Early life nutrition and metabolic programming

Annals of the New York Academy of Sciences

Volumn 1212, Issue , 2010, Pages 78-96

  Fernandez Twinn, Denise S ^a   Ozanne, Susan E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Early life nutritional programming; Insulin resistance; Insulin signaling; Metabolic syndrome

Indexed keywords

INSULIN;

ARTICLE; ENVIRONMENTAL EXPOSURE; HUMAN; MATERNAL NUTRITION; METABOLIC DISORDER; NONHUMAN; NUTRIENT AVAILABILITY; PHENOTYPE; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 78649507541     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2010.05798.x     Document Type: Article

References (188)

1. Ford, E.S., W.H. Giles & W.H. Dietz 2002. Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA 287: 356-359.
2. Diabetes-UK. Diabetes in the UK 2010: Key statistics on diabetes. 2010. Diabetes-UK, United Kingdom
3. Constancia, M., E. Angiolini, I. Sandovici, et al 2005. Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proc. Natl. Acad. Sci. USA 102: 19 219-19 224.
4. Godfrey, K.M. & D.J. Barker 2001. Fetal programming and adult health. Public Health Nutr. 4: 611-624.
5. Hales, C.N., D.J. Barker, P.M. Clark, et al 1991. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303: 1019-1022.
6. Laitinen, J., K. Pietilainen, M. Wadsworth, et al 2004. Predictors of abdominal obesity among 31-yr-old men and women born in Northern Finland in 1966. Eur. J. Clin. Nutr. 58: 180-190.
7. Phillips, D.I. 1998. Birth weight and the future development of diabetes. A review of the evidence. Diabetes Care 21(Suppl 2): B150-B155.
8. Eriksson, J.G., T. Forsen, J. Tuomilehto, et al 1999. Catch-up growth in childhood and death from coronary heart disease: longitudinal study. BMJ 318: 427-431.
9. Forsen, T., J.G. Eriksson, J. Tuomilehto, et al 1999. Growth in utero and during childhood among women who develop coronary heart disease: longitudinal study. BMJ 319: 1403-1407.
10. Caughey, R.W. & K.B. Michels 2009. Birth weight and childhood leukemia: a meta-analysis and review of the current evidence. Int. J. Cancer 124: 2658-2670.
11. English, P.B., D.E. Goldberg, C. Wolff & D. Smith 2003. Parental and birth characteristics in relation to testicular cancer risk among males born between 1960 and 1995 in California (United States). Cancer Causes Control 14: 815-825.
12. Kaijser, M., O. Akre, S. Cnattingius & A. Ekbom 2005. Preterm birth, low birth weight, and risk for esophageal adenocarcinoma. Gastroenterology 128: 607-609.
13. Xu, X., A.B. Dailey, M. Peoples-Sheps, et al 2009. Birth weight as a risk factor for breast cancer: a meta-analysis of 18 epidemiological studies. J. Womens Health (Larchmt) 18: 1169-1178.
14. Xue, F. & K.B. Michels 2007. Intrauterine factors and risk of breast cancer: a systematic review and meta-analysis of current evidence. Lancet Oncol. 8: 1088-1100.
15. Innes, K., T. Byers & M. Schymura 2000. Birth characteristics and subsequent risk for breast cancer in very young women. Am. J. Epidemiol. 152: 1121-1128.
16. Sanderson, M., M.A. Williams, K.E. Malone, et al 1996. Perinatal factors and risk of breast cancer. Epidemiology 7: 34-37.
17. Mellemkjaer, L., M.L. Olsen, H.T. Sorensen, et al 2003. Birth weight and risk of early-onset breast cancer (Denmark). Cancer Causes Control 14: 61-64.
18. Kousta, E. 2006. Premature adrenarche leads to polycystic ovary syndrome? Long-term consequences. Ann. N.Y. Acad. Sci. 1092: 148-157.
19. Main, K.M., R.B. Jensen, C. Asklund, et al 2006. Low birth weight and male reproductive function. Horm. Res. 65(Suppl 3): 116-122.
20. Vikse, B.E., L.M. Irgens, T. Leivestad, et al 2008. Low birth weight increases risk for end-stage renal disease. J. Am. Soc. Nephrol. 19: 151-157.
21. Luyckx, V.A. & B.M. Brenner 2005. Low birth weight, nephron number, and kidney disease. Kidney Int. Suppl. 68: S68-S77.
22. Seidman, L.J., S.L. Buka, J.M. Goldstein, et al 2000. The relationship of prenatal and perinatal complications to cognitive functioning at age 7 in the New England Cohorts of the National Collaborative Perinatal Project. Schizophr. Bull. 26: 309-321.
