgiesser KM, Valovka T, Owen HR, Rehrauer H, Fey M, Lane WS, Hottiger MO (2008) Functional relevance of novel p300-mediated lysine 314 and 315 acetylation of RelA/p65. Nucleic Acids Res 36:1665–1680PubMedPubMedCentral
Calao M, Burny A, Quivy V, Dekoninck A, Van Lint C (2008) A pervasive role of histone acetyltransferases and deacetylases in an NF-kappaB-signaling code. Trends Biochem Sci 33:339–349PubMed
Cao F, Zwinderman MRH, Dekker FJ (2018) The process and strategy for developing selective histone deacetylase 3 inhibitors. Molecules 23:551PubMedCentral
Chen L, Fischle W, Verdin E, Greene WC (2001) Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293:1653–1657
Chen LF, Mu Y, Greene WC (2002) Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J 21:6539–6548PubMedPubMedCentral
Chen X, Barozzi I, Termanini A, Prosperini E, Recchiuti A, Dalli J, Mietton F, Matteoli G, Hiebert S, Natoli G (2012) Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. Proc Natl Acad Sci USA 109:E2865–E2874PubMedPubMedCentral
Chou DH-C, Holson EB, Wagner FF, Tang AJ, Maglathlin RL, Lewis TA, Schreiber SL, Wagner BK (2012) Inhibition of histone deacetylase 3 protects beta cells from cytokine-induced apoptosis. Chem Biol 19:669–673PubMedPubMedCentral
Crujeiras AB, Parra D, Goyenechea E, Martinez JA (2008) Sirtuin gene expression in human mononuclear cells is modulated by caloric restriction. Eur J Clin Investig 38:672–678
Dai H, Sinclair DA, Ellis JL, Steegborn C (2018) Sirtuin activators and inhibitors: promises, achievements, and challenges. Pharmacol Ther 188:140–154PubMedPubMedCentral
Dayeh T, Tuomi T, Almgren P, Perfilyev A, Jansson P-A, de Mello VD, Pihlajamäki J, Vaag A, Groop L, Nilsson E (2016) DNA methylation of loci within ABCG1 and PHOSPHO1 in blood DNA is associated with future type 2 diabetes risk. Epigenetics 11:482–488PubMedPubMedCentral
De Kreutzenberg SV, Ceolotto G, Papparella I, Bortoluzzi A, Semplicini A, Dalla Man C, Cobelli C, Fadini GP, Avogaro A (2010) Downregulation of the longevity-associated protein sirtuin 1 in insulin resistance and metabolic syndrome: potential biochemical mechanisms. Diabetes 59:1006–1015PubMedPubMedCentral
DeFronzo RA, Ferrannini E, Groop L, Henry RR, Herman WH, Holst JJ, Hu FB, Kahn CR, Raz I, Shulman GI (2015) Type 2 diabetes mellitus. Nat Rev Dis Primers 1:15019PubMed
Di Lorenzo A, Bedford MT (2011) Histone arginine methylation. FEBS Lett 585:2024–2031PubMed
Dinarello CA, Donath MY, Mandrup-Poulsen T (2010) Role of IL-1β in type 2 diabetes. Curr Opin Endocrinol Diabetes Obes 17:314–321PubMed
Dirice E, Ng RWS, Martinez R, Hu J, Wagner FF, Holson EB, Wagner BK, Kulkarni RN (2017) Isoform-selective inhibitor of histone deacetylase 3 (HDAC3) limits pancreatic islet infiltration and protects female nonobese diabetic mice from diabetes. J Biol Chem 292:17598–17608PubMedPubMedCentral
Donath MY (2014) Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat Rev Drug Discov 13:465–476PubMed
Donath MY, Shoelson SE (2011) Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11:98–107PubMed
Ea CK, Baltimore D (2009) Regulation of NF-kappaB activity through lysine monomethylation of p65. Proc Natl Acad Sci USA 106:18972–18977PubMedPubMedCentral
Ehses JA, Ellingsgaard H, Böni-Schnetzler M, Donath MY (2009) Pancreatic islet inflammation in type 2 diabetes: from α and β cell compensation to dysfunction. Arch Physiol Biochem 115:240–247PubMed
