Obesity: Epigenetic regulation - Recent observations

Biomolecular Concepts

Volumn 6, Issue 3, 2015, Pages 163-175

  Remely, Marlene ^a   De La Garza, Ana Laura ^b   Magnet, Ulrich ^a   Aumueller, Eva ^a   Haslberger, Alexander G ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSIDAD AUTÓNOMA DE NUEVO LEÓN   (Mexico)

Author keywords

adulthood; animal models; postnatal; prenatal; transgenerational

Indexed keywords

ANIMALIA;

ANIMAL; DIET; EMBRYOLOGY; FOOD; GENETIC EPIGENESIS; GENETICS; HUMAN; LIFESTYLE; OBESITY;

ANIMALS; DIET; EPIGENESIS, GENETIC; FOOD; HUMANS; LIFE STYLE; OBESITY;

EID: 84936746875     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/bmc-2015-0009     Document Type: Review

References (113)

1. World Obesity Federation. World obesity 2014 [cited 2014 23 October 2014]; Available from: http://www.worldobesity.org/.
2. WHO. Available from: http://www.euro.who.int/en/health-topics/noncommunicable-diseases/2013. Accessed 18 October, 2013.
3. Remely M, Aumueller E, Jahn D, Hippe B, Brath H, Haslberger AG. Microbiota and epigenetic regulation of inflammatory mediators in type 2 diabetes and obesity. Benef Microb 2014; 5: 33-43.
4. Remely M, Aumueller E, Merold C, Dworzak S, Hippe B, Zanner J, Pointner A, Brath H, Haslberger AG. Effects of short chain fatty acid producing bacteria on epigenetic regulation of FFAR3 in type 2 diabetes and obesity. Gene 2013; 537: 85-92.
5. Jimenez-Chillaron JC, Díaz R, Martínez D, Pentinat T, Ramón-Krauel M, Ribó S, Plösch T. The role of nutrition on epigenetic modifications and their implications on health. Biochimie 2012; 94: 2242-63.
6. Gallou-Kabani C, Vigé A, Gross MS, Junien C. Nutri-epigenomics: lifelong remodelling of our epigenomes by nutritional and metabolic factors and beyond. Clin Chem Lab Med 2007; 45: 321-7.
7. Choi SW, Friso S. Epigenetics: a new bridge between nutrition and health. Adv Nutr 2010; 1: 8-16.
8. Brandl A, Heinzel T, Kramer OH. Histone deacetylases: salesmen and customers in the post-translational modification market. Biol Cell 2009; 101: 193-205.
9. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 2009; 10: 32-42.
10. Sawicka A, Seiser C. Histone H3 phosphorylation - a versatile chromatin modification for different occasions. Biochimie 2012; 94: 2193-201.
11. Brosch G, Loidl P, Graessle S. Histone modifications and chromatin dynamics: a focus on filamentous fungi. FEMS Microbiol Rev 2008; 32: 409-39.
12. Oliver SS, Denu JM. Dynamic interplay between histone H3 modifications and protein interpreters: emerging evidence for a "histone language". Chembiochem 2011; 12: 299-307.
13. Skinner MK, Manikkam M, Guerrero-Bosagna C. Epigenetic transgenerational actions of endocrine disruptors. Reprod Toxicol 2011; 31: 337-43.
14. Karmaus W, Osuch JR, Eneli I, Mudd LM, Zhang J, Mikucki D, Haan P, Davis S. Maternal levels of dichlorodiphenyl-dichloroethylene (DDE) may increase weight and body mass index in adult female offspring. Occup Environ Med 2009; 66: 143-9.
15. Somm E, Schwitzgebel VM, Toulotte A, Cederroth CR, Combescure C, Nef S, Aubert ML, Hüppi PS. Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect 2009; 117: 1549-55.
16. Newbold RR, Newbold RR, Padilla-Banks E, Snyder RJ, Jefferson WN. Developmental exposure to estrogenic compounds and obesity. Birth Defects Res A Clin Mol Teratol 2005; 73: 478-80.
17. Wang G, Walker SO, Hong X, Bartell TR, Wang X. Epigenetics and early life origins of chronic noncommunicable diseases. J Adolesc Health 2013; 52: Suppl 2: S14-21.
18. Grun F, Blumberg B. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology 2006; 147: 6 Suppl: S50-5.
