Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Oral propylene glycol modifies follicular fluid and gene expression profiles in cumulus–oocyte complexes and embryos in feed-restricted heifers

G. Gamarra A B , C. Ponsart C , S. Lacaze B , F. Nuttinck D H , A. Cordova E , P. Mermillod E , B. Marquant-Le Guienne A , D. Monniaux F , P. Humblot G and A. A. Ponter D H I
+ Author Affiliations
- Author Affiliations

A ALLICE, Département Recherche et Développement, 78350 Jouy en Josas, France.

B AURIVA, 64230 Denguin, France.

C ANSES, Animal Health Laboratory, 94706 Maisons-Alfort, France.

D INRA, UMR 1198 Biologie du Développement et Reproduction, 78350 Jouy-en-Josas, France.

E INRA, UMR 7247 Physiologie de la Reproduction et des Comportements, 37380 Nouzilly, France.

F INRA, UMR 85 Physiologie de la Reproduction et des Comportements, 37380 Nouzilly, France.

G Division of Reproduction, Department of Clinical Sciences, Faculty of Veterinary Medicine and Agricultural Sciences, SLU, PO Box 7054, SE 75007, Uppsala, Sweden.

H Université Paris Est, Ecole Nationale Vétérinaire d’Alfort, UMR 1198 Biologie du Développement et Reproduction, 94704 Maisons-Alfort cedex, France.

I Corresponding author. Email: andrew.ponter@vet-alfort.fr

Reproduction, Fertility and Development 30(3) 417-429 https://doi.org/10.1071/RD17037
Submitted: 2 February 2017  Accepted: 3 July 2017   Published: 21 August 2017

Abstract

Dietary supplementation with propylene glycol (PG) increases in vitro production of high-quality embryos in feed-restricted heifers. The aim of the present study was to evaluate the effects of PG in feed-restricted heifers on follicular fluid insulin and insulin-like growth factor (IGF) 1 concentrations, expression of IGF system genes in oocytes and cumulus cells and the expression of selected genes in blastocysts. Feed-restricted (R) heifers were drenched with water or PG during induced oestrous cycles (400 mL of PG or water/drench, daily drenching at 1600 hours for the first 9 days of the oestrous cycle). Ovum pick-up (OPU) was performed after superovulation to produce in vitro embryos and without superovulation to recover oocytes, cumulus cells and follicular fluid. OPU was also performed in a control group (not feed restricted and no drenching). Follicular fluid IGF1 concentrations were reduced by R, and PG restored IGF1 concentrations to those seen in the control group. In cumulus cells, expression of IGF1, IGF1 receptor (IGF1R) and IGF binding protein 4 (IGFBP4) was decreased in the R group, and fully (IGF1 and IGF1R) or partially (IGFBP4) restored to control levels by PG. Blastocyst perilipin 2 (PLIN2; also known as adipophilin), Bcl-2-associated X protein (BAX), SCL2A1 (facilitated glucose/fructose transporter GLUT1), aquaporin 3 (AQP3), DNA (cytosine-5)-methyltransferase 3A (DNMT3A) and heat shock 70-kDa protein 9 (HSPA9B) expression were decreased in R heifers; PG restored the expression of the last four genes to control levels. In conclusion, these results suggest that, during follicular growth, PG exerts epigenetic regulatory effects on gene expression in blastocyst stage embryos.

Additional keywords: cattle fertility, embryo quality, in vitro embryo production, insulin-like growth factor 1, insulin, superovulation.


References

Alonso, S., Minty, A., Bourlet, Y., and Buckingham, M. (1986). Comparison of three actin-coding sequences in the mouse; evolutionary relationships between the actin genes of warm-blooded vertebrates. J. Mol. Evol. 23, 11–22.
Comparison of three actin-coding sequences in the mouse; evolutionary relationships between the actin genes of warm-blooded vertebrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xhs1aqsLg%3D&md5=8cb3508614bf09fc0bd7f7ba8d9d237aCAS |

Armstrong, D. T. (1993). Recent advances in superovulation in cattle. Theriogenology 39, 7–24.
Recent advances in superovulation in cattle.Crossref | GoogleScholarGoogle Scholar |

