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A conceptual framework for the developmental origins of health and disease

Part of: J DOHaD 10th Anniversary Collection

Published online by Cambridge University Press:  09 December 2009

P. D. Gluckman ,
M. A. Hanson  and
T. Buklijas
P. D. Gluckman*
Affiliation:
Liggins Institute and the National Research Centre for Growth and Development, The University of Auckland, Auckland, New Zealand Singapore Institute for Clinical Sciences, A*STAR (Agency for Science, Technology and Research), Singapore
M. A. Hanson
Affiliation:
Developmental Origins of Health and Disease Division, Institute of Developmental Sciences, University of Southampton, Southampton, UK
T. Buklijas
Affiliation:
Liggins Institute and the National Research Centre for Growth and Development, The University of Auckland, Auckland, New Zealand
*
Address for correspondence: P. D. Gluckman, Liggins Institute, The University of Auckland, Private Bag 92019, Auckland 1023, New Zealand. (Email pd.gluckman@auckland.ac.nz)
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Abstract

In the last decades, the developmental origins of health and disease (DOHaD) have emerged as a vigorous field combining experimental, clinical, epidemiological and public health research. Its goal is to understand how events in early life shape later morbidity risk, especially of non-communicable chronic diseases. As these diseases become the major cause of morbidity and mortality worldwide, research arising from DOHaD is likely to gain significance to public health and economic development. But action may be hindered by the lack of a firm mechanistic explanation and of a conceptual basis, especially regarding the evolutionary significance of the DOHaD phenomenon. In this article, we provide a succinct historical review of the research into the relationship between development and later disease, consider the evolutionary and developmental significance and discuss the underlying mechanisms of the DOHaD phenomenon. DOHaD should be viewed as a part of a broader biological mechanism of plasticity by which organisms, in response to cues such as nutrition or hormones, adapt their phenotype to environment. These responses may be divided into those for immediate benefit and those aimed at prediction of a future environment: disease occurs in the mismatch between predicted and realized future. The likely mechanisms that enable plasticity involve epigenetic processes, affecting the expression of genes associated with regulatory pathways. There is now evidence that epigenetic marks may be inherited and so contribute to non-genomic heritable disease risk. We end by discussing the global significance of the DOHaD phenomenon and its potential applications for public health purposes.

Keywords

developmental origins of health and disease, life history, plasticity
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 1 , Issue 1 , February 2010 , pp. 6 - 18
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2009

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References

1.Goldstein, DB. Common genetic variation and human traits. N Engl J Med. 2009; 360, 1696–1698.CrossRefGoogle ScholarPubMed
2.Hirschhorn, JN. Genome-wide association studies – illuminating biologic pathways. N Engl J Med. 2009; 360, 1699–1701.CrossRefGoogle ScholarPubMed
3.Chi, KR. Human genetics: hit or miss? Nature. 2009; 461, 712–714.CrossRefGoogle ScholarPubMed
4.The Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature. 2007; 447, 661–678.CrossRefGoogle Scholar
5.Maher, B. Personal genomes: the case of the missing heritability. Nature. 2008; 456, 18–21.CrossRefGoogle ScholarPubMed
