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Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Review Article

Key Relevance of Epigenetic Programming of Adiponectin Gene in Pathogenesis of Metabolic Disorders

Author(s): Kaiser Un Nisa and Mohammad Irshad Reza*

Volume 20, Issue 4, 2020

Page: [506 - 517] Pages: 12

DOI: 10.2174/1871530319666190801142637

Price: $65

Abstract

Background & Objective: Significant health and social burdens have been created by the growth of metabolic disorders like type 2 diabetes mellitus (T2DM), atherosclerosis, and non-alcoholic steatohepatitis, worldwide. The number of the affected population is as yet rising, and it is assessed that until 2030, 4−5 million individuals will acquire diabetes. A blend of environmental, genetic, epigenetic, and other factors, such as diet, are accountable for the initiation and progression of metabolic disorders. Several researches have shown strong relevance of adiponectin gene and metabolic disorders. In this review, the potential influence of epigenetic mechanisms of adiponectin gene “ADIPOQ” on increasing the risk of developing metabolic disorders and their potential in treating this major disorder are discussed.

Results & Conclusion: Various studies have postulated that a series of factors such as maternal High fat diet (HFD), oxidative stress, pro-inflammatory mediators, sleep fragmentation throughout lifetime, from gestation to old age, could accumulate epigenetic marks, including histone remodeling, DNA methylation, and microRNAs (miRNAs) that, in turn, alter the expression of ADIPOQ gene and result in hypoadiponectinemia which precipitates insulin resistance (IR) that in turn might induce or accelerate the onset and development of metabolic disorder. A better understanding of global patterns of epigenetic modifications and further their alterations in metabolic disorders will bestow better treatment strategies design.

Keywords: Epigenetic modification, adiponectin, metabolic disorders, DNA methylation, histone modification, microRNA.

Graphical Abstract

[1]
Ahanchi, N.S.; Hadaegh, F.; Alipour, A.; Ghanbarian, A.; Azizi, F.; Khalili, D. Application of Latent Class Analysis to Identify Metabolic Syndrome Components Patterns in adults: Tehran Lipid and Glucose study. Sci. Rep., 2019, 9(1), 1572.
[http://dx.doi.org/10.1038/s41598-018-38095-0] [PMID: 30733469]
[2]
Hamed, A.E.; Elwan, N.; Naguib, M.; Elwakil, R.; Esmat, G.; El Kassas, M.; Abd-Elsalam, S.; Moussa, S. Diabetes association with liver diseases: An overview for clinicians. Endocr. Metab. Immune Disord. Drug Targets, 2019, 19(3), 274-280.
[http://dx.doi.org/10.2174/1871530318666181116111945] [PMID: 30444204]
[3]
Jang, J-Y.; Moon, S.; Cho, S.; Cho, K.H.; Oh, C-M. Visit-to-visit HbA1c and glucose variability and the risks of macrovascular and microvascular events in the general population. Sci. Rep., 2019, 9(1), 1374.
[http://dx.doi.org/10.1038/s41598-018-37834-7] [PMID: 30718626]
[4]
Kovacova, Z.; Tencerova, M.; Roussel, B.; Wedellova, Z.; Rossmeislova, L.; Langin, D.; Polak, J.; Stich, V. The impact of obesity on secretion of adiponectin multimeric isoforms differs in visceral and subcutaneous adipose tissue. Int. J. Obes., 2012, 36(10), 1360-1365.
[http://dx.doi.org/10.1038/ijo.2011.223] [PMID: 22143618]
[5]
Yuan, H-P.; Sun, L.; Li, X-H.; Che, F-G.; Zhu, X-Q.; Yang, F.; Han, J.; Jia, C-Y.; Yang, Z. Association of Adiponectin Polymorphism with Metabolic Syndrome Risk and Adiponectin Level with Stroke Risk: A Meta-Analysis. Sci. Rep., 2016, 6, 31945.
[http://dx.doi.org/10.1038/srep31945] [PMID: 27578536]
[6]
Thundyil, J.; Pavlovski, D.; Sobey, C.G.; Arumugam, T.V. Adiponectin receptor signalling in the brain. Br. J. Pharmacol., 2012, 165(2), 313-327.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01560.x] [PMID: 21718299]
[7]
Okada-Iwabu, M.; Iwabu, M.; Yamauchi, T.; Kadowaki, T. Structure and function analysis of adiponectin receptors toward development of novel antidiabetic agents promoting healthy longevity. Endocr. J., 2018, 65(10), 971-977.
