Effect of duration of the growing phase of ovulatory follicles on oocyte competence in superstimulated cattle
F. C. F. Dias A , E. Costa A , G. P. Adams A , R. J. Mapletoft B , J. Kastelic C , O. Dochi D and J. Singh A EA Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, 52 Campus Drive, Saskatoon, SK S7N 5B4, Canada.
B Department of Large Animal Clinical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, 52 Campus Drive, Saskatoon, SK S7N 5B4, Canada.
C Agriculture and Agri-Food Canada, Lethbridge Research Centre, Lethbridge, AB T1J 4B1, Canada.
D Department of Dairy Science, Rakuno Gakuen University, Ebetsu 069-8501, Japan.
E Corresponding author. Email: jaswant.singh@usask.ca
Reproduction, Fertility and Development 25(3) 523-530 https://doi.org/10.1071/RD11284
Submitted: 5 November 2011 Accepted: 9 April 2012 Published: 14 May 2012
Abstract
In the present study, we tested the hypotheses that oocyte competence is compromised by a longer duration of follicular growth and that it is not affected by FSH starvation. Cows were allocated to short FSH (n = 14), FSH starvation (n = 13) and long FSH (n = 13) groups. The first two groups were given eight doses of FSH, whereas the third group was given 14 doses of FSH, starting from the day of wave emergence (Day 0). A progesterone-releasing device (controlled internal drug release; CIDR) was placed intravaginally at the start of the experiment in all groups. The short FSH group was given prostaglandin (PG) F2α on Day 3, whereas the two other groups received PGF2α on Day 6. In all cows, the CIDR was removed at the time of PGF treatment; porcine (p) LH was given 24 h after CIDR removal and cows were inseminated 24 and 36 h later. Reproductive tracts were collected 4 days after insemination and ova and/or embryos were cultured for ≥6 days. The FSH starvation group had fewer ovulations (P = 0.001), and ova and/or embryos (P < 0.05). No difference in embryo quality was detected between long and short FSH groups at 7, 9 or 10 days after artificial insemination. In conclusion, oocyte competence was not altered by the duration of the follicular growth phase in superstimulated cows, whereas FSH starvation substantially reduced the ability of superstimulated follicles to ovulate.
Additional keywords: cows, follicular aging, FSH, length of follicular wave, progesterone, superstimulation.
References
Adams, G. P. (1998). Control of ovarian follicular wave dynamics in mature and prepubertal cattle for synchronization and superstimulation. In ‘Proceedings of the XX Congress of the World Association for Buiatrics, Sydney’. pp. 595–605.Adams, G. P. (1999). Comparative patterns of follicle development and selection in ruminants. J. Reprod. Fertil. Suppl. 54, 17–32.
| 1:STN:280:DC%2BD3c7lslagsw%3D%3D&md5=91a15913e382f676f1d3447ce1440e32CAS | 10692842PubMed |
Adams, G. P., Matteri, R. L., and Ginther, O. J. (1992). Effect of progesterone on ovarian follicles, emergence of follicular waves and circulating follicle-stimulating hormone in heifers. J. Reprod. Fertil. 96, 627–640.
| Effect of progesterone on ovarian follicles, emergence of follicular waves and circulating follicle-stimulating hormone in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpsVGqsA%3D%3D&md5=902e9a65191d859a641d278f08f00a7dCAS | 1339842PubMed |
Adams, G. P., Kot, K., and Ginther, O. J. (1993). Selection of a dominant follicle and suppression of follicular growth in heifers. Anim. Reprod. Sci. 30, 259–271.
| Selection of a dominant follicle and suppression of follicular growth in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit1Kjsbk%3D&md5=92e76616199d7a2d686a3cef7fcf4f37CAS |
Adams, G. P., Nasser, L. F., Bo, G. A., Garcia, A., Del-Campo, M. R., and Mapletoft, R. J. (1994). Superovulatory response of ovarian follicles of wave 1 vs wave 2 in heifers. Theriogenology 42, 1103–1113.
| Superovulatory response of ovarian follicles of wave 1 vs wave 2 in heifers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVeksw%3D%3D&md5=0886566c10ac51683cc8c4a09c8c9988CAS | 16727614PubMed |
Adams, G. P., Jaiswal, R., Singh, J., and Malhi, P. (2008). Progress in understanding ovarian follicular dynamics in cattle. Theriogenology 69, 72–80.
| Progress in understanding ovarian follicular dynamics in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSmu7nK&md5=cb11fd875473aa7ef95a4a74287eba17CAS | 17980420PubMed |
Ahmad, N., Townsend, E. C., Dailey, R. A., and Inskeep, E. K. (1997). Relationships of hormonal patterns and fertility to occurrence of two or three waves of ovarian follicles, before and after breeding, in beef cows and heifers. Anim. Reprod. Sci. 49, 13–28.
| Relationships of hormonal patterns and fertility to occurrence of two or three waves of ovarian follicles, before and after breeding, in beef cows and heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXns1Wmtr4%3D&md5=ad464062d12d65c89415975dbc064f2aCAS | 9458946PubMed |
Alkemade, S. J., Murphy, B. D., and Mapletoft, R. J. (1993). Superovulation in the cow: effects of biological activity of gonadotropins. In ‘Proceedings of the 12th Annual Convention of AETA, Portland’.
