What obesity research tells us about epigenetic mechanisms

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1609, 2013, Pages

  Youngson, Neil A ^a   Morris, Margaret J ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Developmental programming; Epigenetics; Obesity; Transgenerational epigenetic inheritance

Indexed keywords

DISEASE TREATMENT; GENE EXPRESSION; GENOMICS; GENOTYPE-ENVIRONMENT INTERACTION; HERITABILITY; MEDICINE; OBESITY; PATHOLOGY; PHYSIOLOGY;

EID: 84869431089     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0337     Document Type: Review

References (148)

1. Day FR, Loos RJ. 2011 Developments in obesity genetics in the era of genome-wide association studies. J. Nutrigenet. Nutrigenomics 4, 222-238. (doi:10.1159/000332158)
2. McAllister EJ et al. 2009 Ten putative contributors to the obesity epidemic. Crit. Rev. Food Sci. Nutr. 49, 868-913. (doi:10.1080/10408390903372599)
3. Mavanji V, Billington CJ, Kotz CM, Teske JA. 2012 Sleep and obesity: a focus on animal models. Neurosci. Biobehav. Rev. 36, 1015-1029. (doi:10. 1016/j.neubiorev.2012.01.001)
4. Volkow ND, Wang GJ, Baler RD. 2011 Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn. Sci. 15, 37-46. (doi:10.1016/j.tics.2010.11.001)
5. Gearhardt AN, Grilo CM, DiLeone RJ, Brownell KD, Potenza MN. 2011 Can food be addictive? Public health and policy implications. Addiction 106, 1208-1212. (doi:10.1111/j.1360-0443.2010.03301.x)
6. WHO. 2007 Global database on body mass index. See http://www.who.int/bmi/index.jsp.
7. Morris MJ. 2009 Early life influences on obesity risk: maternal overnutrition and programming of obesity. Expert Rev. Endocronol. Metab. 4, 625-637. (doi:10.1586/eem.09.45)
8. McIntyre HD, Gibbons KS, Flenady VJ, Callaway LK. 2012 Overweight and obesity in Australian mothers: epidemic or endemic? Med. J. Austr. 196, 184-188. (doi:10.5694/mja11.11120)
9. CDC. 2010 Overweight and obesity: childhood overweight and obesity: data and statistics. Centers for Disease Control and Prevention.
10. Watkins M, Clark K, Foster C, Welch K, Kasa-Vubu J. 2007 Relationships among body mass index, parental perceptions, birthweight and parental weight after referral to a weight clinic. J. Natl Med. Assoc. 99, 908-913.
11. Feil R, Fraga MF. 2011 Epigenetics and the environment: emerging patterns and implications. Nat. Rev. Genet. 13, 97-109.
12. Law JA, Jacobsen SE. 2010 Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204-220. (doi:10.1038/nrg2719)
13. Reik W. 2007 Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432. (doi:10.1038/nature05918)
14. Payer B, Lee JT, Namekawa SH. 2011 X-inactivation and X-reactivation: epigenetic hallmarks of mammalian reproduction and pluripotent stem cells. Hum. Genet. 130, 265-280. (doi:10.1007/s00439-011-1024-7)
15. Lange UC, Schneider R. 2010 What an epigenome remembers. BioEssays 32, 659-668. (doi:10.1002/bies.201000030)
16. Faulk C, Dolinoy DC. 2011 Timing is everything: the when and how of environmentally induced changes in the epigenome of animals. Epigenetics 6, 791-797. (doi:10.4161/epi.6.7.16209)
17. Yamagata Y, Szabo P, Szuts D, Bacquet C, Aranyi T, Paldi A. 2012 Rapid turnover of DNA methylation in human cells. Epigenetics 7, 141-145. (doi:10.4161/epi.7.2.18906)
18. Zhou VW, Goren A, Bernstein BE. 2011 Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 12, 7-18. (doi:10.1038/nrg2905)
19. Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS. 2010 Non-coding RNAs: regulators of disease. J. Pathol. 220, 126-139. (doi:10.1002/path.2638)
20. Heneghan HM, Miller N, Kerin MJ. 2010 Role of microRNAs in obesity and the metabolic syndrome. Obes. Rev. 11, 354-361. (doi:10.1111/j.1467-789X. 2009.00659.x)
21. Sun L, Xie H, Mori MA, Alexander R, Yuan B, Hattangadi SM, Liu Q, Kahn CR, Lodish HF. 2011 Mir193b-365 is essential for brown fat differentiation. Nat. Cell Biol. 13, 958-965. (doi:10.1038/ncb2286)
22. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J, Surani MA. 2002 Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 117, 15-23. (doi:10.1016/S0925-4773(02)00181-8)
23. Guibert S, Forne T, Weber M. 2012 Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res. 22, 633-641. (doi:10. 1101/gr.130997.111)
24. Popp C, Dean W, Feng S, Cokus SJ, Andrews S, Pellegrini M, Jacobsen SE, Reik W. 2010 Genomewide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463, 1101-1105. (doi:10.1038/nature08829)
25. Sasaki H, Matsui Y. 2008 Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat. Rev. Genet. 9, 129-140. (doi:10.1038/nrg2295)
26. Hajkova P et al. 2008 Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452, 877-881. (doi:10.1038/nature06714)
27. Ward WS, Coffey DS. 1991 DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol. Reprod. 44, 569-574. (doi:10.1095/biolreprod44.4.569)
28. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A, Meissner A. 2012 A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339-344. (doi:10.1038/nature10960)
29. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J, Reik W. 2003 Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35, 88-93. (doi:10.1002/gene.10168)
30. Li Y, O'Neill C. 2012 Persistence of cytosine methylation of DNA following fertilisation in the mouse. PLoS ONE 7, e30687. (doi:10.1371/journal. pone.0030687)
31. Burton A, Torres-Padilla ME. 2010 Epigenetic reprogramming and development: a unique heterochromatin organization in the preimplantation mouse embryo. Brief. Funct. Genomics 9, 444-454. (doi:10.1093/bfgp/elq027)
32. Hitchins MP. 2010 Inheritance of epigenetic aberrations (constitutional epimutations) in cancer susceptibility. Adv. Genet. 70, 201-243. (doi:10. 1016/B978-0-12-380866-0.60008-3)
33. Martin DI, Cropley JE, Suter CM. 2011 Epigenetics in disease: leader or follower? Epigenetics 6, 843-848. (doi:10.4161/epi.6.7.16498)
34. Hesson LB, Hitchins MP, Ward RL. 2010 Epimutations and cancer predisposition: importance and mechanisms. Curr. Opin. Genet. Dev. 20, 290-298. (doi:10.1016/j.gde.2010.02.005)
35. Lienert F, Wirbelauer C, Som I, Dean A, Mohn F, Schubeler D. 2011 Identification of genetic elements that autonomously determine DNA methylation states. Nat. Genet. 43, 1091-1097. (doi:10.1038/ng.946)
36. Zierath JR, Barres RE. 2011 Nutritional status affects the epigenomic profile of peripheral blood cells. Epigenomics 3, 259-260. (doi:10.2217/epi.11.24)
37. Lavebratt C, Almgren M, Ekstrom TJ. 2011 Epigenetic regulation in obesity. Int. J. Obes. (Lond). 36, 757-765. (doi:10.1038/ijo.2011.178)
38. Lillycrop KA, Burdge GC. 2011 Epigenetic changes in early life and future risk of obesity. Int. J. Obes. (Lond.) 35, 72-83. (doi:10.1038/ijo.2010.122)
39. Campion J, Milagro F, Martinez JA. 2010 Epigenetics and obesity. Prog. Mol. Biol. Transl. Sci. 94, 291-347. (doi:10.1016/B978-0-12-375003-7. 00011-X)
