Embryos, DOHaD and David Barker

Journal of Developmental Origins of Health and Disease

Volumn 6, Issue 5, 2015, Pages 377-383

  Fleming, T P ^a   Velazquez, M A ^a,c   Eckert, J J ^b  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

assisted reproductive treatment (ART); blastocyst; maternal low protein diet; primitive endoderm; trophectoderm

Indexed keywords

ADULT; ANIMAL; CYTOLOGY; EPIGENETICS; FEMALE; HUMAN; MAMMALIAN EMBRYO; MATERNAL NUTRITION; PHYSIOLOGY; PREGNANCY;

ADULT; ANIMALS; EMBRYO, MAMMALIAN; EPIGENOMICS; FEMALE; HUMANS; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PREGNANCY;

EID: 84948381927     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S2040174415001105     Document Type: Review

References (74)

1. Roseboom TJ, Painter RC, van Abeelen AF, Veenendaal MV, de Rooij SR. Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas. 2011; 70, 141-145.
2. Hart R, Norman RJ. The longer-term health outcomes for children born as a result of IVF treatment: Part I-General health outcomes. Hum Reprod Update. 2013; 19, 232-243.
3. Fleming TP, Watkins AJ, Sun C, et al. Do little embryos make big decisions? How maternal dietary protein restriction can permanently change an embryo's potential, affecting adult health. Reprod Fertil Dev. 2015; 27, 684-692.
4. 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.
5. El Hajj N, Haaf T. Epigenetic disturbances in in vitro cultured gametes and embryos: implications for human assisted reproduction. Fertil Steril. 2013; 99, 632-641.
6. Zhang S, Rattanatray L, Morrison JL, et al. Maternal obesity and the early origins of childhood obesity: weighing up the benefits and costs of maternal weight loss in the periconceptional period for the offspring. Exp Diabetes Res. 2011; 2011, 585749.
7. Jungheim ES, Moley KH. Current knowledge of obesity's effects in the pre-and periconceptional periods and avenues for future research. Am J Obstet Gynecol. 2010; 203, 525-530.
8. McMillen IC, MacLaughlin SM, Muhlhausler BS, et al. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic Clin Pharmacol Toxicol. 2008; 102, 82-89.
9. Watkins AJ, Ursell E, Panton R, et al. Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease. Biol Reprod. 2008; 78, 299-306.
10. Watkins AJ, Lucas ES, Torrens C, et al. Maternal low-protein diet during mouse pre-implantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. Br J Nutr. 2010; 103, 1762-1770.
11. Watkins AJ, Lucas ES, Wilkins A, Cagampang FR, Fleming TP. Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age. PLoS One. 2011; 6, e28745.
12. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000; 127, 4195-4202.
13. Watkins AJ, Wilkins A, Cunningham C, et al. Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol. 2008; 586, 2231-2244.
14. Torrens C, Snelling TH, Chau R, et al. Effects of pre-and periconceptional undernutrition on arterial function in adult female sheep are vascular bed dependent. Exp Physiol. 2009; 94, 1024-1033.
15. Todd SE, Oliver MH, Jaquiery AL, Bloomfield FH, Harding JE. Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring. Pediatr Res. 2009; 65(4), 409-413.
16. Hernandez CE, Matthews LR, Oliver MH, Bloomfield FH, Harding JE. Effects of sex, litter size and periconceptional ewe nutrition on offspring behavioural and physiological response to isolation. Physiol Behav. 2010; 101, 588-594.
17. 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.
18. Li Y, Jaddoe VW, Qi L, et al. Exposure to the Chinese famine in early life and the risk of hypertension in adulthood. J Hyperten. 2011; 29(6), 1085-1092.
19. Xu MQ, Sun WS, Liu BX, et al. Prenatal malnutrition and adult schizophrenia: further evidence from the 1959-1961 Chinese famine. Schizophr Bull. 2009; 35, 568-576.
20. Lane M, Zander-Fox DL, Robker RL, McPherson NO. Peri-conception parental obesity, reproductive health, and transgenerational impacts. Trends Endocrinol Metab. 2015; 26, 84-90.
21. Tenenbaum-Gavish K, Hod M. Impact of maternal obesity on fetal health. Fetal Diag Ther. 2013; 34, 1-7.
22. O'Reilly JR, Reynolds RM. The risk of maternal obesity to the long-term health of the offspring. Clin Endocrinol. 2013; 78, 9-16.
23. Ruager-Martin R, Hyde MJ, Modi N. Maternal obesity and infant outcomes. Early Hum Dev. 2010; 86, 715-722.
24. Alfaradhi MZ, Ozanne SE. Developmental programming in response to maternal overnutrition. Front Genet. 2011; 2, 27.
