Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Acute fasting before conception affects metabolic and endocrine status without impacting follicle and oocyte development and embryo gene expression in the rabbit

R. M. García-García A G , P. G. Rebollar B , M. Arias-Álvarez A , O. G. Sakr B F , P. Bermejo-Álvarez C , G. Brecchia D , A. Gutierrez-Adan C , M. Zerani E , C. Boiti D and P. L. Lorenzo A
+ Author Affiliations
- Author Affiliations

A Dpto. Fisiología (Fisiología Animal), Facultad de Veterinaria, Universidad Complutense de Madrid, Ciudad Universitaria, s/n, Madrid 28040, Spain.

B Dpto. Producción Animal, ETSI Agrónomos, Universidad Politécnica de Madrid, Ciudad Universitaria, s/n, Madrid 28040, Spain.

C Dpto. Produccion Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra de La Coruña, Km 5.9, Madrid 28040, Spain.

D Dipartimento di Scienze Biopatologiche e Igiene delle produzioni animali e alimentari, Laboratorio di Biotecnologie fisiologiche, Sezione di Fisiologia veterinaria, Università di Perugia, Via S. Costanzo 4, I-06100, Perugia, Italy.

E Scuola di Scienze Mediche Veterinarie, Università degli Studi di Camerino, via Circonvallazione 93, I-62024 Matelica, Italy.

F Department of Animal Production, Faculty of Agriculture, Cairo University, C.P. 12613, Giza, Egypt.

G Corresponding author. Email: rosa.garcia@vet.ucm.es

Reproduction, Fertility and Development 23(6) 759-768 https://doi.org/10.1071/RD10298
Submitted: 8 November 2010  Accepted: 1 March 2011   Published: 21 June 2011

Abstract

Food deprivation affects female reproduction. The goal of the present study was to elucidate in the rabbit model the effects of acute energy restriction on ovarian function (follicle development, atresia rate and in vitro oocyte maturation) and embryonic development and gene expression of some candidate genes. Serum metabolic parameters (non-esterified fatty acids (NEFA), triglycerides, glucose, insulin and leptin concentrations) and endocrine markers (oestradiol-17β and progesterone concentrations) were also studied. A control group of nulliparous does fed ad libitum and a 72-h fasted group were used. At the end of the nutritional treatment, the ovaries of half of the animals were retrieved while the other animals were re-fed and artificially inseminated to recover embryos at 84 h after insemination, during the luteal phase. At the end of fasting, increased serum NEFA and decreased leptin concentrations were observed in the fasted group, but no differences appeared in serum steroid concentrations, follicle population and atresia rate or nuclear and cytoplasmic oocyte maturation. In the luteal phase, insulin concentrations increased notably in the fasted group. The number of recovered embryos per female and the speed of embryo development were reduced in the food-deprived group. Acute fasting altered both metabolic and endocrine markers and embryo development, but follicle and oocyte development and embryo gene expression were not affected.

Additional keywords: apoptosis, maternal–embryo interaction.


References

Abecia, J. A., Rhind, S. M., Bramley, T. A., and McMillen, S. R. (1995). Steroid production and LH receptor concentrations of ovarian follicles and corpora lutea and associated rates of ova wastage in ewes given high and low levels of food intake before and after mating. Anim. Sci. 61, 57–62.
Steroid production and LH receptor concentrations of ovarian follicles and corpora lutea and associated rates of ova wastage in ewes given high and low levels of food intake before and after mating.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptV2qsr0%3D&md5=3d58aab4eace43eb14c18e51963af8f1CAS |

Alexander, B. M., Kiyma, Z., McFarland, M., Van Kirk, E. A., Hallford, D. M., Hawkins, D. E., Kane, K. K., and Moss, G. E. (2007). Influence of short-term fasting during the luteal phase of the oestrous cycle on ovarian follicular development during the ensuing proestrus of ewes. Anim. Reprod. Sci. 97, 356–363.
Influence of short-term fasting during the luteal phase of the oestrous cycle on ovarian follicular development during the ensuing proestrus of ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1eqtrfJ&md5=39001e7523bf4fca106c35718f1218d5CAS | 16504426PubMed |