[http://dx.doi.org/10.1507/endocrj.EJ18-0310] [PMID: 30282888]
[8]
Simmons, D. Epigenetic Influence and Disease. New Educator, 2008, 1, 6.
[9]
Portela, A.; Esteller, M. Epigenetic modifications and human disease. Nat. Biotechnol., 2010, 28(10), 1057-1068.
[http://dx.doi.org/10.1038/nbt.1685] [PMID: 20944598]
[10]
Barajas-Olmos, F.; Centeno-Cruz, F.; Zerrweck, C.; Imaz-Rosshandler, I.; Martínez-Hernández, A.; Cordova, E.J.; Rangel-Escareño, C.; Gálvez, F.; Castillo, A.; Maydón, H.; Campos, F.; Maldonado-Pintado, D.G.; Orozco, L. Altered DNA methylation in liver and adipose tissues derived from individuals with obesity and type 2 diabetes. BMC Med. Genet., 2018, 19(1), 28.
[http://dx.doi.org/10.1186/s12881-018-0542-8] [PMID: 29466957]
[11]
Greenhill, C. Epigenetics: Obesity-induced hypermethylation of adiponectin gene. Nat. Rev. Endocrinol., 2015, 11(9), 504-505.
[http://dx.doi.org/10.1038/nrendo.2015.116] [PMID: 26170023]
[12]
Koistinen, H.A.; Forsgren, M.; Wallberg-Henriksson, H.; Zierath, J.R. Insulin action on expression of novel adipose genes in healthy and type 2 diabetic subjects. Obes. Res., 2004, 12(1), 25-31.
[http://dx.doi.org/10.1038/oby.2004.5] [PMID: 14742839]
[13]
Fu, Y.; Luo, N.; Klein, R.L.; Garvey, W.T. Adiponectin promotes adipocyte differentiation, insulin sensitivity, and lipid accumulation. J. Lipid Res., 2005, 46(7), 1369-1379.
[http://dx.doi.org/10.1194/jlr.M400373-JLR200] [PMID: 15834118]
[14]
Achari, A.E.; Jain, S.K. Adiponectin, a Therapeutic target for obesity, diabetes, and endothelial dysfunction. Int. J. Mol. Sci., 2017, 18(6), 1321.
[http://dx.doi.org/10.3390/ijms18061321] [PMID: 28635626]
[15]
Goldstein, B.J.; Scalia, R.G.; Ma, X.L. Protective vascular and myocardial effects of adiponectin. Nat. Clin. Pract. Cardiovasc. Med., 2009, 6(1), 27-35.
[http://dx.doi.org/10.1038/ncpcardio1398] [PMID: 19029992]
[16]
Kadowaki, T.; Yamauchi, T.; Kubota, N.; Hara, K.; Ueki, K.; Tobe, K. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J. Clin. Invest., 2006, 116(7), 1784-1792.
[http://dx.doi.org/10.1172/JCI29126] [PMID: 16823476]
[17]
Erzin, G.; Topcuoglu, C.; Kotan, V.O.; Bayram, S.; Fountoulakis, K. Assessment of Irisin, Adiponectin and Leptin Levels in Patients with Schizophrenia. Endocr. Metab. Immune Disord. Drug Targets, 2018, 18, 163-169.
[http://dx.doi.org/10.2174/1871530318666171207142901]
[18]
Crimmins, N.A.; Martin, L.J. Polymorphisms in adiponectin receptor genes ADIPOR1 and ADIPOR2 and insulin resistance. Obes. Rev., 2007, 8(5), 419-423.
[http://dx.doi.org/10.1111/j.1467-789X.2007.00348.x] [PMID: 17716299]
[19]
Tanabe, H.; Fujii, Y.; Okada-Iwabu, M.; Iwabu, M.; Nakamura, Y.; Hosaka, T.; Motoyama, K.; Ikeda, M.; Wakiyama, M.; Terada, T.; Ohsawa, N.; Hato, M.; Ogasawara, S.; Hino, T.; Murata, T.; Iwata, S.; Hirata, K.; Kawano, Y.; Yamamoto, M.; Kimura-Someya, T.; Shirouzu, M.; Yamauchi, T.; Kadowaki, T.; Yokoyama, S. Crystal structures of the human adiponectin receptors. Nature, 2015, 520(7547), 312-316.