25. Picone O, Laigre P, Fortun-Lamothe L, et al. Hyperlipidic hypercholesterolemic diet in prepubertal rabbits affects gene expression in the embryo, restricts fetal growth and increases offspring susceptibility to obesity. Theriogenology. 2011; 75, 287-299.
26. Dunning KR, Russell DL, Robker RL. Lipids and oocyte developmental competence: the role of fatty acids and beta-oxidation. Reproduction. 2014; 148, R15-27.
27. Nicholas LM, Morrison JL, Rattanatray L, et al. Differential effects of exposure to maternal obesity or maternal weight loss during the periconceptional period in the sheep on insulin signalling molecules in skeletal muscle of the offspring at 4 months of age. PLoS One. 2013; 8, e84594.
28. Sasson IE, Vitins AP, Mainigi MA, Moley KH, Simmons RA. Pre-gestational vs gestational exposure to maternal obesity differentially programs the offspring in mice. Diabetologia. 2015; 58, 615-624.
29. Luzzo KM, Wang Q, Purcell SH, et al. High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS One. 2012; 7, e49217.
30. Turner N, Robker RL. Developmental programming of obesity and insulin resistance: does mitochondrial dysfunction in oocytes play a role? Mol Hum Reprod. 2015; 21, 23-30.
31. 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.
32. Grindler NM, Moley KH. Maternal obesity, infertility and mitochondrial dysfunction: potential mechanisms emerging from mouse model systems. Mol Hum Reprod. 2013; 19, 486-494.
33. Wu LL, Russell DL, Wong SL, et al. Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Development. 2015; 142, 681-691.
34. Ge ZJ, Luo SM, Lin F, et al. DNA methylation in oocytes and liver of female mice and their offspring: effects of high-fat-diet-induced obesity. Environ Health Perspect. 2014; 122, 159-164.
35. Wei Y, Yang CR, Wei YP, et al. Enriched environment-induced maternal weight loss reprograms metabolic gene expression in mouse offspring. J Biol Chem. 2015; 290, 4604-4619.
36. Wei Y, Schatten H, Sun QY. Environmental epigenetic inheritance through gametes and implications for human reproduction. Hum Reprod Update. 2015; 21, 194-208.
37. Leary C, Leese HJ, Sturmey RG. Human embryos from overweight and obese women display phenotypic and metabolic abnormalities. Hum Reprod. 2015; 30, 122-132.
38. Bromfield JJ, Schjenken JE, Chin PY, et al. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci USA. 2014; 111, 2200-2205.
39. McPherson NO, Fullston T, Aitken RJ, Lane M. Paternal obesity, interventions, and mechanistic pathways to impaired health in offspring. Ann Nnutr Metab. 2014; 64, 231-238.
40. Watkins AJ, Sinclair KD. Paternal low protein diet affects adult offspring cardiovascular and metabolic function in mice. Am J Physiol Heart Circ Physiol. 2014; 306, H1444-1452.
41. Nicholas LM, Rattanatray L, Morrison JL, et al. Maternal obesity or weight loss around conception impacts hepatic fatty acid metabolism in the offspring. Obesity (Silver Spring). 2014; 22, 1685-1693.
42. Cram LF, Zapata MI, Toy EC, Baker B, 3rd. Genitourinary infections and their association with preterm labor. Am Fam Physician. 2002; 65, 241-248.
43. Williams CL, Teeling JL, Perry VH, Fleming TP. Mouse maternal systemic inflammation at the zygote stage causes blunted cytokine responsiveness in lipopolysaccharide-challenged adult offspring. BMC Biol. 2011; 9, 49.
44. Brison DR, Roberts SA, Kimber SJ. How should we assess the safety of IVF technologies? Reprod Biomed Online. 2013; 27, 710-721.
45. Fauser BC, Devroey P, Diedrich K, et al. Health outcomes of children born after IVF/ICSI: a review of current expert opinion and literature. Reprod Biomed Online. 2014; 28, 162-182.
46. Lazaraviciute G, Kauser M, Bhattacharya S, Haggarty P. A systematic review and meta-analysis of DNA methylation levels and imprinting disorders in children conceived by IVF/ICSI compared with children conceived spontaneously. Hum Reprod Update. 2014; 20, 840-852.
47. Ceelen M, van Weissenbruch MM, Vermeiden JP, van Leeuwen FE, Delemarre-van de Waal HA. Cardiometabolic differences in children born after in vitro fertilization: follow-up study. J Clin Endocrinol Metab. 2008; 93, 1682-1688.
48. Ceelen M, van Weissenbruch MM, Roos JC, et al. Body composition in children and adolescents born after in vitro fertilization or spontaneous conception. J Clin Endocrinol Metab. 2007; 92, 3417-3423.
49. Ceelen M, van Weissenbruch MM, Prein J, et al. Growth during infancy and early childhood in relation to blood pressure and body fat measures at age 8-18 years of IVF children and spontaneously conceived controls born to subfertile parents. Hum Reprod. 2009; 24, 2788-2795.
