Glucogenic supply increases oocyte developmental competence in sheep
F. Berlinguer A E , A. Gonzalez-Bulnes B , I. Contreras-Solis C , A. Spezzigu A , L. Torres-Rovira A , S. Succu A , S. Naitana A and G. G. Leoni D
+ Author Affiliations
- Author Affiliations
A Department of Animal Biology, University of Sassari, Via Vienna 2, 07100 Sassari, Italy.
B Department of Animal Reproduction, INIA, Avda. Puerta de Hierro s/n 28040-Madrid, Spain.
C Institute of Animal Reproduction, Faculty of Veterinary Science, Central University of Venezuela, University Avenue ‘‘El Limon’’ Maracay, Aragua 2101, Venezuela.
D Department of Physiological, Biochemical and Cellular Science, University of Sassari, Via Vienna 2, 07100 Sassari, Italy.
E Corresponding author. Email: berling@uniss.it
Reproduction, Fertility and Development 24(8) 1055-1062 https://doi.org/10.1071/RD11299
Submitted: 1 December 2011 Accepted: 28 February 2012 Published: 4 April 2012
Abstract
The present study aimed to determine the influence of a glucogenic supply on oocyte developmental competence. Oestrous cycles were synchronised in 22 Sarda ewes by the insertion (Day 0) of one intravaginal progestagen-impregnated sponge that was removed after 6 days. After removal, the ewes were randomly allocated into two experimental groups (treated and control ewes) and, from Day 7 to Day 11, treated ewes received oral administration of a glucogenic mixture, whereas control animals received water. Follicular development was stimulated by FSH administration from Days 8 to 10. Glucose metabolism was assessed from Days 7 to 11, whilst follicle and corpus luteum growth dynamics and functionality were evaluated between Days 6 and 11. At Day 11 ovaries were collected and processed for in vitro embryo production. Glucogenic treatment increased both the plasma levels of glucose, progesterone, oestradiol and the number of 2–3-mm follicles (P < 0.05). Higher fertilisation and blastocyst rates (P < 0.05) were obtained after IVM of oocytes recovered from treated ewes compared with control ones. In conclusion, glucogenic treatment modifies follicle and corpus luteum functionality and improves oocyte quality, as evaluated by in vitro developmental kinetics and blastocyst output.
Additional keywords: blastocyst, corpus luteum, follicle.
References
Berlinguer, F., Gonzalez-Bulnes, A., Succu, S., Leoni, G., Mossa, F., Bebbere, D., Ariznavarreta, C., Tresguerres, J. A. F., Veiga-Lopez, A., and Naitana, S. (2007). Effects of progestagens on follicular growth and oocyte developmental competence in FSH-treated ewes. Domest. Anim. Endocrinol. 32, 303–314.| Effects of progestagens on follicular growth and oocyte developmental competence in FSH-treated ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsVGgsbY%3D&md5=73348278107883628433a75c3866f15cCAS | 16713166PubMed |
Campbell, B. K., Scaramuzzi, R. J., and Webb, R. (1995). Control of antral follicle development and selection in sheep and cattle. J. Reprod. Fertil. Suppl. 49, 335–350.
| 1:CAS:528:DyaK2MXmslWitbs%3D&md5=2cfebcf6853aae318ffd8b9c7af54afaCAS | 7623325PubMed |
Chase, C. C., Del Vecchio, R. P., Smith, S. B., and Randel, R. D. (1992). In vitro metabolism of glucose by bovine reproductive tissues obtained during the oestrous cycle and after calving. J. Anim. Sci. 70, 1498–1508.
Clark, A. R., Stokes, Y. M., Lane, M., and Thompson, J. G. (2006). Mathematical modelling of oxygen concentration in bovine and murine cumulus–oocyte complexes. Reproduction 131, 999–1006.
| Mathematical modelling of oxygen concentration in bovine and murine cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xpt1ehtbg%3D&md5=f3d9771e3c1f37b1e2b57c3a04ad24ebCAS | 16735539PubMed |
Contreras-Solis, I., Diaz, T., Lopez, G., Caigua, A., Lopez-Sebastian, A., and Gonzalez-Bulnes, A. (2008). Systemic and intraovarian effects of corpus luteum on follicular dynamics during oestrous cycle in hair-breed sheep. Anim. Reprod. Sci. 104, 47–55.
| Systemic and intraovarian effects of corpus luteum on follicular dynamics during oestrous cycle in hair-breed sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2FgvFSmsw%3D%3D&md5=03f2860206fa85a40dc0744c9e29895eCAS | 17350189PubMed |
de Loos, F. A. M., Bevers, M. M., Dieleman, S. J., and Kruip, Th. A. M. (1991). Follicular and oocyte maturation in cows treated for superovulation. Theriogenology 35, 537–546.
