Bovine dominant follicular fluid promotes the in vitro development of goat preantral follicles
A. B. G. Duarte A E , V. R. Araújo A , R. N. Chaves A , G. M. Silva A , D. M. Magalhães-Padilha A , R. A. Satrapa B , M. A. M. Donato C , C. A. Peixoto C , C. C. Campello A , M. H. T. Matos D , C. M. Barros B and J. R. Figueiredo A
+ Author Affiliations
- Author Affiliations
A Faculty of Veterinary Medicine, Laboratory of Manipulation of Oocytes and Preantral Follicles (LAMOFOPA), State University of Ceará, Fortaleza, 60740-903, CE, Brazil.
B Department of Pharmacology, Institute of Bioscience, University of São Paulo State (UNESP), Botucatu, São Paulo, Brazil.
C Laboratory of Ultrastructure, CPqAM/Fiocruz, Federal University of Pernambuco, Recife, PE, Brazil.
D Nucleus of Biotechnology Applied to Ovarian Follicle Development, Federal University of São Francisco Valley, Petrolina, 48902-300, PE, Brazil.
E Corresponding author. Email: beatriz_duarte34@yahoo.com.br
Abstract
The aim of this study was to evaluate the effect of follicular fluid collected from bovine dominant follicles (bFF) on the in vitro development of goat preantral follicles and determine the best time to add this supplement to the culture medium. The preantral follicles were isolated and randomly distributed into four treatments in absence (control) or presence of 10% of bFF added on Days 0 (FF0–18), 6 (FF6–18) or 12 (FF12–18) of culture onwards. After 18 days, follicular development was assessed based on follicular survival, antral cavity formation, increased follicular diameter as well as fully grown oocyte (>110 μm) viability and meiosis resumption. The oocytes from the cultured follicles were in vitro-matured and processed for fluorescence or ultrastructural analysis. The results showed that on Day 18 the treatment FF0–18 had a significantly higher (P < 0.05) survival than control and FF12–18, but not FF6–18. The addition of bFF at the beginning of culture (FF0–18 and FF6–18) promoted a high percentage of follicular growth, meiosis resumption and early antrum formation. Moreover, this study described for the first time the ultrastructural analysis of caprine oocytes grown in vitro. This evaluation revealed that in the presence of bFF on (FF0–18) the in vitro-grown oocytes presented normal organelle distribution and well-defined, intact plasma and nuclear membranes. In conclusion, bFF originating from dominant follicles maintain the survival and promote the in vitro growth of goat preantral follicles when added at the beginning of culture.
Additional keywords: caprine, cell culture, in vitro growth, oocyte.
References
Algriany, O., Bevers, M., Schoevers, E., Colenbrander, B., and Dieleman, S. (2004). Follicle size-dependent effects of sow follicular fluid on in vitro cumulus expansion, nuclear maturation and blastocyst formation of sow cumulus oocytes complexes. Theriogenology 62, 1483–1497.| Follicle size-dependent effects of sow follicular fluid on in vitro cumulus expansion, nuclear maturation and blastocyst formation of sow cumulus oocytes complexes.Crossref | GoogleScholarGoogle Scholar | 15451257PubMed |
Arshad, H.M., Ahmad, N., Zia-ur-Rahman, H., Samad, A., Akhtar, N., and Ali, S. (2005). Studies on some biochemical constituents of ovarian follicular fluid and peripheral blood in buffaloes. Pakistan Vet J. 25, 189–193.
Arunakumari, G., Shanmugasundaram, N., and Rao, V. H. (2010). Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74, 884–894.
| Development of morulae from the oocytes of cultured sheep preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjosVSktA%3D%3D&md5=f5d235425c3deb9c772a9e13e513e5f7CAS | 20615540PubMed |
Bijttebier, J., Van Soom, A., Meyer, E., Mateusen, B., and Maes, D. (2008). Preovulatory follicular fluid during in vitro maturation decreases polyspermic fertilization of cumulus-intact porcine oocytes. Theriogenology 70, 715–724.
