Non-CpG methylation of the PGC-1α promoter through DNMT3B controls mitochondrial density.
Open accessAbstract
Epigenetic modification through DNA methylation is implicated in metabolic disease. Using whole-genome promoter methylation analysis of skeletal muscle from normal glucose-tolerant and type 2 diabetic subjects, we identified cytosine hypermethylation of peroxisome proliferator-activated receptor gamma (PPARgamma) coactivator-1 alpha (PGC-1alpha) in diabetic subjects. Methylation levels were negatively correlated with PGC-1alpha mRNA and mitochondrial DNA (mtDNA). Bisulfite sequencing revealed that the highest proportion of cytosine methylation within PGC-1alpha was found within non-CpG nucleotides. Non-CpG methylation was acutely increased in human myotubes by exposure to tumor necrosis factor-alpha (TNF-alpha) or free fatty acids, but not insulin or glucose. Selective silencing of the DNA methyltransferase 3B (DNMT3B), but not DNMT1 or DNMT3A, prevented palmitate-induced non-CpG methylation of PGC-1alpha and decreased mtDNA and PGC-1alpha mRNA. We provide evidence for PGC-1alpha hypermethylation, concomitant with reduced mitochondrial content in type 2 diabetic patients, and link DNMT3B to the acute fatty-acid-induced non-CpG methylation of PGC-1alpha promoter.
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PGC-1α expression may also be reduced as a consequence of promoter methylation or caused by insulin itself, obesity, and sustained lipid exposure.
“In turn, PGC-1␣ expression may also be reduced as a consequence of promoter methylation (146) or caused by insulin itself (145), obesity (126), and sustained lipid exposure (126).”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [146]
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Mootha, V. K., Lindgren, C. M., Eriksson, K.-F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstråle, M., Laurila, E., et al. (2003) · Nature Genetics · doi:10.1038/ng1180 · Cited by 10,197 · see citing works
DAVID: Database for Annotation, Visualization, and Integrated Discovery
Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., & Lempicki, R. A. (2003) · Genome Biology · doi:10.1186/gb-2003-4-5-p3 · Cited by 9,327 · see citing works
Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)80611-x · Cited by 4,139 · see citing works
Dysfunction of Mitochondria in Human Skeletal Muscle in Type 2 Diabetes
Kelley, D. E., He, J., Menshikova, E. V., & Ritov, V. B. (2002) · Diabetes · doi:10.2337/diabetes.51.10.2944 · Cited by 2,321 · see citing works
Metabolic control through the PGC-1 family of transcription coactivators
Lin, J., Handschin, C., & Spiegelman, B. M. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.05.004 · Cited by 2,130 · see citing works
Patti, M. E., Butte, A. J., Crunkhorn, S., Cusi, K., Berria, R., Kashyap, S., Miyazaki, Y., Kohane, I., Costello, M., Saccone, R., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1032913100 · Cited by 1,952 · see citing works
Chromatin modification and epigenetic reprogramming in mammalian development
Li, E. (2002) · Nature Reviews Genetics · doi:10.1038/nrg887 · Cited by 1,900 · see citing works
Weber, M., Davies, J. J., Wittig, D., Oakeley, E., Haase, M., Lam, W., & Schübeler, D. (2005) · Nature Genetics · doi:10.1038/ng1598 · Cited by 1,885 · see citing works
Epigenetic inheritance at the agouti locus in the mouse
Morgan, H. D., Sutherland, H. G. E., Martin, D. I. K., & Whitelaw, E. (1999) · Nature Genetics · doi:10.1038/15490 · Cited by 1,476 · see citing works
Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon
Issa, J.-P. J., Ottaviano, Y. L., Celano, P., Hamilton, S. R., Davidson, N. E., & Baylin, S. B. (1994) · Nature Genetics · doi:10.1038/ng0894-536 · Cited by 1,191 · see citing works
