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Current Genomics

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ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

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Review Article

Epigenetic Programming of Adipose Tissue in the Progeny of Obese Dams

Author(s): Simon Lecoutre, Kelvin H.M. Kwok, Paul Petrus, Mélanie Lambert and Christophe Breton*

Volume 20, Issue 6, 2019

Page: [428 - 437] Pages: 10

DOI: 10.2174/1389202920666191118092852

Price: $65

Abstract

According to the Developmental Origin of Health and Disease (DOHaD) concept, maternal obesity and the resulting accelerated growth in neonates predispose offspring to obesity and associated metabolic diseases that may persist across generations. In this context, the adipose tissue has emerged as an important player due to its involvement in metabolic health, and its high potential for plasticity and adaptation to environmental cues. Recent years have seen a growing interest in how maternal obesity induces long-lasting adipose tissue remodeling in offspring and how these modifications could be transmitted to subsequent generations in an inter- or transgenerational manner. In particular, epigenetic mechanisms are thought to be key players in the developmental programming of adipose tissue, which may partially mediate parts of the transgenerational inheritance of obesity. This review presents data supporting the role of maternal obesity in the developmental programming of adipose tissue through epigenetic mechanisms. Inter- and transgenerational effects on adipose tissue expansion are also discussed in this review.

Keywords: Perinatal period, maternal obesity, developmental origin of health and disease, epigenome, gene expression, fat expansion.

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[1]
González-Muniesa, P.; Mártinez-González, M-A.; Hu, F.B.; Després, J-P.; Matsuzawa, Y.; Loos, R.J.F.; Moreno, L.A.; Bray, G.A.; Martinez, J.A. Obesity. Nat. Rev. Dis. Primers, 2017, 3, 17034.
[http://dx.doi.org/10.1038/nrdp.2017.34]
[2]
WHO 2018 Obesity and overweight. Available online at:. http://www.who.int/news-room/factsheets/detail/obesity-and-overweight
[3]
Hanson, M.A. Developmental origins of obesity and non-communicable disease. Endocrinol. Nutr., 2013, 60(Suppl. 1), 10-11.
[http://dx.doi.org/10.1016/S1575-0922(13)70017-2]
[4]
Maher, B. Personal genomes: The case of the missing heritability. Nature, 2008, 456, 18-21.
[http://dx.doi.org/10.1038/456018a]
[5]
Lecoutre, S.; Petrus, P.; Rydén, M.; Breton, C. Transgenerational epigenetic mechanisms in adipose tissue development. Trends Endocrinol. Metab., 2018, 29, 675-685.
[http://dx.doi.org/10.1016/j.tem.2018.07.004]
[6]
Barker, D.J.P. Developmental origins of adult health and disease. J. Epidemiol. Community Health, 2004, 58, 114-115.
[http://dx.doi.org/10.1136/jech.58.2.114]
[7]
Lumey, L.H.; Stein, A.D.; Susser, E. Prenatal famine and adult health. Annu. Rev. Public Health, 2011, 32, 237-262.
[http://dx.doi.org/10.1146/annurev-publhealth-031210-101230]
[8]
Parlee, S.D.; MacDougald, O. Maternal nutrition and risk of obesity in offspring: The Trojan horse of developmental plasticity. Biochim. Biophys. Acta, 2014, 1842, 495-506.
[http://dx.doi.org/10.1016/j.bbadis.2013.07.007]
[9]
Yu, Z.; Han, S.; Zhu, J.; Sun, X.; Ji, C.; Guo, X. Pre-pregnancy body mass index in relation to infant birth weight and offspring overweight/obesity: A systematic review and meta-analysis. PLoS One, 2013. 8e61627
[http://dx.doi.org/10.1371/journal.pone.0061627]
[10]
Gaudet, L.; Ferraro, Z.M.; Wen, S.W.; Walker, M. Maternal obesity and occurrence of fetal macrosomia: A systematic review and meta-analysis. BioMed Res. Int., 2014, 2014, 1-22.
[http://dx.doi.org/10.1155/2014/640291]
[11]
Cedergren, M.I. Maternal morbid obesity and the risk of adverse pregnancy outcome. Obstet. Gynecol., 2004, 103, 219-224.
[http://dx.doi.org/10.1097/01.AOG.0000107291.46159.00]
[12]
Boney, C.M.; Verma, A.; Tucker, R.; Vohr, B.R. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics, 2005, 115, e290-e296.