[http://dx.doi.org/10.1038/nature14301] [PMID: 25855295]
[20]
Parker-Duffen, J.L.; Nakamura, K.; Silver, M.; Zuriaga, M.A.; MacLauchlan, S.; Aprahamian, T.R.; Walsh, K. Divergent roles for adiponectin receptor 1 (AdipoR1) and AdipoR2 in mediating revascularization and metabolic dysfunction in vivo. J. Biol. Chem., 2014, 289(23), 16200-16213.
[http://dx.doi.org/10.1074/jbc.M114.548115] [PMID: 24742672]
[21]
Combs, T.P.; Marliss, E.B. Adiponectin signaling in the liver. Rev. Endocr. Metab. Disord., 2014, 15(2), 137-147.
[http://dx.doi.org/10.1007/s11154-013-9280-6] [PMID: 24297186]
[22]
Combs, T.P.; Pajvani, U.B.; Berg, A.H.; Lin, Y.; Jelicks, L.A.; Laplante, M.; Nawrocki, A.R.; Rajala, M.W.; Parlow, A.F.; Cheeseboro, L.; Ding, Y.Y.; Russell, R.G.; Lindemann, D.; Hartley, A.; Baker, G.R.; Obici, S.; Deshaies, Y.; Ludgate, M.; Rossetti, L.; Scherer, P.E. A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology, 2004, 145(1), 367-383.
[http://dx.doi.org/10.1210/en.2003-1068] [PMID: 14576179]
[23]
Lind, M.I.; Spagopoulou, F. Evolutionary consequences of epigenetic inheritance. Heredity, 2018, 121(3), 205-209.
[http://dx.doi.org/10.1038/s41437-018-0113-y] [PMID: 29976958]
[24]
Kubota, T.; Miyake, K.; Hirasawa, T. The Mechanisms of Epigenetic Modifications During DNA Replication. In: The Mechanisms of DNA Replication; IntechOpen, 2013.
[25]
Rönn, T.; Volkov, P.; Davegårdh, C.; Dayeh, T.; Hall, E.; Olsson, A.H.; Nilsson, E.; Tornberg, A.; Dekker Nitert, M.; Eriksson, K-F.; Jones, H.A.; Groop, L.; Ling, C. A six months exercise intervention influences the genome-wide DNA methylation pattern in human adipose tissue. PLoS Genet., 2013, 9(6) e1003572
[http://dx.doi.org/10.1371/journal.pgen.1003572] [PMID: 23825961]
[26]
Tzika, E.; Dreker, T.; Imhof, A. Epigenetics and Metabolism in Health and Disease. Front. Genet., 2018, 9, 361.
[http://dx.doi.org/10.3389/fgene.2018.00361] [PMID: 30279699]
[27]
Allis, C.D.; Jenuwein, T. The molecular hallmarks of epigenetic control. Nat. Rev. Genet., 2016, 17(8), 487-500.
[http://dx.doi.org/10.1038/nrg.2016.59] [PMID: 27346641]
[28]
Phillips, T. The role of methylation in gene expression. New Educator, 2008, 1, 116.
[29]
Barres, R.; Zierath, J.R. DNA methylation in metabolic disorders. Am. J. Clin. Nutr., 2011, 93(4), 897S-900.
[http://dx.doi.org/10.3945/ajcn.110.001933] [PMID: 21289222]
[30]
Ahmed, S.M.; Johar, D.; El-Badri*, M.M.; A., and N. Insights into the Role of DNA Methylation and Protein Misfolding in Diabetes Mellitus. Endocr. Metab. Immune Disord. Drug Targets, 2019, 19, 1-9.
[http://dx.doi.org/10.2174/1871530319666190305131813]
[31]
Moran-Salvador, E.; Mann, J. Epigenetics and Liver Fibrosis. Cell. Mol. Gastroenterol. Hepatol., 2017, 4(1), 125-134.
