Epigenetics and the Fetal Origins of Adult Health and Disease

  • Lawrence D. Longo
Chapter
Part of the Perspectives in Physiology book series (PHYSIOL, volume 1)

Abstract

Growth and development of the embryo and fetus, once the interest of only a minority of clinicians and public health officials, currently commands the attention of all concerned with the prevalence of a wide array of medical disorders in the adult. These include: diabetes and related metabolic syndrome, coronary artery disease, hypertension, schizophrenia and other neuropsychiatric diseases, as well as cancer and other conditions. As knowledge of human development has increased, evidence has amassed that the foundations for much of our life as adults, are established in our mother’s womb prior to birth. During the past several decades both a number of epidemiologic studies in humans and mechanistic-based experiments in laboratory animals, have given rise to the hypothesis of the “Developmental Origins of Health and Disease” (DOHaD) (Barker et al. 1993; Gluckman et al. 2008). Although much of the evidence is compelling, nonetheless controversy exists as to the basis for many of the associations drawn (Ben-Shlomo and Kuh 2002; Joseph and Kramer 1996; Kramer and Joseph 1996). Of particular relevance in this regard is nutrition. Commonly, we think of famine as a topic of the distant past or of malnutrition as being of limited scope (Delisle 2008). However, with the ever increasing population on the planet, limited resources, rise in commodity prices, and the role of politics in human well-being, the issue of proper nutrition or the lack thereof is a world-wide problem, and its relation to health and disease is of considerable relevance to biomedical scientists and members of the healing profession (Fig. 11.1).

Keywords

Cholesterol Obesity Ischemia Cortisol Nicotine 

References

  1. Aagaard-Tillery KM, Grove K, Bishop J, Ke X, Fu Q, McKnight R, Lane RH (2008) Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 41:91–102PubMedCrossRefGoogle Scholar
  2. Agin DP (2010) More than genes: what science can tell us about toxic chemicals, development, and the risk to our children. Oxford University Press, OxfordGoogle Scholar
  3. Allis CD, Jenuwein T, Reinberg D, Caparros ML (2007) Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  4. [Anonymous]. Editorial (1989) Thrifty genotype rendered detrimental by progress? Lancet 334:839–840CrossRefGoogle Scholar
  5. Anway MD, Skinner MK (2006) Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 147:S43–S49PubMedCrossRefGoogle Scholar
  6. Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466–1469PubMedCrossRefGoogle Scholar
  7. Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM, Nemeroff CB, Reyes TM, Simerly RB, Susser ES, Nestler EJ (2010) Early life programming and neurodevelopmental disorders. Biol Psychiatry 68:314–319PubMedCrossRefGoogle Scholar
  8. Barker DJ (1992) Fetal and infant origins of adult disease. British Medical Journal Publishing, LondonGoogle Scholar
  9. Barker DJ (1994) Mothers, babies, and health in later life. Churchill Livingstone, EdinburghGoogle Scholar
  10. Barker DJ (1995a) Fetal origins of coronary heart disease. Br Med J 311:171–174CrossRefGoogle Scholar
  11. Barker DJ (1995b) Intrauterine programming of adult disease. Mol Med Today 1:418–423PubMedCrossRefGoogle Scholar
  12. Barker DJ (1998a) Mothers, babies, and health in later life, 2nd edn. Churchill Livingstone, EdinburghGoogle Scholar
  13. Barker DJ (1998b) In utero programming of chronic disease. Clin Sci (Lond) 95:115–128CrossRefGoogle Scholar
  14. Barker DJ (2003) The midwife, the coincidence, and the hypothesis. Br Med J 327:1428–1430CrossRefGoogle Scholar
  15. Barker DJ (2004a) The developmental origins of chronic adult disease. Acta Paediatr Suppl 93:26–33PubMedCrossRefGoogle Scholar
  16. Barker DJ (2004b) Fetal origins of adult disease. In: Polin RA, Fox WW, Abman SH (eds) Fetal and neonatal physiology, vol 1, 3rd edn. Saunders, Philadelphia, PA, pp 160–165Google Scholar
  17. Barker DJ, Clark PM (1997) Fetal undernutrition and disease in later life. Rev Reprod 2:105–112PubMedCrossRefGoogle Scholar
  18. Barker DJ, Martyn CN (1992) The maternal and fetal origins of cardiovascular disease. J Epidemiol Community Health 46:8–11PubMedCrossRefGoogle Scholar
  19. Barker DJ, Osmond C (1986a) Diet and coronary heart disease in England and Wales during and after the Second World War. J Epidemiol Community Health 40:37–44PubMedCrossRefGoogle Scholar
  20. Barker DJ, Osmond C (1986b) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1:1077–1081PubMedCrossRefGoogle Scholar
  21. Barker DJ, Osmond C (1987) Death rates from stroke in England and Wales predicted from past maternal mortality. Br Med J 295:83–86CrossRefGoogle Scholar
  22. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME (1989a) Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. Br Med J 298:564–567CrossRefGoogle Scholar
  23. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ (1989b) Weight in infancy and death from ischaemic heart disease. Lancet 2:577–580PubMedCrossRefGoogle Scholar
  24. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS (1993) Fetal nutrition and cardiovascular disease in adult life. Lancet 341:938–941PubMedCrossRefGoogle Scholar
  25. Barker DJ, Sultant HY, Hanson MA, Rodeck CH, Spencer JAD (eds) (1995) Fetal programming of human disease. In Fetus and neonate, physiology and clinical applications, vol III, Growth. Cambridge University Press, Cambridge, pp 255–276Google Scholar