[http://dx.doi.org/10.1542/peds.2004-1808]
[13]
Whitaker, R.C. Predicting preschooler obesity at birth: The role of maternal obesity in early pregnancy. Pediatrics, 2004, 114, e29-e36.
[http://dx.doi.org/10.1542/peds.114.1.e29]
[14]
Brisbois, T.D.; Farmer, A.P.; McCargar, L.J. Early markers of adult obesity: A review. Obes. Rev., 2012, 13, 347-367.
[http://dx.doi.org/10.1111/j.1467-789X.2011.00965.x]
[15]
Cooper, R.; Hyppönen, E.; Berry, D.; Power, C. Associations between parental and offspring adiposity up to midlife: The contribution of adult lifestyle factors in the 1958 British Birth Cohort Study. Am. J. Clin. Nutr., 2010, 92, 946-953.
[http://dx.doi.org/10.3945/ajcn.2010.29477]
[16]
Guenard, F.; Deshaies, Y.; Cianflone, K.; Kral, J.G.; Marceau, P.; Vohl, M-C. Differential methylation in glucoregulatory genes of offspring born before vs. after maternal gastrointestinal bypass surgery. Proc. Natl. Acad. Sci. USA, 2013, 110, 11439-11444.
[http://dx.doi.org/10.1073/pnas.1216959110]
[17]
Desai, M.; Jellyman, J.K.; Ross, M.G. Epigenomics, gestational programming and risk of metabolic syndrome. Int. J. Obes., 2015, 39, 633-641.
[http://dx.doi.org/10.1038/ijo.2015.13]
[18]
Bird, A. Perceptions of epigenetics. Nature, 2007, 447, 396-398.
[http://dx.doi.org/10.1038/nature05913]
[19]
Skvortsova, K.; Iovino, N.; Bogdanović, O. Functions and mechanisms of epigenetic inheritance in animals. Nat. Rev. Mol. Cell Biol., 2018, 19, 774-790.
[http://dx.doi.org/10.1038/s41580-018-0074-2]
[20]
Mikkelsen, T.S.; Xu, Z.; Zhang, X.; Wang, L.; Gimble, J.M.; Lander, E.S.; Rosen, E.D. Comparative epigenomic analysis of murine and human adipogenesis. Cell, 2010, 143, 156-169.
[http://dx.doi.org/10.1016/j.cell.2010.09.006]
[21]
Lu, C.; Thompson, C.B. Metabolic regulation of epigenetics. Cell Metab., 2012, 16, 9-17.
[http://dx.doi.org/10.1016/j.cmet.2012.06.001]
[22]
Berger, S.L.; Sassone-Corsi, P. Metabolic signaling to chromatin. Cold Spring Harb. Perspect. Biol., 2016, 8a019463
[http://dx.doi.org/10.1101/cshperspect.a019463]
[23]
Indrio, F.; Martini, S.; Francavilla, R.; Corvaglia, L.; Cristofori, F.; Mastrolia, S.A.; Neu, J.; Rautava, S.; Russo Spena, G.; Raimondi, F. Epigenetic matters: The link between early nutrition, microbiome, and long-term health development. Front Pediatr., 2017, 5, 178.
[http://dx.doi.org/10.3389/fped.2017.00178]
[24]
Lee, H-S. Impact of maternal diet on the epigenome during in utero life and the developmental programming of diseases in childhood and adulthood. Nutrients, 2015, 7, 9492-9507.
[http://dx.doi.org/10.3390/nu7115467]
[25]
Lecoutre, S.; Breton, C. The cellularity of offspring’s adipose tissue is programmed by maternal nutritional manipulations. Adipocyte, 2014, 3, 256-262.
[http://dx.doi.org/10.4161/adip.29806]
[26]
Lecoutre, S.; Breton, C. Maternal nutritional manipulations program adipose tissue dysfunction in offspring. Front. Physiol., 2015, 6, 158.
[http://dx.doi.org/10.3389/fphys.2015.00158]
[27]
Berry, D.C.; Jiang, Y.; Graff, J.M. Emerging roles of adipose progenitor cells in tissue development, homeostasis, expansion and thermogenesis. Trends Endocrinol. Metab., 2016, 27, 574-585.
[http://dx.doi.org/10.1016/j.tem.2016.05.001]
[28]
Poissonnet, C.M.; Burdi, A.R.; Bookstein, F.L. Growth and development of human adipose tissue during early gestation. Early Hum. Dev., 1983, 8, 1-11.
