Early-life nutritional programming of longevity

Journal of Developmental Origins of Health and Disease

Volumn 5, Issue 5, 2014, Pages 325-338

  Vaiserman, A M ^a  

^a INSTITUTE OF GERONTOLOGY   (Ukraine)

Author keywords

aging associated disease; developmental nutritional programming; epigenetic regulation; longevity

Indexed keywords

ADULT; ANIMAL; DIET; FEMALE; FETAL MALNUTRITION; FETUS DEVELOPMENT; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEALTH STATUS; HUMAN; LONGEVITY; MALE; NUTRITION; NUTRITIONAL DISORDER; NUTRITIONAL STATUS; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; SEASON; STARVATION; TELOMERE SHORTENING;

ADULT; ANIMALS; DIET; EPIGENESIS, GENETIC; FEMALE; FETAL DEVELOPMENT; FETAL NUTRITION DISORDERS; GROWTH AND DEVELOPMENT; HEALTH STATUS; HUMANS; LONGEVITY; MALE; NUTRITION DISORDERS; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; NUTRITIONAL STATUS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEASONS; STARVATION; TELOMERE SHORTENING;

EID: 84931575376     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S2040174414000294     Document Type: Review

References (173)

1. de Magalhães JP. Programmatic features of aging originating in development: aging mechanisms beyond molecular damage? FASEB J. 2012; 26, 4821-4826.
2. Gluckman PD, Hanson MA, Low FM. The role of developmental plasticity and epigenetics in human health. Birth Defects Res C Embryo Today. 2011; 93, 12-18.
3. Hanson M, Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD. Developmental plasticity and developmental origins of non-communicable disease: theoretical considerations and epigenetic mechanisms. Prog Biophys Mol Biol. 2011; 106, 272-280.
4. Barker DJ, Thornburg KL. Placental programming of chronic diseases, cancer and lifespan: a review. Placenta. 2013; 34, 841-845.
5. Tarry-Adkins JL, Ozanne SE. The impact of early nutrition on the ageing trajectory. Proc Nutr Soc. 2014; 73, 289-301.
6. Langley-Evans SC. Nutrition in early life and the programming of adult disease: a review. J Hum Nutr Diet. (in press).
7. Aihie Sayer A, Cooper C, Barker DJ. Is lifespan determined in utero? Arch Dis Child Fetal Neonatal Ed. 1997; 77, F162-F164.
8. Vaiserman AM, Voitenko VP. Early programming of adult longevity: demographic and experimental studies. J Anti Aging Med. 2003; 6, 11-20.
9. Gavrilov LA, Gavrilova NS. Early-life programming of aging and longevity: the idea of high initial damage load (the HIDL hypothesis). Ann N Y Acad Sci. 2004; 1019, 496-501.
10. Lucas A. Programming by early nutrition in man. Ciba Found Symp. 1991; 156, 38-50.
11. Reynolds LP, Borowicz PP, Caton JS, et al. Developmental programming: the concept, large animal models, and the key role of uteroplacental vascular development. J Anim Sci. 2010; 88, E61-E72.
12. Tarry-Adkins JL, Ozanne SE. Mechanisms of early life programming: current knowledge and future directions. Am J Clin Nutr. 2011; 94, 1765S-1771S.
13. Vaiserman AM. Early-life epigenetic programming of human disease and aging. In Epigenetics in Human Disease (ed. Tollefsbol TO), 2012; pp. 545-567. Academic Press: Amsterdam, NY.
14. Neel JV. Diabetes mellitus: a 'thrifty' genotype rendered detrimental by 'progress'? Am J Hum Genet. 1962; 14, 353-362.
15. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595-601.
16. Gluckman PD, Hanson MA. Adult disease: echoes of the past. Eur J Endocrinol. 2006; 155, S47-S50.
17. Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD, Hanson MA. Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr Res. 2007; 61, 5R-10R.
18. Ling C, Groop L. Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes. 2009; 8, 2718-2725.
19. Pinney SE, Simmons RA. Epigenetic mechanisms in the development of type 2 diabetes. Trends Endocr Metab. 2010; 21, 223-229.