40. Gregoire FM, Smas CM, Sul HS. 1998 Understanding adipocyte differentiation. Physiol. Rev. 78, 783-809.
41. Berger J, Bailey P, Biswas C, Cullinan CA, Doebber TW, Hayes NS, Saperstein R, Smith RG, Leibowitz MD. 1996 Thiazolidinediones produce a conformational change in peroxisomal proliferatoractivated receptor-gamma: binding and activation correlate with antidiabetic actions in db/db mice. Endocrinology 137, 4189-4195. (doi:10.1210/en.137.10.4189)
42. Ge K. 2012 Epigenetic regulation of adipogenesis by histone methylation. Biochim. Biophys. Acta 1819, 727-732. (doi:10.1016/j.bbagrm.2011.12.008)
43. Nielsen R et al. 2008 Genome-wide profiling of PPARgamma:RXR and RNA polymerase II occupancy reveals temporal activation of distinct metabolic pathways and changes in RXR dimer composition during adipogenesis. Genes Dev. 22, 2953-2967. (doi:10.1101/gad.501108)
44. Lefterova MI et al. 2008 PPARgamma and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scale. Genes Dev. 22, 2941-2952. (doi:10.1101/gad.1709008)
45. Lee J et al. 2008 Targeted inactivation of MLL3 histone H3-Lys-4 methyltransferase activity in the mouse reveals vital roles for MLL3 in adipogenesis. Proc. Natl Acad. Sci. USA 105, 19 229-19 234. (doi:10.1073/pnas.0810100105)
46. Cho YW, Hong S, Jin Q, Wang L, Lee JE, Gavrilova O, Ge K. 2009 Histone methylation regulator PTIP is required for PPARgamma and C/EBPalpha expression and adipogenesis. Cell Metab. 10, 27-39. (doi:10.1016/j.cmet.2009.05.010)
47. Zhu Y, Kan L, Qi C, Kanwar YS, Yeldandi AV, Rao MS, Reddy JK. 2000 Isolation and characterization of peroxisome proliferator-activated receptor (PPAR) interacting protein (PRIP) as a coactivator for PPAR. J. Biol. Chem. 275, 13 510-13 516. (doi:10.1074/jbc.275.18.13510)
48. Wakabayashi K et al. 2009 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. 29, 3544-3555. (doi:10.1128/MCB.01856-08)
49. Fujiki K, Kano F, Shiota K, Murata M. 2009 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. 7, 38. (doi:10.1186/1741-7007-7-38)
50. Mikkelsen TS, Xu Z, Zhang X, Wang L, Gimble JM, Lander ES, Rosen ED. 2010 Comparative epigenomic analysis of murine and human adipogenesis. Cell 143, 156-169. (doi:10.1016/j.cell.2010.09.006)
51. Wang L, Jin Q, Lee JE, Su IH, Ge K. 2010 Histone H3K27 methyltransferase Ezh2 represses Wnt genes to facilitate adipogenesis. Proc. Natl Acad. Sci. USA 107, 7317-7322. (doi:10.1073/pnas.1000031107)
52. Rada P, Bocarsly ME, Barson JR, Hoebel BG, Leibowitz SF. 2010 Reduced accumbens dopamine in Sprague-Dawley rats prone to overeating a fatrich diet. Physiol. Behav. 101, 394-400. (doi:10. 1016/j.physbeh.2010.07.005)
53. Vucetic Z, Carlin JL, Totoki K, Reyes TM. 2012 Epigenetic dysregulation of the dopamine system in diet-induced obesity. J. Neurochem. 120, 891-898.