DeFronzo, R. A., Gunnarsson, R., Björkman, O., Olsson, M., & Wahren, J. (1985) · Journal of Clinical Investigation · doi:10.1172/jci111938 · Cited by 1,167 · see citing works
Sex-specific, male-line transgenerational responses in humans
The ALSPAC Study Team, Pembrey, M. E., Bygren, L. O., Kaati, G., Edvinsson, S., Northstone, K., Sjöström, M., & Golding, J. (2006) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201538 · Cited by 1,150 · see citing works
Ramsahoye, B., Biniszkiewicz, D., Lyko, F., Clark, V. H., Bird, A., & Jaenisch, R. (2000) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.97.10.5237 · Cited by 1,018 · see citing works
Morino, K., Petersen, K. F., & Shulman, G. I. (2006) · Diabetes · doi:10.2337/db06-s002 · Cited by 853 · see citing works
Borkman, M., Storlien, L. H., Pan, D. A., Jenkins, A. B., Chisholm, D. J., & Campbell, L. V. (1993) · New England Journal of Medicine · doi:10.1056/nejm199301283280404 · Cited by 835 · see citing works
Morino, K. (2005) · Journal of Clinical Investigation · doi:10.1172/jci25151 · Cited by 811 · see citing works
Early Metabolic Defects in Persons at Increased Risk for Non-Insulin-Dependent Diabetes Mellitus
Eriksson, J., Franssila-Kallunki, A., Ekstrand, A., Saloranta, C., Widén, E., Schalin, C., & Groop, L. (1989) · New England Journal of Medicine · doi:10.1056/nejm198908103210601 · Cited by 807 · see citing works
Maternal Methyl Supplements in Mice Affect Epigenetic Variation and DNA Methylation of Offspring
Cooney, C. A., Dave, A. A., & Wolff, G. L. (2002) · Journal of Nutrition · doi:10.1093/jn/132.8.2393s · Cited by 784 · see citing works
Intra-individual Change Over Time in DNA Methylation With Familial Clustering
Bjornsson, H. T. (2008) · JAMA · doi:10.1001/jama.299.24.2877 · Cited by 702 · see citing works
Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle
Boushel, R., Gnaiger, E., Schjerling, P., Skovbro, M., Kraunsøe, R., & Dela, F. (2007) · Diabetologia · doi:10.1007/s00125-007-0594-3 · Cited by 519 · 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
Evidence for an instructive mechanism of de novo methylation in cancer cells
Keshet, I., Schlesinger, Y., Farkash, S., Rand, E., Hecht, M., Segal, E., Pikarsky, E., Young, R. A., Niveleau, A., Cedar, H., et al. (2006) · Nature Genetics · doi:10.1038/ng1719 · Cited by 477 · see citing works
Costello, J., & Plass, C. (2001) · Journal of Medical Genetics · doi:10.1136/jmg.38.5.285 · Cited by 447 · 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
Simoneau, J.-A., & Kelley, D. E. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.83.1.166 · Cited by 441 · see citing works
Siegmund, K. D., Connor, C., Campan, M., Long, T. I., Weisenberger, D. J., Biniszkiewicz, D., Jaenisch, R., Laird, P. W., & Akbarian, S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000895 · Cited by 411 · see citing works
A modified and improved method for bisulphite based cytosine methylation analysis.
Olek, A., Oswald, J., & Walter, J. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.24.5064 · Cited by 411 · see citing works
Dobbins, R. L., Szczepaniak, L. S., Bentley, B., Esser, V., Myhill, J., & McGarry, J. D. (2001) · Diabetes · doi:10.2337/diabetes.50.1.123 · Cited by 315 · see citing works
Karimi, M., Johansson, S., Stach, D., Corcoran, M., Grandér, D., Schalling, M., Bakalkin, G., Lyko, F., Larsson, C., & Ekström, T. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.03.006 · Cited by 311 · see citing works
Michaud, E. J., van Vugt, M. J., Bultman, S. J., Sweet, H. O., Davisson, M. T., & Woychik, R. P. (1994) · Genes & Development · doi:10.1101/gad.8.12.1463 · Cited by 279 · see citing works
G ENETIC E FFECTS OF M ETHYLATION D IETS
den Veyver, I. B. V. (2002) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.22.010402.102932 · Cited by 214 · see citing works
Evidence for cytosine methylation of non‐symmetrical sequences in transgenic Petunia hybrida.