[http://dx.doi.org/10.1016/j.jcmgh.2017.04.007] [PMID: 28593184]
[32]
Wankhade, U.D.; Zhong, Y.; Kang, P.; Alfaro, M.; Chintapalli, S.V.; Thakali, K.M.; Shankar, K. Enhanced offspring predisposition to steatohepatitis with maternal high-fat diet is associated with epigenetic and microbiome alterations. PLoS One, 2017, 12(4) e0175675
[http://dx.doi.org/10.1371/journal.pone.0175675] [PMID: 28414763]
[33]
Wang, P.; Zhao, H.; Li, T.; Zhang, W.; Wu, K.; Li, M.; Bian, Y.; Liu, H.; Ning, Y.; Li, G.; Chen, Z.J. Hypomethylation of the LH/choriogonadotropin receptor promoter region is a potential mechanism underlying susceptibility to polycystic ovary syndrome. Endocrinology, 2014, 155(4), 1445-1452.
[http://dx.doi.org/10.1210/en.2013-1764] [PMID: 24527662]
[34]
Yu, Y-Y.; Sun, C-X.; Liu, Y-K.; Li, Y.; Wang, L.; Zhang, W. Promoter methylation of CYP19A1 gene in Chinese polycystic ovary syndrome patients. Gynecol. Obstet. Invest., 2013, 76(4), 209-213.
[http://dx.doi.org/10.1159/000355314] [PMID: 24157654]
[35]
Pan, J-X.; Tan, Y-J.; Wang, F-F.; Hou, N-N.; Xiang, Y-Q.; Zhang, J-Y.; Liu, Y.; Qu, F.; Meng, Q.; Xu, J.; Sheng, J.Z.; Huang, H.F. Aberrant expression and DNA methylation of lipid metabolism genes in PCOS: a new insight into its pathogenesis. Clin. Epigenetics, 2018, 10, 6.
[http://dx.doi.org/10.1186/s13148-018-0442-y] [PMID: 29344314]
[36]
Ott, R.; Stupin, J.H.; Melchior, K.; Schellong, K.; Ziska, T.; Dudenhausen, J.W.; Henrich, W.; Rancourt, R.C.; Plagemann, A. Alterations of adiponectin gene expression and DNA methylation in adipose tissues and blood cells are associated with gestational diabetes and neonatal outcome. Clin. Epigenetics, 2018, 10(1), 131.
[http://dx.doi.org/10.1186/s13148-018-0567-z] [PMID: 30355290]
[37]
Kim, A.Y.; Park, Y.J.; Pan, X.; Shin, K.C.; Kwak, S-H.; Bassas, A.F.; Sallam, R.M.; Park, K.S.; Alfadda, A.A.; Xu, A.; Kim, J.B. Obesity-induced DNA hypermethylation of the adiponectin gene mediates insulin resistance. Nat. Commun., 2015, 6, 7585.
[http://dx.doi.org/10.1038/ncomms8585] [PMID: 26139044]
[38]
Pham, T.X.; Lee, J-Y. Epigenetic Regulation of Adipokines. Int. J. Mol. Sci., 2017, 18(8), 1740.
[http://dx.doi.org/10.3390/ijms18081740] [PMID: 28796178]
[39]
Lu, Y.; Fan, C.; Liang, A.; Fan, X.; Wang, R.; Li, P.; Qi, K. Effects of SCFA on the DNA methylation pattern of adiponectin and resistin in high-fat-diet-induced obese male mice. Br. J. Nutr., 2018, 120(4), 385-392.
[http://dx.doi.org/10.1017/S0007114518001526] [PMID: 29925443]
[40]
Remely, M.; Ferk, F.; Sterneder, S.; Setayesh, T.; Kepcija, T.; Roth, S.; Noorizadeh, R.; Greunz, M.; Rebhan, I.; Wagner, K-H.; Knasmüller, S.; Haslberger, A. Vitamin E Modifies High-Fat Diet-Induced Increase of DNA Strand Breaks, and Changes in Expression and DNA Methylation of Dnmt1 and MLH1 in C57BL/6J Male Mice. Nutrients, 2017, 9(6), 607.
[http://dx.doi.org/10.3390/nu9060607] [PMID: 28613268]
[41]
Aslibekyan, S.; Do, A.N.; Xu, H.; Li, S.; Irvin, M.R.; Zhi, D.; Tiwari, H.K.; Absher, D.M.; Shuldiner, A.R.; Zhang, T.; Chen, W.; Tanner, K.; Hong, C.; Mitchell, B.D.; Berenson, G.; Arnett, D.K. CPT1A methylation is associated with plasma adiponectin. Nutr. Metab. Cardiovasc. Dis., 2017, 27(3), 225-233.