19. He K, Zhao L, Daviglus ML, Dyer AR, Van Horn L, Garside D, Zhu L, Guo D, Wu Y, Zhou B, Stamler J, INTERMAP Cooperative Research Group. Association of monosodium glutamate intake with overweight in Chinese adults: the INTERMAP Study. Obesity (Silver Spring) 2008; 16: 1875-80.
20. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DI, Roseboom TJ. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 2008; 115: 1243-9.
21. Milagro FI, Mansego ML, De Miguel C, Martínez JA. Dietary factors, epigenetic modifications and obesity outcomes: progresses and perspectives. Mol Aspects Med 2013; 34: 782-812.
22. Clarke-Harris R, Wilkin TJ, Hosking J, Pinkney J, Jeffery AN, Metcalf BS, Keith M. Godfrey, Voss LD, Lillycrop KA, Burdge GC. PGC1α promoter methylation in blood at 5-7 years predicts adiposity from 9 to 14 years (EarlyBird 50). Diabetes 2014; 63: 2528-37.
23. Fraga CG, Galleano M, Verstraeten SV, Oteiza PI. Basic biochemical mechanisms behind the health benefits of polyphenols. Mol Aspects Med 2010; 31: 435-45.
24. Boque N, de la Iglesia R, de la Garza AL, Milagro FI, Olivares M, Bañuelos O, Soria AC, Rodríguez-Sánchez S, Martínez JA, Campión J. Prevention of diet-induced obesity by apple polyphenols in Wistar rats through regulation of adipocyte gene expression and DNA methylation patterns. Mol Nutr Food Res 2013; 57: 1473-8.
25. Milenkovic D, Deval C, Gouranton E, Landrier JF, Scalbert A, Morand C, Mazur A. Modulation of miRNA expression by dietary polyphenols in apoE deficient mice: a new mechanism of the action of polyphenols. PLoS One 2012; 7: e29837.
26. Ayissi VB, Ebrahimi A, Schluesenner H. Epigenetic effects of natural polyphenols: A focus on SIRT1-mediated mechanisms. Mol Nutr Food Res 2014; 58: 22-32.
27. Dolinoy DC, Weidman JR, Waterland RA, Jirtle RL. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect 2006; 114: 567-72.
28. Kilpinen H, Dermitzakis ET. Genetic and epigenetic contribution to complex traits. Hum Mol Genet 2012; 21: R24-8.
29. Tammen SA, Friso S, Choi SW. Epigenetics: the link between nature and nurture. Mol Aspects Med 2013; 34: 753-64.
30. Franks PW, Ling C. Epigenetics and obesity: the devil is in the details. BMC Med 2010; 8: 88.
31. Waterborg JH. Dynamics of histone acetylation in vivo. A function for acetylation turnover? Biochem Cell Biol 2002; 80: 363-78.
32. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J, Surani MA. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 2002; 117: 15-23.
33. Hales CN, Barker DJ. The thrifty phenotype hypothesis. Br Med Bull 2001; 60: 5-20.
34. Pembrey ME. Time to take epigenetic inheritance seriously. Eur J Hum Genet 2002; 10: 669-71.
35. Vickers MH. Developmental programming and transgenerational transmission of obesity. Ann Nutr Metab 2014; 64: Suppl 1: 26-34.
36. Kaati G, Bygren LO, Edvinsson S. Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur J Hum Genet 2002; 10: 682-8.
37. Pentinat T, Ramon-Krauel M, Cebria J, Diaz R, Jimenez-Chillaron JC. Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition. Endocrinology 2010; 151: 5617-23.
38. Fullston T, Palmer NO, Owens JA, Mitchell M, Bakos HW, Lane M. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod 2012; 27: 1391-400.
39. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, Bock C, Li C, Gu H, Zamore PD, Meissner A, Weng Z, Hofmann HA, Friedman N, Rando OJ. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010; 143: 1084-96.
40. Armitage JA, Ishibashi A, Balachandran AA, Jensen RI, Poston L, Taylor PD. Programmed aortic dysfunction and reduced Na+, K+-ATPase activity present in first generation offspring of lardfed rats does not persist to the second generation. Exp Physiol 2007; 92: 583-9.