6.Hayden Check, E. Genomics shifts focus to rare diseases. Nature. 2009; 461, 458–459.CrossRefGoogle Scholar
7.Allis, CD, Jenuwein, T, Reinberg, D (eds) Epigenetics, 2007. Cold Spring Harbor Laboratory Press: Cold Spring Harbor: NY.Google Scholar
8.Amundsen, R. The Changing Role of the Embryo in Evolutionary Thought: Roots of Evo-Devo, 2005. Cambridge University Press: Cambridge.CrossRefGoogle Scholar
9.Gilbert, SF. Ecological developmental biology: developmental biology meets the real world. Dev Biol. 2001; 233, 1–12.CrossRefGoogle ScholarPubMed
10.Oyama, S. The Ontogeny of Information: Developmental Systems and Evolution, 1985. Cambridge University Press: Cambridge.Google Scholar
11.Kramer, MS, Joseph, KS. Enigma of fetal/infant-origins hypothesis. Lancet. 1996; 348, 1254–1255.CrossRefGoogle ScholarPubMed
12.Huxley, R, Neil, A, Collins, R. Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure? Lancet. 2002; 360, 659–665.CrossRefGoogle ScholarPubMed
13.Hopwood, N. Embryology. In The Cambridge History of Science, vol 6: the Modern Biological and Earth Sciences (eds. Bowler PJ, Pickstone JV), 2009; pp. 285–315. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
14.Richards, E. A political anatomy of monsters, hopeful and otherwise: teratogeny, transcendentalism, and evolutionary theorizing. Isis. 1994; 85, 377–411.Google ScholarPubMed
15.Oppenheimer, JM. Some historical relationships between teratology and experimental embryology. Bull Hist Med. 1968; 42, 145–159.Google ScholarPubMed
16.Gliboff, S. “Protoplasm…is soft wax in our hands”: Paul Kammerer and the art of biological transformation. Endeavour. 2005; 29, 162–167.CrossRefGoogle ScholarPubMed
17.Vargas, AO. Did Paul Kammerer discover epigenetic inheritance? a modern look at the controversial midwife toad experiments. J Exp Zool (Mol Dev Evo). 2009; 312B, 667–678.CrossRefGoogle Scholar
18.Roll-Hansen, N. The Lysenko Effect: The Politics of Science, 2005. Humanity Books: Amherst, NJ.Google Scholar
19.Kermack, W, McKendrick, A, McKinlay, P. Death rates in Great Britain and Sweden: some general regularities and their significance. Lancet. 1934; 223, 698–703.CrossRefGoogle Scholar
20.Dörner, G. Die mögliche Bedeutung der prä- und/oder perinatalen Ernährung für die Pathogenese der Obesitas. Acta Biol Med Ger. 1973; 30, 19–22.Google Scholar
21.Dörner, G, Götz, F. Hyperglikämie und Übergewicht in neonatal insulinbehandelten erwachsenen Rättenmänchen. Acta Biol Med Ger. 1972; 29, 467–470.Google Scholar
22.Dörner, G, Haller, K, Leonhardt, M. Zur möglichen Bedeutung der prä- und/oder früh postnatalen Ernährung für die Pathogenese der Arterioskleroze. Acta Biol Med Ger. 1973; 31, 31–35.Google Scholar
23.Dörner, G, Mohnike, A. Zur möglichen Bedeutung der prä- und/oder frühpostnatalen Ernährung für die Pathogenese der Diabetes Mellitus. Acta Biol Med Ger. 1973; 31, 7–10.Google ScholarPubMed
24.Dörner, G, Rodekamp, E, Plagemann, A. Maternal deprivation and overnutrition in early postnatal life and their primary prevention: historical reminiscence of an “ecological” experiment in Germany. Hum ontogenet. 2008; 2, 51–59.CrossRefGoogle Scholar
25.Lucas, A. Programming by early nutrition in man. (discussion 50-55) Ciba Found Symp. 1991; 156, 38–50.Google ScholarPubMed
26.Dörner, G. Günter Dörner, endocrinologist. Hum Ontogenet. 2008; 2, 5–9.CrossRefGoogle Scholar
27.Freinkel, N. Banting lecture 1980. Of pregnancy and progeny. Diabetes. 1980; 29, 1023–1035.CrossRefGoogle ScholarPubMed
28.De Prins, FA, Van Assche, FA. Intrauterine growth retardation and development of endocrine pancreas in the experimental rat. Biologia Neonatorum. 1982; 41, 16–21.Google Scholar
