Transgenerational developmental programming

Human Reproduction Update

Volumn 20, Issue 1, 2014, Pages 63-75

  Aiken, Catherine E ^a   Ozanne, Susan E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Animal models; Development; Fetal; Programming; Transgenerational

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; BENZO[A]PYRENE; BETA ENDORPHIN; DEXAMETHASONE; DIETHYLSTILBESTROL; GLUCOCORTICOID; GLUCOSE; ISOFLAVONE; LUTEINIZING HORMONE; MORPHINE; POLYCHLORINATED BIPHENYL; VINCLOZOLIN;

ADAPTATION; AGE DISTRIBUTION; ALCOHOL CONSUMPTION; ARTICLE; BREEDING; CALORIC RESTRICTION; DEVELOPMENTAL GENETICS; DEVELOPMENTAL TOXICITY; DNA METHYLATION; DNA MODIFICATION; EPIDEMIOLOGICAL DATA; EPIGENETICS; EXERCISE; EXPERIMENTAL MODEL; GENITAL SYSTEM; GENOME ANALYSIS; GENOTOXICITY; GENOTYPE ENVIRONMENT INTERACTION; GERM LINE; HUMAN; INHERITANCE; LIPID DIET; MATERNAL AGE; MEDICAL LITERATURE; NONHUMAN; OVARY DEVELOPMENT; PHENOTYPIC VARIATION; PREGNANCY; PRENATAL DEVELOPMENT; PRENATAL STRESS; PRIORITY JOURNAL; PROGENY; PROTEIN RESTRICTION; REPRODUCTIVE TOXICITY; SITTING; SYSTEMATIC REVIEW; TRANSGENERATIONAL DEVELOPMENTAL PROGRAMMING; UTERUS GROWTH; VITAMIN D DEFICIENCY; ZYGOTE;

ANIMAL MODELS; DEVELOPMENT; FETAL; PROGRAMMING; TRANSGENERATIONAL;

ANIMALS; EPIGENESIS, GENETIC; FEMALE; HUMANS; MATERNAL-FETAL EXCHANGE; PHENOTYPE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84889673681     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmt043     Document Type: Article

References (137)

1. Aerts L, Van Assche FA. Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol 2006;38:894-903.
2. Ahokas RA, Reynolds SL, Anderson GD, Lipshitz J. Maternal organ distribution of cardiac output in the diet-restricted pregnant rat. J Nutr 1984;12:2262-2268.
3. Aiken C, Ozanne S. Sex differences in developmental programming models. Reproduction 2013;145:R1-13.
4. Aiken CE, Cindrova-Davies T, Johnson MH. Variations in mouse mitochondrial DNA copy number from fertilization to birth are associated with oxidative stress. Reprod Biomed Online 2008;6:806-813.
5. 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. Biol Reprod 2006;3:538-544.
6. Anderson CM, Lopez F, Sandeen A, Johnson L. Placental insufficiency: programming of leptin secretion, blood pressure, and postnatal growth in two generations of Sprague-Dawley rats. Biol Res Nurs 2009;3:284-291.
7. Anway MD, Leathers C, Skinner MK. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 2006a;12: 5515-5523.
8. Anway MD, Memon MA, Uzumcu M, Skinner MK. Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. J Androl 2006b; 6:868-879.
9. Anway MD, Rekow SS, Skinner MK. Transgenerational epigenetic programming of the embryonic testis transcriptome. Genomics 2008;1:30-40.
10. Armitage JA, Ishibashi A, Balachandran AA, Jensen RI, Poston L, Taylor PD. Programmed aortic dysfunction and reduced Na+, K+-ATPase activity present in first generation offspring of lard-fed rats does not persist to the second generation. Exp Physiol 2007;3:583-589.
11. BairdDT, Collins J, Egozcue J, Evers LH, Gianaroli L, Leridon H, Sunde A, Templeton A, Van Steirteghem A, Cohen J et al. Fertility and ageing. Hum Reprod Update 2005; 3:261-276.
12. Balasch J, Gratacos E. Delayed childbearing: effects on fertility and the outcome of pregnancy. Curr Opin Obstet Gynecol 2012;3:187-193.
13. Beach RS, Gershwin ME, Hurley LS. Gestational zinc deprivation in mice: persistence of immunodeficiency for three generations. Science 1982;4571:469-471.
