Skip to main content Accessibility help
×
×
Home

DNA methylation: the pivotal interaction between early-life nutrition and glucose metabolism in later life

  • Jia Zheng (a1), Xinhua Xiao (a1), Qian Zhang (a1) and Miao Yu (a1)
Abstract

Traditionally, it has been widely acknowledged that genes together with adult lifestyle factors determine the risk of developing some metabolic diseases such as insulin resistance, obesity and diabetes mellitus in later life. However, there is now substantial evidence that prenatal and early-postnatal nutrition play a critical role in determining susceptibility to these diseases in later life. Maternal nutrition has historically been a key determinant for offspring health, and gestation is the critical time window that can affect the growth and development of offspring. The Developmental Origins of Health and Disease (DOHaD) hypothesis proposes that exposures during early life play a critical role in determining the risk of developing metabolic diseases in adulthood. Currently, there are substantial epidemiological studies and experimental animal models that have demonstrated that nutritional disturbances during the critical periods of early-life development can significantly have an impact on the predisposition to developing some metabolic diseases in later life. The hypothesis that epigenetic mechanisms may link imbalanced early-life nutrition with altered disease risk has been widely accepted in recent years. Epigenetics can be defined as the study of heritable changes in gene expression that do not involve alterations in the DNA sequence. Epigenetic processes play a significant role in regulating tissue-specific gene expression, and hence alterations in these processes may induce long-term changes in gene function and metabolism that persist throughout the life course. The present review focuses on how nutrition in early life can alter the epigenome, produce different phenotypes and alter disease susceptibilities, especially for impaired glucose metabolism.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      DNA methylation: the pivotal interaction between early-life nutrition and glucose metabolism in later life
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      DNA methylation: the pivotal interaction between early-life nutrition and glucose metabolism in later life
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      DNA methylation: the pivotal interaction between early-life nutrition and glucose metabolism in later life
      Available formats
      ×
Copyright
Corresponding author
* Corresponding author: X. Xiao, fax +86 10 69155073, email xiaoxinhua@medmail.com.cn
References
Hide All
1 International Diabetes Federation (2013) IDF Diabetes Atlas, 6th ed. http://www.idf.org/diabetesatlas.
2 Slatkin, M (2009) Epigenetic inheritance and the missing heritability problem. Genetics 182, 845850.
3 Gluckman, PD, Hanson, MA, Buklijas, T, et al. (2009) Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat Rev Endocrinol 5, 401408.
4 Waddington, CH (2012) The epigenotype. 1942. Int J Epidemiol 41, 1013.
5 Holliday, R (2006) Epigenetics: a historical overview. Epigenetics 1, 7680.
6 Holliday, R & Pugh, JE (1975) DNA modification mechanisms and gene activity during development. Science 187, 226232.
7 Turner, BM (1998) Histone acetylation as an epigenetic determinant of long-term transcriptional competence. Cell Mol Life Sci 54, 2131.
8 Aguilera, O, Fernandez, AF, Munoz, A, et al. (2010) Epigenetics and environment: a complex relationship. J Appl Physiol 109, 243251.
9 Fraga, MF (2009) Genetic and epigenetic regulation of aging. Curr Opin Immunol 21, 446453.
10 Skinner, MK, Manikkam, M & Guerrero-Bosagna, C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21, 214222.
11 Bird, A (2002) DNA methylation patterns and epigenetic memory. Gene Dev 16, 621.
12 Gardinergarden, M & Frommer, M (1987) CpG islands in vertebrate genomes. J Mol Biol 196, 261282.
13 Reik, W & Dean, W (2001) DNA methylation and mammalian epigenetics. Electrophoresis 22, 28382843.
14 Kacem, S & Feil, R (2009) Chromatin mechanisms in genomic imprinting. Mamm Genome 20, 544556.
15 Jaenisch, R & Bird, A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33, 245254.
16 Forsdahl, A (1977) Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease? Br J Prev Soc Med 31, 9195.
17 Barker, DJ, Winter, PD, Osmond, C, et al. (1989) Weight in infancy and death from ischaemic heart disease. Lancet 2, 577580.