29.Aerts, L, Van Assche, FA. Is gestational diabetes an acquired condition? J Dev Physiol. 1979; 1, 219–225.Google ScholarPubMed
30.Forsdahl, A. Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease? Br J Prevent Soc Med. 1977; 31, 91–95.Google ScholarPubMed
31.Wadsworth, ME, Cripps, HA, Midwinter, RE, Colley, JR. Blood pressure in a national birth cohort at the age of 36 related to social and familial factors, smoking, and body mass. Br Med J (Clin Res Ed). 1985; 291, 1534–1538.Google Scholar
32.Notkola, V, Punsar, S, Karvonen, MJ, Haapakoski, J. Socio-economic conditions in childhood and mortality and morbidity caused by coronary heart disease in adulthood in rural Finland. Soc Sci Med. 1985; 21, 517–523.CrossRefGoogle ScholarPubMed
33.Barker, DJ, Osmond, C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986; 1, 1077–1081.CrossRefGoogle ScholarPubMed
34.Gennser, G, Rymark, P, Isberg, PE. Low birth weight and risk of high blood pressure in adulthood. Br Med J (Clin Res Ed). 1988; 296, 1498–1500.CrossRefGoogle ScholarPubMed
35.Pettitt, DJ, Aleck, KA, Baird, HR, Carraher, MJ, Bennett, PH, Knowler, WC. Congenital susceptibility to NIDDM. Role of intrauterine environment. Diabetes. 1988; 37, 622–628.CrossRefGoogle ScholarPubMed
36.Godfrey, K. The ‘developmental origins’ hypothesis: epidemiology. In Developmental Origins of Health and Disease (eds. Gluckman PD, Hanson MA), 2006; pp. 6–32. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
37.Cooper, C, Walker-Bone, K, Arden, N, Dennison, E. Novel insights into the pathogenesis of osteoporosis: the role of intrauterine programming. Rheumatology. 2000; 39, 1312–1315.CrossRefGoogle ScholarPubMed
38.Gale, CR, Martyn, CN. Birth weight and later risk of depression in a national birth cohort. Br J Psychiatry. 2004; 184, 28–33.CrossRefGoogle Scholar
39.Wahlbeck, K, Forsen, T, Osmond, C, Barker, DJP, Eriksson, JG. Association of schizophrenia with low maternal body mass index, small size at birth, and thinness during childhood. Arch Gen Psych. 2001; 58, 48–52.CrossRefGoogle ScholarPubMed
40.Barker, DJ, Godfrey, KM, Fall, C, et al. Relation of birth weight and childhood respiratory infection to adult lung function and death from chronic obstructive airways disease. Br Med J. 1991; 303, 671–675.CrossRefGoogle ScholarPubMed
41.Ahlgren, M, Melbye, M, Wohlfahrt, J, Sorensen, TIA. Growth patterns and the risk of breast cancer in women. New Engl J Med. 2004; 351, 1619–1626.CrossRefGoogle ScholarPubMed
42.Jefferis, BJMH, Power, C, Hertzman, C. Birth weight, childhood socioeconomic environment, and cognitive development in the 1958 British birth cohort study. Br Med J. 2002; 325, 305–311.CrossRefGoogle ScholarPubMed
43.Harding, JE. The nutritional basis of the fetal origins of adult disease. Int J Epidemiol. 2001; 30, 15–23.Google Scholar
44.McMullen, S, Mostyn, A. Animal models for the study of the developmental origins of health and disease. Proc Nutr Soc. 2009; 68, 306–320.Google Scholar
45.Mayr, E. Cause and effect in biology. Science. 1961; 134, 1501–1506.Google Scholar
46.Cohen, MN, Armelagos, GJ (eds) Paleopathology at the Origins of Agriculture. Academic Press: Orlando, 1984.Google Scholar
47.Neel, JV. Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am J Hum Genet. 1962; 14, 353–362.Google ScholarPubMed
48.Kuzawa, CW, Gluckman, PD, Hanson, MA, Fantuzzi, G, Mazzone, T. Developmental perspectives on the origin of obesity. In Adipose Tissue and Adipokines in Health and Disease (eds. Fantuzzi G, Mazzone T), 2007; pp. 207–219. Humana Press: Totowa, NJ.Google Scholar
49.Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595–601.CrossRefGoogle ScholarPubMed