  26. Barker DJ, Eriksson JG, Forsén T, Osmond C (2002) Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 31:1235–1239PubMedCrossRefGoogle Scholar
  27. Bateson P, Barker D, Clutton-Brock T, Deb D, D’Udine B, Foley RA, Gluckman P, Godfrey K, Kirkwood T, Lahr MM, McNamara J, Metcalfe NB, Monaghan P, Spencer HG, Sultan SE (2004) Developmental plasticity and human health. Nature 430:419–421PubMedCrossRefGoogle Scholar
  28. Ben-Shlomo Y, Davey Smith G (1991) Deprivation in infancy or in adult life: which is more important for mortality risk? Lancet 337:530–534PubMedCrossRefGoogle Scholar
  29. Ben-Shlomo Y, Kuh D (2002) A life course approach to chronic disease epidemiology: conceptual models, empirical challenges and interdisciplinary perspectives. Int J Epidemiol 31:285–293PubMedCrossRefGoogle Scholar
  30. Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A (2009) An operational definition of epigenetics. Genes Dev 23:781–783PubMedCrossRefGoogle Scholar
  31. Bernstein BE, Meissner A, Lander ES (2007) The mammalian epigenome. Cell 128:669–681PubMedCrossRefGoogle Scholar
  32. Bird A (2007) Perceptions of epigenetics. Nature 447:396–398PubMedCrossRefGoogle Scholar
  33. Bonasio R, Tu S, Reinberg D (2010) Molecular signals of epigenetic states. Science 330:612–616PubMedCrossRefGoogle Scholar
  34. Borrelli E, Nestler EJ, Allis CD, Sassone-Corsi P (2008) Decoding the epigenetic language of neuronal plasticity. Neuron 60:961–974PubMedCrossRefGoogle Scholar
  35. Bota M, Dong HW, Swanson LW (2003) From gene networks to brain networks. Nat Neurosci 6:795–799PubMedCrossRefGoogle Scholar
  36. Brown AS, Susser ES (1997) Sex differences in prevalence of congenital neural defects after periconceptional famine exposure. Epidemiology 8:55–58PubMedCrossRefGoogle Scholar
  37. Brown AS, Susser ES (2008) Prenatal nutritional deficiency and risk of adult schizophrenia. Schizophr Bull 34:1054–1063PubMedCrossRefGoogle Scholar
  38. Brown AS, van Os J, Driessens C, Hoek HW, Susser ES (2000) Further evidence of relation between prenatal famine and major affective disorder. Am J Psychiatry 157:190–195PubMedCrossRefGoogle Scholar
  39. Burger GCE, Drummond JC, Sandstead HR (eds) (1948) Malnutrition and starvation in Western Netherlands, September 1944–July 1945. Parts I and II. General State Printing Office, The Hague, NetherlandsGoogle Scholar
  40. Chen Y, Zhou LA (2007) The long-term health and economic consequences of the 1959–1961 famine in China. J Health Econ 26:659–681PubMedCrossRefGoogle Scholar
  41. Cooney CA, Dave AA, Wolff GL (2002) Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr 132:2393S–2400SPubMedGoogle Scholar
  42. Crews D, Gore AC, Hsu TS, Dangleben NL, Spinetta M, Schallert T, Anway MD, Skinner MK (2007) Transgenerational epigenetic imprints on mate preference. Proc Natl Acad Sci U S A 104:5942–5946PubMedCrossRefGoogle Scholar
  43. De Groot RH, Stein AD, Jolles J, van Boxtel MP, Blauw GJ, van der Bor M, Lumey L (2011) Prenatal famine exposure and cognition at age 59 years. Int J Epidemiol 40:327–337PubMedCrossRefGoogle Scholar
  44. De Rooij SR, Roseboom TJ (2010) Further evidence for an association between self-reported health and cardiovascular as well as cortisol reactions to acute psychological stress. Psychophysiology 47:1172–1175PubMedGoogle Scholar
  45. De Rooij SR, Painter RC, Phillips DIW, Osmond C, Michels RPJ, Godsland IF, Bossuyt PMM, Bleker OP, Roseboom TJ (2006a) Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care 29:1897–1901PubMedCrossRefGoogle Scholar
  46. De Rooij SR, Painter RC, Phillips DIW, Osmond C, Tanck MWT, Defesche JC, Bossuyt PMM, Michels RPJ, Bleker OP, Roseboom TJ (2006b) The effects of the Pro12Ala polymorphism of the peroxisome proliferator-activated receptor-γ2 gene on glucose/insulin metabolism interact with prenatal exposure to famine. Diabetes Care 29:1052–1057PubMedCrossRefGoogle Scholar
  47. De Rooij SR, Painter RC, Roseboom TJ, Phillips DIW, Osmond C, Barker DJP, Tanck MW, Michels RPJ, Bossuyt PMM, Bleker OP (2006c) Glucose tolerance at age 58 and the decline of glucose tolerance in comparison with age 50 in people prenatally exposed to the Dutch famine. Diabetologia 49:637–643PubMedCrossRefGoogle Scholar
  48. De Rooij SR, Painter RC, Holleman F, Bossuyt PMM, Roseboom TJ (2007) The metabolic syndrome in adult prenatally exposed to the Dutch famine. Am J Clin Nutr 86:1219–1224PubMedGoogle Scholar
  49. De Rooij SR, Wouters H, Yonker JE, Painter RC, Roseboom TJ (2010) Prenatal undernutrition and cognitive function in late adulthood. Proc Natl Acad Sci U S A 107:16881–16886PubMedCrossRefGoogle Scholar
  50. Delisle HF (2008) Poverty: the double burden of malnutrition in mothers and the intergenerational impact. Ann N Y Acad Sci 1136:172–184PubMedCrossRefGoogle Scholar
  51. Devaskar SU, Raychaudhuri S (2007) Epigenetics – a science of heritable biological adaptation. Pediatr Res 61:1R–4RPubMedCrossRefGoogle Scholar
  52. Dodd IB, Micheelsen MA, Sneppen K, Thon G (2007) Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 129:813–822PubMedCrossRefGoogle Scholar
  53. Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM (2000) Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod 62:1526–1535PubMedCrossRefGoogle Scholar
  54. Dolinoy DC, Das R, Weidman JR, Jirtle RL (2007a) Metastable epialleles, imprinting, and the fetal origins of adult diseases. Pediatr Res 61:30R–37RPubMedCrossRefGoogle Scholar
