Nutritional programming of disease: Unravelling the mechanism

Journal of Anatomy

Volumn 215, Issue 1, 2009, Pages 36-51

  Langley Evans, Simon C ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Cardiovascular disease; Metabolic syndrome; Nutrition; Pregnancy; Programming

Indexed keywords

DNA; GLUCOCORTICOID;

CARDIOVASCULAR RISK; CAUSAL ATTRIBUTION; CONFERENCE PAPER; DEVELOPMENTAL STAGE; DIETARY INTAKE; DNA METHYLATION; ENVIRONMENTAL FACTOR; FETUS DEVELOPMENT; FETUS GROWTH; FETUS OUTCOME; GENE EXPRESSION REGULATION; GESTATIONAL AGE; HORMONAL REGULATION; HUMAN; LOW BIRTH WEIGHT; MATERNAL HYPERTENSION; MATERNAL NUTRITION; MATERNAL SMOKING; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUTRITIONAL STATUS; OBESITY; PLACENTA FUNCTION; PRIORITY JOURNAL; PROTEIN RESTRICTION; RISK FACTOR;

ANIMALS; CARDIOVASCULAR DISEASES; DIETARY PROTEINS; DISEASE MODELS, ANIMAL; FEMALE; FETAL DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOCORTICOIDS; HUMANS; MATERNAL-FETAL EXCHANGE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA;

ANIMALIA; OVIS ARIES; RODENTIA;

EID: 67449155322     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2008.00977.x     Document Type: Conference Paper

References (109)