Arias-Álvarez, M., García-García, R. M., Rebollar, P. G., Revuelta, L., Millán, P., and Lorenzo, P. L. (2009). Influence of metabolic status on oocyte quality and follicular characteristics at different postpartum periods in primiparous rabbit does. Theriogenology 72, 612–623.
Influence of metabolic status on oocyte quality and follicular characteristics at different postpartum periods in primiparous rabbit does.Crossref | GoogleScholarGoogle Scholar | 19523677PubMed |

Barham, D., and Trinder, P. (1972). An improved colour reagent for the determination of blood glucose by the oxidase system. Analyst 97, 142–145.
An improved colour reagent for the determination of blood glucose by the oxidase system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XhtlOks7Y%3D&md5=05d805eec3955314f82f98989a85947bCAS | 5037807PubMed |

Bermejo-Álvarez, P., Rizos, D., Rath, D., Lonergan, P., and Gutiérrez-Adan, A. (2008). Epigenetic differences between male and female bovine blastocysts produced in vitro. Physiol. Genomics 32, 264–272.
Epigenetic differences between male and female bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 17986520PubMed |

Bermejo-Álvarez, P., Lonergan, P., Rizos, D., and Gutierrez-Adan, A. (2010). Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis. Reprod. Biomed. Online 20, 341–349.
Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis.Crossref | GoogleScholarGoogle Scholar | 20093090PubMed |

Boland, M. P., Lonergan, P., and O’Callaghan, D. (2001). Effect of nutrition on endocrine parameters, ovarian physiology and oocyte and embryo development. Theriogenology 55, 1323–1340.
Effect of nutrition on endocrine parameters, ovarian physiology and oocyte and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSis70%3D&md5=066dd30aee2f1a7577cdda0c568dc291CAS | 11327687PubMed |

Boletin Oficial del Estado (BOE) (2005). Real Decreto 1201/2005. Sobre protección de los animales utilizados para experimentación y otros fines científicos B.O.E. 252, 34 367–34 391.

Brecchia, G., Bonanno, A., Galeati, G., Federici, C., Maranesi, M., Gobbetti, A., Gerani, M., and Boiti, C. (2006). Hormonal and metabolic adaptation to fasting: effects on the hypothalamic–pituitary–ovarian axis and reproductive performance of rabbit does. Domest. Anim. Endocrinol. 31, 105–122.
Hormonal and metabolic adaptation to fasting: effects on the hypothalamic–pituitary–ovarian axis and reproductive performance of rabbit does.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltlKgt7c%3D&md5=3135139b7ed7e526a128b95c7cb1a5f3CAS | 16219443PubMed |

Catalano, S., Mauro, L., Marsico, S., Giordano, C., Rizza, P., Rago, V., Montanaro, D., Maggiolini, M., Panno, M. L., and Andó, S. (2004). Leptin induces, via ERK1/ERK2 signal, functional activation of oestrogen receptor alpha in MCF-7 cells. J. Biol. Chem. 279, 19 908–19 915.
Leptin induces, via ERK1/ERK2 signal, functional activation of oestrogen receptor alpha in MCF-7 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1Wiu7w%3D&md5=9234f6271dc59b8a493e22a258738fb6CAS |

Chavatte-Palmer, P., Al Gubory, K., Picone, O., and Heyman, Y. (2008). Maternal nutrition: effects on offspring fertility and importance of the periconceptional period on long-term development. Gynecol. Obstet. Fertil. 36, 920–929.
| 1:STN:280:DC%2BD1cnjsVyjtg%3D%3D&md5=74ebaef885443f93cdc35a56756b3061CAS | 18693060PubMed |

Chelikani, P. K., Ambrose, J. D., Keisler, D. H., and Kennelly, J. J. (2004). Effect of short-term fasting on plasma concentrations of leptin and other hormones and metabolites in dairy cattle. Domest. Anim. Endocrinol. 26, 33–48.
Effect of short-term fasting on plasma concentrations of leptin and other hormones and metabolites in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFSgsQ%3D%3D&md5=de11bdc4e0ba0972ab5a13c515b0dea8CAS | 14732451PubMed |