  55. Dolinoy DC, Weidman JR, Jirtle RL (2007b) Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod Toxicol 23:297–307PubMedCrossRefGoogle Scholar
  56. Drake AJ, Walker BR (2004) The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk. J Endocrinol 180:1–16PubMedCrossRefGoogle Scholar
  57. Elder GH Jr (1994) Time, human agency, and social change: perspectives on the life course. Soc Psychol Q 57:4–15CrossRefGoogle Scholar
  58. Elford J, Whincup P, Shaper AG (1991) Early life experience and adult cardiovascular disease: longitudinal and case–control studies. Int J Epidemiol 20:833–844PubMedCrossRefGoogle Scholar
  59. Elford J, Shaper AG, Whincup P (1992) Early life experience and cardiovascular disease – ecological studies. J Epidemiol Community Health 46:1–11PubMedCrossRefGoogle Scholar
  60. Elias SG, van Noord PAH, Peeters PHM, den Tonkelaar I, Grobbee DE (2003) Caloric restriction reduces age at menopause: the effect of the 1944–1945 Dutch famine. Menopause 10:399–405PubMedCrossRefGoogle Scholar
  61. Elias SG, Keinan-Boker L, Peeters PHM, Van Gils CH, Kaaks R, Grobbee DE, van Noord PAH (2004a) Long term consequences of the 1944–1945 Dutch famine on the insulin-like growth factor axis. Int J Cancer 108:628–630PubMedCrossRefGoogle Scholar
  62. Elias SG, Peeters PHM, Grobbee DE, van Noord PAH (2004b) Breast cancer risk after caloric restriction during the 1944–1945 Dutch famine. J Natl Cancer Inst 96:539–546PubMedCrossRefGoogle Scholar
  63. Elias SG, van Noord PAH, Peeters PHM, den Tonkelaar I, Grobbee DE (2005) Childhood exposure to the 1944–1945 Dutch famine and subsequent female reproductive function. Hum Reprod 20:2483–2488PubMedCrossRefGoogle Scholar
  64. Eriksson JG, Forsén T, Tuomilehto J, Winter PD, Osmond C, Barker DJP (1999) Catch-up growth in childhood and death from coronary heart disease: longitudinal study. BMJ 318:427–431PubMedCrossRefGoogle Scholar
  65. Fagiolini M, Jensen CL, Champagne FA (2009) Epigenetic influences on brain development and plasticity. Curr Opin Neurobiol 19:207–212PubMedCrossRefGoogle Scholar
  66. Feinberg AP (2007) Phenotypic plasticity and the epigenetics of human disease. Nature 447:433–440PubMedCrossRefGoogle Scholar
  67. Feng J, Fouse S, Fan G (2007) Epigenetic regulation of neural gene expression and neuronal function. Pediatr Res 61:58R–63RPubMedCrossRefGoogle Scholar
  68. Finch JT, Lutter LC, Rhodes D, Brown RS, Rushton B, Levitt M, Klug A (1977) Structure of nucleosome core particles of chromatin. Nature 269:29–36PubMedCrossRefGoogle Scholar
  69. Floud R, Wachter K, Gregory A (1990) Height, health and history. Nutritional status in the United Kingdom, 1750–1980. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  70. Forsdahl A (1973) Points which enlighten the high mortality rate in the county of Finnmark. Can the high mortality rate today be a consequence of bad conditions of life in childhood and adolescence? Tidsskr Nor Laegeforen 93:661–667PubMedGoogle Scholar
  71. Forsdahl A (1977) Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease? Br J Prev Soc Med 31:91–95PubMedGoogle Scholar
  72. Forsdahl A (1978) Living conditions in childhood and subsequent development of risk factors for arteriosclerotic heart disease. The cardiovascular survey in Finnmark 1974–75. J Epidemiol Community Health 32:34–37PubMedCrossRefGoogle Scholar
  73. Fox SE, Levitt P, Nelson CA III (2010) How the timing and quality of early experiences influence the development of brain architecture. Child Dev 81:28–40PubMedCrossRefGoogle Scholar
  74. Franklin TB, Mansuy IM (2010) Epigenetic inheritance in mammals: evidence for the impact of adverse environmental effects. Neurobiol Dis 39:61–65PubMedCrossRefGoogle Scholar
  75. Franzek EJ, Sprangers N, Janssens AC, Van Duijn CM, Van De Wetering BJ (2008) Prenatal exposure to the 1944–45 Dutch ‘hunger winter’ and addiction later in life. Addiction 103:433–438PubMedCrossRefGoogle Scholar
  76. Gheorghe CP, Goyal R, Mittal A, Longo LD (2010) Gene expression in the placenta: maternal stress and epigenetic responses. Int J Dev Biol 54:507–523PubMedCrossRefGoogle Scholar
  77. Gluckman PD, Hanson MA (2006) Mismatch: why our world no longer fits our bodies. Oxford University Press, OxfordGoogle Scholar
  78. Gluckman PD, Hanson MA, Cooper C, Thornburg KL (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359:61–73PubMedCrossRefGoogle Scholar
  79. Godfrey KM, Barker DJ (2001) Fetal programming and adult health. Public Health Nutr 4:611–624PubMedCrossRefGoogle Scholar
  80. Goldberg AD, Allis CD, Bernstein E (2007) Epigenetics: a landscape takes shape. Cell 128:635–638PubMedCrossRefGoogle Scholar
  81. Götz AA, Wittlinger S, Stefanski V (2007) Maternal social stress during pregnancy alters immune function and immune cell numbers in adult male Long-Evans rat offspring during stressful life-events. J Neuroimmunol 185:95–102PubMedCrossRefGoogle Scholar
  82. Goyal R, Longo LD (2012) Maternal protein deprivation: sexually dimorphic programming of hypertension in the mouse. Hypertens Res 36:29–35PubMedCrossRefGoogle Scholar
  83. Goyal R, Galffy A, Field SA, Gheorghe CP, Mittal A, Longo LD (2009) Maternal protein deprivation: changes in systemic renin-angiotensin system of the mouse fetus. Reprod Sci 16:894–904PubMedCrossRefGoogle Scholar
  84. Goyal R, Goyal D, Leitzke A, Gheorghe CP, Longo LD (2010) Brain renin-angiotensin system: fetal epigenetic programming by maternal protein restriction during pregnancy. Reprod Sci 17:227–238PubMedCrossRefGoogle Scholar
