Early life nutrition, epigenetics and programming of later life disease

Nutrients

Volumn 6, Issue 6, 2014, Pages 2165-2178

  Vickers, Mark H ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Developmental programming; DNA methylation; Epigenetics; Maternal nutrition; Transgenerational

Indexed keywords

CHOLINE; CYANOCOBALAMIN; FOLIC ACID; GLUCOCORTICOID RECEPTOR; GLUCOSE TRANSPORTER 4; HISTONE H3; LEPTIN; MESSENGER RNA; MICRORNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; RNA H19; SOMATOMEDIN B RECEPTOR; SOMATOMEDIN C RECEPTOR; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRANSCRIPTION FACTOR PDX 1;

ARTICLE; CPG ISLAND; DEVELOPMENTAL DISORDER; DIABETES MELLITUS; DIET SUPPLEMENTATION; DISEASE TRANSMISSION; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; INTRAUTERINE GROWTH RETARDATION; LIFESTYLE; MATERNAL NUTRITION; META ANALYSIS (TOPIC); MOLECULAR EPIDEMIOLOGY; NONHUMAN; NUTRITIONAL DISORDER; OBESITY; PHENOTYPE; PREGNANCY; AGING; FEMALE; GENETICS; INFANT; INFANT NUTRITION; METABOLIC DISEASES;

AGING; EPIGENOMICS; FEMALE; HUMANS; INFANT; INFANT NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; METABOLIC DISEASES; PREGNANCY;

EID: 84901934284     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu6062165     Document Type: Article

References (78)

