Epigenetic flexibility in metabolic regulation: disease cause and prevention
Abstract
Metabolic diseases, including type 2 diabetes mellitus (T2DM), are increasing worldwide at an alarming rate. Epigenetic DNA modifications such as DNA methylation and histone modifications are thought to play an important role in the development of and predisposition to metabolic diseases. This review highlights the key functions of DNA methylation and histone modifications and elucidates the underlying mechanisms of in utero programming and epigenetic inheritance, which could account for the global increase in obesity and T2DM. The impact of exercise and nutrition on the tissue-specific epigenetic profile is discussed, because these lifestyle factors may modify epigenetic programming and predisposition to obesity and T2DM.
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Short-term, high-intensity exercise decreases muscle promoter methylation of genes involved in mitochondrial function such as PGC1α, TFAM, MEF2A, and PDK4, whereas in patients with T2DM these regions usually have higher methylation levels.
“Short-term, high-intensity exercise decreases muscle promoter methylation of genes involved in mitochondrial function such as PGC1α, TFAM, MEF2A, and PDK4, whereas in patients with T2DM, these regions usually have higher methylation levels (137).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [137]
Cites
The language of covalent histone modifications
Strahl, B. D., & Allis, C. D. (2000) · Nature · doi:10.1038/47412 · Cited by 8,679 · see citing works
Okano, M., Bell, D. W., Haber, D. A., & Li, E. (1999) · Cell · doi:10.1016/s0092-8674(00)81656-6 · Cited by 6,143 · see citing works
Human DNA methylomes at base resolution show widespread epigenomic differences
Lister, R., Pelizzola, M., Dowen, R. H., Hawkins, R. D., Hon, G., Tonti-Filippini, J., Nery, J. R., Lee, L., Ye, Z., Ngo, Q.-M., et al. (2009) · Nature · doi:10.1038/nature08514 · Cited by 4,673 · see citing works
Targeted mutation of the DNA methyltransferase gene results in embryonic lethality
Li, E., Bestor, T. H., & Jaenisch, R. (1992) · Cell · doi:10.1016/0092-8674(92)90611-f · Cited by 3,984 · see citing works
Epigenetic differences arise during the lifetime of monozygotic twins
Fraga, M. F., Ballestar, E., Paz, M. F., Ropero, S., Setien, F., Ballestar, M. L., Heine-Suñer, D., Cigudosa, J. C., Urioste, M., Benitez, J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500398102 · Cited by 3,602 · see citing works
The Role of Chromatin during Transcription
Li, B., Carey, M., & Workman, J. L. (2007) · Cell · doi:10.1016/j.cell.2007.01.015 · Cited by 3,503 · see citing works
Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine
Ito, S., Shen, L., Dai, Q., Wu, S. C., Collins, L. B., Swenberg, J. A., He, C., & Zhang, Y. (2011) · Science · doi:10.1126/science.1210597 · Cited by 3,451 · see citing works
DNA methylation landscapes: Provocative insights from epigenomics
Suzuki, M. M., & Bird, A. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2341 · Cited by 3,039 · see citing works
A decade of exploring the cancer epigenome—biological and translational implications
Baylin, S. B., & Jones, P. A. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3130 · Cited by 2,871 · see citing works
Tet-Mediated Formation of 5-Carboxylcytosine and Its Excision by TDG in Mammalian DNA
He, Y., Li, B.-Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L., et al. (2011) · Science · doi:10.1126/science.1210944 · Cited by 2,776 · see citing works
DNA Modification Mechanisms and Gene Activity During Development
Holliday, R., & Pugh, J. E. (1975) · Science · doi:10.1126/science.187.4173.226 · Cited by 1,973 · see citing works
Epigenetics and the environment: emerging patterns and implications
Feil, R., & Fraga, M. F. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3142 · Cited by 1,929 · see citing works
Obesity in Young Men after Famine Exposure in Utero and Early Infancy
Ravelli, G.-P., Stein, Z. A., & Susser, M. W. (1976) · New England Journal of Medicine · doi:10.1056/nejm197608122950701 · Cited by 1,647 · see citing works
Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes
Wang, Z., Zang, C., Cui, K., Schones, D. E., Barski, A., Peng, W., & Zhao, K. (2009) · Cell · doi:10.1016/j.cell.2009.06.049 · Cited by 1,344 · see citing works
X inactivation, differentiation, and DNA methylation
Riggs, A. D. (2008) · Cytogenetics and Cell Genetics · doi:10.1159/000130315 · Cited by 1,343 · see citing works
Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring
Ng, S.-F., Lin, R. C. Y., Laybutt, D. R., Barres, R., Owens, J. A., & Morris, M. J. (2010) · Nature · doi:10.1038/nature09491 · Cited by 1,327 · see citing works
Control of Pancreas and Liver Gene Expression by HNF Transcription Factors
Odom, D. T., Zizlsperger, N., Gordon, D. B., Bell, G. W., Rinaldi, N. J., Murray, H. L., Volkert, T. L., Schreiber, J., Rolfe, A., Gifford, D. K., et al. (2004) · Science · doi:10.1126/science.1089769 · Cited by 1,312 · see citing works
Bunz, U. H. F. (2005) · Science · doi:10.1126/science.1111098 · Cited by 1,252 · see citing works
Carone, B. R., Fauquier, L., Habib, N., Shea, J. M., Hart, C. E., Li, R., Bock, C., Li, C., Gu, H., Zamore, P. D., et al. (2010) · Cell · doi:10.1016/j.cell.2010.12.008 · Cited by 1,157 · see citing works
Epigenetic mechanisms of gene regulation
Russo, V. E. A., Martienssen, R. A., & Riggs, A. D. (1996) · Medical Entomology and Zoology · Cited by 1,088 · see citing works
Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer
Suzuki, H., Watkins, D. N., Jair, K.-W., Schuebel, K. E., Markowitz, S. D., Chen, W. D., Pretlow, T. P., Yang, B., Akiyama, Y., van Engeland, M., et al. (2004) · Nature Genetics · doi:10.1038/ng1330 · Cited by 1,070 · see citing works
Acute Exercise Remodels Promoter Methylation in Human Skeletal Muscle
Barrès, R., Yan, J., Egan, B., Treebak, J. T., Rasmussen, M., Fritz, T., Caidahl, K., Krook, A., O'Gorman, D. J., & Zierath, J. R. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.001 · Cited by 965 · see citing works
Self-citationKaati, G., Bygren, L., & Edvinsson, S. (2002) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5200859 · Cited by 896 · see citing works
Epigenetic events in mammalian germ-cell development: reprogramming and beyond
Sasaki, H., & Matsui, Y. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2295 · Cited by 873 · see citing works
Cotranscriptional Set2 Methylation of Histone H3 Lysine 36 Recruits a Repressive Rpd3 Complex
Keogh, M., Kurdistani, S. K., Morris, S. A., Ahn, S., Podolny, V., Collins, S. R., Schuldiner, M., Chin, K., Punna, T., Thompson, N. J., et al. (2005) · Cell · doi:10.1016/j.cell.2005.10.025 · Cited by 780 · see citing works
DNA methylation profiles in monozygotic and dizygotic twins
Kaminsky, Z. A., Tang, T., Wang, S.-C., Ptak, C., Oh, G., Wong, A. H. C., Feldcamp, L. A., Virtanen, C., Halfvarson, J., Tysk, C., et al. (2009) · Nature Genetics · doi:10.1038/ng.286 · Cited by 662 · see citing works
Genetic and epigenetic regulators of pluripotency.