14. Beekhuijzen M, Zmarowski A, Emmen H, Frieling W. To mate or not to mate: a retrospective analysis of two-generation studies for evaluation of criteria to trigger additional mating in the extended one-generation design. Reprod Toxicol 2009; 2:203-208.
15. 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;5:1117-1119.
16. 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. Nutr Metab (Lond) 2008;5:26.
17. Bernal AB, Vickers MH, Hampton MB, Poynton RA, Sloboda DM. Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One 2010;12:e15558.
18. Bertram C, Khan O, Ohri S, Phillips DI, Matthews SG, Hanson MA. Transgenerational effects of prenatal nutrient restriction on cardiovascular and hypothalamic- pituitary-adrenal function. J Physiol 2008;8:2217-2229.
19. Bilbo SD, Schwarz JM. The immune system and developmental programming of brain and behavior. Front Neuroendocrinol 2012;3:267-286.
20. Bilhartz TD, Bilhartz PA, Bilhartz TN, Bilhartz RD. Making use of a natural stress test: pregnancy and cardiovascular risk. J Womens Health (Larchmt) 2011;5:695-701.
21. Blondeau B,Avril I, Duchene B, Breant B. Endocrine pancreas development is altered in foetuses from rats previously showing intra-uterine growth retardation in response to malnutrition. Diabetologia 2002;3:394-401.
22. Boloker J, Gertz SJ, Simmons RA. Gestational diabetes leads to the development of diabetes in adulthood in the rat. Diabetes 2002;5:1499-1506.
23. Braunschweig M, Jagannathan V, Gutzwiller A, Bee G. Investigations on transgenerational epigenetic response down the male line in F2 pigs. PLoS One 2012; 2:e30583.
24. Brawley L, Torrens C, Anthony FW, Itoh S, Wheeler T, Jackson AA, Clough GF, Poston L, Hanson MA. Glycine rectifies vascular dysfunction induced by dietary protein imbalance during pregnancy. J Physiol 2004;554(Pt 2):497-504.
25. Brix S, Christensen HR, Barkholt V, Frokiaer H. Effect of maternal dietary cow's milk on the immune response to beta-lactoglobulin in the offspring: a four-generation study in mice. Int Arch Allergy Immunol 2005;3:250-257.
26. Broday L, PengW, Kuo MH, Salnikow K, Zoroddu M, Costa M. Nickel compounds are novel inhibitors of histone H4 acetylation. Cancer Res 2000;2:238-241.
27. Buchwald U, Teupser D, Kuehnel F, Grohmann J, Schmieder N, Beindorff N, Schlumbohm C, Fuhrmann H, Einspanier A. Prenatal stress programs lipid metabolism enhancing cardiovascular risk in the female F1, F2, and F3 generation in the primate model common marmoset (Callithrix jacchus). J Med Primatol 2012; 4:231-240.
28. Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, Lillycrop KA. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr 2007;3:435-439.
29. Burdge GC, Hoile SP, Uller T, Thomas NA, Gluckman PD, Hanson MA, Lillycrop KA. Progressive, transgenerational changes in offspring phenotype and epigenotype following nutritional transition. PLoS One 2011;11:e28282.
30. Bygren LO, Kaati G, Edvinsson S. Longevity determined by paternal ancestors' nutrition during their slow growth period. Acta Biotheor 2001;1:53-59.
31. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, Bock C, Li C, Gu H, Zamore PD et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010;7:1084-1096.
32. Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 2006;6:2909-2915.
33. Chang HS, AnwayMD, RekowSS, Skinner MK. Transgenerational epigenetic imprinting of the male germline by endocrine disruptor exposure during gonadal sex determination. Endocrinology 2006;12:5524-5541.
34. Chernoff N, Gage MI, Stoker TE, Cooper RL, Gilbert ME, Rogers EH. Reproductive effects of maternal and pre-weaning undernutrition in rat offspring: age at puberty, onset of female reproductive senescence and intergenerational pup growth and viability. Reprod Toxicol 2009;4:489-494.
35. Chong E, Yosypiv IV. Developmental programming of hypertension and kidney disease. Int J Nephrol 2012;2012:760580.
36. Costantine MM, Ghulmiyyah LM, Tamayo E, Hankins GD, Saade GR, Longo M. Transgenerational effect of fetal programming on vascular phenotype and reactivity in endothelial nitric oxide synthase knockout mouse model. Am J Obstet Gynecol 2008;3:250 e1-250 e7.