| Follicular and oocyte maturation in cows treated for superovulation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFKrtA%3D%3D&md5=1b74420740da8f99d916d80204e3ad49CAS |
Downing, J., Joss, J., Connell, P., and Scaramuzzi, R. J. (1995). Ovulation rate and the concentrations of gonadotrophic and metabolic hormones in ewes fed lupin grain. J. Reprod. Fertil. 103, 137–145.
| Ovulation rate and the concentrations of gonadotrophic and metabolic hormones in ewes fed lupin grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXksVGht78%3D&md5=e9fa8cd52029183d510ba13e307878daCAS | 7707290PubMed |
Driancourt, M. A. (2001). Regulation of ovarian follicular dynamics in farm animals. Implications for manipulation of reproduction. Theriogenology 55, 1211–1239.
| Regulation of ovarian follicular dynamics in farm animals. Implications for manipulation of reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSisr8%3D&md5=a53fbd14759ece292371455f79c64d30CAS | 11327681PubMed |
Gong, J. G. (2002). Influence of metabolic hormones and nutrition on ovarian follicle development in cattle: practical implications. Reprod. Domest. Anim. 23, 229–241.
| 1:CAS:528:DC%2BD38Xls1Wktbw%3D&md5=0f1abb1d3301104526cbd7af296479fdCAS |
Gonzalez-Bulnes, A., Santiago-Moreno, J., Garcia-Lopez, M., Gomez-Brunet, A., and Lopez-Sebastian, A. (1994). Observacion del ovario en la oveja y eficacia en la deteccion de folıculos y cuerpos luteos mediante ecografıa transrectal. Investigaciòn Agricola 10, 319–329.
Gonzalez-Bulnes, A., Garcia-Garcia, R. M., Santiago-Moreno, J., Lopez-Sebastian, A., and Cocero, M. J. (2002). Effects of follicular status on superovulatory response in ewes is influenced by the presence of corpora lutea at first FSH dose. Theriogenology 58, 1607–1614.
| Effects of follicular status on superovulatory response in ewes is influenced by the presence of corpora lutea at first FSH dose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xms1yntrk%3D&md5=565467bf16f0f0903923387bea068900CAS | 12374130PubMed |
González-Bulnes, A., García-García, R. M., Castellanos, V., Santiago-Moreno, J., Ariznavarreta, C., Domínguez, V., López-Sebastián, A., Tresguerres, J. A. F., and Cocero, M. J. (2003). Influence of maternal environment on the number of transferable embryos obtained in response to superovulatory FSH treatments in ewes. Reprod. Nutr. Dev. 43, 17–28.
| Influence of maternal environment on the number of transferable embryos obtained in response to superovulatory FSH treatments in ewes.Crossref | GoogleScholarGoogle Scholar | 12785447PubMed |
Gonzalez-Bulnes, A., Berlinguer, F., Cocero, M. J., Garcia-Garcia, R. M., Leoni, G., Naitana, S., Rosati, I., Succu, S., and Veiga-Lopez, A. (2005). Induction of the presence of corpus luteum during superovulatory treatments enhances in vivo and in vitro blastocysts output in sheep. Theriogenology 64, 1392–1403.
| Induction of the presence of corpus luteum during superovulatory treatments enhances in vivo and in vitro blastocysts output in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslyjtrs%3D&md5=ada0ceb4d248a0c27aef81970f2325fdCAS | 16139615PubMed |
Hinch, G., and Roelofs, J. (1986). Lupin feeding and insulin infusion during the late luteal phase can increase ovulation rate in sheep. Proceedings of the Australian Society for Reprod. Biol. 18, 43.
Landau, S., Bor, A., Leibovich, H., Zoref, Z., Nistan, Z., and Madar, Z. (1995). The effect of ruminal starch degradability in the diet of Booroola crossbred ewes on induced ovulation rate and prolificacy. Anim. Reprod. Sci. 38, 97–108.
| The effect of ruminal starch degradability in the diet of Booroola crossbred ewes on induced ovulation rate and prolificacy.Crossref | GoogleScholarGoogle Scholar |
Landau, S., Houghton, J. A., Mawhinney, J. R., and Inskeep, E. K. (1996). Protein sources affect follicular dynamics in ewes near the onset of the breeding season. Reprod. Fertil. Dev. 8, 1021–1028.
| Protein sources affect follicular dynamics in ewes near the onset of the breeding season.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtlGkurk%3D&md5=3bad6a18fa216d4b40b1be7b73469c0cCAS | 8896038PubMed |
Leoni, G. G., Succu, S., Berlinguer, F., Rosati, I., Bebbere, D., Bogliolo, L., Ledda, S., and Naitana, S. (2006). Delay on the in vitro kinetic development of prepubertal ovine embryos. Anim. Reprod. Sci. 92, 373–383.