El-Osta A, Brasacchio D, Yao D, Pocai A, Jones PL, Roeder RG, Cooper ME, Brownlee M (2008) Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 205:2409–2417PubMedPubMedCentral
Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N (2014) Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract 105:141–150PubMed
Esteller M (2007) Epigenetic gene silencing in cancer: the DNA hypermethylome. Hum Mol Genet 16:R50–R59PubMed
Fang F, Li G, Jing M, Xu L, Li Z, Li M, Yang C, Liu Y, Qian G, Hu X, Li G, Xie Y, Feng C, Li X, Pan J, Li Y, Feng X, Li Y (2019) C646 modulates inflammatory response and antibacterial activity of macrophage. Int Immunopharmacol 74:105736PubMed
Ghosh S, Banerjee S, Sil PC (2015) The beneficial role of curcumin on inflammation, diabetes and neurodegenerative disease: a recent update. Food Chem Toxicol 83:111–124PubMed
Gillespie J, Savic S, Wong C, Hempshall A, Inman M, Emery P, Grigg R, McDermott MF (2012) Histone deacetylases are dysregulated in rheumatoid arthritis and a novel histone deacetylase 3-selective inhibitor reduces interleukin-6 production by peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Rheum 64:418–422PubMed
Goldfine AB, Shoelson SE (2017) Therapeutic approaches targeting inflammation for diabetes and associated cardiovascular risk. J Clin Invest 127:83–93PubMedPubMedCentral
Gonzales AM, Orlando RA (2008) Curcumin and resveratrol inhibit nuclear factor-kappaB-mediated cytokine expression in adipocytes. Nutr Metab (Lond) 5:17
Greer EL, Shi Y (2012) Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 13:343–357PubMedPubMedCentral
Gu ML, Wang YM, Zhou XX, Yao HP, Zheng S, Xiang Z, Ji F (2016) An inhibitor of the acetyltransferases CBP/p300 exerts antineoplastic effects on gastrointestinal stromal tumor cells. Oncol Rep 36:2763–2770PubMed
Gupta SC, Tyagi AK, Deshmukh-Taskar P, Hinojosa M, Prasad S, Aggarwal BB (2014) Downregulation of tumor necrosis factor and other proinflammatory biomarkers by polyphenols. Arch Biochem Biophys 559:91–99PubMed
Guzik TJ, Cosentino F (2018) Epigenetics and immunometabolism in diabetes and aging. Antioxid Redox Signal 29:257–274PubMedPubMedCentral
Hassan FU, Rehman MS, Khan MS, Ali MA, Javed A, Nawaz A, Yang C (2019) Curcumin as an alternative epigenetic modulator: mechanism of action and potential effects. Front Genet 10:514PubMedPubMedCentral
Hausenblas HA, Schoulda JA, Smoliga JM (2015) Resveratrol treatment as an adjunct to pharmacological management in type 2 diabetes mellitus—systematic review and meta-analysis. Mol Nutr Food Res 59:147–159PubMed
Huang B, Yang XD, Zhou MM, Ozato K, Chen LF (2009) Brd4 coactivates transcriptional activation of NF-kappaB via specific binding to acetylated RelA. Mol Cell Biol 29:1375–1387PubMed
Huang B, Yang XD, Lamb A, Chen LF (2010) Posttranslational modifications of NF-kappaB: another layer of regulation for NF-kappaB signaling pathway. Cell Signal 22:1282–1290PubMedPubMedCentral
Hui X, Zhang M, Gu P, Li K, Gao Y, Wu D, Wang Y, Xu A (2017) Adipocyte SIRT1 controls systemic insulin sensitivity by modulating macrophages in adipose tissue. EMBO Rep 18:645–657PubMedPubMedCentral
Iachettini S, Trisciuoglio D, Rotili D, Lucidi A, Salvati E, Zizza P, Di Leo L, Del Bufalo D, Ciriolo MR, Leonetti C, Steegborn C, Mai A, Rizzo A, Biroccio A (2018) Pharmacological activation of SIRT6 triggers lethal autophagy in human cancer cells. Cell Death Dis 9:996PubMedPubMedCentral