Surani, M., Hayashi, K., & Hájková, P. (2007) · Cell · doi:10.1016/j.cell.2007.02.010 · Cited by 648 · see citing works
5-Methylcytosine as an Endogenous Mutagen in the Human LDL Receptor and p53 Genes
Rideout, W. M., Coetzee, G. A., Olumi, A. F., & Jones, P. A. (1990) · Science · doi:10.1126/science.1697983 · Cited by 640 · see citing works
Park, J. H., Stoffers, D. A., Nicholls, R. D., & Simmons, R. A. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33655 · Cited by 640 · see citing works
Intrauterine Growth Retardation Leads to the Development of Type 2 Diabetes in the Rat
Simmons, R. A., Templeton, L. J., & Gertz, S. J. (2001) · Diabetes · doi:10.2337/diabetes.50.10.2279 · Cited by 638 · see citing works
Non-CpG methylation of the PGC-1α promoter through DNMT3B controls mitochondrial density.
Barrès, R., Osler, M. E., Yan, J., Rune, A., Fritz, T., Caidahl, K., Krook, A., & Zierath, J. R. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2009.07.011 · Cited by 602 · see citing works
Self-citationEmerging roles of non-coding RNAs in brain evolution, development, plasticity and disease
Qureshi, I., & Mehler, M. F. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3234 · Cited by 561 · see citing works
Lu, J., McKinsey, T. A., Zhang, C., & Olson, E. N. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00025-3 · Cited by 547 · see citing works
Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion
Ling, C., Del Guerra, S., Lupi, R., Rönn, T., Granhall, C., Luthman, H., Masiello, P., Marchetti, P., Groop, L., & Del Prato, S. (2008) · Diabetologia · doi:10.1007/s00125-007-0916-5 · Cited by 495 · see citing works
Role of Jhdm2a in regulating metabolic gene expression and obesity resistance
Tateishi, K., Okada, Y., Kallin, E. M., & Zhang, Y. (2009) · Nature · doi:10.1038/nature07777 · Cited by 442 · see citing works
The landscape of histone modifications across 1% of the human genome in five human cell linesPreprint
Andrews, R., Beare, D., Flicek, P., Bruce, A., Carter, N., Clelland, G., Wilcox, S., Beare, D. M., Fowler, J. C., Dovey, O., et al. (2007) · Genome Research · doi:10.1101/gr.5704207 · Cited by 441 · see citing works
Volkmar, M., Dedeurwaerder, S., Cunha, D. A., Ndlovu, M. N., Defrance, M., Deplus, R., Calonne, E., Volkmar, U., Igoillo‐Esteve, M., Naamane, N., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2011.503 · Cited by 420 · see citing works
Czubryt, M. P., McAnally, J., Fishman, G. I., & Olson, E. N. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337639100 · Cited by 418 · see citing works
Histone deacetylase degradation andMEF2 activation promote the formation of slow-twitch myofibers
Potthoff, M. J., Wu, H., Arnold, M., Shelton, J. M., Backs, J., McAnally, J., Richardson, J. A., Bassel‐Duby, R., & Olson, E. N. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31960 · Cited by 416 · see citing works
Control of muscle development by dueling HATs and HDACs
McKinsey, T. A., Zhang, C. L., & Olson, E. N. (2001) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00224-0 · Cited by 414 · see citing works
Nitert, M. D., Dayeh, T., Volkov, P., Elgzyri, T., Hall, E., Nilsson, E., Yang, B. T., Lang, S., Parikh, H. M., Wessman, Y., et al. (2012) · Diabetes · doi:10.2337/db11-1653 · Cited by 405 · see citing works
Maternal constraint of fetal growth and its consequences
Gluckman, P. D., & Hanson, M. A. (2004) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2004.03.001 · Cited by 336 · see citing works
Sandovici, I., Smith, N. H., Nitert, M. D., Ackers-Johnson, M., Uribe-Lewis, S., Ito, Y., Jones, R. H., Marquez, V. E., Cairns, W., Tadayyon, M., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019007108 · Cited by 326 · see citing works
Ollikainen, M., Smith, K. R., Joo, E. J.-H., Ng, H. K., Andronikos, R. H., Novakovic, B., Aziz, N. K. A., Carlin, J. B., Morley, R., Saffery, R., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq336 · Cited by 312 · see citing works
Silander, K., Mohlke, K. L., Scott, L. J., Peck, E. C., Hollstein, P. E., Skol, A. D., Jackson, A., Deloukas, P., Hunt, S. E., Stavrides, G., et al. (2004) · Diabetes · doi:10.2337/diabetes.53.4.1141 · Cited by 266 · see citing works
Kulkarni, R., Jhala, U. S., Winnay, J. N., Krajewski, S., Montminy, M., & Kahn, C. R. (2004) · Journal of Clinical Investigation · doi:10.1172/jci21845 · Cited by 263 · see citing works
Role of nutritional programming in determining adult morbidity.