1. Gluckman, P.D.; Hanson, M.A.; Beedle, A.S.; Spencer, H.G. Predictive adaptive responses in perspective. Trends Endocrinol. Metab. 2008, 19, 109-110.
2. Fernandez-Twinn, D.S.; Ozanne, S.E. Early life nutrition and metabolic programming. Ann. N. Y. Acad. Sci. 2010, 1212, 78-96.
3. Jang, H.; Serra, C. Nutrition, epigenetics, and diseases. Clin. Nutr. Res. 2014, 3, 1-8.
4. Sinclair, K.D.; Allegrucci, C.; Singh, R.; Gardner, D.S.; Sebastian, S.; Bispham, J.; Thurston, A.; Huntley, J.F.; Rees, W.D.; Maloney, C.A., et al. 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, 19351-19356.
5. Lillycrop, K.A.; Phillips, E.S.; Jackson, A.A.; Hanson, M.A.; Burdge, G.C. 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, 1382-1386.
6. Murphy, S.K.; Jirtle, R.L. Imprinting evolution and the price of silence. Bioessays 2003, 25, 577-588.
7. Waterland, R.A.; Lin, J.R.; Smith, C.A.; Jirtle, R.L. Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum. Mol. Genet. 2006, 15, 705-716.
8. Jirtle, R.L.; Skinner, M.K. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 2007, 8, 253-262.
9. Pham, T.D.; MacLennan, N.K.; Chiu, C.T.; Laksana, G.S.; Hsu, J.L.; Lane, R.H. Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 285, R962-R970.
10. Bogdarina, I.; Welham, S.; King, P.J.; Burns, S.P.; Clark, A.J. Epigenetic modification of the renin-angiotensin system in the fetal programming of hypertension. Circ. Res. 2007, 100, 520-526.
11. Weaver, I.C.; Cervoni, N.; Champagne, F.A.; D'Alessio, A.C.; Sharma, S.; Seckl, J.R.; Dymov, S.; Szyf, M.; Meaney, M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7, 847-854.
12. Dudley, K.J.; Sloboda, D.M.; Connor, K.L.; Beltrand, J.; Vickers, M.H. Offspring of mothers fed a high fat diet display hepatic cell cycle inhibition and associated changes in gene expression and DNA methylation. PLoS One 2011, 6, e21662.
13. Wolffe, A.P. Packaging principle: How DNA methylation and histone acetylation control the transcriptional activity of chromatin. J. Exp. Zool. 1998, 282, 239-244.
14. Callinan, P.A.; Feinberg, A.P. The emerging science of epigenomics. Hum. Mol. Genet. 2006, 15, R95-R101.
15. Delage, B.; Dashwood, R.H. Dietary manipulation of histone structure and function. Annu. Rev. Nutr. 2008, 28, 347-366.
16. Iorio, M.V.; Piovan, C.; Croce, C.M. Interplay between microRNAs and the epigenetic machinery: An intricate network. Biochim. Biophys. Acta 2010, 1799, 694-701.
17. Silva, A.J.; White, R. Inheritance of allelic blueprints for methylation patterns. Cell 1988, 54, 145-152.
18. Fraga, M.F.; Ballestar, E.; Paz, M.F.; Ropero, S.; Setien, F.; Ballestar, M.L.; Heine-Suner, D.; Cigudosa, J.C.; Urioste, M.; Benitez, J., et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. USA 2005, 102, 10604-10609.
19. Kaminsky, Z.; Wang, S.C.; Petronis, A. Complex disease, gender and epigenetics. Ann. Med. 2006, 38, 530-544.
20. Heijmans, B.T.; Tobi, E.W.; Stein, A.D.; Putter, H.; Blauw, G.J.; Susser, E.S.; Slagboom, P.E.; Lumey, L.H. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. USA 2008, 105, 17046-17049.
21. Tobi, E.W.; Lumey, L.H.; Talens, R.P.; Kremer, D.; Putter, H.; Stein, A.D.; Slagboom, P.E.; Heijmans, B.T. DNA methylation differences after exposure to prenatal famine are common and timing-and sex-specific. Hum. Mol. Genet. 2009, 18, 4046-4053.
22. McMillen, I.C.; MacLaughlin, S.M.; Muhlhausler, B.S.; Gentili, S.; Duffield, J.L.; Morrison, J.L. Developmental origins of adult health and disease: The role of periconceptional and foetal nutrition. Basic Clin. Pharmacol. Toxicol. 2008, 102, 82-89.
23. McKay, J.A.; Groom, A.; Potter, C.; Coneyworth, L.J.; Ford, D.; Mathers, J.C.; Relton, C.L. Genetic and non-genetic influences during pregnancy on infant global and site specific DNA methylation: Role for folate gene variants and vitamin B12. PLoS One 2012, 7, e33290.