1. Aihie Sayer A, Dunn R, Langley-Evans S, Cooper C (2001) Prenatal exposure to a maternal low protein diet shortens life span in rats. Gerontology 47, 9-14.
2. Andersen HS, Gambling L, Holtrop G, McArdle HJ (2006) Maternal iron deficiency identifies critical windows for growth and cardiovascular development in the rat postimplantation embryo. J Nutr 136, 1171-1177.
3. Arai Y, Gorski RA (1968) Critical exposure time for androgenization of the developing hypothalamus in the female rat. Endocrinology 82, 1010-1014.
4. Arenz S, Rückerl R, Koletzko B, von Kries R (2004) Breast-feeding and childhood obesity -A systematic review. Int J Obes Relat Metab Disord 28, 1247-1256.
5. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ (1989) Weight in infancy and death from ischaemic heart disease. Lancet ii, 577-580.
6. Barker DJ, Bull AR, Osmond C, Simmonds SJ (1990) Fetal and placental size and risk of hypertension in adult life. BMJ 301, 259-262.
7. Barker DJ, Godfrey KM, Osmond C, Bull A (1992) The relation of fetal length, ponderal index and head circumference to blood pressure and the risk of hypertension in adult life. Paediatr Perinat Epidemiol 6, 35-44.
8. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM (1993a) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): Relation to reduced fetal growth. Diabetologia 36, 62-67.
9. Barker DJ, Osmond C, Simmonds SJ, Wield GA (1993b) The relation of small head circumference and thinness at birth to death from cardiovascular disease in adult life. BMJ 306, 422-426.
10. 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.
11. Beach RS, Gershwin ME, Hurley LS (1982) Gestational zinc deprivation in mice: Persistence of immunodeficiency for three generations. Science 218, 469-471.
12. Bellinger L, Lilley C, Langley-Evans SC (2004) Prenatal exposure to a maternal low-protein diet programmes a preference for high-fat foods in the young adult rat. Br J Nutr 92, 513-520.
13. Bellinger L, Sculley DV, Langley-Evans SC (2006) Exposure to undernutrition in fetal life determines fat distribution, locomotor activity and food intake in ageing rats. Int J Obes (Lond) 30, 729-738.
14. Benediktsson R, Lindsay RS, Noble J, Seckl JR, Edwards CR (1993) Glucocorticoid exposure in utero: New model for adult hypertension. Lancet 341, 339-341.
15. Bennis-Taleb N, Remacle C, Hoet JJ, Reusens B (1999) A low-protein isocaloric diet during gestation affects brain development and alters permanently cerebral cortex blood vessels in rat offspring. J Nutr 129, 1613-1619.
16. Bibby E, Stewart A (2004) The epidemiology of preterm birth. Neuro Endocrinol Lett 25 (Suppl. 1), 43-47.
17. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16, 6-21.
18. Brameld JM, Buttery PJ, Dawson JM, Harper JM (1998) Nutritional and hormonal control of skeletal-muscle cell growth and differentiation. Proc Nutr Soc 57, 207-217.
19. Brown JE, Carlson M (2000) Nutrition and multifetal pregnancy. J Am Diet Assoc 100, 343-348.
20. Calder PC, Yaqoob P (2000) The level of protein and type of fat in the diet of pregnant rats both affect lymphocyte function in the offspring. Nutr Res 20, 995-1005.
21. Campbell DM, Hall MH, Barker DJ, Cross J, Shiell AW, Godfrey KM (1996) Diet in pregnancy and the offspring's blood pressure 40 years later. Br J Obstet Gynaecol 103, 273-280.
22. Casillas MA, Lopatina N, Andrews LG, Tollefsbol TO (2003) Transcriptional control of the DNA methyltransferases is altered in aging and neoplastically-transformed human fibroblasts. Mol Cell Biochem 252, 33-43.
23. Celsi G, Kistner A, Aizman R, et al. (1998) Prenatal dexamethasone causes oligonephronia, sodium retention, and higher blood pressure in the offspring. Pediatr Res 44, 317-322.
24. Cheema KK, Dent MR, Saini HK, Aroutiounova N, Tappia PS (2005) Prenatal exposure to maternal undernutrition induces adult cardiac dysfunction. Br J Nutr 93, 471-477.
25. Cleal JK, Lewis RM (2008) The mechanisms and regulation of placental amino acid transport to the human foetus. J Neuroendocrinol 20, 419-426.
26. Daenzer M, Ortmann S, Klaus S, Metges CC (2002) Prenatal high protein exposure decreases energy expenditure and increases adiposity in young rats. J Nutr 132, 142-144.
27. Dahri S, Snoeck A, Reusens-Billen B, Remacle C, Hoet JJ (1991) Islet function in offspring of mothers on low-protein diet during gestation. Diabetes 40 (Suppl. 2), 115-120.
