Exposure of neonatal rats to maternal cafeteria feeding during suckling alters hepatic gene expression and DNA methylation in the insulin signalling pathway

Genes and Nutrition

Volumn 9, Issue 1, 2014, Pages

  Daniel, Zoe C ^a   Akyol, Asli ^b   McMullen, Sarah ^a   Langley Evans, Simon C ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b HACETTEPE UNIVERSITY   (Turkey)

Author keywords

Cafeteria diet; Epigenetics; Insulin signalling; Programming

Indexed keywords

INSULIN RECEPTOR SUBSTRATE 2; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTOME;

AKT1 GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; FEMALE; GENE; GENE EXPRESSION; GLUCOSE TOLERANCE; INFANT FEEDING; INSULIN SIGNALLING PATHWAY; IRB GENE; IRS2 GENE; LACTATION; MALE; MATERNAL NUTRITION; NEWBORN; NONHUMAN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA GENE; PROMOTER REGION; PROTEIN EXPRESSION; RAT; SENSITIVITY ANALYSIS; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SUCKLING ANIMAL; WEANING;

ANIMALIA; RATTUS;

EID: 84890367238     PISSN: 15558932     EISSN: 18653499     Source Type: Journal    
DOI: 10.1007/s12263-013-0365-3     Document Type: Article

References (53)