54. Krugel U, Schraft T, Kittner H, Kiess W, Illes P. 2003 Basal and feeding-evoked dopamine release in the rat nucleus accumbens is depressed by leptin. Eur. J. Pharmacol. 482, 185-187. (doi:10.1016/j. ejphar.2003.09.047)
55. Hommel JD, Trinko R, Sears RM, Georgescu D, Liu ZW, Gao XB, Thurmon JJ, Marinelli M, DiLeone RJ. 2006 Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51, 801-810. (doi:10.1016/j.neuron.2006.08.023)
56. Vucetic Z, Kimmel J, Reyes TM. 2011 Chronic high-fat diet drives postnatal epigenetic regulation of mu-opioid receptor in the brain. Neuropsychopharmacology 36, 1199-1206. (doi:10.1038/npp.2011.4)
57. Wheatley KE, Nogueira LM, Perkins SN, Hurstig SD. 2011 Differential effects of calorie restriction and exercise on the adipose transcriptome in dietinduced obese mice. J. Obes. 2011, 265417. (doi:10. 1155/2011/265417)
58. Nikoshkov A, Sunkari V, Savu O, Forsberg E, Catrina SB, Brismar K. 2011 Epigenetic DNA methylation in the promoters of the Igf1 receptor and insulin receptor genes in db/db mice. Epigenetics 6, 405-409. (doi:10.4161/epi.6.4.14791)
59. Almen MS, Jacobsson JA, Moschonis G, Benedict C, Chrousos GP, Fredriksson R, Schioth HB. 2012 Genome wide analysis reveals association of a FTO gene variant with epigenetic changes. Genomics 99, 132-137. (doi:10.1016/j.ygeno.2011.12.007)
60. Wang X et al. 2010 Obesity related methylation changes in DNA of peripheral blood leukocytes. BMC Med. 8, 87. (doi:10.1186/1741-7015-8-87)
61. Milagro FI, Campion J, Cordero P, Goyenechea E, Gomez-Uriz AM, Abete I, Zulet MA, Martinez JA. 2011 A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. FASEB J. 25, 1378-1389. (doi:10.1096/fj.10-170365)
62. Lee J, Mi Seok S, Yu P, Kim K, Smith Z, Rivas-Astroza M, Zhong S, Kim Kemper J. 2012 Genomic analysis of hepatic farnesoid X receptor (FXR) binding sites reveals altered binding in obesity and direct gene repression by FXR. Hepatology 56, 108-117. (doi:10.1002/hep.25609)
63. Funato H, Oda S, Yokofujita J, Igarashi H, Kuroda M. 2011 Fasting and high-fat diet alter histone deacetylase expression in the medial hypothalamus. PLoS ONE 6, e18950. (doi:10.1371/journal. pone.0018950)
64. Kamei Y et al. 2010 Increased expression of DNA methyltransferase 3a in obese adipose tissue: studies with transgenic mice. Obesity (Silver Spring, MD) 18, 314-321. (doi:10.1038/oby. 2009.246)
65. Tateishi K, Okada Y, Kallin EM, Zhang Y. 2009 Role of Jhdm2a in regulating metabolic gene expression and obesity resistance. Nature 458, 757-761. (doi:10.1038/nature07777)
66. Inagaki T et al. 2009 Obesity and metabolic syndrome in histone demethylase JHDM2a-deficient mice. Genes Cells 14, 991-1001. (doi:10.1111/j. 1365-2443.2009.01326.x)
67. Iyengar S, Farnham PJ. 2011 KAP1 protein: an enigmatic master regulator of the genome. J. Biol. Chem. 286, 26 267-26 276. (doi:10.1074/jbc.R111. 252569)
68. Whitelaw NC, Chong S, Morgan DK, Nestor C, Bruxner TJ, Ashe A, Lambley E, Meehan R, Whitelaw E. 2010 Reduced levels of two modifiers of epigenetic gene silencing, Dnmt3a and Trim28, cause increased phenotypic noise. Genome Biol. 11, R111. (doi:10.1186/gb-2010-11-11-r111)
69. Moretti P, Zoghbi HY. 2006 MeCP2 dysfunction in Rett syndrome and related disorders. Curr. Opin. Genet. Dev. 16, 276-281. (doi:10.1016/j.gde. 2006.04.009)
70. Guy J, Cheval H, Selfridge J, Bird A. 2011 The role of MeCP2 in the brain. Annu. Rev. Cell Dev. Biol. 27, 631-652. (doi:10.1146/annurev-cellbio-092910-154121)
71. Kleefstra T, Yntema HG, Oudakker AR, Romein T, Sistermans E, Nillessen W, van Bokhoven H, de Vries BB, Hamel BC. 2002 De novo MECP2 frameshift mutation in a boy with moderate mental retardation, obesity and gynaecomastia. Clin. Genet. 61, 359-362. (doi:10.1034/j.1399-0004.2002. 610507.x)
