Transmission of programming effects across generations

Pediatric Endocrinology Reviews

Volumn 9, Issue 2, 2011, Pages 566-578

  Drake, Amanda J ^a   Seckl, Jonathan R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Early life programming; Epigenetic; Intergenerational

Indexed keywords

BEHAVIOR; BODY SIZE; CARDIOVASCULAR RISK; CHILD HEALTH; DISEASE PREDISPOSITION; EARLY LIFE PROGRAMMING; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; EPIDEMIOLOGICAL DATA; EPIGENETICS; GERM CELL; HUMAN; HUMAN DEVELOPMENT; INTERGENERATIONAL TRANSMISSION; MATERNAL NUTRITION; MATERNAL OBESITY; MULTIGENERATIONAL TRANSMISSION; NONHUMAN; PEDIATRICIAN; PHENOTYPE; PREGNANCY DIABETES MELLITUS; PRENATAL CARE; PROGENY; REVIEW; ANIMAL; BIOLOGICAL MODEL; CHILD; FAMILY SIZE; FEMALE; GENETIC EPIGENESIS; GENETICS; HUMAN RELATION; LIFE EVENT; MOTHER FETUS RELATIONSHIP; PHYSIOLOGY; PREGNANCY; PREGNANCY COMPLICATION; PRENATAL EXPOSURE;

ANIMALS; CHILD; EPIGENESIS, GENETIC; FAMILY CHARACTERISTICS; FEMALE; HUMANS; INTERGENERATIONAL RELATIONS; LIFE CHANGE EVENTS; MATERNAL-FETAL RELATIONS; MODELS, BIOLOGICAL; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84858810577     PISSN: 15654753     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (155)

1. Barker DJP. In utero programming of chronic disease. Clinical Science 1998;95:115-128 (Pubitemid 28401260)
2. Gluckman PD & Hanson MA. Living with the past: Evolution, development, and patterns of disease. Science 2004;305:1733-1736
3. Phipps K, Barker DJ, Hales CN, Fall CH, Osmond C & Clark PM. Fetal growth and impaired glucose tolerance in men and women. Diabetologia 1993;36:225-228 (Pubitemid 23067083)
4. Barker DJ, Osmond C, Golding J, Kuh D & Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. British Medical Journal 1989;298:564-567 (Pubitemid 19072097)
5. Forsen T, Eriksson JG, Tuomilehto J, Osmond C & Barker DJ. Growth in utero and during childhood among women who develop coronary heart disease: longitudinal study. British Medical Journal 1999;319:1403-1407
6. Ibanez L, Potau N, Marcos MV & De Zegher F. Adrenal hyperandrogenism in adolescent girls with a history of low birthweight and precocious pubarche. Clinical Endocrinology 2000;53:523-527
7. Barker DJ & Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986;1:1077-1081 (Pubitemid 16106274)
8. Forsdahl A. Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease? British Journal of Preventive and Social Medicine 1977;31:91-95 (Pubitemid 8143671)
9. Ellison PT. Morbidity, mortality and menarche. Human Biology 1981; 53:635-643.
10. Weismann A (1892) Essays on Heredity and Kindred Biological Problems. Oxford: Clarendon.
11. Hales CN & Barker DJP. Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis. Diabetologia 1992;35:595-601
12. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA & Robinson JS. Fetal nutrition and cardiovascular disease in adult life. Lancet 1993;341:938-941 (Pubitemid 23109122)
13. Drake AJ & Reynolds RM. Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction 2010;140:387-398
14. Edwards CR, Benediktsson R, Lindsay RS & Seckl JR. Dysfunction of placental glucocorticoid barrier: a link between the fetal environment and adult hypertension? Lancet 1993;341:355-357 (Pubitemid 23039711)
15. Diamanti-Kandarakis E, Bourguignon J-P, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT & Gore AC. Endocrine-disrupting chemicals: An endocrine society scientific statement. Endocrine Reviews 2009;30:293-342
