Transgenerational effects of maternal diet on metabolic and reproductive ageing

Mammalian Genome

Volumn 27, Issue 7-8, 2016, Pages 430-439

  Aiken, Catherine E ^a   Tarry Adkins, Jane L ^a   Ozanne, Susan E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID;

AGING; CELL AGING; EPIGENETICS; GENE EXPRESSION; HUMAN; INHERITANCE; MATERNAL NUTRITION; METABOLISM; NONHUMAN; OUTCOME ASSESSMENT; PROGENY; REPRODUCTION; REVIEW; TRANSGENERATIONAL EFFECT; ANIMAL; DIET THERAPY; DRUG EFFECTS; FEMALE; GENETIC EPIGENESIS; GENETICS; GUINEA PIG; MATERNAL INHERITANCE; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; SHEEP;

AGING; ANIMALS; EPIGENESIS, GENETIC; FEMALE; GUINEA PIGS; HUMANS; MATERNAL INHERITANCE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SHEEP;

EID: 84964555399     PISSN: 09388990     EISSN: 14321777     Source Type: Journal    
DOI: 10.1007/s00335-016-9631-1     Document Type: Review

References (97)

1. Aerts L, Vercruysse L, Van Assche FA (1997) The endocrine pancreas in virgin and pregnant offspring of diabetic pregnant rats. Diabetes Res Clin Pract 38:9–19
2. Aiken CE, Ozanne SE (2014) Transgenerational developmental programming. Hum Reprod Update 20:63–75
3. Aiken CE, Cindrova-Davies T, Johnson MH (2008) Variations in mouse mitochondrial DNA copy number from fertilization to birth are associated with oxidative stress. Reprod Biomed Online 17:806–813
4. Aiken CE, Tarry-Adkins JL, Ozanne SE (2013) Suboptimal nutrition in utero causes DNA damage and accelerated aging of the female reproductive tract. FASEB J 27:3959–3965
5. Aiken CE, Tarry-Adkins JL, Ozanne SE (2015) Transgenerational developmental programming of ovarian reserve. Sci Rep 5:16175
6. Albertini DF (2012) Searching for answers to the riddle of ovarian aging. J Assist Reprod Genet 29:577–578
7. Alwasel SH, Harrath A, Aljarallah JS, Abotalib Z, Osmond C, Al Omar SY, Khaled I, Barker DJ (2013) Intergenerational effects of in utero exposure to Ramadan in Tunisia. Am J Hum Biol 25:341–343
8. Barbieri P, Crivellenti LC, Nishimura RY, Sartorelli DS (2015) Validation of a food frequency questionnaire to assess food group intake by pregnant women. J Hum Nutr Diet 28(Suppl 1):38–44
9. Benyshek DC, Johnston CS, Martin JF (2004) Post-natal diet determines insulin resistance in fetally malnourished, low birthweight rats (F1) but diet does not modify the insulin resistance of their offspring (F2). Life Sci 74:3033–3041
10. Benyshek DC, Johnston CS, Martin JF (2006) Glucose metabolism is altered in the adequately-nourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 49:1117–1119
11. Bernal AB, Vickers MH, Hampton MB, Poynton RA, Sloboda DM (2010) Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One 5:e15558
12. Blondeau B, Avril I, Duchene B, Breant B (2002) Endocrine pancreas development is altered in foetuses from rats previously showing intra-uterine growth retardation in response to malnutrition. Diabetologia 45:394–401
13. Borgel J, Guibert S, Li Y, Chiba H, Schubeler D, Sasaki H, Forne T, Weber M (2010) Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet 42:1093–1100
14. Brewer GJ (2010) Epigenetic oxidative redox shift (EORS) theory of aging unifies the free radical and insulin signaling theories. Exp Gerontol 45:173–179
15. Broekmans FJ, Soules MR, Fauser BC (2009) Ovarian aging: mechanisms and clinical consequences. Endocr Rev 30:465–493