20. Stöger R. The thrifty epigenotype: an acquired and heritable predisposition for obesity and diabetes? Bioessays. 2008; 30, 156-166.
21. 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, F71-F73.
22. Eriksson JG, Forsen T, Tuomilehto J, et al. Catch-up growth in childhood and death from coronary heart disease: longitudinal study. Br Med J. 1999; 318, 427-431.
23. Ozanne SE, Hales CN. Lifespan: catch-up growth and obesity in male mice. Nature. 2004; 427, 411-412.
24. Holliday R. The inheritance of epigenetic defects. Science. 1987; 238, 163-170.
25. Cencioni C, Spallotta F, Martelli F, et al. Oxidative stress and epigenetic regulation in ageing and age-related diseases. Int J Mol Sci. 2013; 14, 17643-17663.
26. Calvanese V, Lara E, Kahn A, Fraga MF. The role of epigenetics in ageing and in age-related diseases. Ageing Res Rev. 2009; 8, 268-276.
27. Tremblay J, Hamet P. Impact of genetic and epigenetic factors from early life to later disease. Metabolism. 2008; 57, S27-S31.
28. Johnson AA, Akman K, Calimport SR, et al. The role of DNA methylation in aging, rejuvenation, and age-related disease. Rejuvenation Res. 2012; 15, 483-494.
29. Gravina S, Vijg J. Epigenetic factors in aging and longevity. Pflugers Arch. 2010; 459, 247-258.
30. Teschendorff AE, West J, Beck S. Age-associated epigenetic drift: implications, and a case of epigenetic thrift? Hum Mol Genet. 2013; 22, R7-R15.
31. Fraga MF, Ballestar E, Paz MF, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA. 2005; 102, 10604-10609.
32. Saffery R, Morley R, Carlin JB, et al. Cohort profile: the peri/post-natal epigenetic twins study. Int J Epidemiol. 2012; 41, 55-61.
33. Vickaryous N, Whitelaw E. The role of the early embryonic environment on epigenotype and phenotype. Reprod Fertil Dev. 2005; 17, 335-340.
34. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001; 293, 1089-1093.
35. Waterland RA, Carza C. Potential mechanisms of metabolic imprinting that lead to chronic disease. Am J Clin Nutr. 1999; 69, 179-197.
36. Hochberg Z, Feil R, Constancia M, et al. Child health, developmental plasticity, and epigenetic programming. Endocr Rev. 2011; 32, 159-224.
37. Haggarty P. Epigenetic consequences of a changing human diet. Proc Nutr Soc. 2013; 72, 363-371.
38. Bouchard L, Thibault S, Guay SP, et al. Leptin gene epigenetic adaptation to impaired glucose metabolism during pregnancy. Diabetes Care. 2010; 33, 2436-2441.
39. Fowden AL, Giussani DA, Forhead AJ. Intrauterine programming of physiological systems: causes and consequences. Physiology (Bethesda). 2006; 21, 29-37.
40. Holt RI. Fetal programming of the growth hormone-insulin-like growth factor axis. Trends Endocrinol Metab. 2002; 13, 392-397.
41. Verkauskiene R, Jaquet D, Deghmoun S, et al. Smallness for gestational age is associated with persistent change in insulin-like growth factor I (IGF-I) and the ratio of IGF-I/IGF-binding protein-3 in adulthood. J Clin Endocrinol Metab. 2005; 10, 5672-5676.
42. Avogaro A, de Kreutzenberg SV, Fadini GP. Insulin signaling and life span. Pflugers Arch. 2010; 459, 301-314.
43. Kajantie E. Early-life events. Effects on aging. Hormones. 2008; 7, 101-113.
44. Rincon M, Muzumdar R, Atzmon G, Barzilai N. The paradox of the insulin/IGF-1 signaling pathway in longevity. Mech Ageing Dev. 2004; 125, 397-403.