Armstrong, D. G., Baxter, G., Gutierrez, C. G., Hogg, C. O., Glazyrin, A. L., Campbell, B. K., Bramley, T. A., and Webb, R. (1998). Insulin-like growth factor-binding protein-2 and -4 messenger ribonucleic acid expression in bovine ovarian follicles: effect of gonadotropins and developmental status. Endocrinology 139, 2146–2154.
Insulin-like growth factor-binding protein-2 and -4 messenger ribonucleic acid expression in bovine ovarian follicles: effect of gonadotropins and developmental status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVKksro%3D&md5=e788e4939d5970633c0f02db67f4f1b5CAS |

Armstrong, D. G., Gutierrez, C. G., Baxter, G., Glazyrin, A. L., Mann, G. E., Woad, K. J., Hogg, C. O., and Webb, R. (2000). Expression of mRNA encoding IGF-I, IGF-II and type 1 IGF receptor in bovine ovarian follicles. J. Endocrinol. 165, 101–113.
Expression of mRNA encoding IGF-I, IGF-II and type 1 IGF receptor in bovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislSjsb4%3D&md5=667d2cd37927c184587f9af61f52c0bcCAS |

Anas, M.-K., Elmileik, A., Maeda, T., and Terada, T. (1998). Effects of epidermal growth factor, insulin like growth factor-1 and insulin on meiotic maturation of bovine denuded oocytes. J. Mamm. Ova Res. 15, 179–184.
Effects of epidermal growth factor, insulin like growth factor-1 and insulin on meiotic maturation of bovine denuded oocytes.Crossref | GoogleScholarGoogle Scholar |

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, 1624–1632.
Effect of dietary energy and protein on bovine follicular dynamics and embryo production in vitro: associations with the ovarian insulin-like growth factor system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFGgsbY%3D&md5=b28285aa490a071beae56c0def386024CAS |

Armstrong, D. G., Baxter, G., Hogg, C. O., and Woad, K. J. (2002a). Insulin-like growth factor (IGF) system in the oocyte and somatic cells of bovine preantral follicles. Reproduction 123, 789–797.
Insulin-like growth factor (IGF) system in the oocyte and somatic cells of bovine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvVCiurg%3D&md5=eebec89d43f770a7a840c1b46e654771CAS |

Armstrong, D. G., Gong, J. G., Gardner, J. O., Baxter, G., Hogg, C. O., and Webb, R. (2002b). Steroidogenesis in bovine granulosa cells: the effect of short-term changes in dietary intake. Reproduction 123, 371–378.
Steroidogenesis in bovine granulosa cells: the effect of short-term changes in dietary intake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Clsrs%3D&md5=c62d5790eff06a1bdf4ba9c61e3db89fCAS |

Balogh, O. G., Fébel, H., Huszenicza, G., Kulcsár, M., Abonyi-Tóth, Z., Endrodi, T., and Gábor, G. (2012). Seasonal fertility differences in synchronised dairy cows: ultrasonic, metabolic and endocrine findings. Acta Vet. Hung. 60, 131–143.
Seasonal fertility differences in synchronised dairy cows: ultrasonic, metabolic and endocrine findings.Crossref | GoogleScholarGoogle Scholar |

Barceló-Fimbres, M., and Seidel, G. E. (2007). Effects of fetal calf serum, phenazine ethosulfate and either glucose or fructose during in vitro culture of bovine embryos on embryonic development after cryopreservation. Mol. Reprod. Dev. 74, 1395–1405.
Effects of fetal calf serum, phenazine ethosulfate and either glucose or fructose during in vitro culture of bovine embryos on embryonic development after cryopreservation.Crossref | GoogleScholarGoogle Scholar |

Bazin, S. (1984). ‘In Grille de notation de l’état d’engraissement des vaches Pie noires.’ (Technipel: Paris.)

Blondin, P., Coenen, K., Guilbault, L. A., and Sirard, M. A. (1997). In vitro production of bovine embryos: developmental competence is acquired before maturation. Theriogenology 47, 1061–1075.
In vitro production of bovine embryos: developmental competence is acquired before maturation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVyjug%3D%3D&md5=905fb3c32dda89a734c76a913137bdb3CAS |

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=46959e79e69ae1a3463877a73c397430CAS |

Bols, P. E. J., Vandenheede, J. M. M., Van Soom, A., and de Kruif, A. (1995). Transvaginal ovum pick-up (OPU) in the cow: a new disposable needle guidance system. Theriogenology 43, 677–687.
Transvaginal ovum pick-up (OPU) in the cow: a new disposable needle guidance system.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVCitA%3D%3D&md5=52f067a51881f873b20dc4a73b77dedeCAS |