[http://dx.doi.org/10.1016/j.numecd.2016.11.004] [PMID: 28139377]
[42]
Davé, V.; Yousefi, P.; Huen, K.; Volberg, V.; Holland, N. Relationship between expression and methylation of obesity-related genes in children. Mutagenesis, 2015, 30(3), 411-420.
[http://dx.doi.org/10.1093/mutage/geu089] [PMID: 25589532]
[43]
Lehnen, H.; Zechner, U.; Haaf, T. Epigenetics of gestational diabetes mellitus and offspring health: the time for action is in early stages of life. Mol. Hum. Reprod., 2013, 19(7), 415-422.
[http://dx.doi.org/10.1093/molehr/gat020] [PMID: 23515667]
[44]
Bouchard, L.; Hivert, M-F.; Guay, S-P.; St-Pierre, J.; Perron, P.; Brisson, D. Placental adiponectin gene DNA methylation levels are associated with mothers’ blood glucose concentration. Diabetes, 2012, 61(5), 1272-1280.
[http://dx.doi.org/10.2337/db11-1160] [PMID: 22396200]
[45]
Khalyfa, A.; Mutskov, V.; Carreras, A.; Khalyfa, A.A.; Hakim, F.; Gozal, D. Sleep fragmentation during late gestation induces metabolic perturbations and epigenetic changes in adiponectin gene expression in male adult offspring mice. Diabetes, 2014, 63(10), 3230-3241.
[http://dx.doi.org/10.2337/db14-0202] [PMID: 24812424]
[46]
Nitert, M.D.; Dayeh, T.; Volkov, P.; Elgzyri, T.; Hall, E.; Nilsson, E.; Yang, B.T.; Lang, S.; Parikh, H.; Wessman, Y.; Weishaupt, H.; Attema, J.; Abels, M.; Wierup, N.; Almgren, P.; Jansson, P.A.; Rönn, T.; Hansson, O.; Eriksson, K.F.; Groop, L.; Ling, C. Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with type 2 diabetes. Diabetes, 2012, 61(12), 3322-3332.
[http://dx.doi.org/10.2337/db11-1653] [PMID: 23028138]
[47]
Grazioli, E.; Dimauro, I.; Mercatelli, N.; Wang, G.; Pitsiladis, Y.; Di Luigi, L.; Caporossi, D. Physical activity in the prevention of human diseases: role of epigenetic modifications. BMC Genomics, 2017, 18(Suppl. 8), 802.
[http://dx.doi.org/10.1186/s12864-017-4193-5] [PMID: 29143608]
[48]
Chrun, E.S.; Modolo, F.; Daniel, F.I. Histone modifications: A review about the presence of this epigenetic phenomenon in carcinogenesis. Pathol. Res. Pract., 2017, 213(11), 1329-1339.
[http://dx.doi.org/10.1016/j.prp.2017.06.013] [PMID: 28882400]
[49]
Peterson, C.L.; Laniel, M-A. Histones and histone modifications. Curr. Biol., 2004, 14(14), R546-R551.
[http://dx.doi.org/10.1016/j.cub.2004.07.007] [PMID: 15268870]
[50]
Rando, O.J.; Chang, H.Y. Genome-wide views of chromatin structure. Annu. Rev. Biochem., 2009, 78, 245-271.
[http://dx.doi.org/10.1146/annurev.biochem.78.071107.134639] [PMID: 19317649]
[51]
Tan, M.; Luo, H.; Lee, S.; Jin, F.; Yang, J.S.; Montellier, E.; Buchou, T.; Cheng, Z.; Rousseaux, S.; Rajagopal, N.; Lu, Z.; Ye, Z.; Zhu, Q.; Wysocka, J.; Ye, Y.; Khochbin, S.; Ren, B.; Zhao, Y. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell, 2011, 146(6), 1016-1028.
[http://dx.doi.org/10.1016/j.cell.2011.08.008] [PMID: 21925322]
[52]
Huertas, D.; Sendra, R.; Muñoz, P. Chromatin dynamics coupled to DNA repair. Epigenetics, 2009, 4(1), 31-42.