45. Mentis AF, Kararizou E. Does ageing originate in utero? Biogerontology. 2010; 11, 725-729.
46. Renehan AG, Zwahlen M, Minder C, et al. Insulin-like growth factor (IGF)-1, IGF binding protein-3, and cancer risk: systematic review and meta-regression analysis. Lancet. 2004; 363, 1346-1353.
47. Martin RM, Holly JM, Middleton N, Davey Smith G, Gunnell D. Childhood diet and insulin-like growth factors in adulthood: 65-year follow-up of the Boyd Orr Cohort. Eur J Clin Nutr. 2007; 61, 1281-1292.
48. Higashi Y, Sukhanov S, Anwar A, Shai SY, Delafontaine P. Aging atherosclerosis, and IGF-1. J Gerontol A Biol Sci Med Sci. 2012; 67, 626-639.
49. Ong K, Kratzsch J, Kiess W, et al. Size at birth and cord blood levels of insulin, insulin-like growth factor I (IGF-I), IGF-II, IGF-binding protein-1 (IGFBP-1), IGFBP-3, and the soluble IGF-II/mannose-6-phosphate receptor in term human infants. The ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. J Clin Endocrinol Metab. 2000; 85, 4266-4269.
50. Sandhu MS, Heald AH, Gibson JM, et al. Circulating concentrations of insulin-like growth factor-I and development of glucose intolerance: a prospective observational study. Lancet. 2002; 359, 1740-1745.
51. Juul A, Scheike T, Davidsen M, Gyllenborg J, Jørgensen T. Low serum insulin-like growth factor I is associated with increased risk of ischemic heart disease: a population-based case-control study. Circulation. 2002; 106, 939-944.
52. Kalmijn S, Janssen JA, Pols HA, Lamberts SW, Breteler MM. A prospective study on circulating insulin-like growth factor I (IGF-I), IGF-binding proteins, and cognitive function in the elderly. J Clin Endocrinol Metab. 2000; 85, 4551-4555.
53. Liu JM, Zhao HY, Ning G, et al. IGF-1 as an early marker for low bone mass or osteoporosis in premenopausal and postmenopausal women. J BoneMinerMetab. 2008; 26, 159-164.
54. Ben-Shlomo Y, Holly J, McCarthy A, et al. Prenatal and postnatal milk supplementation and adult insulin-like growth factor I: long-term follow-up of a randomized controlled trial. Cancer Epidemiol Biomarkers Prev. 2005; 14, 1336-1339.
55. Yang J, Anzo M, Cohen P. Control of aging and longevity by IGF-I signaling. Exp Gerontol. 2005; 40, 867-872.
56. Milman S, Atzmon G, Huffman DM, et al. Low insulin-like growth factor-1 level predicts survival in humans with exceptional longevity. Aging Cell. (in press).
57. Hernández MI, Mericq V. Metabolic syndrome in children born small-for-gestational age. Arq Bras Endocrinol Metabol. 2011; 55, 583-589.
58. Dennison EM, Arden NK, Keen RW, et al. Birthweight, vitamin D receptor genotype and the programming of osteoporosis. Paediatr Perinat Epidemiol. 2001; 15, 211-219.
59. Thompson C, Syddall H, Rodin I, Osmond C, Barker DJ. Birth weight and the risk of depressive disorder in late life. Br J Psychiatry. 2001; 179, 450-455.
60. McMillen IC, MacLaughlin SM, Muhlhausler BS, et al. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic Clin Pharmacol Toxicol. 2008; 102, 82-89.
61. Godfrey KM, Barker DJ. Fetal nutrition and adult disease. Am J Clin Nutr. 2000; 71, 1344S-1352S.
62. Harder T, Rodekamp E, Schellong K, Dudenhausen JW, Plagemann A. Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. Am J Epidemiol. 2007; 165, 849-857.
63. Park SK, Kang D, McGlynn KA, et al. Intrauterine environments and breast cancer risk: meta-analysis and systematic review. Breast Cancer Res. 2008; 10, R8.
64. Baker JL, Olsen LW, Sørensen TI. Weight at birth and all-cause mortality in adulthood. Epidemiology. 2008; 19, 197-203.