Bungartz, L., and Niemann, H. (1994). Assessment of the presence of a dominant follicle and selection of dairy cows suitable for superovulation by a single ultrasound examination. J. Reprod. Fertil. 101, 583–591.
Assessment of the presence of a dominant follicle and selection of dairy cows suitable for superovulation by a single ultrasound examination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2FlsFCjtA%3D%3D&md5=6fdff15f4eb5af4b215b5ea9f0e980b9CAS |

Callesen, H., Løvendahl, P., Bak, A., and Greve, T. (1995). Factors affecting the developmental stage of embryos recovered on Day 7 from superovulated dairy cattle. J. Anim. Sci. 73, 1539–1543.
Factors affecting the developmental stage of embryos recovered on Day 7 from superovulated dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtV2isrw%3D&md5=e37e842d2b7f11f370b4f2e41f757ae5CAS |

Campbell, B. K., Scaramuzzi, R. J., and Webb, R. (1996). Induction and maintenance of oestradiol and immunoreactive inhibin production with FSH by ovine granulosa cells cultured in serum-free media. J. Reprod. Fertil. 106, 7–16.
Induction and maintenance of oestradiol and immunoreactive inhibin production with FSH by ovine granulosa cells cultured in serum-free media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtVCnsw%3D%3D&md5=1994a26aefd7a9dc8ddfe5ec5e687e0fCAS |

Campbell, B. K., Baird, D. T., and Webb, R. (1998). Effects of dose of LH on androgen production and luteinization of ovine theca cells cultured in a serum-free system. J. Reprod. Fertil. 112, 69–77.
Effects of dose of LH on androgen production and luteinization of ovine theca cells cultured in a serum-free system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVKqtrc%3D&md5=0022131904ea4a2d26a6a7aee9b0d6c0CAS |

Corcoran, D., Fair, T., Park, S., Rizos, D., Patel, O. V., Smith, G. W., Coussens, P. M., Ireland, J. J., Boland, M. P., Evans, A. C., and Lonergan, P. (2006). Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo culture bovine embryos. Reproduction 131, 651–660.
Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo culture bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltV2jtr8%3D&md5=c8615c2ec42a54d744ea870ff3ebf9cfCAS |

Cordova, A., Perreau, C., Uzbekova, S., Ponsart, C., Locatelli, Y., and Mermillod, P. (2014). Development rate and gene expression of IVP bovine embryos cocultured with bovine oviduct epithelial cells at early or late stage of preimplantation development. Theriogenology 81, 1163–1173.
Development rate and gene expression of IVP bovine embryos cocultured with bovine oviduct epithelial cells at early or late stage of preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktlWmurc%3D&md5=d13e7d04109503090f3945e0c59b9392CAS |

Corrêa, G. A., Rumpf, R., Mundim, T. C., Franco, M. M., and Dode, M. A. (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim. Reprod. Sci. 104, 132–142.
Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress.Crossref | GoogleScholarGoogle Scholar |

de Oliveira, A. T. D., Lopes, R. F. F., and Rodriguez, J. L. (2005). Gene expression and developmental competence of bovine embryos produced in vitro under varying embryo density conditions. Theriogenology 64, 1559–1572.
Gene expression and developmental competence of bovine embryos produced in vitro under varying embryo density conditions.Crossref | GoogleScholarGoogle Scholar |

Diskin, M. G., Mackey, D. R., Roche, J. F., and Sreenan, J. M. (2003). Effects of nutrition and metabolic status on circulating hormones and ovarian follicle development in cattle. Anim. Reprod. Sci. 78, 345–370.
Effects of nutrition and metabolic status on circulating hormones and ovarian follicle development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksF2gt74%3D&md5=2b0885ebe8893e2629595c5dfcaec759CAS |

Downing, J. A., and Scaramuzzi, R. J. (1991). Nutrient effects on ovulation rate, ovarian function and the secretion of gonadotrophic and metabolic hormones in sheep. J. Reprod. Fertil. Suppl. 43, 209–227.
| 1:CAS:528:DyaK38XktVKks7g%3D&md5=f62ebe5b2eac8701828f0b374ec4de70CAS |