Lucas, A. (1994) · Archives of Disease in Childhood · doi:10.1136/adc.71.4.288 · Cited by 258 · see citing works
Nguyen, C. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.22.4598 · Cited by 246 · see citing works
Exercise and Myocyte Enhancer Factor 2 Regulation in Human Skeletal Muscle
McGee, S. L., & Hargreaves, M. (2004) · Diabetes · doi:10.2337/diabetes.53.5.1208 · Cited by 205 · see citing works
Heterozygous disruption of Hic1 predisposes mice to a gender-dependent spectrum of malignant tumors
Chen, W., Zeng, X., Carter, M. G., Morrell, C. N., Yen, R.-W. C., Esteller, M., Watkins, D. N., Herman, J. G., Mankowski, J. L., & Baylin, S. B. (2003) · Nature Genetics · doi:10.1038/ng1077 · Cited by 201 · see citing works
Ling, C., Poulsen, P., Simonsson, S., Rönn, T., Holmkvist, J., Almgren, P., Hagert, P., Nilsson, E., Mabey, A. G., Nilsson, P. M., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30938 · Cited by 191 · see citing works
Kühnen, P., Mischke, M., Wiegand, S., Sers, C., Horsthemke, B., Lau, S., Keil, T. O. P., Lee, Y., Grueters, A., & Krude, H. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002543 · Cited by 177 · see citing works
Minireview: Epigenetic Programming of Diabetes and Obesity: Animal Models
Seki, Y., Williams, L., Vuguin, P. M., & Charron, M. J. (2012) · Endocrinology · doi:10.1210/en.2011-1805 · Cited by 176 · see citing works
Age influences DNA methylation and gene expression of COX7A1 in human skeletal muscle.
Rönn, T., Poulsen, P., Hansson, O., Holmkvist, J., Almgren, P., Nilsson, P., Tuomi, T., Isomaa, B., Groop, L., Vaag, A., et al. (2008) · Diabetologia · doi:10.1007/s00125-008-1018-8 · Cited by 175 · see citing works
Expansion of adult β-cell mass in response to increased metabolic demand is dependent on HNF-4α
Gupta, R. K., Gao, N., Gorski, R. K., White, P., Hardy, O. T., Rafiq, K., Brestelli, J. E., Chen, G., Stoeckert, C. J., & Kaestner, K. H. (2007) · Genes & Development · doi:10.1101/gad.1535507 · Cited by 161 · see citing works
Eriksson, K., & Liridg�rde, F. (1996) · Diabetologia · doi:10.1007/bf00403304 · Cited by 142 · see citing works
Pinney, S. E., Santos, L. J. J., Han, Y., Stoffers, D. A., & Simmons, R. A. (2011) · Diabetologia · doi:10.1007/s00125-011-2250-1 · Cited by 134 · see citing works
Exercise and skeletal muscle glucose transporter 4 expression: Molecular mechanisms
McGee, S. L., & Hargreaves, M. (2006) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2006.04362.x · Cited by 126 · see citing works
Yu, M., Blomstrand, E., Chibalin, A., Krook, A., & Zierath, J. R. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00273.x · Cited by 121 · see citing works
Eriksson, K., & Lindg�rde, F. (1996) · Diabetologia · doi:10.1007/s001250050480 · Cited by 113 · see citing works
Epigenetic Cancer Therapy Makes Headway
Mack, G. S. (2006) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djj447 · Cited by 108 · see citing works
Briššová, M., Blaha, M. J., Spear, C., Nicholson, W. E., Aramandla, R., Shiota, M., Charron, M. J., Wright, C. V. E., & Powers, A. C. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00252.2004 · Cited by 100 · see citing works
Exercise increases MEF2‐ and GEF DNA‐binding activities in human skeletal muscle
McGee, S. L., Sparling, D., Olson, A., & Hargreaves, M. (2006) · The FASEB Journal · doi:10.1096/fj.05-4671fje · Cited by 100 · see citing works
Maternal Behaviors during Pregnancy Impact Offspring Obesity Risk
Phelan, S., Hart, C. N., PHIPPS, M. G., Abrams, B. F., Schaffner, A. A., Adams, A., & Wing, R. R. (2011) · Experimental Diabetes Research · doi:10.1155/2011/985139 · Cited by 66 · see citing works
Evidence for non-CpG methylation in mammals
Yan, J., Zierath, J. R., & Barrès, R. (2011) · Experimental Cell Research · doi:10.1016/j.yexcr.2011.08.019 · Cited by 61 · see citing works
Transgenerational Genetic Effects
Nelson, V. R., & Nadeau, J. H. (2010) · Epigenomics · doi:10.2217/epi.10.57 · Cited by 58 · see citing works
Vadlamudi, S., Kalhan, S. C., & Patel, M. S. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.269.4.e731 · Cited by 57 · see citing works
Moderate Daily Exercise Activates Metabolic Flexibility to Prevent Prenatally Induced Obesity
Miles-Chan, J. L., Huber, K., Thompson, N. M., Davison, M., & Breier, B. H. (2008) · Endocrinology · doi:10.1210/en.2008-1035 · Cited by 46 · see citing works
Flagged first, then by citations
1 of the 69 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease
Smith, R. L., Soeters, M. R., Wüst, R. C. I., & Houtkooper, R. H. (2018) · Endocrine Reviews · doi:10.1210/er.2017-00211 · Cited by 787 · see citing works
The nexus of chromatin regulation and intermediary metabolism
Gut, P., & Verdin, E. M. (2013) · Nature · doi:10.1038/nature12752 · Cited by 419 · see citing works
Drug-induced liver injury: Interactions between drug properties and host factors
Chen, M., Suzuki, A., Borlak, J. T., Andrade, R. J., & Lucena, M. I. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2015.04.016 · Cited by 404 · see citing works
“Host factors influencing mitochondrial functions are listed in Table 1 [26,69,70].”
BackgroundObesity-induced DNA hypermethylation of the adiponectin gene mediates insulin resistance
Kim, A. Y., Park, Y. J., Pan, X., Shin, K. C., Kwak, S., Bassas, A. F., Sallam, R. M., Park, K. S., Alfadda, A. A., Xu, A., et al. (2015) · Nature Communications · doi:10.1038/ncomms8585 · Cited by 235 · see citing works
The role of diet and exercise in the transgenerational epigenetic landscape of T2DM
Barrès, R., & Zierath, J. R. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.87 · Cited by 198 · see citing works
Tan, X. W., Chapman, C. D., Cedernaes, J., & Benedict, C. (2017) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2017.11.001 · Cited by 194 · see citing works
vel Szic, K. S., Declerck, K., Vidaković, M., & Vanden Berghe, W. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0068-2 · Cited by 192 · see citing works
“dehydrogenase kinase; AKT/PKB, protein kinase B; PGC1, peroxisome proliferat metabolism, cellular signaling, and the epigenetic control of transcription programs [108-116] (Figure 3).”
BackgroundKirchner, H., Sinha, I., Gao, H., Ruby, M. A., Schönke, M., Lindvall, J. M., Barrès, R., Krook, A., Näslund, E. B., Dahlman‐Wright, K., et al. (2016) · Molecular Metabolism · doi:10.1016/j.molmet.2015.12.004 · Cited by 135 · see citing works
“Since DNA methylation can lead to stable alterations in the transcriptional potential, epigenetic mechanisms may partly explain the rapidly increasing prevalence of type 2 diabetes [23].”