16. Waddington CH (1957) The strategy of the genes. London: Allen and Unwin.
17. Jaenisch R & Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics. 2003;33:245-254 (Pubitemid 36278835)
18. Fu Q, Mcknight RA, Yu X, Wang L, Callaway CW & Lane RH. Uteroplacental insufficiency induces site-specific changes in histone H3 covalent modifications and affects DNA-histone H3 positioning in day 0 IUGR rat liver. Physiological Genomics 2004;20:108-116 (Pubitemid 40388510)
19. Burdge GC, Slater-Jefferies JL, Torrens C, Phillips ES, Hanson MA & Lillycrop KA. Dietary protein restriction of pregnant rats in the FO generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. British Journal of Nutrition 2007;97:435-439 (Pubitemid 46662031)
20. 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. Journal of Nutrition 2005;135:1382-1386 (Pubitemid 40799599)
21. Weaver ICG, Cervoni N, Champagne F, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M & Meaney MJ. Epigenetic programming by maternal behavior. Nature Neuroscience 2004;7:847-854 (Pubitemid 38989508)
22. Park JH. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. The Journal of Clinical Investigation 2008;118:2316-2324 (Pubitemid 351872348)
23. Drake AJ & Walker BR. The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk. Journal of Endocrinology 2004;180:1-16 (Pubitemid 38180752)
24. Jablonka E & Lamb MJ (2005) Evolution in four dimensions: Genetic, epigenetic, behavioural and symbolic variation in the history of life: MIT press, Cambridge, Massachusetts
25. Gluckman PD, Hanson MA & Beedle AS. Non-genomic transgenerational inheritance of disease risk Bioessays 2007;29:145-154 (Pubitemid 46340249)
26. Harrison M & Langley-Evans SC. Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. British Journal of Nutrition 2009;101:1020-1030
27. Benyshek DC, Johnston CS, Martin JF & Ross WD. Insulin sensitivity is normalized in the third generation (F3) offspring of developmentally programmed insulin resistant (F2) rats fed an energy-restricted diet. Nutrition and Metabolism 2008;5:26
28. Drake AJ, Walker BR & Seckl JR. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. American Journal of Physiology 2005;288:34-38
29. Youngson NA & Whitelaw E. Transgenerational epigenetic effects. Annual Review of Genomics and Human Genetics 2008;9:233-257
30. Jablonka E & Raz G. Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology 2009;84:131-176
31. Skinner MK. What is an epigenetic transgenerational phenotype? F3 or F2. Reproductive Toxicology 2008;25:2-6
32. Baird D. Changing problems and priorities in obstetrics. British Journal of Obstetrics & Gynaecology 1985;92:115-121 (Pubitemid 15162715)
33. Emanuel I, Filakti H, Alberman E & Evans SJ. Intergenerational studies of human birthweight from the 1958 birth cohort. 1. Evidence for a multigenerational effect. British Journal of Obstetrics & Gynaecology 1992;99:67-74
34. Kaati G, Bygren LO & Edvinson S. Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. European Journal of Human Genetics 2002;10:682-688 (Pubitemid 35460575)
35. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DIW & Roseboom TJ. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG: An International Journal of Obstetrics a Gynaecology 2008;115:1243-1249
36. Berends AL, de Groot CJM, Sijbrands EJ, Sie MPS, Benneheij SH, Pal R, Heydanus R, Oostra BA, van Duijn CM & Steegers EAR Shared constitutional risks for maternal vascular-related pregnancy complications and future cardiovascular disease. Hypertension 2008;51:1034-1041 (Pubitemid 351398955)
37. Nilsson PM, Li X, Sundquist J & Sundquist K. Maternal cardiovascular disease risk in relation to the number of offspring born small for gestational age: national, multi-generational study of 2.7 million births. Acta Paediatrica 2009;98:985-989.
