Adaptive responses of the embryo to maternal diet and consequences for post-implantation development

Reproduction, Fertility and Development

Volumn 24, Issue 1, 2012, Pages 35-44

  Fleming, Tom P ^a   Lucas, Emma S ^a   Watkins, Adam J ^c   Eckert, Judith J ^b  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PROTEIN;

ABNORMAL BEHAVIOR; ADAPTATION; ADULTHOOD; BLASTOCYST; CHRONIC DISEASE; DIASTOLIC BLOOD PRESSURE; EMBRYO; EMBRYO DEVELOPMENT; FEMALE FERTILITY; FERTILIZATION IN VITRO; FETUS DEVELOPMENT; HUMAN; LIPID DIET; MATERNAL NUTRITION; NIDATION; NONHUMAN; NUTRIENT LIMITATION; OBESITY; OOCYTE MATURATION; PERINATAL PERIOD; PROGENY; PROTEIN RESTRICTION; REVIEW; SHEEP; STEROIDOGENESIS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; FERTILITY; HUMANS; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MATERNAL-FETAL EXCHANGE; MICE; MODELS, ANIMAL; PREGNANCY; SHEEP;

EID: 83255192532     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD11905     Document Type: Review

References (102)

1. Aardema, H., Vos, P. L., Lolicato, F., Roelen, B. A., Knijn, H. M., Vaandrager, A. B., Helms, J. B., and Gadella, B. M.2011). Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol. Reprod. 85(1), 62-69. doi:10.1095/ BIOLREPROD.110.088815
2. Adamiak, S. J., Mackie, K., Watt, R. G., Webb, R., and Sinclair, K. D.2005). Impact of nutrition on oocyte quality: cumulative effects of body composition and diet leading to hyperinsulinemia in cattle. Biol. Reprod. 73(5), 918-926. doi:10.1095/BIOLREPROD.105.041483
3. Andersen, H. S., Gambling, L., Holtrop, G., and McArdle, H. J.2006). Maternal iron deficiency identifies critical windows for growth and cardiovascular development in the rat postimplantation embryo. J. Nutr. 136(5), 1171-1177.
4. Armstrong, D. G., McEvoy, T. G., Baxter, G., Robinson, J. J., Hogg, C. O., Woad, K. J., Webb, R., and Sinclair, K. D.2001). Effect of dietary energy and protein on bovine follicular dynamics and embryo production in vitro: associations with the ovarian insulin-like growth factor system. Biol. Reprod. 64(6), 1624-1632. doi:10.1095/BIOLREPROD64.6.1624
5. Ashworth, C. J., Antipatis, C., and Beattie, L.1999a). Effects of pre- and post-mating nutritional status on hepatic function, progesterone concentration, uterine protein secretion and embryo survival in Meishan pigs. Reprod. Fertil. Dev. 11(1), 67-73. doi:10.1071/RD99007
6. Ashworth, C. J., Beattie, L., Antipatis, C., and Vallet, J. L.1999b). Effects of pre- and post-mating feed intake on blastocyst size, secretory function and glucose metabolism in meishan gilts. Reprod. Fertil. Dev. 11(6), 323-327. doi:10.1071/RD99040
7. Ashworth, C. J., Toma, L. M., and Hunter, M. G.2009). Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364(1534), 3351-3361. doi:10.1098/RSTB. 2009.0184
8. Barker, D. J.2007). The origins of the developmental origins theory. J. Intern. Med. 261(5), 412-417. doi:10.1111/J.1365-2796.2007. 01809.X
9. Basatemur, E.,, and Sutcliffe, A.,2008). Follow-up of children born after ART. Placenta 29(Suppl B), 135-140. doi:10.1016/J.PLACENTA. 2008.08.013
10. Bielinska, M., Narita, N., and Wilson, D. B.1999). Distinct roles for visceral endoderm during embryonic mouse development. Int. J. Dev. Biol. 43(3), 183-205.
11. Bishonga, C., Robinson, J. J., McEvoy, T. G., Findlay, P., Aitken, R. P., and Robertson, I.1996). Excess dietary urea intake in ewes and its effect on ovulation rate and embryo development. Jpn. J. Vet. Res. 44(3), 139-151.