Dupont, J., Scaramuzzi, R., and Reverchon, M. (2014). The effect of nutrition and metabolic status on the development of follicles, oocytes and embryos in ruminants. Animal 8, 1031–1044.
The effect of nutrition and metabolic status on the development of follicles, oocytes and embryos in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvVWktrc%3D&md5=c72abedacd9091ddcb3dbcb3f868ab8aCAS |

Ferlay, A., and Chilliard, Y. (1999). Effects of the infusion of non-selective beta-, and selective beta1- or beta2-adrenergic agonists, on body fat mobilisation in underfed or overfed non-pregnant heifers. Reprod. Nutr. Dev. 39, 409–421.
Effects of the infusion of non-selective beta-, and selective beta1- or beta2-adrenergic agonists, on body fat mobilisation in underfed or overfed non-pregnant heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmsFeksL0%3D&md5=f7fa1df68554bf70e42bd2257b02e496CAS |

Fortune, J. E. (1994). Ovarian follicular growth and development in mammals. Biol. Reprod. 50, 225–232.
Ovarian follicular growth and development in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVeju74%3D&md5=cbc7802c443d0cda603007d3722a211cCAS |

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, 783–794.
Reduction of body-weight gain enhances in vitro embryo production in overfed superovulated dairy heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltV2jt7o%3D&md5=40229c233140a1da12209a0ebab985a0CAS |

Gamarra, G., Ponsart, C., Lacaze, S., Le Guienne, B., Deloche, M.-C., Monniaux, D., and Ponter, A. A. (2014). Short term dietary propylene glycol supplementation affects circulating metabolic hormones, progesterone concentrations and follicular growth in dairy heifers. Livest. Sci. 162, 240–251.
Short term dietary propylene glycol supplementation affects circulating metabolic hormones, progesterone concentrations and follicular growth in dairy heifers.Crossref | GoogleScholarGoogle Scholar |

Gamarra, G., Ponsart, C., Lacaze, S., Le Guienne, B., Humblot, P., Deloche, M.-C., Monniaux, D., and Ponter, A. A. (2015). Dietary propylene glycol and in vitro embryo production after ovum pick-up in heifers with different anti-Müllerian hormone profiles. Reprod. Fertil. Dev. 27, 1249–1261.
Dietary propylene glycol and in vitro embryo production after ovum pick-up in heifers with different anti-Müllerian hormone profiles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1Glu7vL&md5=b4246e2c81c2b4a3f8d3604352430385CAS |

Gong, J. G., Lee, W. J., Garnsworthy, P. C., and Webb, R. (2002). Effect of dietary-induced increases in circulating insulin concentrations during the early postpartum period on reproductive function in dairy cows. Reproduction 123, 419–427.
Effect of dietary-induced increases in circulating insulin concentrations during the early postpartum period on reproductive function in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Cls74%3D&md5=98d64f98d7bf541a4ef3f36dc698240dCAS |

Gosden, R. G., Hunter, R. H., Telfer, E., Torrance, C., and Brown, N. (1988). Physiological factors underlying the formation of ovarian follicular fluid. J. Reprod. Fertil. 82, 813–825.
Physiological factors underlying the formation of ovarian follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3gtVWitg%3D%3D&md5=985f046b8b14c3dfae7fa7234241ae80CAS |

Greer, R. C., Staigmiller, R. B., and Parrish, J. J. (1992). Female traits, ovary and follicle characteristics, and the conditional probability of normal oocyte development after superovulation of beef cows. J. Anim. Sci. 70, 263–272.
Female traits, ovary and follicle characteristics, and the conditional probability of normal oocyte development after superovulation of beef cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383lvFegsA%3D%3D&md5=b44ef8c1104c937874a25834e91f18c7CAS |

Gutiérrez, C. G., Oldham, J., Bramley, T. A., Gong, J. G., Campbell, B. K., and Webb, R. (1997). The recruitment of ovarian follicles is enhanced by increased dietary intake in heifers. J. Anim. Sci. 75, 1876–1884.
The recruitment of ovarian follicles is enhanced by increased dietary intake in heifers.Crossref | GoogleScholarGoogle Scholar |

Hara-Chikuma, M., and Verkman, A. S. (2005). Aquaporin-3 functions as a glycerol transporter in mammalian skin. Biol. Cell 97, 479–486.
Aquaporin-3 functions as a glycerol transporter in mammalian skin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovV2mtbw%3D&md5=e35691e19fdbefa0e6a67cb3fe0cffc9CAS |

Huang, H., He, R., Sun, C., Zhang, Y., Meng, Q., and Ma, Y. (2006). Function of aquaporins in female and male reproductive systems. Hum. Reprod. Update 12, 785–795.
Function of aquaporins in female and male reproductive systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFeisbzL&md5=e7231cf98eee8bcdb1c7634bcb079712CAS |

Jorritsma, R. (2003). Negative energy balance in dairy cows as related to fertility. Ph.D. Thesis, Utrecht University.