65. Gillman MW. Developmental origins of health and disease. N Engl J Med. 2005; 353, 1848-1850.
66. Brown AS, Susser ES. Prenatal nutritional deficiency and risk of adult schizophrenia. Schizophr Bull. 2008; 34, 1054-1063.
67. Heijmans BT, Tobi EW, Lumey LH, Slagboom PE. The epigenome: archive of the prenatal environment. Epigenetics. 2009; 4, 526-531.
68. Lumey LH, Stein AD, Susser E. Prenatal famine and adult health. Annu Rev Public Health. 2011; 32, 237-262.
69. Roseboom TJ, Painter RC, van Abeelen AF, Veenendaal MV, de Rooij SR. Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas. 2011; 70, 141-145.
70. Vaiserman AM, Khalangot ND, Strele I, Lumey LH. Early-life exposure to the Ukraine famine of 1933 and type 2 diabetes in adulthood. In Early Life Nutrition and Adult Health and Development. Lessons from Changing Diets, Famines, and Experimental Studies (eds. Lumey LH, Vaiserman AM), 2013; pp. 145-160. Nova Science Publishers: Hauppauge, NY, USA.
71. Li Y, Jaddoe VW, Qi L, et al. Exposure to the Chinese famine in early life and the risk of metabolic syndrome in adulthood. Diabetes Care. 2011; 34, 1014-1018.
72. van Abeelen AF, Veenendaal MV, Painter RC, et al. Survival effects of prenatal famine exposure. Am J Clin Nutr. 2012; 95, 179-183.
73. Lindeboom M, Portrait F, van den Berg GJ. Long-run effects on longevity of a nutritional shock early in life: the Dutch Potato famine of 1846-1847. J Health Econ. 2010; 29, 617-629.
74. Painter RC, Roseboom TJ, Bossuyt PMM, et al. Adult mortality at age 57 after prenatal exposure to the Dutch famine. Eur J Epidemiol. 2005; 20, 673-676.
75. Vaiserman AM, Pisaruk AV, Zabuga OG, Voitenko VP. Does early-life starvation influence age-specific mortality? Evidence from the Ukraine famine of 1933. J Gerontol Geriatr Res. 2012; 1, 258. doi:10.4172/scientificreports.258
76. Kannisto V, Christensen K, Vaupel JW. No increased mortality in later life for cohorts born during famine. Am J Epidemiol. 1997; 145, 987-994.
77. Song S. Does famine have a long-term effect on cohort mortality? Evidence from the 1959-1961 Great Leap Forward Famine in China. J Biosoc Sci. 2009; 41, 469-491.
78. Song S. Mortality consequences of the 1959-1961 Great Leap Forward Famine in China: debilitation, selection, and mortality crossovers. Soc Sci Med. 2010; 71, 551-558.
79. Coale AJ, Kisker EE. Mortality crossovers: reality or bad data? Popul Stud. 1986; 40, 389-401.
80. Elo IT, Preston SH. Effects of early-life conditions on adult mortality: a review. Popul Index. 1992; 58, 186-212.
81. Harding JE, Jaquiery AL, Hernandez CE, et al. Animal studies of the effects of early nutrition on long-term health. Nestlé Nutrition workshop series. Pediatr Program. 2011; 68, 1-11.
82. Doblhammer G, van den Berg GJ, Lumey LH. A re-analysis of the long-term effects on life expectancy of the Great Finnish Famine of 1866-68. Popul Stud (Camb). 2013; 67, 309-322.
83. van den Berg GJ, Doblhammer G, Christensen K. Exogenous determinants of early-life conditions, and mortality later in life. Soc Sci Med. 2009; 68, 1591-1598.
84. van den Berg GJ, Doblhammer-Reiter G, Christensen K. Being born under adverse economic conditions leads to a higher cardiovascular mortality rate later in life: evidence based on individuals born at different stages of the business cycle. Demography. 2011; 48, 507-530.
85. Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA. 2008; 105, 17046-17049.