| Delay on the in vitro kinetic development of prepubertal ovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD287ot1entQ%3D%3D&md5=3446f697b95da4d32942e4a036b51377CAS | 16054784PubMed |
Letelier, C., Gonzalez-Bulnes, A., Herve, M., Correa, J., and Pulido, R. (2008a). Enhancement of ovulatory follicle development in maiden sheep by short-term supplementation with steam-flaked corn. Reprod. Domest. Anim. 43, 222–227.
| Enhancement of ovulatory follicle development in maiden sheep by short-term supplementation with steam-flaked corn.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c7msVektw%3D%3D&md5=75d1bb7cdefbe58bba06f1a01e829d9eCAS | 18067536PubMed |
Letelier, C., Mallo, F., Encinas, T., Ros, J. M., and Gonzalez-Bulnes, A. (2008b). Glucogenic supply increases ovulation rate by modifying follicle recruitment and subsequent development of preovulatory follicles without effects on ghrelin secretion. Reproduction 136, 65–72.
| Glucogenic supply increases ovulation rate by modifying follicle recruitment and subsequent development of preovulatory follicles without effects on ghrelin secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVSgu7c%3D&md5=beb4cda352839e89d5d2ee41e19f29dbCAS | 18390923PubMed |
Martin, G. B., Rodger, J., and Blache, D. (2004). Nutritional and environmental effects on reproduction in small ruminants. Reprod. Fertil. Dev. 16, 491–501.
| Nutritional and environmental effects on reproduction in small ruminants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cvht1WntA%3D%3D&md5=83cc6243975295635333ffae10c124a0CAS | 15315748PubMed |
Muñoz-Gutierrez, 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 |
Muñoz-Gutierrez, M., Blache, D., Martin, G. B., and Scaramuzzi, R. J. (2004). Ovarian follicular expression of mRNA encoding the type I insulin-like growth factor receptor (IGF-IR) and insulin-like growth factor-binding protein 2 (IGFBP2) in anoestrus sheep after 5 days of glucose or glucosamine or supplementary feeding with lupin grain. Reproduction 128, 1–11.
Nishimoto, H., Matsutani, R., Yamamoto, S., Takahashi, T., Hayashi, K. G., Miyamoto, A., Hamano, S., and Tetsuka, M. (2006). Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum. J. Endocrinol. 188, 111–119.
| Gene expression of glucose transporter (GLUT) 1, 3 and 4 in bovine follicle and corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCisL8%3D&md5=2f485225dce7659cb517b2d5b4a6b451CAS | 16394180PubMed |
Oussaid, B., Mariana, J. C., Poulin, N., Fontaine, J., Lonergan, P., Beckers, J. F., and Cognie, Y. (1999). Reduction of the developmental competence of sheep oocytes by inhibition of LH pulses during the follicular phase with a GnRH antagonist. J. Reprod. Fertil. 117, 71–77.
| Reduction of the developmental competence of sheep oocytes by inhibition of LH pulses during the follicular phase with a GnRH antagonist.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlalt7o%3D&md5=96ff6085690b5352173b5a7ce5681063CAS | 10645247PubMed |
Pearse, B. H., Mcmeniman, N. P., and Gardner, I. A. (1994). Influence of body condition on ovulatory response to lupin (Lupinus angustifolius) supplementation of sheep. Small Rumin. Res. 13, 27–32.
| Influence of body condition on ovulatory response to lupin (Lupinus angustifolius) supplementation of sheep.Crossref | GoogleScholarGoogle Scholar |
Robinson, J. J., Ashworth, C. J., Rooke, J. A., Mitchell, L. M., and McEvoy, T. G. (2006). Nutrition and fertility in ruminant livestock. Anim. Feed Sci. Technol. 126, 259–276.
| Nutrition and fertility in ruminant livestock.Crossref | GoogleScholarGoogle Scholar |
Rodríguez-Iglesias, R. M., Ciccioli, N. H., Irazoqui, H., and Giglioli, C. (1996). Ovulation rate in ewes after single oral glucogenic dosage during a ram-induced follicular phase. Anim. Reprod. Sci. 44, 211–221.
| Ovulation rate in ewes after single oral glucogenic dosage during a ram-induced follicular phase.Crossref | GoogleScholarGoogle Scholar |
Romeu, A., Molina, I., Tresguerres, J. A., Pla, M., and Peinado, J. A. (1995). Effect of recombinant human luteinising hormone vs human chorionic gonadotrophin: effects on ovulation, embryo quality and transport, steroid balance and implantation in rabbits. Hum. Reprod. 10, 1290–1296.
| 1:CAS:528:DyaK2MXnt1Omsb0%3D&md5=aa927ce7459f1bc1036841b34b2eaac9CAS | 7657782PubMed |
Rowe, J. B., and Ferguson, J. (1986). Lupin grain as a supplement for sheep grazing cereal stubble. Proceedings of the Australian Society of Animal Production 16, 343–346.