Dallman, M. F., Akana, S. F., Bhatnagar, S., Bell, M. E., Choi, S., Chu, A., Horsley, C., Levin, N., Meijer, O., Soriano, L. R., Strack, A. M., and Viau, V. (1999). Starvation: early signals, sensors and sequelae. Endocrinology 140, 4015–4023.
Starvation: early signals, sensors and sequelae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlslSrsbo%3D&md5=573baad367d735f2347bc2d48552e22dCAS | 10465271PubMed |

da Silva Faria, T., de Bittencourt Brasil, F., Sampaio, F. J., and da Fonte Ramos, C. (2010). Effects of maternal undernutrition during lactation on oestrogen and androgen receptor expressions in rat ovary at puberty. Nutrition 26, 993–999.
Effects of maternal undernutrition during lactation on oestrogen and androgen receptor expressions in rat ovary at puberty.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1eqtLfN&md5=fc08fa87c005d84cb3e5ab2b697f153fCAS | 20097538PubMed |

Duranthon, V. (2009). Rabbit as a pre- and post-implantation developmental model. In ‘Maternal Communication with Gametes and Embryo. Proceeding of the 2nd General Meeting of GEMINI’. Sardinia, Italy, 1–3 October 2009. (Eds A. Fazeli, F. Gandolfi and S. Ledda.) p. 18. (European Co-operation in Science and Technology (COST): Brussels, Belgium.)

Garcia-Garcia, R. M., Arias-Alvarez, M., Rebollar, P. G., Revuelta, L., and Lorenzo, P. L. (2009). Influence of different reproductive rhythms on serum oestradiol, testosterone levels, features of follicular population and atresia rate and oocyte maturation in controlled suckling rabbits. Anim. Reprod. Sci. 114, 423–433.
Influence of different reproductive rhythms on serum oestradiol, testosterone levels, features of follicular population and atresia rate and oocyte maturation in controlled suckling rabbits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosVGhurs%3D&md5=6d3279643b96e657569167899580732bCAS | 19046836PubMed |

Hamilton, T. D., Vizcarra, J. A., Wettemann, R. P., Keefer, B. E., and Spicer, L. J. (1999). Ovarian function in nutritionally induced anoestrous cows: effect of exogenous gonadotrophin-releasing hormone in vivo and effect of insulin and insulin-like growth factor I in vitro. J. Reprod. Fertil. 117, 179–187.
Ovarian function in nutritionally induced anoestrous cows: effect of exogenous gonadotrophin-releasing hormone in vivo and effect of insulin and insulin-like growth factor I in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlaltLg%3D&md5=9011401588be5b3eea1780023256c2d3CAS | 10645259PubMed |

Jorritsma, R., de Groot, M. W., Vos, P. L., Kruip, T. A., Wensing, T., and Noordhuizen, J. P. (2003). Acute fasting in heifers as a model for assessing the relationship between plasma and follicular fluid NEFA concentrations. Theriogenology 60, 151–161.
Acute fasting in heifers as a model for assessing the relationship between plasma and follicular fluid NEFA concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhs1ehs7g%3D&md5=c61f1742c8e581ecce63d683a7182ab9CAS | 12620588PubMed |

Kaji, E., Bornslaeger, E. A., and Schultz, R. M. (1987). Inhibition of mouse oocyte cyclic AMP phosphodiesterase by steroid hormones: a possible mechanism for steroid hormone inhibition of oocyte maturation. J. Exp. Zool. 243, 489–493.
Inhibition of mouse oocyte cyclic AMP phosphodiesterase by steroid hormones: a possible mechanism for steroid hormone inhibition of oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXmt12ntLc%3D&md5=10d20d6c3b3c534f2db4977ffc960a4bCAS | 2824657PubMed |