[http://dx.doi.org/10.1016/0378-3782(83)90028-2]
[29]
Poissonnet, C.M.; Burdi, A.R.; Garn, S.M. The chronology of adipose tissue appearance and distribution in the human fetus. Early Hum. Dev., 1984, 10, 1-11.
[http://dx.doi.org/10.1016/0378-3782(84)90106-3]
[30]
Knittle, J.L.; Timmers, K.; Ginsberg-Fellner, F.; Brown, R.E.; Katz, D. The growth of adipose tissue in children and adolescents. Cross-sectional and longitudinal studies of adipose cell number and size. J. Clin. Invest., 1979, 63, 239-246.
[http://dx.doi.org/10.1172/JCI109295]
[31]
Spalding, K.L.; Arner, E.; Westermark, P.O.; Bernard, S.; Buchholz, B. Dynamics of fat cell turnover in humans. Nature, 2008, 453, 783-787.
[http://dx.doi.org/10.1038/nature06902]
[32]
Du, M.; Yin, J.; Zhu, M.J. Cellular signaling pathways regulating the initial stage of adipogenesis and marbling of skeletal muscle. Meat Sci., 2010, 86, 103-109.
[http://dx.doi.org/10.1016/j.meatsci.2010.04.027]
[33]
Björntorp, P. Number and size of adipose tissue fat cells in relation to metabolism in human obesity. Metabolism, 1971, 20, 703-713.
[http://dx.doi.org/10.1016/0026-0495(71)90084-9]
[34]
Salans, L.B.; Cushman, S.W.; Weismann, R.E. Studies of human adipose tissue adipose cell size and number in non-obese and obese patients. J. Clin. Invest., 1973, 52, 929-941.
[http://dx.doi.org/10.1172/JCI107258]
[35]
Tchoukalova, Y.D.; Votruba, S.B.; Tchkonia, T.; Giorgadze, N.; Kirkland, J.L.; Jensen, M.D. Regional differences in cellular mechanisms of adipose tissue gain with overfeeding. Proc. Natl. Acad. Sci. USA, 2010, 107, 18226-18231.
[http://dx.doi.org/10.1073/pnas.1005259107]
[36]
van Harmelen, V.; Röhrig, K.; Hauner, H. Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from the omental and subcutaneous adipose tissue depot of obese subjects. Metabolism, 2004, 53, 632-637.
[http://dx.doi.org/10.1016/j.metabol.2003.11.012]
[37]
Hepler, C.; Vishvanath, L.; Gupta, R.K. Sorting out adipocyte precursors and their role in physiology and disease. Genes Dev., 2017, 31, 127-140.
[http://dx.doi.org/10.1101/gad.293704.116]
[38]
Chau, Y.; Bandiera, R.; Serrels, A.; Martínez-estrada, O.M.; Qing, W.; Lee, M.; Slight, J.; Thornburn, A.; Berry, R.; Mchaffie, S. Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source., 2014, 16
[http://dx.doi.org/10.1038/ncb2922]
[39]
Billon, N.; Dani, C. Developmental origins of the adipocyte lineage: new insights from genetics and genomics studies. Stem Cell Rev., 2012, 8, 55-66.
[http://dx.doi.org/10.1007/s12015-011-9242-x]
[40]
Sanchez-Gurmaches, J.; Hsiao, W-Y.; Guertin, D.A. Highly selective in vivo labeling of subcutaneous white adipocyte precursors with Prx1-Cre. Stem Cell Rep, 2015, 4, 541-550.
[http://dx.doi.org/10.1016/j.stemcr.2015.02.008]
[41]
Sanchez-Gurmaches, J.; Guertin, D.a. Adipocyte lineages: Tracing back the origins of fat. Biochim. Biophys. Acta Mol. Basis Dis., 2014, 1842, 340-351.
[http://dx.doi.org/10.1016/j.bbadis.2013.05.027]
[42]
Rosen, E.D.; Walkey, C.J.; Puigserver, P.; Spiegelman, B.M. Transcriptional regulation of adipogenesis Transcriptional regulation of adipogenesis., 2000, 1293-1307.
[43]
Cristancho, A.G.; Lazar, M.A. Forming functional fat: A growing understanding of adipocyte differentiation. Nat. Rev. Mol. Cell Biol., 2011, 12, 722-734.
[http://dx.doi.org/10.1038/nrm3198]
[44]
Stahl Madsen, M.; Siersbaek, R.; Boergesen, M.; Nielsen, R.; Mandrup, S. Peroxisome Proliferator-Activated Receptor γ and C/EBPα synergistically activate key metabolic adipocyte genes by assisted loading. Mol. Cell. Biol., 2014, 34, 939-954.