BackgroundNanoparticles in food. Epigenetic changes induced by nanomaterials and possible impact on health
Smolková, B., Yamani, N. E., Collins, A. R., Gutleb, A. C., & Dušinská, M. (2014) · Food and Chemical Toxicology · doi:10.1016/j.fct.2014.12.015 · Cited by 134 · see citing works
“Aberrant DNA methylation was also associated with osteoarthritis (Fernández-Tajes et al., 2014) and cardiovascular disease (Kim et al., 2013), pre-eclampsia (Anderson et al., 2013), rheumatoid arthritis (Liu et al., 2013) and metabolic disorders (Bruce and Cagampang, 2011; Kirchner et al., 2013).”
BackgroundBromodomains and Their Pharmacological Inhibitors
Gallenkamp, D., Gelato, K. A., Haendler, B., & Weinmann, H. (2014) · ChemMedChem · doi:10.1002/cmdc.201300434 · Cited by 126 · see citing works
Diabetes Induces Aberrant DNA Methylation in the Proximal Tubules of the Kidney
Marumo, T., Yagi, S., Kawarazaki, W., Nishimoto, M., Ayuzawa, N., Watanabe, A., Ueda, K., Hirahashi, J., Hishikawa, K., Sakurai, H., et al. (2015) · Journal of the American Society of Nephrology · doi:10.1681/asn.2014070665 · Cited by 115 · see citing works
Epigenetic reprogramming in metabolic disorders: nutritional factors and beyond
Cheng, Z., Zheng, L., & Almeida, F. A. (2017) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2017.10.004 · Cited by 114 · see citing works
“The recognition of epigenetic reprogramming in metabolic diseases has stimulated the interest in identifying epigenetic markers for diagnosis and intervention assessment [24,39,115,127,128].”
Backgrounddos Santos, J. M., Moreli, M. L., Tewari, S., & Benite‐Ribeiro, S. A. (2015) · Metabolism · doi:10.1016/j.metabol.2015.09.013 · Cited by 107 · see citing works
Stephens, N. A., & Sparks, L. M. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-2545 · Cited by 97 · see citing works
“A recent review by Kirchner et al (106) about epigenetic flexibility in metabolic regulation emphasizes the need for a better understanding of lifestyle factors—such as exercise training or lack thereof—that may modify epigenetic programming and a predisposition to conditions such as exercise resistance (Figure 1).”
BackgroundGillberg, L., Perfilyev, A., Brøns, C., THOMASEN, M. L., Grunnet, L. G., Volkov, P., Rosqvist, F., Iggman, D., Dahlman, I. A., Risérus, U., et al. (2016) · Diabetologia · doi:10.1007/s00125-015-3852-9 · Cited by 96 · see citing works
Zhao, H., Ding, T., Ren, Y., Li, T., Li, R., Fan, Y., Yan, J., Zhao, Y., Li, M., Yu, Y., et al. (2016) · Human Reproduction · doi:10.1093/humrep/dev345 · Cited by 78 · see citing works
Vähämiko, S., Laiho, A., Lund, R., Isolauri, E., Salminen, S., & Laitinen, K. (2018) · European Journal of Nutrition · doi:10.1007/s00394-017-1601-1 · Cited by 76 · see citing works
“In particular, when occurring in utero or during the early neonatal stages, these changes in DNA methylation have been postulated to induce long-term changes in gene expression and further to act as causative agents for lifelong effects on health [10, 11].”
BackgroundJacobsen, S. C., Gillberg, L., Bork‐Jensen, J., Ribel‐Madsen, R., Lara, E., Calvanese, V., Ling, C., Fernández, A. F., Fraga, M. F., Poulsen, P., et al. (2014) · Diabetologia · doi:10.1007/s00125-014-3198-8 · Cited by 72 · see citing works
“The involvement of tissue-specific DNA methylation in the pathogenesis of type 2 diabetes is supported by several studies [2–4].”
BackgroundResultAltered promoter methylation of PDK4, IL1 B, IL6, and TNF after Roux-en Y gastric bypass
Kirchner, H., Nylén, C., Laber, S., Barrès, R., Yan, J., Krook, A., Zierath, J. R., & Näslund, E. B. (2014) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2013.12.019 · Cited by 72 · see citing works
“Epigenetic gene regulation plays a role in the pathogenesis of metabolic diseases, such as obesity and type 2 diabetes [1].”
BackgroundGuéant, J., Akoum, R. E., Ziegler, O., Coelho, D., Feigerlová, E., Daval, J., & Guéant‐Rodriguez, R. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1339-4 · Cited by 62 · see citing works
“Consistently, sedentary lifestyle and lack of physical activity may modify epigenetic programming and predisposition to obesity and T2DM, as recently reviewed [94].”
BackgroundOrtega, J. G., Echeverri, I., Plata, C. A., & Castillo, A. (2014) · Nutrition Reviews · doi:10.1093/nutrit/nuu001 · Cited by 62 · see citing works
Grilo, L. F., Tocantins, C., Diniz, M. S., Gomes, R. M., Oliveira, P. J., Matafome, P. N., & Pereira, S. P. (2021) · European Journal of Clinical Investigation · doi:10.1111/eci.13625 · Cited by 62 · see citing works
Gu, T., Gu, H., Hilding, A., Sjöholm, L. K., Östenson, C., Ekström, T., & Brismar, K. (2013) · Clinical Epigenetics · doi:10.1186/1868-7083-5-21 · Cited by 49 · see citing works
“Therefore, epigenetic studies may provide further information to give a better understanding of the pathogenesis of type 2 diabetes [4-6].”
BackgroundSeman, N. A., Mohamud, W. N. W., Östenson, C., Brismar, K., & Gu, H. F. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0049-5 · Cited by 53 · see citing works
“Epigenetic factors mainly including DNA methylation changes have been considered to be involved in the pathogenesis of T2D [13-15].”
BackgroundRecent advances in the managements of type 2 diabetes mellitus and natural hypoglycemic substances
Ning, C., Jiao, Y., Wang, J., Li, W., Zhou, J., Lee, Y., Ma, D., Leung, C., Zhu, R., & Wang, H. (2022) · Food Science and Human Wellness · doi:10.1016/j.fshw.2022.04.004 · Cited by 51 · see citing works
Naidoo, V., Naidoo, M., & Ghai, M. (2018) · Scandinavian Journal of Immunology · doi:10.1111/sji.12723 · Cited by 51 · see citing works
“A genome‐wide association studies (GWASs) identified genes which accounted for just 10% of the heritable risk for T2DM, whilst the remaining “missing” heritability could be contributed by rare variants, gene‐environment interactions, gene‐gene interactions and epigenetic factors.(8) Altered DNAm as well as decreased e…”
BackgroundUnderstanding type 2 diabetes: from genetics to epigenetics
Raciti, G. A., Longo, M., Parrillo, L., Ciccarelli, M., Mirra, P., Ungaro, P., Formisano, P., Miele, C., & Beguinot, F. (2015) · Acta Diabetologica · doi:10.1007/s00592-015-0741-0 · Cited by 49 · see citing works
“modifications of the DNA [1].”