23. Nilsson, E., G. Stalberg, P. Lichtenstein, et al 2005. Fetal growth restriction and schizophrenia: a Swedish twin study. Twin Res. Hum. Genet. 8: 402-408.
24. Lin, H.C., H.C. Lee, C.H. Tang & Y.H. Chen 2010. The relation between maternal schizophrenia and low birth weight is modified by paternal age. Can. J. Psychiatry 55: 377-385.
25. Vestergaard, M., O. Basso, T.B. Henriksen, et al 2002. Risk factors for febrile convulsions. Epidemiology 13: 282-287.
26. Vestergaard, M. & J. Christensen 2009. Register-based studies on febrile seizures in Denmark. Brain Dev. 31: 372-377.
27. Knip, M. & H.K. Akerblom 2005. Early nutrition and later diabetes risk. Adv. Exp. Med. Biol. 569: 142-150.
28. Yajnik, C.S. 2004. Early life origins of insulin resistance and type 2 diabetes in India and other Asian countries. J. Nutr. 134: 205-210.
29. Hattersley, A.T. & J.E. Tooke 1999. The fetal insulin hypothesis: an alternative explanation of the association of low birthweight with diabetes and vascular disease. Lancet 353: 1789-1792.
30. Freathy, R.M., A.J. Bennett, S.M. Ring, et al 2009. Type 2 diabetes risk alleles are associated with reduced size at birth. Diabetes 58: 1428-1433.
31. Dupuis, J., C. Langenberg, I. Prokopenko, et al 2010. New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat. Genet. 42: 105-116.
32. Hales, C.N. & D.J. Barker 2001. The thrifty phenotype hypothesis. Br. Med. Bull. 60: 5-20.
33. Ravelli, A.C., J.H. Van Der Meulen, R.P. Michels, et al 1998. Glucose tolerance in adults after prenatal exposure to famine. Lancet 351: 173-177.
34. Bo, S., P. Cavallo-Perin, L. Scaglione, et al 2000. Low birthweight and metabolic abnormalities in twins with increased susceptibility to Type 2 diabetes mellitus. Diabet. Med. 17: 365-370.
35. Grunnet, L., S. Vielwerth, A. Vaag & P. Poulsen 2007. Birth weight is nongenetically associated with glucose intolerance in elderly twins, independent of adult obesity. J. Intern. Med. 262: 96-103.
36. Poulsen, P., K.O. Kyvik, A. Vaag & H. Beck-Nielsen 1999. Heritability of type II (non-insulin-dependent) diabetes mellitus and abnormal glucose tolerance-a population-based twin study. Diabetologia 42: 139-145.
37. Dunger, D.B., B. Salgin & K.K. Ong 2007. Session 7: early nutrition and later health early developmental pathways of obesity and diabetes risk. Proc. Nutr. Soc. 66: 451-457.
38. Vaag, A., C.B. Jensen, P. Poulsen, et al 2006. Metabolic aspects of insulin resistance in individuals born small for gestational age. Horm. Res. 65(Suppl 3): 137-143.
39. Gluckman, P.D. & M.A. Hanson 2004. Maternal constraint of fetal growth and its consequences. Semin. Fetal Neonatal. Med. 9: 419-425.
40. Jablonka, E. & G. Raz 2009. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84: 131-176.
41. Giussani, D.A., P.S. Phillips, S. Anstee & D.J. Barker 2001. Effects of altitude versus economic status on birth weight and body shape at birth. Pediatr. Res. 49: 490-494.
42. Khalid, M.E., M.E. Ali & K.Z. Ali 1997. Full-term birth weight and placental morphology at high and low altitude. Int. J. Gynaecol. Obstet. 57: 259-265.
43. Julian, C.G., M.J. Wilson, M. Lopez, et al 2009. Augmented uterine artery blood flow and oxygen delivery protect Andeans from altitude-associated reductions in fetal growth. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296: R1564-R1575.
44. McLean, E., M. Cogswell, I. Egli, et al 2009. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr. 12: 444-454.
45. Singla, P.N., M. Tyagi, A. Kumar, et al 1997. Fetal growth in maternal anaemia. J. Trop. Pediatr. 43: 89-92.
46. Steer, P., M.A. Alam, J. Wadsworth & A. Welch 1995. Relation between maternal haemoglobin concentration and birth weight in different ethnic groups. BMJ 310: 489-491.
47. Allen, L.H. 2001. Biological mechanisms that might underlie iron's effects on fetal growth and preterm birth. J. Nutr. 131(2S-2): 581S-589S.
48. Rosario, J.F., M.P. Gomez & P. Anbu 2008. Does the maternal micronutrient deficiency (copper or zinc or vitamin E) modulate the expression of placental 11 beta hydroxysteroid dehydrogenase-2 per se predispose offspring to insulin resistance and hypertension in later life? Indian J. Physiol. Pharmacol. 52: 355-365.