Kaneda, M., Okano, M., Hata, K., Sado, T., Tsujimoto, N., Li, E., and Sasaki, H. (2004). Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429, 900–903.
Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVKltL8%3D&md5=066f6238a719e1a3155861a8780c4033CAS |

Keim, A. L., Chi, M. M., and Moley, K. H. (2001). Hyperglycemia-induced apoptotic cell death in the mouse blastocyst is dependent on expression of p53. Mol. Reprod. Dev. 60, 214–224.
Hyperglycemia-induced apoptotic cell death in the mouse blastocyst is dependent on expression of p53.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslSjsr0%3D&md5=2862473de9c986a05f7ebd4acccce9e8CAS |

Landau, S., Braw-Tal, R., Kaim, M., Bor, A., and Bruckental, I. (2000). Preovulatory follicular status and diet affect the insulin and glucose content of follicles in high-yielding dairy cows. Anim. Reprod. Sci. 64, 181–197.
Preovulatory follicular status and diet affect the insulin and glucose content of follicles in high-yielding dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXovFWis7c%3D&md5=3739dc4ae45c8d8d14894798b032fa1dCAS |

Leroy, J. L., Vanholder, T., Delanghe, J. R., Opsomer, G., Van Soom, A., Bols, P. E., Dewulf, J., and de Kruif, A. (2004a). Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum. Theriogenology 62, 1131–1143.
Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1Kmsr8%3D&md5=488693da9278309bebbaa0263e39be06CAS |

Leroy, J. L., Vanholder, T., Delanghe, J. R., Opsomer, G., Van Soom, A., Bols, P. E., and de Kruif, A. (2004b). Metabolite and ionic composition of follicular fluid from different sized follicles and their relationship to serum concentrations in dairy cows. Anim. Reprod. Sci. 80, 201–211.
Metabolite and ionic composition of follicular fluid from different sized follicles and their relationship to serum concentrations in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1ygtL0%3D&md5=a803a1d9ccef431f0f50220f9b0dbea0CAS |

Leroy, J. L. M. R., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, G., 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=91880a8509879cf03ba237493485d320CAS |

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, 623–632.
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.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cnksVeruw%3D%3D&md5=4e5f105ff7ed4bd2aa266f371d02c0cfCAS |

Li, Y., Liu, Q., Chen, Q., Yan, X., and Li, N. (2016). Insulin-like growth factor 1 promotes cumulus cell expansion and nuclear maturation of oocytes via Pi3K/Akt pathway. J. Clin. Exp. Pathol. 9, 11436–11443.

Lonergan, P., Fair, T., Corcoran, D., and Evans, A. C. O. (2006). Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology 65, 137–152.
Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MnjtFSlsw%3D%3D&md5=6ce9f6e860f538a6be33afff3f849749CAS |

Lorenzo, P. L., Illera, M. J., Illera, J. C., and Illera, M. (1994). Enhancement of cumulus expansion and nuclear maturation during bovine oocyte maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor I. J. Reprod. Fertil. 101, 697–701.
Enhancement of cumulus expansion and nuclear maturation during bovine oocyte maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmsVOjurs%3D&md5=469e95cf56bca32c18d587864727be33CAS |

Lorenzo, P. L., Illera, M. J., Illera, J. C., and Illera, M. (1995). Role of EGF, IGF-I, sera and cumulus cells on maturation in vitro of bovine oocytes. Theriogenology 44, 109–118.
Role of EGF, IGF-I, sera and cumulus cells on maturation in vitro of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1Cjt7Y%3D&md5=56689924a02ffba51dae2638319d88e1CAS |

Lucy, M. C. (2000). Regulation of ovarian follicular growth by somatotropin and insulin like growth factors in cattle. J. Dairy Sci. 83, 1635–1647.
Regulation of ovarian follicular growth by somatotropin and insulin like growth factors in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltVGgtbs%3D&md5=7a51fe495702d0764d57bcd59d3b6e9dCAS |

Majerus, V., De Roover, R., Etienne, D., Kaidi, S., Massip, A., Dessy, F., and Donnay, I. (1999). Embryo production by ovum pick up in unstimulated calves before and after puberty. Theriogenology 52, 1169–1179.
Embryo production by ovum pick up in unstimulated calves before and after puberty.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFaksg%3D%3D&md5=34e19e5c707014ec8f220276c782350cCAS |

Marquant-Le Guienne, B. (1998). Petit atlas de l’ovocyte bovin. Elevage Insémin 288, 24–30.

