Relationship between donor animal age, follicular fluid steroid content and oocyte developmental competence in the pig
Christopher G. Grupen A C , Stephen M. McIlfatrick A , Rodney J. Ashman A , Andrew C. Boquest A , David T. Armstrong B and Mark B. Nottle AA BresaGen Limited, Reproductive Biotechnology Division, Adelaide, SA 5000, Australia.
B Department of Obstetrics and Gynaecology, University of Adelaide, Adelaide, SA 5005, Australia.
C To whom correspondence should be addressed. email: chris.grupen@adelaide.edu.au
Reproduction, Fertility and Development 15(2) 81-87 https://doi.org/10.1071/RD02086
Submitted: 17 October 2002 Accepted: 21 February 2003 Published: 21 February 2003
Abstract
The developmental competence of oocytes recovered from the ovaries of slaughtered prepubertal and adult pigs was evaluated after in vitro maturation, parthenogenetic activation and culture in vitro. In addition, the effect of prepubertal and adult follicular fluid (FF) on the developmental competence of prepubertal and adult oocytes was investigated. When matured in adult FF, the rates of cleavage (92 v. 73%; P < 0.01) and blastocyst formation (57 v. 38%; P < 0.05) were greater for adult oocytes than for prepubertal oocytes. Blastocysts derived from adult oocytes had more trophectoderm cells (43 v. 30; P < 0.05) and total cells (51 v. 36; P < 0.05) than blastocysts derived from prepubertal oocytes. The developmental competence of prepubertal oocytes was not affected by the FF donor age, whereas the developmental competence of adult oocytes was. Blastocysts derived from adult oocytes matured in adult FF had more trophectoderm cells (38 v. 24; P < 0.005), inner cell mass cells (7 v. 3; P < 0.01) and total cells (45 v. 27; P < 0.001) than blastocysts derived from adult oocytes matured in prepubertal FF. Characterization of the steroid content of the FF used to supplement the maturation medium revealed that adult FF contained more progesterone (42 v. 23 ng mL−1; P < 0.005) and androstenedione (70 v. 16 ng mL−1; P < 0.05) than prepubertal FF. In addition, the molar ratios of progesterone to androstenedione, androstenedione to 17β-oestradiol and androstenedione to testosterone differed (P < 0.05) between prepubertal and adult FF. The results support the hypothesis that a greater proportion of adult oocytes than of prepubertal oocytes has completed ‘oocyte capacitation’. The differences in FF steroid content are indicative of the different follicular environments from which the prepubertal and adult oocytes were isolated, and may be attributed to the observed effects on oocyte developmental competence.
Extra keywords: adult
Acknowledgments
We thank the abattoir staff of Chapman’s Quality Meats at Nairne and Mr Drago Bratkovic of Murray Bridge for supplying the ovaries used in this study. The performance of steroid assays by Mr Alan Gilmore of the Department of Obstetrics and Gynaecology at Adelaide University is gratefully acknowledged.
Abeydeera, L. R. (2002). In vitro production of embryos in swine Theriogenology 57, 256–73.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ainsworth, L. , Tsang, B. K. , Downey, B. R. , Marcus, G. J. , and Armstrong, D. T. (1980). Interrelationships between follicular fluid steroid levels, gonadotropic stimuli, and oocyte maturation during preovulatory development of porcine follicles Biol. Reprod. 23, 621–7.
| PubMed |
Ainsworth, L. , Tsang, B. K. , Downey, B. R. , and Marcus, G. J. (1990). The synthesis and actions of steroids and prostaglandins during follicular maturation in the pig J. Reprod. Fertil. 40, 137–50.Suppl.
Armstrong, D. T. (2001). Effects of maternal age on oocyte developmental competence Theriogenology 55, 1303–22.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bavister, B. D. (1989). A consistently successful procedure for in vitro fertilization of golden hamster eggs Gamete Res. 23, 139–58.
| PubMed |
Carolan, C. , Lonergan, P. , Monget, P. , Monniaux, D. , and Mermillod, P. (1996). Effect of follicle size and quality on the ability of follicular fluid to support cytoplasmic maturation of bovine oocytes Mol. Reprod. Dev. 43, 477–83.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dode, M. A. , and Graves, C. (2002). Involvement of steroid hormones on in vitro maturation of pig oocytes Theriogenology 57, 811–21.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Driancourt, M. A. , and Thuel, B. (1998). Control of oocyte growth and maturation by follicular cells and molecules present in follicular fluid. A review Reprod. Nutr. Dev. 38, 345–62.
| PubMed |
Eiler, H. , and Nalbandov, A. V. (1977). Sex steroids in follicular fluid and blood plasma during the estrous cycle of pigs Endocrinology 100, 331–8.
| PubMed |
Geber, S. , Winston, R. M. , and Handyside, A. H. (1995). Proliferation of blastomeres from biopsied cleavage stage human embryos in vitro: an alternative to blastocyst biopsy for preimplantation diagnosis Hum. Reprod. Update 10, 1492–6.