16. Burdge GC, Hoile SP, Uller T, Thomas NA, Gluckman PD, Hanson MA, Lillycrop KA (2011) Progressive, transgenerational changes in offspring phenotype and epigenotype following nutritional transition. PLoS One 6:e28282
17. Bygren LO, Kaati G, Edvinsson S (2001) Longevity determined by paternal ancestors’ nutrition during their slow growth period. Acta Biotheor 49:53–59
18. Bygren LO, Tinghog P, Carstensen J, Edvinsson S, Kaati G, Pembrey ME, Sjostrom M (2014) Change in paternal grandmothers’ early food supply influenced cardiovascular mortality of the female grandchildren. BMC Genet 15:12
19. Chernoff N, Gage MI, Stoker TE, Cooper RL, Gilbert ME, Rogers EH (2009) 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 28:489–494
20. Constantinof A, Moisiadis VG, Matthews SG (2015) Programming of stress pathways: A transgenerational perspective. J Steroid Biochem Mol Biol. doi:10.1016/j.jsbmb.2015.10.008
21. Crudo A, Petropoulos S, Moisiadis VG, Iqbal M, Kostaki A, Machnes Z, Szyf M, Matthews SG (2012) Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects. Endocrinology 153:3269–3283
22. de Rooij SR, van Pelt AM, Ozanne SE, Korver CM, van Daalen SK, Painter RC, Schwab M, Viegas MH, Roseboom TJ (2015) Prenatal undernutrition and leukocyte telomere length in late adulthood: the Dutch famine birth cohort study. Am J Clin Nutr 102:655–660
23. Donovan SJ, Susser E (2011) Commentary: advent of sibling designs. Int J Epidemiol 40:345–349
24. Dunn GA, Bale TL (2011) Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152:2228–2236
25. Entringer S, Buss C, Wadhwa PD (2010) Prenatal stress and developmental programming of human health and disease risk: concepts and integration of empirical findings. Curr Opin Endocrinol Diabetes Obes 17:507–516
26. Entringer S, Epel ES, Lin J, Blackburn EH, Buss C, Shahbaba B, Gillen DL, Venkataramanan R, Simhan HN, Wadhwa PD (2015) Maternal folate concentration in early pregnancy and newborn telomere length. Ann Nutr Metab 66:202–208
27. Fernandez-Twinn DS, Alfaradhi MZ, Martin-Gronert MS, Duque-Guimaraes DE, Piekarz A, Ferland-McCollough D, Bushell M, Ozanne SE (2014) Downregulation of IRS-1 in adipose tissue of offspring of obese mice is programmed cell-autonomously through post-transcriptional mechanisms. Mol Metab 3:325–333
28. Frantz ED, Aguila MB, Pinheiro-Mulder Ada R, Mandarim-de-Lacerda CA (2011) Transgenerational endocrine pancreatic adaptation in mice from maternal protein restriction in utero. Mech Ageing Dev 132:110–116
29. Fullston T, Palmer NO, Owens JA, Mitchell M, Bakos HW, Lane M (2012) Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod 27:1391–1400
30. Fullston T, Ohlsson Teague EM, Palmer NO, DeBlasio MJ, Mitchell M, Corbett M, Print CG, Owens JA, Lane M (2013) Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J 27:4226–4243
31. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, Farinelli L, Miska E, Mansuy IM (2014) Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 17:667–669
32. Gaydos LJ, Wang W, Strome S (2014) Gene repression. H3K27me and PRC2 transmit a memory of repression across generations and during development. Science 345:1515–1518
33. Giussani DA, Davidge ST (2013) Developmental programming of cardiovascular disease by prenatal hypoxia. J Dev Orig Health Dis 4:328–337
34. Gniuli D, Calcagno A, Caristo ME, Mancuso A, Macchi V, Mingrone G, Vettor R (2008) Effects of high-fat diet exposure during fetal life on type 2 diabetes development in the progeny. J Lipid Res 49:1936–1945
