Epigenetic programming of reward function in offspring: a role for maternal diet

Alexandre-Gouabau MC, Bailly E, Moyon TL, Grit IC, Coupé B, Drean GL, Rogniaux HJ, Parnet P (2012) Postnatal growth velocity modulates alterations of proteins involved in metabolism and neuronal plasticity in neonatal hypothalamus in rats born with intrauterine growth restriction. J Nutr Biochem 23:140–152 Arnold AP, Chen X (2009) What does the “four core genotypes” mouse model tell us about sex differences in the brain and other tissues? Front Neuroendocrinol 30:1–9 Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM, Nemeroff CB, Reyes TM, Simerly RB, Susser ES, Nestler EJ (2010) Early life programming and neurodevelopmental disorders. Biol Psychiatry 68:314–319 Begum G, Stevens A, Smith EB, Connor K, Challis JR, Bloomfield F, White A (2012) Epigenetic changes in fetal hypothalamic energy regulating pathways are associated with maternal undernutrition and twinning. FASEB J 26:1694–1703 Bocarsly ME, Barson JR, Hauca JM, Hoebel BG, Leibowitz SF, Avena NM (2012) Effects of perinatal exposure to palatable diets on body weight and sensitivity to drugs of abuse in rats. Physiol Behav 107:568–575 Bohacek J, Gapp K, Saab BJ, Mansuy IM (2013) Transgenerational epigenetic effects on brain functions. Biol Psychiatry 73:313–320 Butler JS, Koutelou E, Schibler AC, Dent SY (2012) Histone-modifying enzymes: regulators of developmental decisions and drivers of human disease. Epigenomics 4:163–177 Carlin J, George R, Reyes TM (2013) Methyl donor supplementation blocks the adverse effects of maternal high fat diet on offspring physiology. PLoS One 85:e63549 Caron E, Ciofi P, Prevot V, Bouret SG (2012) Alteration in neonatal nutrition causes perturbations in hypothalamic neural circuits controlling reproductive function. J Neurosci 32:11486–11494 Chen PY, Ganguly A, Rubbi L, Orozco LD, Morselli M, Ashraf D, Jaroszewicz A, Feng S, Jacobsen SE, Nakano A, Devaskar SU, Pellegrini M (2013) Intrauterine calorie restriction affects placental DNA methylation and gene expression. Physiol Genomics 45:565–576 Clarke M, Cai G, Saleh S, Buller KM, Spencer SJ (2013) Being suckled in a large litter mitigates the effects of early life stress on HPA axis function in the rat. J Neuroendocrinol 25(9):792–802 Coupé B, Dutriez-Casteloot I, Breton C, Lefèvre F, Mairesse J, Dickes-Coopman A, Silhol M, Tapia-Arancibia L, Lesage J, Vieau D (2009) Perinatal undernutrition modifies cell proliferation and brain-derived neurotrophic factor levels during critical time-windows for hypothalamic and hippocampal development in the male rat. J Neuroendocrinol 21:40–48 Cox KH, Rissman EF (2011) Sex differences in juvenile mouse social behavior are influenced by sex chromosomes and social context. Genes Brain Behav 10:465–472 da Silva AA, Borba TK, de Almeida Lira L, Cavalcante TC, de Freitas MF, Leandro CG, do Nascimento E, de Souza SL (2013) Perinatal undernutrition stimulates seeking food reward. Int J Dev Neurosci 31:334–341 Day JJ, Sweatt JD (2010) DNA methylation and memory formation. Nat Neurosci 13:1319–1323 Dunn GA, Bale TL (2009) Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 150:4999–5009 Dunn GA, Bale TL (2011) Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152:2228–2236 Fullston T, Teague EM, Palmer NO, Deblasio MJ, Mitchell M, Corbett M, Print CG, Owens JA, Lane M (2013) Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J 27(10):4226–4243 Gabory A, Attig L, Junien C (2011) Developmental programming and epigenetics. Am J Clin Nutr 94:1943S–1952S Gabory A, Ferry L, Fajardy I, Jouneau L, Gothié JD, Vigé A, Fleur C, Mayeur S, Gallou-Kabani C, Gross MS, Attig L, Vambergue A, Lesage J, Reusens