86. Tobi EW, Lumey LH, Talens RP, et al. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet. 2009; 18, 4046-4053.
87. Banegas JR, Rodríguez-Artalejo F, de la Cruz JJ, et al. Adult men born in spring have lower blood pressure. J Hypertens. 2000; 18, 1763-1766.
88. Wattie N, Ardern CI, Baker J. Season of birth and prevalence of overweight and obesity in Canada. Early Hum Dev. 2008; 84, 539-547.
89. Vaiserman AM, Khalangot MD, Carstensen B, et al. Seasonality of birth in adult type diabetic patients in three Ukrainian regions. Diabetologia. 2009; 52, 2665-2667.
90. Lawlor DA, Davey-Smith G, Mitchell R, Ebrahim S. Temperature at birth, coronary heart disease, and insulin resistance: cross sectional analyses of the British women's heart and health study. Heart. 2004; 90, 381-388.
91. Yuen J, Ekbom A, Trichopoulos D, Hsieh CC, Adami HO. Season of birth and breast cancer risk in Sweden. Br J Cancer. 1994; 70, 564-568.
92. Rowlands IJ, Weinstein P, Nagle CM, Spurdle AB, Webb PM. Australian National Endometrial Cancer Study (ANECS); Australian Ovarian Cancer Study (AOCS). Season of birth and risk of endometrial cancer. Asian Pac J Cancer Prev. 2011; 12, 1193-1196.
93. Doblhammer G. The Late Life Legacy of Very Early Life. 2004. Springer: Berlin, Germany.
94. Gavrilov LA, Gavrilova NS. Season of birth and human longevity. J Anti-aging Med. 1999; 2, 365-366.
95. Doblhammer G, Vaupel JW. Lifespan depends on month of birth. Proc Natl Acad Sci USA. 2001; 98, 2934-2939.
96. Vaiserman AM, Collinson AC, Koshel NM, Belaja II, Voitenko VP. Seasonal programming of adult longevity in Ukraine. Int J Biometeorol. 2002; 47, 49-52.
97. Lerchl A. Month of birth and life expectancy: role of gender and age in a comparative approach. Naturwissenschaften. 2004; 91, 422-425.
98. Flouris AD, Spiropoulos Y, Sakellariou GJ, Koutedakis Y. Effect of seasonal programming on fetal development and longevity: links with environmental temperature. Am J Hum Biol. 2009; 21, 214-216.
99. Gavrilov LA, Gavrilova NS. Season of birth and exceptional longevity: comparative study of American centenarians, their siblings, and spouses. J Aging Res. 2011; Article ID 104616, 11pp, http://dx.doi.org/10.4061/2011/104616
100. Gagnon A. Effect of birth season on longevity: thrifty and hopeful phenotypes in historical Quebec. Am J Hum Biol. 2012; 24, 654-660.
101. Muñoz-Tudurí M, García-Moro C. Season of birth affects short- and long-term survival. Am J Phys Anthropol. 2008; 135, 462-468.
102. Abel EL, Kruger ML. Birth month affects longevity. Death Stud. 2010; 34, 757-763.
103. Moore SE, Cole TJ, Poskitt EME, et al. Season of birth predicts mortality in rural Gambia. Nature. 1997; 388, 434.
104. Ueda P, Edstedt Bonamy AK, Granath F, Cnattingius S. Month of birth and mortality in Sweden: a nation-wide population-based cohort study. PLoS One. 2013; 8, e56425.
105. Watson PE, McDonald BW. Seasonal variation of nutrient intake in pregnancy: effects on infant measures and possible influence on diseases related to season of birth. Eur J Clin Nutr. 2007; 61, 1271-1280.
106. Lowell WE, Davis GE Jr. The light of life: evidence that the sun modulates human lifespan. Med Hypotheses. 2008; 70, 501-507.
107. Finch CE, Crimmins EM. Inflammatory exposure and historical changes in human life-spans. Science. 2004; 305, 1736-1739.