Meyer, P., Niedenhof, I., & ten Lohuis, M. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06483.x · Cited by 191 · 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
Summers, S. A., & Nelson, D. H. (2005) · Diabetes · doi:10.2337/diabetes.54.3.591 · Cited by 185 · 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
Male-line transgenerational responses in humans
Pembrey, M. E. (2010) · Human Fertility · doi:10.3109/14647273.2010.524721 · Cited by 164 · see citing works
Grandjean, V., Yaman, R., Cuzin, F., & Rassoulzadegan, M. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001136 · Cited by 89 · see citing works
Walker, J. A., Hedges, D. J., Perodeau, B. P., Landry, K. E., Stoilova, N., Laborde, M. E., Shewale, J. G., Sinha, S. K., & Batzer, M. A. (2004) · Analytical Biochemistry · doi:10.1016/j.ab.2004.09.036 · Cited by 88 · see citing works
Karlsson, H., Ahlsén, M., Zierath, J. R., Wallberg‐Henriksson, H., & Koistinen, H. A. (2006) · Diabetes · doi:10.2337/db05-0853 · Cited by 86 · see citing works
Self-citationMethTools--a toolbox to visualize and analyze DNA methylation data
Grunau, C. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.5.1053 · Cited by 68 · see citing works
The respiratory quotient as a prognostic factor in weight-loss rebound
Valtueña, S., Salas‐Salvadó, J., & García‐Lorda, P. (1997) · International Journal of Obesity · doi:10.1038/sj.ijo.0800480 · Cited by 62 · see citing works
Identification and characterization of an alternative promoter of the human PGC-1α gene
Yoshioka, T., Inagaki, K., Noguchi, T., Sakai, M., Ogawa, W., Hosooka, T., Iguchi, H., Watanabe, E., Matsuki, Y., Hiramatsu, R., et al. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.02.077 · Cited by 57 · see citing works
Staiger, H., Stefan, N., Machicao, F. E., Fritsche, A., & Häring, H. (2005) · Diabetologia · doi:10.1007/s00125-005-0061-y · Cited by 23 · see citing works
Methylation of newly synthesized and older deoxyribonucleic acid
Adams, R. L. P. (1971) · Biochemical Journal · doi:10.1042/bj1230038pa · Cited by 5 · see citing works
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Regulation of pgc-1α, a nodal regulator of mitochondrial biogenesis
Fernandez-Marcos, P. J., & Auwerx, J. (2011) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.001917 · Cited by 1,237 · see citing works
Sex differences in human adipose tissues – the biology of pear shape
Karastergiou, K., Smith, S. R., Greenberg, A. S., & Fried, S. K. (2012) · Biology of Sex Differences · doi:10.1186/2042-6410-3-13 · Cited by 1,109 · 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
“Evidence is emerging that epigenetic modifications through DNA methylation contribute to the increased risk and development of metabolic disease by modifying the expression of genes controlling whole body energy and glucose homeostasis (Barrès et al., 2009; Klose and Bird, 2006).”
BackgroundInfluentialSelf-citationEpigenetics in Human Obesity and Type 2 Diabetes
Ling, C., & Rönn, T. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.03.009 · Cited by 965 · see citing works
Human body epigenome maps reveal noncanonical DNA methylation variation
Schultz, M. D., He, Y., Whitaker, J. W., Hariharan, M., Mukamel, E. A., Leung, D., Rajagopal, N., Nery, J. R., Urich, M. A., Chen, H., et al. (2015) · Nature · doi:10.1038/nature14465 · Cited by 690 · see citing works
PGC-1 α , Inflammation, and Oxidative Stress: An Integrative View in Metabolism
Rius‐Pérez, S., Torres-Cuevas, I., Millán, I., Ortega, Á., & Pérez, S. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/1452696 · Cited by 648 · see citing works
Rönn, T., Volkov, P., Davegårdh, C., Dayeh, T., Hall, E., Olsson, A. H., Nilsson, E., Tornberg, Å. B., Nitert, M. D., Eriksson, K., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003572 · Cited by 619 · see citing works
Metabolomics reveals signature of mitochondrial dysfunction in diabetic kidney disease
