Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T02:58:40.208Z Has data issue: false hasContentIssue false

In vitro developmental competence of prepubertal goat oocytes cultured with recombinant activin-A

Published online by Cambridge University Press:  31 October 2013

S. Hammami
Affiliation:
Departament de Ciència Animal i dels Aliments, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
D. Izquierdo
Affiliation:
Departament de Ciència Animal i dels Aliments, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
M. G. Catalá
Affiliation:
Departament de Ciència Animal i dels Aliments, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
M. T. Paramio
Affiliation:
Departament de Ciència Animal i dels Aliments, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
R. Morató*
Affiliation:
Department of Biology, Biotechnology of Animal and Human Reproduction (TechnoSperm), Institute of Food and Agricultural Technolog, University of Girona, 17071 Girona, Spain
*
Get access

Abstract

The present study was designed to evaluate the effect of activin-A during the in vitro oocyte maturation (IVM) and in vitro embryo culture (IVC) on nuclear maturation, blastocyst yield and blastocyst quality of prepubertal goat oocytes. In Experiment 1, three groups of oocytes were used during the IVM of prepubertal goat oocytes to determine the optimal concentration of recombinant human activin-A added to the maturation medium. Cumulus–oocyte complexes were matured in an IVM medium containing 0, 10 and 100 ng/ml (groups A0, A10 and A100), fertilized and in vitro cultured using standard procedures. In Experiment 2, the addition of 10 ng/ml activin-A at IVM (A10A0), IVC (A0A10) or IVM+IVC (A10A10) was studied and compared with the control group (A0A0). Results of the first experiment demonstrated that the addition of activin-A yielded similar percentages of maturation (⩽71.0%) and blastocyst formation rates (⩽24.9%) than the control group (A0). Experiment 2 showed that exposure of prepubertal goat oocytes to an IVC medium containing 10 ng/ml activin-A (A0A10) significantly increased the rates of development to the blastocyst stage, as compared with the control group (A0A0) (19.5±2.21% v. 13.1±2.37%, respectively; P<0.05). With regard to the blastocyst quality, total number of cells, inner cell mass (ICM) and trophectoderm of prepubertal goat embryos produced in the presence of activin-A did not differ significantly among experimental groups. In summary, these results indicate that supplementation of the IVC medium with activin-A enhances embryo development of prepubertal goat oocytes.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alak, BM, Smith, GD, Woodruff, TK, Stouffer, RL and Wolf, DP 1996. Enhancement of primate oocyte maturation and fertilization in vitro by inhibin A and activin A. Fertility and Sterility 55, 646653.Google Scholar
Alak, BM, Coskun, S, Friedman, CI, Kennard, EA, Kim, HM and Seifer, DB 1998. Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro. Fertility and Sterility 70, 11261130.CrossRefGoogle ScholarPubMed
Armstrong, DT 2001. Effects of maternal age on oocyte developmental competence. Theriogenology 55, 13031322.CrossRefGoogle ScholarPubMed
Brawtal, R 1994. Expression of messenger-RNA for follistatin and inhibin/activin subunits during follicular-growth and aresia. Journal of Molecular Endocrinology 13, 253264.Google Scholar
Childs, G and Unabia, G 1997. Cytochemical studies of the effects of activin on gonadotropin-releasing hormone (GnRH) binding by pituitary gonadotropes and growth hormone cells. Journal of Histochemistry and Cytochemistry 45, 16031610.Google Scholar
Coskun, S and Lin, Y 1994. Effects of transforming growth-factors and activin A on in-vitro porcine oocyte maturation. Molecular Reproduction and Development 38, 153159.CrossRefGoogle ScholarPubMed
Gandolfi, F, Modina, S, Brevini, T, Passoni, L, Artini, P, Petraglia, F and Lauria, A 1995. Activin beta(A) subunit is expressed in bovine oviduct. Molecular Reproduction and Development 40, 286291.CrossRefGoogle ScholarPubMed
Hata, K, Kilkuchi, K, Tada, K and Tsuiki, S 1988. Analysis of glucose-6-phosphate translocase and hexose-6-phosphatep phosphohydrolase, the 2 obligatory components of microsomal glucose-6-phosphatase system, in rat-liver. Tohoku Journal of Experimental Medicine 155, 173181.CrossRefGoogle ScholarPubMed
Heyner, S, Shan, N, Smith, R, Watson, A and Schultz, G 1993. The role of growth-factors in embryo production. Theriogenology 39, 151161.Google Scholar