49. Christian, P., C.P. Stewart, S.C. LeClerq, et al 2009. Antenatal and postnatal iron supplementation and childhood mortality in rural Nepal: a prospective follow-up in a randomized, controlled community trial. Am. J. Epidemiol. 170: 1127-1136.
50. Fall, C.H., D.J. Fisher, C. Osmond & B.M. Margetts 2009. Multiple micronutrient supplementation during pregnancy in low-income countries: a meta-analysis of effects on birth size and length of gestation. Food Nutr. Bull. 30(4 Suppl): S533-S546.
51. Reinisch, J.M., N.G. Simon, W.G. Karow & R. Gandelman 1978. Prenatal exposure to prednisone in humans and animals retards intrauterine growth. Science 202: 436-438.
52. Clark, P.M. 1998. Programming of the hypothalamo-pituitary-adrenal axis and the fetal origins of adult disease hypothesis. Eur. J. Pediatr. 157(Suppl 1): S7-S10.
53. Vallee, M., W. Mayo, S. Maccari, et al 1996. Long-term effects of prenatal stress and handling on metabolic parameters: relationship to corticosterone secretion response. Brain Res. 712: 287-292.
54. Lesage, J., F. Del-Favero, M. Leonhardt, et al 2004. Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J. Endocrinol. 181: 291-296.
55. Pepe, G.J., M.G. Burch & E.D. Albrecht 2001. Localization and developmental regulation of 11beta-hydroxysteroid dehydrogenase-1 and -2 in the baboon syncytiotrophoblast. Endocrinology 142: 68-80.
56. Seckl, J.R., M. Cleasby & M.J. Nyirenda 2000. Glucocorticoids, 11beta-hydroxysteroid dehydrogenase, and fetal programming. Kidney Int. 57: 1412-1417.
57. McMullen, S., J.C. Osgerby, L.M. Thurston, et al 2004. Alterations in placental 11 beta-hydroxysteroid dehydrogenase (11 betaHSD) activities and fetal cortisol:cortisone ratios induced by nutritional restriction prior to conception and at defined stages of gestation in ewes. Reproduction 127: 717-725.
58. Challis, J.R., D.M. Sloboda, N. Alfaidy, et al 2002. Prostaglandins and mechanisms of preterm birth. Reproduction 124: 1-17.
59. Phillips, D.I., D.J. Barker, C.H. Fall, et al 1998. Elevated plasma cortisol concentrations: a link between low birth weight and the insulin resistance syndrome? J. Clin. Endocrinol. Metab. 83: 757-760.
60. Crowther, N.J., N. Cameron, J. Trusler & I.P. Gray 1998. Association between poor glucose tolerance and rapid post natal weight gain in seven-year-old children. Diabetologia 41: 1163-1167.
61. Forsen, T., J. Eriksson, J. Tuomilehto, et al 2000. The fetal and childhood growth of persons who develop type 2 diabetes. Ann. Intern. Med. 133: 176-182.
62. Yajnik, C. 2000. Interactions of perturbations in intrauterine growth and growth during childhood on the risk of adult-onset disease. Proc. Nutr. Soc. 59: 257-265.
63. Crowther, N.J., J. Trusler, N. Cameron, et al 2000. Relation between weight gain and beta-cell secretory activity and non-esterified fatty acid production in 7-year-old African children: results from the Birth to Ten study. Diabetologia 43: 978-985.
64. Lanigan, J. & A. Singhal 2009. Early nutrition and long-term health: a practical approach. Proc. Nutr. Soc. 68: 422-429.
65. Chan, K.K., L.F. Ho & T.T. Lao 2003. Nutritional intake and placental size in gestational diabetic pregnancies-a preliminary observation. Placenta 24: 985-988.
66. Evers, I.M., H.W. De Valk, B.W. Mol, et al 2002. Macrosomia despite good glycaemic control in Type I diabetic pregnancy; results of a nationwide study in The Netherlands. Diabetologia 45: 1484-1489.
67. Savona-Ventura, C. & M. Chircop 2003. Birth weight influence on the subsequent development of gestational diabetes mellitus. Acta Diabetol. 40: 101-104.
68. Pettitt, D.J., K.M. Narayan, R.L. Hanson & W.C. Knowler 1996. Incidence of diabetes mellitus in women following impaired glucose tolerance in pregnancy is lower than following impaired glucose tolerance in the non-pregnant state. Diabetologia 39: 1334-1337.