50.Denver, R, Mirhadi, N, Phillips, M. Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology. 1998; 79, 1859–1872.Google Scholar
51.Reusens, B, Remacle, C. Programming of impaired insulin secretion versus sensitivity: cause or effect?. In Early Nutrition Programming and Health Outcomes in Later Life: Obesity and Beyond (eds. Koletzko B, Decsi T, Molnar D, de La Hunty A), 2009; pp. 125–131. Springer, Netherlands, Dordrecht.Google Scholar
52.Dawes, GS, Borruto, F, Zacutti, A (eds) Fetal Autonomy and Adaptation, 1990. Wiley: Chichester.Google Scholar
53.Bateson, P. Fetal experience and good adult design. Int J Epidemiol. 2001; 30, 928–934.Google Scholar
54.Gluckman, PD, Hanson, MA. Living with the past: evolution, development, and patterns of disease. Science. 2004; 305, 1733–1736.CrossRefGoogle ScholarPubMed
55.Bateson, P, Barker, D, Clutton-Brock, T, et al. Developmental plasticity and human health. Nature. 2004; 430, 419–421.CrossRefGoogle ScholarPubMed
56.Gluckman, PD, Hanson, MA, Spencer, HG, Bateson, P. Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc Royal Soc Lond B. 2005; 272, 671–677.Google ScholarPubMed
57.Gluckman, PD, Hanson, MA, Spencer, HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005; 20, 527–533.CrossRefGoogle ScholarPubMed
58.Gluckman, PD, Hanson, MA, Beedle, AS. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol. 2007; 19, 1–19.CrossRefGoogle ScholarPubMed
59.Applebaum, SW, Heifetz, Y. Density-dependent physiological phase in insects. Annu Rev Entomol. 1999; 44, 317–341.CrossRefGoogle ScholarPubMed
60.Desai, M, Gayle, D, Babu, J, Ross, MG. Programmed obesity in intrauterine growth restricted newborns: modulation by newborn nutrition. Am J Physiol. 2005; 288, R91–R96.Google Scholar
61.Sloboda, DM, Howie, GJ, Vickers, MH. Early-onset puberty in offspring after maternal undernutrition is exaggerated by a post-weaning high fat diet: sex specific evidence of nutritional mismatch. Early Hum Dev. 2007; 83(Suppl 1), S65–S66.CrossRefGoogle Scholar
62.Mitchell, A, Romano, GH, Groisman, B, et al. Adaptive prediction of environmental changes by microorganisms. Nature. 2009; 460, 220–224.CrossRefGoogle ScholarPubMed
63.Jablonka, E, Oborny, B, Molnar, I, et al. The adaptive advantage of phenotypic memory in changing environments. Philos Trans R Soc Lond B Biol Sci. 1995; 350, 133–141.Google ScholarPubMed
64.Moran, NA. The evolutionary maintenance of alternative phenotypes. Am Nat. 1992; 139, 971–989.CrossRefGoogle Scholar
65.Gluckman, PD, Hanson, MA. The Fetal Matrix: Evolution, Development, and Disease, 2005. Cambridge University Press: Cambridge.Google Scholar
66.Kuzawa, CW. Fetal origins of developmental plasticity: are fetal cues reliable predictors of future nutritional environments? Am J Hum Biol. 2005; 17, 5–21.Google Scholar
67.Bloomfield, FH, Oliver, MH, Hawkins, P, et al. A periconceptional nutritional origin for non-infectious preterm birth. Science. 2003; 300, 606.CrossRefGoogle Scholar
68.Ronnenberg, AG, Wang, X, Xing, H, et al. Low preconception body mass index is associated with birth outcome in a prospective cohort of Chinese women. J Nutr. 2003; 133, 3449–3455.Google Scholar
69.Boyne, MS, Thame, M, Bennett, FI, et al. The relationship among circulating insulin-like growth factor (IGF-1), IGF-binding proteins-1 and -2, and birth anthropometry: a prospective study. J Clin Endocrinol Metab. 2003; 88, 1687–1691.CrossRefGoogle ScholarPubMed
70.Wells, JCK. The thrifty phenotype as an adaptive maternal effect. Biol Rev Camb Philos Soc. 2007; 82, 143–172.CrossRefGoogle ScholarPubMed
71.Smith, CA. Effects of maternal undernutrition upon the newborn infant in Holland (1944–45). J Pediatr. 1947; 30, 229–243.CrossRefGoogle Scholar
