Epigenetic and developmental influences on the risk of obesity, diabetes, and metabolic syndrome

Diabetes, Metabolic Syndrome and Obesity

Volumn 8, Issue , 2015, Pages 295-302

  Smith, Caitlin J ^a   Ryckman, Kelli K ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Epigenetics; Fetal programming; Maternal; Metabolic syndrome; Pregnancy complications

Indexed keywords

ADIPONECTIN; LEPTIN;

DEVELOPMENT; DISEASE PREDISPOSITION; DNA METHYLATION; ENDOTHELIAL DYSFUNCTION; EPIGENETICS; HUMAN; INSULIN RESISTANCE; INTRAUTERINE GROWTH RETARDATION; LOW BIRTH WEIGHT; MACROSOMIA; MALNUTRITION; MATERNAL HYPERTENSION; MATERNAL NUTRITION; MATERNAL OBESITY; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; OVERNUTRITION; PREECLAMPSIA; PREGNANCY COMPLICATION; PREGNANCY DIABETES MELLITUS; PREMATURITY; PRENATAL EXPOSURE; REVIEW; SEX DIFFERENCE; SMALL FOR DATE INFANT; SOCIAL DETERMINANTS OF HEALTH;

EID: 84936950408     PISSN: None     EISSN: 11787007     Source Type: Journal    
DOI: 10.2147/DMSO.S61296     Document Type: Review

References (67)