37. Cottrell EC, Ozanne SE. Early life programming of obesity and metabolic disease. Physiol Behav 2008;1:17-28.
38. Crescenzo R, Lionetti L, Mollica MP, Ferraro M, D'Andrea E, Mainieri D, Dulloo AG, Liverini G, Iossa S. Altered skeletal muscle subsarcolemmal mitochondrial compartment during catch-up fat after caloric restriction. Diabetes 2006; 8:2286-2293.
39. Crews D, Gore AC, Hsu TS, Dangleben NL, Spinetta M, Schallert T, Anway MD, Skinner MK. Transgenerational epigenetic imprints on mate preference. Proc Natl Acad Sci USA 2007;14:5942-5946.
40. Cropley JE, Suter CM, Beckman KB, Martin DI. Germline epigenetic modification of the murine A vy allele by nutritional supplementation. Proc Natl Acad Sci USA 2006; 46:17308-17312.
41. Crudo A, Petropoulos S, Moisiadis VG, Iqbal M, Kostaki A, Machnes Z, Szyf M, Matthews SG. Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects. Endocrinology 2012;7:3269-3283.
42. Csaba G, Karabelyos C, Inczefi-Gonda A, Pallinger E. Three-generation investigation on serotonin content in rat immune cells long after beta-endorphin exposure in late pregnancy. Horm Metab Res 2005;3:172-177.
43. Cummins JM. The role of maternal mitochondria during oogenesis, fertilization and embryogenesis. Reprod Biomed Online 2002;2:176-182.
44. De Flora S, Balansky R, D'Agostini F, Cartiglia C, Longobardi M, Steele VE, Izzotti A. Smoke-induced microRNA and related proteome alterations. Modulation by chemopreventive agents. Int J Cancer 2012;12:2763-2773.
45. Ding GL,Wang FF, Shu J, Tian S, Jiang Y, Zhang D, Wang N, Luo Q, Zhang Y, Jin F et al. Transgenerational glucose intolerance with Igf2/H19 epigenetic alterations in mouse islet induced by intrauterine hyperglycemia. Diabetes 2012;5:1133-1142.
46. Dinsdale EC, Chen J, Ward WE. Early life exposure to isoflavones adversely affects reproductive health in first but not second generation female CD-1 mice. J Nutr 2011;11:1996-2002.
47. Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci USA 2007;32:13056-13061.
48. Drake AJ,Walker BR, Seckl JR. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol 2005;1:R34-R38.
49. Drake AJ, Liu L, Kerrigan D, Meehan RR, Seckl JR. Multigenerational programming in the glucocorticoid programmed rat is associated with generation-specific and parent of origin effects. Epigenetics 2011;11:1334-1343.
50. Dunn GA, Bale TL. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 2011;6:2228-2236.
51. Ferguson SA, Delclos KB, Newbold RR, Flynn KM. Few effects of multi-generational dietary exposure to genistein or nonylphenol on sodium solution intake in male and female Sprague-Dawley rats. Neurotoxicol Teratol 2009;3:143-148.
52. Francis D, Diorio J, Liu D, Meaney MJ. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999; 5442:1155-1158.
53. Frantz ED, Aguila MB, Pinheiro-Mulder Ada R, Mandarim-de-Lacerda CA. Transgenerational endocrine pancreatic adaptation in mice from maternal protein restriction in utero. Mech Ageing Dev 2011;3:110-116.
54. Fullston T, Palmer NO, Owens JA, Mitchell M, Bakos HW, Lane M. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod 2012;5:1391-1400.
55. Gabory A, Attig L, Junien C. Sexual dimorphism in environmental epigenetic programming. Mol Cell Endocrinol 2009;304:8-18.
56. Garg M, Thamotharan M, Dai Y, Lee PW, Devaskar SU. Embryo-transfer of the F2 postnatal calorie restricted female rat offspring into a control intra-uterine environment normalizes the metabolic phenotype. Metabolism 2013;62:432-441.
57. Gauguier D, Bihoreau MT, Ktorza A, Berthault MF, Picon L. Inheritance of diabetes mellitus as consequence of gestational hyperglycemia in rats. Diabetes 1990; 6:734-739.
58. GilbertWM,Nesbitt TS, Danielsen B. Childbearing beyond age 40: pregnancyoutcome in 24,032 cases. Obstet Gynecol 1999;1:9-14.
59. Gill-Randall R, AdamsD, Ollerton RL, Lewis M, Alcolado JC. Type 2 diabetes mellitus- genes or intrauterine environment? An embryo transfer paradigm in rats. Diabetologia 2004;8:1354-1359.