[http://dx.doi.org/10.1128/MCB.01344-13]
[45]
Siersbæk, R.; Baek, S.; Rabiee, A.; Nielsen, R.; Traynor, S.; Clark, N.; Sandelin, A.; Jensen, O.N.; Sung, M.H.; Hager, G.L. Molecular architecture of transcription factor hotspots in early adipogenesis. Cell Rep., 2014, 7, 1434-1442.
[http://dx.doi.org/10.1016/j.celrep.2014.04.043]
[46]
Siersbæk, R.; Nielsen, R.; Mandrup, S. Transcriptional networks and chromatin remodeling controlling adipogenesis. Trends Endocrinol. Metab., 2012, 23, 56-64.
[http://dx.doi.org/10.1016/j.tem.2011.10.001]
[47]
Yi, X.; Wu, P.; Liu, J.; Gong, Y.; Xu, X.; Li, W. Identification of the potential key genes for adipogenesis from human mesenchymal stem cells by RNA-Seq. J. Cell. Physiol., 2019, 234, 20217-20227.
[http://dx.doi.org/10.1002/jcp.28621]
[48]
Karahuseyinoglu, S.; Kocaefe, C.; Balci, D.; Erdemli, E.; Can, A. Functional structure of adipocytes differentiated from human umbilical cord stroma-derived stem cells. Stem Cells, 2008, 26, 682-691.
[http://dx.doi.org/10.1634/stemcells.2007-0738]
[49]
Siersbaek, R.; Nielsen, R.; John, S.; Sung, M-H.; Baek, S.; Loft, A.; Hager, G.L.; Mandrup, S. Extensive chromatin remodelling and establishment of transcription factor ‘hotspots’ during early adipogenesis. EMBO J., 2011, 30, 1459-1472.
[http://dx.doi.org/10.1038/emboj.2011.65]
[50]
Matsumura, Y.; Nakaki, R.; Inagaki, T.; Yoshida, A.; Kano, Y.; Kimura, H.; Tanaka, T.; Tsutsumi, S.; Nakao, M.; Doi, T. H3K4/H3K9me3 bivalent chromatin domains targeted by lineage-specific DNA methylation pauses adipocyte differentiation. Mol. Cell, 2015, 60, 584-596.
[http://dx.doi.org/10.1016/j.molcel.2015.10.025]
[51]
Siersbaek, M.S. Loft, a.; Aagaard, M.M.; Nielsen, R.; Schmidt, S.F.; Petrovic, N.; Nedergaard, J.; Mandrup, S. Genome-wide profiling of peroxisome proliferator-activated receptor in primary epididymal, inguinal, and brown adipocytes reveals depot-selective binding correlated with gene expression. Mol. Cell. Biol., 2012, 32, 3452-3463.
[http://dx.doi.org/10.1128/MCB.00526-12]
[52]
Lefterova, M.I.; Steger, D.J.; Zhuo, D.; Qatanani, M.; Mullican, S.E.; Tuteja, G.; Manduchi, E.; Grant, G.R.; Lazar, M. Cell-specific determinants of peroxisome proliferator-activated receptor gamma function in adipocytes and macrophages. Mol. Cell. Biol., 2010, 30, 2078-2089.
[http://dx.doi.org/10.1128/MCB.01651-09]
[53]
Wakabayashi, K.; Okamura, M.; Tsutsumi, S.; Nishikawa, N.S.; Tanaka, T.; Sakakibara, I.; Kitakami, J.; Ihara, S.; Hashimoto, Y.; Hamakubo, T. The peroxisome proliferator-activated receptor gamma/retinoid X receptor alpha heterodimer targets the histone modification enzyme PR-Set7/Setd8 gene and regulates adipogenesis through a positive feedback loop. Mol. Cell. Biol., 2009, 29, 3544-3555.
[http://dx.doi.org/10.1128/MCB.01856-08]
[54]
Lefterova, M.I.; Haakonsson, A.K.; Lazar, M.; Mandrup, S. PPAR gamma and the global map of adipogenesis and beyond. Trends Endocrinol. Metab., 2014, 25, 293-302.
[http://dx.doi.org/10.1016/j.tem.2014.04.001]
[55]
Öst, A.; Pospisilik, J.A. Epigenetic modulation of metabolic decisions. Curr. Opin. Cell Biol., 2015, 33, 88-94.
[http://dx.doi.org/10.1016/j.ceb.2014.12.005]
[56]
Ghaben, A.L.; Scherer, P.E. Adipogenesis and metabolic health. Nat. Rev. Mol. Cell Biol., 2019, 20, 242-258.