Sharma, K., Karl, B., Mathew, A. V., Gangoiti, J. A., Wassel, C. L., Saito, R., Pu, M., Sharma, S., You, Y.-H., Wang, L., et al. (2013) · Journal of the American Society of Nephrology · doi:10.1681/asn.2013020126 · Cited by 571 · see citing works
Shock, L. S., Thakkar, P. V., Peterson, E. J., Moran, R. G., & Taylor, S. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012311108 · Cited by 555 · see citing works
PGC-1α Is a Master Regulator of Mitochondrial Lifecycle and ROS Stress Response
Abu Shelbayeh, O., Arroum, T., Morris, S., & Busch, K. B. (2023) · Antioxidants · doi:10.3390/antiox12051075 · Cited by 552 · see citing works
The role of mitochondria in the pathogenesis of type 2 diabetes
Patti, M.-E., & Corvera, S. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0027 · Cited by 551 · see citing works
Epigenetic regulation in metabolic diseases: mechanisms and advances in clinical study
Wu, Y., Lin, Z., Li, C., Lin, X. J., Shan, S., Guo, B., Zheng, M.-H., Li, F., Yuan, L., & Li, Z. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01333-7 · Cited by 507 · see citing works
De novo DNA methylation: a germ cell perspective
Smallwood, S. A., & Kelsey, G. (2012) · Trends in Genetics · doi:10.1016/j.tig.2011.09.004 · Cited by 448 · see citing works
The pivotal role of pyruvate dehydrogenase kinases in metabolic flexibility
Zhang, S., Hulver, M. W., McMillan, R. P., Cline, M. A., & Gilbert, E. R. (2014) · Nutrition & Metabolism · doi:10.1186/1743-7075-11-10 · Cited by 450 · see citing works
CpG and non-CpG methylation in epigenetic gene regulation and brain function
Jang, H., Shin, W., Lee, J., & Do, J. (2017) · Genes · doi:10.3390/genes8060148 · Cited by 427 · 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
Villena, J. A. (2014) · FEBS Journal · doi:10.1111/febs.13175 · Cited by 404 · 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
Clare, C., Brassington, A. H., Kwong, W. Y., & Sinclair, K. D. (2018) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-020518-115206 · Cited by 399 · see citing works
Nilsson, E., Jansson, P. A., Perfilyev, A., Volkov, P., Pedersen, M., Svensson, M. K. E., Poulsen, P., Ribel‐Madsen, R., Pedersen, N. L., Almgren, P., et al. (2014) · Diabetes · doi:10.2337/db13-1459 · Cited by 393 · see citing works
Mitochondria and Epigenetics – Crosstalk in Homeostasis and Stress
Matilainen, O., Quirós, P. M., & Auwerx, J. H. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.02.004 · Cited by 368 · see citing works
Human skeletal muscle possesses an epigenetic memory of hypertrophy
Seaborne, R. A., Strauss, J., Cocks, M., Shepherd, S., O’Brien, T. D., van Someren, K. A., Bell, P. G., Murgatroyd, C., Morton, J. P., Stewart, C. E., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-20287-3 · Cited by 334 · see citing works
Sperm epigenetics and influence of environmental factors
Donkin, I., & Barrès, R. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.02.006 · Cited by 331 · see citing works
Self-citationDNA Methylation Biomarkers in Aging and Age-Related Diseases
Salameh, Y., Bejaoui, Y., & Hajj, N. E. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00171 · Cited by 314 · see citing works
Keating, S. T., & El‐Osta, A. (2015) · Circulation Research · doi:10.1161/circresaha.116.303936 · Cited by 315 · see citing works
Dietary factors, epigenetic modifications and obesity outcomes: Progresses and perspectives
Milagro, F. I., Mansego, M. L., de Miguel, C., & Martínez, J. A. (2012) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2012.06.010 · Cited by 310 · see citing works
Yang, B. T., Dayeh, T. A., Volkov, P. A., Kirkpatrick, C. L., Malmgren, S., Jing, X., Renström, E., Wollheim, C. B., Nitert, M. D., & Ling, C. (2012) · Molecular Endocrinology · doi:10.1210/me.2012-1004 · Cited by 301 · see citing works
The role of epigenetics in the pathology of diabetic complications
Villeneuve, L. M., & Natarajan, R. D. (2010) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00200.2010 · Cited by 295 · see citing works