38. Stein AD & Lumey LH. The relationship between maternal and offspring birth weights after maternal prenatal famine exposure: the Dutch Famine Birth Cohort Study. Human Biology 2000;72:641-654
39. Ounsted M & Ounsted C. Rate of intra-uterine growth. Nature 1968;220:599-600
40. Johnstone F & Inglis L. Familial trends in low birth weight. British Medical Journal 1974;3:659-661
41. Klebanoff MA, Meirik O & Berendes HW. Second-generation consequences of small-for-dates birth. Pediatrics 1989;84:343-347 (Pubitemid 19193867)
42. Emanuel I, Leisenring W, Williams MA, Kimpo C, Estee S, O'Brien W & Hale CB. The Washington State Intergenerational Study of Birth Outcomes: methodology and some comparisons of maternal birthweight and infant birthweight and gestation in four ethnic groups. Paediatric and Perinatal Epidemiology 1999;13:352-369
43. Klebanoff MA, Schulsinger C, Mednick BR & Secher NJ. Preterm and small-for-gestational-age birth across generations. American Journal of Obstetrics & Gynecology. 1997;176:521-526 (Pubitemid 27147154)
44. Kaati G, Bygren LO, Pembrey M & Sjostrom M. Transgenerational response to nutrition, early life circumstances and longevity. European Journal of Human Genetics 2007;15:784-790 (Pubitemid 46965412)
45. Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Schroeder-Tanka JM, van Montfrans GA, Michels RP & Bleker OP. Coronary heart disease after prenatal exposure to the Dutch famine, 1944-45. Heart 2000;84:595-598
46. Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC & Bleker OP. Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. American Journal of Clinical Nutrition 2000;72:1101-1106
47. Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ & Bleker OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. American Journal of Clinical Nutrition 1999;70:811-816 (Pubitemid 29512905)
48. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE & Lumey LH. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proceedings of the National Academy of Sciences 2008; 105:17046-17049.
49. Dabelea D, Mayer-Davis EJ, Lamichhane AP, D'Agostino RB, Liese AD, Vehik KS, Narayan KMV, Zeitler P & Hamman RF. Association of intrauterine exposure to maternal diabetes and obesity with type 2 diabetes in youth. Diabetes Care 2008;31:1422-1426
50. Armitage JA, Taylor PD & Poston L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. Journal of Physiology 2005;565:3-8 (Pubitemid 40723685)
51. Kanagalingam MG, Forouhi NG, Greer IA & Sattar N. Changes in booking body mass index over a decade: retrospective analysis from a Glasgow maternity hospital. British Journal of Obstetrics & Gynaecology 2005;112:1431-1433 (Pubitemid 43961277)
52. Heslehurst N, Rankin J, Wilkinson JR & Summerbell CD. A nationally representative study of maternal obesity in England, UK: trends in incidence and demographic inequalities in 619323 births, 1989-2007. International Journal of Obesity 2010;34:420-428
53. Surkan PJ, Hsieh CC, Johansson AL, Dickman PW & Cnattingius S. Reasons for increasing trends in large for gestational age births. Obstetrics & Gynecology 2004;104:720-726 (Pubitemid 40458799)
54. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ & Flegal KM. Prevalence of overweight and obesity in the United States, 1999-2004. JAMA: The Journal of the American Medical Association 2006;295:1549-1555
55. Davis MM, McGonagle K, Schoeni RF & Stafford F. Grandparental and parental obesity influences on childhood overweight: Implications for primary care practice. Journal of the American Board of Family Medicine 2008;21:549-554
56. Lawlor DA, Timpson NJ, Harbord RM, Leary S, Ness A, McCarthy MI, Frayling TM, Hattersley AT & Smith GD. Exploring the developmental overnutrition hypothesis using parental-offspring associations and FTO as an instrumental variable. PLoS Med 2008;5:e33
57. Delisle HF. Poverty. Annals of the New York Academy of Sciences 2008; 1136:172-184
58. Dabelea D, Hanson RL, Bennett PH, Roumain J, Knowler WC & Pettitt DJ. Increasing prevalence of Type II diabetes in American Indian children. Diabetologia 1998; 41:904-910 (Pubitemid 28365976)
59. Lindsay RS, Hanson RL, Bennett PH & Knowler WC. Secular trends in birth weight, BMI, and diabetes in the offspring of diabetic mothers. Diabetes Care 2000; 23:1249-1254.