1. Aagaard-Tillery KM, Grove K, Bishop J, Ke X, Fu Q, McKnight R, Lane RH (2008) Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 41:91-102
2. Akyol A, Langley-Evans SC, McMullen S (2009) Obesity induced by cafeteria feeding and pregnancy outcome in the rat. Br J Nutr 102:1601-1610
3. Akyol A, McMullen S, Langley-Evans SC (2012) Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet. Br J Nutr 107:964-978
4. Altobelli G, Bogdarina I, Stupka E, Clark AJC, Langley-Evans SC (2013) Genome-wide methylation and gene expression changes in newborn rats following maternal protein restriction and reversal by folic acid. PLOS One (in press)
5. Austin RM, Langley-Evans SC (2011) Cultured neonatal rat cardiomyocytes display differences in glucose uptake and sensitivity to dexamethasone related to maternal diet. J DOHAD 2:190-194
6. Bayol SA, Simbi BH, Bertrand JA, Stickland NC (2008) Offspring from mothers fed a 'junk food' diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females. J Physiol 586:3219-3230
7. Bayol SA, Simbi BH, Fowkes RC, Stickland NC (2010) A maternal "junk food" diet in pregnancy and lactation promotes nonalcoholic fatty liver disease in rat offspring. Endocrinology 151:1451-1461
8. Bogdarina I, Haase A, Langley-Evans SC, Clark AJ (2010) Glucocorticoid effects on the programming of AT1b angiotensin receptor gene methylation and expression in the rat. PLoS ONE 5(2):e9237
9. Buettner R, Scholmerich J, Bollheimer LC (2007) High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity 15:798-808
10. Burdge GC, Lillycrop KA, Phillips ES, Slater-Jefferies JL, Jackson AA, Hanson MA (2009) Folic acid supplementation during the juvenile-pubertal period in rats modifies the phenotype and epigenotype induced by prenatal nutrition. J Nutr 139:1054-1060
11. Carlin J, George R, Reyes TM (2013) Methyl donor supplementation blocks the adverse effects of maternal high fat diet on offspring physiology. PLoS ONE 8:e63549
12. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE et al (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084-1096
13. Chen YW, Kao HY, Min MY, Lai WS (2013). A Sex- and Region-Specific Role of Akt1 in the Modulation of Methamphetamine-Induced Hyperlocomotion and Striatal Neuronal Activity: Implications in Schizophrenia and Methamphetamine-Induced Psychosis. Schizophr Bull (in press)
14. Crozier SR, Robinson SM, Borland SE, Inskip HM, SWS Study Group (2006) Dietary patterns in the Southampton Women's Survey. Eur J Clin Nutr 60:1391-1399
15. Duan SZ, Usher MG, Foley EL 4th, Milstone DS, Brosius FC 3rd, Mortensen RM (2010) Sex dimorphic actions of rosiglitazone in generalised peroxisome proliferator-activated receptor-gamma (PPAR-gamma)-deficient mice. Diabetologia 53:1493-1505
16. Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin MS, Hales CN, Ozanne SE (2005) Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol 288:R368-R373
17. Floyd ZE, Stephens JM (2012) Controlling a master switch of adipocyte development and insulin sensitivity: covalent modifications of PPARγ. Biochim Biophys Acta 1822:1090-10955
18. Foryst-Ludwig A, Kreissl MC, Sprang C, Thalke B, Böhm C, Benz V, Gürgen D, Dragun D, Schubert C, Mai K, Stawowy P, Spranger J, Regitz-Zagrosek V, Unger T, Kintscher U (2011) Sex differences in physiological cardiac hypertrophy are associated with exercise-mediated changes in energy substrate availability. Am J Physiol Heart Circ Physiol 301:H115-H122
19. Gambling L, Dunford S, Wallace DI, Zuur G, Solanky N, Srai SK, McArdle HJ (2003) Iron deficiency during pregnancy affects postnatal blood pressure in the rat. J Physiol 552:603-610
20. Jacobsen SC, Brøns C, Bork-Jensen J, Ribel-Madsen R, Yang B, Lara E, Hall E, Calvanese V, Nilsson E, Jørgensen SW, Mandrup S, Ling C, Fernandez AF, Fraga MF, Poulsen P, Vaag A (2012) Effects of short-term high-fat overfeeding on genome-wide DNA methylation in the skeletal muscle of healthy young men. Diabetologia 55:3341-3349
21. Kadowaki K, Fukino K, Negishi E, Ueno K (2007) Sex differences in PPARgamma expressions in rat adipose tissues. Biol Pharm Bull 30:818-820
22. Kahn A (1997) Transcriptional regulation by glucose in the liver. Biochimie 79:113-118
23. Kant AK (2004) Dietary patterns and health outcomes. J Am Diet Assoc 104:615-635
24. Langie SA, Achterfeldt S, Gorniak JP, Halley-Hogg KJ, Oxley D, van Schooten FJ, Godschalk RW, McKay JA, Mathers JC (2013) Maternal folate depletion and high-fat feeding from weaning affects DNA methylation and DNA repair in brain of adult offspring. FASEB J27:3323-3334
25. Langley SC, Jackson AA (1994) Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci 86:217-222
26. Langley-Evans SC, Welham SJ, Jackson AA (1999) Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 64:965-974
27. Lillycrop KA, Burdge GC (2011) Epigenetic changes in early life and future risk of obesity. Int J Obes 35:72-83
28. Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC (2007) Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 97:1064-1073
29. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
30. Masaki T, Chiba S, Noguchi H, Yasuda T, Tobe K, Suzuki R, Kadowaki T, Yoshimatsu H (2004) Obesity in insulin receptor substrate-2-deficient mice: disrupted control of arcuate nucleus neuropeptides. Obes Res 12:878-885
31. McMullen S, Langley-Evans SC (2010) The developmental origins of adult disease. Med Princ Pract 19:87-98
32. Menendez-Gutierrez MP, Roszer T, Ricote M (2012) Biology and therapeutic applications of peroxisome proliferator-activated receptors. Curr Top Med Chem 12:548-584
33. Rothwell NJ, Stock MJ (1979) Regulation of energy balance in two models of reversible obesity in the rat. J Comp Physiol Psychol 93:1024-1034
34. Ryan KJP, Elmes MJ, Gardner DS, Langley-Evans SC (2012) The effects of prenatal protein restriction on ß-adrenergic signalling of the adult rat heart during ischaemia. J Nutr Metab 12:397389
35. Sampey BP, Vanhoose AM, Winfield HM, Freemerman AJ, Muehlbauer MJ, Fueger PT, Newgard CB, Makowski L (2011) Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity 19:1109-1117
36. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EH, Piersma AH, Ozanne SE, Twinn DF, Remacle C, Rowlerson A, Poston L, Taylor PD (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
37. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473:337-342
38. Seki Y, Williams L, Vuguin PM, Charron MJ (2012) Minireview: epigenetic programming of diabetes and obesity: animal models. Endocrinology 153:1031-1038
39. Shankar K, Harrell A, Liu X, Gilchrist JM, Ronis MJ, Badger TM (2008) Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 294:R528-R538
40. 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 (2007) DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA 104:19351-19356
41. Swali A, McMullen S, Hayes H, Gambling L, McArdle H, Langley-Evans SC (2011) Cell cycle regulation and cytoskeletal remodelling are critical processes in the nutritional programming of embryonic development. PLoS ONE 6:e23189
42. Swali A, McMullen S, Hayes H, Gambling L, McArdle HJ, Langley-Evans SC (2012) Processes underlying the nutritional programming of embryonic development by iron deficiency in the rat. PLoS ONE 7:e48133
43. Szyf M (2009) The early life environment and the epigenome. Biochim Biophys Acta 1790:878-885
44. Torrens C, Hanson MA, Gluckman PD, Vickers MH (2009) Maternal undernutrition leads to endothelial dysfunction in adult male rat offspring independent of postnatal diet. Br J Nutr 101:27-33
45. Viana Abranches M, Esteves de Oliveira FC, Bressan J (2011) Peroxisome proliferator-activated receptor: effects on nutritional homeostasis, obesity and diabetes mellitus. Nutr Hosp 26:271-279
46. Vickers MH, Breier BH, McCarthy D, Gluckman PD (2003) Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. Am J Physiol Regul Integr Comp Physiol 285:R271-R273
47. Vogel C, Abreu Rde S, Ko D, Le SY, Shapiro BA, Burns SC, Sandhu D, Boutz DR, Marcotte EM, Penalva LO (2010) Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol Syst Biol 6:400
48. Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, Reyes TM (2010) Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151:4756-4764
49. Vucetic Z, Kimmel J, Reyes TM (2011) Chronic high-fat diet drives postnatal epigenetic regulation of μ-opioid receptor in the brain. Neuropsychopharmacology 36:1199-1206
50. Wright T, Langley-Evans SC, Voigt JP (2011a) The impact of maternal cafeteria diet on anxiety-related behaviour and exploration in the offspring. Physiology and Behaviour 103:164-172
51. Wright T, Fone K, Langley-Evans SC, Voigt JP (2011b) Exposure to maternal consumption of cafeteria diet during the lactation period programmes feeding behaviour in the rat. Int J Develop Neurosci 29:785-793
52. Yates Z, Tarling EJ, Langley-Evans SC, Salter AM (2008) Maternal undernutrition programmes atherosclerosis in the Apo E*3 Leiden mouse. Br J Nutr 101:1185-1194
53. Zhou Z, Yuan Q, Mash DC, Goldman D (2011) Substance-specific and shared transcription and epigenetic changes in the human hippocampus chronically exposed to cocaine and alcohol. Proc Natl Acad Sci USA 108:6626-6631