12. Bloomfield, F. H., Oliver, M. H., Hawkins, P., Campbell, M., Phillips, D. J., Gluckman, P. D., Challis, J. R., and Harding, J. E.2003). A periconceptional nutritional origin for noninfectious preterm birth. Science 300(5619), 606. doi:10.1126/SCIENCE.1080803
13. Bloomfield, F.H.,Oliver,M.H.,Hawkins, P.,Holloway,A. C.,Campbell,M., Gluckman, P. D., Harding, J. E., and Challis, J. R.2004). Periconceptional undernutrition in sheep accelerates maturation of the fetal hypothalamic- pituitary-adrenal axis in late gestation. Endocrinology 145(9), 4278-4285. doi:10.1210/EN.2004-0424
14. Borowczyk, E., Caton, J. S., Redmer, D. A., Bilski, J. J., Weigl, R. M., Vonnahme, K. A., Borowicz, P. P., Kirsch, J. D., Kraft, K. C., Reynolds, L. P., and Grazul-Bilska, A. T.2006). Effects of plane of nutrition on in vitro fertilization and early embryonic development in sheep. J. Anim. Sci. 84(6), 1593-1599.
15. Carrell, D. T., Jones, K. P., Peterson, C. M., Aoki, V., Emery, B. R., and Campbell, B. R.2001). Body mass index is inversely related to intrafollicular HCGconcentrations, embryo quality and IVF outcome. Reprod. Biomed. Online 3(2), 109-111. doi:10.1016/S1472-6483(10)61977-3
16. Ceelen, M., van Weissenbruch,M. M., Prein, J., Smit, J. J., Vermeiden, J. P., Spreeuwenberg, M., van Leeuwen, F. E., and Delemarre-van de Waal, H. A.2008a). Cardiometabolic differences in children born after in vitro fertilization: follow-up study. J. Clin. Endocrinol. Metab. 93(5), 1682-1688. doi:10.1210/JC.2007-2432
17. Ceelen, M., van Weissenbruch,M. M., Vermeiden, J. P., van Leeuwen, F. E., and Delemarre-van de Waal, H. A.2008b). Growth and development of children born after in vitro fertilization. Fertil. Steril. 90(5), 1662-1673. doi:10.1016/J.FERTNSTERT.2007.09.005
18. Ceelen, M., van Weissenbruch,M. M., Vermeiden, J. P., van Leeuwen, F. E., and Delemarre-van de Waal, H. A.2009). 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. 24(11), 2788-2795. doi:10.1093/ HUMREP/DEP273
19. Cerri, R. L., Juchem, S. O., Chebel, R. C., Rutigliano, H. M., Bruno, R. G., Galvao, K. N., Thatcher, W. W., and Santos, J. E.2009). Effect of fat source differing in fatty acid profile on metabolic parameters, fertilization, and embryo quality in high-producing dairy cows. J. Dairy Sci. 92(4), 1520-1531. doi:10.3168/JDS.2008-1614
20. Cetin, I., Berti, C., and Calabrese, S.2010). Role of micronutrients in the periconceptional period. Hum. Reprod. Update 16(1), 80-95. doi:10.1093/HUMUPD/DMP025
21. Chagas, L. M., Bass, J. J., Blache, D., Burke, C. R., Kay, J. K., Lindsay, D. R., Lucy, M. C., Martin, G. B., Meier, S., Rhodes, F. M., Roche, J. R., Thatcher, W. W., and Webb, R.2007). Invited review: New perspectives on the roles of nutrition and metabolic priorities in the subfertility of high-producing dairy cows. J. Dairy Sci. 90(9), 4022-4032. doi:10.3168/JDS.2006- 852
22. Chobanian, A. V., Bakris, G. L., Black, H. R., Cushman, W. C., Green, L. A., Izzo, J. L., Jones, D. W., Materson, B. J., Oparil, S., Wright, J. T., Roccella, E. J., and Natl High Blood Pressure Educ, P.2003). Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Hypertension 42(6), 1206-1252. doi:10.1161/01.HYP. 0000107251.49515.C2
23. Cleal, J. K., Poore, K. R., Newman, J. P., Noakes, D. E., Hanson, M. A., and Green, L. R.2007). The effect of maternal undernutrition in early gestation on gestation length and fetal and postnatal growth in sheep. Pediatr. Res. 62(4), 422-427.