60. Wild S, Roglic G, Green A, Sicree R & King H. Global prevalence of diabetes:estimates for the year 2000 and projections for 2030. Diabetes Care 2004;27:1047-1053 (Pubitemid 38579764)
61. Feig DS & Palda VA. Type 2 diabetes in pregnancy: a growing concern. The Lancet 2002;359:1690-1692 (Pubitemid 34518536)
62. Bell R, Bailey K, Cresswell T, Hawthorne G, Critchley J, Lewis-Barned N & Northern Diabetic Pregnancy Survey Steering G. Trends in prevalence and outcomes of pregnancy in women with pre-existing type I and type II diabetes. BJOG: An International Journal of Obstetrics & Gynaecology 2008;115:445-452
63. Skinner MK, Manikkam M & Guerrero-Bosagna C. Epigenetic transgenerational actions of endocrine disruptors. Reproductive Toxicology 2011;31:337-343
64. Goldberg JM & Falcone T. Effect of diethylstilbestrol on reproductive function. Fertility and Sterility 1999;72:1-7 (Pubitemid 29300252)
65. Senekjian EK, Potkul RK, Frey K & Herbst AL. Infertility among daughters either exposed or not exposed to diethytstilbestrol. American Journal of Obstetrics & Gynecology 1988;158:493-498 (Pubitemid 18088191)
66. Palmer JR, Hatch EE, Rao RS, Kaufman RH, Herbst AL, Noller KL, Titus-Emstoff L & Hoover RN. Infertility among women exposed prenatally to diethylstilbestrol. American Journal of Epidemiology 2001;154:316-321 (Pubitemid 32756627)
67. Greenwald P, Barlow JJ, Nasca PC & Burnett WS. Vaginal cancer after maternal treatment with synthetic estrogens. New England Journal of Medicine 1971; 285:390-392.
68. Herbst AL, Ulfelder H & Poskanzer DC. Adenocarcinoma of the vagina. New England Journal of Medicine 1971;284:878-881
69. Titus-Ernstoff L, Troisi R, Hatch EE, Wise LA, Palmer J, Hyer M, Kaufman R, Adam E, Strohsnitter W, Noller K, Herbst AL, Gibson-Chambers J, Hartge P & Hoover RN. Menstrual and reproductive characteristics of women whose mothers were exposed in utero to diethylstilbestrol (DES). International Journal of Epidemiology 2006;35:862-868 (Pubitemid 44540734)
70. Brouwers MM, Feitz WFJ, Roelofs LAJ, Kiemeney LALM, de Gier RPE & Roeleveld N. Hypospadias: a transgenerational effect of diethylstilbestrol? Human Reproduction 2006;21:666-669 (Pubitemid 43372971)
71. Klip H, Verloop J, van Gool JD, Koster META, Burger CW & van Leeuwen FE. Hypospadias in sons of women exposed to diethylstilbestrol in utero: a cohort study. The Lancet 2002;359:1102-1107 (Pubitemid 34270733)
72. Palmer JR, Wise LA, Robboy SJ, Titus-Ernstoff L, Noller KL, Herbst AL, Troisi R & Hoover RN. Hypospadias in sons of women exposed to diethylstilbestrol in utero. Epidemiology 2005;16:583-586 (Pubitemid 40847848)
73. Pentinat T, Ramon-Krauel M, Cebria J, Diaz R & Jimenez-Chillaron JC. Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition. Endocrinology 2010;151:5617-5623
74. Jimenez-Chillaron JC, Isganaitis E, Charalambous M, Gesta S, Pentinat-Pelegrin T, Faucette RR, Otis JP, Chow A, Diaz R, Ferguson-Smith A & Patti M-E. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 2009;58:460-468
75. Ng S-F, Lin RCY, Laybutt DR, Barres R, Owens JA & Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 2010;467:963-966
76. Anderson CM, Lopez F, Zimmer A & Benoit JN. Placental insufficiency leads to developmental hypertension and mesenteric artery dysfunction in two generations of Sprague-Dawley rat offspring. Biology of Reproduction 2006;74:538-544 (Pubitemid 43271358)
77. Franklin TB, Russig H, Weiss IC, Gräff J, Linder N, Michaion A, Vizi S & Mansuy IM. Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry 2010;68:408-415
78. Benyshek DC, Johnston CS & Martin JF. Glucose metabolism is altered in the adequately-nourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 2006;49:1117-1119
79. Stouder C & Paoloni-Giacobino A. Specific transgenerational imprinting effects of the endocrine disruptor methoxychlor on male gametes. Reproduction 2011;141:207-216
80. Anway MD, Cupp AS, Uzumcu M & Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005;308:1466-1469 (Pubitemid 40791300)
81. Subramanian SV, Ackerson LK, Davey Smith G & John NA. Association of maternal height with child mortality, anthropometric failure, and anemia in India. Journal of the American Medical Association 2009;301:1691-1701
82. Ramakrishnan U, Martorell R, Schroeder DG & Flores R. Role of intergenerational effects on linear growth. Journal of Nutrition 1999; 129:5445-5495.