72. Couvert P et al. 2001 MECP2 is highly mutated in Xlinked mental retardation. Hum. Mol. Genet. 10, 941-946. (doi:10.1093/hmg/10.9.941)
73. Fyffe SL et al. 2008 Deletion of Mecp2 in Sim1-expressing neurons reveals a critical role for MeCP2 in feeding behavior, aggression, and the response to stress. Neuron 59, 947-958. (doi:10.1016/j. neuron.2008.07.030)
74. Yang J et al. 2011 Genome partitioning of genetic variation for complex traits using common SNPs. Nat. Genet. 43, 519-525. (doi:10.1038/ng.823)
75. Bogardus C. 2009 Missing heritability and GWAS utility. Obesity (Silver Spring, MD) 17, 209-210. (doi:10.1038/oby.2008.613)
76. Matarazzo MR, De Bonis ML, Vacca M, Della Ragione F, D'Esposito M. 2009 Lessons from two human chromatin diseases, ICF syndrome and Rett syndrome. Int. J. Biochem. Cell Biol. 41, 117-126. (doi:10.1016/j.biocel.2008.07.026)
77. Csoka AB, Szyf M. 2009 Epigenetic side-effects of common pharmaceuticals: a potential new field in medicine and pharmacology. Med. Hypotheses 73, 770-780. (doi:10.1016/j.mehy.2008.10.039)
78. Newbold RR. 2010 Impact of environmental endocrine disrupting chemicals on the development of obesity. Hormones (Athens) 9, 206-217.
79. Verrotti A, Basciani F, De Simone M, Trotta D, Morgese G, Chiarelli F. 2002 Insulin resistance in epileptic girls who gain weight after therapy with valproic acid. J. Child Neurol. 17, 265-268. (doi:10. 1177/088307380201700405)
80. Qiao L, Kinney B, Yoo HS, Lee B, Schaack J, Shao J. 2012 Adiponectin increases skeletal muscle mitochondrial biogenesis by suppressing mitogenactivated protein kinase phosphatase-1. Diabetes 61, 1463-1470. (doi:10.2337/db11-1475)
81. Qiao L, Schaack J, Shao J. 2006 Suppression of adiponectin gene expression by histone deacetylase inhibitor valproic acid. Endocrinology 147, 865-874. (doi:10.1210/en.2005-1030)
82. Brill J, Lee M, Zhao S, Fernald RD, Huguenard JR. 2006 Chronic valproic acid treatment triggers increased neuropeptide y expression and signaling in rat nucleus reticularis thalami. J. Neurosci. 26, 6813-6822. (doi:10.1523/JNEUROSCI.5320-05.2006)
83. Pogribny IP, Shpyleva SI, Muskhelishvili L, Bagnyukova TV, James SJ, Beland FA. 2009 Role of DNA damage and alterations in cytosine DNA methylation in rat liver carcinogenesis induced by a methyl-deficient diet. Mutat. Res. 669, 56-62. (doi:10.1016/j.mrfmmm.2009.05.003)
84. Pogribny IP, Tryndyak VP, Bagnyukova TV, Melnyk S, Montgomery B, Ross SA, Latendresse JR, Rusyn I, Beland FA. 2009 Hepatic epigenetic phenotype predetermines individual susceptibility to hepatic steatosis in mice fed a lipogenic methyl-deficient diet. J. Hepatol. 51, 176-186. (doi:10.1016/j.jhep. 2009.03.021)
85. Tryndyak VP, Muskhelishvili L, Kovalchuk O, Rodriguez-Juarez R, Montgomery B, Churchwell MI, Ross SA, Beland FA, Pogribny IP. 2006 Effect of long-term tamoxifen exposure on genotoxic and epigenetic changes in rat liver: implications for tamoxifen-induced hepatocarcinogenesis. Carcinogenesis 27, 1713-1720. (doi:10.1093/carcin/bgl050)
86. Pogribny IP, Karpf AR, James SR, Melnyk S, Han T, Tryndyak VP. 2008 Epigenetic alterations in the brains of Fisher 344 rats induced by long-term administration of folate/methyl-deficient diet. Brain Res. 1237, 25-34. (doi:10.1016/j.brainres. 2008.07.077)
87. Pogribny IP, James SJ, Beland FA. 2012 Molecular alterations in hepatocarcinogenesis induced by dietary methyl deficiency. Mol. Nutr. Food Res. 56, 116-125. (doi:10.1002/mnfr.201100524)
88. Waterland RA. 2006 Assessing the effects of high methionine intake on DNA methylation. J. Nutr. 136(Suppl. 6), S1706-S1710.