1. Tobi EW, Goeman JJ, Monajemi R, et al. DNA methylation signatures link prenatal famine exposure to growth and metabolism. Nat Commun. 2014;5:5592.
2. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992;35(7):595-601.
3. Alsnes IV, Janszky I, Forman MR, Vatten LJ, Okland I. A population-based study of associations between preeclampsia and later cardiovascular risk factors. Am J Obstet Gynecol. 2014;211(6):657. e1-e7.
4. Barker DJ, Martyn CN, Osmond C, Hales CN, Fall CH. Growth in utero and serum cholesterol concentrations in adult life. BMJ. 1993; 307(6918):1524-1527.
5. Boney CM, Verma A, Tucker R, Vohr BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005;115(3):e290-e296.
6. Leeson CP, Kattenhorn M, Morley R, Lucas A, Deanfield JE. Impact of low birth weight and cardiovascular risk factors on endothelial function in early adult life. Circulation. 2001;103(9):1264-1268.
7. de Boo HA, Harding JE. The developmental origins of adult disease (Barker) hypothesis. Aust N Z J Obstet Gynaecol. 2006;46(1):4-14.
8. Kajantie E, Strang-Karlsson S, Hovi P, et al. Insulin sensitivity and secretory response in adults born preterm: the Helsinki study of very low birth weight adults. J Clin Endocrinol Metab. 2015;100(1):244-250.
9. Koleganova N, Piecha G, Ritz E. Prenatal causes of kidney disease. Blood Purif. 2009;27(1):48-52.
10. Cardozo E, Pavone ME, Hirshfeld-Cytron JE. Metabolic syndrome and oocyte quality. Trends Endocrinol Metab. 2011;22(3):103-109.
11. Robker RL. Evidence that obesity alters the quality of oocytes and embryos. Pathophysiology. 2008;15(2):115-121.
12. Ornoy A. Prenatal origin of obesity and their complications: Gestational diabetes, maternal overweight and the paradoxical effects of fetal growth restriction and macrosomia. Reprod Toxicol. 2011;32(2):205-212.
13. Nistala R, Hayden MR, Demarco VG, Henriksen EJ, Lackland DT, Sowers JR. Prenatal Programming and Epigenetics in the Genesis of the Cardiorenal Syndrome. Cardiorenal Med. 2011;1(4):243-254.
14. Whitelaw NC, Whitelaw E. How lifetimes shape epigenotype within and across generations. Hum Mol Genet. 2006;15 Spec No 2:R131-R137.
15. Hanson MA, Gluckman PD. Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol Rev. 2014;94(4):1027-1076.
16. Lillycrop KA. Effect of maternal diet on the epigenome: implications for human metabolic disease. Proc Nutr Soc. 2011;70(1):64-72.
17. Bursztyn M, Ariel I. Maternal-fetal deprivation and the cardiometabolic syndrome. J Cardiometab Syndr. 2006;1(2):141-145.
18. Ponzio BF, Carvalho MH, Fortes ZB, do Carmo Franco M. Implications of maternal nutrient restriction in transgenerational programming of hypertension and endothelial dysfunction across F1-F3 offspring. Life Sci. 2012;90(15-16):571-577.
19. Gray C, Vickers MH, Segovia SA, Zhang XD, Reynolds CM. A maternal high fat diet programmes endothelial function and cardiovascular status in adult male offspring independent of body weight, which is reversed by maternal conjugated linoleic acid (CLA) supplementation. PloS One. 2015;10(2):e0115994.
20. Kaar JL, Crume T, Brinton JT, Bischoff KJ, McDuffie R, Dabelea D. Maternal obesity, gestational weight gain, and offspring adiposity: the exploring perinatal outcomes among children study. J Pediatr. 2014;165(3):509-515.
21. Wen LM, Simpson JM, Rissel C, Baur LA. Maternal "junk food" diet during pregnancy as a predictor of high birthweight: findings from the healthy beginnings trial. Birth. 2013;40(1):46-51.
22. Sampey BP, Vanhoose AM, Winfield HM, et al. Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity (Silver Spring). 2011;19(6):1109-1117.
23. Fan L, Lindsley SR, Comstock SM, et al. Maternal high-fat diet impacts endothelial function in nonhuman primate offspring. Int J Obes (Lond). 2013;37(2):254-262.
24. Marco A, Kisliouk T, Tabachnik T, Meiri N, Weller A. Overweight and CpG methylation of the Pomc promoter in offspring of high-fat-diet-fed dams are not "reprogrammed" by regular chow diet in rats. FASEB J. 2014;28(9):4148-4157.
25. Briffa JF, McAinch AJ, Romano T, Wlodek ME, Hryciw DH. Leptin in pregnancy and development: a contributor to adulthood disease? Am J Physiol Endocrinol Metab. 2015;308(5):E335-E350.
26. Wild SH, Byrne CD. Evidence for fetal programming of obesity with a focus on putative mechanisms. Nutr Res Rev. 2004;17(2):153-162.
27. Barbero A, Astiz S, Lopez-Bote CJ, et al. Maternal malnutrition and offspring sex determine juvenile obesity and metabolic disorders in a swine model of leptin resistance. PloS One. 2013;8(10):e78424.
28. Shasa DR, Odhiambo JF, Long NM, Tuersunjiang N, Nathanielsz PW, Ford SP. Multigenerational impact of maternal overnutrition/obesity in the sheep on the neonatal leptin surge in granddaughters. Int J Obes (Lond). 2015;39(4):695-701.
29. Bouret SG, Draper SJ, Simerly RB. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science. 2004;304(5667):108-110.
30. Ferezou-Viala J, Roy AF, Serougne C, et al. Long-term consequences of maternal high-fat feeding on hypothalamic leptin sensitivity and diet-induced obesity in the offspring. Am J Physiol Regul Integr Comp Physiol. 2007;293(3):R1056-R1062.
31. Blue EK, Ballman K, Boyle F, et al. Fetal hyperglycemia and a high-fat diet contribute to aberrant glucose tolerance and hematopoiesis in adult rats. Pediatr Res. 2015;77(2):316-325.
32. Fisman EZ, Tenenbaum A. Adiponectin: a manifold therapeutic target for metabolic syndrome, diabetes, and coronary disease? Cardiovasc Diabetol. 2014;13:103.
33. Hou M, Chu Z, Liu T, et al. A high-fat maternal diet decreases adiponectin receptor-1 expression in offspring. J Matern Fetal Neonatal Med. 2015;28(2):216-221.
34. Doblado M, Moley KH. Glucose metabolism in pregnancy and embryogenesis. Curr Opin Endocrinol Diabetes Obes. 2007;14(6): 488-493.