Epigenetic Regulation of PDX-1 in Type 2 Diabetes Mellitus
Liu, J.-M., Lang, G., & Shi, J.-S. (2021) · Diabetes, Metabolic Syndrome and Obesity : Targets and Therapy · doi:10.2147/dmso.s291932 · Cited by 39 · see citing works
Personalized Medicine and Type 2 Diabetes: Lesson from Epigenetics
Raciti, G. A., Nigro, C., Longo, M., Parrillo, L., Miele, C., Formisano, P., & Bèguinot, F. (2014) · Epigenomics · doi:10.2217/epi.14.10 · Cited by 47 · see citing works
Post‐translational modifications of the cardiac proteome in diabetes and heart failure
Wende, A. R. (2015) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.201500052 · Cited by 49 · see citing works
“Although epigenetics can be transgenerational [57], the associated modifications can be dynamically regulated by lifestyle [58].”
BackgroundBourlier, V., Saint-Laurent, C., Louche, K., Badin, P.-M., Thalamas, C., de Glisezinski, I., Langin, D., Sengenès, C., & Moro, C. (2013) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2013-1727 · Cited by 51 · see citing works
“Lifestyle factors such as exercise and nutrition could influence epigenetic metabolic programming of muscle cells and predisposition to obesity and T2DM, as recently discussed (29).”
BackgroundEpigenetic inheritance of metabolic state
Palu, R. A. S., & Thummel, C. S. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2014.03.008 · Cited by 43 · see citing works
“Because these chromatin marks tend to be more dynamic than DNA methylation, their levels have not been examined as closely [25].”
BackgroundSen, S., Sanyal, S., Srivastava, D. K., Dasgupta, D., Roy, S., & Das, C. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.786863 · Cited by 41 · see citing works
“Further, alteration in H3K4Me2/3 status in the adipocyte cells has been reported in T2D patients (11).”
BackgroundInfluentialMaternal diabetes, programming of beta-cell disorders and intergenerational risk of type 2 diabetes
Chavey, A., Kioon, M. D. A., Bailbé, D., Movassat, J., & Portha, B. (2014) · Diabetes & Metabolism · doi:10.1016/j.diabet.2014.02.003 · Cited by 38 · see citing works
“However, recent research has provided vidence that epigenetic mechanisms are flexible, allowing rapid daptation to a changing environment such as altered nutrition, nd may contribute to the development and transgenerational nheritance of obesity and T2D [69].”
BackgroundMałodobra-Mazur, M., Dziewulska, A., Koziński, K., Dobrzyń, P., Kolczyńska, K., Janikiewicz, J., & Dobrzyń, A. (2014) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2014.08.005 · Cited by 37 · see citing works
Elevated CpG island methylation of GCK gene predicts the risk of type 2 diabetes in Chinese males
Tang, L., Ye, H., Hong, Q., Wang, L., Wang, Q., Wang, H., Xu, L., Bu, S., Zhang, L., Cheng, J. R., et al. (2014) · Gene · doi:10.1016/j.gene.2014.06.062 · Cited by 36 · see citing works
Kijimoto, T., Snell‐Rood, E. C., Pespeni, M. H., Rocha, G., Kafadar, K., & Moczek, A. P. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.2084 · Cited by 36 · see citing works
“Moreover, dysfunctional nutrition-dependent gene expression is thought to underlie many human diseases such as diabetes, obesity, Crohn’s disease and possibly even cancer [4–8].”
BackgroundOlioso, D., Dauriz, M., Bacchi, E., Negri, C., Santi, L., Bonora, E., & Moghetti, P. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-01820 · Cited by 37 · see citing works
“The effect of environmental factors on metabolic regulation has recently gained molecular rationale by insights brought by epigenetics (6, 7).”
Epigenetics and Helicobacter pylori
Capparelli, R., & Iannelli, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031759 · Cited by 35 · see citing works
“In addition to cancer, epigenetics also influences infectious diseases (see below) and metabolic diseases (type 2 diabetes, obesity, cardiovascular diseases) [24,25].”
BackgroundEnquobahrie, D. A., Moore, A. L., Muhie, S. Y., Tadesse, M. G., Lin, S., & Williams, M. A. (2015) · Reproductive Sciences · doi:10.1177/1933719115570903 · Cited by 33 · see citing works
“Variations in DNA methylation have been associated with the pathogenesis of metabolic diseases, including type 2 diabetes (T2D).(2,3) Gestational diabetes mellitus (GDM), abnormal glucose metabolism first diagnosed during pregnancy, is a complex disorder that shares risk factors and pathophysiological characteristics…”
BackgroundThe metabolic-epigenetic nexus in type 2 diabetes mellitus
Davison, G. W., Irwin, R. E., & Walsh, C. P. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.12.025 · Cited by 35 · see citing works
Association of Interleukin-10 Methylation Levels With Gestational Diabetes in a Taiwanese Population
Kang, J., Lee, C., Li, H., Hsu, K.-H., Wang, S., & Lin, S. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00222 · Cited by 32 · see citing works
Mudry, J. M., Lassiter, D. G., Nylén, C., García-Calzón, S., Näslund, E. B., Krook, A., & Zierath, J. R. (2016) · Diabetes · doi:10.2337/db16-0882 · Cited by 32 · see citing works
“Skeletal muscle insulin resistance may arise in part from a dysfunctional metabolic program, either of an epigenetic or genetic origin (6).”
BackgroundNilsson, E., Ernst, B., Voisin, S. A. C., Almén, M. S., Benedict, C., Mwinyi, J., Fredriksson, R., Schultes, B., & Schiöth, H. B. (2015) · PLoS ONE · doi:10.1371/journal.pone.0115186 · Cited by 30 · see citing works
“These findings may form the basis for further investigations to unravel the molecular effects of gastric bypass surgery, as epigenetic modifications are proposed to play an important role in the development of metabolic diseases, including type 2 diabetes and obesity [15].”