24. Soubry, A.; Murphy, S.K.; Wang, F.; Huang, Z.; Vidal, A.C.; Fuemmeler, B.F.; Kurtzberg, J.; Murtha, A.; Jirtle, R.L.; Schildkraut, J.M.; et al. Newborns of obese parents have altered DNA methylation patterns at imprinted genes. Int. J. Obes. (Lond.) 2013, doi:10.1038/ijo.2013.193.
25. Soubry, A.; Schildkraut, J.M.; Murtha, A.; Wang, F.; Huang, Z.; Bernal, A.; Kurtzberg, J.; Jirtle, R.L.; Murphy, S.K.; Hoyo, C. Paternal obesity is associated with IGF2 hypomethylation in newborns: Results from a Newborn Epigenetics Study (NEST) cohort. BMC Med. 2013, 11, 29.
26. Gicquel, C.; El-Osta, A.; Le Bouc, Y. Epigenetic regulation and fetal programming. Best Pract. Res. Clin. Endocrinol. Metab. 2008, 22, 1-16.
27. MacLennan, N.K.; James, S.J.; Melnyk, S.; Piroozi, A.; Jernigan, S.; Hsu, J.L.; Janke, S.M.; Pham, T.D.; Lane, R.H. Uteroplacental insufficiency alters DNA methylation, one-carbon metabolism, and histone acetylation in IUGR rats. Physiol. Genomics 2004, 18, 43-50.
28. Vanhees, K.; Vonhogen, I.G.; van Schooten, F.J.; Godschalk, R.W. You are what you eat, and so are your children: The impact of micronutrients on the epigenetic programming of offspring. Cell. Mol. Life Sci. 2014, 71, 271-285.
29. Lie, S.; Morrison, J.L.; Williams-Wyss, O.; Suter, C.M.; Humphreys, D.T.; Ozanne, S.E.; Zhang, S.; Maclaughlin, S.M.; Kleemann, D.O.; Walker, S.K., et al. Periconceptional undernutrition programs changes in insulin-signaling molecules and microRNAs in skeletal muscle in singleton and twin fetal sheep. Biol. Reprod. 2014, 90, 5.
30. Cho, C.E.; Sanchez-Hernandez, D.; Reza-Lopez, S.A.; Huot, P.S.; Kim, Y.I.; Anderson, G.H. High folate gestational and post-weaning diets alter hypothalamic feeding pathways by DNA methylation in Wistar rat offspring. Epigenetics 2013, 8, 710-719.
31. Lillycrop, K.A.; Slater-Jefferies, J.L.; Hanson, M.A.; Godfrey, K.M.; Jackson, A.A.; Burdge, G.C. 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. 2007, 97, 1064-1073.
32. Burdge, G.C.; Lillycrop, K.A.; Jackson, A.A.; Gluckman, P.D.; Hanson, M.A. The nature of the growth pattern and of the metabolic response to fasting in the rat are dependent upon the dietary protein and folic acid intakes of their pregnant dams and post-weaning fat consumption. Br. J. Nutr. 2007, 99, 540-549.
33. Hoile, S.P.; Lillycrop, K.A.; Grenfell, L.R.; Hanson, M.A.; Burdge, G.C. Increasing the folic acid content of maternal or post-weaning diets induces differential changes in phosphoenolpyruvate carboxykinase mRNA expression and promoter methylation in rats. Br. J. Nutr. 2012, 108, 852-857.
34. Zeisel, S.H. Importance of methyl donors during reproduction. Am. J. Clin. Nutr. 2009, 89, 673S-677S.
35. Davison, J.M.; Mellott, T.J.; Kovacheva, V.P.; Blusztajn, J.K. Gestational choline supply regulates methylation of histone H3, expression of histone methyltransferases G9a (Kmt1c) and Suv39h1 (Kmt1a), and DNA methylation of their genes in rat fetal liver and brain. J. Biol. Chem. 2009, 284, 1982-1989.
36. Zinkhan, E.K.; Fu, Q.; Wang, Y.; Yu, X.; Callaway, C.W.; Segar, J.L.; Scholz, T.D.; McKnight, R.A.; Joss-Moore, L.; Lane, R.H. Maternal hyperglycemia disrupts histone 3 lysine 36 trimethylation of the IGF-1 gene. J. Nutr. Metab. 2012, 2012, 930364.
37. Fu, Q.; McKnight, R.A.; Yu, X.; Wang, L.; Callaway, C.W.; Lane, R.H. Uteroplacental insufficiency induces site-specific changes in histone H3 covalent modifications and affects DNA-histone H3 positioning in day 0 IUGR rat liver. Physiol. Genomics 2004, 20, 108-116.
38. Tosh, D.N.; Fu, Q.; Callaway, C.W.; McKnight, R.A.; McMillen, I.C.; Ross, M.G.; Lane, R.H.; Desai, M. Epigenetics of programmed obesity: Alteration in IUGR rat hepatic IGF1 mRNA expression and histone structure in rapid vs. delayed postnatal catch-up growth. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G1023-G1029.
39. Park, J.H.; Stoffers, D.A.; Nicholls, R.D.; Simmons, R.A. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J. Clin. Investig. 2008, 118, 2316-2324.
