The impact of early nutrition on the ageing trajectory

Proceedings of the Nutrition Society

Volumn 73, Issue 2, 2014, Pages 289-301

  Tarry Adkins, Jane L ^a   Ozanne, Susan E ^a  

^a INSTITUTE OF METABOLIC SCIENCE   (United Kingdom)

Author keywords

Cellular ageing; Developmental programming; Mechanisms; Oxidative stress

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; GLUCAGON; GLUCOSE; INSULIN; NEUROPEPTIDE; RETINOL; SELENIUM; TRANSCRIPTION FACTOR;

APOPTOSIS; APPETITE; CALORIC RESTRICTION; CARDIOMETABOLIC RISK; CARDIOVASCULAR DISEASE; CELL AGING; CONFERENCE PAPER; DNA DAMAGE; DNA METHYLATION; EPIDEMIOLOGICAL DATA; EPIGENETICS; FETAL MALNUTRITION; GENE EXPRESSION; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; HEART VENTRICLE HYPERTROPHY; HISTONE MODIFICATION; HUMAN; HUNGER; HYPERGLYCEMIA; HYPERINSULINEMIA; HYPERTENSION; HYPOXIA; INSULIN RESISTANCE; INTRAUTERINE GROWTH RETARDATION; IRON RESTRICTION; KIDNEY FAILURE; LIPID DIET; LOW BIRTH WEIGHT; MALNUTRITION; MATERNAL NUTRITION; MATERNAL OBESITY; MATERNAL STRESS; METABOLIC SYNDROME X; NITROSATIVE STRESS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; NONHUMAN; NUTRITION; OBESITY; OXIDATIVE STRESS; PHENOTYPE; PLACENTA INSUFFICIENCY; POSTNATAL GROWTH; PREGNANCY DIABETES MELLITUS; PREGNANT WOMAN; PRENATAL EXPOSURE; PROTEIN RESTRICTION; TELOMERE SHORTENING; AGING; ANIMAL; CALORIC INTAKE; CARDIOVASCULAR DISEASES; DIABETES MELLITUS, TYPE 2; FEMALE; FETUS DEVELOPMENT; GENETICS; PREGNANCY;

AGING; ANIMALS; CARDIOVASCULAR DISEASES; CELL AGING; DIABETES MELLITUS, TYPE 2; DNA DAMAGE; ENERGY INTAKE; FEMALE; FETAL DEVELOPMENT; HUMANS; OXIDATIVE STRESS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; TELOMERE SHORTENING;

EID: 84898469108     PISSN: 00296651     EISSN: 14752719     Source Type: Journal    
DOI: 10.1017/S002966511300387X     Document Type: Conference Paper

References (160)

1. Hales CN & Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60, 5-20
2. Barker DJ, Winter PD, Osmond C, et al. (1989) Weight in infancy and death from ischaemic heart disease. Lancet 2, 577-580
3. Hales CN, Barker DJ, Clark PMS, et al. (1991) Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303, 1019-1022
4. Phipps K, Barker DJ, Hales CN, et al. (1993) Fetal growth and impaired glucose tolerance in men and women. Diabetologia 36, 973-974
5. Lithell HO, McKeigue PM, Berglund L, et al. (1996) Relation of size at birth to non-insulin dependent diabetes and insulin concentrations in men aged 50-60 years. BMJ 312, 406-410
6. Pouslen P, Vaag AA, Kyvik KK, et al. (1997) Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs. Diabetolgia 40, 439-446
7. Pouslen P, Kyvik KO, Vaag A, et al. (1999) Heritability of type 2 (non-insulin dependent) diabetes mellitus and abnormal glucose tolerance-A population twin study. Diabetolgia 42, 139-145
8. Bo S, Cavelli-Perin P, Scaglione L, et al. (2000) Low birthweight and metabolic abnormalities in twins with increased susceptibility of Type 2 diabetes mellitus. Diabet Med 5, 365-370
9. Monrad RN, Grunnet LG, Rasmussen EL, et al. (2009) Age-dependent nongenetic influences of birth weight and adult body fat on insulin sensitivity in twins. J Clin Endocrinol Metab 94, 2394-2399
10. Grunnett L, Vielworth S, Vaag AA, et al. (2007) Birth weight is non-genetically associated with glucose intolerance in elderly twins, independent of obesity. J Intern Med 262, 96-103
11. Ravelli GP, Stein ZA & Susser MW (1976) Obesity in young men after famine exposure in utero and early infancy. J Med 295, 349-353