83. Collins JW, Wu SY & David RJ. Differing intergenerational birth weights among the descendants of US-born and foreign-born Whites and African Americans in Illinois. American Journal of Epidemiology 2002;155:210-216 (Pubitemid 34126350)
84. Jasienska G. Low birth weight of contemporary African Americans: An intergenerational effect of slavery? American Journal of Human Biology 2009;21:16-24
85. Kuzawa CW & Sweet E. Epigenetics and the embodiment of race: Developmental origins of US racial disparities in cardiovascular health. American Journal of Human Biology 2009;21:2-15
86. Collins JW, Jr., Rankin KM & David RJ. African American women's lifetime upward economic mobility and preterm birth: The effect of fetal programming. American Journal of Public Health 2011;101:714-719
87. Lahmann PH, Wills R-A & Coory M. Trends in birth size and macrosomia in Queensland, Australia, from 1988 to 2005. Paediatric and Perinatal Epidemiology 2009;23:533-541
88. Schack-Nielsen L, Molgaard C, Sorensen TIA, Greisen G & Michaelsen KF. Secular change in size at birth from 1973 to 2003: National data from Denmark. Obesity 2006;14:1257-1263 (Pubitemid 46219692)
89. Klebanoff MA, Secher NJ, Mednick BR & Schulsinger C. Maternal size at birth and the development of hypertension during pregnancy: a test of the Barker hypothesis. Archives of Internal Medicine. 1999;159:1607-1612 (Pubitemid 29340315)
90. Denton KM, Flower RL, Stevenson KM & Anderson WP. Adult rabbit offspring of mothers with secondary hypertension have increased blood pressure. Hypertension 2003;41:634-639 (Pubitemid 36314566)
91. Dabelea D, Hanson RL, Lindsay RS, Pettitt DJ, Imperatore G, Gabir MM, Roumain J, Bennett PH & Knowler WC. Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes 2000;49:2208-2211
92. Vadlamudi S, Kalhan S & Patel M. Persistence of metabolic consequences in the progeny of rats fed a HC formula in their early postnatal life. American Journal of Physiology 1995;269:731-738
93. Buchbinder A, Sibai BM, Caritis S, Macpherson C, Hauth J, Lindheimer MD, Klebanoff M, Vandorsten P, Landon M, Paul R, Miodovnik M, Meis P & Thurnau G. Adverse perinatal outcomes are significantly higher in severe gestational hypertension than in mild preeclampsia. American Journal of Obstetrics & Gynecology 2002;186:66-71 (Pubitemid 34093742)
94. Levitt NS, Lindsay RS, Holmes MC & Seckl JR. Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. Neuroendocrinology 1996;64:412-418 (Pubitemid 27007194)
95. Metzger BE, Lowe LP, Dyer AR, Trimble ER, Chaovarindr U, Coustan DR, Hadden DR, McCance DR, Hod M, McIntyre HD, Oats JJ, Persson B, Rogers MS & Sacks DA. Hyperglycemia and adverse pregnancy outcomes. New England Journal of Medicine 2008;358:1991-2002
96. Walton A & Hammond J. The maternal effects on growth and conformation in Shire horse-Shetland pony crosses. Proceedings of the Royal Society of London. Series B, Biological Sciences 1938;125:311-335
97. Cawley RH, McKeown T & Record RG. Parental stature and birth weight. Annals of Human Genetics 1954;6:448-456
98. Emanuel I. Invited commentary: an assessment of maternal intergenerational factors in pregnancy outcome. American Journal of Epidemiology 1997;146:820-825
99. Ozaltin E, Hill K & Subramanian SV. Association of maternal stature with offspring mortality, underweight, and stunting in low- to middle-income countries. JAMA: The Journal of the American Medical Association 2010;303:1507-1516
100. Christian P. Maternal height and risk of child mortality and undernutrition. JAMA: The Journal of the American Medical Association 2010;303:1539-1540