69. Williams, M.A., I. Emanuel, C. Kimpo, et al 1999. A population-based cohort study of the relation between maternal birthweight and risk of gestational diabetes mellitus in four racial/ethnic groups. Paediatr. Perinat. Epidemiol. 13: 452-465.
70. Nelson, S.M., P. Matthews & L. Poston 2010. Maternal metabolism and obesity: modifiable determinants of pregnancy outcome. Hum. Reprod. Update 16: 255-275.
71. Catalano, P.M., L. Presley, J. Minium & S. Hauguel-de Mouzon 2009. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care 32: 1076-1080.
72. Voldner, N., K.F. Froslie, K. Bo, et al 2008. Modifiable determinants of fetal macrosomia: role of lifestyle-related factors. Acta Obstet. Gynecol. Scand. 87: 423-429.
73. Olsen, S.F., T.I. Halldorsson, W.C. Willett, et al 2007. Milk consumption during pregnancy is associated with increased infant size at birth: prospective cohort study. Am. J. Clin. Nutr. 86: 1104-1110.
74. Hedderson, M.M., M.A. Williams, V.L. Holt, et al 2008. Body mass index and weight gain prior to pregnancy and risk of gestational diabetes mellitus. Am. J. Obstet. Gynecol. 198: 409 e1-e7.
75. Huda, S.S., L.E. Brodie & N. Sattar 2009. Obesity in pregnancy: prevalence and metabolic consequences. Semin. Fetal Neonatal. Med. 15: 70-76.
76. Catalano, P.M. & H.M. Ehrenberg 2006. The short- and long-term implications of maternal obesity on the mother and her offspring. BJOG 113: 1126-1133.
77. Stewart, F.M., D.J. Freeman, J.E. Ramsay, et al 2007. Longitudinal assessment of maternal endothelial function and markers of inflammation and placental function throughout pregnancy in lean and obese mothers. J. Clin. Endocrinol. Metab. 92: 969-975.
78. Ramsay, J.E., W.R. Ferrell, L. Crawford, et al 2002. Maternal obesity is associated with dysregulation of metabolic, vascular, and inflammatory pathways. J. Clin. Endocrinol. Metab. 87: 4231-4237.
79. Toescu, V., S.L. Nuttall, U. Martin, et al 2002. Oxidative stress and normal pregnancy. Clin. Endocrinol. (Oxf.) 57: 609-613.
80. Sanchez-Vera, I., B. Bonet, M. Viana, et al 2007. Changes in plasma lipids and increased low-density lipoprotein susceptibility to oxidation in pregnancies complicated by gestational diabetes: consequences of obesity. Metabolism 56: 1527-1533.
81. Zwirska-Korczala, K., J. Jagodzinska, T. Wielkoszynski, et al 2001. [Plasma oxysterols and vitamin E concentrations and lipid profile in morbidly obese women]. Pol. Arch. Med. Wewn. 106: 909-915.
82. Alkazemi, D., G. Egeland, J. Vaya, et al 2008. Oxysterol as a marker of atherogenic dyslipidemia in adolescence. J. Clin. Endocrinol. Metab. 93: 4282-4289.
83. Jansson, T., L. Myatt & T.L. Powell 2009. The role of trophoblast nutrient and ion transporters in the development of pregnancy complications and adult disease. Curr. Vasc. Pharmacol. 7: 521-533.
84. Fowden, A.L., J.W. Ward, F.P. Wooding, et al 2006. Programming placental nutrient transport capacity. J. Physiol. 572(Pt 1): 5-15.
85. Myatt, L. 2006. Placental adaptive responses and fetal programming. J. Physiol. 572(Pt 1): 25-30.
86. Jansson, N., J. Pettersson, A. Haafiz, et al 2006. Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet. J. Physiol. 576(Pt 3): 935-946.
87. Fowden, A.L., A.N. Sferruzzi-Perri, P.M. Coan, et al 2009. Placental efficiency and adaptation: endocrine regulation. J. Physiol. 587(Pt 14): 3459-3472.
88. Woodall, S.M., B.H. Breier, B.M. Johnston & P.D. Gluckman 1996. A model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: effects on the somatotrophic axis and postnatal growth. J. Endocrinol. 150: 231-242.
89. Coan, P.M., Vaughan, O.R., Sekita, Y., et al 2010. Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J. Physiol. 588(Pt 3): 527-538.
90. Langley-Evans, S.C., D.S. Gardner & A.A. Jackson 1996. Association of disproportionate growth of fetal rats in late gestation with raised systolic blood pressure in later life. J. Reprod. Fertil. 106: 307-312.
91. Fernandez-Twinn, D.S., S.E. Ozanne, S. Ekizoglou, et al 2003. The maternal endocrine environment in the low-protein model of intra-uterine growth restriction. Br. J. Nutr. 90: 815-822.