[http://dx.doi.org/10.1038/s41580-018-0093-z]
[57]
Reilly, S.M.; Saltiel, A.R. Adapting to obesity with adipose tissue inflammation. Nat. Rev. Endocrinol., 2017, 13, 633-643.
[http://dx.doi.org/10.1038/nrendo.2017.90]
[58]
Muhlhausler, B.; Smith, S.R. Early-life origins of metabolic dysfunction: role of the adipocyte. Trends Endocrinol. Metab., 2009, 20, 51-57.
[http://dx.doi.org/10.1016/j.tem.2008.10.006]
[59]
Yang, Q-Y.; Liang, J-F.; Rogers, C.J.; Zhao, J-X.; Zhu, M-J.; Du, M. Maternal obesity induces epigenetic modifications to facilitate Zfp423 expression and enhance adipogenic differentiation in fetal mice. Diabetes, 2013, 62, 3727-3735.
[http://dx.doi.org/10.2337/db13-0433]
[60]
Liang, X.; Yang, Q.; Fu, X.; Rogers, C.J.; Wang, B.; Pan, H.; Zhu, M-J.; Nathanielsz, P.W.; Du, M. Maternal obesity epigenetically alters visceral fat progenitor cell properties in male offspring mice. J. Physiol., 2016, 594, 4453-4466.
[http://dx.doi.org/10.1113/JP272123]
[61]
Borengasser, S.J.; Zhong, Y.; Kang, P.; Lindsey, F.; Ronis, M.J.J.; Badger, T.M.; Gomez-Acevedo, H.; Shankar, K. Maternal obesity enhances white adipose tissue differentiation and alters genome-scale DNA methylation in male rat offspring. Endocrinology, 2013, 154, 4113-4125.
[http://dx.doi.org/10.1210/en.2012-2255]
[62]
Desai, M.; Jellyman, J.K.; Han, G.; Lane, R.H.; Ross, M.G. Programmed regulation of rat offspring adipogenic transcription factor (PPARγ) by maternal nutrition. J. Dev. Orig. Health Dis., 2015, 6, 530-538.
[http://dx.doi.org/10.1017/S2040174415001440]
[63]
Lecoutre, S.; Pourpe, C.; Butruille, L.; Marousez, L.; Laborie, C.; Guinez, C.; Lesage, J.; Vieau, D.; Eeckhoute, J.; Gabory, A. Reduced PPARγ2 expression in adipose tissue of male rat offspring from obese dams is associated with epigenetic modifications. FASEB J., 2018, 32, 2768-2778.
[http://dx.doi.org/10.1096/fj.201700997R]
[64]
Gupta, R.K.; Arany, Z.; Seale, P.; Mepani, R.J.; Ye, L.; Conroe, H.M.; Roby, Y.A.; Kulaga, H.; Reed, R.R.; Spiegelman, B.M. Transcriptional control of preadipocyte determination by Zfp423. Nature, 2010, 464, 619-623.
[http://dx.doi.org/10.1038/nature08816]
[65]
Hammarstedt, A.; Hedjazifar, S.; Jenndahl, L.; Gogg, S.; Grünberg, J.; Gustafson, B.; Klimcakova, E.; Stich, V.; Langin, D.; Laakso, M. WISP2 regulates preadipocyte commitment and PPARγ activation by BMP4. Proc. Natl. Acad. Sci. USA, 2013, 110, 2563-2568.
[http://dx.doi.org/10.1073/pnas.1211255110]
[66]
Wang, B.; Yang, Q.; Harris, C.L.; Nelson, M.L.; Busboom, J.R.; Zhu, M-J.; Du, M. Nutrigenomic regulation of adipose tissue development - role of retinoic acid: A review. Meat Sci., 2016, 120, 100-106.
[http://dx.doi.org/10.1016/j.meatsci.2016.04.003]
[67]
Fujiki, K.; Kano, F.; Shiota, K.; Murata, M. Expression of the peroxisome proliferator activated receptor gamma gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes. BMC Biol., 2009, 7, 38.
[http://dx.doi.org/10.1186/1741-7007-7-38]
[68]
Zwamborn, R.A.J.; Slieker, R.C.; Mulder, P.C.A.; Zoetemelk, I.; Verschuren, L.; Suchiman, H.E.D.; Toet, K.H.; Droog, S.; Slagboom, P.E.; Kooistra, T. Prolonged high-fat diet induces gradual and fat depot-specific DNA methylation changes in adult mice. Sci. Rep., 2017, 7, 43261.