Inagaki Y, Shiraki K, Sugimoto K, Yada T, Tameda M, Ogura S, Yamamoto N, Takei Y, Ito M (2016) Epigenetic regulation of proliferation and invasion in hepatocellular carcinoma cells by CBP/p300 histone acetyltransferase activity. Int J Oncol 48:533–540PubMed
Jain SK, Rains J, Croad J, Larson B, Jones K (2009) Curcumin supplementation lowers TNF-alpha, IL-6, IL-8, and MCP-1 secretion in high glucose-treated cultured monocytes and blood levels of TNF-alpha, IL-6, MCP-1, glucose, and glycosylated hemoglobin in diabetic rats. Antioxid Redox Signal 11:241–249PubMedPubMedCentral
Kaikkonen MU, Lam MT, Glass CK (2011) Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc Res 90:430–440PubMedPubMedCentral
Kawahara TL, Michishita E, Adler AS, Damian M, Berber E, Lin M, McCord RA, Ongaigui KC, Boxer LD, Chang HY, Chua KF (2009) SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB- dependent gene expression and organismal life span. Cell 136:62–74PubMedPubMedCentral
Kiernan R, Bres V, Ng RW, Coudart MP, El Messaoudi S, Sardet C, Jin DY, Emiliani S, Benkirane M (2003) Post-activation turn-off of NF-kappa B-dependent transcription is regulated by acetylation of p65. J Biol Chem 278:2758–2766PubMed
Kim HJ, Kim SH, Yun J-M (2012) Fisetin inhibits hyperglycemia-induced proinflammatory cytokine production by epigenetic mechanisms. Evid Based Complement Alternat Med 2012:639469PubMedPubMedCentral
Kitada M, Ogura Y, Monno I, Koya D (2019) Sirtuins and type 2 diabetes: role in inflammation, oxidative stress, and mitochondrial function. Front Endocrinol (Lausanne) 10:187
Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705PubMed
Kuang J, Zhang Y, Liu Q, Shen J, Pu S, Cheng S, Chen L, Li H, Wu T, Li R, Li Y, Zou M, Zhang Z, Jiang W, Xu G, Qu A, Xie W, He J (2017) Fat-specific SIRT6 ablation sensitizes mice to high-fat diet-induced obesity and insulin resistance by inhibiting lipolysis. Diabetes 66:1159–1171PubMed
Lappas M (2012) Anti-inflammatory properties of sirtuin 6 in human umbilical vein endothelial cells. Med Inflamm 2012:597514
Lasko LM, Jakob CG, Edalji RP, Qiu W, Montgomery D, Digiammarino EL, Hansen TM, Risi RM, Frey R, Manaves V, Shaw B, Algire M, Hessler P, Lam LT, Uziel T, Faivre E, Ferguson D, Buchanan FG, Martin RL, Torrent M, Chiang GG, Karukurichi K, Langston JW, Weinert BT, Choudhary C, de Vries P, Van Drie JH, McElligott D, Kesicki E, Marmorstein R, Sun C, Cole PA, Rosenberg SH, Michaelides MR, Lai A, Bromberg KD (2017) Discovery of a selective catalytic p300/CBP inhibitor that targets lineage-specific tumours. Nature 550:128–132PubMedPubMedCentral
Lee JH, Song MY, Song EK, Kim EK, Moon WS, Han MK, Park JW, Kwon KB, Park BH (2009) Overexpression of SIRT1 protects pancreatic beta-cells against cytokine toxicity by suppressing the nuclear factor-kappaB signaling pathway. Diabetes 58:344–351PubMedPubMedCentral
Lee Y, Ka SO, Cha HN, Chae YN, Kim MK, Park SY, Bae EJ, Park BH (2017) Myeloid Sirtuin 6 deficiency causes insulin resistance in high-fat diet-fed mice by eliciting macrophage polarization toward an M1 phenotype. Diabetes 66:2659–2668PubMed
Leibowitz G, Ktorza A, Cerasi E (2014) The role of txnip in the pathophysiology of diabetes and its vascular complications: a concise review. Medicographia 36:391–397
Leus NG, van der Wouden PE, van den Bosch T, Hooghiemstra WTR, Ourailidou ME, Kistemaker LE, Bischoff R, Gosens R, Haisma HJ, Dekker FJ (2016a) HDAC 3-selective inhibitor RGFP966 demonstrates anti-inflammatory properties in RAW 264.7 macrophages and mouse precision-cut lung slices by attenuating NF-κB p65 transcriptional activity. Biochem Pharmacol 108:58–74PubMedPubMedCentral