Parkinson's disease, insulin resistance and novel agents of neuroprotection
Avilés-Olmos, I., Limousin, P. D., Lees, A. J., & Foltynie, T. (2012) · Brain · doi:10.1093/brain/aws009 · Cited by 284 · see citing works
Weight Loss after Gastric Bypass Surgery in Human Obesity Remodels Promoter Methylation
Barrès, R., Kirchner, H., Rasmussen, M., Yan, J., Kantor, F. R., Krook, A., Näslund, E. B., & Zierath, J. R. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.03.018 · Cited by 281 · see citing works
Self-citationDistinct Epigenomic Features in End-Stage Failing Human Hearts
Movassagh, M., Choy, M., Knowles, D. A., Cordeddu, L., Haider, S. A., Down, T. A., Siggens, L., Vujić, A., Simeoni, I., Penkett, C., et al. (2011) · Circulation · doi:10.1161/circulationaha.111.040071 · Cited by 281 · see citing works
Molecular mechanisms for mitochondrial adaptation to exercise training in skeletal muscle
Drake, J. C., Wilson, R. J., & Yan, Z. (2016) · The FASEB Journal · doi:10.1096/fj.15-276337 · Cited by 263 · see citing works
Non-CG Methylation in the Human Genome
He, Y., & Ecker, J. R. (2015) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-090413-025437 · Cited by 263 · see citing works
The Control Region of Mitochondrial DNA Shows an Unusual CpG and Non-CpG Methylation Pattern
Bellizzi, D., D’Aquila, P., Scafone, T., Giordano, M., Riso, V., Riccio, A., & Passarino, G. (2013) · DNA Research · doi:10.1093/dnares/dst029 · Cited by 267 · see citing works
Parkin loss leads to PARIS-dependent declines in mitochondrial mass and respiration
Stevens, D. A., Lee, Y., Kang, H. C., Lee, B. D., Lee, Y.-I., Bower, A., Jiang, H., Kang, S.-U., Andrabi, S. A., Dawson, V. L., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1500624112 · Cited by 257 · see citing works
Regulation of mitochondrial biogenesis and PGC-1α under cellular stress
Wenz, T. (2013) · Mitochondrion · doi:10.1016/j.mito.2013.01.006 · Cited by 259 · see citing works
Yang, B. T., Dayeh, T. A., Kirkpatrick, C. L., Taneera, J., Kumar, R., Groop, L., Wollheim, C. B., Nitert, M. D., & Ling, C. (2011) · Diabetologia · doi:10.1007/s00125-010-1967-6 · Cited by 251 · see citing works
H19 lncRNA alters DNA methylation genome wide by regulating S-adenosylhomocysteine hydrolase
Zhou, J., Yang, L., Zhong, T., Mueller, M., Men, Y., Zhang, N., Xie, J., Giang, K., Chung, H., Sun, X., et al. (2015) · Nature Communications · doi:10.1038/ncomms10221 · Cited by 254 · see citing works
Alibegovic, A. C., Sonne, M. P., Højbjerre, L., Bork-Jensen, J., Jacobsen, S., Nilsson, E., Færch, K., Hiscock, N., Mortensen, B., Friedrichsen, M., et al. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00590.2009 · Cited by 247 · see citing works
PGC-1α-mediated adaptations in skeletal muscle
Olesen, J., Kiilerich, K., & Pilegaard, H. (2010) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-010-0834-0 · Cited by 244 · see citing works
Metabolic rearrangements in primary liver cancers: cause and consequences
Satriano, L., Lewińska, M., Rodrigues, P. M., Bañales, J. M., & Andersen, J. B. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0217-8 · Cited by 241 · see citing works
Epigenetic Mechanisms of Transmission of Metabolic Disease across Generations
Sales, V., Ferguson‐Smith, A. C., & Patti, M. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.02.016 · Cited by 242 · see citing works
Obesity-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
Laker, R., Lillard, T. S., Okutsu, M., Zhang, M., Hoehn, K. L., Connelly, J., & Yan, Z. (2014) · Diabetes · doi:10.2337/db13-1614 · Cited by 205 · see citing works
Movassagh, M., Choy, M., Goddard, M. J., Bennett, M. R., Down, T. A., & Foo, R. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008564 · Cited by 224 · see citing works
Recent progress in genetic and epigenetic research on type 2 diabetes
Kwak, S. H., & Park, K. S. (2016) · Experimental & Molecular Medicine · doi:10.1038/emm.2016.7 · Cited by 225 · see citing works