Grupen, C. G. , Nagashima, H. , and Nottle, M. B. (1997). Role of epidermal growth factor and insulin-like growth factor-I on porcine oocyte maturation and embryonic development in vitro. Reprod. Fertil. Dev. 9, 571–5.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grupen, C. G. , Mau, J. C. , McIlfatrick, S. M. , Maddocks, S. , and Nottle, M. B. (2002). Effect of 6-dimethylaminopurine on electrically activated in vitro matured porcine oocytes Mol. Reprod. Dev. 62, 387–96.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Guler, A. , Poulin, N. , Mermillod, P. , Terqui, M. , and Cognie, Y. (2000). Effect of growth factors, EGF and IGF-I, and estradiol on in vitro maturation of sheep oocytes Theriogenology 54, 209–18.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hemsworth, P. H. (1990). Mating management. In
Hyttel, P. , Fair, T. , Callesen, H. , and Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle Theriogenology 47, 23–32.
| Crossref | GoogleScholarGoogle Scholar |
Lane, M. , and Gardner, D. K. (1997). Differential regulation of mouse embryo development and viability by amino acids J. Reprod. Fertil. 109, 153–64.Suppl.
| PubMed |
Marchal, R. , Feugang, J. M. , Perreau, C. , Venturi, E. , Terqui, M. , and Mermillod, P. (2001). Meiotic and developmental competence of prepubertal and adult swine oocytes Theriogenology 56, 17–29.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marchal, R. , Vigneron, C. , Perreau, C. , Bali-Papp, A. , and Mermillod, P. (2002). Effect of follicular size on meiotic and developmental competence of porcine oocytes Theriogenology 57, 1523–32.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Meo, H., and Cleary, G. (2000).
Mermillod, P. , Oussaid, B. , and Cognie, Y. (1999). Aspects of follicular and oocyte maturation that affect the developmental potential of embryos J. Reprod. Fertil. 54, 449–60.Suppl.
Nagashima, H. , Grupen, C. G. , Ashman, R. J. , and Nottle, M. B. (1996). Developmental competence of in vivo and in vitro matured porcine oocytes after subzonal sperm injection Mol. Reprod. Dev. 45, 359–63.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
O’Brien, J. K. , Dwarte, D. , Ryan, J. P. , Maxwell, W. M. , and Evans, G. (1996). Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep Reprod. Fertil. Dev. 8, 1029–37.
| PubMed |
O’Brien, J. K. , Catt, S. L. , Ireland, K. A. , Maxwell, W. M. C. , and Evans, G. (1997). In vitro and in vivo developmental capacity of oocytes from prepubertal and adult sheep Theriogenology 47, 1433–43.
| Crossref | GoogleScholarGoogle Scholar |
O’Brien, J. K. , Dwarte, D. , Ryan, J. P. , Maxwell, W. M. C. , and Evans, G. (2000). Comparison of in vitro maturation, in vitro fertilization, metabolism and ultrastructure of oocytes from prepubertal and adult pigs Reprod. Domest. Anim. 34, 101–7.
| Crossref | GoogleScholarGoogle Scholar |
Petters, R. M. , and Wells, K. D. (1993). Culture of pig embryos J. Reprod. Fertil. 48, 61–73.Suppl.
Revel, F. , Mermillod, P. , Peynot, N. , Renard, J. P. , and Heyman, Y. (1995). Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows J. Reprod. Fertil. 103, 115–20.
| PubMed |
Salamone, D. F. , Damiani, P. , Fissore, R. A. , Robl, J. M. , and Duby, R. T. (2001). Biochemical and developmental evidence that ooplasmic maturation of prepubertal bovine oocytes is compromised Biol. Reprod. 64, 1761–8.
| PubMed |
Singh, B. , Barbe, G. J. , and Armstrong, D. T. (1993). Factors influencing resumption of meiotic maturation and cumulus expansion of porcine oocyte–cumulus cell complexes in vitro Mol. Reprod. Dev. 36, 113–19.
| PubMed |
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.
| PubMed |