B, Vieau D, Remacle C, Jais JP, Junien C (2012) Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLoS One 7:e47986 Gallou-Kabani C, Gabory A, Tost J, Karimi M, Mayeur S, Lesage J, Boudadi E, Gross MS, Taurelle J, Vigé A, Breton C, Reusens B, Remacle C, Vieau D, Ekström TJ, Jais JP, Junien C (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 Goyal R, Goyal D, Leitzke A, Gheorghe CP, Longo LD (2010) Brain renin-angiotensin system: fetal epigenetic programming by maternal protein restriction during pregnancy. Reprod Sci 17:227–238 Gräff J, Tsai LH (2013) Histone acetylation: molecular mnemonics on the chromatin. Nat Rev Neurosci 14:97–111 Grissom NM, Reyes TM (2013) Gestational overgrowth and undergrowth affect neurodevelopment: similarities and differences from behavior to epigenetics. Int J Dev Neurosci 31(6):406–414 Grissom NM, Lyde R, Christ L, Sasson IE, Carlin J, Vitins AP, Simmons RA, Reyes TM (2013) Obesity at conception programs the opioid system in the offspring brain. Neuropsychopharmacology doi: 10.1038/npp.2013.193 Grossniklaus U, Kelly B, Ferguson-Smith AC, Pembrey M, Lindquist S (2013) Transgenerational epigenetic inheritance: how important is it? Nat Rev Genet 14:228–235 Guest PC, Urday S, Ma D, Stelzhammer V, Harris LW, Amess B, Pietsch S, Oheim C, Ozanne SE, Bahn S (2012) Proteomic analysis of the maternal protein restriction rat model for schizophrenia: identification of translational changes in hormonal signaling pathways and glutamate neurotransmission. Proteomics 12:3580–3589 Hager R, Cheverud JM, Wolf JB (2009) Change in maternal environment induced by cross-fostering alters genetic and epigenetic effects on complex traits in mice. Proc Biol Sci 276:2949–2954 Hutnick LK, Golshani P, Namihira M, Xue Z, Matynia A, Yang XW, Silva AJ, Schweizer FE, Fan G (2009) DNA hypomethylation restricted to the murine forebrain induces cortical degeneration and impairs postnatal neuronal maturation. Hum Mol Genet 18:2875–2888 Jimenez-Chillaron JC, Isganaitis E, Charalambous M, Gesta S, Pentinat-Pelegrin T, Faucette RR, Otis JP, Chow A, Diaz R, Ferguson-Smith A, Patti ME (2009) Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 58:460–468 Karlić R, Chung HR, Lasserre J, Vlahovicek K, Vingron M (2010) Histone modification levels are predictive for gene expression. Proc Natl Acad Sci USA 107:2926–2931 Kofink D, Boks MP, Timmers HT, Kas MJ (2013) Epigenetic dynamics in psychiatric disorders: environmental programming of neurodevelopmental processes. Neurosci Biobehav Rev 37:831–845 Lim JP, Brunet A (2013) Bridging the transgenerational gap with epigenetic memory. Trends Genet 29:176–186 Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA, Johnson ND, Lucero J, Huang Y, Dwork AJ, Schultz MD, Yu M, Tonti-Filippini J, Heyn H, Hu S, Wu JC, Rao A, Esteller M, He C, Haghighi FG, Sejnowski TJ, Behrens MM, Ecker JR (2013) Global epigenomic reconfiguration during mammalian brain development. Science 341(6146):1237905 Livy DJ, Miller EK, Maier SE, West JR (2003) Fetal alcohol exposure and temporal vulnerability: effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicol Teratol 25:447–458 Morganstern I, Lukatskaya O, Moon SH, Guo WR, Shaji J, Karatayev O, Leibowitz SF (2013) Stimulation of nicotine reward and central cholinergic activity in Sprague-Dawley rats exposed perinatally to a fat-rich diet. Psychopharmacology (Berl) Doi: 10.1007/s00213-013-3178-6 Naef L, Srivastava L, Gratton A, Hendrickson H, Owens SM, Walker CD (2008) Maternal high fat diet during the perinatal period alters mesocorticolimbic dopamine in the adult rat offspring: reduction in the behavioral responses to repeated amphetamine administration. Psychopharmacology (Berl) 