Karamouti, M., Kollia, P., Karligiotou, E., Kallitsaris, A., Prapas, N., Kollios, G., Seferiadis, K., Vamvakopoulos, N., and Messinis, I. E. (2003). Absence of leptin expression and secretion by human luteinized granulosa cells. J. Mol. Endocrinol. 31, 233–239.
Absence of leptin expression and secretion by human luteinized granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFejur0%3D&md5=10c3047ba43dc76f1496a5e00d6f64e6CAS | 12914539PubMed |

Kasuya, K. (1995). The process of apoptosis in follicular epithelial cells in the rabbit ovary, with special reference to involvement by macrophages. Arch. Histol. Cytol. 58, 257–264.
The process of apoptosis in follicular epithelial cells in the rabbit ovary, with special reference to involvement by macrophages.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28%2FovVCgsQ%3D%3D&md5=3057f512ca4d691ad617c5751bc2fdccCAS | 7576877PubMed |

Keim, A. L., Chi, M. M., and Moley, K. H. (2001). Hyperglycaemia-induced apoptotic cell death in the mouse blastocyst is dependent on expression of p53. Mol. Reprod. Dev. 60, 214–224.
Hyperglycaemia-induced apoptotic cell death in the mouse blastocyst is dependent on expression of p53.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslSjsr0%3D&md5=6e1512bb870c48b6b38ad205d2a3c7c1CAS | 11553921PubMed |

Kendrick, K. W., Bailey, T. L., Garst, A. S., Pryor, A. W., Ahmadzadeh, A., Akers, R. M., Eyestone, W. E., Pearson, R. E., and Gwazdauskas, F. C. (1999). Effects of energy balance of hormones, ovarian activity and recovered oocytes in lactating Holstein cows using transvaginal follicular aspiration. J. Dairy Sci. 82, 1731–1741.
Effects of energy balance of hormones, ovarian activity and recovered oocytes in lactating Holstein cows using transvaginal follicular aspiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsVykur8%3D&md5=ccfc2bc424d35f3e7cbf9b1bdd48fd3fCAS | 10480099PubMed |

Kiyma, Z., Alexander, B. M., Van Kirk, E. A., Murdoch, W. J., Hallford, D. M., and Moss, G. E. (2004). Effects of feed restriction on reproductive and metabolic hormones in ewes. J. Anim. Sci. 82, 2548–2557.
| 1:CAS:528:DC%2BD2cXntlCqtrY%3D&md5=ffc0e7db906c035157267771ba31069aCAS | 15446470PubMed |

Korbonits, M., Blaine, D., Elia, M., and Powell-Tuck, J. (2007). Metabolic and hormonal changes during the re-feeding period of prolonged fasting. Eur. J. Endocrinol. 157, 157–166.
Metabolic and hormonal changes during the re-feeding period of prolonged fasting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXps1Kjt7o%3D&md5=1cf52540d1466e30433ae6ccc783abebCAS | 17656593PubMed |

Kranzfelder, D., Korr, H., Mestwerdt, W., and Maurer-Schulze, B. (1984). Follicle growth in the ovary of the rabbit after ovulation-inducing application of human chorionic gonadotrophin. Cell Tissue Res. 238, 611–620.
Follicle growth in the ovary of the rabbit after ovulation-inducing application of human chorionic gonadotrophin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtVKmt74%3D&md5=58f1ab92e23c6873d54ff8d2219091c7CAS | 6525623PubMed |

Larivière, F., Chiasson, J. L., Schiffrin, A., Taveroff, A., and Hoffer, L. J. (1994). Effects of dietary protein restriction on glucose and insulin metabolism in normal and diabetic humans. Metabolism 43, 462–467.
Effects of dietary protein restriction on glucose and insulin metabolism in normal and diabetic humans.Crossref | GoogleScholarGoogle Scholar | 8159104PubMed |

Leroy, J. L., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., and Van Soom, A. (2005). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130, 485–495.
Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rJ&md5=28b8e4b714ca8128dba0a3e5acb8b0b5CAS | 16183866PubMed |