101. Stewart RJ, Preece RF & Sheppard HG. Twelve generations of marginal protein deficiency. British Journal of Nutrition 1975;33:233-253
102. Ibanez L, Potau N, Enriquez G & de Zegher F. Reduced uterine and ovarian size in adolescent girls born small for gestational age. Pediatric Research 2000; 47:575-577 (Pubitemid 30249842)
103. Williams MA, Emanuel I, Kimpo C, Leisenring WM & Hale CB. A population-based cohort study of the relation between maternal birthweight and risk of gestational diabetes mellitus in four racial/ethnic groups. Paediatric and Perinatal Epidemiology. 1999;13:452-465 (Pubitemid 29515844)
104. Egeland GM, Skjaerven R & Irgens LM. Birth characteristics of women who develop gestational diabetes: population based study. British Medical Journal 2000;321:546-547
105. Forsen T, Eriksson J, Tuomilehto J, Reunanen A, Osmond C & Barker D. The fetal and childhood growth of persons who develop type 2 diabetes. Annals of Internal Medicine 2000;133:176-182 (Pubitemid 30617055)
106. Innes KE, Byers TE, Marshall JA, Baron A, Orleans M & Hamman RF. Association of a woman's own birth weight with subsequent risk for gestational diabetes. Journal of the American Medical Association 2002;287:2534-2541 (Pubitemid 34517199)
107. Seghieri G, Anichini R, De Bellis A, Alviggi L, Franconi F & Breschi MC. Relationship between gestational diabetes mellitus and low maternal birth weight. Diabetes Care. 2002;25:1761-1765 (Pubitemid 41071083)
108. Pettitt DJ, Nelson RG, Saad MF, Bennett PH & Knowler WC. Diabetes and obesity in the offspring of Pima Indian women with diabetes during pregnancy. Diabetes Care. 1993;16:310-314 (Pubitemid 23013867)
109. Gillman MW, Rifas-Shiman S, Berkey CS, Field AE & Colditz GA. Maternal gestational diabetes, birth weight, and adolescent obesity. Pediatrics. 2003;111:e221-226
110. Catalano PM, Kirwan JP, Haugel-De Mouzon S & King J. Gestational diabetes and insulin resistance: Role in short- and long-term implications for mother and fetus. Journal of Nutrition 2003;133
111. Francis D, Diorio J, Liu D & Meaney MJ. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999;286:1155-1158
112. Doumas D, Margolin G & John RS. The intergenerational transmission of aggression across 3 generations. Journal of Family Violence 1994;9:157-175
113. Kerr DC, Capaldi DM, Pears KC & Owen LD. A prospective three generational study of fathers' constructive parenting: influences from family of origin, adolescent adjustment, and offspring temperament. Developmental Psychology 2009;45:1257-1275
114. Smith CA & Farrington DP. Continuities in antisocial behavior and parenting across three generations. Journal of Child Psychology and Psychiatry 2004; 45:230-247 (Pubitemid 38240271)
115. Matthews SG & Phillips DI. Transgenerational inheritance of stress pathology. Experimental Neurology 2011; In Press
116. Reik W, Dean W & Walter J. Epigenetic reprogramming in mammalian development. Science 2001;293:1089-1093 (Pubitemid 32758081)
117. Hemberger M, Dean W & Reik W. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nature Reviews Molecular and Cellular Biology 2009; 10:526-537
118. Ginsburg M, Snow MH & McLaren A. Primordial germ cells in the mouse embryo during gastrulation. Development 1990;110:521-528 (Pubitemid 20330528)
119. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J & Surani MA. Epigenetic reprogramming in mouse primordial germ cells. Mechanisms of Development 2002;117:15-23 (Pubitemid 36158711)
120. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J & Reik W. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 2003;35:88-93