[http://dx.doi.org/10.1038/srep43261]
[69]
Salma, N.; Xiao, H.; Mueller, E.; Imbalzano, A.N. Temporal recruitment of transcription factors and SWI/SNF chromatin-remodeling enzymes during adipogenic induction of the peroxisome proliferator-activated receptor gamma nuclear hormone receptor. Mol. Cell. Biol., 2004, 24, 4651-4663.
[http://dx.doi.org/10.1128/MCB.24.11.4651-4663.2004]
[70]
Lecoutre, S.; Deracinois, B.; Laborie, C.; Eberlé, D.; Guinez, C.; Panchenko, P.E.; Lesage, J.; Vieau, D.; Junien, C.; Gabory, A. Depot- and sex-specific effects of maternal obesity in offspring’s adipose tissue. J. Endocrinol., 2016, 230, 39-53.
[http://dx.doi.org/10.1530/JOE-16-0037]
[71]
Corrales, P.; Vidal-Puig, A.; Medina-Gómez, G. PPARs and metabolic disorders associated with challenged adipose tissue plasticity. Int. J. Mol. Sci., 2018, 19, 2124.
[http://dx.doi.org/10.3390/ijms19072124]
[72]
Lukaszewski, M-A.; Mayeur, S.; Fajardy, I.; Delahaye, F.; Dutriez-Casteloot, I.; Montel, V.; Dickes-Coopman, A.; Laborie, C.; Lesage, J.; Vieau, D. Maternal prenatal undernutrition programs adipose tissue gene expression in adult male rat offspring under high-fat diet. Am. J. Physiol. Endocrinol. Metab., 2011, 301, E548-E559.
[http://dx.doi.org/10.1152/ajpendo.00011.2011]
[73]
Butruille, L.; Marousez, L.; Pourpe, C.; Oger, F.; Lecoutre, S.; Catheline, D.; Görs, S.; Metges, C.C.; Guinez, C.; Laborie, C. Maternal high-fat diet during suckling programs visceral adiposity and epigenetic regulation of adipose tissue stearoyl-CoA desaturase-1 in offspring. Int. J. Obes., 2019.
[http://dx.doi.org/10.1038/s41366-018-0310-z]
[74]
Fujiki, K.; Shinoda, A.; Kano, F.; Sato, R.; Shirahige, K.; Murata, M. PPARγ-induced PARylation promotes local DNA demethylation by production of 5-hydroxymethylcytosine. Nat. Commun., 2013, 4, 2262.
[http://dx.doi.org/10.1038/ncomms3262]
[75]
Caron, A.; Lee, S.; Elmquist, J.K.; Gautron, L. Leptin and brain-adipose crosstalks. Nat. Rev. Neurosci., 2018, 19, 153-165.
[http://dx.doi.org/10.1038/nrn.2018.7]
[76]
Abella, V.; Scotece, M.; Conde, J.; Pino, J.; Gonzalez-Gay, M.A.; Gómez-Reino, J.J.; Mera, A.; Lago, F.; Gómez, R.; Gualillo, O. Leptin in the interplay of inflammation, metabolism and immune system disorders. Nat. Rev. Rheumatol., 2017, 13, 100-109.
[http://dx.doi.org/10.1038/nrrheum.2016.209]
[77]
Lecoutre, S.; Oger, F.; Pourpe, C.; Butruille, L.; Marousez, L.; Dickes-Coopman, A.; Laborie, C.; Guinez, C.; Lesage, J.; Vieau, D. Maternal obesity programs increased leptin gene expression in rat male offspring via epigenetic modifications in a depot-specific manner. Mol. Metab., 2017, 6, 922-930.
[http://dx.doi.org/10.1016/j.molmet.2017.05.010]
[78]
Masuyama, H.; Mitsui, T.; Nobumoto, E.; Hiramatsu, Y. The effects of high-fat diet exposure in utero on the obesogenic and diabetogenic traits through epigenetic changes in adiponectin and leptin gene expression for multiple generations in female mice. Endocrinology, 2015, 156, 2482-2491.
[http://dx.doi.org/10.1210/en.2014-2020]
[79]
Masuyama, H.; Hiramatsu, Y. Additive effects of maternal high fat diet during lactation on mouse offspring. PLoS One, 2014, 9e92805
[http://dx.doi.org/10.1371/journal.pone.0092805]
[80]
Masuyama, H.; Hiramatsu, Y. Effects of a high-fat diet exposure in utero on the metabolic syndrome-like phenomenon in mouse offspring through epigenetic changes in adipocytokine gene expression. Endocrinology, 2012, 153, 2823-2830.