28. Dejana E (1996) Endothelial adherens junctions: Implications in the control of vascular permeability and angiogenesis, J Clin Invest 98 1949-1953.
29. Desai M, Byrne CD, Zhang J, Petry CJ, Lucas A, Hales CN (1997) Programming of hepatic insulin-sensitive enzymes in offspring of rat dams fed a protein-restricted diet. Am J Physiol 272, G1083-G1090.
30. Dodic M, Abouantoun T, O'Connor A, Wintour EM, Moritz KM (2002) Programming effects of short prenatal exposure to dexamethasone in sheep. Hypertension 40, 729-734.
31. Edwards CR, Benediktsson R, Lindsay RS, Seckl JR (1996) 11 beta-Hydroxysteroid dehydrogenases: Key enzymes in determining tissue-specific glucocorticoid effects. Steroids 61, 263-269.
32. 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 ischaemia-reperfusion injury. Br J Nutr 98, 93-100.
33. Erhuma A, Salter AM, Sculley DV, Langley-Evans SC, Bennett AJ (2007) Prenatal exposure to a low-protein diet programs disordered regulation of lipid metabolism in the aging rat. Am J Physiol 292, E1702-E1714.
34. Ericsson A, Säljö K, Sjöstrand E, et al. (2007) Brief hyperglycaemia in the early pregnant rat increases fetal weight at term by stimulating placental growth and affecting placental nutrient transport. J Physiol 581, 1323-1332.
35. Eriksson JG, Lindi V, Uusitupa M, et al. (2002a) The effects of the Pro12Ala polymorphism of the peroxisome proliferator-activated receptor-gamma2 gene on insulin sensitivity and insulin metabolism interact with size at birth. Diabetes 51, 2321-2324.
36. Eriksson JG, Forsen T, Tuomilehto J, Jaddoe VW, Osmond C, Barker DJ (2002b) Effects of size at birth and childhood growth on the insulin resistance syndrome in elderly individuals. Diabetologia 45, 342-348.
37. Fall CH, Pandit AN, Law CM, et al. (1995) Size at birth and plasma insulin-like growth factor-1 concentrations. Arch Dis Child 73, 287-293.
38. Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin MS, Hales CN, Ozanne SE (2005) Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol. 288, R368-R373.
39. Fraga MF, Esteller M (2007) Epigenetics and aging: The targets and the marks. Trends Genet 23, 413-418.
40. Gambling L, Dunford S, Wallace DI, et al. (2003) Iron deficiency during pregnancy affects postnatal blood pressure in the rat. J Physiol 552, 603-610.
41. Gillman MW, Rifas-Shiman SL, Kleinman KP, Rich-Edwards JW, Lipshultz SE (2004) Maternal calcium intake and offspring blood pressure. Circulation 110, 1990-1995.
42. Gluckman PD, Hanson MA (2004) Living with the past: Evolution, development, and patterns of disease. Science 305, 1733-1736.
43. Gopalakrishnan GS, Gardner DS, Dandrea J, et al. (2005) Influence of maternal pre-pregnancy body composition and diet during early-mid pregnancy on cardiovascular function and nephron number in juvenile sheep. Br J Nutr 94, 938-947.
44. Groot PH, van Vlijmen BJ, Benson GM, et al. (1996) Quantitative assessment of aortic atherosclerosis in APOE*3 Leiden transgenic mice and its relationship to serum cholesterol exposure. Arterioscler Thromb Vasc Biol 16, 926-933.
45. Hales CN, Barker DJ, Clark PM, et al. (1991) Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303, 1019-1022.
46. Harding J (2004) Nutritional basis for the fetal origins of adult disease. In Fetal Nutrition and Adult Disease (eds Langley-Evans SC), pp. 21-54. CABI, Wallingford, UK.
47. Harrison M, Langley-Evans SC (2008) Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. Br J Nutr. in press.
48. Hughson M, Farris AB, Douglas-Denton R, Hoy WE, Bertram JF (2003) Glomerular number and size in autopsy kidneys: The relationship to birth weight. Kidney Int 63, 2113-2122.
49. Huxley R, Neil A, Collins R (2002) Unravelling the fetal origins hypothesis: Is there really an inverse association between birthweight and subsequent blood pressure? Lancet 360, 659-665.
50. Jackson AA, Dunn RL, Marchand MC, Langley-Evans SC (2003) Increased systolic blood pressure in rats induced by a maternal low-protein diet is reversed by dietary supplementation with glycine. Clin Sci (Lond) 103, 633-639.
51. Jansson N, Pettersson J, Haafiz A, 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, 935-946.
52. Jensen DM, Damm P, Sørensen B, et al. (2003) Pregnancy outcome and prepregnancy body mass index in 2459 glucose-tolerant Danish women. Am J Obs Gynecol 189, 239-244.
53. Joseph KS, Kramer MS (1996) Review of the evidence on fetal and early childhood antecedents of adult chronic disease. Epidemiol Rev 18, 158-174.