Rubianes, E., Ungerfeld, R., Viñoles, C., Rivero, A., and Adams, G. P. (1997). Ovarian response to gonadotrophin treatment initiated relative to wave emergence in ultrasonographically monitored ewes. Theriogenology 47, 1479–1488.
| Ovarian response to gonadotrophin treatment initiated relative to wave emergence in ultrasonographically monitored ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjvVyjurg%3D&md5=f915640a7b4e5dd598f0979923d6a5eeCAS | 16728092PubMed |
Rubio, J. M., Hallford, D. M., and Hawkins, D. E. (1997). Effect of glucose administration during the oestrous cycle on serum hormone profiles, mRNA for steroidogenic enzymes and breeding performance of ewes. J. Anim. Sci. 75, 775–780.
| 1:CAS:528:DyaK2sXitVeitbo%3D&md5=3a94674223bae202fc97568f0f6cc002CAS | 9078496PubMed |
Scaramuzzi, R., Campbell, B., Downing, J., Kendall, N., Khalid, M., Muñoz-Gutierrez, 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=9ca7c8bc7fecdf25b230c385e7e4d876CAS | 16824444PubMed |
Smith, A., and Stewart, R. (1990). Effects of nutrition on the ovulation rate of ewes. In ‘Reproductive Physiology of Merino Sheep: Concepts and Consequences’. (Eds C. M. Oldham, G. B. Martin, I. W. Martin and I. Purvis.) pp. 85–101. (School of Agriculture, University of Western Australia: Perth.)
Stewart, R., and Oldham, C. (1986). Feeding lupins to ewes for four days during the luteal phase can increase ovulation rate. Proceedings of the Australian Society of Animal Production 16, 367–370.
Stokes, Y. M., Clark, A. R., and Thompson, J. G. (2008). Mathematical modelling of glucose supply toward successful in vitro maturation of mammalian oocytes. Tissue Eng. Part A 14, 1539–1547.
| Mathematical modelling of glucose supply toward successful in vitro maturation of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWlt7jM&md5=655345e21fc5e905ec641a4787b5ca7fCAS | 18665760PubMed |
Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2005). Effect of hexoses and gonadotrophin supplementation on bovine oocyte nuclear maturation during in vitro maturation in a synthetic follicle fluid medium. Reprod. Fertil. Dev. 17, 407–415.
| Effect of hexoses and gonadotrophin supplementation on bovine oocyte nuclear maturation during in vitro maturation in a synthetic follicle fluid medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFOktbs%3D&md5=495f8e3267cf80bd95d9d644857e276dCAS | 15899152PubMed |
Teleni, E., Rowe, J., Croker, K., Murray, P., and King, W. (1989). Lupins and energy-yielding nutrients in ewes. II. Responses in ovulation rate in ewes to increased availability of glucose, acetate and amino acids. Reprod. Fertil. Dev. 1, 117–125.
| Lupins and energy-yielding nutrients in ewes. II. Responses in ovulation rate in ewes to increased availability of glucose, acetate and amino acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsV2qtrw%3D&md5=2f603290b1519ab5864bd1bd11810790CAS | 2798941PubMed |
Thompson, J. G., Lane, M., and Gilchrist, R. B. (2007). Metabolism of the bovine cumulus–oocyte complex and influence on subsequent developmental competence. Soc. Reprod. Fertil. Suppl. 64, 179–190.
| 1:CAS:528:DC%2BD1cXpvVyrs7o%3D&md5=42f8ff288e55903c54b9e5bb093af622CAS | 17491147PubMed |
Vázquez, M. I., Blanch, M. S., Alanis, G. A., Chaves, M. A., and Gonzalez-Bulnes, A. (2010). Effects of treatment with a prostaglandin analogue on developmental dynamics and functionality of induced corpora lutea in goats. Anim. Reprod. Sci. 118, 42–47.
| Effects of treatment with a prostaglandin analogue on developmental dynamics and functionality of induced corpora lutea in goats.Crossref | GoogleScholarGoogle Scholar | 19541434PubMed |
Veiga-Lopez, A., Encinas, T., McNeilly, A. S., and Gonzalez-Bulnes, A. (2008). Timing of preovulatory LH surge and ovulation in superovulated sheep are affected by follicular status at start of the FSH treatment. Reprod. Domest. Anim. 43, 92–98.
| 1:CAS:528:DC%2BD1cXivFGrsb0%3D&md5=e2520d051aee4b894380ef7a3c39e33fCAS | 18199264PubMed |
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=91eaac353af4faf45faa324ee8a63d4cCAS | 11732990PubMed |