121. Morgan HD, Sutherland HG, Martin DI & Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nature Genetics 1999;23:314-318 (Pubitemid 29526429)
122. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV & Whitelaw E. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proceedings of the National Academy of Sciences 2003;100:2538-2543 (Pubitemid 36297534)
123. Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I & Cuzin F. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 2006;441:469-474 (Pubitemid 44050143)
124. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT & Cairns BR. Distinctive chromatin in human sperm packages genes for embryo development. Nature 2009;460:473-478
125. Lalancette C, Miller DJ, Li Y & Krawetz SA. Paternal contributions: New functional insights for spermatozoal RNA. Journal of Cellular Biochemistry 2008;104:1570-1579
126. Guerrero-Bosagna C, Settles M, Lucker B & Skinner MK. Epigenetic transgenerational actions of Vinclozolin on promoter regions of the sperm epigenome. PLoS ONE 2011;5:e13100
127. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, Bock C, Li C, Gu H, Zamore PD, Meissner A, Weng Z, Hofmann HA, Friedman N & Rando OJ. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010;143:1084-1096
128. Skinner MK. Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics 2011;6:838-842
129. Anway MD, Leathers C & Skinner MK. Endocrine disrupter vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 2006; 147:5515-5523. (Pubitemid 44833467)
130. Stouder C & Paoloni-Giacobino A. Transgenerational effects of the endocrine disrupter vinclozolin on the methylation pattern of imprinted genes in the mouse sperm. Reproduction 2010;139:373-379
131. Chan JC, Malik V, Jia W, Kadowaki T, Yajnik CS, Yoon KH & Hu FB. Diabetes in Asia: epidemiology, risk factors, and pathophysiology. Journal of the American Medical Association 2009;301:2129-2140
132. Yajnik CS & Deshmukh US. Maternal nutrition, intrauterine programming and consequential risks in the offspring. Reviews in Endocrine and Metabolic Disorders 2008;9:203-211
133. Chike-Obi U, David RJ, Coutinho R & Wu SY. Birth weight has increased over a generation. American Journal of Epidemiology. 1996;144:563-569 (Pubitemid 26304401)
134. Skjaerven R, Gjessing HK & Bakketeig LS. Birthweight by gestational age in Norway. Acta Obstetricia et Gynecologica Scandinavica. 2000;79:440-449 (Pubitemid 30326124)
135. Kramer MS, Morin I, Yang H, Platt RW, Usher R, McNamara H, Joseph KS & Wen SW. Why are babies getting bigger? Temporal trends in fetal growth and its determinants. Journal of Pediatrics. 2002;141:538-542 (Pubitemid 35193320)
136. Dowse GK, Zimmet PZ, Finch CF & Collins VR. Decline in incidence of epidemic glucose intolerance in Nauruans: implications for the "thrifty genotype". American Journal of Epidemiology 1991;133:1093-1104
137. Ozanne SE & Hales CN. Thrifty yes, genetic no. Diabetologia 1998;41:485-487 (Pubitemid 28157422)
138. Waterland RA, Travisano M, Tahiliani KG, Rached MT & Mirza S. Methyl donor supplementation prevents transgenerational amplification of obesity. International Journal of Obesity 2008;32:1373-1379
139. Solomons NW. Developmental origins of health and disease: concepts, caveats, and consequences for public health nutrition. Nutrition Reviews 2009;67:12-16
140. Muthayya S, Kurpad AV, Duggan CP, Bosch RJ, Dwarkanath P, Mhaskar A, Mhaskar R, Thomas A, Vaz M, Bhat S & Fawzi WW. Low maternal vitamin B12 status is associated with intrauterine growth retardation in urban South Indians. European Journal of Clinical Nutrition. 2006;60:791-801 (Pubitemid 43842235)