Mermillod, P., and Marchal, R. (1999). La maturation de l’ovocyte de mammifères. Med. Sci. 15, 148–156.

Mollo, M. R., Rumpf, R., Martins, A. C., Carrijo, L. H. D., Saueressig, M. G., and Sartori, R. (2007). Embryo production in superovulated Nelore heifers under low or high feed intake. Acta Sci. Vet. 35, 1241.

Monget, P., Monniaux, D., Pisselet, C., and Durand, P. (1993). Changes in insulin-like growth factor-I (IGF-I), IGF-II and their binding proteins during growth and atresia of ovine ovarian follicles. Endocrinology 132, 1438–1446.
Changes in insulin-like growth factor-I (IGF-I), IGF-II and their binding proteins during growth and atresia of ovine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit1Kmuro%3D&md5=6f1f97860a50e8d69c9bbfb8ec10d50cCAS |

Monget, P., Besnard, N., Huet, C., Pisselet, C., and Monniaux, D. (1996). Insulin-like growth factor-binding proteins and ovarian folliculogenesis. Horm. Res. 45, 211–217.
Insulin-like growth factor-binding proteins and ovarian folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhvFKnu7k%3D&md5=040b5359f27e8f2211271771e494ae4dCAS |

Monget, P., Fabre, S., Mulsant, P., Lecerf, F., Elsen, J. M., Mazerbourg, S., Pisselet, C., and Monniaux, D. (2002). Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals. Domest. Anim. Endocrinol. 23, 139–154.
Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1WktLs%3D&md5=a35bc511e364c7221e659bbd0c868892CAS |

Monniaux, D., and Pisselet, C. (1992). Control of proliferation and differentiation of ovine granulosa cells by insulin-like growth factor-I and follicle-stimulating hormone in vitro. Biol. Reprod. 46, 109–119.
Control of proliferation and differentiation of ovine granulosa cells by insulin-like growth factor-I and follicle-stimulating hormone in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xht1WksLo%3D&md5=0c7f7fc5af54b4363bb4258a5f7743c9CAS |

Nielsen, N. I., and Ingvartsen, K. L. (2004). Propylene glycol for dairy cows: a review of the metabolism of propylene glycol and its effects on physiological parameters, feed intake, milk production and risk of ketosis. Anim. Feed Sci. Technol. 115, 191–213.
Propylene glycol for dairy cows: a review of the metabolism of propylene glycol and its effects on physiological parameters, feed intake, milk production and risk of ketosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvVels78%3D&md5=91398b5eec664d6563c2d97500e0f2cdCAS |

Nuttinck, F., Charpigny, G., Mermillod, P., Loosfelt, H., Meduri, G., Freret, S., Grimard, B., and Heyman, Y. (2004). Expression of components of the insulin-like growth factor system and gonadotropin receptors in bovine cumulus–oocyte complexes during oocyte maturation. Domest. Anim. Endocrinol. 27, 179–195.
Expression of components of the insulin-like growth factor system and gonadotropin receptors in bovine cumulus–oocyte complexes during oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1Wmtrk%3D&md5=32e90b023c57ae95727db157731f074bCAS |

Nuttinck, F., Gall, L., Ruffini, S., Laffont, L., Clement, L., Reinaud, P., Adenot, P., Grimard, B., Charpigny, G., and Marquant-Le Guienne, B. (2011). PTGS2-related PGE2 affects oocyte MAPK phosphorylation and meiosis progression in cattle: late effects on early embryonic development. Biol. Reprod. 84, 1248–1257.
PTGS2-related PGE2 affects oocyte MAPK phosphorylation and meiosis progression in cattle: late effects on early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFemu7s%3D&md5=3f7c92af42c1872123ab98ec5f6fc50dCAS |