41. Dunn GA, Bale TL. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 2011; 152: 2228-36.
42. Blondeau B, Avril I, Duchene B, Bréant B. Endocrine pancreas development is altered in foetuses from rats previously showing intra-uterine growth retardation in response to malnutrition. Diabetologia 2002; 45: 394-401.
43. Thamotharan M, Garg M, Oak S, Rogers LM, Pan G, Sangiorgi F, Lee PW, Devaskar SU. Transgenerational inheritance of the insulin-resistant phenotype in embryo-transferred intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 2007; 292: E1270-9.
44. Benyshek DC, Johnston CS, Martin JF, Ross WD. Insulin sensitivity is normalized in the third generation (F3) offspring of developmentally programmed insulin resistant (F2) rats fed an energy-restricted diet. Nutr Metab (Lond) 2008; 5: 26.
45. Pinheiro AR, Salvucci ID, Aguila MB, Mandarim-de-Lacerda CA. Protein restriction during gestation and/or lactation causes adverse transgenerational effects on biometry and glucose metabolism in F1 and F2 progenies of rats. Clin Sci (Lond) 2008; 114: 381-92.
46. Peixoto-Silva N, Frantz ED, Mandarim-de-Lacerda CA, Pinheiro-Mulder A. Maternal protein restriction in mice causes adverse metabolic and hypothalamic effects in the F1 and F2 generations. Br J Nutr 2011; 106: 1364-73.
47. Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, Lillycrop KA. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr 2007; 97: 435-9.
48. Frantz ED, Aguila MB, Pinheiro-Mulder Ada R, Mandarim-de-Lacerda CA. Transgenerational endocrine pancreatic adaptation in mice from maternal protein restriction in utero. Mech Ageing Dev 2011; 132: 110-6.
49. Torrens C, Poston L, Hanson MA. Transmission of raised blood pressure and endothelial dysfunction to the F2 generation induced by maternal protein restriction in the F0, in the absence of dietary challenge in the F1 generation. Br J Nutr 2008; 100: 760-6.
50. Harrison M, Langley-Evans SC. Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. Br J Nutr 2009; 101: 1020-30.
51. Benyshek DC, Johnston CS, Martin JF. Glucose metabolism is altered in the adequately-nourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 2006; 49: 1117-9.
52. Drake AJ, Walker BR, Seckl JR. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol 2005; 288: R34-8.
53. Burdge GC, Hoile SP, Uller T, Thomas NA, Gluckman PD, Hanson MA, Lillycrop KA. Progressive, transgenerational changes in offspring phenotype and epigenotype following nutritional transition. PLoS One 2011; 6: e28282.
54. Chang HS, Anway MD, Rekow SS, Skinner MK. Transgenerational epigenetic imprinting of the male germline by endocrine disruptor exposure during gonadal sex determination. Endocrinology 2006; 147: 5524-41.
55. Walker DM, Gore AC. Transgenerational neuroendocrine disruption of reproduction. Nat Rev Endocrinol 2011; 7: 197-207.
56. Grun F, Watanabe H, Zamanian Z, Maeda L, Arima K, Cubacha R, Gardiner DM, Kanno J, Iguchi T, Blumberg B. Endocrine-disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Mol Endocrinol 2006; 20: 2141-55.
57. Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, Reyes TM. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 2010; 151: 4756-64.
58. Archer E. The childhood obesity epidemic as a result of nongenetic evolution: the maternal resources hypothesis. Mayo Clin Proc 2014; 90: 77-92.
59. Ge ZJ, Liang QX, Hou Y, Han ZM, Schatten H, Sun QY, Zhang CL. Maternal obesity and diabetes may cause DNA methylation alteration in the spermatozoa of offspring in mice. Reprod Biol Endocrinol 2014; 12: 29.