| Preovulatory follicular fluid during in vitro maturation decreases polyspermic fertilization of cumulus-intact porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvovVGhsw%3D%3D&md5=0a42f7b9cb43dba1ed7173adfe5f9b61CAS | 18572236PubMed |
Bruno, J. B., Celestino, J. J. H., Lima-Verde, I. B., Lima, L. F., Matos, M. H. T., Araújo, V. R., Saraiva, M. V., Martins, F. S., Name, K. P. O., Campello, C. C., Báo, S. N., Silva, J. R. V., and Figueiredo, J. R. (2009). Expression of vascular endothelial growth factor (VEGF) receptor in goat ovaries and improvement of in vitro caprine preantral follicle survival and growth with VEGF. Reprod. Fertil. Dev. 21, 679–687.
| Expression of vascular endothelial growth factor (VEGF) receptor in goat ovaries and improvement of in vitro caprine preantral follicle survival and growth with VEGF.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsVCrurs%3D&md5=825ceeb0507942e4f1d38d8f7e0e1c1eCAS | 19486605PubMed |
Celestino, J. J. H., Bruno, J. B., Lima-Verde, I. B., Matos, M. H. T., Saraiva, M. V. A., Chaves, R. N., Martins, F. S., Lima, L. F., Name, K. P. O., Campello, C. C., Silva, J. R. V., Báo, S. N., and Figueiredo, J. R. (2009). Recombinant epidermal growth factor maintains follicular ultrastructure and promotes the transition to primary follicles in caprine ovarian tissue cultured in vitro. Reprod. Sci. 16, 239–246.
| Recombinant epidermal growth factor maintains follicular ultrastructure and promotes the transition to primary follicles in caprine ovarian tissue cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsVGqsLg%3D&md5=ccdfcc097472032d0798a8d549c0c4fbCAS |
Chaves, R. N., Martins, F. S., Saraiva, M. V. A., Celestino, J. J. H., Lopes, C. A. P., Correia, J. C., Lima Verde, I. B., Matos, M. H. T., Báo, S. N., Name, K. P. O., Campello, C. C., Silva, J. R. V., and Figueiredo, J. R. (2008). Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro. Reprod. Fertil. Dev. 20, 640–647.
| Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvgvVelsg%3D%3D&md5=7df531ed7e39a78ea497f09e86e9ee75CAS | 18577361PubMed |
Chi, H. J., Kim, D. H., Koo, J. J., and Chang, S. S. (1998). The suitability and efficiency of human follicular fluid as a protein supplement in human in vitro fertilization programs Fertil. Steril. 70, 871–877.
| The suitability and efficiency of human follicular fluid as a protein supplement in human in vitro fertilization programsCrossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FitFCjtA%3D%3D&md5=1269c4f3894c0a37b102caf28401c608CAS | 9806569PubMed |
Clarke, H. G., Hope, S. A., Byers, S., and Rodgers, R. J. (2006). Formation of ovarian follicular fluid may be due to the osmotic potential of large glycosaminoglycans and proteoglycans. Reproduction 132, 119–131.
| Formation of ovarian follicular fluid may be due to the osmotic potential of large glycosaminoglycans and proteoglycans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot1OgtrY%3D&md5=cd9249e9963efbd7d1e659308412aff0CAS | 16816338PubMed |
Das, K., Phipps, W. R., Hensleigh, H. C., and Tagatz, G. E. (1992). Epidermal growth factor in human follicular fluid stimulates mouse oocyte maturation in vitro. Fertil. Steril. 57, 895–901.
| 1:STN:280:DyaK383gvFOqug%3D%3D&md5=d9329ff9ef407d8fd45a05b64df16ad7CAS | 1555705PubMed |
Dell’Aquila, M. E., Cho, Y. S., Minoia, P., Traina, V., Lacalandra, G. M., and Maritato, F. (1997). Effects of follicular fluid supplementation of in vitro maturation medium on the fertilization and development of equine oocytes after in vitro fertilization or intracytoplasmic sperm injection. Hum. Reprod. 12, 2766–2772.
| Effects of follicular fluid supplementation of in vitro maturation medium on the fertilization and development of equine oocytes after in vitro fertilization or intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7hsFertw%3D%3D&md5=971c93ee726ee166e1bcece19bfcf0f1CAS | 9455850PubMed |
Eppig, J. J., and Schroeder, A. C. (1989). Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation and fertilization in vitro. Biol. Reprod. 41, 268–276.
| Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation and fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2FivVGhsA%3D%3D&md5=50b6efc96722af0f6203388c32f45917CAS | 2508774PubMed |
Ferreira, E. M., Vireque, A. A., Adona, P. R., Meirelles, F. V., Ferriani, R. A., and Navarro, P. A. A. S. (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–848.
| Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVSgs7k%3D&md5=179b674d5a6944e2a68733179da2cf47CAS | 19121865PubMed |
Figueiredo, J. R., Celestino, J. J. H., Rodrigues, A. P. R., and Silva, J. R. V. (2007). Importância da biotécnica de MOIFOPA para o estudo da foliculogênese e produção in vitro de embriões em larga escala. Rev. Bras. Reprod. Anim 31, 143–152.
Franks, S., Neagle, G., Leake, R., Mason, H., Harlow, C., and Winston, R. (1987). Epidermal growth factor (EGF) concentrations in follicular fluid from normal or polycystic ovaries (PCO) J. Endocrinol. 112, 120–121.
Gosden, R. G., Hunter, R. H. F., 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=2439b5e01936542f41401c45ddf4f965CAS | 3283348PubMed |
Gupta, P. S. P., Ramesh, H. S., Manjunatha, B. M., Nandi, S., and Ravindra, J. P. (2008). Production of buffalo embryos using oocytes from in vitro grown preantral follicles. Zygote 16, 57–63.
| Production of buffalo embryos using oocytes from in vitro grown preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVGmt74%3D&md5=4bd24fe95de99179b9d8a85ae54bedfcCAS |
Hofmann, G. E., Scott, R. T., Bryzski, R. G., and Jones, H. W. (1990). Immunoreactive epidermal growth factor concentrations in follicular fluid obtained from in vitro fertilization. Fertil. Steril. 54, 303–307.
| 1:STN:280:DyaK3czjs1yksg%3D%3D&md5=c9314d6d6de347aa5bcd292d7bf69243CAS | 2116331PubMed |
Hsu, C. J., Holmes, S. D., and Hammond, J. M. (1987). Ovarian epidermal growth factor activity, concentration in porcine follicular fluid during follicular enlargement. Biochem. Biophys. Res. Commun. 147, 242–247.
| Ovarian epidermal growth factor activity, concentration in porcine follicular fluid during follicular enlargement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlsVyis74%3D&md5=6c3476c7853cc73fe3d244ae57f56e80CAS | 3498484PubMed |
Ito, M., Iwata, H., Kitagawa, M., Kon, Y., Kuwayama, T., and Monji, Y. (2008). Effect of follicular fluid collected from various diameter follicles on the progression of nuclear maturation and developmental competence of pig oocytes. Anim. Reprod. Sci. 106, 421–430.
| Effect of follicular fluid collected from various diameter follicles on the progression of nuclear maturation and developmental competence of pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1yku7Y%3D&md5=caa4cf2cd36f31168c726b7f323f5e70CAS | 17644281PubMed |
Iwata, H., Hashimoto, S., Ohota, M., Kimura, K., Shibano, K., and Miyake, M. (2004). Effects of follicle size and electrolytes and glucose in maturation medium on nuclear maturation and developmental competence of bovine oocytes. Reproduction 127, 159–164.
| Effects of follicle size and electrolytes and glucose in maturation medium on nuclear maturation and developmental competence of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitVWrt7w%3D&md5=af0776c59cca89c014edf12f44ae2c15CAS | 15056781PubMed |
Kawano, Y., Hasan, K. Z., Fukuda, J., Mine, S., and Miyakawa, I. (2003). Production of vascular endothelial growth factor and angiogenic factor in human follicular fluid. Mol. Cell. Endocrinol. 202, 19–23.
| Production of vascular endothelial growth factor and angiogenic factor in human follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFSns7Y%3D&md5=4072969ef60382e95117b281efaf255fCAS | 12770725PubMed |
Khatir, H., Carolan, C., Lonergan, P., and Mermillod, P. (1997). Characterization of calf follicular fluid and its ability to support cytoplasmic maturation of cow and calf oocytes. J. Reprod. Fertil. 111, 267–275.