92. Hay, W.W. Jr. 1994. Placental transport of nutrients to the fetus. Horm. Res. 42: 215-222.
93. Sugden, M.C., M.L. Langdown, M.J. Munns & M.J. Holness 2001. Maternal glucocorticoid treatment modulates placental leptin and leptin receptor expression and materno-fetal leptin physiology during late pregnancy, and elicits hypertension associated with hyperleptinaemia in the early-growth-retarded adult offspring. Eur. J. Endocrinol. 145: 529-539.
94. Lesage, J., D. Hahn, M. Leonhardt, et al 2002. Maternal undernutrition during late gestation-induced intrauterine growth restriction in the rat is associated with impaired placental GLUT3 expression, but does not correlate with endogenous corticosterone levels. J. Endocrinol. 174: 37-43.
95. Efstratiadis, A. 1998. Genetics of mouse growth. Int. J. Dev. Biol. 42: 955-976.
96. Martin, P.M. & A.E. Sutherland 2001. Exogenous amino acids regulate trophectoderm differentiation in the mouse blastocyst through an mTOR-dependent pathway. Dev. Biol. 240: 182-193.
97. Wen, H.Y., S. Abbasi, R.E. Kellems & Y. Xia 2005. mTOR: a placental growth signaling sensor. Placenta 26(Suppl A): S63-S69.
98. Roos, S., N. Jansson, I. Palmberg, et al 2007. Mammalian target of rapamycin in the human placenta regulates leucine transport and is down-regulated in restricted fetal growth. J. Physiol. 582(Pt 1): 449-459.
99. Palm, M., O. Axelsson, L. Wernroth & S. Basu 2009. F(2)-isoprostanes, tocopherols and normal pregnancy. Free Radic. Res. 43: 546-552.
100. Toescu, V., S.L. Nuttall, U. Martin, et al 2004. Changes in plasma lipids and markers of oxidative stress in normal pregnancy and pregnancies complicated by diabetes. Clin. Sci. (Lond.) 106: 93-98.
101. Burton, G.J., J. Hempstock & E. Jauniaux 2001. Nutrition of the human fetus during the first trimester-a review. Placenta 22(Suppl A): S70-S77.
102. Myatt L. 2010. Review: reactive oxygen and nitrogen species and functional adaptation of the placenta. Placenta 31(Suppl): S66-S69.
103. Symonds, M.E. & H. Budge 2009. Nutritional models of the developmental programming of adult health and disease. Proc. Nutr. Soc. 68: 173-178.
104. Garofano, A., P. Czernichow & B. Breant 1997. In utero undernutrition impairs rat beta-cell development. Diabetologia 40: 1231-1234.
105. Garofano, A., P. Czernichow & B. Breant 1998. Beta-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat. Diabetologia 41: 1114-1120.
106. Vickers, M.H., B.H. Breier, W.S. Cutfield, et al 2000. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am. J. Physiol. Endocrinol. Metab. 279: E83-E87.
107. Vickers, M.H., B.A. Ikenasio & B.H. Breier 2001. IGF-I treatment reduces hyperphagia, obesity, and hypertension in metabolic disorders induced by fetal programming. Endocrinology 142: 3964-3973.
108. Vickers, M.H., P.D. Gluckman, A.H. Coveny, et al 2005. Neonatal leptin treatment reverses developmental programming. Endocrinology 146: 4211-4216.
109. Dumortier, O., B. Blondeau, B. Duvillie, et al 2007. Different mechanisms operating during different critical time-windows reduce rat fetal beta cell mass due to a maternal low-protein or low-energy diet. Diabetologia 50: 2495-2503.
110. Snoeck, A., C. Remacle, B. Reusens & J.J. Hoet 1990. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol. Neonate. 57: 107-118.
111. Langley-Evans, S.C. & M. Nwagwu 1998. Impaired growth and increased glucocorticoid-sensitive enzyme activities in tissues of rat fetuses exposed to maternal low protein diets. Life Sci. 63: 605-615.
112. Hoet, J.J., S. Dahri, A. Snoeck, et al 1992. [Importance of diets and their effect on fetal development: function and structure of the endocrine pancreas following protein deficiency during intrauterine life]. Bull. Mem. Acad. R. Med. Belg. 147: 174-181; discussion 81-83.
113. Petry, C.J., M.W. Dorling, D.B. Pawlak, et al 2001. Diabetes in old male offspring of rat dams fed a reduced protein diet. Int. J. Exp. Diabetes Res. 2: 139-143.
114. Ozanne, S.E., B.T. Nave, C.L. Wang, et al 1997. Poor fetal nutrition causes long-term changes in expression of insulin signaling components in adipocytes. Am. J. Physiol. 273(1 Pt 1): E46-E51.