72.Painter, RC, Roseboom, TJ, Bleker, OP. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol. 2005; 20, 345–352.Google Scholar
73.MacLaughlin, SM, Walker, SK, Roberts, CT, Kleemann, DO, McMillen, IC. Periconceptional nutrition and the relationship between maternal body weight changes in the periconceptional period and feto-placental growth in the sheep. J Physiol. 2005; 565, 111–124.CrossRefGoogle ScholarPubMed
74.Sloboda, DM, Hart, R, Doherty, DA, Pennell, CE, Hickey, M. Age at menarche: influences of prenatal and postnatal growth. J Clin Endocrinol Metab. 2007; 92, 46–50.Google Scholar
75.Gale, CR, Jiang, B, Robinson, SM, et al. Maternal diet during pregnancy and carotid intima-media thickness in children. Arterioscler Thromb Vasc Biol. 2006; 26, 1877–1882.Google Scholar
76.Gluckman, PD, Hanson, MA. Mismatch: Why our World no Longer fits our Bodies, 2006. Oxford University Press: Oxford.Google Scholar
77.Gluckman, PD, Hanson, MA. Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med. 2004; 9, 419–425.Google Scholar
78.Sultan, SE, Spencer, HG. Metapopulation structure favors plasticity over local adaptation. Am Nat. 2002; 160, 271–283.CrossRefGoogle ScholarPubMed
79.Cordain, L, Eaton, SB, Sebastian, A, et al. Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr. 2005; 81, 341–354.Google Scholar
80.Norman, JF, LeVeen, RF. Maternal atherogenic diet in swine is protective against early atherosclerosis development in offspring consuming an atherogeneic diet post-natally. Atherosclerosis. 2001; 157, 41–47.Google Scholar
81.Forsen, T, Eriksson, J, Tuomilehto, J, et al. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med. 2000; 133, 176–182.Google Scholar
82.Gluckman, PD, Hanson, MA, Beedle, AS, Raubenheimer, D. Fetal and neonatal pathways to obesity. Front Horm Res. 2008; 36, 61–72.CrossRefGoogle ScholarPubMed
83.Pettitt, DJ, Lawrence, JM, Beyer, J, et al. Association between maternal diabetes in utero and age at offspring’s diagnosis of type 2 diabetes. Diabetes Care. 2008; 31, 2126–2130.CrossRefGoogle ScholarPubMed
84.McCurdy, CE, Bishop, JM, Williams, SM, et al. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest. 2009; 119, 323–335.Google ScholarPubMed
85.Stettler, N, Tershakovec, AM, Zemel, BS, et al. Early risk factors for increased adiposity: a cohort study of African American subjects followed from birth to young adulthood. Am J Clin Nutr. 2000; 72, 378–383.Google Scholar
86.Lawlor, DA, Timpson, NJ, Harbord, RM, et al. Exploring the developmental overnutrition hypothesis using parental-offspring associations and FTO as an instrumental variable. PLoS Med. 2008; 5, 0484–0493.Google Scholar
87.Sloboda, DM, Howie, GJ, Pleasants, A, Gluckman, PD, Vickers, MH. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One. 2009; 4, 1–8.Google Scholar
88.Hanson, M, Fall, C, Robinson, S, Baird, J. Early Life Nutrition and Lifelong Health, 2009. British Medical Association: London.Google Scholar
89.Meaney, MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci. 2001; 24, 1161–1192.CrossRefGoogle Scholar
90.Ross, MG, Desai, M, Guerra, C, Wang, S. Prenatal programming of hypernatremia and hypertension in neonatal lambs. Am J Physiol. 2005; 288, R25–R33.Google Scholar
91.Diamond, J. Pearl Harbor and the Emperor’s physiologists. Nat Hist. 1991, 2–7.Google ScholarPubMed
92.Gluckman, PD, Hanson, MA, Cooper, C, Thornburg, KL. Effect of in utero and early-life conditions on adult health and disease. New Engl J Med. 2008; 359, 61–73.CrossRefGoogle ScholarPubMed