54. Khan IY, Taylor PD, Dekou V, et al. (2003) Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension 41, 168-175.
55. Khan IY, Dekou V, Douglas G, et al. (2005) A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol 288, R127-R133.
56. Klerk M, Verhoef P, Clarke R, Blom HJ, Kok FJ, Schouten EG; MTHFR Studies Collaboration Group (2002) MTHFR 677C→T polymorphism and risk of coronary heart disease: A meta-analysis. JAMA 288, 2023-2031.
57. Langley-Evans SC (1997a) Intrauterine programming of hypertension by glucocorticoids. Life Sci 60, 1213-1221.
58. Langley-Evans SC (1997b) Maternal carbenoxolone treatment lowers birthweight and induces hypertension in the offspring of rats fed a protein-replete diet. Clin Sci (Lond) 93, 423-429.
59. Langley-Evans SC (2006) Developmental programming of health and disease. Proc Nutr Soc 65, 97-105.
60. Langley SC, Jackson AA (1994) Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond) 86, 217-222.
61. Langley-Evans SC, Jackson AA (1995) Captopril normalises systolic blood pressure in rats with hypertension induced by fetal exposure to maternal low protein diets. Comp Biochem Physiol 110, 223-228.
62. Langley-Evans AJ, Langley-Evans SC (2003) Relationship between maternal nutrient intakes in early and late pregnancy and infants weight and proportions at birth: Prospective cohort study. J R Soc Health 123, 210-216.
63. Langley-Evans SC, Nwagwu M (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.
64. Langley-Evans SC, Sculley DV (2005) Programming of hepatic antioxidant capacity and oxidative injury in the ageing rat. Mech Ageing Dev 126, 804-812.
65. Langley-Evans SC, Phillips GJ, Jackson AA (1994) In utero exposure to maternal low protein diets induces hypertension in weanling rats, independently of maternal blood pressure changes. Clinical Nutrition 13, 319-324.
66. Langley-Evans SC, Gardner DS, Jackson AA (1996a) Association of disproportionate growth of fetal rats in late gestation with raised systolic blood pressure in later life. J Reprod Fertil 106, 307-312.
67. Langley-Evans SC, Phillips GJ, Benediktsson R, et al. (1996b) Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta 17, 169-172.
68. Langley-Evans SC, Gardner DS, Jackson AA (1996c) Maternal protein restriction influences the programming of the rat hypothalamic-pituitary-adrenal axis. J Nutr 126, 1578-1585.
69. Langley-Evans SC, Welham SJ, Jackson AA (1999) Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 64, 965-974.
70. Langley-Evans SC, Lilley C, McMullen S (2006) Maternal protein restriction and fetal growth: Lack of evidence of a role for homocysteine in fetal programming. Br J Nutr 96, 578-586.
71. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC (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.
72. Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC (2007) Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr 97, 1064-1073.
73. Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, Burdge GC (2008) Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPARalpha promoter of the offspring. Br J Nutr, in press.
74. Mackenzie HS, Brenner BM (1995) Fewer nephrons at birth: A missing link in the etiology of essential hypertension? Am J Kidney Dis 26, 91-98.
75. Martin RM, Ben-Shlomo Y, Gunnell D, Elwood P, Yarnell JW, Davey Smith G (2005) Breast feeding and cardiovascular disease risk factors, incidence, and mortality: The Caerphilly study. J Epidemiol Commun Health 59, 121-129.
76. Martyn CN, Barker DJ, Jespersen S, Greenwald S, Osmond C, Berry C (1995) Growth in utero, adult blood pressure, and arterial compliance. Br Heart J 73, 116-121.
77. Mathews F, Yudkin P, Neil A (1999) Influence of maternal nutrition on outcome of pregnancy: Prospective cohort study. BMJ 319, 339-343.
78. McMullen S, Langley-Evans SC (2005) Maternal low-protein diet in rat pregnancy programs blood pressure through sex-specific mechanisms. Am J Physiol 288, R85-R90.
79. McMullen S, Gardner DS, Langley-Evans SC (2004) Prenatal programming of angiotensin II type 2 receptor expression in the rat. Br J Nutr 91, 133-140.
80. Milnes MR, Roberts RN, Guillette LJ (2002) Effects of incubation temperature and estrogen exposure on aromatase activity in the brain and gonads of embryonic alligators. Environ Health Perspect 110, 393-396.