141. Yajnik CS, Deshpande SS, Jackson AA, Refsum H, Rao S, Fisher DJ, Bhat DS, Naik SS, Coyaji KJ, Joglekar CV, Joshi N, Lubree HG, Deshpande VU, Rege SS & Fall CH. Vitamin B12 and folate concentrations during pregnancy and insulin resistance in the offspring: the Pune Maternal Nutrition Study. Diabetologia 2008;51:29-38 (Pubitemid 350197985)
142. Katz J, Christian P, Dominici F & Zeger SL. Treatment effects of maternal micronutrient supplementation vary by percentiles of the birth weight distribution in rural Nepal. Journal of Nutrition 2006;136:1389-1394
143. Fall CH, Yajnik CS, Rao S, Davies AA, Brown N & Farrant HJ. Micronutrients and fetal growth. Journal of Nutrition 2003;133:1747-1756
144. Smith J, Cianflone K, Biron S, Houtd FS, Lebel S, Marceau S, Lescelleur O, Biertho L, Simard S, Kral JG & Marceau P. Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity. Journal of Clinical Endocrinology and Metabolism 2009;94:4275-4283
145. Howie GJ, Sloboda DM, Kamal T & Vickers MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. The Journal of Physiology 2009;587:905-915
146. Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, Gertler A, Breier BH & Harris M. Neonatal leptin treatment reverses developmental programming. Endocrinology 2005;146:4211-4216 (Pubitemid 41324016)
147. Ong KK, Ahmed ML, Emmett PM, Preece MA & Dunger DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. British Medical Journal 2000;320:967-971 (Pubitemid 30192864)
148. Ekelund U, Ong K, Linne Y, Neovius M, Brage S, Dunger DB, Wareham NJ & Rossner S. Upward weight percentile crossing in infancy and early childhood independently predicts fat mass in young adults: the Stockholm Weight Development Study (SWEDES). American Journal of Clinical Nutrition 2006;83:324-330 (Pubitemid 44713194)
149. Kramer MS, Matush L, Vanilovich I, Platt RW, Bogdanovich N, Sevkovskaya Z, Dzikovich I, Shishko G, Collet J-P, Martin RM, Davey Smith G, Gillman MW, Chalmers B, Hodnett E & Shapiro S. Effects of prolonged and exclusive breastfeeding on child height, weight, adiposity, and blood pressure at age 6.5 y: evidence from a large randomized trial. American Journal of Clinical Nutrition 2007;86:1717-1721 (Pubitemid 350232188)
150. Owen CG, Martin RM, Whincup PH, Smith GD & Cook DG. Does breastfeeding influence risk of type 2 diabetes in later life? A quantitative analysis of published evidence. American Journal of Clinical Nutrition 2006;84:1043-1054 (Pubitemid 44730374)
151. Owen CG, Martin RM, Whincup P, Smith GD & Cook DG. Effect of infant feeding on the risk of obesity across the life course: a quantitative review of published evidence. Pediatrics 2005;115:1367-1377 (Pubitemid 43843245)
152. Lumey LH, Stein AD & Emanuel I. Offspring birth weights after maternal intrauterine undernutrition: A comparison within sibships. American Journal of Epidemiology 1997;146:810-825 (Pubitemid 27498099)
153. Zambrano E, Martinez-Samayoa PM, Bautista CJ, Deas M, Guillen L, Rodriguez-Gonzalez GL, Guzman C, Larrea F & Nathanielsz PW. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. Journal of Physiology 2005;566.1:225-236 (Pubitemid 40984216)
154. Skinner MK, Anway MD, Savenkova MI, Gore AC & Crews D. Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior. PLoS ONE 2008;3:e3745
155. Nilsson EE, Anway MD, Stanfield J & Skinner MK. Transgenerational epigenetic effects of the endocrine disrupter vinclozolin on pregnancies and female adult onset disease. Reproduction 2008;135:713-721 (Pubitemid 351676454)