108. Cava E, Fontana L. Will calorie restriction work in humans? Aging (Albany NY). 2013; 5, 507-514.
109. Barnes SK, Ozanne SE. Pathways linking the early environment to long-term health and lifespan. Prog Biophys Mol Biol. 2011; 106, e323-e336.
110. McArdle HJ, Andersen HS, Jones H, Gambling L. Fetal programming: causes and consequences as revealed by studies of dietary manipulation in rats - a review. Placenta. 2006; 27, S56-S60.
111. Langley-Evans SC, Welham SJ, Jackson AA. Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci. 1999; 64, 965-974.
112. Lewis RM, Petry CJ, Ozanne SE, Hales CN. Effects of maternal iron restriction in the rat on blood pressure, glucose tolerance, and serum lipids in the 3-month-old offspring. Metabolism. 2001; 50, 562-567.
113. Simmons RA, Templeton LJ, Gertz SJ. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes. 2001; 50, 2279-2286.
114. Dyer JS, Rosenfeld CR. Metabolic imprinting by prenatal, perinatal, and postnatal overnutrition: a review. Semin Reprod Med. 2011; 29, 266-276.
115. Taylor PD, McConnell J, Khan IY, et al. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R134-R139.
116. Akyol A, McMullen S, Langley-Evans SC. Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet. Br J Nutr. 2012; 107, 964-978.
117. Ozanne SE. Metabolic programming in animals: type 2 diabetes. Br Med Bull. 2001; 60, 143-152.
118. Manning J, Vehaskari VM. Low birth weight-associated adult hypertension in the rat. Pediatr Nephrol. 2001; 16, 417-422.
119. Aihie Sayer A, Dunn R, Langley-Evans S, Cooper C. Prenatal exposure to a maternal low protein diet shortens life span in rats. Gerontology. 2001; 47, 9-14.
120. Langley-Evans SC, Sculley DV. The association between birthweight and longevity in the rat is complex and modulated by maternal protein intake during fetal life. FEBS Lett. 2006; 580, 4150-4153.
121. Desai M, Crowther NJ, Lucas A, Hales CN. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 1996; 76, 591-603.
122. Hales CN, Desai M, Ozanne SE, Crowther NJ. Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochem Soc Trans. 1996; 24, 341-350.
123. Jennings BJ, Ozanne SE, Dorling MW, Hales CN. Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. FEBS Lett. 1999; 448, 4-8.
124. Ozanne SE, Hales CN. Poor fetal growth followed by rapid postnatal catch-up growth leads to premature death. Mech Ageing Dev. 2005; 126, 852-854.
125. Whitaker KW, Totoki K, Reyes TM. Metabolic adaptations to early life protein restriction differ by offspring sex and postweaning diet in the mouse. Nutr Metab Cardiovasc Dis. 2012; 22, 1067-1074.
126. Martin-Gronert MS, Tarry-Adkins JL, Cripps RL, Chen JH, Ozanne SE. Maternal protein restriction leads to early life alterations in the expression of key molecules involved in the aging process in rat offspring. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R494-R500.
127. Shelley P, Tarry-Adkins J, Martin-Gronert M, et al. Rapid neonatal weight gain in rats results in a renal ubiquinone (CoQ) deficiency associated with premature death. Mech Ageing Dev. 2007; 128, 681-687.
128. Reusens B, Remacle C. Programming of the endocrine pancreas by the early nutritional environment. Int J Biochem Cell Biol. 2006; 38, 913-922.
129. Erhuma A, Salter AM, Sculley DV, Langley-Evans SC, Bennett AJ. Prenatal exposure to a low protein diet programs disordered regulation of lipid metabolism in the aging rat. Am J Physiol Endocrinol Metab. 2007; 292, E1702-E1714.
130. Ozanne SE, Olsen GS, Hansen LL, et al. Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol. 2003; 177, 235-241.
131. Fernandez-Twinn DS, Wayman A, Ekizoglou S, et al. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol. 2005; 288, R368-R373.