[http://dx.doi.org/10.4161/epi.4.1.7733] [PMID: 19218832]
[53]
Christensen, D.P.; Dahllöf, M.; Lundh, M.; Rasmussen, D.N.; Nielsen, M.D.; Billestrup, N.; Grunnet, L.G.; Mandrup-Poulsen, T. Histone deacetylase (HDAC) inhibition as a novel treatment for diabetes mellitus. Mol. Med., 2011, 17(5-6), 378-390.
[http://dx.doi.org/10.2119/molmed.2011.00021] [PMID: 21274504]
[54]
Gluckman, P.D.; Hanson, M.A.; Buklijas, T.; Low, F.M.; Beedle, A.S. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat. Rev. Endocrinol., 2009, 5(7), 401-408.
[http://dx.doi.org/10.1038/nrendo.2009.102] [PMID: 19488075]
[55]
Balcerczyk, A.; Chriett, S.; Pirola, L. Insulin Action, Insulin Resistance, and Their Link to Histone Acetylation.Handbook ofNutrition, Diet, and Epigenetics; Preedy, V.R; Patel, V.B., Ed.; Springer International Publishing, 2017, pp. 1-22.
[http://dx.doi.org/10.1007/978-3-319-31143-2_57-1]
[56]
Yoo, E.J.; Chung, J-J.; Choe, S.S.; Kim, K.H.; Kim, J.B. Down-regulation of histone deacetylases stimulates adipocyte differentiation. J. Biol. Chem., 2006, 281(10), 6608-6615.
[http://dx.doi.org/10.1074/jbc.M508982200] [PMID: 16407282]
[57]
Masuyama, H.; Mitsui, T.; Eguchi, T.; Tamada, S.; Hiramatsu, Y. The effects of paternal high-fat diet exposure on offspring metabolism with epigenetic changes in the mouse adiponectin and leptin gene promoters. Am. J. Physiol. Circ. Physiol, 2016, 311, 236-245.
[http://dx.doi.org/10.1152/ajpendo.00095.2016]
[58]
Sakurai, N.; Mochizuki, K.; Goda, T. Modifications of histone H3 at lysine 9 on the adiponectin gene in 3T3-L1 adipocytes. J. Nutr. Sci. Vitaminol. (Tokyo), 2009, 55(2), 131-138.
[http://dx.doi.org/10.3177/jnsv.55.131] [PMID: 19436139]
[59]
Musri, M.M.; Corominola, H.; Casamitjana, R.; Gomis, R.; Párrizas, M. Histone H3 lysine 4 dimethylation signals the transcriptional competence of the adiponectin promoter in preadipocytes. J. Biol. Chem., 2006, 281(25), 17180-17188.
[http://dx.doi.org/10.1074/jbc.M601295200] [PMID: 16613853]
[60]
Musri, M.M.; Carmona, M.C.; Hanzu, F.A.; Kaliman, P.; Gomis, R.; Párrizas, M. Histone demethylase LSD1 regulates adipogenesis. J. Biol. Chem., 2010, 285(39), 30034-30041.
[http://dx.doi.org/10.1074/jbc.M110.151209] [PMID: 20656681]
[61]
Reza, M.I.; Goel, D.; Rahman, Z.; Aamer, S. Microrna and Rna Binding Proteins: The Posttranscriptional Regulators of Foxo Expression. J. Crit. Rev, 2018, 5, 1.
[http://dx.doi.org/10.22159/jcr.2018v5i2.24774]
[62]
Lim, L.P.; Lau, N.C.; Garrett-Engele, P.; Grimson, A.; Schelter, J.M.; Castle, J.; Bartel, D.P.; Linsley, P.S.; Johnson, J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature, 2005, 433(7027), 769-773.
[http://dx.doi.org/10.1038/nature03315] [PMID: 15685193]
[63]
Sathyapalan, T.; David, R.; Gooderham, N.J.; Atkin, S.L. Increased expression of circulating miRNA-93 in women with polycystic ovary syndrome may represent a novel, non-invasive biomarker for diagnosis. Sci. Rep., 2015, 5, 16890.
[http://dx.doi.org/10.1038/srep16890] [PMID: 26582398]
[64]
Morales, S.; Monzo, M.; Navarro, A. Epigenetic regulation mechanisms of microRNA expression. Biomol. Concepts, 2017, 8(5-6), 203-212.