Leus NG, Zwinderman MR, Dekker FJ (2016b) Histone deacetylase 3 (HDAC 3) as emerging drug target in NF-κB-mediated inflammation. Curr Opin Chem Biol 33:160–168PubMedPubMedCentral
Li M-F, Zhang R, Li T-T, Chen M-Y, Li L-X, Lu J-X, Jia W-P (2016) High glucose increases the expression of inflammatory cytokine genes in macrophages through H3K9 methyltransferase mechanism. J Interferon Cytokine Res 36:48–61PubMed
Liang F, Kume S, Koya D (2009) SIRT1 and insulin resistance. Nat Rev Endocrinol 5:367–373PubMed
Ling C, Groop L (2009) Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 58:2718–2725PubMedPubMedCentral
Liu Z, Chen L, Deng X, Song H, Liao Y, Zeng T, Zheng J, Li H (2012) Methylation status of CpG sites in the MCP-1 promoter is correlated to serum MCP-1 in Type 2 diabetes. J Endocrinol Invest 35:585–589PubMed
Lo Sasso G, Menzies KJ, Mottis A, Piersigilli A, Perino A, Yamamoto H, Schoonjans K, Auwerx J (2014) SIRT2 deficiency modulates macrophage polarization and susceptibility to experimental colitis. PLoS One 9:e103573PubMedPubMedCentral
Lo W-S, Trievel RC, Rojas JR, Duggan L, Hsu J-Y, Allis CD, Marmorstein R, Berger SL (2000) Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol Cell 5:917–926PubMed
Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389:251–260PubMed
Lundh M, Christensen D, Nielsen MD, Richardson S, Dahllöf M, Skovgaard T, Berthelsen J, Dinarello C, Stevenazzi A, Mascagni P (2012) Histone deacetylases 1 and 3 but not 2 mediate cytokine-induced beta cell apoptosis in INS-1 cells and dispersed primary islets from rats and are differentially regulated in the islets of type 1 diabetic children. Diabetologia 55:2421–2431PubMed
Lundh M, Galbo T, Poulsen SS, Mandrup-Poulsen T (2015) Histone deacetylase 3 inhibition improves glycaemia and insulin secretion in obese diabetic rats. Diabetes Obes Metab 17:703–707PubMed
Mandrup-Poulsen T (2013) Type 2 diabetes mellitus: a metabolic autoinflammatory disease. Dermatol Clin 31:495–506PubMed
Manzo F, Tambaro FP, Mai A, Altucci L (2009) Histone acetyltransferase inhibitors and preclinical studies. Expert Opin Ther Pat 19:761–774PubMed
Margueron R, Trojer P, Reinberg D (2005) The key to development: interpreting the histone code? Curr Opin Genet Dev 15:163–176PubMed
Matsui M, Corey DR (2017) Non-coding RNAs as drug targets. Nat Rev Drug Discov 16:167–179PubMed
Mattick JS, Makunin IV (2006) Non-coding RNA. Hum Mol Genet 15:R17–R29PubMed
Meier BC, Wagner BK (2014) Inhibition of HDAC3 as a strategy for developing novel diabetes therapeutics. Epigenomics 6:209–214PubMed
Mendes KL, Lelis DF, Santos SHS (2017) Nuclear sirtuins and inflammatory signaling pathways. Cytokine Growth Factor Rev 38:98–105PubMed
Miao F, Gonzalo IG, Lanting L, Natarajan R (2004) In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions. J Biol Chem 279:18091–18097PubMed
Michishita E, McCord RA, Berber E, Kioi M, Padilla-Nash H, Damian M, Cheung P, Kusumoto R, Kawahara TL, Barrett JC, Chang HY, Bohr VA, Ried T, Gozani O, Chua KF (2008) SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452:492–496PubMedPubMedCentral
Miranda TB, Jones PA (2007) DNA methylation: the nuts and bolts of repression. J Cell Physiol 213:384–390PubMed
Mullican SE, Gaddis CA, Alenghat T, Nair MG, Giacomin PR, Everett LJ, Feng D, Steger DJ, Schug J, Artis D, Lazar MA (2011) Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev 25:2480–2488PubMedPubMedCentral