197:83–94 Naef L, Moquin L, Bo GD, Giros B, Gratton A, Walker CD (2011) Maternal high-fat intake alters presynaptic regulation of dopamine in the nucleus accumbens and increases motivation for fat rewards in the offspring. Neuroscience 176:225–236 Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ (2010) Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 467:963–966 Nicholas LM, Rattanatray L, Maclaughlin SM, Ozanne SE, Kleemann DO, Walker SK, Morrison JL, Zhang S, Muhlhäusler BS, Martin-Gronert MS, McMillen IC (2013) Differential effects of maternal obesity and weight loss in the periconceptional period on the epigenetic regulation of hepatic insulin-signaling pathways in the offspring. FASEB J 27(9):3786–3796 Ong ZY, Muhlhausler BS (2011) Maternal “junk-food” feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. FASEB J 25:2167–2179 Pan S, Zheng Y, Zhao R, Yang X (2013) MicroRNA-130b and microRNA-374b mediate the effect of maternal dietary protein on offspring lipid metabolism in Meishan pigs. Br J Nutr 109:1731–1738 Parra P, Serra F, Palou A (2010) Expression of adipose microRNAs is sensitive to dietary conjugated linoleic acid treatment in mice. PLoS One 5:e13005 Penn NW (1976) Modification of brain deoxyribonucleic acid base content with maturation in normal and malnourished rats. Biochem J 155:709–712 Pinney SE, Simmons RA (2010) Epigenetic mechanisms in the development of type 2 diabetes. Trends Endocrinol Metab 21:223–229 Plagemann A, Harder T, Brunn M, Harder A, Roepke K, Wittrock-Staar M, Ziska T, Schellong K, Rodekamp E, Melchior K, Dudenhausen JW (2009) Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: an epigenetic model of obesity and the metabolic syndrome. J Physiol 587:4963–4976 Qureshi IA, Mehler MF (2012) Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nat Rev Neurosci 13:528–541 Resnick O, Morgane PJ, Hasson R, Miller M (1982) Overt and hidden forms of chronic malnutrition in the rat and their relevance to man. Neurosci Biobehav Rev 6:55–75 Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL (2013) Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci 33:9003–9012 Roth TL (2012) Epigenetics of neurobiology and behavior during development and adulthood. Dev Psychobiol 54:590–597 Sartor GC, St Laurent G 3rd, Wahlestedt C (2012) The emerging role of non-coding RNAs in drug addiction. Front Genet 3:106 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 Tamashiro KL, Moran TH (2010) Perinatal environment and its influences on metabolic programming of offspring. Physiol Behav 100:560–566 Tonkiss J, Shukitt-Hale B, Formica RN, Rocco FJ, Galler JR (1990) Prenatal protein malnutrition alters response to reward in adult rats. Physiol Behav 48:675–680 Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC (2013) Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 16:42–47 Viana LC, Lima CM, Oliveira MA, Borges RP, Cardoso TT, Almeida IN, Diniz DG, Bento-Torres J, Pereira A, Batista-de-Oliveira M, Lopes AA, Silva RF, Abadie-Guedes R, Santos AAD, Lima DS, Vasconcelos PF, Cunningham C, Guedes RC, Picanço-Diniz CW (2013) Litter size, age-related memory impairments, and microglial changes in rat dentate gyrus: stereological analysis and three dimensional morphometry. Neuroscience 238:280–296 Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, Reyes TM (2010a) Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151:4756–4764 Vucetic Z, Totoki K, Schoch H, Whitaker KW, Hill-Smith T, Lucki I, Reyes TM (2010b) Early life protein restriction alters dopamine circuitry. Neuroscience 168:359–370 Wang J, Cui Q (2012) Specific roles of microRNAs in their interactions with environmental factors. J Nucleic Acids 2012:978384