60. Mathers JC. Session 2: personalised nutrition. Epigenomics: a basis for understanding individual differences? Proc Nutr Soc 2008; 67: 390-4.
61. Waterland RA. Assessing the effects of high methionine intake on DNA methylation. J Nutr 2006; 136: 6 Suppl: 1706S-10S.
62. Waterland RA, Travisano M, Tahiliani KG, Rached MT, Mirza S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond) 2008; 32: 1373-9.
63. Scarlett JM, Zhu X, Enriori PJ, Bowe DD, Batra AK, Levasseur PR, Grant WF, Meguid MM, Cowley MA, Marks DL. Regulation of agouti-related protein messenger ribonucleic acid transcription and peptide secretion by acute and chronic inflammation. Endocrinology 2008; 149: 4837-45.
64. El Hajj N, Schneider E, Lehnen H, Haaf T. Epigenetics and life-long consequences of an adverse nutritional and diabetic intrauterine environment. Reproduction 2014; 148: R111-20.
65. Guerrero-Bosagna CM, Sabat P, Valdovinos FS, Valladares LE, Clark SJ. Epigenetic and phenotypic changes result from a continuous pre and post natal dietary exposure to phytoestrogens in an experimental population of mice. BMC Physiol 2008; 8: 17.
66. Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci USA 2007; 104: 13056-61.
67. Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, Thurston A, Huntley JF, Rees WD, Maloney CA, Lea RG, Craigon J, McEvoy TG, Young LE. DNA methylation, insulin resistance and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA 2007; 104: 19351-6.
68. Fernandez JR, Klimentidis YC, Dulin-Keita A, Casazza K. Genetic influences in childhood obesity: recent progress and recommendations for experimental designs. Int J Obes (Lond) 2012; 36: 479-84.
69. Soubry A, Murphy SK, Wang F, Huang Z, Vidal AC, Fuemmeler BF, Kurtzberg J, Murtha A, Jirtle RL, Schildkraut JM, Hoyo C. Newborns of obese parents have altered DNA methylation patterns at imprinted genes. Int J Obes (Lond) 2015; 39: 650-7.
70. Zheng J, Xiao X, Zhang Q, Yu M. DNA methylation: the pivotal interaction between early-life nutrition and glucose metabolism in later life. Br J Nutr 2014; 112: 1850-7.
71. Kyle UG, Pichard C. The Dutch Famine of 1944-1945: a pathophysiological model of long-term consequences of wasting disease. Curr Opin Clin Nutr Metab Care 2006; 9: 388-94.
72. Khulan B, Cooper WN, Skinner BM, Bauer J, Owens S, Prentice AM, Belteki G, Constancia M, Dunger D, Affara NA. Periconceptional maternal micronutrient supplementation is associated with widespread gender related changes in the epigenome: a study of a unique resource in the Gambia. Hum Mol Genet 2012; 21: 2086-101.
73. Cooper WN, Khulan B, Owens S, Elks CE, Seidel V, Prentice AM, Belteki G, Ong KK, Affara NA, Constância M, Dunger DB. DNA methylation profiling at imprinted loci after periconceptional micronutrient supplementation in humans: results of a pilot randomized controlled trial. FASEB J 2012; 26: 1782-90.
74. Li J, Chen L, Yu P, Liu B, Zhu J, Yang Y. Telmisartan exerts antitumor effects by activating peroxisome proliferator-activated receptor-gamma in human lung adenocarcinoma A549 cells. Molecules 2014; 19: 2862-76.
75. Menale C, Piccolo MT, Cirillo G, Calogero RA, Papparella A, Mita L, Miraglia Del Giuduce E, Diano N, Crispi S, Mita DG. Bisphenol A effects on gene expression in children adipocytes: association to metabolic disorders. J Mol Endocrinol 2015 Apr 15. pii: JME-14-0282.
76. Dick KJ, Nelson CP, Tsaprouni L, Sandling JK, Aïssi D, Wahl S, Meduri E, Morange PE, Gagnon F, Grallert H, Waldenberger M, Peters A, Erdmann J, Hengstenberg C, Cambien F, Goodall AH, Ouwehand WH, Schunkert H, Thompson JR, Spector TD, Gieger C, Trégouët DA, Delouka P. DNA methylation and body-mass index: a genome-wide analysis. Lancet 2014; 383: 1990-8.