24. Connor, K. L., Bloomfield, F. H., Oliver, M. H., Harding, J. E., and Challis, J. R.2009a). Effect of periconceptional undernutrition in sheep on late gestation expression of mRNA and protein from genes involved in fetal adrenal steroidogenesis and placental prostaglandin production. Reprod. Sci. 16(6), 573-583. doi:10.1177/1933719109332827
25. Connor, K. L., Challis, J. R., van Zijl, P., Rumball, C. W., Alix, S., Jaquiery, A. L., Oliver, M. H., Harding, J. E., and Bloomfield, F. H.2009b). Do alterations in placental 11beta-hydroxysteroid dehydrogenase11betaHSD) activities explain differences in fetal hypothalamicpituitary- adrenalHPA) function following periconceptional undernutrition or twinning in sheep? Reprod. Sci. 16(12), 1201-1212. doi:10.1177/1933719109345162
26. Edwards, L. J., and McMillen, I. C.2002a). Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamo-pituitary adrenal axis in sheepduring late gestation. Biol. Reprod. 66(5), 562-1569. doi:10.1095/ BIOLREPROD66.5.1562
27. Edwards, L. J., and McMillen, I. C.2002b). Periconceptional nutrition programs development of the cardiovascular system in the fetal sheep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283(3), R669-R679.
28. Ferguson, E. M., Ashworth, C. J., Edwards, S. A., Hawkins, N., Hepburn, N., and Hunter, M. G.2003). Effect of different nutritional regimens before ovulation on plasma concentrations of metabolic and reproductive hormones and oocyte maturation in gilts. Reproduction 126(1), 61-71. doi:10.1530/REP.0. 1260061
29. Ferguson, E. M., Slevin, J., Edwards, S. A., Hunter, M. G., and Ashworth, C. J.2006). Effect of alterations in the quantity and composition of the pre-mating diet on embryo survival and foetal growth in the pig. Anim. Reprod. Sci. 96(1-2), 89-103. doi:10.1016/J.ANIREPROSCI. 2005.11.007
30. Ferguson, E. M., Slevin, J., Hunter, M. G., Edwards, S. A., and Ashworth, C. J.2007). Beneficial effects of a high fibre diet on oocyte maturity and embryo survival in gilts. Reproduction 133(2), 433-439. doi:10.1530/ REP-06-0018
31. Ferreira, F. A., Gomez, R. G., Joaquim, D. C., Watanabe, Y. F., de Castro, E. P. L. A., Binelli, M., and Rodrigues, P. H.2011). Short-term urea feeding decreases in vitro hatching of bovine blastocysts. Theriogenology 76(2), 312-319.e1. doi:10.1016/J.THERIOGENOLOGY. 2011.02.008
32. Fouladi-Nashta,A. A., Gutierrez, C. G., Gong, J. G., Garnsworthy, P. C., and Webb, R.2007). Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biol. Reprod. 77(1), 9-17. doi:10.1095/BIOLREPROD.106.058578
33. Fouladi-Nashta, A. A., Wonnacott, K. E., Gutierrez, C. G., Gong, J. G., Sinclair, K. D., Garnsworthy, P. C., and Webb, R.2009). Oocyte quality in lactating dairy cows fed on high levels of n-3 and n-6 fatty acids. Reproduction 138(5), 771-781. doi:10.1530/REP-08-0391
34. Freret, S., Grimard, B., Ponter, A. A., Joly, C., Ponsart, C., and Humblot, P.2006). Reduction of body-weight gain enhances in vitro embryo production in overfed superovulated dairy heifers. Reproduction 131(4), 783-794. doi:10.1530/REP.1.00689
35. Gardner, D. S., Pearce, S., Dandrea, J., Walker, R., Ramsay, M. M., Stephenson, T., and Symonds, M. E.2004). Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension 43(6), 1290-1296. doi:10.1161/ 01.HYP.0000126991.67203.7B