Baruselli, P. S., de Sa Filho, M. F., Martins, C. M., Nasser, L. F., Nogueira, M. F., Barros, C. M., and Bo, G. A. (2006). Superovulation and embryo transfer in Bos indicus cattle. Theriogenology 65, 77–88.
| Superovulation and embryo transfer in Bos indicus cattle.Crossref | GoogleScholarGoogle Scholar | 16290257PubMed |
Berfelt, D. R., Lightfoot, K. C., and Adams, G. P. (1994). Ovarian synchronization following ultrasound-guided follicular ablation in heifers. Theriogenology 42, 895–907.
| Ovarian synchronization following ultrasound-guided follicular ablation in heifers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVemsA%3D%3D&md5=6ccde56232743d253a242cda6b3f663dCAS | 16727595PubMed |
Blondin, P., Guilbault, L. A., and Sirard, M. A. (1997). The time interval between FSH-P administration and slaughter can influence the developmental competence of beef heifer oocytes. Theriogenology 48, 803–813.
| The time interval between FSH-P administration and slaughter can influence the developmental competence of beef heifer oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXms1Shsrw%3D&md5=f516e7941915a292897dcdc6e50cb4dcCAS | 16728173PubMed |
Blondin, P., Bousquet, D., Twagiramungu, H., Barnes, F., and Sirard, M. A. (2002). Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol. Reprod. 66, 38–43.
| Manipulation of follicular development to produce developmentally competent bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1ylsA%3D%3D&md5=64d62e92116101b74458d5ba5881991aCAS | 11751261PubMed |
Buccione, R., Schroeder, A. C., and Eppig, J. J. (1990). Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol. Reprod. 43, 543–547.
| Interactions between somatic cells and germ cells throughout mammalian oogenesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7ksFGiuw%3D%3D&md5=742d8c820498209ecafbb6a60d551746CAS | 2289008PubMed |
Dias, F. C., Mapletoft, R. J., Kastelic, J. P., Adams, G. P., Colazo, M. G., Stover, B. C., Dochi, O., and Singh, J. (2012). Effect of length of progesterone exposure during ovulatory wave development on pregnancy rate. Theriogenology 77, 437–444.
| Effect of length of progesterone exposure during ovulatory wave development on pregnancy rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1Whtw%3D%3D&md5=9095e86a18270cf68bb23d681de5b020CAS | 21975220PubMed |
Evans, A. C., Adams, G. P., and Rawlings, N. C. (1994). Endocrine and ovarian follicular changes leading up to the first ovulation in prepubertal heifers. J. Reprod. Fertil. 100, 187–194.
| Endocrine and ovarian follicular changes leading up to the first ovulation in prepubertal heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXis1Wks7s%3D&md5=396e12862e5f54d2431caac9f2e85349CAS | 8182588PubMed |
Ginther, O. J., Kastelic, J. P., and Knopf, L. (1989a). Composition and characteristics of follicular waves during the bovine estrous cycle. Anim. Reprod. Sci. 20, 187–200.
| Composition and characteristics of follicular waves during the bovine estrous cycle.Crossref | GoogleScholarGoogle Scholar |
Ginther, O. J., Knopf, L., and Kastelic, J. P. (1989b). Temporal associations among ovarian events in cattle during oestrous cycles with two and three follicular waves. J. Reprod. Fertil. 87, 223–230.
| Temporal associations among ovarian events in cattle during oestrous cycles with two and three follicular waves.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c7ls1WrsQ%3D%3D&md5=5919044e6ec9740ffa3c2ee698cd32d7CAS | 2621698PubMed |
Ginther, O. J., Bergfelt, D. R., Kulick, L. J., and Kot, K. (1998). Pulsatility of systemic FSH and LH concentrations during follicular-wave development in cattle. Theriogenology 50, 507–519.
| Pulsatility of systemic FSH and LH concentrations during follicular-wave development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFGkurw%3D&md5=14198183c1aafd8826c6e02459851e11CAS | 10732143PubMed |
Gonzalez, A., Lussier, J. G., Carruthers, T. D., Murphy, B. D., and Mapletoft, R. J. (1990). Superovulation of beef heifers with Folltropin: a new FSH preparation containing reduced LH activity. Theriogenology 33, 519–529.
| Superovulation of beef heifers with Folltropin: a new FSH preparation containing reduced LH activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXktVSltLY%3D&md5=f658036204a5fd3cd250117c2807b221CAS | 16726748PubMed |
Jaiswal, R. S. (2007). Regulation of follicular wave pattern in cattle. PhD Thesis. University of Saskatchewan.