  85. Goyal R, Leitzke A, Goyal D, Gheorghe CP, Longo LD (2011a) Antenatal maternal hypoxic stress: epigenetic adaptations in fetal lung renin-angiotensin system. Reprod Sci 18:180–189PubMedCrossRefGoogle Scholar
  86. Goyal R, Lister R, Goyal D, Gheorghe CP, Longo LD (2011b) Antenatal maternal hypoxic stress: adaptations of the placental renin-angiotensin system in the mouse. Placenta 32:134–139PubMedCrossRefGoogle Scholar
  87. Goyal R, Wong C, Van Wickle J, Longo LD (2013) Antenatal maternal protein deprivation: sexually dimorphic programming of the pancreatic renin-angiotensin system. J Renin Angiotensin Aldosterone Syst 14:137–145PubMedCrossRefGoogle Scholar
  88. Green LR, Hanson MA (2004) Programming of the fetal circulation. In: Polin RA, Fox WW, Abman SH (eds) Fetal and neonatal physiology, vol 1, 3rd edn. Saunders, Philadelphia, PA, pp 727–732Google Scholar
  89. Hales CN, Barker DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595–601PubMedCrossRefGoogle Scholar
  90. Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5–20PubMedCrossRefGoogle Scholar
  91. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD (1991) Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303:1019–1022PubMedCrossRefGoogle Scholar
  92. Halfon N, Hochstein M (2002) Life course health development: an integrated framework for developing health, policy, and research. Milbank Q 80:433–479PubMedCrossRefGoogle Scholar
  93. Hanson MA, Gluckman PD (2005) Developmental processes and the induction of cardiovascular function: conceptual aspects. J Physiol (Lond) 565:27–34CrossRefGoogle Scholar
  94. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 105:17046–17049PubMedCrossRefGoogle Scholar
  95. Hertz-Picciotto I, Park H-Y, Dostal M, Kocan A, Trnovec T, Sram R (2008) Prenatal exposures to persistent and non-persistent organic compounds and effects on immune system development. Basic Clin Pharmacol Toxicol 102:146–154PubMedCrossRefGoogle Scholar
  96. Hoek HW, Susser E, Buck KA, Lumey LH, Lin SP, Gorman JM (1996) Schizoid personality disorder after prenatal exposure to famine. Am J Psychiatry 153:1637–1639PubMedGoogle Scholar
  97. Holness MJ, Sugden MC (2006) Epigenetic regulation of metabolism in children born small for gestational age. Curr Opin Clin Nutr Metab Care 9:482–488PubMedCrossRefGoogle Scholar
  98. Huang C, Li Z, Wang M, Martorell R (2010) Early life exposure to the 1959–1961 Chinese famine has long-term health consequences. J Nutr 140:1874–1878PubMedCrossRefGoogle Scholar
  99. Hulshoff Pol HE, Hoek HW, Susser E, Brown AS, Dingemans A, Schnack HG, van Haren NE, Pereira Ramos LM, Gispen-de Wied CC, Kahn RS (2000) Prenatal exposure to famine and brain morphology in schizophrenia. Am J Psychiatry 157:1170–1172PubMedCrossRefGoogle Scholar
  100. Hult M, Tornhammar P, Ueda P, Chima C, Bonamy AK, Ozumba B, Norman M (2010) Hypertension, diabetes and overweight: looming legacies of the Biafran famine. PLoS One 5:e13582PubMedCrossRefGoogle Scholar
  101. Huxley RR, Neil HA (2004) Does maternal nutrition in pregnancy and birth weight influence levels of CHD risk factors in adult life? Br J Nutr 91:459–468PubMedCrossRefGoogle Scholar
  102. Huxley RR, Lloyd BB, Goldacre M, Neil HA (2000) Nutritional research in World War 2: the Oxford Nutrition Survey and its research potential 50 years later. Br J Nutr 84:247–251PubMedGoogle Scholar
  103. 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 360:659–665PubMedCrossRefGoogle Scholar
  104. Jablonka E, Lamb MJ (2002) The changing concept of epigenetics. Ann NY Acad Sci 981:82–96PubMedCrossRefGoogle Scholar
  105. Jansson T, Powell TL (2007) Role of the placenta in fetal programming: underlying mechanisms and potential interventional approaches. Clin Sci 113:1–13PubMedCrossRefGoogle Scholar
  106. Jirtle RL, Skinner MK (2007) Environmental epigenomics and disease susceptibility. Nat Rev Genet 8:253–262PubMedCrossRefGoogle Scholar
  107. Joseph KS, Kramer MS (1996) Review of the evidence on fetal and early childhood antecedents of adult chronic disease. Epidemiol Rev 18:158–174PubMedCrossRefGoogle Scholar
  108. Kahn HS, Graff M, Stein AD, Zybert PA, McKeague IW, Lumey LH (2008) A fingerprint characteristic associated with the early prenatal environment. Am J Hum Biol 20:59–65PubMedCrossRefGoogle Scholar
  109. Kannel WB, Dawber TR (1972) Atherosclerosis as a pediatric problem. J Pediatr 80:544–554PubMedCrossRefGoogle Scholar
  110. Kermack WO, McKendrick AG, McKinlay PL (1934) Death-rates in Great Britain and Sweden. Some general regularities and their significance. Lancet 1:698–703CrossRefGoogle Scholar
  111. Klose RJ, Kallin EM, Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7:715–727PubMedCrossRefGoogle Scholar
  112. Kramer MS, Joseph KS (1996) Enigma of fetal/infant-origins hypothesis. Lancet 348:1254–1255PubMedCrossRefGoogle Scholar
  113. Kyle UG, Pichard C (2006) The Dutch Famine of 1944–1945: a pathophysiological model of long-term consequences of wasting disease. Curr Opin Clin Nutr Metab Care 9:388–394PubMedCrossRefGoogle Scholar
  114. Landrigan PJ, Kimmel CA, Correa A, Eskenazi B (2004) Children’s health and the environment: public health issues and challenges for risk assessment. Environ Health Perspect 112:257–265PubMedCrossRefGoogle Scholar
  115. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J, Reik W (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35:88–93PubMedCrossRefGoogle Scholar