Leroy, J. L., Vanholder, T., Opsomer, G., Van Soom, A., and de Kruif, A. (2006). The in vitro development of bovine oocytes after maturation in glucose and beta-hydroxybutyrate concentrations associated with negative energy balance in dairy cows. Reprod. Domest. Anim. 41, 119–123.
The in vitro development of bovine oocytes after maturation in glucose and beta-hydroxybutyrate concentrations associated with negative energy balance in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVygsrc%3D&md5=699cb9a2ba68818cda465729830cf5d2CAS | 16519716PubMed |

Leroy, J. L., Van Hoeck, V., Clemente, M., Rizos, D., Gutierrez-Adan, A., Van Soom, A., Uytterhoeven, M., and Bols, P. E. (2010). The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality. Hum. Reprod. 25, 768–778.
The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFeitr8%3D&md5=b0f7e6536db7b75d0e41d7a38ffd1f76CAS | 20007613PubMed |

Manal, A. F., Tony, M. A., and Ezzo, O. H. (2010). Feed restriction of pregnant nulliparous rabbit does: consequences on reproductive performance and maternal behaviour. Anim. Reprod. Sci. 120, 179–186.
Feed restriction of pregnant nulliparous rabbit does: consequences on reproductive performance and maternal behaviour.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3czktVOltQ%3D%3D&md5=c9dc0fedf41a4aba86b3b36100b21c94CAS | 20434279PubMed |

McLaughlin, E. A., and McIver, S. C. (2009). Awakening the oocyte: controlling primordial follicle development. Reproduction 137, 1–11.
Awakening the oocyte: controlling primordial follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVKgsL4%3D&md5=1a3f80d40d994c68816260b879343797CAS | 18827065PubMed |

Muñoz-Gutiérrez, M., Blache, D., Martin, G. B., and Scaramuzzi, R. J. (2002). Folliculogenesis and ovarian expression of mRNA encoding aromatase in anoestrous sheep after 5 days of glucose or glucosamine infusion or supplementary lupin feeding. Reproduction 124, 721–731.
Folliculogenesis and ovarian expression of mRNA encoding aromatase in anoestrous sheep after 5 days of glucose or glucosamine infusion or supplementary lupin feeding.Crossref | GoogleScholarGoogle Scholar | 12417011PubMed |

Navarrete Santos, A., Tonack, S., Kirstein, M., Kietz, S., and Fischer, B. (2004). Two insulin-responsive glucose transporter isoforms and the insulin receptor are developmentally expressed in rabbit preimplantation embryos. Reproduction 128, 503–516.
Two insulin-responsive glucose transporter isoforms and the insulin receptor are developmentally expressed in rabbit preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 15509696PubMed |

Novak, S., Almeida, F. R., Cosgrove, J. R., Dixon, W. T., and Foxcroft, G. R. (2003). Effect of pre- and post-mating nutritional manipulation on plasma progesterone, blastocyst development and the oviductal environment during early pregnancy in gilts. J. Anim. Sci. 81, 772–783.
| 1:CAS:528:DC%2BD3sXit1WhtrY%3D&md5=bba3a559ba9a1615edefe5d883d2015bCAS | 12661658PubMed |

Papadopoulos, S., Lonergan, P., Gath, V., Quinn, K. M., Evans, A. C., O’Callaghan, D., and Boland, M. P. (2001). Effect of diet quantity and urea supplementation on oocyte and embryo quality in sheep. Theriogenology 55, 1059–1069.
Effect of diet quantity and urea supplementation on oocyte and embryo quality in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1Srurw%3D&md5=4912fbcddb218c053930cfa64d357825CAS | 11322234PubMed |

Pereda, N. (2010). Evaluation of bioelectric impedance analysis technique to predict the body composition: use in rabbits under different feeding regimes during the rearing period. PhD Thesis, Polythecnic University of Madrid. [In Spanish]