12. Ravelli AC, van der Mullen JH, Michels RP, et al. (1998) Glucose intolerance in elderly twins, independent of adults after pre-natal exposure to famine. Lancet 351, 173-177
13. Crowther NJ, Cameron N, Trusler J, et al. (1998) Association between poor glucose tolerance and rapid postnatal weight gain in seven year-old children. Diabetologia 41, 1163-1167
14. Yajnik C (2000) Interactions of perturbations in intrauterine growth and growth during childhood on the risk of adult-onset disease. Proc Nat Soc 59, 257-265
15. Eriksson JG, Forsen T, Tuomilehto J, et al. (1999) Catch-up growth in childhood and death from coronary heart disease: Longitudinal study. BMJ 318, 427-431
16. Ibanez L, Ong K, Dunger DB, et al. (2006) Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-Age children. J Clin Endocrinol Metab 91, 2153-2158
17. Snoeck A, Remacle C, Reusens B, et al. (1990) Effects of low protein during pregnancy on the fetal pancreas. Biol Neonate 57, 107-118
18. Dahri S, Snoeck A, Reusens-Billen B, et al. (1991) Islet function in offspring of mothers on low protein diet during gestation. Diabetes 40, 115-120
19. Petrik J, Reusens B, Arany E, et al. (1999) A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with insulin-like growth factor-II. Endocrinology 140, 4861-4873
20. Cherif H, Reusens B, Dahri S, et al. (2001) A protein restricted diet during pregnancy alters in-vitro insulin secretion from islets of fetal Wistar rats. J Nutr 131, 1555-1559
21. Ozanne SE, Jensen CB, Tingey KT, et al. (2005) Low birth weight is associated with specific changes in muscle insulin signalling protein expression. Diabetologia 48, 547-552
22. Ozanne SE, Olsen GE, Hansen LL, et al. (2003) Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol 177, 235-242
23. Petry CJ, Ozanne SE, Wang CL, et al. (2000) Effects of early low protein restriction and adult obesity on rat pancreatic hormone content and glucose tolerance. Horm Metab Res 32, 233-239
24. Shepherd PR, Crowther NJ, Desai M, et al. (1997) Altered adipocyte properties in the offspring of protein-restricted rats. Br J Nutr 78, 121-129
25. Petry CJ, Dorling MW, Pawlak DB, et al. (2001) Diabetes in old male offspring of rat dams fed a reduced protein diet. Int J Exp Diabet Res 2, 139-143
26. Chen M, Bergman RN, Pacini G, et al. (1985) Pathogenesis of age-related glucose tolerance in man: Insulin resistance and decreased β-cell function. J Clin Endocrinol Metab 60, 13-20
27. Nwagwu MO, Cook A & Langley-Evans SC (2000) Evidence of progressive deterioration of renal function of renal function in rats exposed to maternal low-protein diet in utero. Br J Nutr 83, 79-85
28. Engeham S, Mdaki K, Jewell K, et al. (2012) Mitochondrial respiration is decreased in rat kidney following fetal exposure to a maternal low-protein diet. J Nutr Metab (Epublication ahead of print version
29. Elmes MJ, Gardner DS & Langley-Evans SC (2007) Fetal exposure to a maternal low protein diet is associated with altered left ventricular pressure response to ischaemiareperfusion injury. Br J Nutr 98, 93-100
30. Hayflick L & Moorhead PS (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25, 585-621
31. Harman D (1956) Aging: A theory based on free-radical and radiation chemistry. J Gerontol 3, 298-300
32. Stadtman ER (1992) Protein oxidation and aging. Science 257, 1220-1224
33. Sohal RS, Agarwal S, Dubey A, et al. (1993) Protein oxidative damage is associated with life expectancy of houseflies. Proc Natl Acad Sci USA 90, 7255-7259