  116. Law CM, Shiell AW (1996) Is blood pressure inversely related to birth weight? The strength of evidence from a systematic review of the literature. J Hypertens 14:935–941PubMedCrossRefGoogle Scholar
  117. Lawrence J, Xiao D, Xue Q, Rejali M, Yang S, Zhang L (2008) Prenatal nicotine exposure increases heart susceptibility to ischemia/reperfusion injury in adult offspring. J Pharmacol Exp Ther 324:331–341PubMedCrossRefGoogle Scholar
  118. Li Y, He Y, Qi L, Jaddoe W, Feskens EJ, Yang X, Ma G, Hu FB (2010) Exposure to the Chinese famine in early life and the risk of hyperglycemia and type 2 diabetes in adulthood. Diabetes 59:2400–2406PubMedCrossRefGoogle Scholar
  119. Li Y, Xiao D, Dasgupta C, Xiong F, Tong W, Yang S, Zhang L (2012) Perinatal nicotine exposure increases vulnerability of hypoxic-ischemic brain injury in neonatal rats: role of angiotensin II receptors. Stroke 43:2483–2490PubMedCrossRefGoogle Scholar
  120. Lopuhaa CE, Roseboom TJ, Osmond C, Barker DJ, Ravelli AC, Bleker OP, van der Zee JS, van der Meulen JH (2000) Atopy, lung function, and obstructive airways disease after prenatal exposure to famine. Thorax 55:555–561PubMedCrossRefGoogle Scholar
  121. Lucas A (1991) Programming by early nutrition in man. Ciba Found Symp 156:38–55PubMedGoogle Scholar
  122. Lucas A, Morley R (1994) Does early nutrition in infants born before term programme later blood pressure? BMJ 309:304–308PubMedCrossRefGoogle Scholar
  123. Lucas A, Fewtrell MS, Cole TJ (1999) Fetal origins of adult disease – the hypothesis revisited. BMJ 319:245–249PubMedCrossRefGoogle Scholar
  124. Lumey LH, Ravelli ACJ, Wiessing LG, Koppe JG, Treffers PE, Stein ZA (1993) The Dutch famine birth cohort study: design, validation of exposure, and selected characteristics of subjects after 43 years follow-up. Paediatr Perinat Epidemiol 7:354–367PubMedCrossRefGoogle Scholar
  125. Lumey LH, Stein AD, Kahn HS, Romijn JA (2009) Lipid profiles in middle-aged men and women after famine exposure during gestation: the Dutch Hunger Winter Families Study. Am J Clin Nutr 89:1737–1743PubMedCrossRefGoogle Scholar
  126. Lumey LH, Stein AD, Susser E (2011) Prenatal famine and adult health. Annu Rev Public Health 32:237–262PubMedCrossRefGoogle Scholar
  127. Lussana F, Painter RC, Ocke MC, Buller HR, Bossuyt PM, Roseboom TJ (2008) Prenatal exposure to the Dutch famine is associated with a preference for fatty foods and a more atherogenic lipid profile. Am J Clin Nutr 88:1648–1652PubMedCrossRefGoogle Scholar
  128. Lynch J, Davey Smith G (2005) A life course approach to chronic disease epidemiology. Annu Rev Public Health 26:1–35PubMedCrossRefGoogle Scholar
  129. Mao C, Zhang H, Xiao D, Zhu L, Ding Y, Zhang Y, Wu L, Xu Z, Zhang L (2008) Perinatal nicotine exposure alters AT1 and AT2 receptor expression pattern in the brain of fetal and offspring rats. Brain Res 1243:47–52PubMedCrossRefGoogle Scholar
  130. Martin C, Zhang Y (2005) The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 6:838–849PubMedCrossRefGoogle Scholar
  131. Martyn CN, Barker DJ, Osmond C (1996) Mothers’ pelvic size, fetal growth, and death from stroke and coronary heart disease in men in the UK. Lancet 348:1264–1268PubMedCrossRefGoogle Scholar
  132. Martyn CN, Gale CR, Jespersen S, Sherriff SB (1998) Impaired fetal growth and atherosclerosis of carotid and peripheral arteries. Lancet 352:173–178PubMedCrossRefGoogle Scholar
  133. McEwen BS (2004) Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann N Y Acad Sci 1032:1–7PubMedCrossRefGoogle Scholar
  134. McKinney WT Jr, Bunney WE Jr (1969) Animal model of depression. I. Review of evidence: implications for research. Arch Gen Psychiat 21:240–248PubMedCrossRefGoogle Scholar
  135. Merlot E, Couret D, Otten W (2008) Prenatal stress, fetal imprinting and immunity. Brain Behav Immun 22:42–51PubMedCrossRefGoogle Scholar
  136. Meyer K, Zhang L (2007) Fetal programming of cardiac function and disease. Reprod Sci 14:209–216PubMedCrossRefGoogle Scholar
  137. Monk M (1988) Genomic imprinting. Genes Dev 2:921–925PubMedCrossRefGoogle Scholar
  138. Morgan HD, Sutherland HGE, Martin DIK, Whitelaw E (1999) Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23:314–318PubMedCrossRefGoogle Scholar
  139. Morgan HD, Jin XL, Li A, Whitelaw E, O’Neil C (2008) The culture of zygotes to the blastocyst stage changes the postnatal expression of an epigenetically labile allele, agouti viable yellow, in mice. Biol Reprod 79:618–623PubMedCrossRefGoogle Scholar
  140. Morgane PJ, Austin-LaFrance R, Bronzino J, Tonkiss J, Diaz-Cintra S, Cintra L, Kemper T, Galler JR (1993) Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev 17:91–128PubMedCrossRefGoogle Scholar
  141. Mullin PM, Ching C, Schoenberg F, MacGibbon K, Romero R, Goodwin TM, Fejzo MS (2012) Risk factors, treatments, and outcomes associated with prolonged hyperemesis gravidarum. J Matern Fetal Neonatal Med 25:632–636PubMedCrossRefGoogle Scholar
  142. Murrell A, Rakyan VK, Beck S (2005) From genome to epigenome. Hum Molec Genet 14(Suppl 1):R3–R10PubMedCrossRefGoogle Scholar
  143. Nanney DL (1958) Epigenetic control systems. Proc Natl Acad Sci U S A 44:712–717PubMedCrossRefGoogle Scholar
  144. Neel JV (1962) Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am J Hum Genet 14:353–362PubMedGoogle Scholar
  145. Neugebauer R (2005) Accumulating evidence for prenatal nutritional origins of mental disorders. JAMA 294:621–623PubMedCrossRefGoogle Scholar