77. Xu X, Su S, Barnes VA, De Miguel C, Pollock J, Ownby D, Shi H, Zhu H, Snieder H, Wang X. A genome-wide methylation study on obesity: differential variability and differential methylation. Epigenetics 2013; 8: 522-33.
78. Davis KE, Neinast MD, Sun K, Skiles WM, Bills JD, Zehr JA, Zeve D, Hahner LD, Cox DW, Gent LM, Xu Y, Wang ZV, Khan SA, Clegg DJ. The sexually dimorphic role of adipose and adipocyte estrogen receptors in modulating adipose tissue expansion, inflammation and fibrosis. Mol Metab 2013; 2: 227-42.
79. Feinberg AP, Irizarry RA, Fradin D, Aryee MJ, Murakami P, Aspelund T, Eiriksdottir G, Harris TB, Launer L, Gudnason V, Fallin MD. Personalized epigenomic signatures that are stable over time and covary with body mass index. Sci Transl Med 2010; 2: 49ra67.
80. Na YK, Hong HS, Lee DH, Lee WK, Kim DS. Effect of body mass index on global DNA methylation in healthy Korean women. Mol Cells 2014; 37: 467-72.
81. Campion J, Milagro FI, Goyenechea E, Martínez JA. TNF-alpha promoter methylation as a predictive biomarker for weight-loss response. Obesity (Silver Spring) 2009; 17: 1293-7.
82. Moleres A, Campión J, Milagro FI, Marcos A, Campoy C, Garagorri JM, Gómez-Martínez S, Martínez JA, Azcona-Sanjulián MC, Martí A, EVASYON Study Group. Differential DNA methylation patterns between high and low responders to a weight loss intervention in overweight or obese adolescents: the EVASYON study. FASEB J 2013; 27: 2504-12.
83. Milagro FI, Campión J, Cordero P, Goyenechea E, Gómez-Uriz AM, Abete I, Zulet MA, Martínez JA. A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. FASEB J 2011; 25: 1378-89.
84. Nilsson EK, Ernst B, Voisin S, Almén MS, Benedict C, Mwinyi J, Fredriksson R, Schultes B, Schiöth HB. Roux-en Y gastric bypass surgery induces genome-wide promoter-specific changes in DNA methylation in whole blood of obese patients. PLoS One 2015; 10: e0115186.
85. Okamura M, Inagaki T, Tanaka T, Sakai J. Role of histone methylation and demethylation in adipogenesis and obesity. Organogenesis 2010; 6: 24-32.
86. Farmer SR. Transcriptional control of adipocyte formation. Cell Metab 2006; 4: 263-73.
87. Ortega FJ, Mercader JM, Catalán V, Moreno-Navarrete JM, Pueyo N, Sabater M, Gómez-Ambrosi J, Anglada R, Fernández-Formoso JA, Ricart W, Frühbeck G, Fernández-Real JM. Targeting the circulating microRNA signature of obesity. Clin Chem 2013; 59: 781-92.
88. Yeh CL, Cheng IC, Hou YC, Wang W, Yeh SL. MicroRNA-125a-3p expression in abdominal adipose tissues is associated with insulin signalling gene expressions in morbid obesity: observations in Taiwanese. Asia Pac J Clin Nutr 2014; 23: 331-7.
89. McKay JA, Mathers JC. Diet induced epigenetic changes and their implications for health. Acta Physiol (Oxf) 2011; 202: 103-18.
90. Panchal SK, Brown L. Rodent models for metabolic syndrome research. J Biomed Biotechnol 2011; 2011: 351982.
91. Speakman J, Hambly C, Mitchell S, Król E. The contribution of animal models to the study of obesity. Lab Anim 2008; 42: 413-32.
92. Milagro FI, Campión J, García-Díaz DF, Goyenechea E, Paternain L, Martínez JA. High fat diet-induced obesity modifies the methylation pattern of leptin promoter in rats. J Physiol Biochem 2009; 65: 1-9.
93. Fontana L, Klein S, Holloszy JO. Effects of long-term calorie restriction and endurance exercise on glucose tolerance, insulin action and adipokine production. Age (Dordr) 2010; 32: 97-108.
94. Seki Y, Williams L, Vuguin PM, Charron MJ. Minireview: Epigenetic programming of diabetes and obesity: animal models. Endocrinology 2012; 153: 1031-8.