34. Bergendi L, Benes L, Durackova Z, et al. (1999) Chemistry, physiology and pathology of free radicals. Life Sci 65, 1865-1874
35. Valko M, Rhodes CJ, Moncol J, et al. (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160, 1-40
36. Valko M, Leibfritz D, Moncol J, et al. (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39, 44-84
37. Salgo MG, Bermudez E, Squadrito GL, et al. (1995) Peroxynitrite causes DNA-damage and oxidation of thiols peroxynitrite causes in rat thymocytes (corrected) Arch. Biochem Biophys 322, 500-505
38. Kukreja RC & Hess ML (1992) The oxygen free-radical system-From equations through membrane-protein interactions to cardiovascular injury and protection. Cardiovasc Res 26, 641-655
39. Csiszar A, Pacher P, Kaley G, et al. (2005) Role of nitrosative and oxidative stress, longevity genes, and Poly (ADP-ribose) polymerase in cardiovascular dysfunction associated with aging. Curr Vasc Pharmacol 3, 285-291
40. Valko M, Izakovic M, Mazur M, et al. (2004) Role of oxidative stress in DNA damage and cancer incidence. Mol Cell Biochem 266, 37-56
41. Jenner P (2003) Oxidative stress in Parkinson's disease. Ann Neurol 53, S26-S36
42. Sayre LM, Smith MA & Perry G (2001) Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr Med Chem 8, 721-738
43. Rosca MG, Mustata TG, Kinter MT, et al. (2005) Glycation of mitochondrial proteins from diabetic rat kidney is associated with excess superoxide formation. Am J Renal Physiol 289, F420-F430
44. Leonard SS, Harris GK & Shi X (2004) Metal-induced oxidative stress and signal transduction. Free Radic Biol Med 37, 1921-1942
45. Valko M, Morris H & Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12, 1161-1208
46. Tarry-Adkins JL, Chen JH, Jones RH, et al. (2009) Poor maternal nutrition leads to alterations in oxidative stress, antioxidant defense capacity, and markers of fibrosis in rat islets. FASEB J 24, 2762-2771
47. He ZX, Sun ZH, Tan ZL, et al. (2012) Effects of protein or energy restriction during late gestation on antioxidant status of plasma and immune tissues in postnatal goats. J Anim Sci 90, 4319-4326
48. Blackburn EH (1991) Structure and function of telomeres. Nature 350, 569-573
49. Oikawa S & Kawanishi S (1999) Site-specific DNA damage at GGG sequence by oxidative stress may accelerate telomere shortening. FEBS Lett 453, 365-368
50. Kawanishi S & Oikawa S (2004) Mechanism of telomere shortening by oxidative stress. Ann NY Acad Sci 1019, 278-284
51. Olivnikov AM (1971) Principle of marginotomy in template synthesis of polynucleotides. Dokl Akad Nauk SSSR 201, 1469-1499
52. Armanios M (2013) Telomeres and age-related disease: How telomere biology informs clinical paradigms. J Clin Inv 123, 996-1002
53. Greider CW & Blackburn EH (1996) Telomeres, telomerase and cancer. Sci Am 274, 92-97
54. Richter T & von Zglinicki T (2007) A continuous correlation between oxidative stress and telomere length in fibroblasts. Exp Gerontol 11, 1039-1042
55. von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 7, 339-344
56. von Zglinicki T, Pilger R & Sitte N (2000) Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts. Free Radic Biol Med 28, 64-74
57. Honda S, Hjelmeland LM & Handa JT (2001) Oxidative stress-induced single-strand breaks in chromosomal telomeres of human retinal pigment epithelial cells in vitro. Invest Opthalmol Vis Sci 42, 2139-2144
58. Petersen S, Saretzki G & von Zglinicki T (1998) Preferential accumulation of single-stranded regions in telomeres of human fibroblasts. Exp Cell Res 239, 152-160