36. Garnsworthy, P. C., Fouladi-Nashta, A. A., Mann, G. E., Sinclair, K. D., and Webb, R.2009). Effect of dietary-induced changes in plasma insulin concentrations during the early post partum period on pregnancy rate in dairy cows. Reproduction 137(4), 759-768. doi:10.1530/ REP-08-0488
37. Hernandez, C. E., Harding, J. E., Oliver, M. H., Bloomfield, F. H., Held, S. D., and Matthews, L. R.2009). Effects of litter size, sex and periconceptional ewe nutrition on side preference and cognitive flexibility in the offspring. Behav. Brain Res. 204(1), 82-87. doi:10.1016/J.BBR.2009.05.019
38. Hernandez, C. E., Matthews, L. R., Oliver, M. H., Bloomfield, F. H., and Harding, J. E.2010). Effects of sex, litter size and periconceptional ewe nutrition on offspring behavioural and physiological response to isolation. Physiol. Behav. 101(5), 588-594. doi:10.1016/J.PHYSBEH. 2010.08.020
39. Hughes, J., Kwong, W. Y., Li, D., Salter, A. M., Lea, R. G., and Sinclair, K. D.2011). Effects of omega-3 and -6 polyunsaturated fatty acids on ovine follicular cell steroidogenesis, embryo development and molecular markers of fatty acid metabolism. Reproduction 141(1), 105-118. doi:10.1530/REP-10-0337
40. Igosheva, N., Abramov, A. Y., Poston, L., Eckert, J. J., Fleming, T. P., Duchen, M. R., and McConnell, J.2010). Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS ONE 5(4), e10074. doi:10.1371/JOURNAL.PONE. 0010074
41. Jaquiery, A. L., Oliver, M. H., Bloomfield, F. H., Connor, K. L., Challis, J. R., and Harding, J. E.2006). Fetal exposure to excess glucocorticoid is unlikely to explain the effects of periconceptional undernutrition in sheep. J. Physiol. 572(Pt 1), 109-118.
42. Jaquiery, A. L., Oliver, M. H., Rumball, C. W., Bloomfield, F. H., and Harding, J. E.2009). Undernutrition before mating in ewes impairs the development of insulin resistance during pregnancy. Obstet. Gynecol. 114(4), 869-876. doi:10.1097/AOG.0B013E3181B8FB86
43. Jungheim, E. S., Schoeller, E. L., Marquard, K. L., Louden, E. D., Schaffer, J. E., and Moley, K. H.2010). Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology 151(8), 4039-4046. doi:10.1210/EN.2010-0098
44. Kakar, M. A., Maddocks, S., Lorimer, M. F., Kleemann, D. O., Rudiger, S. R., Hartwich, K. M., and Walker, S. K.2005). The effect of periconception nutrition on embryo quality in the superovulated ewe. Theriogenology 64(5), 1090-1103. doi:10.1016/J.THERIOGENOLOGY. 2004.12.017
45. Kulie, T., Slattengren, A., Redmer, J., Counts, H., Eglash,A., and Schrager, S.2011). Obesity and women's health: an evidence-based review. J. Am. Board Fam. Med. 24(1), 75-85. doi:10.3122/JABFM.2011.01.100076
46. Kumarasamy, V., Mitchell, M. D., Bloomfield, F. H., Oliver, M. H., Campbell, M. E., Challis, J. R., and Harding, J. E.2005). Effects of periconceptional undernutrition on the initiation of parturition in sheep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288(1), R67-R72. doi:10.1152/AJPREGU. 00357.2004
47. Kwong, W. Y., Wild, A. E., Roberts, P., Willis, A. C., and Fleming, T. P.2000). Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 127(19), 4195-4202.