60. Gluckman PD, Hanson MA, Beedle AS. Non-genomic transgenerational inheritance of disease risk. Bioessays 2007;2:145-154.
61. Gniuli D,Calcagno A, Caristo ME, Mancuso A, Macchi V, Mingrone G, Vettor R. Effects of high-fat diet exposure during fetal life on type 2 diabetes development in the progeny. J Lipid Res 2008;9:1936-1945.
62. Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell 2007; 4:635-638.
63. Harrison M, Langley-Evans SC. Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. Br J Nutr 2009;7:1020-1030.
64. Hemmings DG, Veerareddy S, Baker PN, Davidge ST. Increased myogenic responses in uterine but not mesenteric arteries from pregnant offspring of diet-restricted rat dams. Biol Reprod 2005;4:997-1003.
65. Herbst AL, Ulfelder H, Poskanzer DC. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 1971;15:878-881.
66. Hou L, Wang D, Baccarelli A. Environmental chemicals and microRNAs. Mutat Res 2011;714:105-112.
67. Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, McConnell J. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 2010;4:e10074.
68. Inawaka K, Kawabe M, Takahashi S, Doi Y, Tomigahara Y, Tarui H, Abe J, Kawamura S, Shirai T. Maternal exposure to anti-androgenic compounds, vinclozolin, flutamide and procymidone, has no effects on spermatogenesis and DNA methylation in male rats of subsequent generations. Toxicol Appl Pharmacol 2009; 2:178-187.
69. Jimenez-Chillaron JC, Isganaitis E, Charalambous M, Gesta S, Pentinat-Pelegrin T, Faucette RR, Otis JP, Chow A, Diaz R, Ferguson-Smith A et al. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 2009;2:460-468.
70. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007;4:253-262.
71. Kaati G, Bygren LO, Edvinsson S. Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur J Hum Genet 2002;11:682-688.
72. Karrow NA, Guo TL, Delclos KB, Newbold RR, Weis C, Germolec DR, White KL Jr, McCay JA. Nonylphenol alters the activity of splenic NK cells and the numbers of leukocyte subpopulations in Sprague-Dawley rats: a two-generation feeding study. Toxicology 2004;3:237-245.
73. Knudsen TB, Green ML. Response characteristics of the mitochondrial DNA genome in developmental health and disease. Birth Defects Res C Embryo Today 2004; 4:313-329.
74. Laboratory TJ. Biology of the Laboratory Mouse. New York: Dover, 1976.
75. Lam MK, Homewood J, Taylor AJ, Mazurski EJ. Second generation effects of maternal alcohol consumption during pregnancy in rats. Prog Neuropsychopharmacol Biol Psychiatry 2000;4:619-631.
76. Lees-Murdock DJ, Walsh CP. DNA methylation reprogramming in the germline. Adv Exp Med Biol 2008; 1:1-15.
77. Leese HJ, Hugentobler SA, Gray SM, MorrisDG, Sturmey RG, Whitear SL, Sreenan JM. Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod Fertil Dev 2008;1:1-8.
78. Liang H, XiongW, Zhang Z. Effect of maternal food restriction during gestation on early development of F1 and F2 offspring in the rat-like hamster (Cricetulus triton). Zoology (Jena) 2007;2:118-126.
79. Lie RT. Intergenerational exchange and perinatal risks: a note on interpretation of generational recurrence risks. Paediatr Perinat Epidemiol 2007;21 (Suppl 1):13-18.
80. Mahsoudi B, Li A, O'Neill C. Assessment of the long-term and transgenerational consequences of perturbing preimplantation embryo development in mice. Biol Reprod 2007;5:889-896.
81. Martin JF, Johnston CS, HanCT, BenyshekDC. Nutritional origins of insulin resistance: a rat model for diabetes-prone human populations. J Nutr 2000;4:741-744.
82. Martin JR, Lieber SB, McGrath J, Shanabrough M, Horvath TL, Taylor HS. Maternal ghrelin deficiency compromises reproduction in female progeny through altered uterine developmental programming. Endocrinology 2011;5:2060-2066.
83. Martin-Gronert MS, Ozanne SE. Mechanisms underlying the developmental origins of disease. Rev Endocr Metab Disord 2012a;2:85-92.
84. Martin-Gronert MS, Ozanne SE. Metabolic programming of insulin action and secretion. Diabetes Obes Metab 2012b;14 (Suppl 3):29-39.