[http://dx.doi.org/10.1210/en.2011-2161]
[81]
Murabayashi, N.; Sugiyama, T.; Zhang, L.; Kamimoto, Y.; Umekawa, T.; Ma, N.; Sagawa, N. Maternal high-fat diets cause insulin resistance through inflammatory changes in fetal adipose tissue. Eur. J. Obstet. Gynecol. Reprod. Biol., 2013, 169, 39-44.
[http://dx.doi.org/10.1016/j.ejogrb.2013.02.003]
[82]
del Bas, J.M.; Crescenti, A.; Arola-Arnal, A.; Oms-Oliu, G.; Arola, L.; Caimari, A. Grape seed procyanidin supplementation to rats fed a high-fat diet during pregnancy and lactation increases the body fat content and modulates the inflammatory response and the adipose tissue metabolism of the male offspring in youth. Int. J. Obes., 2015, 39, 7-15.
[http://dx.doi.org/10.1038/ijo.2014.159]
[83]
Ding, Y.; Li, J.; Liu, S.; Zhang, L.; Xiao, H.; Chen, H.; Petersen, R.B.; Huang, K.; Zheng, L. DNA hypomethylation of inflammation-associated genes in adipose tissue of female mice after multigenerational high fat diet feeding. Int. J. Obes., 2014, 38, 198-204.
[http://dx.doi.org/10.1038/ijo.2013.98]
[84]
Umekawa, T.; Sugiyama, T.; Du, Q.; Murabayashi, N.; Zhang, L.; Kamimoto, Y.; Yoshida, T.; Sagawa, N.; Ikeda, T. A maternal mouse diet with moderately high-fat levels does not lead to maternal obesity but causes mesenteric adipose tissue dysfunction in male offspring. J. Nutr. Biochem., 2015, 26, 259-266.
[http://dx.doi.org/10.1016/j.jnutbio.2014.10.012]
[85]
Shimobayashi, M.; Albert, V.; Woelnerhanssen, B.; Frei, I.C.; Weissenberger, D.; Meyer-Gerspach, A.C.; Clement, N.; Moes, S.; Colombi, M.; Meier, J.A. Insulin resistance causes inflammation in adipose tissue. J. Clin. Invest., 2018, 128, 1538-1550.
[http://dx.doi.org/10.1172/JCI96139]
[86]
Kammoun, H.L.; Kraakman, M.J.; Febbraio, M.A. Adipose tissue inflammation in glucose metabolism. Rev. Endocr. Metab. Disord., 2014, 15, 31-44.
[http://dx.doi.org/10.1007/s11154-013-9274-4]
[87]
Kraakman, M.J.; Kammoun, H.L.; Allen, T.L.; Deswaerte, V.; Henstridge, D.C.; Estevez, E.; Matthews, V.B.; Neill, B.; White, D.A.; Murphy, A.J. Blocking IL-6 trans-signaling prevents high-fat diet-induced adipose tissue macrophage recruitment but does not improve insulin resistance. Cell Metab., 2015, 21, 403-416.
[http://dx.doi.org/10.1016/j.cmet.2015.02.006]
[88]
Heard, E.; Martienssen, R.A. Transgenerational epigenetic inheritance: Myths and mechanisms. Cell, 2014, 157, 95-109.
[http://dx.doi.org/10.1016/j.cell.2014.02.045]
[89]
Grossniklaus, U.; Kelly, W.G.; Kelly, B.; Ferguson-Smith, A.C.; Pembrey, M.; Lindquist, S. Transgenerational epigenetic inheritance: how important is it? Nat. Rev. Genet., 2013, 14, 228-235.
[http://dx.doi.org/10.1038/nrg3435]
[90]
Sharma, U.; Rando, O.J. Metabolic inputs into the epigenome. Cell Metab., 2017, 25, 544-558.
[http://dx.doi.org/10.1016/j.cmet.2017.02.003]
[91]
Kaati, G.; Bygren, L.O.; Pembrey, M.; Sjöström, M. Transgenerational response to nutrition, early life circumstances and longevity. Eur. J. Hum. Genet., 2007, 15, 784-790.
[http://dx.doi.org/10.1038/sj.ejhg.5201832]
[92]
Davis, M.M.; McGonagle, K.; Schoeni, R.F.; Stafford, F. Grandparental and parental obesity influences on childhood overweight: implications for primary care practice. J. Am. Board Fam. Med., 2008, 21, 549-554.