59. Harley CB, Fuchter AB & Greider CW (1990) Telomeres shorten during ageing of fibroblasts. Nature 345, 448-460
60. Stein GH, Drullinger LF, Soulard A, et al. (1999) Differential roles for cyclin-dependent kinase inhibitors p21 and p16 in the mechanisms of senescence and differentiation in human fibroblasts. Mol Cell Biol 19, 2109-2117
61. Jennings BJ, Ozanne SE & Hales CN (1999) Early growth determines longevity in male rats and may be related to telomere shortening. FEBS Lett 488, 4-8
62. Tarry-Adkins JL, Martin-Gronert MS, Chen JH, et al. (2008) Maternal diet influences DNA damage, aortic telomere length oxidative stress and antioxidant defense capacity in rats. FASEB J 6, 2037-2044
63. Tarry-Adkins JL, Chen JH, Smith NS, 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 5, 1521-1528
64. Tarry-Adkins JL, Martin-Gronert MS, Fernandez-Twinn DS, et al. (2013) Poor maternal nutrition followed by accelerated postnatal catch up growth leads to alterations in DNA damage and repair, oxidative and nitrosative stress and oxidative defense capacity in rat heart. FASEB J 1, 379-390
65. Shelley P, Tarry-Adkins J, Martin-GronertMet al. (2007) Rapid neonatal weight gain results in a ubiquinone (CoQ) deficiency associated with premature death. Mech Age Dev 128, 681-687
66. Ozanne SE & Hales CN (2004) Lifespan: Catch-up growth and obesity in male mice. Nature 427, 411-412
67. Minois N (2000) Longevity and aging: Beneficial effects of exposure to mild stress. Biogerontology 1, 15-29
68. Le Bourg E (2009) Hormesis, aging and longevity. Biochim Biophys Acta 1790, 1030-1039
69. Simmons RA, Gounis AS, Bangalore SA, et al. (1992) Intrauterine growth retardation: Fetal glucose transport is diminished in the lung but spared in the brain. Pediatr Res 31, 59-63
70. Ogata ES, Bussey M & Finley S (1986) Altered gas exchange, limited glucose, branched amino acids and hypoinsulinism retard fetal growth in the rat. Metabolism 35, 970-977
71. Unterman T, Lascon R, Gotway M, et al. (1990) Circulating levels of insulin-like growth factor binding protein-1 (IGFBP-1) and hepatic mRNA are increased in the small for gestational age fetal rat. Endocrinology 127, 2035-2037
72. Simmons RA, Templeton LJ & Gertz SJ (2001) Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 10, 2279-2286
73. Maccuza MQ, Wlodek ME, Dragomir NM, et al. (2010) Uteroplacental insufficiency programs regional vascular dysfunction and alters arterial stiffness in female offspring. J Physiol 588, 1997-2010
74. Moritz KM, Maccuza MQ, Siebel AL, et al. (2009) Uteroplacental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension in with ageing in female rats. J Physiol 587, 2635-2646
75. Heltemes A, Gingery A, Soldner ELB, et al. (2010) Chronic placental ischemia alters amniotic milieu and results in impaired glucose tolerance, insulin resistance and hyperleptinemia in young rats. Exp Biol Med (Maywood) 235, 892-899
76. Karowicz-Bilinska A, Suzin J & Sieroszewski P (2002) Evaluation of oxidative stress indices during treatment in pregnant women with intrauterine growth retardation. Med Sci Monit 8, CR211-CR216
77. Kato H, Yoneyama Y & Araki T (1997) Fetal plasma lipid peroxidase levels in pregnancies complicated with preeclampsia. Gynecol Obstet Invest 43, 158-161
78. Bowen RS, Moodley J, Dutton MF, et al. (2001) Oxidative stress in pre-eclampsia. Acta Obstet Gynecol Scand 80, 719-725
79. Wang Y & Walsh SW (2001) Increased superoxide generation is associated with decreased superoxide dismutase activity and mRNA expression in placental trophoblast cells in pre-eclampsia. Placenta 22, 206-212