Pisani, L. F., Antonini, S., Pocar, P., Ferrari, S., Brevini, T. A., Rhind, S. M., and Gandolfi, F. (2008). Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction 136, 303–312.
Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1GmtLzE&md5=bb468a51d1551b3de4a89a7857ab1125CAS | 18515315PubMed |

Rebollar, P. G., Ubilla, E., Alvariño, J. M. R., Illera, J. C., and Silván, G. (1992). Influence of sexual receptivity on plasma 17β-oestradiol and ovulatory response during postpartum period in rabbit does. Rev. Esp. Fisiol. 48, 13–18.
| 1:CAS:528:DyaK3sXkt1Sktrk%3D&md5=b9c8ac6c2e6201b6db63b603159f626aCAS | 1410765PubMed |

Rebollar, P. G., Bonanno, A., Di Grigoli, A., Tornambè, G., and Lorenzo, P. L. (2008). Endocrine and ovarian response after a 2-day controlled suckling and eCG treatment in lactating rabbit does. Anim. Reprod. Sci. 104, 316–328.
Endocrine and ovarian response after a 2-day controlled suckling and eCG treatment in lactating rabbit does.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOmsbc%3D&md5=34c15f0132ff735f1a4d00d47a23efe2CAS | 17428626PubMed |

Rommers, J. M., Meijerhof, R., Noordhuizen, J. P. T. M., and Kemp, B. (2001). Effect of different feeding levels during rearing and age at first insemination on body development, body composition, and puberty characteristics of rabbit does. World Rabbit Sci. 9, 101–108.

SAS (1999–2001). ‘SAS 7. STAT User’s Guide (Release 8.2).’ (SAS Inst. Inc.: Cary, NC, USA.)

Scaramuzzi, R. J., Campbell, B. K., Downing, J. A., Kendall, N. R., Khalid, M., Muñoz-Gutiérrez, M., and Somchit, A. (2006). A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate. Reprod. Nutr. Dev. 46, 339–354.
A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOnsrzF&md5=9155c3712574418876097eba185cbdf6CAS | 16824444PubMed |

Schmittgen, T. D., and Livak, K. J. (2008). Analysing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
Analysing real-time PCR data by the comparative C(T) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVemt7c%3D&md5=326055183ec16e38bb47352e74a2bb28CAS | 18546601PubMed |

Sosa, C., Abecia, J. A., Forcada, F., Viñoles, C., Tasende, C., Valares, J. A., Palacín, I., Martin, G. B., and Meikle, A. (2006). Effect of undernutrition on uterine progesterone and oestrogen receptors and on endocrine profiles during the ovine oestrous cycle. Reprod. Fertil. Dev. 18, 447–458.
Effect of undernutrition on uterine progesterone and oestrogen receptors and on endocrine profiles during the ovine oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtV2huro%3D&md5=a2d87be45a42f60a654861032f57acf4CAS | 16737638PubMed |

Sosa, C., Abecia, J. A., Carriquiry, M., Forcada, F., Martin, G. B., Palacín, I., and Meikle, A. (2009). Early pregnancy alters the metabolic responses to restricted nutrition in sheep. Domest. Anim. Endocrinol. 36, 13–23.
Early pregnancy alters the metabolic responses to restricted nutrition in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVerurrL&md5=03f3d1de70a6cdfd993c311a35024ceeCAS | 18838244PubMed |

Sosa, C., Gonzalez-Bulnes, A., Abecia, J., Forcada, F., and Meikle, A. (2011). Short-term undernutrition affects final development of ovulatory follicles in sheep synchronized for ovulation. Reprod. Domest. Anim. , .
Short-term undernutrition affects final development of ovulatory follicles in sheep synchronized for ovulation.Crossref | GoogleScholarGoogle Scholar |

Tietz, N. W. (1995). ‘Clinical Guide to Laboratory Tests.’ 3rd edn. (Ed. W. B. Saunders.) pp. 518–519. (W. B. Saunders Co.: Philadelphia, USA.)