Oropeza, A., Wrenzycki, C., Herrmann, D., Hadeler, K.-G., and Niemann, H. (2004). Improvement of the developmental capacity of oocytes from prepubertal cattle by intraovarian insulin-like growth factor-I application. Biol. Reprod. 70, 1634–1643.
Improvement of the developmental capacity of oocytes from prepubertal cattle by intraovarian insulin-like growth factor-I application.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOmtr8%3D&md5=627499a6d5d476d6f0aa524060e97e0bCAS |

Pantaleon, M., Ryan, J. P., Gil, M., and Kaye, P. L. (2001). An unusual subcellular localization of GLUT1 and link with metabolism in oocytes and preimplantation mouse embryos. Biol. Reprod. 64, 1247–1254.
An unusual subcellular localization of GLUT1 and link with metabolism in oocytes and preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1aqsr0%3D&md5=9db9974762e55d9415867d5a155de1c7CAS |

Peynot, N., Duranthon, V., and Khan, D. R. (2015). Gene expression analysis in early embryos through reverse transcription quantitative PCR (RT-qPCR). Methods Mol. Biol. 1222, 181–196.
Gene expression analysis in early embryos through reverse transcription quantitative PCR (RT-qPCR).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVGmtbnI&md5=c98e7ab5b2ad6e7690f3be9943d11940CAS |

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=fc70df59139e52e21fa1c2624e787471CAS |

Rizos, D., Lonergan, P., Boland, M. P., Arroyo-García, R., Pintado, B., de la Fuente, J., and Gutiérrez-Adán, A. (2002). Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocysts quality. Biol. Reprod. 66, 589–595.
Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocysts quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVeitLo%3D&md5=2d67efea798b42b5a3d22757f5ac271aCAS |

Rizos, D., Gutiérrez-Adán, A., Pérez-Garnelo, S., De La Fuente, J., Boland, M. P., and Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68, 236–243.
Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFWj&md5=e26815a79f88578cc9a508423632b5e8CAS |

Sakaguchi, M., Dominko, T., Leibfried-Rutledge, M. L., Nagai, T., and First, N. L. (2000). A combination of EGF and IGF-1 accelerates the progression of meiosis in bovine follicular oocytes and fetal calf serum neutralizes the acceleration effect. Theriogenology 54, 1327–1342.
A combination of EGF and IGF-1 accelerates the progression of meiosis in bovine follicular oocytes and fetal calf serum neutralizes the acceleration effect.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktV2gsQ%3D%3D&md5=f32166dca235a4103614f1d80874dc55CAS |

Sakaguchi, M., Dominko, T., Yamauchi, N., Leibfried-Rutledge, M. L., Nagai, T., and First, N. L. (2002). Possible mechanism for acceleration of meiotic progression of bovine follicular oocytes by growth factors in vitro. Reproduction 123, 135–142.
Possible mechanism for acceleration of meiotic progression of bovine follicular oocytes by growth factors in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtV2gsL0%3D&md5=443ae43928d2b1610babee58855d16baCAS |

Santos, J. E. P., Cerri, R. L. A., and Sartori, R. (2008). Nutritional management of the donor cow. Theriogenology 69, 88–97.
Nutritional management of the donor cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSmu7nE&md5=b97b2597169ae4dc612a04e25d3c1382CAS |

Sastre, D., Nogueira da Costa, N., Alves de Sá, A. L., Dhúllia Braga Conceição, S., Chiaratti, M. R., Adona, P. R., Guemra, S., Vieira Meirelles, F., Damasceno Santos, S., Sena, L., Mitio Ohashi, O., Melo dos Santos, E. J., and dos Santos Miranda, M. S. (2014). Expression of PLIN2 and PLIN3 during oocyte maturation and early embryo development in cattle. Theriogenology 81, 326–331.
Expression of PLIN2 and PLIN3 during oocyte maturation and early embryo development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsleks7nK&md5=944c98f1c42c491c3a1f059c18e5ae36CAS |

Seidel, G. E. (2006). Modifying oocytes and embryos to improve their cryopreservation. Theriogenology 65, 228–235.
Modifying oocytes and embryos to improve their cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Gitr3O&md5=b2d7e3b69e2623dc7046d9a8c1af9c23CAS |

Silva-Santos, K. C., Marinho, L. S. R., Santos, G. M. G., Machado, F. Z., Gonzalez, S. M., Lisboa, L. A., and Seneda, M. M. (2013). Ovarian follicle reserve: emerging concepts and applications. Anim. Reprod. 10, 180–186.