80. Miquel J, Economos AC, Fleming J, et al. (1980) Mitochondrial role in cell aging. Exp Gerontol 15, 575-591
81. Sohal RS, Sohal BH (1991) Hydrogen peroxide release by mitochondria increases during aging. Mech Ageing Dev 57 187-202
82. Wei YH & Lee HC (2002) Oxidative stress, mitochondrial DNA mutation and impairment of antioxidant enzymes in aging. Exp Biol Med 227, 671-682
83. Pang CY, Ma YS & Wei YH (2008) MtDNA mutations, functional decline and turnover of mitochondria in aging. Front Biosci 13, 3661-3675
84. Yen TC, Chen YS, King KL, et al. (1989) Liver mitochondrial respiratory function declines with age. Biochem Biophys Res Commun 165, 944-1003
85. Trounce I, Byrne E & Marzuki S (1989) Decline in skeletal muscle mitochondrial respiratory chain function: Possible factor in aging. Lancet 1, 637-639
86. Sugiyama S, Takasawa M, Hayakawa M, et al. (1993) Changes in skeletal muscle, heart and liver of rats and dogs of various ages Biochem Mol Biol Int 30, 937-944
87. Selak M, Storey BT, Peterside IE, et al. (2003) Impaired oxidative phosphorylation in skeletal muscle of intrauterine growth-retarded rats. Am J Physiol Endocrinol Metab 285, E130-E137
88. Peterside IE, Selak M & Simmons RA (2003) Impaired oxidative phosphorylation in hepatic mitochondria in growth-retarded rats. Am J Physiol Endocrinol Metab 285, E1258-E1266
89. Simmons RA, Suponitsky-Kroyter I & Selak MA (2005) Progressive decline of mitochondrial DNA mutations and decline in mitochondrial function lead to β-cell failure. J Biol Chem 31, 28785-28791
90. Esposti MD & McLennan H (1998) Mitochondria and cells produce reactive oxygen species in virtual anaerobiosis: Relevance to ceramide induced apoptosis. FEBS Lett 430, 338-342
91. Chandel NS, Budinger GRS & Schumaker PT (1996) Molecular oxygen modulates cytochrome C oxidase function. J Biol Chem 271, 8672-8677
92. Barry JS, Rozance PJ & Anthony RV (2008) An animal model of placental insufficiency-induced intrauterine growth restriction. Semin Perinatol 32, 225-230
93. Zamudo S, Torricos T, Fik E, et al. (2010) Hypoglycemia and the origin of hypoxia-induced reduction of fetal growth. PLoS ONE 5, e8851
94. Kingdom JC & Kaufman P (1997) Oxygen and placental villous development: Origins of fetal hypoxia. Placenta 18, 613-621
95. De Grauw TJ, Myers R & Scott WJ (1986) Fetal growth in rats from different levels of hypoxia. Biol Neonate 49, 85-89
96. Jacobs R, Robinson JS, Owens JA, et al. (1988) The effect of prolonged hypobaric hypoxia on growth of fetal sheep. J Dev Physiol 10, 97-112
97. Giussani DA, Salinas CE, Villena M, et al. (2007) The role of oxygen in prenatal growth: Studies in the chick embryo. J Physiol 583, 911-917
98. Herrera EA, Camm EJ, Cross CM, et al. (2011) Morphological and functional alterations in the aorta of the chronically hypoxic fetal rat. J Vasc Res 49, 50-58
99. Giussani DA, Camm EJ, Nui Y, et al. (2012) Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS ONE 7, e31017
100. Rouwet EV, Tintu AN, Schellings MW, et al. (2002) Hypoxia induces aortic hypertrophic growth, left ventricular dysfunction, and sympathetic hyperinnervation of peripheral arteries in the chick embryo. Circulation 105 2791-2796
101. Camm EJ, Hansell JA, Kane AD, et al. (2010) Partial contributions of developmental hypoxia and undernutrition to prenatal alterations in somatic growth and cardiovascular structure and function. Am J Obstet Gynecol 5, e24-e34