35. Thakali KM, Saben J, Faske JB, et al. Maternal pregravid obesity changes gene expression profiles toward greater inflammation and reduced insulin sensitivity in umbilical cord. Pediatr Res. 2014;76(2):202-210.
36. West NA, Crume TL, Maligie MA, Dabelea D. Cardiovascular risk factors in children exposed to maternal diabetes in utero. Diabetologia. 2011;54(3):504-507.
37. Fernandez-Twinn DS, Ozanne SE. Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome. Physiol Behav. 2006;88(3):234-243.
38. Yogev Y, Visser GH. Obesity, gestational diabetes and pregnancy outcome. Semin Fetal Neonatal Med. 2009;14(2):77-84.
39. Yessoufou A, Moutairou K. Maternal diabetes in pregnancy: early and long-term outcomes on the offspring and the concept of "metabolic memory". Exp Diabetes Res. 2011;2011:218598.
40. O'Brien T, Nguyen TT, Zimmerman BR. Hyperlipidemia and diabetes mellitus. Mayo Clin Proc. 1998;73(10):969-976.
41. Li CC, Young PE, Maloney CA, et al. Maternal obesity and diabetes induces latent metabolic defects and widespread epigenetic changes in isogenic mice. Epigenetics. 2013;13;8(6):602-611.
42. Xu J, Ye J, Wu Y, et al. Reduced fetal telomere length in gestational diabetes. PloS One. 2014;9(1):e86161.
43. Dahlhoff M, Pfister S, Blutke A, et al. Peri-conceptional obesogenic exposure induces sex-specific programming of disease susceptibilities in adult mouse offspring. Biochim Biophys Acta. 2014;1842(2):304-317.
44. Hwang LL, Wang CH, Li TL, et al. Sex differences in high-fat diet-induced obesity, metabolic alterations and learning, and synaptic plasticity deficits in mice. Obesity (Silver Spring). 2010;18(3):463-469.
45. Fernandez-Twinn DS, Alfaradhi MZ, Martin-Gronert MS, et al. Downregulation of IRS-1 in adipose tissue of offspring of obese mice is programmed cell-autonomously through post-transcriptional mechanisms. Mol Metab. 2014;3(3):325-333.
46. Leduc L, Levy E, Bouity-Voubou M, Delvin E. Fetal programming of atherosclerosis: possible role of the mitochondria. Eur J Obstet Gynecol Reprod Biol. 2010;149(2):127-130.
47. Tenhola S, Rahiala E, Halonen P, Vanninen E, Voutilainen R. Maternal preeclampsia predicts elevated blood pressure in 12-year-old children: evaluation by ambulatory blood pressure monitoring. Pediatr Res. 2006;59(2):320-324.
48. Miettola S, Hartikainen AL, Vaarasmaki M, et al. Offspring's blood pressure and metabolic phenotype after exposure to gestational hypertension in utero. Eur J Epidemiol. 2013;28(1):87-98.
49. Lawlor DA, Macdonald-Wallis C, Fraser A, et al. Cardiovascular biomarkers and vascular function during childhood in the offspring of mothers with hypertensive disorders of pregnancy: findings from the Avon Longitudinal Study of Parents and Children. Eur Heart J. 2012; 33(3):335-345.
50. Kvehaugen AS, Dechend R, Ramstad HB, Troisi R, Fugelseth D, Staff AC. Endothelial function and circulating biomarkers are disturbed in women and children after preeclampsia. Hypertension. 2011;58(1): 63-69.
51. He J, Zhang A, Fang M, et al. Methylation levels at IGF2 and GNAS DMRs in infants born to preeclamptic pregnancies. BMC Genomics. 2013;14:472.
52. Cianfarani S, Germani D, Branca F. Low birthweight and adult insulin resistance: the "catch-up growth" hypothesis. Arch Dis Child Fetal Neonatal Ed. 1999;81(1):F71-F73.
53. Hermann GM, Dallas LM, Haskell SE, Roghair RD. Neonatal macrosomia is an independent risk factor for adult metabolic syndrome. Neonatology. 2010;98(3):238-244.
54. Seki Y, Williams L, Vuguin PM, Charron MJ. Minireview: Epigenetic programming of diabetes and obesity: animal models. Endocrinology. 2012;153(3):1031-1038.
55. Ozanne SE. Metabolic programming in animals. Br Med Bull. 2001;60: 143-152.
56. Jansson T, Lambert GW. Effect of intrauterine growth restriction on blood pressure, glucose tolerance and sympathetic nervous system activity in the rat at 3-4 months of age. J Hypertens. 1999;17(9):1239-1248.
57. Dellschaft NS, Alexandre-Gouabau MC, Gardner DS, et al. Effect of pre- and postnatal growth and post-weaning activity on glucose metabolism in the offspring. J Endocrinol. 2015;224(2):171-182.
58. Slavik L, Prochazkova J, Prochazka M, Simetka O, Hlusi A, Ulehlova J. The pathophysiology of endothelial function in pregnancy and the usefulness of endothelial markers. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2011;155(4):333-337.
59. Bellamy L, Casas JP, Hingorani AD, Williams DJ. Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ. 2007;335(7627):974.
60. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science. 2005;308(5728):1592-1594.
61. Stocker CJ, Cawthorne MA. The influence of leptin on early life programming of obesity. Trends Biotechnol. 2008;26(10):545-551.
62. Mamun AA. Maternal obesity during pregnancy is associated with adult offspring cardiovascular morbidity and mortality but may represent confounding by other factors. Evid Based Med. 2014;19(3):111.
63. Snelgrove JW, Murphy KE. Preterm birth and social inequality: Assessing the effects of material and psychosocial disadvantage in a UK birth cohort. Acta Obstet Gynecol Scand. Epub April 4, 2015.
64. Tobias DK, Zhang C, Chavarro J, et al. Prepregnancy adherence to dietary patterns and lower risk of gestational diabetes mellitus. Am J Clin Nutr. 2012;96(2):289-295.
65. Timmermans S, Steegers-Theunissen RP, Vujkovic M, et al. The Mediterranean diet and fetal size parameters: the Generation R Study. Br J Nutr. 2012;108(8):1399-1409.
66. Gesteiro E, Rodriguez Bernal B, Bastida S, Sanchez-Muniz FJ. Maternal diets with low healthy eating index or Mediterranean diet adherence scores are associated with high cord-blood insulin levels and insulin resistance markers at birth. Eur J Clin Nutr. 2012;66(9):1008-1015.
67. Gesteiro E, Bastida S, Rodriguez Bernal B, Sanchez-Muniz FJ. Adherence to Mediterranean diet during pregnancy and serum lipid, lipoprotein and homocysteine concentrations at birth. Eur J Nutr. Epub November 20, 2014.