Hulshof, S, Figueiredo, J, Beckers, J, Bevers, M, Vanderstichele, H and Van den Hurk, R 1997. Bovine preantral follicles and activin: Immunohistochemistry for activin and activin receptor and the effect of bovine activin A in vitro. Theriogenology 48, 133142.CrossRefGoogle ScholarPubMed
Itoh, M, Igarashi, M, Yamada, K, Hasegawa, Y, Seki, M, Eto, Y and Shibai, H 1990. Activin A stimulates meiotic maturation of the rat oocyte in vitro. Biochemical and Biophysical Research Communications 166, 14791484.Google Scholar
Izadyar, F, Zeinstra, E, Colenbrander, B, Vanderstichele, H and Bevers, M 1996. In vitro maturation of bovine oocytes in the presence of bovine activin A does not affect the number of embryos. Animal Reproduction Science 45, 3745.CrossRefGoogle Scholar
Izadyar, F, Dijkstra, G, Van Tol, H, van de Eljnden-Van Raaij, A, Van den Hurk, R, Colenbrander, B and Bevers, M 1998. Immunohistochemical localization and mRNA expression of activin, inhibin, follistatin, and activin receptor in bovine cumulus–oocyte complexes during in vitro maturation. Molecular Reproduction and Development 49, 186195.Google Scholar
Khatir, H, Lonergan, P and Mermillod, P 1998. Kinetics of nuclear maturation and protein profiles of oocytes from prepubertal and adult cattle during in vitro maturation. Theriogenology 50, 917929.Google Scholar
Koeman, J, Keefer, C, Baldassarre, H and Downey, B 2003. Developmental competence of prepubertal and adult goat oocytes cultured in semi-defined media following laparoscopic recovery. Theriogenology 60, 879889.Google Scholar
Ledda, S, Bogliolo, L, Calvia, P, Leoni, G and Naitana, S 1997. Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes. Journal of Reproduction and Fertility 109, 7378.Google Scholar
Lee, K, Bettegowda, A, Wee, G, Ireland, JJ and Smith, GW 2009. Molecular determinants of oocyte competence: potential functional role for maternal (oocyte-derived) follistatin in promoting bovine early embryogenesis. Endocrinology 150, 24632471.Google Scholar
Leoni, GG, Succu, S, Satta, V, Paolo, M, Bogliolo, L, Bebbere, D, Spezzigu, A, Madeddu, M, Berlinguer, F, Ledda, S and Naitana, S 2009. In vitro production and cryotolerance of prepubertal and adult goat blastocysts obtained from oocytes collected by laparoscopic oocyte-pick-up (LOPU) after FSH treatment. Reproduction Fertility and Development 21, 901908.Google Scholar
Lu, R, Matsuyama, S, Nishihara, M and Takahashi, M 1993. Developmental expression of activin/inhibin beta A, beta B, and alpha subunits, and activin receptor-IIB genes in preimplantation mouse embryos. Biology of Reproduction 49, 11631169.Google Scholar
Marchal, R, Feugang, J, Perreau, C, Venturi, E, Terqui, M and Mermillod, P 2001. Meiotic and developmental competence of prepubertal and adult swine oocytes. Theriogenology 56, 1729.Google Scholar
Mather, JP, Moore, A and Li, RH 1997. Activins, inhibins, and follistatins: further thoughts on a growing family of regulators. Proceedings of the Society for Experimental Biology and Medicine 215, 209222.Google Scholar
Norwitz, E, Xu, S, Jeong, K, Bedecarrats, G, Winebrenner, L, Chin, W and Kaiser, U 2002. Activin A augments GnRH-mediated transcriptional activation of the mouse GnRH receptor gene. Endocrinology 143, 985997.Google Scholar
Park, JE, Oh, HJ, Hong, SG, Jang, G, Kim, MK and Lee, BC 2010. Effects of activin A on the in vitro development and mRNA expression of bovine embryos cultured in chemically-defined two-step culture medium. Reproduction in Domestic Animals 45, 585593.Google ScholarPubMed
Parrish, J, Suskoparrish, J, Leibfriedrutledge, M, Cristser, E, Eyestone, W and First, N 1986. Bovine in vitro fertilization with frozen-thawed semen. Theriogenology 25, 591600.Google Scholar
Patel, O, Bettegowda, A, Ireland, J, Coussens, P, Lonergan, P and Smith, G 2007. Functional genomics studies of oocyte competence: evidence that reduced transcript abundance for follistatin is associated with poor developmental competence of bovine oocytes. Reproduction 133, 95106.Google Scholar
Presicce, G, Jiang, S, Simkin, M, Zhang, L, Looney, C, Godke, R and Yang, X 1997. Age and hormonal dependence of acquisition of oocyte competence for embryogenesis in prepubertal calves. Biology of Reproduction 56, 386392.Google Scholar
Rodriguez-Gonzalez, E, Lopez-Bejar, M, Velilla, E and Paramio, M 2002. Selection of prepubertal goat oocytes using the brilliant cresyl blue test. Theriogenology 57, 13971409.Google Scholar
Romaguera, R, Casanovas, A, Morato, R, Izquierdo, D, Catala, M, Jimenez-Macedo, AR, Mogas, T and Paramio, MT 2010. Effect of follicle diameter on oocyte apoptosis, embryo development and chromosomal ploidy in prepubertal goats. Theriogenology 74, 364373.Google Scholar