102. Morton JS, Rueda-Clausen CF & Davidge ST (2011) Flow-mediated vasodilation is impaired in adult rat offspring exposed to prenatal exposure. J Appl Physiol 4, 1073-1082
103. Richter HG, Camm EJ, Modi BN, et al. (2012) Ascorbate prevents placental oxidative stress and enhances birth weight in hypoxic pregnancy in rats. J Physiol 590, 1377-1387
104. Thakor AS, Richer HG, Kane AD, et al. (2010) Redox modulation of the fetal cardiovascular defence to hypoxia. J Physiol 588, 4235-4247
105. Herrara EA, Kane AD, Hansell JA, et al. (2012) A role for xanthine oxidase in the control of fetal cardiovascular function in late gestation sheep. J Physiol 15, 1825-1837
106. French NP, Hagan R, Evans SF, et al. (1999) Repeated antenatal glucocorticoids: Size at birth and subsequent development. Am J Obest Gynecol 180, 114-121
107. Newnham JP & Moss TJ (2001) Antenatal glucocorticoids and growth: Single versus multiple doses in animal and human studies. Sem Neonatal 6, 285-292
108. Reinisch JM, Simon NG, Karow WG, et al. (1978) Prenatal exposure to prednisone in humans and animals retards intra-uterine growth. Science 202, 436-438
109. Nyirenda MJ, Lindsay RS, Kenyon CJ, et al. (1998) Glucocorticoid exposure in late gestation permanently programmes rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose tolerance in adult offspring. J Clin Invest 101, 2174-2181
110. Sloboda DM, Newnham JP & Challis JRG (2002) Repeated maternal glucocorticoid administration and the developing liver in fetal sheep. J Endocrinol 175, 535-543
111. Drake AJ, Walker BR & Seckl JR (2005) Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol 288, R34-R38
112. Seckl JR & Holmes MC (2007) Mechanisms of disease: Glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology. Nat Clin Pract Endocrinol Metab 3, 479-488
113. Entringer S, Epel ES, Kumsta R, et al. (2011) Stress exposure in intrauterine life is associated with shorter telomere length in young adulthood. Proc Natl Acad Sci USA 108, E513-E518
114. Haussmann MF, Longenecker AS, Marchetto NM, et al. (2012) Embryonic exposure of corticosterone modifies the juvenile stress response, oxidative stress response and telomere length. Proc Biol Sci 279, 1447-1456
115. Ahlbom E, Goqvadze V, Chen M, et al. (2000) Prenatal exposure to high levels of glucocorticoids increases the susceptibility of cerebellar granule cells to oxidative-stress induced cell death. Proc Natl Acad Sci USA 97, 14726-14730
116. Walther FJ, Jobe AH & Ikegami M (1998) Repetitive prenatal glucocorticoid exposure reduces oxidative stress in the lungs of pre-Term lambs. J Appl Physiol 85, 273-278
117. Dani C, Corsini I, Burchielli S, et al. (2009) Natural surfactant combined with beclomethasone decreases oxidative lung-injury in the pre-Term lamb. Pediatr Pulmonol 44, 1159-1167
118. Garofano A, Czernichow P & Breant B (1998) Postnatal somatic growth and insulin contents in moderate or severe growth retardation in the rat. Biol Neonate 73, 89-98
119. Garofano A, Czernichow P & Breant B (1999) Effect of aging on beta-cell mass and function in rats malnourished during the perinatal period. Diabetologia 45, 711-718
120. Franco Mdo C, Arruda RM, Fortes ZB, et al. (2002) Severe nutritional restriction in pregnant rats aggravates hypertension, altered vascular reactivity, and renal development in spontaneously hypertensive rats offspring. J Cardiovasc Pharmacol 39, 369-377
121. Franco Mdo C, Dantas AP, Akamine EH, et al. (2002) Enhanced oxidative stress as a potential mechanism underlying the programming of hypertension in utero. J Cardiovasc Pharmacol 40, 501-509