[http://dx.doi.org/10.1515/bmc-2017-0024] [PMID: 29161231]
[65]
Rottiers, V.; Näär, A.M. MicroRNAs in metabolism and metabolic disorders. Nat. Rev. Mol. Cell Biol., 2012, 13(4), 239-250.
[http://dx.doi.org/10.1038/nrm3313] [PMID: 22436747]
[66]
Vienberg, S.; Geiger, J.; Madsen, S.; Dalgaard, L.T. MicroRNAs in metabolism. Acta Physiol. (Oxf.), 2017, 219(2), 346-361.
[http://dx.doi.org/10.1111/apha.12681] [PMID: 27009502]
[67]
Alexander, R.; Lodish, H.; Sun, L. MicroRNAs in adipogenesis and as therapeutic targets for obesity. Expert Opin. Ther. Targets, 2011, 15(5), 623-636.
[http://dx.doi.org/10.1517/14728222.2011.561317] [PMID: 21355787]
[68]
Ge, Q.; Gérard, J.; Noël, L.; Scroyen, I.; Brichard, S.M. MicroRNAs regulated by adiponectin as novel targets for controlling adipose tissue inflammation. Endocrinology, 2012, 153(11), 5285-5296.
[http://dx.doi.org/10.1210/en.2012-1623] [PMID: 23015294]
[69]
Ishida, M.; Shimabukuro, M.; Yagi, S.; Nishimoto, S.; Kozuka, C.; Fukuda, D.; Soeki, T.; Masuzaki, H.; Tsutsui, M.; Sata, M. MicroRNA-378 regulates adiponectin expression in adipose tissue: a new plausible mechanism. PLoS One, 2014, 9(11) e111537
[http://dx.doi.org/10.1371/journal.pone.0111537] [PMID: 25379946]
[70]
Belarbi, Y.; Mejhert, N.; Lorente-Cebrián, S.; Dahlman, I.; Arner, P.; Rydén, M.; Kulyté, A. MicroRNA-193b Controls Adiponectin Production in Human White Adipose Tissue. J. Clin. Endocrinol. Metab., 2015, 100(8), E1084-E1088.
[http://dx.doi.org/10.1210/jc.2015-1530] [PMID: 26020766]
[71]
Kang, M.; Yan, L-M.; Zhang, W-Y.; Li, Y-M.; Tang, A-Z.; Ou, H-S. Role of microRNA-21 in regulating 3T3-L1 adipocyte differentiation and adiponectin expression. Mol. Biol. Rep., 2013, 40(8), 5027-5034.
[http://dx.doi.org/10.1007/s11033-013-2603-6] [PMID: 23793828]
[72]
Esteller, M. Epigenetics in evolution and disease. Lancet, 2008, 372, S90-S96.
[http://dx.doi.org/10.1016/S0140-6736(08)61887-5]
[73]
Bruce, K.D.; Cagampang, F.R. Epigenetic priming of the metabolic syndrome. Toxicol. Mech. Methods, 2011, 21(4), 353-361.
[http://dx.doi.org/10.3109/15376516.2011.559370] [PMID: 21495873]
[74]
Martin-Gronert, M.S.; Ozanne, S.E. Programming of appetite and type 2 diabetes. Early Hum. Dev., 2005, 81(12), 981-988.
[http://dx.doi.org/10.1016/j.earlhumdev.2005.10.006] [PMID: 16257499]
[75]
Wazen, R.M.; Kuroda, S.; Nishio, C.; Sellin, K.; Brunski, J.B. Developmental Exposure to Estradiol and Bisphenol A Increases Susceptibility to Prostate Carcinogenesis and Epigenetically Regulates Phosphodiesterase Type 4 Variant 4. Cancer Res., 2014, 8, 1385-1395.
[76]
Gouri, A.; Dekaken, A. Epigenetic pathways in type 2 diabetes and its complications. Ann. Clin. Lab. Res., 2013, 1, 1-5.
[77]
Kim, A.Y.; Park, Y.J.; Pan, X.; Shin, K.C.; Kwak, S-H.; Bassas, A.F.; Sallam, R.M.; Park, K.S.; Alfadda, A.A.; Xu, A.; Kim, J.B. Obesity-induced DNA hypermethylation of the adiponectin gene mediates insulin resistance. Nat. Commun., 2015, 6, 7585.