Romaguera, R, Moll, X, Morato, R, Roura, M, Palomo, MJ, Catala, MG, Jimenez-Macedo, AR, Hammami, S, Izquierdo, D, Mogas, T and Paramio, MT 2011. Prepubertal goat oocytes from large follicles result in similar blastocyst production and embryo ploidy than those from adult goats. Theriogenology 76, 111.Google Scholar
Sidis, Y, Fujiwara, T, Leykin, L, Isaacson, K, Toth, T and Schneyer, A 1998. Characterization of inhibin/activin subunit, activin receptor, and follistatin messenger ribonucleic acid in human and mouse oocytes: evidence for activin’s paracrine signaling from granulosa cells to oocytes. Biology of Reproduction 59, 807812.Google Scholar
Silva, J, van den Hurk, R, van Tol, H, Roelen, B and Figueiredo, J 2004. Gene expression and protein localisation for activin-A, follistatin and activin receptors in goat ovaries. Journal of Endocrinology 183, 405415.Google Scholar
Silva, J, Tharasanit, T, Taverne, M, Van der Weijden, G, Santos, R, Figueiredo, J and Van den Hurk, R 2006. The activin-follistatin system and in vitro early follicle development in goats. Journal of Endocrinology 189, 113125.Google Scholar
Sirard, MA, Richard, F, Blondin, P and Robert, C 2006. Contribution of the oocyte to embryo quality. Theriogenology 65, 126136.Google Scholar
Stock, A, Woodruff, T and Smith, L 1997. Effects of inhibin A and activin A during in vitro maturation of bovine oocytes in hormone- and serum-free medium. Biology of Reproduction 56, 15591564.Google Scholar
Takahashi, Y and First, NL 1992. In vitro development of bovine one cell embryos influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology 37, 963978.Google Scholar
Thomas, FH, Armstrong, DG and Telfer, EE 2003. Activin promotes oocyte development in ovine preantral follicles in vitro. Reproductive Biology and Endocrinology 1, 76.CrossRefGoogle ScholarPubMed
Thouas, GA, Korfiatis, NA, French, AJ, Jones, GM and Trounson, AO 2001. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reproductive BioMedicine Online 3, 2529.CrossRefGoogle ScholarPubMed
Trigal, B, Gomez, E, Diez, C, Caamano, JN, Martin, D, Carrocera, S and Munoz, M 2011. In vitro development of bovine embryos cultured with activin A. Theriogenology 75, 584588.CrossRefGoogle ScholarPubMed
Trigal, B, Gomez, E, Diez, C, Caamano, JN, Molina, I, Carrocera, S, Martin, D and Munoz, M 2010. In vitro development of bovine morulae produced and/or cultured with activin. Reproduction Fertility and Development 22, 236.Google Scholar
Tsuchiya, M, Minegishi, T, Kishi, H, Tano, M, Kameda, T, Hirakawa, T, Ibuki, Y, Mizutani, T and Miyamoto, K 1999. Control of the expression of luteinizing hormone receptor by local factors in rat granulosa cells. Archives of Biochemistry and Biophysics 367, 185192.Google Scholar
Van den Hurk, R and Van de Pavert, S 2001. Localization of an activin/activin receptor system in the porcine ovary. Molecular Reproduction and Development 60, 463471.Google Scholar
VanSoom, A, Ysebaert, M and DeKruif, A 1997. Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Molecular Reproduction and Development 47, 4756.3.0.CO;2-Q>CrossRefGoogle Scholar
Vantol, H, Deloos, F, Vanderstichele, H and Bevers, M 1994. Bovine activin A does not affect the in vitro maturation of bovine oocytes. Theriogenology 41, 673679.Google Scholar
Ying, S 1988. Inhibins, activins, and follistatins – gonadal proteins modulating the secretion of follicle-stimulating-hormone. Endocrine Reviews 9, 267293.Google Scholar
Yoshioka, K and Kamomae, H 1996. Recombinant human activin a stimulates development of bovine one-cell embryos matured and fertilized in vitro. Molecular Reproduction and Development 45, 151156.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Yoshioka, K, Suzuki, C and Iwamura, S 1998a. Activin A and follistatin regulate developmental competence of in vitro-produced bovine embryos. Biology of Reproduction 59, 10171022.Google Scholar
Yoshioka, K, Takata, M, Taniguchi, T, Yamanaka, H and Sekikawa, K 1998b. Differential expression of activin subunits, activin receptors and follistatin genes in bovine oocytes and preimplantation embryos. Reproduction Fertility and Development 10, 293298.Google Scholar
Younis, A, Zuelke, K, Happer, K, Oliveira, M and Brackett, B 1991. Invitro fertilization of goat oocytes. Biology of Reproduction 44, 11771182.Google Scholar
Zhao, J, Taverne, M, van der Weijden, G, Bevers, M and Van den Hurk, R 2001. Effect of activin A on in vitro development of rat preantral follicles and localization of activin A and activin receptor II. Biology of Reproduction 65, 967977.CrossRefGoogle ScholarPubMed