Tripp, W., Ju, J. C., Hoagland, T. A., Riesen, J. W., Yang, X., and Zinn, S. A. (2000). Influence of somatotropin and nutrition on bovine oocyte retrieval and in vitro development. Theriogenology 53, 1581–1590.
Influence of somatotropin and nutrition on bovine oocyte retrieval and in vitro development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvVOmtbs%3D&md5=7606dbeac48f91b32a231d11e70719bcCAS | 10883845PubMed |

Vazquez, M. I., Forcada, F., Casao, A., Abecia, J., Sosa, C., and Palacín, I. (2010). Undernutrition and exogenous melatonin can affect the in vitro developmental competence of ovine oocytes on a seasonal basis. Reprod. Domest. Anim. 45, 677–684.
| 1:CAS:528:DC%2BC3cXhtVOntbbI&md5=f93aaba0df0bbc5715adf841cd22ca79CAS | 19281597PubMed |

Viñoles, C., Forsberg, M., Martin, G. B., Cajarville, C., Repetto, J., and Meikle, A. (2005). Short-term nutritional supplementation of ewes in low body condition affects follicle development due to an increase in glucose and metabolic hormones. Reproduction 129, 299–309.
Short-term nutritional supplementation of ewes in low body condition affects follicle development due to an increase in glucose and metabolic hormones.Crossref | GoogleScholarGoogle Scholar | 15749957PubMed |

Vizcarra, J. A., Wettemann, R. P., Spitzer, J. C., and Morrison, D. G. (1998). Body condition at parturition and postpartum weight gain influence luteal activity and concentrations of glucose, insulin and non-esterified fatty acids in plasma of primiparous beef cows. J. Anim. Sci. 76, 927–936.
| 1:CAS:528:DyaK1cXis1Ggt7k%3D&md5=93853641365450b428ef9471baed9c92CAS | 9581913PubMed |

Wang, Z. Q., Fung, M. R., Barlow, D. P., and Erwin, F. W. (1994). Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature 372, 464–467.
Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisVGqtrg%3D&md5=b1df3adce65e4e5a226e6f9f7f63560eCAS | 7984240PubMed |

Williams, S. A., Blache, D., Martin, G. B., Foot, R., Blackberry, M. A., and Scaramuzzi, R. J. (2001). Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells. Reproduction 122, 947–956.
Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVWitw%3D%3D&md5=9aca974f05414a5e2168a3ab176f260bCAS | 11732990PubMed |

Yan, J., Zhou, B., Jie, A., Yang, J., Tai, P., Chen, X., Zhang, H., Zhang, M., and Xia, G. (2008). Glucose can reverse the effects of acute fasting on mouse ovulation and oocyte maturation. Reprod. Fertil. Dev. 20, 703–712.
Glucose can reverse the effects of acute fasting on mouse ovulation and oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlCnu74%3D&md5=dddb89ef47d8b3381a163b301cff1b03CAS | 18671918PubMed |

Young, L. E., Fernandes, K., McEvoy, T. G., Butterwith, S. C., Gutierrez, C. G., Carolan, C., Broadbent, P. J., Robinson, J. J., Wilmut, I., and Sinclair, K. D. (2001). Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153–154.
Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFGktL8%3D&md5=2077e1e455edac4e7e3dc16f0fc255adCAS | 11175780PubMed |

Younis, A. I., Brackett, B. G., and Fayrer-Hosken, R. A. (1989). Influence of serum and hormones on bovine oocyte maturation and fertilization in vitro. Gamete Res. 23, 189–201.
Influence of serum and hormones on bovine oocyte maturation and fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXksFSmt7w%3D&md5=68bd01f228c8f52810794e60742979d4CAS | 2499525PubMed |

Zerani, M., Boiti, C., Zampini, D., Brecchia, G., Dall’Aglio, C., Ceccarelli, P., and Gobbetti, A. (2004). Ob receptor in rabbit ovary and leptin in vitro regulation of corpora lutea. J. Endocrinol. 183, 279–288.
Ob receptor in rabbit ovary and leptin in vitro regulation of corpora lutea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVGlsbvP&md5=931fc7fa2a50268f440fe67c85c5ba8dCAS | 15531716PubMed |