89. Waterland RA, Lin JR, Smith CA, Jirtle RL. 2006 Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum. Mol. Genet. 15, 705-716. (doi:10.1093/hmg/ddi484)
90. Tian W, Zhao M, Li M, Song T, Zhang M, Quan L, Li S, Sun ZS. 2012 Reversal of cocaine-conditioned place preference through methyl supplementation in mice: altering global DNA methylation in the prefrontal cortex. PLoS ONE 7, e33435. (doi:10.1371/journal.pone.0033435)
91. Waterland RA, Travisano M, Tahiliani KG, Rached MT, Mirza S. 2008 Methyl donor supplementation prevents transgenerational amplification of obesity. Int. J. Obes. (Lond.) 32, 1373-1379. (doi:10.1038/ijo.2008.100)
92. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. 2004 Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854. (doi:10.1038/nn1276)
93. Szyf M, Weaver I, Meaney M. 2007 Maternal care, the epigenome and phenotypic differences in behavior. Reprod. Toxicol. 24, 9-19. (doi:10.1016/j. reprotox.2007.05.001)
94. Hanson M, Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD. 2011 Developmental plasticity and developmental origins of non-communicable disease: theoretical considerations and epigenetic mechanisms. Prog. Biophys. Mol. Biol. 106, 272-280. (doi:10.1016/j.pbiomolbio.2010.12.008)
95. Pervanidou P, Chrousos GP. 2011 Metabolic consequences of stress during childhood and adolescence. Metabolism 61, 611-619. (doi:10. 1016/j.metabol.2011.10.005)
96. Bruce KD, Cagampang FR. 2011 Epigenetic priming of the metabolic syndrome. Toxicol. Mech. Methods 21, 353-361. (doi:10.3109/15376516.2011.559370)
97. Bateson P. 2001 Fetal experience and good adult design. Int. J. Epidemiol. 30, 928-934. (doi:10. 1093/ije/30.5.928)
98. Gluckman PD, Hanson MA. 2004 The developmental origins of the metabolic syndrome. Trends Endocrinol. Metab. 15, 183-187. (doi:10.1016/j. tem.2004.03.002)
99. Gluckman PD, Hanson MA, Spencer HG. 2005 Predictive adaptive responses and human evolution. Trends Ecol. Evol. 20, 527-533. (doi:10.1016/j.tree. 2005.08.001)
100. Budge H, Gnanalingham MG, Gardner DS, Mostyn A, Stephenson T, Symonds ME. 2005 Maternal nutritional programming of fetal adipose tissue development: long-term consequences for later obesity. Birth Defects Res. C 75, 193-199. (doi:10.1002/bdrc.20044)
101. Taylor PD, Poston L. 2007 Developmental programming of obesity in mammals. Exp. Physiol. 92, 287-298. (doi:10.1113/expphysiol. 2005.032854)
102. Samuelsson AM et al. 2008 Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 51, 383-392. (doi:10. 1161/HYPERTENSIONAHA.107.101477)
103. Martinez JA, Cordero P, Campion J, Milagro FI. 2012 Interplay of early-life nutritional programming on obesity, inflammation and epigenetic outcomes. Proc. Nutr. Soc. 71, 276-283. (doi:10.1017/S0029665112000055)
104. Wang J, Wu Z, Li D, Li N, Dindot SV, Satterfield MC, Bazer FW, Wu G. 2012 Nutrition, epigenetics, and metabolic syndrome. Antioxid. Redox Signal. 17, 282-301. (doi:10.1089/ars.2011.4381)
105. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH. 2008 Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl Acad. Sci. USA 105, 17 046-17 049. (doi:10.1073/pnas. 0806560105)
106. Godfrey KM et al. 2011 Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes 60, 1528-1534. (doi:10.2337/db10-0979)
107. Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, Reyes TM. 2010 Maternal high-fat diet alters methylation and gene expression of dopamine and opioidrelated genes. Endocrinology 151, 4756-4764. (doi:10.1210/en.2010-0505)