[http://dx.doi.org/10.3122/jabfm.2008.06.070140]
[93]
Dunn, G.A.; Bale, T.L. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology, 2011, 152, 2228-2236.
[http://dx.doi.org/10.1210/en.2010-1461]
[94]
Sarker, G.; Berrens, R.; von Arx, J.; Pelczar, P.; Reik, W.; Wolfrum, C.; Peleg-Raibstein, D. Transgenerational transmission of hedonic behaviors and metabolic phenotypes induced by maternal overnutrition. Transl. Psychiatry, 2018, 8, 195.
[http://dx.doi.org/10.1038/s41398-018-0243-2]
[95]
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. Metab., 2016, 311, E236-E245.
[http://dx.doi.org/10.1152/ajpendo.00095.2016]
[96]
Fullston, T.; McPherson, N.O.; Owens, J.A.; Kang, W.X.; Sandeman, L.Y.; Lane, M. Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an “obesogenic” diet. Physiol. Rep., 2015.3e12336.
[http://dx.doi.org/10.14814/phy2.12336]
[97]
de Castro Barbosa, T.; Ingerslev, L.R.; Alm, P.S.; Versteyhe, S.; Massart, J.; Rasmussen, M.; Donkin, I.; Sjögren, R.; Mudry, J.M.; Vetterli, L. High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Mol. Metab., 2016, 5, 184-197.
[http://dx.doi.org/10.1016/j.molmet.2015.12.002]
[98]
de Castro Barbosa, T.; Alm, P.S.; Krook, A.; Barrès, R.; Zierath, J.R. Paternal high-fat diet transgenerationally impacts hepatic immunometabolism. FASEB J., 2019.fj.201801879RR..
[http://dx.doi.org/10.1096/fj.201801879RR]
[99]
Wei, Y.; Yang, C-R.; Wei, Y-P.; Zhao, Z-A.; Hou, Y.; Schatten, H.; Sun, Q-Y. Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc. Natl. Acad. Sci. USA, 2014, 111, 1873-1878.
[http://dx.doi.org/10.1073/pnas.1321195111]
[100]
Donkin, I.; Barrès, R. Sperm epigenetics and influence of environmental factors. Mol. Metab., 2018, 14, 1-11.
[http://dx.doi.org/10.1016/j.molmet.2018.02.006]
[101]
Champroux, A.; Cocquet, J.; Henry-Berger, J.; Drevet, J.R.; Kocer, A. A decade of exploring the mammalian sperm epigenome: Paternal epigenetic and transgenerational inheritance. Front. Cell Dev. Biol., 2018, 6, 50.
[http://dx.doi.org/10.3389/fcell.2018.00050]
[102]
Holoch, D.; Moazed, D. RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet., 2015, 16, 71-84.
[http://dx.doi.org/10.1038/nrg3863]
[103]
Hur, S.S.J.; Cropley, J.E.; Suter, C.M. Paternal epigenetic programming: Evolving metabolic disease risk. J. Mol. Endocrinol., 2017, 58, R159-R168.
[http://dx.doi.org/10.1530/JME-16-0236]
[104]
Thakore, P.I.; Black, J.B.; Hilton, I.B.; Gersbach, C.A. Editing the epigenome: Technologies for programmable transcription and epigenetic modulation. Nat. Methods, 2016, 13, 127-137.
[http://dx.doi.org/10.1038/nmeth.3733]
[105]
Burdge, G.C.; Lillycrop, K.A.; Phillips, E.S.; Slater-Jefferies, J.L.; Jackson, A.A.; Hanson, M.A. Folic acid supplementation during the juvenile-pubertal period in rats modifies the phenotype and epigenotype induced by prenatal nutrition. J. Nutr., 2009, 139, 1054-1060.
[http://dx.doi.org/10.3945/jn.109.104653]
[106]
Cordero, P.; Milagro, F.I.; Campion, J.; Martinez, J.A. Maternal methyl donors supplementation during lactation prevents the hyperhomocysteinemia induced by a high-fat-sucrose intake by dams. Int. J. Mol. Sci., 2013, 14, 24422-24437.
[http://dx.doi.org/10.3390/ijms141224422]
[107]
Arrowsmith, C.H.; Bountra, C.; Fish, P.V.; Lee, K.; Schapira, M. Epigenetic protein families: A new frontier for drug discovery. Nat. Rev. Drug Discov., 2012, 11, 384-400.
[http://dx.doi.org/10.1038/nrd3674]

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