122. Vieira-Filho LD, Lara LS, Silva PA, et al. (2009) Placental oxidative stress in malnourished rats and changes in kidney proximal tubule sodium ATPases in offspring. Clin Exp Pharmacol Physiol 36, 1157-116
123. Desia M, Gayle D, Babu J, et al. (2005) Programmed obesity in intrauterine growth-restricted newborns: Modulation by newborn nutrition. Am J Physiol Regul Interg Comp Physiol 288, R91-R96
124. Cox LA, Nijland MJ, Gilbert JS, et al. (2006) Effect of 30 percent maternal nutrient restriction from 0•16 to 0•5 gestation on fetal baboon kidney gene expression. J Physiol 572, 67-85
125. Nijland MJ, Schlabritz-Loutsevitch NE, Hubbard GB, et al. (2007) Non-human primate fetal kidney transciptome analysis indicates mammalian target of rapamycin (mTOR) is a central nutrient-responsive pathway. J Physiol 579, 643-656
126. Pettitt DJ, Moll PP, Knowler WC, et al. (1993) Insulinemia in children at low and high risk of NIDDM. Diabet Care 16, 608-615
127. Boney CM, Verma A, Tucker R, et al. (2005) Metabolic syndrome in childhood: Association with birth weight, maternal obesity and gestational diabetes mellitus. Pediatrics 1153, e290-e296
128. Boerschmann H, Pfluger M, Henneberger M, et al. (2010) Prevalence and predictors of overweight and insulin resistance in offspring of mothers with gestational diabetes mellitus. Diabet Care 33, 1845-1849
129. Zielinsky P & Piccoli AL Jr (2012) Myocardial hypertrophy and dysfunction in maternal diabetes. Early Hum Dev 88, 273-278
130. Krishnaveni GV, Venna SR, Hill JC, et al. (2010) Intrauterine exposure to maternal diabetes is associated with higher adiposity and insulin resistance and clustering of cardiovascular risk markers in Indian children. Diabet Care 33, 402-404
131. Lee H, Jang HC, Park HK, et al. (2007) Early manifestation of cardiovascular disease risk factors in offspring of mothers with previous history of gestational diabetes mellitus. Diabet Res Clin Pract 78, 238-245
132. Samuelsson AM, Matthews PA, Argenton M, et al. (2008) Diet-induced obesity in female mice leads to hyperphagia, adiposity, hypertension and insulin resistance in a novel murine model of developmental programming. Hypertension 51, 383-392
133. Nivoit P, Morens C, Van Assche FA, et al. (2009) Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia 52, 1133-1142
134. Shelley P, Martin-Gronert MS, Rowlerson A, 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 293, R675-R681
135. Fernandez-Twinn DS, Blackmore HL, Siggens L, et al. (2012) The programming of cardiac hypertrophy in the offspring by maternal obesity is associated with hyperinsulinaemia, AKT, ERK and mTOR activation. Endocrinology 153, 5961-5971
136. Igosheva N, Abramov AY, Poston L, et al. (2010) Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS ONE 5, e10074
137. Bayol SA, Farrington SJ & Stickland NC (2007) A maternal 'junk food' diet in pregnancy and lactation promotes an exacerbated taste for 'junk food' and a greater propensity for obesity in rat offspring. Br J Nutr 98, 843-851
138. Bayol SA, Simbi BH, Bertrand JA, et al. (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
139. Bayol SA, Simbi BH, Fowkes RC, et al. (2010) A maternal 'junk food' diet in pregnancy and lactation promotes nonalcoholic fatty liver disease in rat offspring. Endocrinology 151, 1451-1461
140. Beard J (2007) Recent evidence from human and animal studies regarding iron status and infant development. J Nutr 137, 524S-530S.