132. Chen JH, Martin-Gronert MS, Tarry-Adkins J, Ozanne SE. Maternal protein restriction affects postnatal growth and the expression of key proteins involved in lifespan regulation in mice. PLoS One. 2009; 4, e4950. doi: 10.1371/journal. pone.0004950.
133. Yates Z, Tarling EJ, Langley-Evans SC, Salter AM. Maternal undernutrition programmes atherosclerosis in the ApoE3- Leiden mouse. Br J Nutr. 2009; 101, 1185-1194.
134. Ogawa T, Rakwal R, Shibato J, et al. Seeking gene candidates responsible for developmental origins of health and disease. Congenit Anom (Kyoto). 2011; 51, 110-125.
135. Tarry-Adkins JL, Joles JA, Chen JH, et al. Protein restriction in lactation confers nephroprotective effects in the male rat and is associated with increased antioxidant expression. Am J Physiol Regul Integr Comp Physiol. 2007; 293, R1259-R1266.
136. McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005; 85, 571-633.
137. Snoeck A, Remacle C, Reusens B, Hoet JJ. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate. 1990; 57, 107-118.
138. Plagemann A, Harder T, Rake A, et al. Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr. 2000; 130, 2582-2589.
139. Bennis-Taleb N, Remacle C, Hoet JJ, Reusens B. A low-protein isocaloric diet during gestation affects brain development and alters permanently cerebral cortex blood vessels in rat offspring. J Nutr. 1999; 129, 1613-1619.
140. Mehta G, Roach HI, Langley-Evans SC, et al. Intrauterine exposure to a maternal low protein diet reduces adult bone mass and alters growth plate morphology. Calc Tiss Intl. 2002; 79, 493-498.
141. Mallinson J, Sculley DV, Craigon J, et al. Fetal exposure to a maternal low protein diet during mid gestation results in muscle-specific effects on fibre type composition in young rats. Br J Nutr. 2007; 98, 292-299.
142. Chen JH, Tarry-Adkins JL, Heppolette CA, Palmer DB, Ozanne SE. Early-life nutrition influences thymic growth in male mice that may be related to the regulation of longevity. Clin Sci (Lond). 2009; 118, 429-438.
143. Chen JH, Tarry-Adkins JL, Matharu K, Yeo GS, Ozanne SE. Maternal protein restriction affects gene expression profiles in the kidney at weaning with implications for the regulation of renal function and lifespan. Clin Sci (Lond). 2010; 119, 373-384.
144. Tarry-Adkins JL, Martin-Gronert MS, Chen JH, Cripps RL, Ozanne SE. Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. FASEB J. 2008; 22, 2037-2044.
145. Tarry-Adkins JL, Chen JH, Smith NS, et al. Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB J. 2009; 23, 1521-1528.
146. Tarry-Adkins JL, Martin-Gronert MS, Fernandez-Twinn DS, et al. Poor maternal nutrition followed by accelerated postnatal growth leads to alterations in DNA damage and repair, oxidative and nitrosative stress, and oxidative defense capacity in rat heart. FASEB J. 2013; 27, 379-390.
147. Tarry-Adkins JL, Blackmore HL, Martin-Gronert MS, et al. Coenzyme Q10 prevents accelerated cardiac aging in a rat model of poor maternal nutrition and accelerated postnatal growth. Mol Metab. 2013; 2, 480-490.
148. Geiger S, Le Vaillant M, Lebard T, et al. Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol Ecol. 2012; 21, 1500-1510.
149. Crespi EJ. A mechanistic understanding of ageing revealed by studying the young. Mol Ecol. 2012; 21, 1307-1310.
150. Hallows SE, Regnault TR, Betts DH. The long and short of it: the role of telomeres in fetal origins of adult disease. J Pregnancy. 2012; 2012, 638476.
151. Chen JH, Cottrell EC, Ozanne SE. Early growth and ageing. Nestle Nutr Workshop Ser Pediatr Program. 2010; 65, 41-50.
152. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005; 135, 1382-1386.
153. Lillycrop KA, Slater-Jefferies JL, Hanson MA, et al. 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. 2007; 97, 1064-1073.