48. Kwong,W. Y.,Miller, D. J.,Ursell, E.,Wild,A.E., Wilkins, A. P.,Osmond, C., Anthony, F. W., and Fleming, T. P.2006). Imprinted gene expression in the rat embryo-fetal axis is altered in response to periconceptional maternal low protein diet. Reproduction 132(2), 265-277. doi:10.1530/ REP.1.01038
49. Kwong, W. Y., Miller, D. J., Wilkins, A. P., Dear, M. S., Wright, J. N., Osmond, C., Zhang, J., and Fleming, T. P.2007). Maternal low protein diet restricted to the preimplantation period induces a gender-specific change on hepatic gene expression in rat fetuses. Mol. Reprod. Dev. 74(1), 48-56. doi:10.1002/MRD.20606
50. Laanpere, M., Altmae, S., Stavreus-Evers, A., Nilsson, T. K., Yngve, A., and Salumets, A.2010). Folate-mediated one-carbon metabolism and its effect on female fertility and pregnancy viability. Nutr. Rev. 68(2), 99-113. doi:10.1111/J.1753-4887.2009.00266.X
51. Leroy, J. L., Van Soom, A., Opsomer, G., Goovaerts, I. G., and Bols, P. E.2008). Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part II. Mechanisms linking nutrition and reduced oocyte and embryo quality in high-yielding dairy cows. Reprod. Domest. Anim. 43(5), 623-632. doi:10.1111/J.1439-0531.2007.00961.X
52. Lintern-Moore, S.1978). A differential effect of protein and calorie deficiency on ovarian follicular growth in the sow. Mech. Ageing Dev. 7(3), 199-207. doi:10.1016/0047-6374(78)90066-0
53. Luo, L. L., Chen, X. C., Fu, Y. C., Xu, J. J., Li, L., Lin, X. H., Xiang, Y. F., and Zhang, X. M.2011). Effects of caloric restriction and a high-fat diet on the ovarian lifespan in rats and the expression of SIRT1 and SIRT6 proteins. Aging Clin. Exp. Res., in press.
54. MacLaughlin, S. M., Walker, S. K., Kleemann, D. O., Tosh, D. N., and McMillen, I. C.2010). Periconceptional undernutrition and being a twin each alter kidney development in the sheep fetus during early gestation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298(3), R692-R699. doi:10.1152/AJPREGU. 00495.2009
55. Manipalviratn, S., DeCherney, A., and Segars, J.2009). Imprinting disorders and assisted reproductive technology. Fertil. Steril. 91(2), 305-315. doi:10.1016/J.FERTNSTERT.2009.01.002
56. McEvoy, T. G., Robinson, J. J., Aitken, R. P., Findlay, P. A., and Robertson, I. S.1997). Dietary excesses of urea influence the viability and metabolism of preimplantation sheep embryos and may affect fetal growth among survivors. Anim. Reprod. Sci. 47(1-2), 71-90. doi:10.1016/S0378-4320(96)01627-2
57. Meza-Herrera, C. A., Ross, T. T., Hallford, D. M., Hawkins, D. E., and Gonzalez-Bulnes, A.2010). High periconceptional protein intake modifies uterine and embryonic relationships increasing early pregnancy losses and embryo growth retardation in sheep. Reprod. Domest. Anim. 45(4), 723-728.
58. Minge, C. E., Bennett, B. D., Norman, R. J., and Robker, R. L.2008). Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone reverses the adverse effects of diet-induced obesity on oocyte quality. Endocrinology 149(5), 2646-2656. doi:10.1210/EN.2007-1570
59. Mitchell, M., Schulz, S. L., Armstrong, D. T., and Lane, M.2009). Metabolic and mitochondrial dysfunction in early mouse embryos following maternal dietary protein intervention. Biol. Reprod. 80(4), 622-630. doi:10.1095/BIOLREPROD.108.072595
60. Muños, G., and Bongiorni-Malave, I.1979). Influence of dietary protein restriction on ovulation, fertilization rates and pre-implantation embryonic development in mice. J. Exp. Zool. 210(2), 253-257. doi:10.1002/ JEZ.1402100208
61. Nolan, R., O'Callaghan, D., Duby, R. T., Lonergan, P., and Boland, M. P.1998). The influence of short-term nutrient changes on follicle growth and embryo production following superovulation in beef heifers. Theriogenology 50(8), 1263-1274. doi:10.1016/S0093-691X(98) 00225-8
62. Ocon, O. M., and Hansen, P. J.2003). Disruption of bovine oocytes and preimplantation embryos by urea and acidic pH. J. Dairy Sci. 86(4), 1194-1200. doi:10.3168/JDS.S0022-0302(03)73703-5
63. Odom, L. N., and Segars, J.2010). Imprinting disorders and assisted reproductive technology. Curr. Opin. Endocrinol. Diabetes Obes. 17(6), 517-522. doi:10.1097/MED.0B013E32834040A3
64. Oliver, M. H., Hawkins, P., and Harding, J. E.2005). Periconceptional undernutrition alters growth trajectory and metabolic and endocrine responses to fasting in late-gestation fetal sheep. Pediatr. Res. 57(4), 591-598. doi:10.1203/01.PDR.0000155942.18096.9C
65. Painter, R. C., de Rooij, S. R., Bossuyt, P. M., Simmers, T. A., Osmond, C., Barker, D. J., Bleker, O. P., and Roseboom, T. J.2006). Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am. J. Clin. Nutr. 84(2), 322-327.