35. Graus-Nunes F, Dalla Corte Frantz E, Lannes WR, da Silva Menezes MC, Mandarim-de-Lacerda CA, Souza-Mello V (2015) Pregestational maternal obesity impairs endocrine pancreas in male F1 and F2 progeny. Nutrition 31:380–387
36. Hemmings DG, Veerareddy S, Baker PN, Davidge ST (2005) Increased myogenic responses in uterine but not mesenteric arteries from pregnant offspring of diet-restricted rat dams. Biol Reprod 72:997–1003
37. Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, McConnell J (2010) Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 5:e10074
38. Ingvorsen C, Brix S, Ozanne SE, Hellgren LI (2015) The effect of maternal Inflammation on foetal programming of metabolic disease. Acta Physiol (Oxf) 214:440–449
39. Iqbal M, Moisiadis VG, Kostaki A, Matthews SG (2012) Transgenerational effects of prenatal synthetic glucocorticoids on hypothalamic-pituitary-adrenal function. Endocrinology 153:3295–3307
40. Ishihara J (2015) Challenges in dietary exposure assessment in epidemiology: research trends. J Nutr Sci Vitaminol (Tokyo) 61:S33–S35
41. Jennings BJ, Ozanne SE, Dorling MW, Hales CN (1999) Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. FEBS Lett 448:4–8
42. Jimenez-Chillaron JC, Ramon-Krauel M, Ribo S, Diaz R (2015) Transgenerational epigenetic inheritance of diabetes risk as a consequence of early nutritional imbalances. Proc Nutr Soc 75:1–12
43. Kaiser LL, Campbell CG, Academy Positions Committee W (2014) Practice paper of the Academy of Nutrition and Dietetics abstract: nutrition and lifestyle for a healthy pregnancy outcome. J Acad Nutr Diet 114:1447
44. Khashan AS, McNamee R, Henriksen TB, Pedersen MG, Kenny LC, Abel KM, Mortensen PB (2011) Risk of affective disorders following prenatal exposure to severe life events: a Danish population-based cohort study. J Psychiatr Res 45:879–885
45. Laplante DP, Brunet A, Schmitz N, Ciampi A, King S (2008) Project Ice Storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry 47:1063–1072
46. Leese HJ, Hugentobler SA, Gray SM, Morris DG, Sturmey RG, Whitear SL, Sreenan JM (2008) Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod Fertil Dev 20:1–8
47. Li Q, Geng X, Zheng W, Tang J, Xu B, Shi Q (2012) Current understanding of ovarian aging. Sci China Life Sci 55:659–669
48. Li J, Na L, Ma H, Zhang Z, Li T, Lin L, Li Q, Sun C, Li Y (2015) Multigenerational effects of parental prenatal exposure to famine on adult offspring cognitive function. Sci Rep 5:13792
49. Long NM, Ford SP, Nathanielsz PW (2013) Multigenerational effects of fetal dexamethasone exposure on the hypothalamic-pituitary-adrenal axis of first- and second-generation female offspring. Am J Obstet Gynecol 208(217):e211–e218
50. Lumey LH, Stein AD, Kahn HS, van der Pal-de Bruin KM, Blauw GJ, Zybert PA, Susser ES (2007) Cohort profile: the Dutch Hunger Winter families study. Int J Epidemiol 36:1196–1204
51. 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 89:1737–1743
52. Mahmood S, Smiraglia DJ, Srinivasan M, Patel MS (2013) Epigenetic changes in hypothalamic appetite regulatory genes may underlie the developmental programming for obesity in rat neonates subjected to a high-carbohydrate dietary modification. J Dev Orig Health Dis 4:479–490