50. Sakka SD, Loutradis D, Kanaka-Gantenbein C, et al. Absence of insulin resistance and low-grade inflammation despite early metabolic syndrome manifestations in children born after in vitro fertilization. Fertil Steril. 2010; 94, 1693-1699.
51. Zandstra H, Van Montfoort AP, Dumoulin JC. Does the type of culture medium used influence birthweight of children born after IVF? Hum Reprod. 2015; 30, 530-542.
52. Vergouw CG, Kostelijk EH, Doejaaren E, et al. The influence of the type of embryo culture medium on neonatal birthweight after single embryo transfer in IVF. Hum Reprod. 2012; 27, 2619-2626.
53. Hart R, Norman RJ. The longer-term health outcomes for children born as a result of IVF treatment. Part II-Mental health and development outcomes. Hum Reprod Update. 2013; 19, 244-250.
54. Watkins AJ, Platt D, Papenbrock T, et al. Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure. Proc Natl Acad Sci USA. 2007; 104, 5449-5454.
55. Scott KA, Yamazaki Y, Yamamoto M, et al. Glucose parameters are altered in mouse offspring produced by assisted reproductive technologies and somatic cell nuclear transfer. Biol Reprod. 2010; 83, 220-227.
56. Donjacour A, Liu X, Lin W, Simbulan R, Rinaudo PF. In vitro fertilization affects growth and glucose metabolism in a sex-specific manner in an outbred mouse model. Biol Reprod. 2014; 90, 80.
57. Feuer SK, Donjacour A, Simbulan RK, et al. Sexually dimorphic effect of in vitro fertilization (IVF) on adult mouse fat and liver metabolomes. Endocrinology. 2014; 155, 4554-4567.
58. Ecker DJ, Stein P, Xu Z, et al. Long-term effects of culture of preimplantation mouse embryos on behavior. Proc Natl Acad Sci USA. 2004; 101, 1595-1600.
59. Fernandez-Gonzalez R, Moreira P, Bilbao A, et al. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc Natl Acad Sci USA. 2004; 101, 5880-5885.
60. Strata F, Giritharan G, Sebastiano FD, et al. Behavior and brain gene expression changes in mice exposed to preimplantation and prenatal stress. Reprod Sci. 2015; 22, 23-30.
61. Banrezes B, Sainte-Beuve T, Canon E, et al. Adult body weight is programmed by a redox-regulated and energy-dependent process during the pronuclear stage in mouse. PLoS One. 2011; 6, e29388.
62. Sinclair KD, Young LE, Wilmut I, McEvoy TG. In-utero overgrowth in ruminants following embryo culture: lessons from mice and a warning to men. Hum Reprod. 2000; 15(Suppl. 5), 68-86.
63. Fritz R, Jain C, Armant DR. Cell signaling in trophoblast-uterine communication. Int J Dev Biol. 2014; 58, 261-271.
64. Cantone I, Fisher AG. Epigenetic programming and reprogramming during development. Nat Struct Mol Biol. 2013; 20, 282-289.
65. Eckert JJ, Porter R, Watkins AJ, et al. Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health. PLoS One. 2012; 7, e52791.
66. Lane M, Gardner DK. Differential regulation of mouse embryo development and viability by amino acids. J Reprod Fertil. 1997; 109, 153-164.
67. Kaye PL, Gardner HG. Preimplantation access to maternal insulin and albumin increases fetal growth rate in mice. Hum Reprod. 1999; 14, 3052-3059.
68. Martin PM, Sutherland AE. Exogenous amino acids regulate trophectoderm differentiation in the mouse blastocyst through an mTOR-dependent pathway. Dev Biol. 2001; 240, 182-193.
69. Martin PM, Sutherland AE, Van Winkle LJ. Amino acid transport regulates blastocyst implantation. Biol Reprod. 2003; 69, 1101-1108.
70. Wang X, Proud CG. Nutrient control of TORC1, a cell-cycle regulator. Trends Cell Biol. 2009; 19, 260-267.
71. Sun C, Velazquez MA, Marfy-Smith S, et al. Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition. Development. 2014; 141, 1140-1150.
72. Sun C, Denisenko O, Sheth B, et al. Epigenetic regulation of histone modifications and Gata6 gene expression induced by maternal diet in mouse embryoid bodies in a model of developmental programming. BMC Dev Biol. 2015; 15, 3.
73. Coan PM, Vaughan OR, McCarthy J, et al. Dietary composition programmes placental phenotype in mice. J Physiol. 2011; 589(Pt 14), 3659-3670.
74. Velazquez MA, Sheth B, Marfy-Smith S, Eckert J, Fleming TP Insulin and branched-chain amino acid depletion during mouse in vitro preimplantation embryo development alters postnatal growth and cardiovascular physiology. World Congress of Animal Reproduction 2014, Edinburgh, UK. Reproduction Abstracts. 2014; 1, P096.