66. Papadopoulos, S., Lonergan, P., Gath, V., Quinn, K. M., Evans, A. C., O'Callaghan, D., and Bolan, M. P.2001). Effect of diet quantity and urea supplementation on oocyte and embryo quality in sheep. Theriogenology 55(5), 1059-1069. doi:10.1016/S0093-691X(01)00466-6
67. Picone, O., Laigre, P., Fortun-Lamothe, L., Archilla, C., Peynot, N., Ponter, A. A., Berthelot, V., Cordier, A. G., Duranthon, V., and Chavatte- Palmer, P.2011). Hyperlipidic hypercholesterolemic diet in prepubertal rabbits affects gene expression in the embryo, restricts fetal growth and increases offspring susceptibility to obesity. Theriogenology 75(2), 287-299. doi:10.1016/J.THERIOGENOLOGY.2010.08.015
68. Prunier, A., and Quesnel, H.2000). Influence of the nutritional status on ovarian development in female pigs. Anim. Reprod. Sci. 60]61, 185-197. doi:10.1016/S0378-4320(00)00093-2
69. Quesnel, H., Pasquier, A., Mounier, A. M., and Prunier, A.2000). Feed restriction in cyclic gilts: gonadotrophin-independent effects on follicular growth. Reprod. Nutr. Dev. 40(4), 405-414. doi:10.1051/ RND:2000108
70. Quesnel, H., Boulot, S., Serriere, S., Venturi, E., and Martinat-Botte, F.2010). Post-insemination level of feeding does not influence embryonic survival and growth in highly prolific gilts. Anim. Reprod. Sci. 120(1-4), 120-124. doi:10.1016/J.ANIREPROSCI.2010.04.006
71. Rattanatray, L., MacLaughlin, S. M., Kleemann, D. O., Walker, S. K., Muhlhausler, B. S., and McMillen, I. C.2010). Impact of maternal periconceptional overnutrition on fat mass and expression of adipogenic and lipogenic genes in visceral and subcutaneous fat depots in the postnatal lamb. Endocrinology 151(11), 5195-5205. doi:10.1210/ EN.2010-0501
72. Rhoads, M. L., Rhoads, R. P., Gilbert, R. O., Toole, R., and Butler, W. R.2006). Detrimental effects of high plasma urea nitrogen levels on viability of embryos from lactating dairy cows. Anim. Reprod. Sci. 91(1-2), 1-10. doi:10.1016/J.ANIREPROSCI.2005.02.009
73. Rizos, D., Clemente, M., Bermejo-Alvarez, P., de La Fuente, J., Lonergan, P., and Gutierrez-Adan, A.2008). Consequences of in vitro culture conditions on embryo development and quality. Reprod. Domest. Anim. 43(Suppl 4), 44-50. doi:10.1111/J.1439-0531.2008.01230.X
74. Robker, R. L.2008). Evidence that obesity alters the quality of oocytes and embryos. Pathophysiology 15(2), 115-121. doi:10.1016/J.PATHOPHYS. 2008.04.004
75. Robker, R. L., Akison, L. K., Bennett, B. D., Thrupp, P. N., Chura, L. R., Russell, D. L., Lane, M., and Norman, R. J.2009). Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J. Clin. Endocrinol. Metab. 94(5), 1533-1540. doi:10.1210/JC.2008-2648
76. Rumball, C. W., Bloomfield, F. H., and Harding, J. E.2008a). Cardiovascular adaptations to pregnancy in sheep and effects of periconceptional undernutrition. Placenta 29(1), 89-94. doi:10.1016/J.PLACENTA. 2007.09.004
77. Rumball, C. W., Harding, J. E., Oliver, M. H., and Bloomfield, F. H.2008b). Effects of twin pregnancy and periconceptional undernutrition on maternal metabolism, fetal growth and glucose-insulin axis function in ovine pregnancy. J. Physiol. 586(5), 1399-1411. doi:10.1113/JPHYSIOL. 2007.144071
78. Rumball, C. W., Oliver, M. H., Thorstensen, E. B., Jaquiery, A. L., Husted, S. M., Harding, J. E., and Bloomfield, F. H.2008c). Effects of twinning and periconceptional undernutrition on late-gestation hypothalamicpituitary- adrenal axis function in ovine pregnancy. Endocrinology 149(3), 1163-1172. doi:10.1210/EN.2007-1306
79. Santos, J. E., Bilby, T. R., Thatcher, W. W., Staples, C. R., and Silvestre, F. T.2008). Long chain fatty acids of diet as factors influencing reproduction in cattle. Reprod. Domest. Anim. 43(Suppl 2), 23-30. doi:10.1111/J.1439-0531.2008.01139.X
80. Sinclair, K. D., Kuran, M., Gebbie, F. E., Webb, R., and McEvoy, T. G.2000). 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. 78(10), 2670-2680.