40. Raychaudhuri, N.; Raychaudhuri, S.; Thamotharan, M.; Devaskar, S.U. Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring. J. Biol. Chem. 2008, 283, 13611-13626.
41. Dolinoy, D.C.; Weidman, J.R.; Waterland, R.A.; Jirtle, R.L. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ. Health Perspect. 2006, 114, 567-572.
42. Waterland, R.A.; Michels, K.B. Epigenetic epidemiology of the developmental origins hypothesis. Annu. Rev. Nutr. 2007, 27, 363-388.
43. Waterland, R.A.; Dolinoy, D.C.; Lin, J.R.; Smith, C.A.; Shi, X.; Tahiliani, K.G. Maternal methyl supplements increase offspring DNA methylation at Axin Fused. Genesis 2006, 44, 401-406.
44. Liu, H.W.; Mahmood, S.; Srinivasan, M.; Smiraglia, D.J.; Patel, M.S. Developmental programming in skeletal muscle in response to overnourishment in the immediate postnatal life in rats. J. Nutr. Biochem. 2013, 24, 1859-1869.
45. Marco, A.; Kisliouk, T.; Weller, A.; Meiri, N. High fat diet induces hypermethylation of the hypothalamic Pomc promoter and obesity in post-weaning rats. Psychoneuroendocrinology 2013, 38, 2844-2853.
46. Hoile, S.P.; Irvine, N.A.; Kelsall, C.J.; Sibbons, C.; Feunteun, A.; Collister, A.; Torrens, C.; Calder, P.C.; Hanson, M.A.; Lillycrop, K.A., et al. Maternal fat intake in rats alters 20, 4n-6 and 22, 6n-3 status and the epigenetic regulation of Fads2 in offspring liver. J. Nutr. Biochem. 2013, 24, 1213-1220.
47. Vucetic, Z.; Kimmel, J.; Totoki, K.; Hollenbeck, E.; Reyes, T.M. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 2010, 151, 4756-4764.
48. Aagaard-Tillery, K.M.; Grove, K.; Bishop, J.; Ke, X.; Fu, Q.; McKnight, R.; Lane, R.H. Developmental origins of disease and determinants of chromatin structure: Maternal diet modifies the primate fetal epigenome. J. Mol. Endocrinol. 2008, 41, 91-102.
49. Strakovsky, R.S.; Zhang, X.; Zhou, D.; Pan, Y.X. The regulation of hepatic Pon1 by a maternal high-fat diet is gender specific and may occur through promoter histone modifications in neonatal rats. J. Nutr. Biochem. 2014, 25, 170-176.
50. Suter, M.A.; Chen, A.; Burdine, M.S.; Choudhury, M.; Harris, R.A.; Lane, R.H.; Friedman, J.E.; Grove, K.L.; Tackett, A.J.; Aagaard, K.M. A maternal high-fat diet modulates fetal SIRT1 histone and protein deacetylase activity in nonhuman primates. FASEB J. 2012, 26, 5106-5114.
51. Tan, Y.; Zhang, B.; Wu, T.; Skogerbo, G.; Zhu, X.; Guo, X.; He, S.; Chen, R. Transcriptional inhibiton of Hoxd4 expression by miRNA-10a in human breast cancer cells. BMC Mol. Biol. 2009, 10, 12.
52. Hawkins, P.G.; Morris, K.V. RNA and transcriptional modulation of gene expression. Cell Cycle 2008, 7, 602-607.
53. Yan, X.; Huang, Y.; Zhao, J.X.; Rogers, C.J.; Zhu, M.J.; Ford, S.P.; Nathanielsz, P.W.; Du, M. Maternal obesity downregulates microRNA let-7g expression, a possible mechanism for enhanced adipogenesis during ovine fetal skeletal muscle development. Int. J. Obes. (Lond.) 2013, 37, 568-575.
54. Vickers, M.H.; Gluckman, P.D.; Coveny, A.H.; Hofman, P.L.; Cutfield, W.S.; Gertler, A.; Breier, B.H.; Harris, M. Neonatal leptin treatment reverses developmental programming. Endocrinology 2005, 146, 4211-4216.
55. Gluckman, P.D.; Lillycrop, K.A.; Vickers, M.H.; Pleasants, A.B.; Phillips, E.S.; Beedle, A.S.; Burdge, G.C.; Hanson, M.A. Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc. Natl. Acad. Sci. USA 2007, 104, 12796-12800.
56. Holness, M.J.; Sugden, M.C. Epigenetic regulation of metabolism in children born small for gestational age. Curr. Opin. Clin. Nutr. Metab. Care 2006, 9, 482-488.
57. Iliopoulos, D.; Malizos, K.N.; Tsezou, A. Epigenetic regulation of leptin affects MMP-13 expression in osteoarthritic chondrocytes: Possible molecular target for osteoarthritis therapeutic intervention. Ann. Rheum. Dis. 2007, 66, 1616-1621.