  146. Neugebauer R, Hoek HW, Susser E (1999) Prenatal exposure to wartime famine and development of antisocial personality disorder in early adulthood. JAMA 282:455–462PubMedCrossRefGoogle Scholar
  147. Nijland MJ, Ford SP, Nathanielsz PW (2008) Prenatal origins of adult disease. Curr Opin Obstet Gynecol 20:132–138PubMedCrossRefGoogle Scholar
  148. Olness K (2003) Effects on brain development leading to cognitive impairment: a worldwide epidemic. J Dev Behav Pediatr 24:120–130PubMedCrossRefGoogle Scholar
  149. Ong KK, Dunger DB (2000) Thrifty genotypes and phenotypes in the pathogenesis of type 2 diabetes mellitus. J Pediatr Endocrinol Metab 13(Suppl 6):1419–1424PubMedGoogle Scholar
  150. Osmond C, Barker DJ, Winter PD, Fall CH, Simmonds SJ (1993) Early growth and death from cardiovascular disease in women. Br Med J 307:1519–1524CrossRefGoogle Scholar
  151. Painter RC, Roseboom TJ, Bleker OP (2005a) Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol 20:345–352PubMedCrossRefGoogle Scholar
  152. Painter RC, Roseboom TJ, Bossuyt PMM, Osmond C, Barker DJP, Bleker OP (2005b) Adult mortality at age 57 after prenatal exposure to the Dutch famine. Eur J Epidemiol 20:673–676PubMedCrossRefGoogle Scholar
  153. Painter RC, Roseboom TJ, van Montfrans GA, Bossuyt PM, Krediet RT, Osmond C, Barker DJ, Bleker OP (2005c) Microalbuminuria in adults after prenatal exposure to the Dutch famine. J Am Soc Nephrol 16:189–194PubMedCrossRefGoogle Scholar
  154. Painter RC, de Rooij SR, Bossuyt PM, Osmond C, Barker DJ, Bleker OP, Roseboom TJ (2006a) A possible link between prenatal exposure to famine and breast cancer: a preliminary study. Am J Hum Biol 18:853–856PubMedCrossRefGoogle Scholar
  155. Painter RC, de Rooij SR, Bossuyt PM, Phillips DI, Osmond C, Barker DJ, Bleker OP, Roseboom TJ (2006b) Blood pressure response to psychological stressors in adults after prenatal exposure to the Dutch famine. J Hypertens 24:1771–1778PubMedCrossRefGoogle Scholar
  156. Painter RC, de Rooij SR, Bossuyt PM, Simmers TA, Osmond C, Barker DJ, Bleker OP, Roseboom TJ (2006c) Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am J Clin Nutr 84:322–327PubMedGoogle Scholar
  157. Painter RC, de Rooij SR, Bossuyt PM, de Groot E, Stok WJ, Osmond C, Barker DJ, Bleker OP, Roseboom TJ (2007a) Maternal nutrition during gestation and carotid arterial compliance in the adult offspring: the Dutch famine birth cohort. J Hypertens 25:533–540PubMedCrossRefGoogle Scholar
  158. Painter RC, de Rooij SR, Hutten BA, Bossuyt PM, de Groot E, Osmond C, Barker DJ, Bleker OP, Roseboom TJ (2007b) Reduced intima media thickness in adults after prenatal exposure to the Dutch famine. Atherosclerosis 193:421–427PubMedCrossRefGoogle Scholar
  159. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DIW, Roseboom TJ (2008a) Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 115:1243–1249PubMedCrossRefGoogle Scholar
  160. Painter RC, Westendorp RGJ, de Rooij SR, Osmond C, Barker DJ, Roseboom TJ (2008b) Increased reproduction success of women after prenatal undernutrition. Hum Reprod 23:2591–2595PubMedCrossRefGoogle Scholar
  161. Paul AM (2010) Origins. How the nine months before birth shape the rest of our lives. Free Press, New York, NYGoogle Scholar
  162. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjöström M, Golding J, ALSPAC Study Team (2006) Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 14:159–166PubMedCrossRefGoogle Scholar
  163. Petronis A (2010) Epigenetics as a unifying principle in the aetiology of complex traits and diseases. Nature 465:721–727PubMedCrossRefGoogle Scholar
  164. Prentice AM, Rayco-Solon P, Moore SE (2005) Insights from the developing world: thrifty genotypes and thrifty phenotypes. Proc Nutr Soc 64:153–161PubMedCrossRefGoogle Scholar
  165. Pryce CR, Ruedi-Bettschen D, Dettling AC, Feldon J (2002) Early life stress: long-term physiological impact in rodents and primates. News Physiol Sci 17:150–155PubMedGoogle Scholar
  166. Rahnama F, Shafiei F, Gluckman PD, Mitchell MD, Lobie PE (2006) Epigenetic regulation of human trophoblastic cell migration and invasion. Endocrinology 147:5275–5283PubMedCrossRefGoogle Scholar
  167. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV, Whitelaw E (2003) Transgenerational inheritance of epigenetic states at the murine Axin Fu allele occurs after maternal and paternal transmission. Proc Natl Acad Sci U S A 100:2538–2543PubMedCrossRefGoogle Scholar
  168. Ravelli AC, van der Meulen JH, Michels RP, Osmond C, Barker DJ, Hales CN, Bleker OP (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet 351:173–177PubMedCrossRefGoogle Scholar
  169. Ravelli AC, van der Meulen JH, Osmond C, Barker DJ, Bleker OP (1999) Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr 70:811–816PubMedGoogle Scholar
  170. Reik W (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447:425–432PubMedCrossRefGoogle Scholar
  171. Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293:1089–1093PubMedCrossRefGoogle Scholar
  172. Reynolds RM, Godfrey KM, Barker M, Osmond C, Phillips DI (2007) Stress responsiveness in adult life: influence of mother’s diet in late pregnancy. J Clin Endocrinol Metab 92:2208–2210PubMedCrossRefGoogle Scholar
  173. Richards M, Hardy R, Kuh D, Wadsworth ME (2001) Birth weight and cognitive function in the British 1946 birth cohort: longitudinal population based study. BMJ 322:199–203PubMedCrossRefGoogle Scholar
  174. Robinson JJ (1977) The influence of maternal nutrition on ovine foetal growth. Proc Nutr Soc 36:9–16PubMedCrossRefGoogle Scholar