108. Stevens A, Begum G, Cook A, Connor K, Rumball C, Oliver M, Challis J, Bloomfield F, White A. 2010 Epigenetic changes in the hypothalamic proopiomelanocortin and glucocorticoid receptor genes in the ovine fetus after periconceptional undernutrition. Endocrinology 151, 3652-3664. (doi:10.1210/en.2010-0094)
109. Raychaudhuri N, Raychaudhuri S, Thamotharan M, Devaskar SU. 2008 Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring. J. Biol. Chem. 283, 13 611-13 626. (doi:10.1074/jbc. M800128200)
110. McKay JA, Waltham KJ, Williams EA, Mathers JC. 2011 Folate depletion during pregnancy and lactation reduces genomic DNA methylation in murine adult offspring. Genes Nutr. 6, 189-196. (doi:10.1007/s12263-010-0199-1)
111. Hollingsworth JW et al. 2008 In utero supplementation with methyl donors enhances allergic airway disease in mice. J. Clin. Invest. 118, 3462-3469.
112. Waterland RA, Jirtle RL. 2003 Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell. Biol. 23, 5293-5300. (doi:10.1128/MCB.23.15. 5293-5300.2003)
113. van Montfoort AP, Hanssen LL, de Sutter P, Viville S, Geraedts JP, de Boer P. 2012 Assisted reproduction treatment and epigenetic inheritance. Hum. Reprod. Update 18, 171-197. (doi:10.1093/humupd/dmr047)
114. Zhang S, Rattanatray L, McMillen IC, Suter CM, Morrison JL. 2011 Periconceptional nutrition and the early programming of a life of obesity or adversity. Prog. Biophys. Mol. Biol. 106, 307-314. (doi:10.1016/j.pbiomolbio.2010.12.004)
115. Trottier G, Koski KG, Brun T, Toufexis DJ, Richard D, Walker CD. 1998 Increased fat intake during lactation modifies hypothalamic-pituitary-adrenal responsiveness in developing rat pups: a possible role for leptin. Endocrinology 139, 3704-3711. (doi:10.1210/en.139.9.3704)
116. Stein AD, Lumey LH. 2000 The relationship between maternal and offspring birth weights after maternal prenatal famine exposure: the Dutch Famine Birth Cohort Study. Hum. Biol. 72, 641-654.
117. Kaati G, Bygren LO, Edvinsson S. 2002 Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur. J. Hum. Genet. 10, 682-688. (doi:10.1038/sj.ejhg.5200859)
118. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, Golding J. 2006 Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 14, 159-166. (doi:10.1038/sj.ejhg.5201538)
119. Whitaker RC. 2004 Predicting preschooler obesity at birth: the role of maternal obesity in early pregnancy. Pediatrics 114, e29-e36. (doi:10.1542/peds.114.1.e29)
120. Li M, Sloboda M, Vickers MH. 2011 Maternal obesity and developmental programming of metabolic disorders in offspring: evidence from animal models. Exp. Diabetes Res. 2011, 1-9. (doi:10. 1155/2011/592408)
121. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. 2010 Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467, 963-966. (doi:10.1038/nature09491)
122. Carone BR et al. 2010 Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 1084-1096. (doi:10.1016/j.cell.2010.12.008)
123. Youngson NA, Whitelaw E. 2011 The effects of acquired paternal obesity on the next generation. Asian J. Androl. 13, 195-196. (doi:10.1038/aja. 2010.163)
124. Youngson NA, Whitelaw E. 2008 Transgenerational epigenetic effects. Annu. Rev. Genomics Hum. Genet. 9, 233-257. (doi:10.1146/annurev.genom.9. 081307.164445)
125. Skinner MK. 2008 What is an epigenetic transgenerational phenotype? F3 or F2. Reprod. Toxicol. 25, 2-6. (doi:10.1016/j.reprotox.2007.09.001)
126. Anway MD, Cupp AS, Uzumcu M, Skinner MK. 2005 Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308, 1466-1469. (doi:10.1126/science.1108190)
127. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. 1999 Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23, 314-318. (doi:10. 1038/15490)
128. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV, Whitelaw E. 2003 Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc. Natl Acad. Sci. USA 100, 2538-2543. (doi:10.1073/pnas.0436776100)
129. Cuzin F, Rassoulzadegan M. 2010 Non-Mendelian epigenetic heredity: gametic RNAs as epigenetic regulators and transgenerational signals. Essays Biochem. 48, 101-106. (doi:10.1042/bse0480101)
130. Daxinger L, Whitelaw E. 2012 Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet. 13, 153-162. (doi:10.1038/nrm3288)
131. Daxinger L, Whitelaw E. 2010 Transgenerational epigenetic inheritance: more questions than answers. Genome Res. 20, 1623-1628. (doi:10. 1101/gr.106138.110)
132. Benyshek DC, Johnston CS, Martin JF. 2006 Glucose metabolism is altered in the adequately-nourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 49, 1117-1119. (doi:10.1007/s00125-006-0196-5)
133. Fullston T, Palmer NO, Owens JA, Mitchell M, Bakos HW, Lane M. 2012 Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum. Reprod. 27, 1391-1400. (doi:10.1093/humrep/des030)
134. Dunn GA, Bale TL. 2011 Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152, 2228-2236. (doi:10.1210/en.2010-1461)
135. Dunn GA, Bale TL. 2009 Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 150, 4999-5009. (doi:10.1210/en.2009-0500)
136. Pentinat T, Ramon-Krauel M, Cebria J, Diaz R, Jimenez-Chillaron JC. 2010 Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition. Endocrinology 151, 5617-5623. (doi:10.1210/en.2010-0684)
137. Yazbek SN, Spiezio SH, Nadeau JH, Buchner DA. 2010 Ancestral paternal genotype controls body weight and food intake for multiple generations. Hum. Mol. Genet. 19, 4134-4144. (doi:10.1093/hmg/ddq332)
138. Kobayashi H et al. 2012 Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 8, e1002440. (doi:10.1371/journal.pgen.1002440)
139. Arpanahi A et al. 2009 Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res. 19, 1338-1349. (doi:10. 1101/gr.094953.109)
140. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. 2009 Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478.
141. Brykczynska U et al. 2010 Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17, 679-687. (doi:10.1038/nsmb.1821)
142. Borgel J, Guibert S, Li Y, Chiba H, Schubeler D, Sasaki H, Forne T, Weber M. 2010 Targets and dynamics of promoter DNA methylation during early mouse development. Nat. Genet. 42, 1093-1100. (doi:10.1038/ng.708)
143. Weinstein LS, Xie T, Qasem A, Wang J, Chen M. 2010 The role of GNAS and other imprinted genes in the development of obesity. Int. J. Obes. (Lond.) 34, 6-17. (doi:10.1038/ijo.2009.222)
144. Gallou-Kabani C et al. 2010 Sex-and diet-specific changes of imprinted gene expression and DNA methylation in mouse placenta under a high-fat diet. PLoS ONE 5, e14398. (doi:10.1371/journal. pone.0014398)
145. Stouder C, Paoloni-Giacobino A. 2011 Specific transgenerational imprinting effects of the endocrine disruptor methoxychlor on male gametes. Reproduction 141, 207-216. (doi:10. 1530/REP-10-0400)
146. Stouder C, Paoloni-Giacobino A. 2010 Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm. Reproduction 139, 373-379. (doi:10.1530/REP-09-0340)
147. Stouder C, Deutsch S, Paoloni-Giacobino A. 2009 Superovulation in mice alters the methylation pattern of imprinted genes in the sperm of the offspring. Reprod. Toxicol. 28, 536-541. (doi:10. 1016/j.reprotox.2009.06.009)
148. Radford EJ et al. 2012 An unbiased assessment of the role of imprinted genes in an intergenerational model of developmental programming. PLoS genetics 8, e1002605. (doi:10.1371/journal.pgen. 1002605)