81. Thangavelu, G., Colazo, M. G., Ambrose, D. J., Oba, M., Okine, E. K., and Dyck, M. K.2007). Diets enriched in unsaturated fatty acids enhance early embryonic development in lactating Holstein cows. Theriogenology 68(7), 949-957. doi:10.1016/J.THERIOGENOLOGY. 2007.07.002
82. Thompson, J. G.2006). The impact of nutrition of the cumulus oocytecomplex and embryo on subsequent development in ruminants. J. Reprod. Dev. 52(1), 169-175. doi:10.1262/JRD.17089
83. Thompson, J. G., Mitchell, M., and Kind, K. L.2007). Embryo culture and long-term consequences. Reprod. Fertil. Dev. 19(1), 43-52. doi:10.1071/RD06129
84. Todd, S. E., Oliver, M. H., Jaquiery, A. L., Bloomfield, F. H., and Harding, J. E.2009). Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring. Pediatr. Res. 65(4), 409-413. doi:10.1203/PDR.0B013E3181975EFA
85. Torrens, C., Snelling, T. H., Chau, R., Shanmuganathan, M., Cleal, J. K., Poore, K. R., Noakes, D. E., Poston, L., Hanson, M. A., and Green, L. R.2009). Effects of pre- and periconceptional undernutrition on arterial function in adult female sheep are vascular bed dependent. Exp. Physiol. 94(9), 1024-1033. doi:10.1113/EXPPHYSIOL.2009.047340
86. Wakefield, S. L., Lane, M., Schulz, S. J., Hebart, M. L., Thompson, J. G., and Mitchell, M.2008). Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. Am. J. Physiol. Endocrinol. Metab. 294(2), E425-E434. doi:10.1152/AJPENDO.00409.2007
87. Watkins, A. J., Platt, D., Papenbrock, T., Wilkins, A., Eckert, J. J., Kwong, W. Y., Osmond, C., Hanson, M., and Fleming, T. P.2007). Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure. Proc. Natl. Acad. Sci. USA 104(13), 5449-5454. doi:10.1073/PNAS. 0610317104
88. Watkins, A. J., Papenbrock, T., and Fleming, T. P.2008a). The preimplantation embryo: handle with care. Semin. Reprod. Med. 26(2), 175-185. doi:10.1055/S-2008-1042956
89. Watkins, A. J., Ursell, E., Panton, R., Papenbrock, T., Hollis, L., Cunningham, C., Wilkins, A., Perry, V. H., Sheth, B., Kwong, W. Y., Eckert, J. J., Wild, A. E., Hanson, M. A., Osmond, C., and Fleming, T. P.2008b). Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease. Biol. Reprod. 78(2), 299-306. doi:10.1095/BIOLREPROD.107.064220
90. Watkins, A. J., Wilkins, A., Cunningham, C., Perry, V. H., Seet, M. J., Osmond, C., Eckert, J. J., Torrens, C., Cagampang, F. R., Cleal, J., Gray, W. P., Hanson, M. A., and Fleming, T. P.2008c). Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J. Physiol. 586(8), 2231-2244. doi:10.1113/JPHYSIOL. 2007.149229
91. Watkins, A. J., Lucas, E. S., Torrens, C., Cleal, J. K., Green, L., Osmond, C., Eckert, J. J., Gray, W. P., Hanson, M. A., and Fleming, T. P.2010). Maternal low-protein diet during mouse pre-implantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. Br. J. Nutr. 103(12), 1762-1770. doi:10.1017/S0007114509993783
92. Wonnacott, K. E., Kwong, W. Y., Hughes, J., Salter, A. M., Lea, R. G., Garnsworthy, P. C., and Sinclair, K. D.2010). Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos. Reproduction 139(1), 57-69. doi:10.1530/REP-09-0219
93. Wrenzycki, C., De Sousa, P., Overstrom, E. W., Duby, R. T., Herrmann, D., Watson, A. J., Niemann, H., O'Callaghan, D., and Boland, M. P.2000). Effects of superovulated heifer diet type and quantity on relative mRNA abundances and pyruvate metabolism in recovered embryos. J. Reprod. Fertil. 118(1), 69-78.