Picard, M., Hepple, R. T., & Burelle, Y. (2012) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00368.2011 · Cited by 214 · see citing works
Jacobsen, S., Brøns, C., Bork-Jensen, J., Ribel-Madsen, R., Yang, B., Lara, E., Hall, E., Calvanese, V., Nilsson, E., Jørgensen, S. W., et al. (2012) · Diabetologia · doi:10.1007/s00125-012-2717-8 · Cited by 197 · see citing works
The evidence for functional non-CpG methylation in mammalian cells
Patil, V., Ward, R. L., & Hesson, L. B. (2014) · Epigenetics · doi:10.4161/epi.28741 · Cited by 203 · see citing works
Ribel‐Madsen, R., Fraga, M. F., Jacobsen, S. B., Bork‐Jensen, J., Lara, E., Calvanese, V., Fernández, A. F., Friedrichsen, M. H., Vind, B. F., Højlund, K., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051302 · Cited by 200 · see citing works
Epigenetic mechanisms in diabetic vascular complications
Reddy, M. A., & Natarajan, R. D. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvr024 · Cited by 198 · see citing works
Gao, L., Emperle, M., Guo, Y., Grimm, S. A., Ren, W., Adam, S., Uryu, H., Zhang, Z., Chen, D., Yin, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17109-4 · Cited by 198 · 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
Self-citationDefining the underlying defect in insulin action in type 2 diabetes
Batista, T. M., Haider, N., & Kahn, C. R. (2021) · Diabetologia · doi:10.1007/s00125-021-05415-5 · Cited by 204 · see citing works
DNA methylation in the pathogenesis of type 2 diabetes in humans
Davegårdh, C., García-Calzón, S., Bacos, K., & Ling, C. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.01.022 · 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
Potential in vivo roles of nucleic acid triple-helices
Buske, F. A., Mattick, J. S., & Bailey, T. L. (2011) · RNA Biology · doi:10.4161/rna.8.3.14999 · Cited by 192 · see citing works
Brøns, C., Jacobsen, S. B., Nilsson, E., Rönn, T., Jensen, C. B., Storgaard, H., Poulsen, P., Groop, L., Ling, C., Astrup, A. V., et al. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2413 · Cited by 193 · see citing works
PPAR control: it's SIRTainly as easy as PGC
Sugden, M. C., Caton, P., & Holness, M. J. (2009) · Journal of Endocrinology · doi:10.1677/joe-09-0359 · Cited by 189 · see citing works
Kelly, R. D., Mahmud, A., McKenzie, M., Trounce, I. A., & John, J. C. S. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks770 · Cited by 193 · see citing works
Nilsson, E., Matte, A., Perfilyev, A., de Mello, V. D., Käkelä, P., Pihlajamäki, J., & Ling, C. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-3204 · Cited by 194 · see citing works
Hernández-Alvarez, M. I., Thabit, H., Burns, N., Shah, S., Brema, I., Hatunic, M., Finucane, F., Liesa, M., Chiellini, C., Naon, D., et al. (2010) · Diabetes Care · doi:10.2337/dc09-1305 · Cited by 189 · see citing works
Yang, X., Luo, C., Cai, J., Powell, D. W., Yu, D., Kuehn, M. H., & Tezel, G. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.11-8152 · Cited by 183 · see citing works
Sharples, A. P., Stewart, C. E., & Seaborne, R. A. (2016) · Aging Cell · doi:10.1111/acel.12486 · Cited by 180 · see citing works
Global DNA Methylation Is Associated With Insulin Resistance
Zhao, J., Goldberg, J. H., Bremner, J. D., & Vaccarino, V. (2011) · Diabetes · doi:10.2337/db11-1048 · Cited by 175 · see citing works
DNA methylation in metabolic disorders
Barres, R., & Zierath, J. R. (2011) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.001933 · Cited by 174 · see citing works
Self-citationHenagan, T. M., Stefañska, B., Fang, Z., Navard, A. M., Ye, J., Lenard, N. R., & Devarshi, P. P. (2015) · British Journal of Pharmacology · doi:10.1111/bph.13058 · Cited by 172 · see citing works
Keil, K. P., & Lein, P. J. (2016) · Environmental Epigenetics · doi:10.1093/eep/dvv012 · Cited by 167 · see citing works
How epigenetics impacts on human diseases
Farsetti, A., Illi, B., & Gaetano, C. (2023) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2023.05.036 · Cited by 166 · see citing works