BackgroundKasch, J., Kanzleiter, I., Saussenthaler, S., Schürmann, A., Keijer, J., van Schothorst, E. M., Klaus, S., & Schumann, S. (2018) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2018.03.015 · Cited by 30 · see citing works
Ciccarelli, M., Vastolo, V., Albano, L., Lecce, M., Cabaro, S., Liotti, A., Longo, M., Oriente, F., Russo, G. L., Macchia, P. E., et al. (2015) · Diabetologia · doi:10.1007/s00125-015-3774-6 · Cited by 30 · see citing works
“understanding of the molecular events involved in the remarkable impact of the environment on type 2 diabetes risk [12, 13]”
BackgroundHernández‐Aguilera, A., Fernández‐Arroyo, S., Cuyàs, E., Luciano‐Mateo, F., Cabré, N., Camps, J., López‐Miranda, J., Menéndez, J. A., & Joven, J. (2016) · Food and Chemical Toxicology · doi:10.1016/j.fct.2016.08.006 · Cited by 30 · see citing works
“Therefore, available data provide evidence that diet-induced metabolic changes might influence preconceptional behavior (Kirchner et al., 2013; Patti, M AN US CR IP T AC CE PT ED 28 2013), but mechanistic insights are not sufficient to explain the overall picture.”
BackgroundBengtsen, M., Winje, I. M., Eftestøl, E., Landskron, J., Sun, C., Nygård, K., Domańska, D., Millay, D. P., Meza‐Zepeda, L. A., & Gundersen, K. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009907 · Cited by 26 · see citing works
“Epigenetic mechanisms like histone modifications and chromatin structure have been suggested to play an important role in the development of and predisposition for metabolic syndrome [12], but data supporting this is currently scarce.”
BackgroundEpigenetics and type II diabetes mellitus: underlying mechanisms of prenatal predisposition
Sterns, J. D., Smith, C. B., Steele, J. R., Stevenson, K. L., & Gallicano, G. I. (2014) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2014.00015 · Cited by 27 · see citing works
“…interplays with the enormous epigenetic variation induced postnatally by various environmental stimuli and aging, pharmaceutical intervention, and lifestyle choices such as exercise (Fraga et al., 2005; Kaminsky et al., 2009; Pinney et al., 2011; Nitert et al., 2012; Kirchner et al., 2013).”
BackgroundResultA decrease in hepatic microRNA-9 expression impairs gluconeogenesis by targeting FOXO1 in obese mice
Yan, C., Chen, J., Li, M., Xuan, W., Su, D., You, H., Huang, Y., Chen, N., & Liang, X. (2016) · Diabetologia · doi:10.1007/s00125-016-3932-5 · Cited by 27 · see citing works
“Recent research has shown that epigenetic DNA modifications contribute to the development of type 2 diabetes [22, 23].”
BackgroundAberrant DNA methylation of Tgfb1 in diabetic kidney mesangial cells
Oba, S., Ayuzawa, N., Nishimoto, M., Kawarazaki, W., Ueda, K., Hirohama, D., Kawakami-Mori, F., Shimosawa, T., Marumo, T., & Fujita, T. (2018) · Scientific Reports · doi:10.1038/s41598-018-34612-3 · Cited by 27 · see citing works
Woelfel, J. R., Dudley-Javoroski, S., & Shields, R. (2018) · Physical Therapy · doi:10.1093/ptj/pzy092 · Cited by 21 · see citing works
Inflammation, Advancing Age and Nutrition
(2014) · Elsevier eBooks · doi:10.1016/c2011-0-08000-6 · Cited by 25 · see citing works
“intercellular/extracellular energetic status, nutrientresponsive metabolites, such as ATP, acetyl-CoA, UDP-N-acetylglucosamine (UDP-GlcNAc), and SAM, mediate crosstalk between metabolism, cellular signaling, and epigenetic control of transcriptional programs [40–48].”
BackgroundYonamine, C. Y., Alves-Wagner, A. B., Esteves, J. V. D. C., Okamoto, M. M., Corrêa‐Giannella, M. L., Giannella‐Neto, D., & Machado, U. F. (2018) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2018.11.006 · Cited by 23 · see citing works
Geißler, C., Krause, C., Neumann, A., Britsemmer, J. H., Taege, N., Grohs, M., Kaehler, M., Cascorbi, I., Lewis, A. G., Seeley, R. J., et al. (2021) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2021.108907 · Cited by 22 · see citing works
Social Environment and Epigenetics
Merrill, S. M., Gladish, N., & Kobor, M. S. (2019) · Current topics in behavioral neurosciences · doi:10.1007/7854_2019_114 · Cited by 23 · see citing works
The effect of diet on the intestinal epigenome
Johnson, I. T., & Belshaw, N. J. (2014) · Epigenomics · doi:10.2217/epi.14.8 · Cited by 21 · see citing works
BCL11A gene DNA methylation contributes to the risk of type 2 diabetes in males
Tang, L., Wang, L., Ye, H., Xu, X., Hong, Q., WANG, H., Xu, L., Bu, S., Zhang, L., Cheng, J. R., et al. (2014) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2014.1783 · Cited by 21 · see citing works
“DNA methylation and histone modification have become alternative approaches that have aided the understanding of β -cell dysfunction in the pathogenesis (11) and the high growth rate of T2D (12).”
Longitudinal genome-wide DNA methylation changes in response to kidney failure replacement therapy
Witasp, A., Luttropp, K., Qureshi, A. R., Barany, P. F., Heimbürger, O., Wennberg, L. M., Ekström, T. J., Shiels, P. G., Stenvinkel, P., & Nordfors, L. (2022) · Scientific Reports · doi:10.1038/s41598-021-04321-5 · Cited by 20 · see citing works
Epigenetic Downregulation of FASN in Visceral Adipose Tissue of Insulin Resistant Subjects
Sievert, H., Krause, C., Geißler, C., Grohs, M., Gammal, A. T. E., Wolter, S., Mann, O., Lehnert, H., & Kirchner, H. (2020) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/a-1150-7446 · Cited by 20 · see citing works
Yonamine, C. Y., Passarelli, M., Suemoto, C. K., Pasqualucci, C. A., Filho, W. J., Alves, V. A. F., Marie, S. K. N., Corrêa‐Giannella, M. L., Britto, L. R., & Machado, U. F. (2023) · Cells · doi:10.3390/cells12091250 · Cited by 18 · see citing works
“Among PTMs, lysine acetylation of histone 3 and 4 (H3Kac, H4Kac) are the most studied [64], and changes in H3Kac content have already been reported to be triggered by DM in the Slc2a4 promoter, accompanying a reduction in muscle Slc2a4/GLUT4 expression [51,65].”