85. McLachlan JA, Burow M, Chiang TC, Li SF. Gene imprinting in developmental toxicology: a possible interface between physiology and pathology. Toxicol Lett 2001;120:161-164.
86. Mohamedel SA, Song WH, Oh SA, Park YJ, You YA, Lee S, Choi JY, Kim YJ, Jo I, Pang MG. The transgenerational impact of benzo(a)pyrene on murine male fertility. Hum Reprod 2010;10:2427-2433.
87. Morgan CP, Bale TL. Early prenatal stress epigenetically programs dysmasculinization in second-generationoffspring viathepaternal lineage. JNeurosci2011;33:11748-11755.
88. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 1999;3:314-318.
89. Nascimento FA, Ceciliano TC, Aguila MB, Mandarim-de-Lacerda CA. Maternal vitamin D deficiency delays glomerular maturity in F1 and F2 offspring. PLoS One 2012; 8:e41740.
90. Newbold RR, Padilla-Banks E, Jefferson WN. Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 2006;6(Suppl):S11-S17.
91. Nilsson EE, Anway MD, Stanfield J, Skinner MK. Transgenerational epigenetic effects of the endocrine disruptor vinclozolin on pregnancies and female adult onset disease. Reproduction 2008;5:713-721.
92. Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA. Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 2004;6988:154.
93. Ozanne SE, Constancia M. Mechanisms of disease: the developmental origins of disease and the role of the epigenotype. Nat Clin Pract Endocrinol Metab 2007;7:539-546.
94. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DI, Roseboom TJ. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 2008;10:1243-1249.
95. Palanza PL, Howdeshell KL, Parmigiani S, vom Saal FS. Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ Health Perspect 2002;110 (Suppl 3):415-422.
96. Pallinger E, Tothfalusi L, Csaba G. Prolonged effect of endorphin treatment during pregnancy in the rat on the histamine content of immune cells of F1 and F2 offspring generations. Cell Biochem Funct 2006;4:287-290.
97. Palmer JR, Hatch EE, Rao RS, Kaufman RH, Herbst AL, Noller KL, Titus-Ernstoff L, Hoover RN. Infertility among women exposed prenatally to diethylstilbestrol. Am J Epidemiol 2001;4:316-321.
98. Parasramka MA, Ho E, Williams DE, Dashwood RH. MicroRNAs, diet, and cancer:new mechanistic insights on the epigenetic actions of phytochemicals. Mol Carcinog 2012; 3:213-230.
99. Peixoto-Silva N, Frantz ED, Mandarim-de-Lacerda CA, Pinheiro-Mulder A. Maternal protein restriction in mice causes adverse metabolic and hypothalamic effects in the F1 and F2 generations. Br J Nutr 2011;9:1364-1373.
100. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, Golding J, Team AS. Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 2006;2:159-166.
101. 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;12:5617-5623.
102. Pinheiro AR, Salvucci ID, Aguila MB, Mandarim-de-Lacerda CA. Protein restriction during gestation and/or lactation causes adverse transgenerational effects on biometry and glucose metabolism in F1 and F2 progenies of rats. Clin Sci (Lond) 2008;5:381-392.
103. Pinto ML, Shetty PS. Influence of exercise-induced maternal stress on fetal outcome in Wistar rats: inter-generational effects. Br J Nutr 1995;5:645-653.
104. Pollard I, Claassens R. Caffeine-mediated effects on reproductive health over two generations in rats. Reprod Toxicol 1992;6:541-545.
105. Radford EJ, Isganaitis E, Jimenez-Chillaron J, Schroeder J, Molla M, Andrews S, Didier N, Charalambous M, McEwen K, Marazzi G et al. An unbiased assessment of the role of imprinted genes in an intergenerational model of developmental programming. PLoS Genet 2012;4:e1002605.
106. Raikkonen K, Pesonen AK, Roseboom TJ, Eriksson JG. Early determinants of mental health. Best Pract Res Clin Endocrinol Metab 2012;5:599-611.
107. 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. Proc Natl Acad Sci USA 2003; 5:2538-2543.
108. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001;5532:1089-1093.
109. Rivera RM, Ross JW. Epigenetics in fertilization and preimplantation embryo development. Prog Biophys Mol Biol 2013;pii: S0079-6107(13)00005-9.
110. Salem Yaniv S, Levy A, Wiznitzer A, Holcberg G, Mazor M, Sheiner E. Asignificant linear association exists between advanced maternal age and adverse perinatal outcome. Arch Gynecol Obstet 2011;4:755-759.