141. Singla PN, Tyagi M, Kumar A, et al. (1997) Fetal growth in maternal anaemia. J Trop Pediatr 43, 89-92
142. Lee HS, Kim MS, Kim MH, et al. (2006) Iron status and its association with pregnancy outcome in Korean pregnant women. Eur J Clin Nutr 60, 1130-1135
143. Godfrey KM, Redman CW, Barker DJ, et al. (1991) The effect of maternal anaemia and iron deficiency on the ratio of fetal weight to placental weight. Br J Obstet Gynaecol 98, 886-891
144. Gambling L, Charinia Z, Hannah L, et al. (2002) Effect of iron deficiency on placental cytokine expression and fetal growth in the pregnant rat. Biol Reprod 66, 516-532
145. Lewis RM, Forhead AJ, Petry CJ, et al. (2002) Long term programming of blood pressure by maternal dietary iron restriction in the rat. Br J Nutr 88, 283-290
146. Gambling L, Dunford S, Wallace DI, et al. (2003) Iron deficiency during pregnancy affects post-natal blood pressure in the rat. J Physiol 552, 603-610
147. Lisle SJ, Lewis RM, Petry CJ, et al. (2003) Effect of iron restriction during pregnancy on renal morphology in the adult rat offspring. Br J Nutr 90, 33-39
148. Lewis RM, Doherty CB, James LA, et al. (2001) Effects of maternal iron restriction on placental vascularization in the rat. Placenta 22, 534-539
149. Park JH, Stoffers DA, Nicholls RD, et al. (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
150. Lillycrop KA, Phillips ES, Jackson AA, et al. (2005) Dietary protein restriction of pregnant rats induces and folic supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135, 1382-1386
151. Sandovici I, Smith NH, Dekker-Nitert M, 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 USA 108, 5449-5454
152. Cerda S & Weitzman SA (1997) Influence of oxygen radical injury on DNA methylation. Mutat Res 386, 141-152
153. Franco Mdo C, Dantas AP, Akamine EH, et al. (2007) Biomarkers of oxidative stress and antioxidant status in children born small for gestational age. Pediatr Res 62, 204-208
154. Chiavaroli V, Giannini C, D'Adamo T, et al. (2009) Insulin resistance and oxidative stress in children born small and large for gestational age. Pediatrics 124, 695-702
155. Hracsko Z, Orvos H, Norvak Z, et al. (2008) Evaluation of oxidative stress markers in neonates with intra-uterine growth retardation. Redox Rep 13, 11-16
156. Sen S & Simmons RA (2010) Maternal antioxidant supplementation prevents adiposity in Western diet fed rats. Diabetes 59, 3058-3065
157. Cambonie G, Comte B, Yzdorczyk C, et al. (2007) Antenatal oxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. Am J Regul Interg Comp Physiol 292, R1236-R1245
158. Derks JB, Oudijk HL, Torrence HL, et al. (2010) Allopurinol reduces oxidative stress in the ovine fetal cardiovascular system after repeated episodes of ischemiareperfusion. Pediatr Res 68, 374-380
159. Curhan GC, Willet WC, Rimm EB, et al. (1996) Birth weight and adult hypertension, diabetes mellitus and obesity in US men. Circulation 15, 3246-3250
160. Mi J, Law C, Zhang KL, et al. (2000) Effects of infant birthweight and maternal body mass index in pregnancy on components of the insulin resistance syndrome in China. Ann Intern Med 15, 253-260