115. Ozanne, S.E., G.S. Olsen, L.L. Hansen, et al 2003. Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J. Endocrinol. 177: 235-241.
116. Ozanne, S.E., C.B. Jensen, K.J. Tingey, et al 2006. Decreased protein levels of key insulin signalling molecules in adipose tissue from young men with a low birthweight: potential link to increased risk of diabetes Diabetologia 49: 2993-2999.
117. Ozanne, S.E., C.B. Jensen, K.J. Tingey, et al 2005. Low birthweight is associated with specific changes in muscle insulin-signalling protein expression. Diabetologia 48: 547-552.
118. Hales, C.N., M. Desai, S.E. Ozanne & N.J. Crowther 1996. Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochem. Soc. Trans. 24: 341-350.
119. Jennings, B.J., S.E. Ozanne, M.W. Dorling & C.N. Hales 1999. Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. FEBS Lett. 448: 4-8.
120. Tarry-Adkins, J.L., J.H. Chen, N.S. Smith, et al 2009. Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB J. 23: 1521-1528.
121. Ozanne, S.E. & C.N. Hales 2004. Lifespan: catch-up growth and obesity in male mice. Nature 427: 411-412.
122. Ozanne, S.E. & C. Nicholas Hales 2005. Poor fetal growth followed by rapid postnatal catch-up growth leads to premature death. Mech. Ageing Dev. 126: 852-854.
123. Ozanne, S.E., R. Lewis, B.J. Jennings & C.N. Hales 2004. Early programming of weight gain in mice prevents the induction of obesity by a highly palatable diet. Clin. Sci. (Lond.) 106: 141-145.
124. Isganaitis, E., J. Jimenez-Chillaron, M. Woo, et al 2009. Accelerated postnatal growth increases lipogenic gene expression and adipocyte size in low-birth weight mice. Diabetes 58: 1192-1200.
125. Bol, V.V., A.I. Delattre, B. Reusens, et al 2009. Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297: R291-R299.
126. Sutton, G.M., A.V. Centanni & A.A. Butler 2010. Protein malnutrition during pregnancy in C57BL/6J mice results in offspring with altered circadian physiology before obesity. Endocrinology 151: 1570-1580.
127. Robinson, L.K. & L.S. Hurley 1981. Effect of maternal zinc deficiency of food restriction on rat fetal pancreas. 2. Insulin and glucagon. J. Nutr. 111: 869-877.
128. Padmavathi, I.J., Y.D. Kishore, L. Venu, et al 2009. Prenatal and perinatal zinc restriction: effects on body composition, glucose tolerance and insulin response in rat offspring. Exp. Physiol. 94: 761-769.
129. Lisle, S.J., R.M. Lewis, C.J. Petry, et al 2003. Effect of maternal iron restriction during pregnancy on renal morphology in the adult rat offspring. Br. J. Nutr. 90: 33-39.
130. Lewis, R.M., A.J. Forhead, C.J. Petry, et al 2002. Long-term programming of blood pressure by maternal dietary iron restriction in the rat. Br. J. Nutr. 88: 283-290.
131. Illsley, N.P., I. Caniggia & S. Zamudio 2010. Placental metabolic reprogramming: do changes in the mix of energy-generating substrates modulate fetal growth? Int. J. Dev. Biol. 54: 409-419.
132. Schaffer, L., J. Vogel, C. Breymann, et al 2006. Preserved placental oxygenation and development during severe systemic hypoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290: R844-R851.
133. Haggarty, P., S. Allstaff, G. Hoad, et al 2002. Placental nutrient transfer capacity and fetal growth. Placenta 23: 86-92.
134. Styrud, J., U.J. Eriksson, V. Grill & I. Swenne 2005. Experimental intrauterine growth retardation in the rat causes a reduction of pancreatic B-cell mass, which persists into adulthood. Biol. Neonate. 88: 122-128.
135. Simmons, R.A., L.J. Templeton & S.J. Gertz 2001. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 50: 2279-2286.
136. Merlet-Benichou, C., T. Gilbert, M. Muffat-Joly, et al 1994. Intrauterine growth retardation leads to a permanent nephron deficit in the rat. Pediatr. Nephrol. 8: 175-180.
137. Schreuder, M.F., J.R. Nyengaard, M. Fodor, et al 2005. Glomerular number and function are influenced by spontaneous and induced low birth weight in rats. J. Am. Soc. Nephrol. 16: 2913-2919.
138. Boloker, J., S.J. Gertz & R.A. Simmons 2002. Gestational diabetes leads to the development of diabetes in adulthood in the rat. Diabetes 51: 1499-1506.