94. Wu, L. L., Dunning, K. R., Yang, X., Russell, D. L., Lane, M., Norman, R. J., and Robker, R. L.2010). High-fat diet causes lipotoxicity responses in cumulus-oocyte complexes and decreased fertilization rates. Endocrinology 151(11), 5438-5445. doi:10.1210/EN.2010-0551
95. Yaakub, H., O'Callaghan, D., and Boland, M. P.1999a). Effect of roughage type and concentrate supplementation on follicle numbers and in vitro fertilisation and development of oocytes recovered from beef heifers. Anim. Reprod. Sci. 55(1), 1-12. doi:10.1016/S0378-4320(99)00002-0
96. Yaakub, H., O'Callaghan, D., and Boland, M. P.1999b). Effect of type and quantity of concentrates on superovulation and embryo yield in beef heifers. Theriogenology 51(7), 1259-1266. doi:10.1016/S0093-691X99)00070-9
97. Yan, J., Zhou, B.,Yang, J.,Tai,P., Chen,X., Zhang, H.,Zhang,M., andXia,G.2008). Glucose can reverse the effects of acute fasting on mouse ovulation and oocyte maturation. Reprod. Fertil. Dev. 20(6), 703-712. doi:10.1071/RD08034
98. Zachut,M.,Dekel, I., Lehrer,H.,Arieli,A.,Arav,A., Livshitz, L.,Yakoby, S., and Moallem, U.2010). Effects of dietary fats differing in n-6:n-3 ratio fed to high-yielding dairy cows on fatty acid composition of ovarian compartments, follicular status, and oocyte quality. J. Dairy Sci. 93(2), 529-545. doi:10.3168/JDS.2009-2167
99. Zeron, Y., Sklan, D., and Arav, A.2002). Effect of polyunsaturated fatty acid supplementation on biophysical parameters and chilling sensitivity of ewe oocytes. Mol. Reprod. Dev. 61(2), 271-278. doi:10.1002/ MRD.1156
100. Zhang, S., Rattanatray, L., MacLaughlin, S. M., Cropley, J. E., Suter, C. M., Molloy, L., Kleemann, D., Walker, S. K., Muhlhausler, B. S., Morrison, J. L., and McMillen, I. C.2010). Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring. FASEB J. 24(8), 2772-2782. doi:10.1096/FJ.09-154294
101. Zhou, D. S., Fang, Z. F., Wu, D., Zhuo, Y., Xu, S. Y., Wang, Y. Z., Zhou, P., and Lin, Y.2010). Dietary energy source and feeding levels during the rearing period affect ovarian follicular development and oocyte maturation in gilts. Theriogenology 74(2), 202-211. doi:10.1016/ J.THERIOGENOLOGY.2010.02.002
102. Zhu, M. J., Du, M., Hess, B. W., Nathanielsz, P. W., and Ford, S. P.2007). Periconceptional nutrient restriction in the ewe alters MAPK/ERK1/2 and PI3K/Akt growth signaling pathways and vascularity in the placentome. Placenta 28(11-12), 1192-1199. doi:10.1016/J.PLACENTA. 2007.05.004