18 Painter, RC, Roseboom, TJ & Bleker, OP (2005) Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol 20, 345352.
19 Curhan, GC, Willett, WC, Rimm, EB, et al. (1996) Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation 94, 32463250.
20 Hales, CN, Barker, DJP, Clark, PMS, et al. (1991) Fetal and infant growth and impaired glucose-tolerance at age 64. Brit Med J 303, 10191022.
21 Tobi, EW, Lumey, LH, Talens, RP, et al. (2009) DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet 18, 40464053.
22 Steegers-Theunissen, RP, Obermann-Borst, SA, Kremer, D, et al. (2009) Periconceptional maternal folic acid use of 400 microg per day is related to increased methylation of the IGF2 gene in the very young child. PLoS ONE 4, e7845.
23 Godfrey, KM, Sheppard, A, Gluckman, PD, et al. (2011) Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes 60, 15281534.
24 Chong, S & Whitelaw, E (2004) Epigenetic germline inheritance. Curr Opin Genet Dev 14, 692696.
25 Stefan, M, Zhang, W, Concepcion, E, et al. (2013) DNA methylation profiles in type 1 diabetes twins point to strong epigenetic effects on etiology. J Autoimmun 50, 3337.
26 Zhao, J, Goldberg, J, Bremner, JD, et al. (2012) Global DNA methylation is associated with insulin resistance: a monozygotic twin study. Diabetes 61, 542546.
27 Grunnet, L, Vielwerth, S, Vaag, A, et al. (2007) Birth weight is nongenetically associated with glucose intolerance in elderly twins, independent of adult obesity. J Intern Med 262, 96103.
28 Vaag, A, Henriksen, JE, Madsbad, S, et al. (1995) Insulin secretion, insulin action, and hepatic glucose production in identical twins discordant for non-insulin-dependent diabetes mellitus. J Clin Invest 95, 690698.
29 Loke, YJ, Galati, JC, Morley, R, et al. (2013) Association of maternal and nutrient supply line factors with DNA methylation at the imprinted IGF2/H19 locus in multiple tissues of newborn twins. Epigenetics 8, 10691079.
30 Ribel-Madsen, R, Fraga, MF, Jacobsen, S, et al. (2012) Genome-wide analysis of DNA methylation differences in muscle and fat from monozygotic twins discordant for type 2 diabetes. PlOS ONE 7, e51302.
31 Loke, YJ, Novakovic, B, Ollikainen, M, et al. (2013) The Peri/postnatal Epigenetic Twins Study (PETS). Twin Res Hum Genet 16, 1320.
32 El Hajj, N, Pliushch, G, Schneider, E, et al. (2013) Metabolic programming of MEST DNA methylation by intrauterine exposure to gestational diabetes mellitus. Diabetes 62, 13201328.
33 Houde, AA, Hivert, MF & Bouchard, L (2013) Fetal epigenetic programming of adipokines. Adipocyte 2, 4146.
34 Bocock, PN & Aagaard-Tillery, KM (2009) Animal models of epigenetic inheritance. Sem Reprod Med 27, 369379.
35 Rees, WD, Hay, SM, Brown, DS, et al. (2000) Maternal protein deficiency causes hypermethylation of DNA in the livers of rat fetuses. J Nutr 130, 18211826.
36 Burdge, GC, Slater-Jefferies, J, Torrens, C, et al. (2007) 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 97, 435439.
37 Lillycrop, KA, Phillips, ES, Jackson, AA, et al. (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135, 13821386.
38 Sandovici, I, Smith, NH, Nitert, MD, et al. (2011) Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. Proc Natl Acad Sci U S A 108, 54495454.
39 Jousse, C, Parry, L, Lambert-Langlais, S, et al. (2011) Perinatal undernutrition affects the methylation and expression of the leptin gene in adults: implication for the understanding of metabolic syndrome. FASEB J 25, 32713278.