BackgroundKhatun, M., Lundin, K., Naillat, F., Loog, L., Saarela, U., Tuuri, T., Salumets, A., Piltonen, T., & Tapanainen, J. S. (2023) · Stem Cell Reviews and Reports · doi:10.1007/s12015-023-10627-w · Cited by 17 · see citing works
“Epigenetic alterations and both heritable and non-heritable changes in gene expression not affecting underlying DNA sequences, have also been offered as a possible explanation for missing heritability in this complex metabolic disorder [79, 84, 85].”
BackgroundTranscriptional and epigenetic control of adipocyte remodeling during obesity
Barilla, S., Treuter, E., & Venteclef, N. (2021) · Obesity · doi:10.1002/oby.23248 · Cited by 18 · see citing works
“DNA methylation can potentially be the result of the interaction between genetics and the environment, which can influence metabolic homeostasis and predispose one to metabolic disease (84).”
BackgroundPrenatal inflammation exposure-programmed cardiovascular diseases and potential prevention
Deng, Y., Song, L., Nie, X., Shou, W., & Li, X. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.05.009 · Cited by 18 · see citing works
Engineered nanoparticle-induced epigenetic changes: An important consideration in nanomedicine
Zhang, W., Liu, S., Han, D., & He, Z. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.09.034 · Cited by 17 · see citing works
Deligiannidou, G.-E., Athina, S., Berghe, W. V., Christos, K., & Constantinides, T. K. (2019) · Current Pharmaceutical Biotechnology · doi:10.2174/1573407215666190628150921 · Cited by 17 · see citing works
Huang, C.-C., Chen, M., Lan, C.-W., Wu, C.-E., Huang, M.-C., Kuo, H., & Ho, H. (2019) · Fertility and Sterility · doi:10.1016/j.fertnstert.2019.05.004 · Cited by 16 · see citing works
Yan, L., Huang, J., Xie, Z., Wang, C., Li, Y., Hua, Y., Liu, C., & Yuan, R. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1282077 · Cited by 15 · see citing works
Esefeld, K., Kreß, S., Behrens, M., Zimmer, P., Stümvoll, M., Thurm, U., Gehr, B., Brinkmann, C. K., & Halle, M. (2020) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/a-1284-6097 · Cited by 15 · see citing works
Embryonic programming of heart disease in response to obesity during pregnancy
Ahmed, A., & Delgado-Olguı́n, P. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2019.01.028 · Cited by 14 · see citing works
Lü, X., Hu, S., Liao, Y., Zheng, J., Zeng, T., Zhong, X., Liu, G., Gou, L., & Chen, L. (2020) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00090.2020 · Cited by 14 · see citing works
Terra, M. M., Fontoura, T. S., Nogueira, A. O., Lopes, J. F., Mathias, P. C. D. F., Andreazzi, A. E., Guerra, M. D. O., & Peters, V. M. (2019) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174419000503 · Cited by 13 · see citing works
Guarasci, F., D’Aquila, P., Montesanto, A., Corsonello, A., Bellizzi, D., & Passarino, G. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666191112095655 · Cited by 14 · see citing works
Davis, R., Murgia, C., Dordevic, A. L., Bonham, M. P., & Huggins, C. E. (2021) · Clinical Nutrition · doi:10.1016/j.clnu.2021.01.011 · Cited by 13 · see citing works
Lysine-Specific Demethylase 1 in Energy Metabolism: A Novel Target for Obesity
Wang, D., Kuang, Y., Zhang, G., Xiao, K., & Liu, Y. (2022) · Journal of Nutrition · doi:10.1093/jn/nxac080 · Cited by 12 · see citing works
Kemmer, F., Halle, M., Stümvoll, M., Thurm, U., & Zimmer, P. (2011) · Diabetologie und Stoffwechsel · doi:10.1055/s-0031-1283771 · Cited by 12 · see citing works
Current epigenetic aspects the clinical kidney researcher should embrace.
Witasp, A., Craenenbroeck, A. V. V., Shiels, P., Ekström, T., Stenvinkel, P., & Nordfors, L. (2017) · Clinical science · doi:10.1042/cs20160596 · Cited by 11 · see citing works
Varghese, D. S., Alawathugoda, T. T., Sheikh, M. A., Challagandla, A. K., Emerald, B. S., & Ansari, S. A. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05125-9 · Cited by 11 · see citing works
“Identifying epigenetic biomarkers in individuals with a genetic predisposition to obesity could be considered to avoid further exacerbation due to geneenvironment interactions [27].”
BackgroundKernel machine methods for integrative analysis of genome‐wide methylation and genotyping studies
Zhao, N., Zhan, X., Huang, Y., Almli, L. M., Smith, A. K., Epstein, M. P., Conneely, K. N., & Wu, M. C. (2017) · Genetic Epidemiology · doi:10.1002/gepi.22100 · Cited by 11 · see citing works
“The etiology for most common human diseases is believed to be multifactorial, with risk factors including heritable genetic variants as well as environmental, behavioral factors and possible interactions between them (Luzzatto and Pandolfi, 2015; Kirchner et al., 2013).”
BackgroundHigh-Throughput Analysis of Global DNA Methylation Using Methyl-Sensitive Digestion
Shiratori, H., Feinweber, C., Knothe, C., Lötsch, J., Thomas, D., Geißlinger, G., Parnham, M. J., & Resch, E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0163184 · Cited by 11 · see citing works
Sen, D., Maniyadath, B., Chowdhury, S., Kaur, A., Khatri, S., Chakraborty, A., Mehendale, N., Nadagouda, S., Sandra, U. S., Kamat, S. S., et al. (2023) · iScience · doi:10.1016/j.isci.2023.107128 · Cited by 10 · see citing works
Integration of epigenomics and metabolomics: From biomarkers discovery to personalized medicine
Baghel, R., Maan, K., Haritwal, T., & Rana, P. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-85652-2.00002-6 · Cited by 10 · see citing works
Metaboloepigenetics: The Emerging Network in Stem Cell Homeostasis Regulation
Avitabile, D., Magenta, A., Lauri, A., Gambini, E., Spaltro, G., & Vinci, M. C. (2016) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x11666151203223839 · Cited by 10 · see citing works
Epigenetic regulation and heart failure
Cao, D. J. (2014) · Expert Review of Cardiovascular Therapy · doi:10.1586/14779072.2014.942285 · Cited by 10 · see citing works
“The offspring of these parents were predisposed to develop obesity and Type 2 diabetes [108].”
BackgroundChildhood obesity: a (re) programming disease?