  175. Rose G (1964) Familial patterns in ischaemic heart disease. Br J Prev Soc Med 18:75–80PubMedGoogle Scholar
  176. Roseboom TJ, van der Meulen JH, Ravelli AC, van Montfrans GA, Osmond C, Barker DJ, Bleker OP (1999) Blood pressure in adults after prenatal exposure to famine. J Hypertens 17:325–330PubMedCrossRefGoogle Scholar
  177. Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Bleker OP (2000a) Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. Am J Clin Nutr 72:1101–1106PubMedGoogle Scholar
  178. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP (2000b) Plasma fibrinogen and factor VII concentrations in adults after prenatal exposure to famine. Br J Haematol 111:112–117PubMedCrossRefGoogle Scholar
  179. Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Bleker OP (2001a) Adult survival after prenatal exposure to the Dutch famine 1944–45. Paediatr Perinat Epidemiol 15:220–225PubMedCrossRefGoogle Scholar
  180. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP (2001b) Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol 185:93–98PubMedCrossRefGoogle Scholar
  181. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP (2001c) Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Twin Res 4:293–298PubMedGoogle Scholar
  182. Roseboom TJ, van der Meulen JH, van Montfrans GA, Ravelli AC, Osmond C, Barker DJ, Bleker OP (2001d) Maternal nutrition during gestation and blood pressure in later life. J Hypertens 19:29–34PubMedCrossRefGoogle Scholar
  183. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP (2003) Perceived health of adults after prenatal exposure to the Dutch famine. Paediatr Perinat Epidemiol 17:391–397PubMedCrossRefGoogle Scholar
  184. Roseboom TJ, de Rooij S, Painter R (2006) The Dutch famine and its long-term consequences for adult health. Early Hum Dev 82:485–491PubMedCrossRefGoogle Scholar
  185. Russo VEA, Martienssen RA, Riggs AD (eds) (1996) Epigenetic mechanisms of gene regulation. Cold Spring Harbor Laboratory Press, Woodbury, NYGoogle Scholar
  186. Sarma K, Reinberg D (2005) Histone variants meet their match. Nat Rev Mol Cell Biol 6:139–149PubMedCrossRefGoogle Scholar
  187. Sayer AA, Cooper C, Evans JR, Rauf A, Wormald RPL, Osmond C, Barker DJ (1998) Are rates of ageing determined in utero? Age Ageing 27:579–583PubMedCrossRefGoogle Scholar
  188. Selye H (1950) The physiology and pathology of exposure to STRESS. A treatise based on the concepts of the General-Adaptation-Syndrome and the Diseases of Adaptation. Acta Inc., MontrealGoogle Scholar
  189. Slager K, Feis N, van der Gaag P (1985) Hongerwinter: verhalen om te onthouden. Link, Amsterdam, The NetherlandsGoogle Scholar
  190. Smil V (1999) Education and debate. China’s great famine: 40 years later. BMJ 319:1619–1621PubMedCrossRefGoogle Scholar
  191. Smith CA (1947a) Effects of maternal undernutrition upon the newborn infant in Holland (1944–1945). J Pediatr 30:229–243PubMedCrossRefGoogle Scholar
  192. Smith CA (1947b) The effect of wartime starvation in Holland upon pregnancy and its product. Am J Obstet Gynecol 53:599–608PubMedGoogle Scholar
  193. Smith FM, Garfield AS, Ward A (2006) Regulation of growth and metabolism by imprinted genes. Cytogenet Genome Res 113:279–291PubMedCrossRefGoogle Scholar
  194. St. Clair D, Xu M, Wang P, Yu Y, Fang Y, Zhang F, Zheng X, Gu N, Feng G, Sham P, He L (2005) Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959–1961. JAMA 294:557–562PubMedCrossRefGoogle Scholar
  195. Stanner SA, Yudkin JS (2001) Fetal programming and the Leningrad siege study. Twin Res 4:287–292PubMedGoogle Scholar
  196. Stanner SA, Bulmer K, Andres C, Lantseva OE, Borodina V, Poteen VV, Yudkin JS (1997) Does malnutrition in utero determine diabetes and coronary heart disease in adulthood? Results from the Leningrad siege study, a cross sectional study. BMJ 315:1342–1349PubMedCrossRefGoogle Scholar
  197. Stein AD, Lumey LH (2000) The relationship between maternal and offspring birth weights after maternal prenatal famine exposure: the Dutch Famine Birth Cohort Study. Hum Biol 72:641–654PubMedGoogle Scholar
  198. Stein Z, Susser M (1975a) Fertility, fecundity, famine: food rations in the Dutch Famine 1944/5 have a causal relation to fertility, and probably to fecundity. Hum Biol 47:131–154PubMedGoogle Scholar
  199. Stein Z, Susser M (1975b) The Dutch famine, 1944–1945, and the reproductive process. I. Effects on six indices at birth. Pediatr Res 9:70–76PubMedGoogle Scholar
  200. Stein Z, Susser M (1975c) The Dutch Famine, 1944–1945 and the reproductive process. II. Interrelations of caloric rations and six indices at birth. Pediatr Res 9:76–83PubMedGoogle Scholar
  201. Stein Z, Susser M, Saenger G, Marolla F (1972) Nutrition and mental performance. Prenatal exposure to the Dutch famine of 1944–1945 seems not related to mental performance at age 19. Science 178:708–713PubMedCrossRefGoogle Scholar
  202. Stein Z, Susser M, Saenger G, Marolla F (1975a) Famine and human development. The Dutch Hunger Winter of 1944–1945. Oxford University Press, New York, NYGoogle Scholar
  203. Stein Z, Susser M, Sturmans F (1975b) Famine and mortality. Tijdschr Soc Geneeskd 53:134–141Google Scholar
  204. Stein AD, Ravelli AC, Lumey LH (1995) Famine, third-trimester pregnancy weight gain, and intrauterine growth: the Dutch Famine Birth Cohort Study. Hum Biol 67:135–150PubMedGoogle Scholar
  205. Stein AD, Kahn HS, Rundle A, Zybert PA, van der Pal-de Bruin K, Lumey LH (2007) Anthropometric measures in middle age after exposure to famine during gestation: evidence from the Dutch famine. Am J Clin Nutr 85:869–876PubMedGoogle Scholar