154. Lillycrop KA, Phillips ES, Torrens C, et al. 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. 2008; 100, 278-282.
155. Bol VV, Reusens BM, Remacle CA. Postnatal catch-up growth after fetal protein restriction programs proliferation of rat preadipocytes. Obesity (Silver Spring). 2008; 16, 2760-2763.
156. Guan H, Arany E, van Beek JP, et al. Adipose tissue gene expression profiling reveals distinct molecular pathways that define visceral adiposity in offspring of maternal proteinrestricted rats. Am J Physiol Endocrinol Metab. 2005; 288, E663-E673.
157. Orozco-Solís R, Matos RJ, Guzmán-Quevedo O, et al. Nutritional programming in the rat is linked to long-lasting changes in nutrient sensing and energy homeostasis in the hypothalamus. PLoS One. 2010; 5, e13537. doi: 10.1371/ journal.pone.0013537.
158. Zheng S, Rollet M, Pan YX. Protein restriction during gestation alters histone modifications at the glucose transporter 4 (GLUT4) promoter region and induces GLUT4 expression in skeletal muscle of female rat offspring. J Nutr Biochem. 2012; 23, 1064-1071.
159. Zeng Y, Gu P, Liu K, Huang P. Maternal protein restriction in rats leads to reduced PGC-1α expression via altered DNA methylation in skeletal muscle. Mol Med Rep. 2013; 7, 306-312.
160. Sohi G, Marchand K, Revesz A, Arany E, Hardy DB. Maternal protein restriction elevates cholesterol in adult rat offspring due to repressive changes in histone modifications at the cholesterol 7{alpha}-hydroxylase promoter. Mol Endocrinol 2011; 25, 785-798.
161. Sandovici I, Smith NH, Nitert MD, et al. 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. 2011; 108, 5449-5454.
162. Ozanne SE, Sandovici I, Constância M. Maternal diet, aging and diabetes meet at a chromatin loop. Aging (Albany NY). 2011; 3, 548-554.
163. Carone BR, Fauquier L, Habib N, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell. 2010; 143, 1084-1096.
164. Stevens A, Begum G, Cook A, et al. Epigenetic changes in the hypothalamic proopiomelanocortin and glucocorticoid receptor genes in the ovine fetus after periconceptional undernutrition. Endocrinology. 2010; 151, 3652-3664.
165. Seki Y, Williams L, Vuguin PM, Charron MJ. Minireview: epigenetic programming of diabetes and obesity: animal models. Endocrinology. 2012; 153, 1031-1038.
166. Niculescu MD, Lupu DS. Nutritional influence on epigenetics and effects on longevity. Curr Opin Clin Nutr Metab Care. 2011; 14, 35-40.
167. Bacalini MG, Friso S, Olivieri F, et al. Present and future of anti-ageing epigenetic diets. Mech Ageing Dev. 2014; 136-137, 101-115.
168. Thompson RF, Einstein FH. Epigenetic basis for fetal origins of age-related disease. J Womens Health (Larchmt). 2010; 19, 581-587.
169. Haggarty P. Epigenetic consequences of a changing human diet. Proc Nutr Soc. 2013; 72, 363-371.
170. Jackson AA, Dunn RL, Marchand MC, Langley-Evans SC. Increased systolic blood pressure in rats induced by a maternal low-protein diet is reversed by dietary supplementation with glycine. Clin Sci (Lond). 2003; 103, 633-639.
171. Torrens C, Brawley L, Anthony FW, et al. Folate supplementation during pregnancy improves offspring cardiovascular dysfunction induced by protein restriction. Hypertension. 2006; 47, 982-987.
172. Engeham SF, Haase A, Langley-Evans SC. Supplementation of a maternal low-protein diet in rat pregnancy with folic acid ameliorates programming effects upon feeding behaviour in the absence of disturbances to the methionine-homocysteine cycle. Br J Nutr. 2010; 103, 996-1007.
173. Park LK, Friso S, Choi SW. Nutritional influences on epigenetics and age-related disease. Proc Nutr Soc. 2012; 71, 75-83.