Jaiswal, R. S., Singh, J., Nagra, H. S., Grafton, T., Ratto, M. H., Malhi, P. S., and Adams, G. P. (2006). Oocyte competence under different progestational environments. Biol. Reprod. 109, Abstract 166.
Jaiswal, R. S., Singh, J., Marshall, L., and Adams, G. P. (2009). Repeatability of 2-wave and 3-wave patterns of ovarian follicular development during the bovine estrous cycle. Theriogenology 72, 81–90.
| Repeatability of 2-wave and 3-wave patterns of ovarian follicular development during the bovine estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MzosVyktA%3D%3D&md5=887427403ecdcb2423d40e39ab665083CAS | 19329173PubMed |
Lawrence, T. S., Dekel, N., and Beers, W. H. (1980). Binding of human chorionic gonadotropin by rat cumuli oophori and granulosa cells: a comparative study. Endocrinology 106, 1114–1118.
| Binding of human chorionic gonadotropin by rat cumuli oophori and granulosa cells: a comparative study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhvFWltr8%3D&md5=b2bbe9d1d20ab346d8798e17994689e1CAS | 7358027PubMed |
Mapletoft, R. J., Steward, K. B., and Adams, G. P. (2002). Recent advances in the superovulation in cattle. Reprod. Nutr. Dev. 42, 601–611.
| Recent advances in the superovulation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1ymtr8%3D&md5=18b09d4c6bb19af7006a027e83de8573CAS | 12625424PubMed |
Merton, J. S., de Roos, A. P., Mullaart, E., de Ruigh, L., Kaal, L., Vos, P. L., and Dieleman, S. J. (2003). Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry. Theriogenology 59, 651–674.
| Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38jjslKrtA%3D%3D&md5=fe439915d796f29f45df110700ee3aa1CAS | 12499010PubMed |
Mihm, M., Crowe, M. A., Knight, P. G., and Austin, E. J. (2002). Follicle wave growth in cattle. Reprod. Domest. Anim. 37, 191–200.
| Follicle wave growth in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVynsbc%3D&md5=43eaf0256f5886a73f6067ff6cb9f5a1CAS | 12173983PubMed |
Nasser, L. F., Adams, G. P., Bo, G. A., and Mapletoft, R. J. (1993). Ovarian superstimulatory response relative to follicular wave emergence in heifers. Theriogenology 40, 713–724.
| Ovarian superstimulatory response relative to follicular wave emergence in heifers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVWitg%3D%3D&md5=6aa4723e4ad1abf484eb6f0ae21761fcCAS | 16727353PubMed |
Quirk, S. M., Cowan, R. G., Harman, R. M., Hu, C. L., and Porter, D. A. (2004). Ovarian follicular growth and atresia: the relationship between cell proliferation and survival. J. Anim. Sci. 82, E40–E52.
| 15471814PubMed |
Rosenkrans, C. F., Zeng, G. Q., McNamara, G. T., Schoff, P. K., and First, N. L. (1993). Development of bovine embryos in vitro as affected by energy substrates. Biol. Reprod. 49, 459–462.
| Development of bovine embryos in vitro as affected by energy substrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFWk&md5=a5231f5d00bc660fd97a1a11cc3bcc8aCAS | 8399836PubMed |
Sirard, M. A., Florman, H. M., Leibfried-Rutledge, M. L., Barnes, F. L., Sims, M. L., and First, N. L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–1263.
| Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlsFWitLo%3D&md5=1c45774f838a4ce7ffa06878666d58dfCAS | 2775818PubMed |
Sirard, M. A., Picard, L., Dery, M., Coenen, K., and Blondin, P. (1999). The time interval between FSH administration and ovarian aspiration influences the development of cattle oocytes. Theriogenology 51, 699–708.
| The time interval between FSH administration and ovarian aspiration influences the development of cattle oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsFegtbs%3D&md5=580286b136105228bb508f8034508391CAS | 10728995PubMed |
Stringfellow, D. A., and Seidel, S. M. (Eds) (1998). ‘Manual of the International Embryo Transfer Society, 3rd edn.’ (International Embryo Transfer Society: Savoy, IL, USA.)
Townson, D. H., Tsang, P. C., Butler, W. R., Frajblat, M., Griel, L. C., Johnson, C. J., Milvae, R. A., Niksic, G. M., and Pate, J. L. (2002). Relationship of fertility to ovarian follicular waves before breeding in dairy cows. J. Anim. Sci. 80, 1053–1058.
| 1:CAS:528:DC%2BD38XmvV2itL8%3D&md5=33fbe22e22509cae1ea60db59aeb379dCAS | 12008660PubMed |