Metabolic memory: mechanisms and diseases
Dong, H., Sun, Y., Nie, L., Cui, A., Zhao, P., Leung, W. K., & Wang, Q. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01755-x · Cited by 181 · see citing works
Evidence Suggesting Absence of Mitochondrial DNA Methylation
Mechta, M., Ingerslev, L. R., Fabre, O., Picard, M., & Barrès, R. (2017) · Frontiers in Genetics · doi:10.3389/fgene.2017.00166 · Cited by 157 · see citing works
Self-citationPhysiological functions of peroxisome proliferator-activated receptor β
Neels, J. G., & Grimaldi, P. A. (2014) · Physiological Reviews · doi:10.1152/physrev.00027.2013 · Cited by 161 · see citing works
Novel targets of antifibrotic and anti-inflammatory treatment in CKD
Declèves, A., & Sharma, K. (2014) · Nature Reviews Nephrology · doi:10.1038/nrneph.2014.31 · Cited by 155 · see citing works
Developmental programming and epigenetics
Gabory, A., Attig, L., & Junien, C. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.000927 · Cited by 154 · see citing works
DNA methylation and its role in the pathogenesis of diabetes
Bansal, A., & Pinney, S. E. (2017) · Pediatric Diabetes · doi:10.1111/pedi.12521 · Cited by 156 · see citing works
Florath, I., Butterbach, K., Heiss, J. A., Bewerunge‐Hudler, M., Zhang, Y., Schöttker, B., & Brenner, H. (2015) · Diabetologia · doi:10.1007/s00125-015-3773-7 · Cited by 145 · see citing works
Mitochondrial regulation of epigenetics and its role in human diseases
Minocherhomji, S., Tollefsbol, T. O., & Singh, K. K. (2012) · Epigenetics · doi:10.4161/epi.19547 · Cited by 149 · see citing works
Human mitochondrial DNA is extensively methylated in a non-CpG context
Patil, V., Cuenin, C., Chung, F. F., Rodríguez‐Aguilera, J. R., Fernández‐Jiménez, N., Garmendia, I. R., Bilbao, J. R., Cahais, V., Rothwell, J. A., & Herceg, Z. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz762 · Cited by 151 · see citing works
Mitochondria and PGC-1α in Aging and Age-Associated Diseases
Wenz, T. (2011) · Journal of Aging Research · doi:10.4061/2011/810619 · Cited by 149 · see citing works
Epigenetic associations of type 2 diabetes and BMI in an Arab population
Al‐Muftah, W., Al-Shafai, M. N., Zaghlool, S. B., Visconti, A., Tsai, P.-C., Kumar, P., Spector, T. D., Bell, J. T., Falchi, M., & Suhre, K. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0177-6 · Cited by 144 · see citing works
Epigenetic flexibility in metabolic regulation: disease cause and prevention
Kirchner, H., Osler, M. E., Krook, A., & Zierath, J. R. (2013) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.11.008 · Cited by 143 · see citing works
Self-citationRole of Epigenetics in Inflammation-Associated diseases
Shanmugam, M. K., & Sethi, G. (2013) · Subcellular Biochemistry · doi:10.1007/978-94-007-4525-4_27 · Cited by 141 · see citing works
Hall, E., Volkov, P., Dayeh, T., Bacos, K., Rönn, T., Nitert, M. D., & Ling, C. (2014) · BMC Medicine · doi:10.1186/1741-7015-12-103 · Cited by 139 · see citing works
Rowlands, D., Page, R., Sukala, W., Giri, M., Ghimbovschi, S., Hayat, I., Cheema, B., Lys, I., Leikis, M., Sheard, P., et al. (2014) · Physiological Genomics · doi:10.1152/physiolgenomics.00024.2014 · Cited by 120 · see citing works
Nature or nurture: Let food be your epigenetic medicine in chronic inflammatory disorders
Szic, K. S. V., Ndlovu, ’. N., Haegeman, G., & Berghe, W. V. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.07.029 · Cited by 138 · see citing works
Kirchner, 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
Self-citationMinireview: Epigenetics of Obesity and Diabetes in Humans
Slomko, H., Heo, H. J., & Einstein, F. H. (2012) · Endocrinology · doi:10.1210/en.2011-1759 · Cited by 134 · see citing works
Epigenetics and Cardiovascular Disease
Webster, A., Yan, M. S.-C., & Marsden, P. A. (2012) · Canadian Journal of Cardiology · doi:10.1016/j.cjca.2012.10.023 · Cited by 133 · see citing works
Epigenetic regulation on gene expression induced by physical exercise.