53. Martinez D, Pentinat T, Ribo S, Daviaud C, Bloks VW, Cebria J, Villalmanzo N, Kalko SG, Ramon-Krauel M, Diaz R, Plosch T, Tost J, Jimenez-Chillaron JC (2014) In utero undernutrition in male mice programs liver lipid metabolism in the second-generation offspring involving altered Lxra DNA methylation. Cell Metab 19:941–951
54. Masuyama H, Mitsui T, Nobumoto E, Hiramatsu Y (2015) The effects of high-fat diet exposure in utero on the obesogenic and diabetogenic traits through epigenetic changes in adiponectin and leptin gene expression for multiple generations in female mice. Endocrinology 156:2482–2491
55. Mathias PC, Elmhiri G, de Oliveira JC, Delayre-Orthez C, Barella LF, Tofolo LP, Fabricio GS, Chango A, Abdennebi-Najar L (2014) Maternal diet, bioactive molecules, and exercising as reprogramming tools of metabolic programming. Eur J Nutr 53:711–722
56. Michalakis K, Mintziori G, Kaprara A, Tarlatzis BC, Goulis DG (2013) The complex interaction between obesity, metabolic syndrome and reproductive axis: a narrative review. Metabolism 62:457–478
57. Misra DP, Astone N, Lynch CD (2005) Maternal smoking and birth weight: interaction with parity and mother’s own in utero exposure to smoking. Epidemiology 16:288–293
58. Nascimento FA, Ceciliano TC, Aguila MB, Mandarim-de-Lacerda CA (2013) Transgenerational effects on the liver and pancreas resulting from maternal vitamin D restriction in mice. J Nutr Sci Vitaminol (Tokyo) 59:367–374
59. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, Mullany EC, Biryukov S, Abbafati C, Abera SF, Abraham JP, Abu-Rmeileh NM, Achoki T, AlBuhairan FS, Alemu ZA, Alfonso R, Ali MK, Ali R, Guzman NA, Ammar W, Anwari P, Banerjee A, Barquera S, Basu S, Bennett DA, Bhutta Z, Blore J, Cabral N, Nonato IC, Chang JC, Chowdhury R, Courville KJ, Criqui MH, Cundiff DK, Dabhadkar KC, Dandona L, Davis A, Dayama A, Dharmaratne SD, Ding EL, Durrani AM, Esteghamati A, Farzadfar F, Fay DF, Feigin VL, Flaxman A, Forouzanfar MH, Goto A, Green MA, Gupta R, Hafezi-Nejad N, Hankey GJ, Harewood HC, Havmoeller R, Hay S, Hernandez L, Husseini A, Idrisov BT, Ikeda N, Islami F, Jahangir E, Jassal SK, Jee SH, Jeffreys M, Jonas JB, Kabagambe EK, Khalifa SE, Kengne AP, Khader YS, Khang YH, Kim D, Kimokoti RW, Kinge JM, Kokubo Y, Kosen S, Kwan G, Lai T, Leinsalu M, Li Y, Liang X, Liu S, Logroscino G, Lotufo PA, Lu Y, Ma J, Mainoo NK, Mensah GA, Merriman TR, Mokdad AH, Moschandreas J, Naghavi M, Naheed A, Nand D, Narayan KM, Nelson EL, Neuhouser ML, Nisar MI, Ohkubo T, Oti SO, Pedroza A, Prabhakaran D, Roy N, Sampson U, Seo H, Sepanlou SG, Shibuya K, Shiri R, Shiue I, Singh GM, Singh JA, Skirbekk V, Stapelberg NJ, Sturua L, Sykes BL, Tobias M, Tran BX, Trasande L, Toyoshima H, van de Vijver S, Vasankari TJ, Veerman JL, Velasquez-Melendez G, Vlassov VV, Vollset SE, Vos T, Wang C, Wang X, Weiderpass E, Werdecker A, Wright JL, Yang YC, Yatsuya H, Yoon J, Yoon SJ, Zhao Y, Zhou M, Zhu S, Lopez AD, Murray CJ, Gakidou E (2014a) Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384:766–781
60. Ng SF, Lin RC, Maloney CA, Youngson NA, Owens JA, Morris MJ (2014b) Paternal high-fat diet consumption induces common changes in the transcriptomes of retroperitoneal adipose and pancreatic islet tissues in female rat offspring. FASEB J 28:1830–1841
61. Ong TP, Ozanne SE (2015) Developmental programming of type 2 diabetes: early nutrition and epigenetic mechanisms. Curr Opin Clin Nutr Metab Care 18:354–360
62. Ozanne S (2014) Nutrigenomic programming of cardiovascular and metabolic diseases. Free Radic Biol Med 75(Suppl 1):S11
63. Ozanne SE (2015) Epigenetics and metabolism in 2014: metabolic programming–knowns, unknowns and possibilities. Nat Rev Endocrinol 11:67–68
64. Ozanne SE, Hales CN (2004) Lifespan: catch-up growth and obesity in male mice. Nature 427:411–412
65. Padmanabhan V, Veiga-Lopez A (2014) Reproduction Symposium: developmental programming of reproductive and metabolic health. J Anim Sci 92:3199–3210
66. Padmanabhan V, Cardoso RC, Puttabyatappa M (2016) Developmental programming, a pathway to disease. Endocrinology. Endocrinology. doi:10.1210/en.2016-1003
67. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DI, Roseboom TJ (2008) Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 115:1243–1249
68. Peckham CS (1973) A national study of child development (NCDS 1958 cohort). Preliminary findings in a national sample of 11-year-old children. Proc R Soc Med 66:701–703
69. Pembrey M, Saffery R, Bygren LO, Network in Epigenetic E (2014) Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research. J Med Genet 51:563–572
70. Penfold NC, Ozanne SE (2015) Developmental programming by maternal obesity in 2015: outcomes, mechanisms, and potential interventions. Horm Behav 76:143–152
71. Pentinat T, Ramon-Krauel M, Cebria J, Diaz R, Jimenez-Chillaron JC (2010) Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition. Endocrinology 151:5617–5623
72. Radford EJ, Isganaitis E, Jimenez-Chillaron J, Schroeder J, Molla M, Andrews S, Didier N, Charalambous M, McEwen K, Marazzi G, Sassoon D, Patti ME, Ferguson-Smith AC (2012) An unbiased assessment of the role of imprinted genes in an intergenerational model of developmental programming. PLoS Genet 8:e1002605
73. Radford EJ, Ito M, Shi H, Corish JA, Yamazawa K, Isganaitis E, Seisenberger S, Hore TA, Reik W, Erkek S, Peters AH, Patti ME, Ferguson-Smith AC (2014) In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 345:1255903
74. 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 70:811–816
75. Reynolds CM, Gray C, Li M, Segovia SA, Vickers MH (2015) Early life nutrition and energy balance disorders in offspring in later life. Nutrients 7:8090–8111
76. Rickard IJ, Courtiol A, Prentice AM, Fulford AJ, Clutton-Brock TH, Lummaa V (2012) Intergenerational effects of maternal birth season on offspring size in rural Gambia. Proc Biol Sci 279:4253–4262
77. Rodriguez-Gonzalez GL, Reyes-Castro LA, Vega CC, Boeck L, Ibanez C, Nathanielsz PW, Larrea F, Zambrano E (2014) Accelerated aging of reproductive capacity in male rat offspring of protein-restricted mothers is associated with increased testicular and sperm oxidative stress. Age (Dordr) 36:9721
78. 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 17:325–330
79. Segovia SA, Vickers MH, Zhang XD, Gray C, Reynolds CM (2015) Maternal supplementation with conjugated linoleic acid in the setting of diet-induced obesity normalises the inflammatory phenotype in mothers and reverses metabolic dysfunction and impaired insulin sensitivity in offspring. J Nutr Biochem 26:1448–1457
80. Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, Santos F, Popp C, Thienpont B, Dean W, Reik W (2012) The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48:849–862
81. Sharp GC, Lawlor DA, Richmond RC, Fraser A, Simpkin A, Suderman M, Shihab HA, Lyttleton O, McArdle W, Ring SM, Gaunt TR, Davey Smith G, Relton CL (2015) Maternal pre-pregnancy BMI and gestational weight gain, offspring DNA methylation and later offspring adiposity: findings from the Avon Longitudinal Study of Parents and Children. Int J Epidemiol 44:1288–1304
82. Shasa DR, Odhiambo JF, Long NM, Tuersunjiang N, Nathanielsz PW, Ford SP (2015) Multigenerational impact of maternal overnutrition/obesity in the sheep on the neonatal leptin surge in granddaughters. Int J Obes (Lond) 39:695–701
83. Skinner MK (2008) What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol 25:2–6
84. Sloboda DM, Hickey M, Hart R (2011) Reproduction in females: the role of the early life environment. Hum Reprod Update 17:210–227
85. 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 72:641–654
86. Strakovsky RS, Zhang X, Zhou D, Pan YX (2014) The regulation of hepatic Pon1 by a maternal high-fat diet is gender specific and may occur through promoter histone modifications in neonatal rats. J Nutr Biochem 25:170–176
87. Susser E, Kirkbride JB, Heijmans BT, Kresovich JK, Lumey LH, Stein AD (2012) Maternal prenatal nutrition and health in grandchildren and subsequent generations. Annu Rev Anthropol 41:577–610
88. Tarry-Adkins JL, Chen JH, Smith NS, Jones RH, Cherif H, Ozanne SE (2009) Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB J 23:1521–1528
89. Tarry-Adkins JL, Martin-Gronert MS, Fernandez-Twinn DS, Hargreaves I, Alfaradhi MZ, Land JM, Aiken CE, Ozanne SE (2012) Poor maternal nutrition followed by accelerated postnatal growth leads to alterations in DNA damage and repair, oxidative and nitrosative stress, and oxidative defense capacity in rat heart. FASEB J. doi:10.1096/fj.12-218685
90. Tarry-Adkins JL, Fernandez-Twinn DS, Chen JH, Hargreaves IP, Martin-Gronert MS, McConnell JM, Ozanne SE (2014) Nutritional programming of coenzyme Q: potential for prevention and intervention? FASEB J 28:5398–5405
91. Thamotharan M, Garg M, Oak S, Rogers LM, Pan G, Sangiorgi F, Lee PW, Devaskar SU (2007) Transgenerational inheritance of the insulin-resistant phenotype in embryo-transferred intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 292:E1270–E1279
92. Veenendaal MV, Painter RC, de Rooij SR, Bossuyt PM, van der Post JA, Gluckman PD, Hanson MA, Roseboom TJ (2013) Transgenerational effects of prenatal exposure to the 1944-45 Dutch famine. BJOG 120:548–553
93. Yarde F, Broekmans FJ, van der Pal-de Bruin KM, Schonbeck Y, te Velde ER, Stein AD, Lumey LH (2013) Prenatal famine, birthweight, reproductive performance and age at menopause: the Dutch hunger winter families study. Hum Reprod 28:3328–3336
94. Zambrano E, Martinez-Samayoa PM, Bautista CJ, Deas M, Guillen L, Rodriguez-Gonzalez GL, Guzman C, Larrea F, Nathanielsz PW (2005) 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 566:225–236
95. Zambrano E, Guzman C, Rodriguez-Gonzalez GL, Durand-Carbajal M, Nathanielsz PW (2014) Fetal programming of sexual development and reproductive function. Mol Cell Endocrinol 382:538–549
96. Zambrano E, Ibanez C, Martinez-Samayoa PM, Lomas-Soria C, Durand-Carbajal M, Rodriguez-Gonzalez GL (2016) Maternal obesity: lifelong metabolic outcomes for offspring from poor developmental trajectories during the perinatal period. Arch Med Res 47(1):1–12
97. Zander-Fox DL, Fullston T, McPherson NO, Sandeman L, Kang WX, Good SB, Spillane M, Lane M (2015) Reduction of mitochondrial function by fccp during mouse cleavage stage embryo culture reduces birth weight and impairs the metabolic health of offspring. Biol Reprod 92:124