Naidoo V, Naidoo M, Ghai M (2018) Cell- and tissue-specific epigenetic changes associated with chronic inflammation in insulin resistance and type 2 diabetes mellitus. Scand J Immunol 88:e12723PubMed
Nicoglou A, Merlin F (2017) Epigenetics: a way to bridge the gap between biological fields. Stud Hist Philos Biol Biomed Sci 66:73–82PubMed
Nilsson E, Jansson PA, Perfilyev A, Volkov P, Pedersen M, Svensson MK, Poulsen P, Ribel-Madsen R, Pedersen NL, Almgren P (2014) Altered DNA methylation and differential expression of genes influencing metabolism and inflammation in adipose tissue from subjects with type 2 diabetes. Diabetes 63:2962–2976PubMed
Okabe J, Orlowski C, Balcerczyk A, Tikellis C, Thomas MC, Cooper ME, El-Osta A (2012) Distinguishing hyperglycemic changes by set7 in vascular endothelial cells. Circ Res 110:1067–1076PubMed
Pais TF, Szego EM, Marques O, Miller-Fleming L, Antas P, Guerreiro P, de Oliveira RM, Kasapoglu B, Outeiro TF (2013) The NAD-dependent deacetylase sirtuin 2 is a suppressor of microglial activation and brain inflammation. EMBO J 32:2603–2616PubMedPubMedCentral
Paneni F, Costantino S, Battista R, Castello L, Capretti G, Chiandotto S, Scavone G, Villano A, Pitocco D, Lanza G (2014) Adverse epigenetic signatures by histone methyltransferase set7 contribute to vascular dysfunction in patients with type 2 diabetes. Circ Cardiovasc Genet 8:150–158PubMed
Parikh H, Carlsson E, Chutkow WA, Johansson LE, Storgaard H, Poulsen P, Saxena R, Ladd C, Schulze PC, Mazzini MJ (2007) TXNIP regulates peripheral glucose metabolism in humans. PLoS Med 4:e158PubMedPubMedCentral
Pirola L, Balcerczyk A, Tothill RW, Haviv I, Kaspi A, Lunke S, Ziemann M, Karagiannis T, Tonna S, Kowalczyk A (2011) Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells. Genome Res 21:1601–1615PubMedPubMedCentral
Pivari F, Mingione A, Brasacchio C, Soldati L (2019) Curcumin and type 2 diabetes mellitus: prevention and treatment. Nutrients 11:1837PubMedCentral
Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136:629–641PubMed
Portela A, Esteller M (2010) Epigenetic modifications and human disease. Nat Biotechnol 28:1057–1068PubMed
Puthanveetil P, Chen S, Feng B, Gautam A, Chakrabarti S (2015) Long non-coding RNA MALAT1 regulates hyperglycaemia induced inflammatory process in the endothelial cells. J Cell Mol Med 19:1418–1425PubMedPubMedCentral
Raghuraman S, Donkin I, Versteyhe S, Barres R, Simar D (2016) The emerging role of epigenetics in inflammation and immunometabolism. Trends Endocrinol Metab 27:782–795PubMed
Reddy MA, Jin W, Villeneuve L, Wang M, Lanting L, Todorov I, Kato M, Natarajan R (2012) Proinflammatory role of microrna-200 in vascular smooth muscle cells from diabetic mice. Arterioscler Thromb Vasc Biol 32:721–729PubMedPubMedCentral
Reddy MA, Chen Z, Park JT, Wang M, Lanting L, Zhang Q, Bhatt K, Leung A, Wu X, Putta S (2014) Regulation of inflammatory phenotype in macrophages by a diabetes-induced long non-coding RNA. Diabetes 63:4249–4261PubMedPubMedCentral
Reddy MA, Das S, Zhuo C, Jin W, Wang M, Lanting L, Natarajan R (2016) Regulation of vascular smooth muscle cell dysfunction under diabetic conditions by miR-504. Arterioscler Thromb Vasc Biol 36:864–873PubMedPubMedCentral
Roshanzamir N, Hassan-Zadeh V (2019) Methylation of specific CpG sites in IL-1β and IL1R1 genes is affected by hyperglycaemia in type 2 diabetic patients. Immunol Invest 3:1–12