Spicer, L. J., Echternkamp, S. E., Wong, E. A., Hamilton, D. T., and Vernon, R. K. (1995). Serum hormones, follicular fluid steroids, insulin-like growth factors and their binding proteins, and ovarian IGF mRNA in sheep with different ovulation rates. J. Anim. Sci. 73, 1152–1163.
Serum hormones, follicular fluid steroids, insulin-like growth factors and their binding proteins, and ovarian IGF mRNA in sheep with different ovulation rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkvV2gtb0%3D&md5=d1e6e9ac96885e4f81299831aaf96babCAS |

Stefanello, J. R., Barreta, M. H., Porciuncula, P. M., Arruda, J. N., Oliveira, J. F., Oliveira, M. A., and Gonçalves, P. B. (2006). Effect of angiotensin II with follicle cells and insulin-like growth factor-I or insulin on bovine oocyte maturation and embryo development. Theriogenology 66, 2068–2076.
Effect of angiotensin II with follicle cells and insulin-like growth factor-I or insulin on bovine oocyte maturation and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SmsLnI&md5=3bcb9579533c4f63734b4634381bb400CAS |

Sutton, M. L., Gilchrist, R. B., and Thompson, J. G. (2003). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. Update 9, 35–48.
Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVelt7Y%3D&md5=473ece3b9c541a7afa871571d18ed002CAS |

Touzard, E., Reinaud, P., Dubois, O., Guyader-Joly, C., Humblot, P., Ponsart, C., and Charpigny, G. (2013). Specific expression patterns and cell distribution of ancient and modern PAG in bovine placenta during pregnancy. Reproduction 146, 347–362.
Specific expression patterns and cell distribution of ancient and modern PAG in bovine placenta during pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1ygtrzL&md5=c51f6343f43bcefcf3be55b90dc7b7d0CAS |

van den Hurk, R., and Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–1751.
Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitF2js70%3D&md5=897b28fa4955d5155ce9ad9d878fb8c1CAS |

van Knegsel, A. T. M., van den Brand, H., Dijkstra, J., Tamminga, S., and Kemp, B. (2005). Effect of dietary energy source on energy balance, production, metabolic disorders and reproduction in lactating dairy cattle. Reprod. Nutr. Dev. 45, 665–688.
Effect of dietary energy source on energy balance, production, metabolic disorders and reproduction in lactating dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOjsro%3D&md5=9ed64f1923362bbbecbfdda68dc37994CAS |

Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034.1.
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar |

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, E425–E434.
Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1ykur0%3D&md5=cc45b37cd0cefa3443e20966fc5fc124CAS |

Walters, A. H., Pryor, A. W., Bailey, T. L., Pearson, R. E., and Gwazdauskas, F. C. (2002). Parity related changes in bovine follicle and oocyte populations, oocyte quality, and hormones to 90 days postpartum. J. Dairy Sci. 85, 824–832.
Parity related changes in bovine follicle and oocyte populations, oocyte quality, and hormones to 90 days postpartum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjtlemsrg%3D&md5=22a17b21375e186a4cea8a19bcc9967eCAS |

Warzych, E., Cieslak, A., Pawlak, P., Renska, N., Pers-Kamczyc, E., and Lechniak, D. (2011). Maternal nutrition affects the composition of follicular fluid and transcript content in gilt oocytes. Vet. Med. 56, 156–167.
| 1:CAS:528:DC%2BC3MXmtFWit70%3D&md5=9836c2cf1fdc8db0759fb89f857fff28CAS |

Wrenzycki, C., De Sousa, P., Overström, 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, 69–78.
| 1:CAS:528:DC%2BD3cXpsl2nsw%3D%3D&md5=0025798130754507162f927585783da6CAS |

Yang, M. Y., and Rajamahendran, R. (2002). Expression of BCL-2 and BAX proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim. Reprod. Sci. 70, 159–169.
Expression of BCL-2 and BAX proteins in relation to quality of bovine oocytes and embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis1egu7c%3D&md5=8d96aa3241e392c9db2199ed3bd2754bCAS |

Yotov, W. V., and St-Arnaud, R. (1993). Cloning and functional expression analysis of the alpha subunit of mouse ATP synthase. Biochem. Biophys. Res. Commun. 191, 142–148.
Cloning and functional expression analysis of the alpha subunit of mouse ATP synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit12jtbc%3D&md5=ea8d079a88579c70e702e28c046e945eCAS |