Ntanasis‐Stathopoulos, I., Tzanninis, J. G., Philippou, Α., & Koutsilieris, M. (2013) · PubMed · Cited by 132 · see citing works
Genetic and epigenetic control of metabolic health
Schwenk, R. W., Vogel, H., & Schürmann, A. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.09.002 · Cited by 132 · see citing works
Ringholm, S., Biensø, R. S., Kiilerich, K., Guadalupe‐Grau, A., Aachmann‐Andersen, N. J., Saltin, B., Plomgaard, P., Lundby, C., Wojtaszewski, J. F. P., Calbet, J. A. L., et al. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00230.2011 · Cited by 130 · see citing works
Mitochondrial metabolism and DNA methylation: a review of the interaction between two genomes
Lopes, A. F. C. (2020) · Clinical Epigenetics · doi:10.1186/s13148-020-00976-5 · Cited by 127 · see citing works
Dnmt3a is an epigenetic mediator of adipose insulin resistance
You, D., Nilsson, E., Tenen, D. E., Lyubetskaya, A., Lo, J. C., Jiang, R., Deng, J., Dawes, B. A., Vaag, A. A., Ling, C., et al. (2017) · eLife · doi:10.7554/elife.30766 · Cited by 124 · see citing works
Obesity, oxidative stress, and fibrosis in chronic kidney disease
Sharma, K. (2014) · Kidney International Supplements · doi:10.1038/kisup.2014.21 · Cited by 125 · see citing works
Epigenetics of type 2 diabetes mellitus and weight change — a tool for precision medicine?
Ling, C., Bacos, K., & Rönn, T. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00671-w · Cited by 130 · see citing works
Ronald, C. W., Tutino, G., Lillycrop, K. A., Hanson, M. A., & Tam, W. H. (2015) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2015.02.010 · Cited by 125 · see citing works
Volkov, P., Olsson, A. H., Gillberg, L., Jørgensen, S. W., Brøns, C., Eriksson, K., Groop, L., Jansson, P., Nilsson, E., Rönn, T., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157776 · Cited by 121 · see citing works
Bravard, A., Lefai, É., Meugnier, E., Pesenti, S., Disse, E., Vouillarmet, J., Peretti, N., RABASA-LHORET, R. P. R., Laville, M., Vidal, H., et al. (2010) · Diabetes · doi:10.2337/db10-0281 · Cited by 124 · see citing works
Radiation-induced epigenetic alterations after low and high LET irradiations
Aypar, U., Morgan, W. F., & Baulch, J. E. (2010) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2010.12.003 · Cited by 123 · see citing works
Epigenetic Mechanisms Underlying the Link between Non-Alcoholic Fatty Liver Diseases and Nutrition
Lee, J. Y., Friso, S., & Choi, S. (2014) · Nutrients · doi:10.3390/nu6083303 · Cited by 121 · see citing works
- Authors
- Barrès, R., Osler, M. E., Yan, J., Rune, A., Fritz, T., Caidahl, K., Krook, A., & Zierath, J. R.
- Affiliations
- Karolinska University Hospital (SE)
- Corresponding author
- Zierath, Juleen R.
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2009-09
- Volume
- 10
- Issue
- 3
- Pages
- 189-198
- ISSN
- 1550-4131 (ISSN-L)
- OpenAlex
- W1985280131
- Semantic Scholar
- 4a04e95dbe0297f0a51059b2ab7890362fad1e57
- Cited by
- 602
- References
- 44
- Citations by year
- 2026: 26 · 2025: 16 · 2024: 27 · 2023: 24 · 2022: 26 · 2021: 37 · 2020: 24 · 2019: 35 · 2018: 36 · 2017: 41 · 2016: 50 · 2015: 57 · 2014: 49 · 2013: 43 · 2012: 39
- FWCI
- 14.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1451 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- Novo Nordisk UK Research Foundation
- Vetenskapsrådet
- European Commission (LSHM-CT-2004-005272, LSHM-CT-2004-512013 EUGENE2)
- European Research Council
- European Foundation for the Study of Diabetes
- Knut och Alice Wallenbergs Stiftelse
- Glenn Foundation for Medical Research
- Stockholms Läns Landsting
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- PGC-1α, DNMT3B, promoter methylation, mitochondrial density, type 2 diabetes, skeletal muscle, mitochondrial DNA, free fatty acids, palmitate, TNF-α, myotubes, DNA methyltransferases, epigenetic regulation
- MeSH terms
- Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, DNA Methyltransferase 3B, Base Sequence, Diabetes Mellitus, Type 2, DNA (Cytosine-5-)-Methyltransferases, DNA, Mitochondrial, Fatty Acids, Heat-Shock Proteins, Humans, Mitochondria, Promoter Regions, Genetic, RNA, Messenger, Transcription Factors, Tumor Necrosis Factor-alpha, CpG Islands, DNA Methylation, Muscle Cells, RNA, Small Interfering
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