Rothgiesser KM, Erener S, Waibel S, Lüscher B, Hottiger MO (2010) SIRT2 regulates NF-kappaB dependent gene expression through deacetylation of p65 Lys310. J Cell Sci 123:4251–4258PubMed
Santer FR, Höschele PP, Oh SJ, Erb HH, Bouchal J, Cavarretta IT, Parson W, Meyers DJ, Cole PA, Culig Z (2011) Inhibition of the acetyltransferases p300 and CBP reveals a targetable function for p300 in the survival and invasion pathways of prostate cancer cell lines. Mol Cancer Ther 10:1644–1655PubMed
Sathishkumar C, Prabu P, Mohan V, Balasubramanyam M (2018) Linking a role of lncRNAs (long non-coding RNAs) with insulin resistance, accelerated senescence, and inflammation in patients with type 2 diabetes. Hum Genom 12:41
Schug TT, Xu Q, Gao H, Peres-da-Silva A, Draper DW, Fessler MB, Purushotham A, Li X (2010) Myeloid deletion of SIRT1 induces inflammatory signaling in response to environmental stress. Mol Cell Biol 30:4712–4721PubMedPubMedCentral
Sheedy FJ, Palsson-McDermott E, Hennessy EJ, Martin C, O’Leary JJ, Ruan Q, Johnson DS, Chen Y, O’Neill LA (2010) Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol 11:141–147PubMed
Singh AK, Bishayee A, Pandey AK (2018) Targeting histone deacetylases with natural and synthetic agents: an emerging anticancer strategy. Nutrients 10:731PubMedCentral
Smith KM et al (2012) miR-29ab1 deficiency identifies a negative feedback loop controlling Th1 bias that is dysregulated in multiple sclerosis. J Immunol 189:1567–1576PubMed
Sterner DE, Berger SL (2000) Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev 64:435–459PubMedPubMedCentral
Suraweera A, O’Byrne KJ, Richard DJ (2018) Combination therapy with histone deacetylase inhibitors (HDACi) for the treatment of cancer: achieving the full therapeutic potential of HDACi. Front Oncol 8:92PubMedPubMedCentral
Szabo M, Mate B, Csep K, Benedek T (2018) Epigenetic modifications linked to T2D, the heritability gap, and potential therapeutic targets. Biochem Genet 56:553–574PubMed
Taganov KD, Boldin MP, Chang KJ, Baltimore D (2006) NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 103:12481–12486PubMedPubMedCentral
Tahrani AA, Barnett AH, Bailey CJ (2016) Pharmacology and therapeutic implications of current drugs for type 2 diabetes mellitus. Nat Rev Endocrinol 12:566–592PubMed
Takeda-Watanabe A, Kitada M, Kanasaki K, Koya D (2012) SIRT1 inactivation induces inflammation through the dysregulation of autophagy in human THP-1 cells. Biochem Biophys Res Commun 427:191–196PubMed
Timmers S, Konings E, Bilet L, Houtkooper RH, van de Weijer T, Goossens GH, Hoeks J, van der Krieken S, Ryu D, Kersten S (2011) Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab 14:612–622PubMed
van den Bosch T, Boichenko A, Leus NGJ, Ourailidou ME, Wapenaar H, Rotili D, Mai A, Imhof A, Bischoff R, Haisma HJ, Dekker FJ (2016) The histone acetyltransferase p300 inhibitor C646 reduces pro-inflammatory gene expression and inhibits histone deacetylases. Biochem Pharmacol 102:130–140PubMed
Villeneuve LM, Reddy MA, Lanting LL, Wang M, Meng L, Natarajan R (2008) Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci USA 105:9047–9052PubMedPubMedCentral
Villeneuve LM, Kato M, Reddy MA, Wang M, Lanting L, Natarajan R (2010) Enhanced levels of microRNA-125b in vascular smooth muscle cells of diabetic db/db mice lead to increased inflammatory gene expression by targeting the histone methyltransferase Suv39h1. Diabetes 59:2904–2915PubMedPubMedCentral