Paes, S. T., Gonçalves, C., Terra, M. M., Fontoura, T. S., Guerra, M. D. O., Peters, V., Mathias, P. C. D. F., & Andreazzi, A. (2015) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174415007837 · Cited by 13 · see citing works
“Consequently, this can either enhance or silence the expression of genes affecting body weight control and appetite.(24,29) It is necessary to develop and encourage preventive measures and attenuation of the incidence of obesity in the early periods of life, as the early adoption of positive metabolic stimuli could ev…”
BackgroundInfluentialVascular Smooth Muscle as a Target for Novel Therapeutics
Porter, K. E., & Riches‐Suman, K. (2015) · Current Diabetes Reports · doi:10.1007/s11892-015-0647-9 · Cited by 8 · see citing works
Esefeld, K., Kreß, S., Behrens, M., Zimmer, P., Stümvoll, M., Thurm, U., Gehr, B., Brinkmann, C. K., & Halle, M. (2021) · Diabetologie und Stoffwechsel · doi:10.1055/a-1515-8792 · Cited by 8 · see citing works
Oelkrug, R., Herrmann, B., Geißler, C., Harder, L., Koch, C. E., Lehnert, H., Oster, H., Kirchner, H., & Mittag, J. (2017) · Molecular Metabolism · doi:10.1016/j.molmet.2017.06.016 · Cited by 7 · see citing works
S-Nitrosoglutathione Reverts Dietary Sucrose-Induced Insulin Resistance
Sousa‐Lima, I., Fernandes, A. B., Patarrão, R. S., Kim, Y., & Macedo, M. P. (2020) · Antioxidants · doi:10.3390/antiox9090870 · Cited by 7 · see citing works
“The development of T2D is now agreed to be a consequence of both lifestyle and genetic background [2,3].”
BackgroundInsulin-like growth factor binding protein 1 DNA methylation in type 2 diabetes
Hafez, S. M., Abou-Youssef, H. S., Awad, M. A. M., Kamel, S., Youssef, R. N., Elshiekh, S. M., Raslan, H., & Salah, N. (2021) · Egyptian Journal of Medical Human Genetics · doi:10.1186/s43042-021-00153-0 · Cited by 7 · see citing works
“Due to the limited information provided on epigenetic factors associated with T2D until now, further epigenetic studies have been required, to help in better understand T2D pathogenesis [4].”
BackgroundDeriving at candidate genes of metabolic stress from pancreas of WNIN/GR-Ob mutant rats
Singh, H., Nappanveettil, G., Bhonde, R. R., & Venkatesan, V. (2013) · Islets · doi:10.4161/isl.25520 · Cited by 6 · see citing works
Esefeld, K., Heinicke, V., Kreß, S., Behrens, M., Zimmer, P., Stümvoll, M., Brinkmann, C. K., & Halle, M. (2020) · Ernährung & Medizin · doi:10.1055/a-1126-9975 · Cited by 5 · see citing works
Esefeld, K., Kreß, S., Behrens, M., Zimmer, P., Stümvoll, M., Thurm, U., Gehr, B., Halle, M., & Brinkmann, C. K. (2023) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/a-1946-3768 · Cited by 5 · see citing works
Lu, X., Lou, Y., Zhou, K., Jiang, S., & Shi, J. (2022) · Nucleosides Nucleotides & Nucleic Acids · doi:10.1080/15257770.2022.2057534 · Cited by 5 · see citing works
“In other words, metabolic diseases maybe related with the DNA character.[30] So, the binding interaction of FBST with DNA has great significance for further understanding the pharmacological and toxicological functions of FBST.”
Transcriptome profiling of liver of non-genetic low birth weight and long term health consequences
Miranda, A., López-Cardona, A., Laguna-Barraza, R., Calle, A., López-Vidriero, I., Pintado, B., & Gutiérrez-Adán, A. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-327 · Cited by 4 · see citing works
“The mechanisms whereby an event that occurs early in life may have long term effects on the phenotype of an organism many years later are only now starting to emerge [14-17].”
BackgroundSleep disorders interactions with obesity and type 2 diabetes
Brodovskaya, T. O., Grishina, I. F., Babykina, G., Николаенко, О. В., Андреевич, К. Е., Bazhenova, O. V., Beresneva, V. E., & Buharova, S. Y. (2019) · Obesity and metabolism · doi:10.14341/omet9963 · Cited by 4 · see citing works
Esefeld, K., Kreß, S., Behrens, M., Zimmer, P., Stümvoll, M., Thurm, U., Gehr, B., Brinkmann, C. K., & Halle, M. (2020) · Diabetologie und Stoffwechsel · doi:10.1055/a-1193-3901 · Cited by 4 · see citing works
Hasan, N. S., Dine, H. G. E., Kamel, S. A., Hamed, M., Youssef, R. N., Hassan, E. M., Abdelrahman, A. H., Musa, N. I., Ali, A., & Awadallah, E. A. (2023) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2023.110677 · Cited by 3 · see citing works
Esefeld, K., Heinicke, V., Kreß, S., Behrens, M., Zimmer, P., Stümvoll, M., Brinkmann, C. K., & Halle, M. (2020) · Der Diabetologe · doi:10.1007/s11428-020-00610-1 · Cited by 3 · see citing works
Early introduction of exercise prevents insulin resistance in postnatal overfed rats
Fischer, S. V., Appel, M. H., Naliwaiko, K., Pagliosa, D. D., Araújo, D. N., Capote, A. E., Oliveira, B. A. C., & Fernandes, L. C. (2022) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x2022e11987 · Cited by 2 · see citing works
- Authors
- Kirchner, H., Osler, M. E., Krook, A., & Zierath, J. R.
- Affiliations
- Karolinska Institutet (SE)
- Corresponding author
- Zierath, Juleen R.
- Venue
- Trends in Cell Biology
- Publisher
- Elsevier BV
- Published
- 2013-05
- Volume
- 23
- Issue
- 5
- Pages
- 203-209
- ISSN
- 0962-8924 (ISSN-L)
- OpenAlex
- W2082220761
- Cited by
- 143
- References
- 69
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 3 · 2023: 9 · 2022: 9 · 2021: 12 · 2020: 10 · 2019: 12 · 2018: 12 · 2017: 8 · 2016: 15 · 2015: 19 · 2014: 19 · 2013: 7
- FWCI
- 1.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Keywords
- epigenetics, DNA methylation, histone modifications, metabolic disorders, type 2 diabetes, obesity, in utero programming, epigenetic inheritance, physical activity, nutrition, disease prevention
- MeSH terms
- Diabetes Mellitus, Type 2, Environment, Female, Fetal Growth Retardation, Histones, Humans, Life Style, Obesity, Pregnancy, Exercise, DNA Methylation, Genetic Predisposition to Disease, Maternal Nutritional Physiological Phenomena, Epigenesis, Genetic, Fetal Development
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