| Characterization of calf follicular fluid and its ability to support cytoplasmic maturation of cow and calf oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsFertg%3D%3D&md5=0124bdf56d8d85c0b69073fecb92453aCAS | 9462295PubMed |
Kim, K. S., Mitsumizo, N., Fujita, K., and Utsumi, K. (1996). The effects of follicular fluid on in vitro maturation, oocyte fertilization and the development of bovine embryos. Theriogenology 45, 787–799.
| The effects of follicular fluid on in vitro maturation, oocyte fertilization and the development of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVGqug%3D%3D&md5=11238ffdaf7e9ba1d8e29ab6b84961bbCAS |
Koga, K., Osuga, Y., Tsutsumi, O., Momoeda, M., Suenaga, A., Kugu, K., Fujiwara, T., Takai, Y., Yano, T., and Taketani, Y. (2000). Evidence for the presence of angiogenin in human follicular fluid and the upregulation of its production by human chorionic gonadotropin and hypoxia. J. Clin. Endocrinol. Metab. 85, 3352–3355.
| Evidence for the presence of angiogenin in human follicular fluid and the upregulation of its production by human chorionic gonadotropin and hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsVKqsbo%3D&md5=29f576deefe5eb0fdbe44e4fed7409f0CAS | 10999833PubMed |
Krisher, R. L., and Bavister, B. D. (1998). Responses of oocytes and embryos to the culture environment. Theriogenology 49, 103–114.
| Responses of oocytes and embryos to the culture environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFCrtQ%3D%3D&md5=01de0069dc9ee321d9a3f3b714fb1a68CAS | 10732124PubMed |
Krisher, R. L., Brad, A. M., Herrick, J. R., Sparman, M. L., and Swain, J. E. (2007). A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation. Anim. Reprod. Sci. 98, 72–96.
| A comparative analysis of metabolism and viability in porcine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1Sksrw%3D&md5=c68a63c9df9130302b75ca30504e4298CAS | 17110061PubMed |
Li, R., Norman, R. J., Armstrong, D. T., and Gilchrist, R. B. (2000). Oocyte secreted factor(s) determine the functional differences between bovine mural granulosa cells and cumulus cells. Biol. Reprod. 53, 1243–1250.
Lucci, C. M., Silva, R. V., Carvalho, C. A., Figueiredo, R., and Báo, N. (2001). Light microscopical and ultrastructural characterization of goat preantral follicles. Small Rumin. Res. 41, 61–69.
| Light microscopical and ultrastructural characterization of goat preantral follicles.Crossref | GoogleScholarGoogle Scholar | 11423235PubMed |
Magalhães, D. M., Duarte, A. B. G., Araújo, V. R., Brito, I. R., Soares, T. G., Lima, I. M. T., Lopes, C. A. P., Campello, C. C., Rodrigues, A. P. R., and Figueiredo, J. R. (2011). In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology 75, 182–188.
| In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone.Crossref | GoogleScholarGoogle Scholar | 20875671PubMed |
Metoki, T., Iwata, H., Itoh, M., Kasai, M., Takajyo, A., Suzuki, A., Kuwayama, T., and Monji, Y. (2008). Effects of follicular fluids on the growth of porcine preantral follicle and oocyte. Zygote 16, 239–247.
| Effects of follicular fluids on the growth of porcine preantral follicle and oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovV2gsb0%3D&md5=6aadc5bb01683e2e7517e122f3629717CAS | 18578948PubMed |
Nandi, S., Girish, K. V., Manjunatha, B. M., Ramesh, H. S., and Gupta, P. S. P. (2008). Follicular fluid concentrations of glucose, lactate and pyruvate in buffalo and sheep, and their effects on cultured oocytes, granulosa and cumulus cells. Theriogenology 69, 186–196.
| Follicular fluid concentrations of glucose, lactate and pyruvate in buffalo and sheep, and their effects on cultured oocytes, granulosa and cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyrsg%3D%3D&md5=326e32bf8e4172fb0e5cd32c31931f85CAS | 17950822PubMed |
O’Brien, M. J., Pendola, J. K., and Eppig, J. J. (2003). A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod. 68, 1682–1686.
| A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt12ltrY%3D&md5=94d6118d4011b7aaad01d67cd1c9128cCAS | 12606400PubMed |
Orsi, N. M., Gopichandran, N., Leese, H. J., Picton, H. M., and Harri, S. E. (2005). Fluctuations in bovine ovarian follicular fluid composition throughout the oestrous cycle. Reproduction 129, 219–228.