81. Nüsken KD, Dötsch J, Rauh M, Rascher W, Schneider H (2008) Uteroplacental insufficiency after bilateral uterine artery ligation in the rat: Impact on postnatal glucose and lipid metabolism and evidence for metabolic programming of the offspring by sham operation. Endocrinology 149, 1056-1063.
82. Ozanne SE, Olsen GS, 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, 235-241.
83. Paneth N, Ahmed F, Stein AD (1996) Early nutritional origins of hypertension: A hypothesis still lacking support. J Hypertens 14, S121-S129.
84. Plagemann A, Harder T, Rake A, Melchior K, Rohde W, Dorner G (2001) Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr 130, 2582-2589.
85. Poston L (2006) Endothelial dysfunction in pre-eclampsia. Pharmacol Reports 58. Suppl, 69-74.
86. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP (2001) Effects of prenatal exposure to the Dutch famine on adult disease in later life: An overview. Mol Cell Endocrinol 185, 93-98.
87. Rutland CS, Latunde-Dada AO, Thorpe A, Plant R, Langley-Evans S, Leach L (2007) Effect of gestational nutrition on vascular integrity in the murine placenta. Placenta 28, 734-742.
88. Samuelsson AM, Matthews PA, Argenton M, 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.
89. Sherman RC, Langley-Evans SC (1998) Early administration of angiotensin-converting enzyme inhibitor captopril, prevents the development of hypertension programmed by intrauterine exposure to a maternal low-protein diet in the rat. Clin Sci (Lond) 94, 373-381.
90. Sherman RC, Langley-Evans SC (2000) Antihypertensive treatment in early postnatal life modulates prenatal dietary influences upon blood pressure in the rat. Clin Sci 98, 269-275.
91. 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 USA 104, 19351-19356.
92. Singh GR, Hoy WE (2004) Kidney volume, blood pressure, and albuminuria: findings in an Australian aboriginal community. Am J Kidney Dis 43, 254-259.
93. Smits L, Krabbendam L, de Bie R, Essed G, van Os J (2006) Lower birth weight of Dutch neonates who were in utero at the time of the 9/11 attacks. J Psychosom Res 61, 715-717.
94. Snoeck A, Remacle C, Reusens B, Hoet JJ (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57, 107-118.
95. Stein AD (2004) Birthweight and the development of overweight and obesity. In Fetal Nutrition and Adult Disease (eds Langley-Evans SC), pp. 195-210. CABI, Wallingford, UK.
96. Stoltzfus RJ (2003) Iron deficiency: Global prevalence and consequences. Food Nutr Bull 24, S99-S103.
97. Tappia PS, Nijjar MS, Mahay A, Aroutiounova N, Dhalla NS (2005) Phospholipid profile of developing heart of rats exposed to low-protein diet in pregnancy. Am J Physiol 289, R1400-R1406.
98. Torrens C, Brawley L, Anthony FW, et al. (2006) Folate supplementation during pregnancy improves offspring cardiovascular dysfunction induced by protein restriction. Hypertension 47, 982-987.
99. Vehaskari VM, Aviles DH, Manning J (2001) Prenatal programming of adult hypertension in the rat. Kidney Int 59, 238-245.
100. Vickers MH, Breier BH, McCarthy D, Gluckman PD (2003) Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. Am J Physiol 285, R271-R273.
101. Walters E, Edwards RG (2004) Further thoughts regarding evidence offered in support of the 'Barker hypothesis'. Reprod Biomed Online 9, 129-131.
102. Walton A, Hammond J (1938) The maternal effects on growth and conformation in Shire horse-Shetland pony crosses. Proc R Soc Lond B Biol Sci 125, 311-335.
103. Waterland RA, Jirtle RL (2003) Transposable elements: Targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23, 5293-5300.
104. Willett WC (2006) Trans fatty acids and cardiovascular disease - epidemiological data. Atherosclerosis 7, 5-8.
105. Woodall SM, Johnston BM, Breier BH, Gluckman PD (1996) Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Ped Res 40, 438-443.
106. World Cancer Research Fund (2007) Food, Nutrition, Physical Activity and the Prevention of Cancer. London: WCRF.
107. Yajnik CS, Fall CH, Vaidya U, et al. (1995) Fetal growth and glucose and insulin metabolism in four-year-old Indian children. Diabet Med 12, 330-336.
108. Yates Z, Tarling EJ, Langley-Evans SC, Salter AM (2008) Maternal undernutrition programmes atherosclerosis in the Apo E*3 Leiden mouse. Br J Nutr, in press.
109. Zhang J, Lewis RM, Wang C, Hales N, Byrne CD (2005) Maternal dietary iron restriction modulates hepatic lipid metabolism in the fetuses. Am J Physiol 288, R104-R111.