In vivo and in vitro maturation of rabbit oocytes differently affects the gene expression profile, mitochondrial distribution, apoptosis and early embryo development
M. Arias-Álvarez A E , R. M. García-García B , J. López-Tello A , P. G. Rebollar C , A. Gutiérrez-Adán D and P. L. Lorenzo BA Department of Producción Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, Ciudad Universitaria, s/n, 28040, Madrid, Spain.
B Department of Fisiología (Fisiología Animal), Facultad de Veterinaria, Universidad Complutense de Madrid, Ciudad Universitaria, s/n, 28040, Madrid, Spain.
C Department of Producción Agraria, Escuela Técnica Superior de Ingenieros Agrónomos, Universidad Politécnica de Madrid, Ciudad Universitaria, s/n, 28040, Madrid, Spain.
D Department of Reproducción Animal, Instituto Nacional de Investigación y Tecnología Agraria, Carretera de La Coruña, Kilómetro 5.9, 28040, Madrid, Spain.
E Corresponding author. Email: m.arias@vet.ucm.es
Reproduction, Fertility and Development 29(9) 1667-1679 https://doi.org/10.1071/RD15553
Submitted: 30 December 2015 Accepted: 16 August 2016 Published: 28 September 2016
Abstract
In vivo-matured cumulus–oocyte complexes are valuable models in which to assess potential biomarkers of rabbit oocyte quality that contribute to enhanced IVM systems. In the present study we compared some gene markers of oocytes and cumulus cells (CCs) from immature, in vivo-matured and IVM oocytes. Moreover, apoptosis in CCs, nuclear maturation, mitochondrial reallocation and the developmental potential of oocytes after IVF were assessed. In relation to cumulus expansion, gene expression of gap junction protein, alpha 1, 43 kDa (Gja1) and prostaglandin-endoperoxide synthase 2 (Ptgs2) was significantly lower in CCs after in vivo maturation than IVM. In addition, there were differences in gene expression after in vivo maturation versus IVM in both oocytes and CCs for genes related to cell cycle regulation and apoptosis (V-Akt murine thymoma viral oncogene homologue 1 (Akt1), tumour protein 53 (Tp53), caspase 3, apoptosis-related cysteine protease (Casp3)), oxidative response (superoxide dismutase 2, mitochondrial (Sod2)) and metabolism (glucose-6-phosphate dehydrogenase (G6pd), glyceraldehyde-3-phosphate dehydrogenase (Gapdh)). In vivo-matured CCs had a lower apoptosis rate than IVM and immature CCs. Meiotic progression, mitochondrial migration to the periphery and developmental competence were higher for in vivo-matured than IVM oocytes. In conclusion, differences in oocyte developmental capacity after IVM or in vivo maturation are accompanied by significant changes in transcript abundance in oocytes and their surrounding CCs, meiotic rate, mitochondrial distribution and apoptotic index. Some of the genes investigated, such as Gja1, could be potential biomarkers for oocyte developmental competence in the rabbit model, helping improve in vitro culture systems in these species.
Additional keywords: assisted reproductive technologies, laboratory animal, oocyte maturation.
References
Adona, P. R., Leal, C. L., Biase, F. H., De Bem, T. H., Mesquita, L. G., Meirelles, F. V., Ferraz, A. L., Furlan, L. R., Monzani, P. S., and Guemra, S. (2016). In vitro maturation alters gene expression in bovine oocytes. Zygote 24, 624–633.| 1:CAS:528:DC%2BC28XhtVOisbzI&md5=fb4136f54d33a681893efd06a83a9a1dCAS | 26885679PubMed |
Adriaenssens, T., Wathlet, S., Segers, I., Verheyen, G., De Vos, A., Van der Elst, J., Coucke, W., Devroey, P., and Smitz, J. (2010). Cumulus cell gene expression is associated with oocyte developmental quality and influenced by patient and treatment characteristics. Hum. Reprod. 25, 1259–1270.
| Cumulus cell gene expression is associated with oocyte developmental quality and influenced by patient and treatment characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFOjsbY%3D&md5=9f90f78b0bad7eb0da40f0e35b0a1c43CAS | 20228394PubMed |
Agca, C., Yakan, A., and Agca, Y. (2013). Estrus synchronization and ovarian hyper-stimulation treatments have negligible effects on cumulus oocyte complex gene expression whereas induction of ovulation causes major expression changes. Mol. Reprod. Dev. 80, 102–117.
| Estrus synchronization and ovarian hyper-stimulation treatments have negligible effects on cumulus oocyte complex gene expression whereas induction of ovulation causes major expression changes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVSku74%3D&md5=b11170a19392196fc97fa42ab2f853a1CAS | 23239112PubMed |
Arias-Álvarez, M., García-García, R. M., Rebollar, P. G., Revuelta, L., Millán, P., and Lorenzo, P. L. (2009). Influence of metabolic status on oocyte quality and follicular characteristics at different postpartum periods in primiparous rabbit does. Theriogenology 72, 612–623.
| Influence of metabolic status on oocyte quality and follicular characteristics at different postpartum periods in primiparous rabbit does.Crossref | GoogleScholarGoogle Scholar | 19523677PubMed |
Arias-Álvarez, M., García-García, R. M., Rebollar, P. G., Nicodemus, N., Millán, P., Revuelta, L., and Lorenzo, P. L. (2010). Follicular, oocyte and embryo features related to metabolic status in primiparous lactating does fed with high-fibre rearing diets. Reprod. Domest. Anim. 45, e91–e100.
| 19968836PubMed |
Arias-Alvarez, M., García-García, R. M., Rebollar, P. G., Gutiérrez-Adán, A., López-Béjar, M., and Lorenzo, P. L. (2013a). Ovarian response and embryo gene expression patterns after nonsuperovulatory gonadotropin stimulation in primiparous rabbits does. Theriogenology 79, 323–330.
| Ovarian response and embryo gene expression patterns after nonsuperovulatory gonadotropin stimulation in primiparous rabbits does.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Kqs7fI&md5=07cab681c959afa772a717d6d6712fd9CAS | 23154142PubMed |
Arias-Álvarez, M., García-García, R. M., Lorenzo, P. L., Gutiérrez-Adán, A., Sakr, O. G., González-Bulnes, A., and Rebollar, P. G. (2013b). Embryo gene expression in response to maternal supplementation with glycogenic precursors in the rabbit. Anim. Reprod. Sci. 142, 173–182.
| Embryo gene expression in response to maternal supplementation with glycogenic precursors in the rabbit.Crossref | GoogleScholarGoogle Scholar | 24358512PubMed |
Assidi, M., Dufort, I., Ali, A., Hamel, M., Algriany, O., Dielemann, S., and Sirard, M. A. (2008). Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbolmyristate acetate in vitro. Biol. Reprod. 79, 209–222.
| Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbolmyristate acetate in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFWms7o%3D&md5=82a94538eafa6640c56f29b6c47d2f6aCAS | 18417710PubMed |
Assou, S., Haouzi, D., De Vos, J., and Hamamah, S. (2010). Human cumulus cells as biomarkers for embryo and pregnancy outcomes. Mol. Hum. Reprod. 16, 531–538.
| Human cumulus cells as biomarkers for embryo and pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptlegt70%3D&md5=209df48276b428999b334067c45e9ac9CAS | 20435608PubMed |
Bachvarova, R. (1985). Gene expression during oogenesis and oocyte development in mammals. Dev. Biol. (N. Y. 1985) 1, 453–524.
| 1:STN:280:DyaK3c7gsVOiuw%3D%3D&md5=3a9275dab548cc1213238f9109f3ffd3CAS |
Bavister, B. D., and Squirrell, J. M. (2000). Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 15, 189–198.
| Mitochondrial distribution and function in oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 11041524PubMed |
Bermejo-Álvarez, P., Lonergan, P., Rizos, D., and Gutiérrez-Adan, A. (2010). Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis. Reprod. Biomed. Online 20, 341–349.
| Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis.Crossref | GoogleScholarGoogle Scholar | 20093090PubMed |
Blaha, M., Nemcova, L., Kepkova, K. V., Vodicka, P., and Prochazka, R. (2015). Gene expression analysis of pig cumulus–oocyte complexes stimulated in vitro with follicle stimulating hormone or epidermal growth factor-like peptides. Reprod. Biol. Endocrinol. 13, 113.
| Gene expression analysis of pig cumulus–oocyte complexes stimulated in vitro with follicle stimulating hormone or epidermal growth factor-like peptides.Crossref | GoogleScholarGoogle Scholar | 26445099PubMed |
Boerboom, D., and Sirois, J. (1998). Molecular characterization of equine prostaglandin G/H synthase-2 and regulation of its messenger ribonucleic acid in preovulatory follicles. Endocrinology 139, 1662–1670.
| 1:CAS:528:DyaK1cXitVKmurY%3D&md5=1d218b14af7742f76edb88aefce2cfa4CAS | 9528947PubMed |
Brevini-Gandolfi, T. A., Favetta, L. A., Mauri, L., Luciano, A. M., Cillo, F., and Gandolfi, F. (1999). Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. Mol. Reprod. Dev. 52, 427–433.
| Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsl2hsrs%3D&md5=79bbbc30928a9ff7aa7a418367d6a69fCAS | 10092123PubMed |
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=52d536e64311e9f127b6ac1f26845453CAS | 2289008PubMed |
Burnik Papler, T., Vrtacnik Bokal, E., Lovrecic, L., Kopitar, A. N., and Maver, A. (2015). No specific gene expression signature in human granulosa and cumulus cells for prediction of oocyte fertilisation and embryo implantation. PLoS One 10, e0115865.
| No specific gene expression signature in human granulosa and cumulus cells for prediction of oocyte fertilisation and embryo implantation.Crossref | GoogleScholarGoogle Scholar | 25769026PubMed |
Calder, M. D., Caveney, A. N., Smith, L. C., and Watson, A. J. (2003). Responsiveness of bovine cumulus–oocyte-complexes (COC) to porcine and recombinant human FSH, and the effect of COC quality on gonadotropin receptor and Cx43 marker gene mRNAs during maturation in vitro. Reprod. Biol. Endocrinol. 1, 14–25.
| Responsiveness of bovine cumulus–oocyte-complexes (COC) to porcine and recombinant human FSH, and the effect of COC quality on gonadotropin receptor and Cx43 marker gene mRNAs during maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 12646061PubMed |
Cecconi, S., Rossi, G., Santilli, A., Stefano, L. D., Hoshino, Y., Sato, E., Palmerini, M. G., and Macchiarelli, G. (2010). Akt expression in mouse oocytes matured in vivo and in vitro. Reprod. Biomed. Online 20, 35–41.
| Akt expression in mouse oocytes matured in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFegsLjE&md5=9ca442dfb86418c9388f4f3cb60b0053CAS | 20158985PubMed |
Cho, S. J., Lee, K. L., Kim, Y. G., Kim, D. H., Yoo, J. G., Yang, B. C., Park, J. K., and Kong, I. K. (2016). Differential gene-expression profiles from canine cumulus cells of ovulated versus in vitro-matured oocytes. Reprod. Fertil. Dev. 28, 278–285.
| Differential gene-expression profiles from canine cumulus cells of ovulated versus in vitro-matured oocytes.Crossref | GoogleScholarGoogle Scholar | 25004936PubMed |
Combelles, C. M. H., Gupta, S., and Agarwal, A. (2009). Could oxidative stress influence the in vitro maturation of oocytes? Reprod. Biomed. Online 18, 864–880.
| Could oxidative stress influence the in vitro maturation of oocytes?Crossref | GoogleScholarGoogle Scholar |
Cui, X. S., Li, X. Y., Yin, X. J., Kong, I. K., Kang, J. J., and Kim, N. H. (2007). Maternal gene transcription in mouse oocytes: genes implicated in oocyte maturation and fertilization. J. Reprod. Dev. 53, 405–418.
| Maternal gene transcription in mouse oocytes: genes implicated in oocyte maturation and fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlslOjsbs%3D&md5=faeb789d18d424d2c2c644374ebe7177CAS | 17179655PubMed |
Davis, B. J., Lennard, D. E., Lee, C. A., Tiano, H. F., Morham, S. G., Wetsel, W. C., and Langenbach, R. (1999). Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta. Endocrinology 140, 2685–2695.
| 1:CAS:528:DyaK1MXjtlKhtb4%3D&md5=567da5b5a69241dccf75a5a575a1d798CAS | 10342859PubMed |
De los Reyes, M., Palomino, J., Parraguez, V. H., Hidalgo, M., and Saffie, P. (2011). Mitochondrial distribution and meiotic progression in canine oocytes during in vivo and in vitro maturation. Theriogenology 75, 346–353.
| Mitochondrial distribution and meiotic progression in canine oocytes during in vivo and in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M%2FlsFeisw%3D%3D&md5=af36b4304c36f65b271b574f4541e8c2CAS | 21074834PubMed |
Downs, S. M., Humpherson, P. G., and Leese, H. J. (1998). Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol. Reprod. 58, 1084–1094.
| Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXit1KhtL0%3D&md5=e51d09ce2950df706c5b7dd8b3036205CAS | 9546744PubMed |
Dumollard, R., Ward, Z., Carroll, J., and Duchen, M. R. (2007). Regulation of redox metabolism in the mouse oocyte and embryo. Development 134, 455–465.
| Regulation of redox metabolism in the mouse oocyte and embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlWgs7g%3D&md5=b08482cc8df9e9fa6fe473da45e01cfaCAS | 17185319PubMed |
Dumollard, R., Carroll, J., Duchen, M. R., Campbell, K., and Swann, K. (2009). Mitochondrial function and redox state in mammalian embryos. Semin. Cell Dev. Biol. 20, 346–353.
| Mitochondrial function and redox state in mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltVCmsLo%3D&md5=2168f99bda6b3e14602c9fc3ba380f6bCAS | 19530278PubMed |
Edry, I., Sela-Abramovich, S., and Dekel, N. (2006). Meiotic arrest of oocytes depends on cell-to-cell communication in the ovarian follicle. Mol. Cell. Endocrinol. 252, 102–106.
| Meiotic arrest of oocytes depends on cell-to-cell communication in the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmtlajs7c%3D&md5=ecc21ba79e449ab80ba04fbd115b2f0aCAS | 16647194PubMed |
Eppig, J. J., Chesnel, F., Hirao, Y., O’Brien, M. J., Pendola, F. L., Watanabe, S., and Wigglesworth, K. (1997). Oocyte control of granulosa cell development: how and why. Hum. Reprod. 12, 127–132.
| 1:STN:280:DyaK1c%2FpsVSmug%3D%3D&md5=1bdd1ca95051727c9571d19dd225a21cCAS | 9433969PubMed |
Feuerstein, P., Cadoret, V., Dalbies-Tran, R., Guerif, F., Bidault, R., and Royere, D. (2007). Gene expression in human cumulus cells: one approach to oocyte competence. Hum. Reprod. 22, 3069–3077.
| Gene expression in human cumulus cells: one approach to oocyte competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlKltLjP&md5=e8b8eecf896a63a8e810cce867ec116eCAS | 17951581PubMed |
Fischer, B., Chavatte-Palmer, P., Viebahn, C., Navarrete Santos, A., and Duranthon, V. (2012). Rabbit as a reproductive model for human health. Reproduction 144, 1–10.
| Rabbit as a reproductive model for human health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtV2ht7rK&md5=81aff50416a8c87485141c935745fdfaCAS | 22580370PubMed |
Foster, R., Segers, I., Smart, D., Adriaenssens, T., Smitz, J., Arce, J. C., and Princivalle, M. (2010). A differential cytokine expression profile is induced by highly purified human menopausal gonadotropin and recombinant follicle-stimulating hormone in a pre- and postovulatory mouse follicle culture model. Fertil. Steril. 93, 1464–1476.
| A differential cytokine expression profile is induced by highly purified human menopausal gonadotropin and recombinant follicle-stimulating hormone in a pre- and postovulatory mouse follicle culture model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkslyjtLg%3D&md5=a2c7e73a1ff053991f5ad96f81ed3a63CAS | 19362302PubMed |
Gendelman, M., and Roth, Z. (2012). In vivo vs. in vitro models for studying the effects of elevated temperature on the GV-stage oocyte, subsequent developmental competence and gene expression. Anim. Reprod. Sci. 134, 125–134.
| In vivo vs. in vitro models for studying the effects of elevated temperature on the GV-stage oocyte, subsequent developmental competence and gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtF2rurjM&md5=947f88b293315e6f33a656fe1049d0b6CAS | 22898494PubMed |
Gittens, J. E., and Kidder, G. M. (2005). Differential contributions of connexin37 and connexin43 to oogenesis revealed in chimeric reaggregated mouse ovaries. J. Cell Sci. 118, 5071–5078.
| Differential contributions of connexin37 and connexin43 to oogenesis revealed in chimeric reaggregated mouse ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1ynsbbO&md5=9b0f982f79029a2717aff3e13215d2a0CAS | 16254245PubMed |
Guérin, P., El Mouatassim, S., and Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–189.
| Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings.Crossref | GoogleScholarGoogle Scholar | 11284661PubMed |
Gutiérrez-Adán, A., Rizos, D., Fair, T., Moreira, P. N., Pintado, B., de la Fuente, J., Boland, M. P., and Lonergan, P. (2004). Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro. Mol. Reprod. Dev. 68, 441–448.
| Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 15236328PubMed |
Hasegawa, J., Yanaihara, A., Iwasaki, S., Mitsukawa, K., Negishi, M., and Okai, T. (2007). Reduction of connexin 43 in human cumulus cells yields good embryo competence during ICSI. J. Assist. Reprod. Genet. 24, 463–466.
| Reduction of connexin 43 in human cumulus cells yields good embryo competence during ICSI.Crossref | GoogleScholarGoogle Scholar | 17846881PubMed |
Jang, Y. J., Park, J. I., Moon, W. J., Dam, P. T., Cho, M. K., and Chun, S. Y. (2015). Cumulus cell-expressed type I interferons induce cumulus expansion in mice. Biol. Reprod. 92, 20.
| Cumulus cell-expressed type I interferons induce cumulus expansion in mice.Crossref | GoogleScholarGoogle Scholar | 25429090PubMed |
Jelíanková, L., Kubelka, M., Motlík, J., and Guerrier, P. (1994). Chromatin condensation and histone H1 kinase activity during growth and maturation of rabbits oocytes. Mol. Reprod. Dev. 37, 210–215.
| Chromatin condensation and histone H1 kinase activity during growth and maturation of rabbits oocytes.Crossref | GoogleScholarGoogle Scholar |
Jeong, Y. J., Choi, H. W., Shin, H. S., Cui, X. S., Kim, N. H., Gerton, G. L., and Jun, J. H. (2005). Optimization of real time RT-PCR methods for the analysis of gene expression in mouse eggs and preimplantation embryos. Mol. Reprod. Dev. 71, 284–289.
| Optimization of real time RT-PCR methods for the analysis of gene expression in mouse eggs and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltFyiu7c%3D&md5=5bf4762aafc1a360977adba795af91b4CAS | 15806558PubMed |
Jones, G. M., Cram, D. S., Song, B., Magli, M. C., Gianaroli, L., Lacham-Kaplan, O., Findlay, J. K., Jenkin, G., and Trounson, A. O. (2008). Gene expression profiling of human oocytes following in vivo or in vitro maturation. Hum. Reprod. 23, 1138–1144.
| Gene expression profiling of human oocytes following in vivo or in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1agsrw%3D&md5=c7b3546d63ff8d4829dca27585729664CAS | 18346995PubMed |
Kably Ambe, A., Ruiz Anguas, J., Carballo Mondragón, E., Corona de Lau, C., and Karchmerand Krivitsky, S. (2004). [Correlation between follicle levels of superoxide dismutase and oocyte quality, fertilization rates and embryo development.] Ginecol. Obstet. Mex. 72, 335–344.
| 15469172PubMed |
Kalous, J., Solc, P., Baran, V., Kubelka, M., Schultz, R. M., and Motlik, J. (2006). PKB/AKT is involved in resumption of meiosis in mouse oocytes. Biol. Cell 98, 111–123.
| PKB/AKT is involved in resumption of meiosis in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlOrsg%3D%3D&md5=3879062571277b00e9f939c3a9188811CAS | 15842198PubMed |
Kang, J. T., Atikuzzaman, M., Kwon, D. K., Park, S. J., Kim, S. J., Moon, J. H., Koo, O. J., Jang, G., and Lee, B. C. (2012). Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations. Zygote 20, 1–8.
| Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1arug%3D%3D&md5=57ce80ab1a5e168d7f9c34ca1c783e0aCAS | 21791162PubMed |
Kimura, N., Hoshino, Y., Totsukawa, K., and Sato, E. (2007). Cellular and molecular events during oocyte maturation in mammals: molecules of cumulus–oocyte complex matrix and signalling pathways regulating meiotic progression. Soc. Reprod. Fertil. Suppl. 63, 327–342.
| 1:CAS:528:DC%2BD1cXpvVyktb4%3D&md5=fd59f52dbea8721cfbc9cfe8322bc478CAS | 17566282PubMed |
Kohata, C., Izquierdo-Rico, M. J., Romar, R., and Funahashi, H. (2013). Development competence and relative transcript abundance of oocytes derived from small and medium follicles of prepubertal gilts. Theriogenology 80, 970–978.
| Development competence and relative transcript abundance of oocytes derived from small and medium follicles of prepubertal gilts.Crossref | GoogleScholarGoogle Scholar | 23987988PubMed |
Lee, K. S., Joo, B. S., Na, Y. J., Yoon, M. S., Choi, O. H., and Kim, W. W. (2001). Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET. J. Assist. Reprod. Genet. 18, 490–498.
| Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrmsVKisQ%3D%3D&md5=e301c352d384991b47a198c74c0a46eaCAS | 11665664PubMed |
Li, S. H., Lin, M. H., Hwu, Y. M., Lu, C. H., Yeh, L. Y., Chen, Y. J., and Lee, R. K. (2015). Correlation of cumulus gene expression of GJA1, PRSS35, PTX3, and SERPINE2 with oocyte maturation, fertilization, and embryo development. Reprod. Biol. Endocrinol. 13, 93.
| Correlation of cumulus gene expression of GJA1, PRSS35, PTX3, and SERPINE2 with oocyte maturation, fertilization, and embryo development.Crossref | GoogleScholarGoogle Scholar | 26276571PubMed |
Liu, S., Li, Y., Gao, X., Yan, J.-H., and Chen, Z.-J. (2010). Changes in the distribution of mitochondria before and after in vitro maturation of human oocytes and the effect of in vitro maturation on mitochondria distribution. Fertil. Steril. 93, 1550–1555.
| Changes in the distribution of mitochondria before and after in vitro maturation of human oocytes and the effect of in vitro maturation on mitochondria distribution.Crossref | GoogleScholarGoogle Scholar | 19423101PubMed |
Lonergan, P., Khatir, H., Piumi, F., Rieger, D., Humblot, P., and Boland, M. P. (1999). Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos. J. Reprod. Fertil. 117, 159–167.
| Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlaltLo%3D&md5=a386395cd34ae93f9a5d3c8653f8a7e9CAS | 10645257PubMed |
Lord, C. E., Dauphinee, A. N., Watts, R. L., and Gunawardena, A. H. (2013). Unveiling interactions among mitochondria, caspase-like proteases, and the actin cytoskeleton during plant programmed cell death (PCD). PLoS One 8, e57110.
| Unveiling interactions among mitochondria, caspase-like proteases, and the actin cytoskeleton during plant programmed cell death (PCD).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktlSqtLw%3D&md5=4e3e5546eadc19584abe1f73bcec8c6aCAS | 23483897PubMed |
Lorenzo, P. L., Rebollar, P. G., Illera, M. J., Illera, J. C., Illera, M., and Alvariño, J. M. (1996). Stimulatory effect of insulin-like growth factor I and epidermal growth factor on the maturation of rabbit oocytes in vitro. J. Reprod. Fertil. 107, 109–117.
| Stimulatory effect of insulin-like growth factor I and epidermal growth factor on the maturation of rabbit oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK283ntlertA%3D%3D&md5=a896506c1ae80b2596becf5da6a8f9bcCAS | 8699422PubMed |
Maître, B., Jornot, L., and Junod, A. F. (1993). Effects of inhibition of catalase and superoxide dismutase activity on antioxidant enzyme mRNA levels. Am. J. Physiol. 265, L636–L643.
| 8279580PubMed |
McKenzie, L. J., Pangas, S. A., Carson, S. A., Kovanci, E., Cisneros, P., Buster, J. E., Amato, P., and Matzuk, M. M. (2004). Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum. Reprod. 19, 2869–2874.
| Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2crotVyisA%3D%3D&md5=35f3308ea5a9e2fc4f55c70c84c6e06cCAS | 15471935PubMed |
Nazmara, Z., Salehnia, M., and HosseinKhani, S. (2014). Mitochondrial distribution and ATP content of vitrified, in vitro matured mouse oocytes. Avicenna J. Med. Biotechnol. 6, 210–217.
| 25414783PubMed |
Nivet, A. L., Vigneault, C., Blondin, P., and Sirard, M. A. (2013). Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine. Reproduction 145, 555–565.
| Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVWmsbnJ&md5=7dca1a8711cd5df006a7bed6515d7179CAS | 23564726PubMed |
Nuttinck, F., Reinaud, P., Tricoire, H., Vigneron, C., Peynot, N., Mialot, J. P., Mermillod, P., and Charpigny, G. (2002). Cyclooxygenase-2 is expressed by cumulus cells during oocyte maturation in cattle. Mol. Reprod. Dev. 61, 93–101.
| Cyclooxygenase-2 is expressed by cumulus cells during oocyte maturation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptVejuro%3D&md5=e2e4f3b6df54334145f38ac78aca7c54CAS | 11774380PubMed |
Ouandaogo, Z. G., Frydman, N., Hesters, L., Assou, S., Haouzi, D., Dechaud, H., Frydman, R., and Hamamah, S. (2012). Differences in transcriptomic profiles of human cumulus cells isolated from oocytes at GV, MI and MII stages after in vivo and in vitro oocyte maturation. Hum. Reprod. 27, 2438–2447.
| Differences in transcriptomic profiles of human cumulus cells isolated from oocytes at GV, MI and MII stages after in vivo and in vitro oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFantrfJ&md5=9fe658110b48cac8deacaea567d952f1CAS | 22617121PubMed |
Paynton, B. V., and Bachvarova, R. (1994). Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse. Mol. Reprod. Dev. 37, 172–180.
| Polyadenylation and deadenylation of maternal mRNAs during oocyte growth and maturation in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlt1Kksb0%3D&md5=491089997d4ed2d87ca876802686b811CAS | 7910030PubMed |
Rizos, D., Clemente, M., Bermejo-Alvarez, P., de La Fuente, J., Lonergan, P., and Gutiérrez-Adán, A. (2008). Consequences of in vitro culture conditions on embryo development and quality. Reprod. Domest. Anim. 43, 44–50.
| Consequences of in vitro culture conditions on embryo development and quality.Crossref | GoogleScholarGoogle Scholar | 18803756PubMed |
Schmittgen, T. D., and Livak, K. J. (2008). Analysing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101–1108.
| Analysing real-time PCR data by the comparative C(T) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVemt7c%3D&md5=c9af4cd1fb90fdc7f3a7e145ccaafe84CAS | 18546601PubMed |
Shao, L., Chian, R. C., Xu, Y., Yan, Z., Zhang, Y., Gao, C., Gao, L., Liu, J., and Cui, Y. (2015). Genomic expression profiles in cumulus cells derived from germinal vesicle and MII mouse oocytes. Reprod. Fertil. Dev. , .
| Genomic expression profiles in cumulus cells derived from germinal vesicle and MII mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 25989843PubMed |
Sirard, M. A. (2001). Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–1254.
| Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSisr0%3D&md5=62dbd41536109a614fa23ff1a4d2a6e2CAS | 11327682PubMed |
Smitz, J., Andersen, A. N., Devroey, P., and Arce, J. C. (2007). Endocrine profile in serum and follicular fluid differs after ovarian stimulation with HP-hMG or recombinant FSH in IVF patients. Hum. Reprod. 22, 676–687.
| Endocrine profile in serum and follicular fluid differs after ovarian stimulation with HP-hMG or recombinant FSH in IVF patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVCqsbo%3D&md5=373e5272ca066e8a843f51cc1a52bbddCAS | 17110397PubMed |
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=3faf9abcc57c7bc8b4b76b3cd340653aCAS | 11207207PubMed |
Sun, Q. Y., Wu, G. M., Lai, L., Park, K. W., Cabot, R., Cheong, H. T., Day, B. N., Prather, R. S., and Schatten, H. (2001). Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155–163.
| Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis7g%3D&md5=304f8053916c1ac5ad3509a46f2799faCAS | 11425340PubMed |
Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–695.
| The pivotal role of glucose metabolism in determining oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltFajtr0%3D&md5=c465b83355bc254d53da580f2c639bcbCAS | 20089664PubMed |
Tesfaye, D., Ghanem, N., Carter, F., Fair, T., Sirard, M. A., Hoelker, M., Schellander, K., and Lonergan, P. (2009). Gene expression profile of cumulus cells derived from cumulus–oocyte complexes matured either in vivo or in vitro. Reprod. Fertil. Dev. 21, 451–461.
| Gene expression profile of cumulus cells derived from cumulus–oocyte complexes matured either in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFemsb8%3D&md5=9975f8c175358885b38e3ca969ea55fdCAS | 19261222PubMed |
Thouas, G. A., Trounson, A. O., Wolvetang, E. J., and Jones, G. M. (2004). Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol. Reprod. 71, 1936–1942.
| Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsr3O&md5=b0e71189515ac685532ab662885d968eCAS | 15286028PubMed |
Torner, H., Brüsow, K., Alm, H., Ratky, J., Pöhland, R., Tuchscherer, A., and Kamitz, W. (2004). Mitochondrial aggregation patterns and activation in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation. Theriogenology 61, 1675–1689.
| Mitochondrial aggregation patterns and activation in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslWnu70%3D&md5=82c9d2574d1b30ffaa8300e543060e1eCAS | 15019463PubMed |
Torner, H., Alm, H., Kanitz, W., Goellnitz, K., Becker, F., Poehland, R., Bruessow, K. P., and Tuchscherer, A. (2007). Effect of initial cumulus morphology on meiotic dynamic and status of mitochondria in horse oocytes during IVM. Reprod. Domest. Anim. 42, 176–183.
| Effect of initial cumulus morphology on meiotic dynamic and status of mitochondria in horse oocytes during IVM.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7kvF2qsw%3D%3D&md5=e54faa62b9759e2c68a2a52f05062ee8CAS | 17348975PubMed |
Tsutsumi, O., Satoh, K., Taketani, Y., and Kato, T. (1992). Determination of enzyme activities of energy metabolism in the maturing rat oocyte. Mol. Reprod. Dev. 33, 333–337.
| Determination of enzyme activities of energy metabolism in the maturing rat oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhsVChsb4%3D&md5=2e498d96812a0638d066b468cad72d6dCAS | 1449800PubMed |
Urner, F., and Sakkas, D. (1999). Characterization of glycolysis and pentose phosphate pathway activity during sperm entry into the mouse oocyte. Biol. Reprod. 60, 973–978.
| Characterization of glycolysis and pentose phosphate pathway activity during sperm entry into the mouse oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitVGqtLc%3D&md5=83bdd6f38f2387901c908cc858e8a3f2CAS | 10084974PubMed |
Van Blerkom, J. (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.
| Mitochondrial function in the human oocyte and embryo and their role in developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWrsrzM&md5=e79f56d1afcd71cadf1251b829ae64aaCAS | 20933103PubMed |
Viudes-de-Castro, M. P., Moce, E., Vicente, J. S., Marco-Jimenez, S., and Lavara, R. (2005). In vitro evaluation of in vivo fertilizing ability of frozen rabbit semen. Reprod. Domest. Anim. 40, 136–140.
| In vitro evaluation of in vivo fertilizing ability of frozen rabbit semen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M7ovVGqsQ%3D%3D&md5=1de7ddde5a38949f11f917812918e59bCAS | 15819963PubMed |
Wang, H. L., Sui, H. S., Liu, Y., Miao, D. Q., Lu, J. H., Liang, B., and Tan, J. H. (2009). Dynamic changes of germinal vesicle chromatin configuration and transcriptional activity during maturation of rabbit follicles. Fertil. Steril. 91, 1589–1594.
| Dynamic changes of germinal vesicle chromatin configuration and transcriptional activity during maturation of rabbit follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsF2ns70%3D&md5=a6c66f30334b5f73380db5d5b90a439cCAS | 19100534PubMed |
Wang, L., Lin, J., Huang, J., Wang, J., Zhao, Y., and Chen, T. (2012). Selection of ovine oocytes by brilliant cresyl blue staining. J. Biomed. Biotechnol. 2012, 161372.
| Selection of ovine oocytes by brilliant cresyl blue staining.Crossref | GoogleScholarGoogle Scholar | 22675245PubMed |
Wathlet, S., Adriaenssens, T., Segers, I., Verheyen, G., Van de Velde, H., Coucke, W., Ron El, R., Devroey, P., and Smitz, J. (2011). Cumulus cell gene expression predicts better cleavage-stage embryo or blastocyst development and pregnancy for ICSI patients. Hum. Reprod. 26, 1035–1051.
| Cumulus cell gene expression predicts better cleavage-stage embryo or blastocyst development and pregnancy for ICSI patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlehtrg%3D&md5=770fd895ff0adc916d84ad0da4c75dcaCAS | 21372047PubMed |
Wilding, M., Dale, B., Marino, M., di Matteo, L., Alviggi, C., Pisaturo, M. L., Lombardi, L., and De Placido, G. (2001). Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16, 909–917.
| Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvitlCktw%3D%3D&md5=228bf47a7e429ffe2b4f7914389ca64bCAS | 11331637PubMed |
Yu, Y., Dumollard, R., Rossbach, A., Lai, F., and Swann, K. (2010). Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J. Cell. Physiol. 224, 672–680.
| Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosVWntLo%3D&md5=85ab1d137585a73c2210003a26670fc1CAS | 20578238PubMed |
Yuan, Y., Hao, Z. D., Liu, J., Wu, Y., Yang, L., Liu, G. S., Tian, J. H., Zhu, S. E., and Zeng, S. M. (2008). Heat shock at the germinal vesicle breakdown stage induces apoptosis in surrounding cumulus cells and reduces maturation rates of porcine oocytes in vitro. Theriogenology 70, 168–178.
| Heat shock at the germinal vesicle breakdown stage induces apoptosis in surrounding cumulus cells and reduces maturation rates of porcine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1Ois7s%3D&md5=5169b289f1849a63a03b53899243f878CAS | 18448159PubMed |
Zeng, S. M., Zhu, S. E., Wang, Y. S., Chen, X. J., Zhang, Z. C., and Chen, Y. F. (1999). An efficient method for in vitro fertilization in rabbits. Anim. Biotechnol. 10, 15–23.
| An efficient method for in vitro fertilization in rabbits.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7hvVGrug%3D%3D&md5=3214d96de8acac1aaa1668e9ca59d870CAS | 10654427PubMed |
Zheng, P., Patel, B., McMenamin, M., Moran, E., Paprocki, A. M., Kihara, M., Schramm, R. D., and Latham, K. E. (2005a). Effects of follicle size and oocyte maturation conditions on maternal messenger RNA regulation and gene expression in rhesus monkey oocytes and embryos. Biol. Reprod. 72, 890–897.
| Effects of follicle size and oocyte maturation conditions on maternal messenger RNA regulation and gene expression in rhesus monkey oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis12hs7s%3D&md5=0108e8078e4688a012a0c708c75fc7e8CAS | 15590902PubMed |
Zheng, P., Schramm, R. D., and Latham, K. E. (2005b). Developmental regulation and in vitro culture effects on expression of DNA repair and cell cycle checkpoint control genes in rhesus monkey oocytes and embryos. Biol. Reprod. 72, 1359–1369.
| Developmental regulation and in vitro culture effects on expression of DNA repair and cell cycle checkpoint control genes in rhesus monkey oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksFGqsLY%3D&md5=942c90bbb1d10f08d08bdc7b6c073cfeCAS | 15703371PubMed |
Zhuang, X.-J., Huang, Y., Duan, Y.-P., Zhang, M., Lu, Y.-Q., and Lu, K.-H. (2012). Translocation of active mitochondria during buffalo (Bubalus bubalis) oocytes in vitro maturation, fertilization and preimplantation embryo development. Reprod. Domest. Anim. 47, 443–448.
| Translocation of active mitochondria during buffalo (Bubalus bubalis) oocytes in vitro maturation, fertilization and preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar | 21950622PubMed |