40 Vo, TX, Revesz, A, Sohi, G, et al. (2013) Maternal protein restriction leads to enhanced hepatic gluconeogenic gene expression in adult male rat offspring due to impaired expression of the liver X receptor. J Endocrinol 218, 8597.
41 Cong, R, Jia, Y, Li, R, et al. (2012) Maternal low-protein diet causes epigenetic deregulation of HMGCR and CYP7α1 in the liver of weaning piglets. J Nutr Biochem 23, 16471654.
42 Zhang, S, Rattanatray, L, MacLaughlin, SM, et al. (2010) Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring. FASEB J 24, 27722782.
43 Sinclair, KD, Allegrucci, C, Singh, R, et al. (2007) DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci U S A 104, 1935119356.
44 Thompson, RF, Fazzari, MJ, Niu, H, et al. (2010) Experimental intrauterine growth restriction induces alterations in DNA methylation and gene expression in pancreatic islets of rats. J Biol Chem 285, 1511115118.
45 Vucetic, Z, Kimmel, J, Totoki, K, et al. (2010) Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151, 47564764.
46 Vucetic, Z, Kimmel, J & Reyes, TM (2011) Chronic high-fat diet drives postnatal epigenetic regulation of μ-opioid receptor in the brain. Neuropsychopharmacology 36, 11991206.
47 Khalyfa, A, Carreras, A, Hakim, F, et al. (2013) Effects of late gestational high-fat diet on body weight, metabolic regulation and adipokine expression in offspring. Int J Obes (Lond) 37, 14811489.
48 Gallou-Kabani, C, Gabory, A, Tost, J, 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.
49 Kulkarni, A, Dangat, K, Kale, A, et al. (2011) Effects of altered maternal folic acid, vitamin B12 and docosahexaenoic acid on placental global DNA methylation patterns in Wistar rats. PLoS ONE 6, e17706.
50 Sharpe, RM (2010) Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365, 16971712.
51 Robertson, SA (2005) Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res 322, 4352.
52 Ng, SF, Lin, RC, Laybutt, DR, et al. (2010) Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 467, 963966.
53 Carone, BR, Fauquier, L, Habib, N, et al. (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 10841096.
54 Wei, Y, Yang, CR, Wei, YP, et al. (2014) Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc Natl Acad Sci U S A 111, 18731878.
55 Roemer, I, Reik, W, Dean, W, et al. (1997) Epigenetic inheritance in the mouse. Curr Biol 7, 277280.
56 Gniuli, D, Calcagno, A, Caristo, ME, et al. (2008) Effects of high-fat diet exposure during fetal life on type 2 diabetes development in the progeny. J Lipid Res 49, 19361945.
57 Ding, GL, Wang, FF, Shu, J, et al. (2012) Transgenerational glucose intolerance with Igf2/H19 epigenetic alterations in mouse islet induced by intrauterine hyperglycemia. Diabetes 61, 11331142.
58 Burdge, GC, Hanson, MA, Slater-Jefferies, JL, et al. (2007) Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life? Br J Nutr 97, 10361046.
59 Waterland, RA, Travisano, M & Tahiliani, KG (2007) Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J 21, 33803385.
60 Vickers, MH, Breier, BH, Cutfield, WS, et al. (2000) Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab 279, E83E87.
61 Vickers, MH, Gluckman, PD, Coveny, AH, et al. (2005) Neonatal leptin treatment reverses developmental programming. Endocrinology 146, 42114216.
62 Gluckman, PD, Lillycrop, KA, Vickers, MH, et al. (2007) Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci U S A 104, 1279612800.
63 Weaver, IC, Cervoni, N, Champagne, FA, et al. (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7, 847854.
64 Weaver, IC, Champagne, FA, Brown, SE, et al. (2005) Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 25, 1104511054.
65 Weaver, IC (2007) Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: let's call the whole thing off. Epigenetics 2, 2228.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed