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The role of early life nutrition in programming of reproductive function

Published online by Cambridge University Press:  16 August 2013

S. Chadio  and
B. Kotsampasi
S. Chadio*
Affiliation:
Department of Anatomy and Physiology of Domestic Animals, Faculty of Animal Science, Agricultural University of Athens, Athens, Greece
B. Kotsampasi
Affiliation:
Animal Research Institute, Hellenic Agricultural Organization-DEMETER, Giannitsa, Greece
*
*Address for correspondence: Dr S. Chadio, Department of Anatomy and Physiology of Domestic Animals, Faculty of Animal Science, Agricultural University of Athens, 75, Iera odos, 11855 Athens, Greece. (Email [email protected])
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Abstract

Accumulating evidence suggest that the concept of programming can also be applied to reproductive development and function, representing an ever expanding research area. Recently issues such as peri- or even preconceptional nutrition, transgenerational effects and underlying mechanisms have received considerable attention. The present chapter presents the existed evidence and reviews the available data from numerous animal and human studies on the effects of early life nutritional environment on adult reproductive function. Specific outcomes depend on the severity, duration and stage of development when nutritional perturbations are imposed, while sex-specific effects are also manifested. Apart from undernutrition, effects of relative overnutrition as well as the complex interactions between pre- and postnatal nutrition is of high importance, especially in the context of our days obesity epidemic. Mechanisms underlying reproductive programming are yet unclear, but may include a role for epigenetic modifications. Epigenetic modulation of critical genes involved in the control of reproductive function and potential intergenerational effects represent an exciting area of interdisciplinary research toward the development of new nutritional approaches during pre- and postnatal periods to ensure reproductive health in later life.

Keywords

early nutritionepigeneticsprogrammingreproduction
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 5 , Issue 1 , February 2014 , pp. 2 - 15
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2013 

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References

1. Armitage, JA, Khan, IY, Taylor, PD, Nathanielsz, PW, Poston, L. Developmental programming of metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J Physiol Online. 2004; 561, 355–377.CrossRefGoogle ScholarPubMed
2. McMillen, IC, Robinson, JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005; 85, 571–633.CrossRefGoogle ScholarPubMed
3. Ojeda, NB, Grigore, D, Alexander, BT. Developmental programming of hypertension: insight from animal models of nutritional manipulation. Hypertension. 2008; 52, 44–50.CrossRefGoogle ScholarPubMed
4. Gardner, DS, Ozanne, SE, Sinclair, KD. Effect of the early-life nutritional environment on fecundity and fertility of mammals. Philos T Roy Soc B. 2009; 364, 3419–3427.CrossRefGoogle ScholarPubMed
5. Sloboda, DM, Hickey, M, Hart, R. Reproduction in females: the role of the early life environment. Hum Reprod Update. 2010; 17, 1–19.Google ScholarPubMed
6. Dupont, C, Cordier, AG, Junien, C, et al. Maternal environment and the reproductive function of the offspring. Theriogenology. 2012; 78, 1405–1414.CrossRefGoogle ScholarPubMed
7. Fleming, TP, Velazquez, MA, Eckert, JJ, Lucas, ES, Watkins, AJ. Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring. Anim Reprod Sci. 2012; 130, 193–197.CrossRefGoogle ScholarPubMed
8. Ebling, JFP. The neuroendocrine timing of puberty. Reproduction. 2005; 129, 675–683.CrossRefGoogle ScholarPubMed
9. Seminara, SB, Messager, S, Chatzidaki, EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003; 349, 1614–1627.CrossRefGoogle ScholarPubMed
10. Teles, MG, Bianco, SD, Brito, VN, et al. A GPR54-activating mutation in a patient with central precocious puberty. N Engl J Med. 2008; 358, 709–715.CrossRefGoogle Scholar
11. Semple, RK, Achermann, JC, Ellery, J, et al. Two novel missense mutations in g protein-coupled receptor 54 in a patient with hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2005; 90, 1849–1855.CrossRefGoogle Scholar
12. Pinilla, L, Aguilar, E, Dieguez, C, Millar, RP, Manuel Tena-Sempere, M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev. 2012; 92, 1235–1316.CrossRefGoogle ScholarPubMed
13. Fink, G, Pfaff, DW, Levine, J. Neuroendocrine mechanisms of puberty. Handbook of Neuroendocrinology, 2012; pp. 434–484. London: Academic Press.Google Scholar
14. Gottsch, ML, Cunningham, MJ, Smith, JT, et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology. 2004; 145, 4073–4077.CrossRefGoogle ScholarPubMed
15. Messager, S, Chatzidaki, EE, Ma, D, et al. Kisspeptin directly stimulates gonadotropin- releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA. 2005; 102, 1761–1766.CrossRefGoogle ScholarPubMed
16. Dhillo, WS, Chaudhri, OB, Patterson, M, et al. Kisspeptin-54 stimulates the hypothalamic–pituitary gonadal axis in human males. J Clin Endocrinol Metab. 2005; 90, 6609–6615.CrossRefGoogle ScholarPubMed
17. Lehman, MN, Merkley, CM, Coolen, LM, Goodman, RL. Anatomy of the kisspeptin neural network in mammals. Brain Res. 2010; 1364, 90–102.CrossRefGoogle ScholarPubMed
18. Goodman, RL, Lehman, MN. Kisspeptin neurons from mice to men: similarities and differences. Endocrinology. 2012; 153, 5105–5118.CrossRefGoogle ScholarPubMed
19. Roa, J, García-Galiano, D, Castellano, JM, et al. Metabolic control of puberty onset: new players, new mechanisms. Mol Cell Endocrinol. 2010; 324, 87–94.CrossRefGoogle ScholarPubMed
20. Caron, E, Ciofi, P, Prevot, V, Bouret, SG. Alteration in neonatal nutrition causes perturbations in hypothalamic neural circuits controlling reproductive function. J Neurosci. 2012; 32, 11486–11494.CrossRefGoogle ScholarPubMed
21. Messager, S, Chatzidaki, EE, Ma, D, et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA. 2005; 102, 1761–1766.CrossRefGoogle ScholarPubMed
22. Gamba, M, Pralong, F. Control of GnRH neuronal activity by metabolic factors: the role of leptin and insulin. Mol and cell endocr. 2006; 254-255, 133–139.CrossRefGoogle ScholarPubMed
23. Castellano, JM, Bentsen, AH, Mikkelsen, JD, Tena-Sempere, M. Kisspeptins: bridging energy homeostasis and reproduction. Brain Res. 2010; 1364, 129–138.CrossRefGoogle ScholarPubMed
24. Cameron, NM, Del Corpo, A, Diorio, J, et al. Maternal programming of sexual behaviour and hypothalamic–pituitary–gonadal function in the female rat. PLoS One. 2008; 3: e2210. doi:10.137/journal.pone.0002210.CrossRefGoogle ScholarPubMed
25. Cameron, NM. Maternal programming of reproductive function and behaviour in the female rat. Front Evol Neurosci. 2011; 3, 1–10.CrossRefGoogle ScholarPubMed
26. Engelbregt, MJ, Houdijk, T, Popp-Snijders, M, Delemarre-Van de Waal, HA. The effects of intra-uterine growth retardation and postnatal undernutrition on onset of puberty in male and female rats. Pediatr Res. 2000; 48, 803–807.CrossRefGoogle ScholarPubMed
27. Leonhardt, M, Lesage, J, Croix, D, et al. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod. 2003; 68, 390–400.CrossRefGoogle ScholarPubMed
28. Iwasa, T, Matsuzaki, T, Murakami, M, et al. Effects of intrauterine undernutrition on hypothalamic Kiss 1 expression and the timing of puberty in female rats. J Physiol. 2010; 88, 821–829.CrossRefGoogle Scholar
29. Castellano, JM, Bentsen, AH, Sánchez-Garrido, MA, et al. Early metabolic programming of puberty onset: impact of changes in postnatal feeding and rearing conditions on the timing of puberty and development of the hypothalamic kisspeptin system. Endocrinology. 2011; 152, 3396–3408.CrossRefGoogle ScholarPubMed
30. Sloboda, DM, Howie, GJ, Pleasants, A, Gluckman, PD, Vickers, MH. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One. 2009; 4, e6744.CrossRefGoogle ScholarPubMed
31. Rae, MT, Palassio, S, Kyle, CE, et al. Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Reproduction. 2001; 122, 915–922.CrossRefGoogle ScholarPubMed
32. Da Silva, P, Aiken, RP, Rhind, SM, Racey, PA, Wallace, JM. Influence of placentally mediated fetal growth restriction on the onset of puberty in male and female lambs. Reproduction. 2001; 122, 375–383.CrossRefGoogle ScholarPubMed
33. Kotsampasi, B, Chadio, S, Papadomichelakis, G, et al. Effects of maternal undenutrition on the hypothalamic–pituitary–gonadal axis function in female sheep offspring. Reprod Domest Anim. 2009; 44, 677–684.CrossRefGoogle Scholar
34. Kotsampasi, B, Balaskas, C, Papadomichelakis, G, Chadio, SE. Reduced Sertoli cell number and altered pituitary responsiveness in male lambs undernourished in utero . Anim Reprod Sci. 2009; 114, 135–147.CrossRefGoogle ScholarPubMed
35. Chumlea, WC, Schubert, CM, Roche, AF, et al. Age at menarche and racial comparisons in US girls. Pediatrics. 2003; 111, 110–113.CrossRefGoogle ScholarPubMed
36. Karlbeg, J. Secular trends in pubertal development. Horm Res. 2002; 57, 19–30.Google Scholar
37. Papadimitriou, A, Fytanidis, G, Douros, K, et al. Age at menarche in contemporary Greek girls: evidence for levelling-off of the secular trend. Acta Paediatr. 2008; 97, 812–815.CrossRefGoogle ScholarPubMed
38. Hernández, MI, Mericq, V. Pubertal development in girls born small for gestational age. J Pediatr Endocr Metab. 2008; 21, 201–208.CrossRefGoogle ScholarPubMed
39. Sloboda, DM, Hickey, M, Hart, R. Reproduction in females: the role of the early life environment. Hum Reprod Update. 2011; 17, 210–227.CrossRefGoogle ScholarPubMed
40. Cooper, C, Kuh, D, Egger, P, Wadsworth, M, Barker, D. Childhood growth and age at menarche. Br J Obstet Gynaec. 1996; 103, 814–817.CrossRefGoogle ScholarPubMed
41. Ibanez, L, Ferrer, A, Marcos, MV, Hierro, FR, de Zegher, F. Early puberty: rapid progression and reduced final height in girls with low birth weight. Pediatrics. 2000; 106, e72.CrossRefGoogle ScholarPubMed
42. Lazar, L, Pollak, U, Kalter-Leibovici, O, Pertzelan, A, Phillip, M. Pubertal course of persistently short children born small for gestational age (SGA) compared with idiopathic short children born appropriate for gestational age. Eur J Endocrinol. 2003; 149, 425–432.CrossRefGoogle ScholarPubMed
43. Sloboda, DM, Hart, R, Doherty, DA, Pennell, CE, Hickey, M. Age at menarche: influences of prenatal and postnatal growth. J Clin Endocr Metab. 2007; 92, 46–50.CrossRefGoogle ScholarPubMed
44. Karaolis-Danckert, N, Buyken, AE, Sonntag, A, Kroke, A. Birth and early life influences on the timing of puberty onset: results from the DONALD (Dortmund Nutritional and Anthropometric Longitudinally Designed Study). Am J Clin Nutr. 2009; 90, 1559–1565.CrossRefGoogle ScholarPubMed
45. Kuzawa, CW, McDade, TW, Adair, LS, Lee, N. Rapid weight gain after birth predicts life history and reproductive strategy in Filipino males. Proc Nat Acad Sci. 2010; 107, 16800–16805.CrossRefGoogle ScholarPubMed
46. Ong, K, Ahmed, ML, Emmett, PM, Preece, MA, Dunger, DB, the ALSPAC Study Team. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. Brit Med J. 2000; 320, 967–971.CrossRefGoogle ScholarPubMed
47. Dunger, DB, Ahmed, ML, Ong, K. Early and late weight gain and the timing of puberty. Mol Cell Endocrinol. 2006; 140, 254–255.Google Scholar
48. Ibanez, L, Valls, C, Ong, K, Dunger, DB, de Zegher, F. Metformin therapy during puberty delays menarche, prolongs pubertal growth, and augments adult height: a randomized study in low-birth-weight girls with early-normal onset of puberty. J Clin Endocr Metab. 2006; 91, 2068–2073.CrossRefGoogle ScholarPubMed
49. Ibanez, L, Lopez Bermejo, A, Diaz, M, Marcos, MV, de Zegher, F. Metformin treatment for 4 years to reduce total and visceral fat in low birth weight girls with precocious pubarche. J Clin Endocr Metab. 2008; 93, 1841–1845.CrossRefGoogle ScholarPubMed
50. Hales, CN, Ozanne, SE. The dangerous road of catch-up growth. J Physiol. 2003; 547, 5–10.CrossRefGoogle ScholarPubMed
51. Sarraj, A, Drummond, AE. Mammalian foetal ovarian development: consequences for health and disease. Reproduction. 2012; 143, 151–163.CrossRefGoogle ScholarPubMed
52. Eddy, EM, Clark, JM, Gong, D, Fenderson, BA. Origin and migration of primordial germ cells in mammals. Gamete Res. 1981; 4, 333–362.CrossRefGoogle Scholar
53. Sawyer, HR, Smith, P, Heath, DA, et al. Formation of ovarian follicles during fetal development in sheep. Biol Reprod. 2002; 66, 1134–1150.CrossRefGoogle ScholarPubMed
54. Suh, CS, Sonntag, B, Erickson, GF. The ovarian life cycle: a contemporary view. Rev Endocr Metab Disord. 2002; 3, 5–12.CrossRefGoogle ScholarPubMed
55. Merchant-Larios, H. Rat gonadal and ovarian organogenesis with and without germ cells. An ultrastructural study. Dev Biol. 1975; 44, 1–21.CrossRefGoogle Scholar
56. Juengel, JL, Sawyer, HR, Smith, PR, et al. Origin of follicular cells and ontogeny of steroidogenesis in ovine fetal ovaries. Mol Cell Endocr. 2002; 191, 1–10.CrossRefGoogle ScholarPubMed
57. Francavilla, S, Cordeschi, G, Properzi, G, et al. Ultrastructure of fetal human gonad before sexual differentiation and during early testicular and ovarian development. J Submicrosc Cytol Pathol. 1990; 22, 389–400.Google ScholarPubMed
58. Bayne, RA, Martins da Silva, SJ, Anderson, RA. Increased expression of the FIGLA transcription factor is associated with primordial follicle formation in the human fetal ovary. Mol Hum Reprod. 2004; 10, 373–381.CrossRefGoogle ScholarPubMed
59. Rajah, R, Glaser, EM, Hirshfield, AN. The changing architecture of the neonatal rat ovary during histogenesis. Dev Dyn. 1992; 194, 177–192.CrossRefGoogle ScholarPubMed
60. McGee, EA, Hsueh, AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev. 2000; 21, 200–214.Google ScholarPubMed
61. Gougeon, A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev. 1996; 17, 121–155.CrossRefGoogle ScholarPubMed
62. Sharpe, RM, McKinnell, C, Kivlin, C, Fisher, JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction. 2003; 125, 769–784.CrossRefGoogle ScholarPubMed
63. Plant, TM, Marshall, GR. The functional significance of FSH in spermatogenesis and the control of its secretion in male primates. Endocr Rev. 2001; 22, 764–786.CrossRefGoogle ScholarPubMed
64. Zambrano, E, Rodriguez-Gonzalez, GL, Guzman, C, et al. A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol Online. 2005; 563, 275–284.CrossRefGoogle ScholarPubMed
65. Da Silva, P, Aitken, RP, Rhind, SM, Racey, PA, Wallace, JM. Effect of maternal overnutrition during pregnancy on pituitary gonadotrophin gene expression and gonadal morphology in female and male foetal sheep at day 103 of gestation. Placenta. 2003; 24, 248–257.CrossRefGoogle ScholarPubMed
66. Bielli, A, Perez, R, Pedrana, G, et al. Low maternal nutrition during pregnancy reduces the number of Sertoli cells in the newborn lamb. Reprod Fert Develop. 2002; 14, 333–337.CrossRefGoogle Scholar
67. Orth, JM, Gunsalus, GL, Lamperti, AA. Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology. 1988; 122, 787–794.CrossRefGoogle ScholarPubMed
68. Rae, MT, Rhind, SM, Fowler, PA, et al. Effect of maternal undernutrition on fetal testicular steroidogenesis during the CNS androgen-responsive period in male sheep fetuses. Reproduction. 2002; 124, 33–39.CrossRefGoogle ScholarPubMed
69. Rae, MT, Rhind, SM, Kyle, CE, Miller, DW, Brooks, AN. Maternal undernutrition alters triiodothyronine concentrations and pituitary response to GnRH in fetal sheep. J Endocrinol. 2002; 173, 449–455.CrossRefGoogle ScholarPubMed
70. Deligeorgis, SG, Chadio, S, Menegatos, J. Pituitary responsiveness to GnRH in lambs undernourished during fetal life. Anim Reprod Sci. 1996; 43, 113–121.CrossRefGoogle Scholar
71. da Silva Faria, T, de Bittencourt, F, Sampaio, FJ, da Fonte Ramos, C. Maternal malnutrition during lactation alters the folliculogenesis and gonadotropins and estrogen isoforms receptors in the offspring at puberty. J Endocrinol. 2008; 198, 625–634.CrossRefGoogle Scholar
72. 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; 5, 1–12.CrossRefGoogle ScholarPubMed
73. Connor, KL, Vickers, MH, Beltrand, J, Meaney, MJ, Sloboda, DM. Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J Physiol. 2012; 590, 2167–2180.CrossRefGoogle ScholarPubMed
74. Borwick, C, Rhind, SM, McMillen, SR, Racey, PA. Effect of undernutrition of ewes from the time of mating on fetal ovarian development in mid gestation. Reprod Fert Develop. 1997; 9, 711–715.CrossRefGoogle ScholarPubMed
75. Lea, RG, Andrade, LP, Rae, MT, et al. Effects of maternal undernutrition during early pregnancy on apoptosis regulators in the ovine fetal ovary. Reproduction. 2006; 131, 113–124.CrossRefGoogle ScholarPubMed
76. Pereira, OCM. Endocrine disruptors and hypothalamic sexual differentiation. Annu Rev Biomed Sci. 2003; 5, 87–94.Google Scholar
77. Grigore, D, Ojeda, NB, Alexander, BT. Sex differences in the fetal programming of hypertension. Gend Med. 2008; 5(Suppl A), S121–S132.CrossRefGoogle ScholarPubMed
78. Chadio, S, Balaskas, C, Kotsampasi, B, Papadomichelakis, G, Kalogiannis, D. Gonadal effects of maternal undernutrition in sheep offspring. Proceedings of the 7th International Congress on FARM Animal Endocrinilogy Bern, Switzerland, August 24–26, 2011.Google Scholar
79. Genovese, P, Núñez, ME, Pombo, C, Bielli, A. Undernutrition during foetal and post-natal life affects testicular structure and reduces the number of Sertoli cells in the adult rat. Reprod Domest Anim. 2010; 45, 233–236.CrossRefGoogle ScholarPubMed
80. Niswender, GD, Juengel, JL, Silva, PJ, Rollyson, MK, McIntush, EW. Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev. 2000; 80, 1–29.CrossRefGoogle ScholarPubMed
81. Gunn, RG, Sim, DA, Hunter, EA. Effects of nutrition in utero and in early life on the subsequent lifetime reproductive performance of Scottish Blackface ewes in two management systems. Anim Sci. 1995; 60, 223–230.CrossRefGoogle Scholar
82. Rhind, SM, Elston, DA, Jones, JR, et al. Effects of restriction of growth and development of Brecon Cheviot ewe lambs on subsequent lifetime reproductive performance. Small Rum Res. 1998; 30, 121–126.CrossRefGoogle Scholar
83. Da Silva, P, Aitken, RP, Rhind, SM, Racey, PA, Wallace, JM. Impact of maternal nutrition during pregnancy on pituitary gonadotrophin gene expression and ovarian development in growth-restricted and normally grown late gestation sheep fetuses. Reproduction. 2002; 123, 769–777.CrossRefGoogle ScholarPubMed
84. Ford, SP, Long, NM. Evidence for similar changes in offspring phenotype following either maternal undernutrition or overnutrition: potential impact on fetal epigenetic mechanisms. Reprod Fertil Develop. 2011; 24, 105–111.CrossRefGoogle ScholarPubMed
85. de Bruin, JP, Dorland, M, Bruinse, HW, et al. Fetal growth retardation as a cause of impaired ovarian development. Early Hum Dev. 1998; 51, 39–46.CrossRefGoogle ScholarPubMed
86. de Bruin, JP, Nikkels, PGJ, Bruinse, HW, et al. Morphometry of human ovaries in normal and growth-restricted fetuses. Early Hum Dev. 2001; 60, 179–192.CrossRefGoogle ScholarPubMed
87. Ibanez, L, Potau, N, Enriquez, G, de Zegher, F. Reduced uterine and ovarian size in adolescent girls born small for gestational age. Pediatr Res. 2000; 41, 440–442.Google Scholar
88. Ibanez, L, Potau, N, Ferrer, A, et al. Reduced ovulation rate in adolescent girls born small for gestational age. J Clin Endocr Metab. 2002; 87, 3391–3393.CrossRefGoogle ScholarPubMed
89. Ibanez, L, Valis, C, Cols, M, et al. Hyper secretion of FSH in infant boys and girls born small for gestational age. J Clin Endocr Metab. 2002; 87, 1986–1988.CrossRefGoogle Scholar
90. Ibanez, L, Potau, N, Ferrer, A, et al. Anovulation in eumenorrheic, nonobese adolescent girls born small for gestational age: insulin sensitization induces ovulation, increases lean body mass, and reduces abdominal fat excess, dyslipidemia, and subclinical hyperandrogenism. J Clin Endcr Metab. 2002; 87, 5702–5705.CrossRefGoogle ScholarPubMed
91. Cicognani, A, Alessandroni, R, Pasini, A, et al. Low birth weight for gestational age and subsequent male gonadal function. J Pediatr. 2002; 41, 376–379.CrossRefGoogle Scholar
92. Ibanez, L, Potau, N, de Zegher, F. Ovarian hyporesponsiveness to follicle stimulating hormone in adolescent girls born small for gestational age. J Clin Endocr Metab. 2000; 5, 2624–2626.CrossRefGoogle Scholar
93. Allvin, K, Ankarberg-Lindgren, C, Fors, H, Dahlgren, J. Elevated serum levels of estradiol, dihydrotestosterone, and inhibin B in adult males born small for gestational age. J Clin Endoc Metab. 2008; 3, 1464–1469.CrossRefGoogle Scholar
94. Jensen, RB, Vielwerth, S, Larsen, T, et al. Pituitary-gonadal function in adolescent males born appropriate or small for gestational age with or without intrauterine growth restriction. J Clin Endocrinol Metab. 2007; 92, 1353–1357.CrossRefGoogle ScholarPubMed
95. Main, KM, Jensen, RB, Asklund, C, Høi-Hansen, CE, Skakkebaek, NE. Low birth weight and male reproductive function. Horm Res. 2006; 65(Suppl 3), 116–122.Google ScholarPubMed
96. Lumey, LH, Stein, AD. In utero exposure to famine and subsequent fertility: The Dutch Famine Birth Cohort Study. Am J Public Health. 1997; 7, 1962–1966.CrossRefGoogle Scholar
97. Lumey, LH. Reproductive outcomes in women prenatally exposed to undernutrition: a review of findings from the Dutch famine birth cohort. Proc Nutr Soc. 1998; 7, 129–135.CrossRefGoogle Scholar
98. Meas, T, Efgmoun, S, Levy-Marchal, C, Bouyer, J. Fertility is not altered in young adults born small for gestational age. Hum Reprod. 2010; 25, 2354–2359.CrossRefGoogle Scholar
99. Leidy Sievert, L. Menopause: A Biocultural Perspective, 2006. Rutgers University Press: New Jersey.Google Scholar
100. Tom, SE, Cooper, R, Kuh, D, et al. Fetal environment and early age at natural menopause in a British birth cohort study. Hum Reprod. 2010; 25, 791–798.CrossRefGoogle Scholar
101. Gardner, DS, Ozanne, SE, Sinclair, KD. Effect of the early-life nutritional environment on fecundity and fertility of mammals. Philos T Roy Soc B. 2009; 364, 3419–3427.CrossRefGoogle ScholarPubMed
102. Long, NM, Nijland, MJ, Nathanielsz, PW, Ford, SP. The effect of early to mid-gestational nutrient restriction on female offspring fertility and hypothalamic–pituitary–adrenal axis response to stress. J Anim Sci. 2010; 88, 2029–2037.CrossRefGoogle ScholarPubMed
103. Ramlau-Hansen, CH, Hansen, M, Jensen, CR, et al. Semen quality and reproductive hormones according to birth weight and body mass index in childhood and adult life: two decades of follow-up. Fertil Steril. 2010; 94, 610–618.CrossRefGoogle ScholarPubMed
104. Vanbillemont, G, Lapauw, B, Bogaert, V, et al. Birth weight in relation to sex steroid status and body composition in young healthy male siblings. J Clin Endoc Metab. 2010; 95, 1587–1594.CrossRefGoogle ScholarPubMed
105. Francois, I, De Zegher, F, Spiessens, C, D’ Hooghe, T, Vanderschueren, D. Low birth weight and subsequent male subfertility. Pediat Res. 1997; 42, 899–901.CrossRefGoogle ScholarPubMed
106. Gluckman, PD. Nutrition, glucocorticoids, birth size, and adult disease. Endocrinology. 2001; 142, 1689–1691.CrossRefGoogle ScholarPubMed
107. Singhal, A, Lucas, A. Early origins of cardiovascular disease: is there a unifying hypothesis? Lancet. 2004; 363, 1642–1645.CrossRefGoogle Scholar
108. Cameron, N. Growth patterns in adverse environments. Am J Hum Biol. 2007; 19, 615–621.CrossRefGoogle ScholarPubMed
109. Gluckman, PD, Hanson, MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab. 2004; 15, 183–187.CrossRefGoogle ScholarPubMed
110. Ellison, PT, Jasienska, G. Constraint, pathology, and adaptation: how can we tell them apart? Am J Hum Biol. 2007; 19, 622–630.CrossRefGoogle ScholarPubMed
111. Jonathan, CKW. Flaws in the theory of predictive adaptive responses. Trends Endocr Metab. 2007; 19, 331–337.Google Scholar
112. Jasienska, G, Inger, T, Ellison, PT. Fatness at birth predicts adult susceptibility to ovarian suppression: an empirical test of the Predictive Adaptive Response hypothesis. PNAS. 2006; 103, 12759–12762.CrossRefGoogle ScholarPubMed
113. Kuzawa, CW, Quin, EA. Developmental origins of adult function and health: Evolutionary Hypothesis. Annu Rev Anthropol. 2009; 38, 131–147.CrossRefGoogle Scholar
114. Ellison, PT. Developmental influences on adult ovarian hormonal unction. Am J Hum Biol. 1996; 8, 725–734.3.0.CO;2-S>CrossRefGoogle Scholar
115. Mermillod, P, Dalbiès-Tran, R, Uzbekova, S, et al. Factors affecting oocyte quality. Who is driving the follicle? Reprod Dom Anim. 2008; 43, 393–400.CrossRefGoogle ScholarPubMed
116. Ashworth, J, Toma, LM, Hunter, MG. Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos Trans R Soc Lond B Biol Sci. 2009; 364, 3351–3361.CrossRefGoogle ScholarPubMed
117. Sirard, MA, Richard, F, Blondin, P, Robert, C. Contribution of the oocyte to embryo quality. Theriogenology. 2006; 65, 126–136.CrossRefGoogle ScholarPubMed
118. Fleming, TP, Kwong, WY, Porter, R, et al. The embryo and its future. Biol Reprod. 2004; 71, 1046–1054.CrossRefGoogle ScholarPubMed
119. Sinclair, KD, Kuran, M, Gebbie, FE, Webb, R, McEvoy, TG. Nitrogen metabolism and fertility in cattle: II. Development of oocytes recovered from heifers offered diets differing in their rate of nitrogen release in the rumen. J Anim Sci. 2000; 78, 2670–2680.CrossRefGoogle ScholarPubMed
120. Papadopoulos, S, Lonergan, P, Gath, V, et al. Effect of diet quantity and urea supplementation on oocyte and embryo quality in sheep. Theriogenology. 2001; 55, 1059–1069.CrossRefGoogle ScholarPubMed
121. Borowczyk, E, Caton, JS, Redmer, DA, et al. Effects of plane of nutrition on in vitro fertilization and early embryonic development in sheep. J Anim Sci. 2006; 84, 1593–1599.CrossRefGoogle ScholarPubMed
122. Grazul-Bilska, AT, Borowczyk, E, Bilski, JJ, et al. Overfeeding and underfeeding have detrimental effects on oocyte quality measured by in vitro fertilization and early embryonic development in sheep. Domest Anim Endocrinol. 2012; 43, 289–298.CrossRefGoogle ScholarPubMed
123. Pisani, LF, Antonini, S, Pocar, P, et al. Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction. 2008; 136, 303–312.CrossRefGoogle ScholarPubMed
124. Purcell, SH, Moley, KH. The impact of obesity on egg quality. J Assist Reprod Gen. 2011; 28, 517–524.CrossRefGoogle ScholarPubMed
125. Minge, CE, Bennett, BD, Norman, RJ, Robker, RL. Peroxisome proliferator-activated receptor-γ agonist rosiglitazone reverses the adverse effects of diet-induced obesity on oocyte quality. Endocrinology. 2008; 149, 2646–2656.CrossRefGoogle ScholarPubMed
126. Jungheim, ES, Schoeller, EL, Marquard, KL, et al. Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology. 2010; 151, 4039–4046.CrossRefGoogle ScholarPubMed
127. Velazquez, MA, Hermann, D, Kues, WA, Niemann, H. Increased apoptosis in bovine blastocysts exposed to high levels of IGF1 is not associated with downregulation of the IGF1 receptor. Reproduction. 2011; 141, 91–103.CrossRefGoogle Scholar
128. Igosheva, N, Abramov, AY, Poston, L, et al. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One. 2010; 5, e10074.CrossRefGoogle ScholarPubMed
129. Palmer, NO, Bakos, HW, Fullston, T, Lane, M. Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis. 2012; 2, 253–263.CrossRefGoogle ScholarPubMed
130. O'Reilly, JR, Reynolds, RM. The risk of maternal obesity to the long term health of the offspring. Clin Endocrinol. 2013; 78, 9–16.CrossRefGoogle Scholar
131. Drake, AJ, Reynolds, RM. Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction. 2010; 140, 387–398.CrossRefGoogle ScholarPubMed
132. Alfraradhi, MZ, Ozanne, SE. Developmental programming in response to maternal overnutrition. Front Genet. 2011; 2, 27.Google Scholar
133. Fowden, AL, Li, J, Forhead, AJ. Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance? Proc Nutr Soc. 1998; 57, 113–122.CrossRefGoogle ScholarPubMed
134. Fowden, AL, Giussani, DA, Forhead, AJ. Intrauterine programming of physiological systems: causes and consequences. Physiology. 2006; 21, 29–37.CrossRefGoogle ScholarPubMed
135. Harding, JE, Derraik, JG, Bloomfield, FH. Maternal undernutrition and endocrine development. Expert Rev Endocrinol Metab. 2010; 5, 297–312.CrossRefGoogle ScholarPubMed
136. Seckl, JR. Prenatal glucocorticoids and long-term programming. Eur J Endocrinol. 2004; 151, U49–U62.CrossRefGoogle ScholarPubMed
137. Bloomfield, FH, Oliver, MH, Hawkins, P, et al. Periconceptional undernutrition in sheep accelerates maturation of the fetal hypothalamic–pituitary–adrenal axis in late gestation. Endocrinology. 2004; 145, 4278–4285.CrossRefGoogle ScholarPubMed
138. Gardner, DS, Van Bon, BW, Dandrea, J, et al. Effect of periconceptional undernutrition and gender on hypothalamic–pituitary–adrenal axis function in young adult sheep. J Endocrinol. 2006; 190, 203–212.CrossRefGoogle ScholarPubMed
139. Chadio, SE, Kotsampasi, B, Papadomichelakis, G, et al. Impact of maternal undernutrition on the hypothalamic–pituitary–adrenal axis responsiveness in sheep at different ages postnatal. J Endocrinol. 2007; 192, 495–503.CrossRefGoogle ScholarPubMed
140. Poore, KR, Boullin, JP, Cleal, JK, et al. Sex- and age-specific effects of nutrition in early gestation and early postnatal life on hypothalamo–pituitary–adrenal axis and sympathoadrenal function in adult sheep. J Physiol. 2010; 588, 2219–2237.CrossRefGoogle ScholarPubMed
141. Oliver, MH, Bloomfield, FH, Jaquiery, AL, et al. Periconceptional undernutrition suppresses cortisol response to arginine vasopressin and corticotropinreleasing hormone challenge in adult sheep offspring. J Dev Orig Health Dis. 2012; 3, 52–58.CrossRefGoogle ScholarPubMed
142. Harris, A, Seckl, J. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav. 2011; 59, 279–289.CrossRefGoogle ScholarPubMed
143. Killen, SM, Szabo, M, Strasser, GA, et al. Corticosterone selectively increases follicle stimulating hormone beta subunit messenger ribonucleic acid in primary anterior pituitary cells culture without affecting its half life. Endocrinology. 1996; 137, 3802–3807.CrossRefGoogle Scholar
144. Michael, AE, Pestet, LA, Curtis, P, et al. Direct inhibition of ovarian sterioidogenesis by cortisol and the modulatory role of 11-beta hydroxysteroid dehydrogemase. Clin Endocrinol (Oxf). 1993; 38, 641–644.CrossRefGoogle Scholar
145. Dufourny, L, Skinner, DC. Progesterone receptor, estrogen receptor α, and the type II glucocorticoid receptor are coexpressed in the same neurons of the ovine preoptic area and arcurate nucleus: a trile immunolabelling study. Biol Reprod. 2002; 67, 1605–1612.CrossRefGoogle Scholar
146. Crudo, A, Petropoulos, S, Moisiadis, VG, et al. Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects. Endocrinology. 2012; 153, 3269–3283.CrossRefGoogle ScholarPubMed
147. Sinclair, KD, Lea, RG, Rees, WD. The developmental origins of health and disease: current theories and epigenetic mechanisms. Soc Reprod Fertil Suppl. 2007; 64, 424–443.Google ScholarPubMed
148. Gabory, A, Attig, L, Junien, CL. Developmental programming and epigenetics. Am J Clin Nutr. 2011; 94, 1943S–1952S.CrossRefGoogle ScholarPubMed
149. Burdge, GC, Hanson, MA, Jo, L, Slater-Jefferies, JL, Lillycrop, KA. Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life? Br J Nutr. 2007; 97, 1036–1046.CrossRefGoogle ScholarPubMed
150. Wadhwa, PD, Buss, C, Entringer, S, Swanson, JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2009; 27, 358–368.CrossRefGoogle ScholarPubMed
151. Hochberg, Z, Feil, R, Constancia, M, et al. Child health, developmental plasticity, and epigenetic programming. Endocr Rev. 2011; 32, 159–224.CrossRefGoogle ScholarPubMed
152. Mukhopadhaya, N, Arulkumaran, S. Reproductive outcomes after in-vitro fertilization. Curr Opin Obstet Gynecol. 2007; 19, 13–119.CrossRefGoogle ScholarPubMed
153. Thompson, JG, Kind, KL, Roberts, CT, Robertson, SA, Robinson, JS. Epigenetic risks related to assisted reproductive technologies short- and long-term consequences for the health of children conceived through assisted reproduction technology: more reason for caution? Hum Reprod. 2002; 17, 2783–2786.CrossRefGoogle Scholar
154. Young, LE, Fairburn, HR. Improving the safety of embryo technologies: possible role of genomic imprinting. Theriogenology. 2000; 53, 627–648.CrossRefGoogle ScholarPubMed
155. Fleming, TP, Kwong, WY, Porter, R, et al. The embryo and its future. Biol Reprod. 2004; 71, 1046–1054.CrossRefGoogle ScholarPubMed
156. Doherty, AS, Mann, MR, Tremblay, KD, Bartolomei, MS, Schultz, RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod. 2000; 62, 1526–1535.CrossRefGoogle ScholarPubMed
157. Thompson, SL, Konfortova, G, Gregory, RI, et al. Environmental effects on genomic imprinting in mammals. Toxicol Lett. 2001; 120, 143–150.CrossRefGoogle ScholarPubMed
158. Sinclair, KD, Allegrucci, C, Singh, R, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA. 2007; 104, 19351–19356.CrossRefGoogle ScholarPubMed
159. Lillycrop, KA, Phillips, ES, Jackson, AA, Hanson, MA, Burdge, GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005; 135, 1382–1386.CrossRefGoogle ScholarPubMed
160. Kwong, WY, Miller, DJ, Ursell, E, et al. Imprinted gene expression in the rat embryo–fetal axis is altered in response to periconceptional maternal low protein diet. Reproduction. 2006; 132, 265–277.CrossRefGoogle ScholarPubMed
161. Naimeh, LG, Schutte, BC, Hamilton, WS, Tsalikian, E. Ontogeny of the H19 gene in sheep and effect of maternal fasting on its expression in the fetus. Endocr Res. 2001; 27, 417–431.CrossRefGoogle ScholarPubMed
162. Gonzalez, CG, Garcia, FD, Fernandez, SF, Patterson, AM. Role of 17-beta estradiol and progesterone on glucose homeostasis: effects of food restriction (50%) in pregnant and non-pregnant rats. J Endocrinol Invest. 1997; 20, 397–403.CrossRefGoogle ScholarPubMed
163. Fernandez-Twinn, DS, Ozanne, SE, Ekizoglou, S, et al. The maternal endocrine environment in the low-protein model of intra-uterine growth restriction. Br J Nutr. 2003; 90, 815–822.CrossRefGoogle ScholarPubMed
164. Fowden, AL, Forhead, AJ. Hormones as epigenetic signals in developmental programming. Exp Physiol. 2010; 94, 607–625.CrossRefGoogle Scholar
165. Bermejo-Alvarez, P, Rizos, D, Lonergan, P, Gutierrez-Adan, A. Transcriptional sexual dimorphism during preimplantation embryo development and its consequences for developmental competence and adult health and disease. Reproduction. 2011; 141, 563–570.CrossRefGoogle ScholarPubMed
166. Gabory, A, Attig, L, Junien, C. Sexual dimorphism in environmental epigenetic programming. Mol Cel Endocrinol. 2009; 304, 8–18.CrossRefGoogle ScholarPubMed
167. Foecking, EM, McDevitt, MA, Acosta-Martinez, M, Hortpn, TH, Levine, JE. Neuroendocrine consequences of androgen excess in female rodents. Horm Behav. 2008; 53, 673–692.CrossRefGoogle ScholarPubMed
168. Roseboom, TJ, Watson, ED. The next generation of disease risk: are the effects of prenatal nutrition transmitted across generations Evidence from animal and human studies. Placenta. 2012; 33, e40–e44.CrossRefGoogle ScholarPubMed
169. Anway, MD, Cupp, AS, Uzumcu, M, Skinner, MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005; 308, 1466–1469.CrossRefGoogle ScholarPubMed
170. Gore, AC. Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front Neuroendocrinol. 2008; 29, 358–374.CrossRefGoogle ScholarPubMed
171. Barouki, R, Gluckman, PD, Grandjean, P, Hanson, M, Heindel, JJ. Developmental origins of non-communicable disease: implications for research and public health. Environ Health. 2012; 11, 42.CrossRefGoogle ScholarPubMed
172. Mitchell, M, Fullston, T, Palmer, NO, et al. The effect of paternal obesity in mice on reproductive and metabolic fitness of F1 male offspring. Reprod Fertil Dev. 2010; 22, 21 http://dx.doi.org/10.1071/SRB10Abs1032010.CrossRefGoogle Scholar
173. Fullston, T, Palmer, NO, Owens, JA, et al. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod. 2012; 27, 1391–1400.CrossRefGoogle ScholarPubMed
174. Palmer, NO, Fullston, T, Mitchell, M, Setchell, BP, Lane, M. SIRT6 in mouse spermatogenesis is modulated by diet induced obesity. Reprod Feritil Dev. 2011; 23, 929–939.CrossRefGoogle ScholarPubMed
175. Ohlsson Teague, EMC, Fullston, T, Palmer, NO, et al. Sperm microRNAs are differentially expressed in obese fathers-novel candidate paternal dietary signals offspring. Aust N Z J Obstet Gynaecol. 2011.Google Scholar
176. Clement, TM, Savenkova, MI, Settles, M, Anway, MD, Skinner, MK. Alterations in the developing testis transcriptome following embryonic vinclozolin exposure. Reprod Toxicol. 2010; 30, 353–364.CrossRefGoogle ScholarPubMed
177. Guerrero-Bosagna, CM, Skinner, MK. Epigenetic transgenerational effects of endocrine disruptors on male reproduction. Semin Reprod Med. 2009; 27, 403–408.CrossRefGoogle ScholarPubMed