93.Bertram, C, Trowern, AR, Copin, N, Jackson, AA, Whorwood, CB. The maternal diet during pregnancy programs altered expression of the glucocorticoid receptor and type 2 11beta-hydroxysteroid dehydrogenase: potential molecular mechanisms underlying the programming of hypertension in utero. Endocrinology. 2001; 142, 2841–2853.Google Scholar
94.Reik, W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature. 2007; 447, 425–432.CrossRefGoogle ScholarPubMed
95.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.Google Scholar
96.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.CrossRefGoogle ScholarPubMed
97.Park, JH, Stoffers, DA, Nicholls, RD, Simmons, RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest. 2008; 118, 2316–2324.Google Scholar
98.Aagaard-Tillery, KM, Grove, K, Bishop, J, et al. Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol. 2008; 41, 91–102.CrossRefGoogle ScholarPubMed
99.Sinclair, KD, Allegrucci, C, Singh, R, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA. 2007; 104, 19351–19356.CrossRefGoogle ScholarPubMed
100.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.Google Scholar
101.Amaral, PP, Dinger, ME, Mercer, TR, Mattick, JS. The eukaryotic genome as an RNA machine. Science. 2008; 319, 1787–1789.CrossRefGoogle ScholarPubMed
102.Vickers, MH, Gluckman, PD, Coveny, AH, et al. Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005; 146, 4211–4216.CrossRefGoogle ScholarPubMed
103.Gluckman, PD, Lillycrop, KA, Vickers, MH, et al. Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci USA. 2007; 104, 12796–12800.Google Scholar
104.Bouret, SG, Simerly, RB. Leptin and development of hypothalamic feeding circuits. Endocrinology. 2004; 145, 2621–2626.CrossRefGoogle ScholarPubMed
105.Delahaye, F, Breton, C, Risold, PY, et al. Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology. 2008; 149, 470–475.Google Scholar
106.Morioka, T, Asilmaz, E, Hu, J, et al. Disruption of leptin receptor expression in the pancreas directly affects beta cell growth and function in mice. J Clin Invest. 2007; 117, 2860–2868.Google Scholar
107.Elinav, E, Niv-Spector, L, Price, TO, et al. Pegylated leptin antagonist is a potent orexigenic agent: preparation and mechanism of activity. Endocrinology. 2009; 150, 3083–3091.CrossRefGoogle ScholarPubMed
108.Stoffers, DA, Desai, BM, DeLeon, DD, Simmons, RA. Neonatal exendin-4 prevents the development of diabetes in the intrauterine growth retarded rat. Diabetes. 2003; 52, 734–740.CrossRefGoogle ScholarPubMed
109.Wyrwoll, CS, Mark, PJ, Mori, TA, Puddey, IB, Waddell, BJ. Prevention of programmed hyperleptinemia and hypertension by postnatal dietary omega-3 fatty acids. Endocrinology. 2006; 147, 599–606.Google Scholar
110.Whincup, PH, Gilg, JA, Papacosta, O, et al. Early evidence of ethnic differences in cardiovascular risk: cross sectional comparison of British South Asian and white children. Br Med J. 2002; 324, 1–6.CrossRefGoogle ScholarPubMed
111.Yajnik, CS, Fall, CHD, Coyaji, KJ, et al. Neonatal anthropometry: the thin-fat Indian baby. The Pune maternal nutrition study. Int J Obes. 2003; 27, 173–180.Google Scholar
112.Jahoor, F, Badaloo, A, Reid, M, et al. Unique metabolic characteristics of the major syndromes of severe childhood malnutrition. In The Tropical Metabolism Research Unit, The University of the West Indies, Jamaica 1956–2006: The House that John Built (eds. Forrester T, Picou D, Walker S), 2007; pp. 23–60. Ian Randle Publishers, Kingston.Google Scholar
113.Godfrey, KM, Gluckman, PD, Lillycrop, KA, et al. Epigenetic marks at birth predict childhood body composition at age 9 years. Abstract O-8A-72 presented at the 6th World Congress of Developmental Origins of Health and Disease, Santiago de Chile, November 2009. J DOHaD. 2009; 1(Suppl. 1), S44.Google Scholar