139. O'Regan, D., C.J. Kenyon, J.R. Seckl & M.C. Holmes 2004. Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology. Am. J. Physiol. Endocrinol. Metab. 287: E863-E870.
140. Lindsay, R.S., R.M. Lindsay, C.R. Edwards & J.R. Seckl 1996. Inhibition of 11-beta-hydroxysteroid dehydrogenase in pregnant rats and the programming of blood pressure in the offspring. Hypertension 27: 1200-1204.
141. Seckl, J.R. 2004. Prenatal glucocorticoids and long-term programming. Eur. J. Endocrinol. 151(Suppl 3): U49-U62.
142. McMullen, S. & S.C. Langley-Evans 2005. Sex-specific effects of prenatal low-protein and carbenoxolone exposure on renal angiotensin receptor expression in rats. Hypertension 46: 1374-1380.
143. Holemans, K., L. Aerts & F.A. Van Assche 2003. Fetal growth restriction and consequences for the offspring in animal models. J. Soc. Gynecol. Investig. 10: 392-399.
144. Van Assche, F.A., K. Holemans & L. Aerts 1998. Fetal growth and consequences for later life. J. Perinat. Med. 26: 337-346.
145. Samuelsson, A.M., P.A. Matthews, M. Argenton, et al 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.
146. Kirk, S.L., A.M. Samuelsson, M. Argenton, et al 2009. Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLoS One 4: e5870; 1-13.
147. Oben, J.A., A. Mouralidarane, A.M. Samuelsson, et al 2010. Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. J. Hepatol. 52: 913-920.
148. Shelley, P., M.S. Martin-Gronert, A. Rowlerson, et al 2009. Altered skeletal muscle insulin signaling and mitochondrial complex II-III linked activity in adult offspring of obese mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297: R675-R681.
149. Harder, T., A. Plagemann, W. Rohde & G. Dorner 1998. Syndrome X-like alterations in adult female rats due to neonatal insulin treatment. Metabolism 47: 855-862.
150. Yura, S., H. Itoh, N. Sagawa, et al 2005. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab. 1: 371-378.
151. Bouret, S.G., S.J. Draper & R.B. Simerly 2004. Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J. Neurosci. 24: 2797-2805.
152. Turrens, J.F. 2003. Mitochondrial formation of reactive oxygen species. J Physiol 552(Pt 2): 335-344.
153. Passos, J.F., G. Saretzki, S. Ahmed, et al 2007. Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. PLoS Biol. 5: 1138-1151.
154. Tarry-Adkins, J.L., J.H. Chen, R.H. Jones, et al 2010. Poor maternal nutrition leads to alterations in oxidative stress, antioxidant defense capacity, and markers of fibrosis in rat islets: potential underlying mechanisms for development of the diabetic phenotype in later life. FASEB J. 24: 2762-2771.
155. Theys, N., T. Bouckenooghe, M.T. Ahn, et al 2009. Maternal low-protein diet alters pancreatic islet mitochondrial function in a sex-specific manner in the adult rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297: R1516-R1525.
156. Fernandez-Twinn, D.S., A. Wayman, S. Ekizoglou, et al 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.
157. Selak, M.A., B.T. Storey, I. Peterside & R.A. Simmons 2003. Impaired oxidative phosphorylation in skeletal muscle of intrauterine growth-retarded rats. Am. J. Physiol. Endocrinol. Metab. 285: E130-E137.
158. Peterside, I.E., M.A. Selak & R.A. Simmons 2003. Impaired oxidative phosphorylation in hepatic mitochondria in growth-retarded rats. Am. J. Physiol. Endocrinol. Metab. 285: E1258-E1266.
159. Simmons, R.A., I. Suponitsky-Kroyter & M.A. Selak 2005. Progressive accumulation of mitochondrial DNA mutations and decline in mitochondrial function lead to beta-cell failure. J. Biol. Chem. 280: 28785-28791.
160. Igosheva, N., A.Y. Abramov, L. Poston, et al 2010. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 5: e10074;1-8.
161. Goelz, S.E., B. Vogelstein, S.R. Hamilton & A.P. Feinberg 1985. Hypomethylation of DNA from benign and malignant human colon neoplasms. Science 228: 187-190.
162. Suter, C.M., D.I. Martin & R.L. Ward 2004. Hypomethylation of L1 retrotransposons in colorectal cancer and adjacent normal tissue. Int. J. Colorectal. Dis. 19: 95-101.
163. Yegnasubramanian, S., M.C. Haffner, Y. Zhang, et al 2008. DNA hypomethylation arises later in prostate cancer progression than CpG island hypermethylation and contributes to metastatic tumor heterogeneity. Cancer Res. 68: 8954-8967.