95. Wheatley KE, Nogueira LM, Perkins SN, Hursting SD. Differential effects of calorie restriction and exercise on the adipose transcriptome in diet-induced obese mice. J Obes 2011; 2011: 265417.
96. Zhang S, Rattanatray L, MacLaughlin SM, Cropley JE, Suter CM, Molloy L, Kleemann D, Walker SK, Muhlhausler BS, Morrison JL, McMillen IC. Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring. FASEB J 2010; 24: 2772-82.
97. Vaquero A, Reinberg D. Calorie restriction and the exercise of chromatin. Genes Dev 2009; 23: 1849-69.
98. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 2005; 135: 1382-6.
99. Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, Burdge GC. Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr 2008; 100: 278-82.
100. Sohi G, Marchand K, Revesz A, Arany E, Hardy DB. Maternal protein restriction elevates cholesterol in adult rat offspring due to repressive changes in histone modifications at the cholesterol 7alpha-hydroxylase promoter. Mol Endocrinol 2011; 25: 785-98.
101. Boque N, Campión J, Paternain L, García-Díaz DF, Galarraga M, Portillo MP, Milagro FI, Ortiz de Solórzano C, Martínez JA. Influence of dietary macronutrient composition on adiposity and cellularity of different fat depots in Wistar rats. J Physiol Biochem 2009; 65: 387-95.
102. Lomba A, Martínez JA, García-Díaz DF, Paternain L, Marti A, Campión J, Milagro FI. Weight gain induced by an isocaloric pair-fed high fat diet: a nutriepigenetic study on FASN and NDUFB6 gene promoters. Mol Genet Metab 2010; 101: 273-8.
103. Vucetic Z, Carlin JL, Totoki K, Reyes TM. Epigenetic dysregulation of the dopamine system in diet-induced obesity. J Neurochem 2012; 120: 891-8.
104. Vucetic Z, Kimmel J, Reyes TM. Chronic high-fat diet drives postnatal epigenetic regulation of mu-opioid receptor in the brain. Neuropsychopharmacology 2011; 36: 1199-206.
105. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 2010; 467: 963-6.
106. Rinella ME, Elias MS, Smolak RR, Fu T, Borensztajn J, Green RM. Mechanisms of hepatic steatosis in mice fed a lipogenic methionine choline-deficient diet. J Lipid Res 2008; 49: 1068-76.
107. Pogribny IP, Tryndyak VP, Bagnyukova TV, Melnyk S, Montgomery B, Ross SA, Latendresse JR, Rusyn I, Beland FA. Hepatic epigenetic phenotype predetermines individual susceptibility to hepatic steatosis in mice fed a lipogenic methyl-deficient diet. J Hepatol 2009; 51: 176-86.
108. Uthus EO, Ross SA, Davis CD. Differential effects of dietary selenium (se) and folate on methyl metabolism in liver and colon of rats. Biol Trace Elem Res 2006; 109: 201-14.
109. Campion J, Milagro FI, Martinez JA. Individuality and epigenetics in obesity. Obes Rev 2009; 10: 383-92.
110. Su SY, Dodson MV, Li XB, Li QF, Wang HW, Xie Z. The effects of dietary betaine supplementation on fatty liver performance, serum parameters, histological changes, methylation status and the mRNA expression level of Spot14alpha in Landes goose fatty liver. Comp Biochem Physiol A Mol Integr Physiol 2009; 154: 308-14.
111. Unterberger A, Szyf M, Nathanielsz PW, Cox LA. Organ and gestational age effects of maternal nutrient restriction on global methylation in fetal baboons. J Med Primatol 2009; 38: 219-27.
112. Buescher JL, Musselman LP, Wilson CA, Lang T, Keleher M, Baranski TJ, Duncan JG. Evidence for transgenerational metabolic programming in Drosophila. Dis Model Mech 2013; 6: 1123-32.
113. Matzkin LM, Johnson S, Paight C, Markow TA. Preadult parental diet affects offspring development and metabolism in Drosophila melanogaster. PLoS One 2013; 8: e59530.