114.Jablonka, E, Raz, G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol. 2009; 84, 131–176.Google Scholar
115.Burdge, GC, Hanson, MA, Slater-Jeffries, JL, Lillycrop, KA. Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life? Br J Nutr. 2007; 97, 1036–1046.Google Scholar
116.Gluckman, PD, Hanson, MA, Beedle, AS. Non-genomic transgenerational inheritance of disease risk. Bioessays. 2007; 29, 149–154.Google Scholar
117.Waterland, RA, Travisano, M, Tahiliani, KG, Rached, MT, Mirza, S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes. 2008; 32, 1373–1379.Google Scholar
118.Arpanahi, A, Brinkworth, M, Iles, D, et al. Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Gen Res. 2009; 19, 1338–1349.Google Scholar
119.Anway, MD, Cupp, AS, Uzumcu, M, Skinner, MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005; 308, 1466–1469.CrossRefGoogle ScholarPubMed
120.Rassoulzadegan, M, Grandjean, V, Gounon, P, et al. RNA-mediated non-Mendelian inheritance of an epigenetic change in the mouse. Nature. 2006; 441, 469–474.Google Scholar
121.Ibáñez, L, Potau, N, Enriquez, G, Marcos, MV, DeZegher, F. Hypergonadotrophinaemia with reduced uterine and ovarian size in women born small-for-gestational-age. Hum Reprod. 2003; 18, 1565–1569.Google Scholar
122.Bossdorf, O, Richards, CL, Pigliucci, M. Epigenetics for ecologists. Ecol Lett. 2008; 11, 106–115.CrossRefGoogle ScholarPubMed
123.O’Flaherty, M, Ford, E, Allender, S, Scarborough, P, Capewell, S. Coronary heart disease trends in England and Wales from 1984 to 2004: concealed levelling of mortality rates among young adults. Heart. 2008; 94, 178–181.Google Scholar
124.WHO. Preventing Chronic Diseases: a Vital Investment. 2005. World Health Organization: Geneva.Google Scholar
125.Zhang, XL, Shu, XO, Yang, G, et al. Abdominal adiposity and mortality in Chinese women. Arch Int Med. 2007; 167, 886–892.Google Scholar
126.Gluckman, PD, Beedle, AS, Hanson, MA, Yap, EP. Developmental perspectives on individual variation: implications for understanding nutritional needs. In Personalized Nutrition for the Diverse Needs of Infants and Children (eds. Bier DM, German JB, Lonnerdal B), 2008; pp. 1–12. Karger, Basel.Google Scholar
127.Fall, CH, Stein, CE, Kumaran, K, et al. Size at birth, maternal weight, and type 2 diabetes in South India. Diabet Med. 1998; 15, 220–227.Google Scholar
128.Wong, L, Tan, ASA. The glucose challenge test for screening gestational diabetes in pregnant women with no risk factors. Singapore Med J. 2001; 42, 517–521.Google Scholar
129.Seshiah, V, Balaji, V, Balaji, MS, Sanjeevi, CB, Green, A. Gestational diabetes mellitus in India. J Assoc Physicians India. 2004; 52, 707–711.Google Scholar
130.Moore, SE, Cole, TJ, Collinson, AC, et al. Prenatal or early postnatal events predict infectious deaths in young adulthood in rural Africa. Int J Epidemiol. 1999; 28, 1088–1095.Google Scholar
131.Gluckman, PD, Hanson, MA, Bateson, P, et al. Towards a new developmental synthesis: adaptive developmental plasticity and human disease. Lancet. 2009; 373, 1654–1657.Google Scholar
132.Alderman, H, Behrman, JR. Estimated Economic Benefits of Reducing low Birth Weight in low-income Countries. Health, Nutrition and Population (HNP) Discussion Paper of the World Bank’s Human Development Network. 2004. World Bank: Washington, DC.Google Scholar
133.O’Connor, KC, Morton, SMB, Gluckman, PD. Modelling the economic antecedents and costs of low birth weight: multidimensional challenges in the international poor start to life project. Early Hum Dev. 2007; 83(Suppl 1), S39.Google Scholar
134.Butland, B, Jebb, S, Kopelman, P, et al. Tackling Obesities: Future Choices (Foresight Project Report), 2008. Government Office for Science: London.Google Scholar