164. Florl, A.R., C. Steinhoff, M. Muller, et al 2004. Coordinate hypermethylation at specific genes in prostate carcinoma precedes LINE-1 hypomethylation. Br. J. Cancer 91: 985-994.
165. Ehrlich, M., C.B. Woods, M.C. Yu, et al 2006. Quantitative analysis of associations between DNA hypermethylation, hypomethylation, and DNMT RNA levels in ovarian tumors. Oncogene 25: 2636-2645.
166. Wild, L. & J.M. Flanagan 2010. Genome-wide hypomethylation in cancer may be a passive consequence of transformation. Biochim. Biophys. Acta. 1806: 50-57.
167. Nagarajan, R.P., A.R. Hogart, Y. Gwye, et al 2006. Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics 1: e1-e11.
168. Waterland, R.A. & R.L. Jirtle 2004. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition 20: 63-68.
169. Waterland, R.A. 2008. Epigenetic epidemiology of obesity: application of epigenomic technology. Nutr. Rev. 66(Suppl 1): S21-S23.
170. Ozanne, S.E. & M. Constancia 2007. Mechanisms of disease: the developmental origins of disease and the role of the epigenotype. Nat. Clin. Pract. Endocrinol. Metab. 3: 539-546.
171. Sinclair, K.D., C. Allegrucci, R. Singh, 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. USA 104: 19351-19356.
172. Waterland, R.A., R. Kellermayer, M.T. Rached, et al 2009. Epigenomic profiling indicates a role for DNA methylation in early postnatal liver development. Hum. Mol. Genet. 18: 3026-3038.
173. Lillycrop, K.A., E.S. Phillips, A.A. Jackson, 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: 1382-1386.
174. Lillycrop, K.A., E.S. Phillips, C. Torrens, et al 2008. Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br. J. Nutr. 100: 278-282.
175. Bogdarina, I., S. Welham, P.J. King, et al 2007. Epigenetic modification of the renin-angiotensin system in the fetal programming of hypertension. Circ. Res. 100: 520-526.
176. Park, J.H., D.A. Stoffers, R.D. Nicholls & R.A. Simmons 2008. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J. Clin. Invest. 118: 2316-2324.
177. Thompson, R.F., M.J. Fazzari, H. Niu, et al 2010. Experimental intrauterine growth restriction induces alterations in DNA methylation and gene expression in pancreatic islets of rats. J. Biol. Chem. 285: 15111-15118.
178. Raychaudhuri, N., S. Raychaudhuri, M. Thamotharan & S.U. Devaskar 2008. Histone code modifications repress glucose transporter 4
179. Heijmans, B.T., E.W. Tobi, A.D. Stein, et al 2008. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. USA 105: 17046-17049.
180. Einstein, F., R.F. Thompson, T.D. Bhagat, et al 2010. Cytosine methylation dysregulation in neonates following intrauterine growth restriction. PLoS One 5: e8887;1-11.
181. Alkemade, F.E., P. Van Vliet, P. Henneman, et al 2010. Prenatal exposure to apoE deficiency and postnatal hypercholesterolemia are associated with altered cell-specific lysine methyltransferase and histone methylation patterns in the vasculature. Am. J. Pathol. 176: 542-548.
182. Doyle, M.E. & J.M. Egan 2007. Mechanisms of action of glucagon-like peptide 1 in the pancreas. Pharmacol. Ther. 113: 546-593.
183. Stoffers, D.A., B.M. Desai, D.D. DeLeon & R.A. Simmons 2003. Neonatal exendin-4 prevents the development of diabetes in the intrauterine growth retarded rat. Diabetes 52: 734-740.
184. Pinney, S.E., H. Niu, F. Li & R.A. Simmons 2007. Neonatal exendin-4 administration normalises epigenetic modifications of the proximal promoter of Pdx-1. Early Hum. Dev. 83(Suppl. 1): S71. Abstract 5B-4.
185. Reddy, S. & R.B. Elliott 1988. Ontogenic development of peptide hormones in the mammalian fetal pancreas. Experientia 44: 1-9.
186. Scaglia, L., F.E. Smith & S. Bonner-Weir 1995. Apoptosis contributes to the involution of beta cell mass in the post partum rat pancreas. Endocrinology 136: 5461-5468.
187. Gatford, K.L., R.A. Simmons, M.J. De Blasio, et al 2010. Review: placental programming of postnatal diabetes and impaired insulin action after IUGR. Placenta 31(Suppl): S60-S65.
188. Gatford, K.L., S.A. Sulaiman, S.N.B. Mohammad, et al 2009. Interventions to Prevent Diabetes after IUGR - Preliminary Outcomes in the Twin IUGR Lamb. Fetal and Neonatal Physiology Workshop. Darwin Australia