58. Melzner, I.; Scott, V.; Dorsch, K.; Fischer, P.; Wabitsch, M.; Bruderlein, S.; Hasel, C.; Moller, P. Leptin gene expression in human preadipocytes is switched on by maturation-induced demethylation of distinct CpGs in its proximal promoter. J. Biol. Chem. 2002, 277, 45420-45427.
59. Stoger, R. In vivo methylation patterns of the leptin promoter in human and mouse. Epigenetics 2006, 1, 155-162.
60. Palou, M.; Pico, C.; McKay, J.A.; Sanchez, J.; Priego, T.; Mathers, J.C.; Palou, A. Protective effects of leptin during the suckling period against later obesity may be associated with changes in promoter methylation of the hypothalamic pro-opiomelanocortin gene. Br. J. Nutr. 2011, 106, 769-778.
61. Yokomori, N.; Tawata, M.; Onaya, T. DNA demethylation modulates mouse leptin promoter activity during the differentiation of 3T3-L1 cells. Diabetologia 2002, 45, 140-148.
62. Yokomori, N.; Tawata, M.; Onaya, T. DNA demethylation during the differentiation of 3T3-L1 cells affects the expression of the mouse GLUT4 gene. Diabetes 1999, 48, 685-690.
63. Carretero, M.V.; Torres, L.; Latasa, U.; Garcia-Trevijano, E.R.; Prieto, J.; Mato, J.M.; Avila, M.A. Transformed but not normal hepatocytes express UCP2. FEBS Lett. 1998, 439, 55-58.
64. Pinney, S.E.; Jaeckle Santos, L.J.; Han, Y.; Stoffers, D.A.; Simmons, R.A. Exendin-4 increases histone acetylase activity and reverses epigenetic modifications that silence Pdx1 in the intrauterine growth retarded rat. Diabetologia 2011, 54, 2606-2614.
65. Cheng, Z.; Almeida, F.A. Mitochondrial alteration in type 2 diabetes and obesity: An epigenetic link. Cell Cycle 2014, 13, 890-897.
66. Cordero, P.; Gomez-Uriz, A.M.; Campion, J.; Milagro, F.I.; Martinez, J.A. Dietary supplementation with methyl donors reduces fatty liver and modifies the fatty acid synthase DNA methylation profile in rats fed an obesogenic diet. Genes Nutr. 2013, 8, 105-113.
67. 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.
68. Martinez, J.A.; Cordero, P.; Campion, J.; Milagro, F.I. Interplay of early-life nutritional programming on obesity, inflammation and epigenetic outcomes. Proc. Nutr. Soc. 2012, 71, 276-283.
69. Aiken, C.E.; Ozanne, S.E. Transgenerational developmental programming. Hum. Reprod. Update 2014, 20, 63-75.
70. 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.
71. Benyshek, D.C.; Johnston, C.S.; Martin, J.F. Glucose metabolism is altered in the adequately-nourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 2006, 49, 1117-1119.
72. Waterland, R.A.; Travisano, M.; Tahiliani, K.G.; Rached, M.T.; Mirza, S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int. J. Obes. (Lond.) 2008, 32, 1373-1379.
73. Fullston, T.; Ohlsson Teague, E.M.; Palmer, N.O.; DeBlasio, M.J.; Mitchell, M.; Corbett, M.; Print, C.G.; Owens, J.A.; Lane, M. 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. 2013, 27, 4226-4243.
74. Ding, G.L.; Wang, F.F.; Shu, J.; Tian, S.; Jiang, Y.; Zhang, D.; Wang, N.; Luo, Q.; Zhang, Y.; Jin, F., et al. Transgenerational glucose intolerance with Igf2/H19 epigenetic alterations in mouse islet induced by intrauterine hyperglycemia. Diabetes 2012, 61, 1133-1142.
75. Drake, A.J.; Liu, L.; Kerrigan, D.; Meehan, R.R.; Seckl, J.R. Multigenerational programming in the glucocorticoid programmed rat is associated with generation-specific and parent of origin effects. Epigenetics 2011, 6, 1334-1343.
76. Radford, E.J.; Isganaitis, E.; Jimenez-Chillaron, J.; Schroeder, J.; Molla, M.; Andrews, S.; Didier, N.; Charalambous, M.; McEwen, K.; Marazzi, G., et al. An unbiased assessment of the role of imprinted genes in an intergenerational model of developmental programming. PLoS Genet. 2012, 8, e1002605.
77. Morgan, D.K.; Whitelaw, E. The case for transgenerational epigenetic inheritance in humans. Mamm. Genome 2008, 19, 394-397.
78. Milagro, F.I.; Mansego, M.L.; de Miguel, C.; Martinez, J.A. Dietary factors, epigenetic modifications and obesity outcomes: Progresses and perspectives. Mol. Aspects Med. 2013, 34, 782-812.