[http://dx.doi.org/10.1038/ncomms8585] [PMID: 26139044]
[78]
You, D.; Nilsson, E.; Tenen, D.E.; Lyubetskaya, A.; Lo, J.C.; Jiang, R.; Deng, J.; Dawes, B.A.; Vaag, A.; Ling, C.; Rosen, E.D.; Kang, S. Dnmt3a is an epigenetic mediator of adipose insulin resistance. eLife, 2017, 6, 1-20.
[http://dx.doi.org/10.7554/eLife.30766] [PMID: 29091029]
[79]
Sun, C.; Zhang, F.; Ge, X.; Yan, T.; Chen, X.; Shi, X.; Zhai, Q. SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B. Cell Metab., 2007, 6(4), 307-319.
[http://dx.doi.org/10.1016/j.cmet.2007.08.014] [PMID: 17908559]
[80]
Li, C.; Ebert, P.J.R.; Li, Q.J. T cell receptor (TCR) and transforming growth factor β (TGF-β) signaling converge on DNA (cytosine-5)-methyltransferase to control forkhead box protein 3 (foxp3) locus methylation and inducible regulatory T cell differentiation. J. Biol. Chem., 2013, 288(26), 19127-19139.
[http://dx.doi.org/10.1074/jbc.M113.453357] [PMID: 23687305]
[81]
Catalanotto, C.; Cogoni, C.; Zardo, G. MicroRNA in Control of Gene Expression: An Overview of Nuclear Functions. Int. J. Mol. Sci., 2016, 17(10), 1712.
[http://dx.doi.org/10.3390/ijms17101712] [PMID: 27754357]
[82]
Place, R.F.; Li, L.C.; Pookot, D.; Noonan, E.J.; Dahiya, R. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc. Natl. Acad. Sci. USA, 2008, 105(5), 1608-1613.
[http://dx.doi.org/10.1073/pnas.0707594105] [PMID: 18227514]
[83]
Wang, Z.; Hu, J.; Hamzah, S.S.; Ge, S.; Lin, Y.; Zheng, B.; Zeng, S.; Lin, S. n-Butanol Extract of Lotus Seeds Exerts Antiobesity Effects in 3T3-L1 Preadipocytes and High-Fat Diet-Fed Mice via Activating Adenosine Monophosphate-Activated Protein Kinase. J. Agric. Food Chem., 2019, 67(4), 1092-1103.
[http://dx.doi.org/10.1021/acs.jafc.8b05281] [PMID: 30621393]
[84]
Wang, Z.; Lam, K.L.; Hu, J.; Ge, S.; Zhou, A.; Zheng, B.; Zeng, S.; Lin, S. Chlorogenic acid alleviates obesity and modulates gut microbiota in high-fat-fed mice. Food Sci. Nutr., 2019, 7(2), 579-588.
[http://dx.doi.org/10.1002/fsn3.868] [PMID: 30847137]
[85]
Cheng, Z.; Zheng, L.; Almeida, F.A. Epigenetic reprogramming in metabolic disorders: nutritional factors and beyond. J. Nutr. Biochem., 2018, 54, 1-10.
[http://dx.doi.org/10.1016/j.jnutbio.2017.10.004] [PMID: 29154162]
[86]
Ranheim, T.; Haugen, F.; Staff, A.C.; Braekke, K.; Harsem, N.K.; Drevon, C.A. Adiponectin is reduced in gestational diabetes mellitus in normal weight women. Acta Obstet. Gynecol. Scand., 2004, 83(4), 341-347.
[http://dx.doi.org/10.1111/j.0001-6349.2004.00413.x] [PMID: 15005780]
[87]
Luo, Z.C.; Nuyt, A.M.; Delvin, E.; Fraser, W.D.; Julien, P.; Audibert, F.; Girard, I.; Shatenstein, B.; Deal, C.; Grenier, E.; Garofalo, C.; Levy, E. Maternal and fetal leptin, adiponectin levels and associations with fetal insulin sensitivity. Obesity (Silver Spring), 2013, 21(1), 210-216.
[http://dx.doi.org/10.1002/oby.20250] [PMID: 23505188]

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