111. Salian S, Doshi T, Vanage G. Impairment in protein expression profile of testicular steroid receptor coregulators in male rat offspring perinatally exposed to Bisphenol A. Life Sci 2009;85:11-18.
112. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 2008;2:129-140.
113. Shorter J, Lindquist S. Prions as adaptive conduits of memory and inheritance. Nat Rev Genet 2005;6:435-450.
114. Skinner MK. What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol 2008;1:2-6.
115. Slamberova R, Riley MA, Vathy I. Cross-generational effect of prenatal morphine exposure on neurobehavioral development of rat pups. Physiol Res 2005;6: 655-660.
116. 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;8:e6744.
117. Sloboda DM, Hickey M, Hart R. Reproduction in females: the role of the early life environment. Hum Reprod Update 2011;2:210-227.
118. Steinberg RM, Walker DM, Juenger TE, Woller MJ, Gore AC. Effects of perinatal polychlorinated biphenyls on adult female rat reproduction: development, reproductive physiology, and second generational effects. Biol Reprod 2008; 6:1091-1101.
119. Stewart RJ, Preece RF, Sheppard HG. Twelve generations of marginal protein deficiency. Br J Nutr 1975;2:233-253.
120. Stone AI, Bales KL. Intergenerational transmission of the behavioral consequences of early experience in prairie voles. Behav Processes 2010;3:732-738.
121. Tarry-Adkins JL, Ozanne SE. Mechanisms of early life programming: current knowledge and future directions. Am J Clin Nutr 2011;6(Suppl):1765S-1771S.
122. Thamotharan M, Garg M, Oak S, Rogers LM, Pan G, Sangiorgi F, LeePW, Devaskar SU. Transgenerational inheritance of the insulin-resistant phenotype in embryotransferred intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 2007;5:E1270-E1279.
123. Theys N, Bouckenooghe T, Ahn MT, Remacle C, Reusens B. Maternal low-protein diet alters pancreatic islet mitochondrial function in a sex-specific manner in the adult rat. Am J Physiol Regul Integr Comp Physiol 2009;5:R1516-R1525.
124. Titus-Ernstoff L, Troisi R, Hatch EE, Palmer JR, Hyer M, Kaufman R, Adam E, Noller K, Hoover RN. Birth defects in the sons and daughters of women who were exposed in utero to diethylstilbestrol (DES). Int J Androl 2010;2:377-384.
125. Torrens C, Brawley L, Barker AC, Itoh S, Poston L, Hanson MA. Maternal protein restriction in the rat impairs resistance artery but not conduit artery function in pregnant offspring. J Physiol 2003;547(Pt 1):77-84.
126. Torrens C, Poston L, Hanson MA. Transmission of raised blood pressure and endothelial dysfunction to the F2 generation induced by maternal protein restriction in the F0, in the absence of dietary challenge in the F1 generation. Br J Nutr 2008;4:760-766.
127. Veena SR, Geetha S, Leary SD, Saperia J, Fisher DJ, Kumaran K, Coakley P, Stein CE, Fall CH. Relationships of maternal and paternal birthweights to features of the metabolic syndrome in adult offspring: an inter-generational study in South India. Diabetologia 2007;1:43-54.
128. Verier-Mine O. Outcomes in women with a history of gestational diabetes. Screening and prevention of type 2 diabetes. Literature review. Diabetes Metab 2010;6(Pt 2):595-616.
129. Vickers MH. Developmental programming of the metabolic syndrome - critical windows for intervention. World J Diabetes 2011;9:137-148.
130. Walker DM, GoreAC. Transgenerational neuroendocrine disruption of reproduction. Nat Rev Endocrinol 2011;4:197-207.
131. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 2003;15:5293-5300.
132. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. Epigenetic programming by maternal behavior. Nat Neurosci 2004;8:847-854.
133. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res 2004;3:e38.
134. 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. J Physiol 2005;566(Pt 1):225-236.
135. Zamenhof S, van Marthens E, Grauel L. DNA (cell number) in neonatal brain: second generation (F2) alteration by maternal (F0) dietary protein restriction. Science 1971; 3985:850-851.
136. Zentner GE, Henikoff S. Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 2013;3:259-266.
137. Zhou X, Sun H, Ellen TP, Chen H, Costa M. Arsenite alters global histone H3 methylation. Carcinogenesis 2008;9:1831-1836