Wagner FF, Lundh M, Kaya T, McCarren P, Zhang YL, Chattopadhyay S, Gale JP, Galbo T, Fisher SL, Meier BC, Vetere A, Richardson S, Morgan NG, Christensen DP, Gilbert TJ, Hooker JM, Leroy M, Walpita D, Mandrup-Poulsen T, Wagner BK, Holson EB (2016) An isochemogenic set of inhibitors to define the therapeutic potential of histone deacetylases in β-Cell protection. ACS Chem Biol 11:363–374PubMed
Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y (2004) Role of histone H2A ubiquitination in Polycomb silencing. Nature 431:873–878PubMed
Wang R, He Y, Robinson V, Yang Z, Hessler P, Lasko LM, Lu X, Bhathena A, Lai A, Uziel T, Lam LT (2018) Targeting lineage-specific MITF pathway in human melanoma cell lines by A-485, the selective small-molecule inhibitor of p300/CBP. Mol Cancer Ther 17:2543–2550PubMed
Xiao C, Wang RH, Lahusen TJ, Park O, Bertola A, Maruyama T, Reynolds D, Chen Q, Xu X, Young HA, Chen WJ, Gao B, Deng CX (2012) Progression of chronic liver inflammation and fibrosis driven by activation of c-JUN signaling in SIRT6 mutant mice. J Biol Chem 287:41903–41913PubMedPubMedCentral
Xu Z, Tong Q, Zhang Z, Wang S, Zheng Y, Liu Q, Qian LB, Chen SY, Sun J, Cai L (2017) Inhibition of HDAC3 prevents diabetic cardiomyopathy in OVE26 mice via epigenetic regulation of DUSP5-ERK1/2 pathway. Clin Sci (Lond) 131:1841–1857
Yan G, Eller MS, Elm C, Larocca CA, Ryu B, Panova IP, Dancy BM, Bowers EM, Meyers D, Lareau L, Cole PA, Taverna SD, Alani RM (2013) Selective inhibition of p300 HAT blocks cell cycle progression, induces cellular senescence, and inhibits the DNA damage response in melanoma cells. J Invest Dermatol 133:2444–2452PubMedPubMedCentral
Yang XD, Huang B, Li M, Lamb A, Kelleher NL, Chen LF (2009) Negative regulation of NF-kappaB action by Set9-mediated lysine methylation of the RelA subunit. EMBO J 28:1055–1066PubMedPubMedCentral
Ye EA, Liu L, Jiang Y, Jan J, Gaddipati S, Suvas S, Steinle JJ (2016) miR-15a/16 reduces retinal leukostasis through decreased proinflammatory signaling. J Neuroinflamm 13:305
Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW (2004) Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 23:2369–2380PubMedPubMedCentral
Yoshizaki T, Milne JC, Imamura T, Schenk S, Sonoda N, Babendure JL, Lu J-C, Smith JJ, Jirousek MR, Olefsky JM (2009) SIRT1 exerts anti-inflammatory effects and improves insulin sensitivity in adipocytes. Mol Cell Biol 29:1363–1374PubMed
Yoshizaki T, Schenk S, Imamura T, Babendure JL, Sonoda N, Bae EJ, Oh DY, Lu M, Milne JC, Westphal C (2010) SIRT1 inhibits inflammatory pathways in macrophages and modulates insulin sensitivity. Am J Physiol Endocrinol Metab 298:E419–E428PubMed
Yu X-Y, Geng Y-J, Liang J-L, Zhang S, Lei H-P, Zhong S-L, Lin Q-X, Shan Z-X, Lin S-G, Li Y (2012) High levels of glucose induce “metabolic memory” in cardiomyocyte via epigenetic histone H3 lysine 9 methylation. Mol Biol Rep 39:8891–8898PubMed
Yun J-M, Jialal I, Devaraj S (2011) Epigenetic regulation of high glucose-induced proinflammatory cytokine production in monocytes by curcumin. J Nutr Biochem 22:450–458PubMed
Zampetaki A et al (2010) Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res 107:810–817PubMed
Zhang R, Chen HZ, Liu JJ, Jia YY, Zhang ZQ, Yang RF, Zhang Y, Xu J, Wei YS, Liu DP, Liang CC (2010) SIRT1 suppresses activator protein-1 transcriptional activity and cyclooxygenase-2 expression in macrophages. J Biol Chem 285:7097–7110PubMed
Zhang H, Liu J, Qu D, Wang L, Luo J-Y, Lau CW, Liu P, Gao Z, Tipoe GL, Lee HK (2016) Inhibition of miR-200c restores endothelial function in diabetic mice through suppression of COX-2. Diabetes 65:1196–1207PubMed