| Fluctuations in bovine ovarian follicular fluid composition throughout the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis1yrsro%3D&md5=c27ec0bd5d5960d263d82f587bc4ff24CAS | 15695616PubMed |
Picton, H. M., Harris, S. E., Muruvi, W., and Chambers, E. L. (2008). The in vitro growth and maturation of follicles. Reproduction 136, 703–715.
| The in vitro growth and maturation of follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXns1CktA%3D%3D&md5=13c86828dacd13132d8c0afca05288d2CAS | 19074213PubMed |
Rodgers, R. J., and Irving-Rodgers, H. F. (2010). Formation of the ovarian follicular antrum and follicular fluid. Biol. Reprod. 82, 1021–1029.
| Formation of the ovarian follicular antrum and follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVCgtrs%3D&md5=e2ee9ee10043456d619d66956e8f75e8CAS | 20164441PubMed |
Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
| Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVKjtrk%3D&md5=1c33fa33a77fabe3ffd8504ad8c8ffc9CAS | 11207207PubMed |
Tatemoto, H., Muto, N., Sunagawa, I., Shinjo, A., and Nakada, T. (2004). Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biol. Reprod. 71, 1150–1157.
| Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqt7c%3D&md5=b95a3238317b4124a8aad1db3d30cbe3CAS | 15175235PubMed |
von Otte, S., Jurgen, R. J., Becker, P. S., Konig, S., Fobker, M., Greb, R. R., Kiesel, L., Assmann, G., Diedrich, K., and Nofer, J. R. (2006). Follicular fluid high density lipoprotein-associated sphingosine 1-phosphate is a novel mediator of ovarian angiogenesis. J. Biol. Chem. 281, 5398–5405.
| Follicular fluid high density lipoprotein-associated sphingosine 1-phosphate is a novel mediator of ovarian angiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvVejs7c%3D&md5=8a6f483ac410ff60e3cb97bcaa3e80cfCAS | 16365044PubMed |
Wang, T. H., Chang, C. L., Wu, H. M., Chiu, Y. M., Chen, C. K., and Wang, H. S. (2006). Insulin-like growth factor-II (IGF-II), IGF-binding protein-3 (IGFBP-3), and IGFBP-4 in follicular fluid are associated with oocyte maturation and embryo development. Fertil. Steril. 86, 1392–1401.
| Insulin-like growth factor-II (IGF-II), IGF-binding protein-3 (IGFBP-3), and IGFBP-4 in follicular fluid are associated with oocyte maturation and embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWnurnJ&md5=4b8649d7bf3b9a7f9ce50e3fe5f23eb7CAS | 17070193PubMed |
Wu, J., Emery, B. R., and Carrell, D. T. (2001). In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles. Biol. Reprod. 64, 375–381.
| In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFCruw%3D%3D&md5=caaa1e2583421488e4a5140fccc42c92CAS | 11133696PubMed |
Yoon, K. W., Shin, T. Y., Park, J. I., Roh, S., Lim, J. M., Lee, B. C., Hwang, W. S., and Lee, E. S. (2000). Development of porcine oocytes from preovulatory follicles of different sizes after maturation in media supplemented with follicular fluids. Reprod. Fertil. Dev. 12, 133–139.
| Development of porcine oocytes from preovulatory follicles of different sizes after maturation in media supplemented with follicular fluids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvjsFejtw%3D%3D&md5=22d53b3625b181caac0cded006f81964CAS | 11302422PubMed |
Zeng, H. T., Yeung, W. S., Cheung, M. P., Ho, P. C., Lee, C. K., Zhuang, G. L., and Liang, X. Y. (2009). In vitro-matured rat oocytes have low mitochondrial deoxyribonucleic acid and adenosine triphosphate contents and have abnormal mitochondrial redistribution. Fertil. Steril. 91, 900–907.
| In vitro-matured rat oocytes have low mitochondrial deoxyribonucleic acid and adenosine triphosphate contents and have abnormal mitochondrial redistribution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnslWmsb4%3D&md5=904e0b5dfbbe4522110deae9ce08cabeCAS | 18321496PubMed |