  206. Stein AD, Pierik FH, Verrips GHW, Susser ES, Lumey LH (2009a) Maternal exposure to the Dutch famine before conception and during pregnancy: quality of life and depressive symptoms in adult offspring. Epidemiology 20:909–915PubMedCrossRefGoogle Scholar
  207. Stein AD, Rundle A, Wada N, Goldbohm RA, Lumey LH (2009b) Associations of gestational exposure to famine with energy balance and macronutrient density of the diet at age 58 years differ according to the reference population used. J Nutr 139:1555–1561PubMedCrossRefGoogle Scholar
  208. Stöger R (2008) The thrifty epigenotype: an acquired and heritable predisposition for obesity and diabetes? Bioessays 30:156–166PubMedCrossRefGoogle Scholar
  209. Susser ES, Lin SP (1992) Schizophrenia after prenatal exposure to the Dutch Hunger Winter of 1944–1945. Arch Gen Psychiatry 49:983–988PubMedCrossRefGoogle Scholar
  210. Susser M, Stein Z (1994) Timing in prenatal nutrition: a reprise of the Dutch Famine Study. Nutr Rev 52:84–94PubMedCrossRefGoogle Scholar
  211. Susser E, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, Gorman JM (1996) Schizophrenia after prenatal famine. Further evidence. Arch Gen Psychiatry 53:25–31PubMedCrossRefGoogle Scholar
  212. Susser E, Hoek HW, Brown A (1998) Neurodevelopmental disorders after prenatal famine. The story of the Dutch Famine Study. Am J Epidemiol 147:213–216PubMedCrossRefGoogle Scholar
  213. Susser E, St. Clair D, He L (2008) Latent effects of prenatal malnutrition on adult health. The example of schizophrenia. Ann N Y Acad Sci 1136:185–192PubMedCrossRefGoogle Scholar
  214. Sweatt JD (2009) Experience-dependent epigenetic modifications in the central nervous system. Biol Psychiatry 65:191–197PubMedCrossRefGoogle Scholar
  215. Szyf M, Weaver I, Meaney M (2007) Maternal care, the epigenome and phenotypic differences in behavior. Reprod Toxicol 24:9–19PubMedCrossRefGoogle Scholar
  216. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, Slagboom PE, Heijmans BT (2009) DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet 18:4046–4053PubMedCrossRefGoogle Scholar
  217. Tost J (ed) (2008) Epigenetics. Caister Academic Press, NorfolkGoogle Scholar
  218. Trichopoulos D (1990) Hypothesis: does breast cancer originate in utero? Lancet 335:939–940PubMedCrossRefGoogle Scholar
  219. Trienekens G (2000) The food supply in The Netherlands during the Second World War. In: Smith DF, Phillips J (eds) Food, science, policy and regulation in the twentieth century. Routledge, London, pp 117–133Google Scholar
  220. Tu MT, Grunau RE, Petrie-Thomas J, Haley DW, Weinberg J, Whitfield MF (2007) Maternal stress and behavior modulate relationships between neonatal stress, attention, and basal cortisol at 8 months in preterm infants. Dev Psychobiol 49:150–164PubMedCrossRefGoogle Scholar
  221. Van Abeelen AF, de Rooij SR, Osmond C, Painter RC, Veenendaal MV, Bossuyt PM, Elias SG, Grobbee DE, van der Schouw YT, Barker DJ, Roseboom TJ (2011) The sex-specific effects of famine on the association between placental size and later hypertension. Placenta 32:694–698PubMedCrossRefGoogle Scholar
  222. Waddington CH (1939) Preliminary notes on the development of the wings in normal and mutant strains of drosophila. Proc Natl Acad Sci U S A 25:299–307PubMedCrossRefGoogle Scholar
  223. Waddington CH (1940) Organisers and genes. Cambridge University Press, CambridgeGoogle Scholar
  224. Waddington CH (1942) The epigenotype. Endeavour 1:18–20Google Scholar
  225. Waddington CH (1957) The strategy of the genes. Allen & Unwin, LondonGoogle Scholar
  226. Waddington CH (1959) Evolutionary systems; animal and human. Nature 183:1634–1638PubMedCrossRefGoogle Scholar
  227. Wadhwa PD, Buss C, Entringer S, Swanson JM (2009) Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med 27:358–368PubMedCrossRefGoogle Scholar
  228. Waterland RA, Michels KB (2007) Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr 27:363–388PubMedCrossRefGoogle Scholar
  229. Whincup PH, Cook DG, Papacosta O (1992) Do maternal and intrauterine factors influence blood pressure in childhood? Arch Dis Child 67:1423–1429PubMedCrossRefGoogle Scholar
  230. Willard HF, Brown CJ, Carrel L, Hendrich B, Miller AP (1993) Epigenetic and chromosomal control of gene expression: molecular and genetic analysis of X chromosome inactivation. Cold Spring Harb Symp Quant Biol 58:315–322PubMedCrossRefGoogle Scholar
  231. Wolffe AP, Matzke MA (1999) Epigenetics: regulation through repression. Science 286:481–486PubMedCrossRefGoogle Scholar
  232. Xiao D, Xu Z, Huang X, Longo LD, Yang S, Zhang L (2008) Prenatal gender-related nicotine exposure increases blood pressure response to angiotensin II in adult offspring. Hypertension 51:1239–1247PubMedCrossRefGoogle Scholar
  233. Xiao D, Huang X, Yang S, Zhang L (2011) Antenatal nicotine induces heightened oxidative stress and vascular dysfunction in rat offspring. Br J Pharmacol 164:1400–1409PubMedCrossRefGoogle Scholar
  234. Yang J (2012) Tombstone: the great Chinese famine, 1958–1962. Farrar, Strauss and Giroux, New York, NY, Translated from the Chinese by Mosher S, Jian GGoogle Scholar

Copyright information

© American Physiological Society 2013

Authors and Affiliations

  • Lawrence D. Longo
    • 1
  1. 1.Center for Perinatal BiologyLoma Linda University School of MedicineLoma LindaUSA

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