Zhang J, Xu Z, Gu J, Jiang S, Liu Q, Zheng Y, Freedman JH, Sun J, Cai L (2018) HDAC3 inhibition in diabetic mice may activate Nrf2 preventing diabetes-induced liver damage and FGF21 synthesis and secretion leading to aortic protection. Am J Physiol Endocrinol Metab 315:E150–E162PubMed
Zhang L, Chen Y, Jiang Q, Song W, Zhang L (2019) Therapeutic potential of selective histone deacetylase 3 inhibition. Eur J Med Chem 162:534–542PubMed
Zheng J, Cheng J, Zheng S, Feng Q, Xiao X (2018) Curcumin, a polyphenolic curcuminoid with its protective effects and molecular mechanisms in diabetes and diabetic cardiomyopathy. Front Pharmacol 9:472PubMedPubMedCentral
Zhong S, Goto H, Inagaki M, Dong Z (2003) Phosphorylation at serine 28 and acetylation at lysine 9 of histone H3 induced by trichostatin A. Oncogene 22:5291–5297PubMed
Zhou J, Rossi J (2017) Aptamers as targeted therapeutics: current potential and challenges. Nat Rev Drug Discov 16:181–202PubMed
Zhou S, Tang X, Chen HZ (2018) Sirtuins and insulin resistance. Front Endocrinol (Lausanne) 9:748
Zhu B, Zheng Y, Pham A-D, Mandal SS, Erdjument-Bromage H, Tempst P, Reinberg D (2005) Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol Cell 20:601–611PubMed
Zhu E, Wang X, Zheng B, Wang Q, Hao J, Chen S, Zhao Q, Zhao L, Wu Z, Yin Z (2014) miR-20b suppresses Th17 differentiation and the pathogenesis of experimental autoimmune encephalomyelitis by targeting RORgammat and STAT3. J Immunol 192:5599–5609PubMed
Zhu X, Wu C, Qiu S, Yuan X, Li L (2017) Effects of resveratrol on glucose control and insulin sensitivity in subjects with type 2 diabetes: systematic review and meta-analysis. Nutr Metab 14:60
Ziesché E, Kettner-Buhrow D, Weber A, Wittwer T, Jurida L, Soelch J, Müller H, Newel D, Kronich P, Schneider H, Dittrich-Breiholz O, Bhaskara S, Hiebert SW, Hottiger MO, Li H, Burstein E, Schmitz ML, Kracht M (2013) The coactivator role of histone deacetylase 3 in IL-1-signaling involves deacetylation of p65 NF-κB. Nucleic Acids Res 41:90–109PubMed
Metadata
Title
The inflammatory effect of epigenetic factors and modifications in type 2 diabetes
Authors
Mohamad Akbari
Vahideh Hassan-Zadeh
Publication date
01-04-2020
Publisher
Springer International Publishing
Published in
Inflammopharmacology / Issue 2/2020
Print ISSN: 0925-4692
Electronic ISSN: 1568-5608
DOI
https://doi.org/10.1007/s10787-019-00663-9

Other articles of this Issue 2/2020

Inflammopharmacology 2/2020 Go to the issue

Original Article

Anti-inflammatory activities of Waltheria indica extracts by modulating expression of IL-1B, TNF-α, TNFRII and NF-κB in human macrophages

Original Article

Microglial-induced apoptosis is potentially responsible for hyperalgesia variations during CFA-induced inflammation

Original Article

Analysis of lncRNA expression profiles by sequencing reveals that lnc-AL928768.3 and lnc-AC091493.1 are novel biomarkers for disease risk and activity of rheumatoid arthritis

Original Article

Deferoxamine regulates neuroinflammation and oxidative stress in rats with diabetes-induced cognitive dysfunction

Original Article

Chromium picolinate attenuates cognitive deficit in ICV-STZ rat paradigm of sporadic Alzheimer’s-like dementia via targeting neuroinflammatory and IRS-1/PI3K/AKT/GSK-3β pathway

Original Article

VPR-254: an inhibitor of ROR-gamma T with potential utility for the treatment of inflammatory bowel disease