A prematuration approach to equine IVM: considering cumulus morphology, seasonality, follicle of origin, gap junction coupling and large-scale chromatin configuration in the germinal vesicle
Valentina Lodde A , Silvia Colleoni B , Irene Tessaro A , Davide Corbani A , Giovanna Lazzari B C , Alberto M. Luciano A , Cesare Galli B C and Federica Franciosi
A D
+ Author Affiliations
- Author Affiliations
A Dipartimento di Scienze Veterinarie per la Salute la Produzione Animale e la Sicurezza Alimentare ‘Carlo Cantoni’, Reproductive and Developmental Biology Lab, Università degli Studi di Milano, via Celoria, 10 20133 Milano, Italy.
B Laboratory of Reproductive Technologies, Avantea, Cremona, Via Porcellasco, 7f 26100 Cremona, Italy.
C Fondazione Avantea, Via Porcellasco, 7f 26100 Cremona, Italy.
D Corresponding author. Email: federica.franciosi1@unimi.it
Reproduction, Fertility and Development 31(12) 1793-1804 https://doi.org/10.1071/RD19230
Submitted: 18 June 2019 Accepted: 13 September 2019 Published: 21 October 2019
Abstract
Several studies report that a two-step culture where mammalian oocytes are first kept under meiosis-arresting conditions (prematuration) followed by IVM is beneficial to embryo development. The most promising results were obtained by stratifying the oocyte population using morphological criteria and allocating them to different culture conditions to best meet their metabolic needs. In this study, horse oocytes were characterised to identify subpopulations that may benefit from prematuration. We investigated gap-junction (GJ) coupling, large-scale chromatin configuration and meiotic competence in compact and expanded cumulus–oocyte complexes (COCs) according to follicle size (<1, 1–2, >2 cm) and season. Then we tested the effect of cilostamide-based prematuration in compact COCs collected from follicles <1 and 1–2 cm in diameter on embryo development. Meiotic competence was not affected by prematuration, whereas COCs from follicles 1–2 cm in diameter yielded embryos with a higher number of cells per blastocyst than oocytes that underwent direct IVM (P < 0.01, unpaired Mann–Whitney test), suggesting improved developmental competence. Oocytes collected from follicles <1 cm in diameter were not affected by prematuration. This study represents an extensive characterisation of the functional properties of immature horse oocytes and is the first report of the effects of cilostamide-based prematuration in horse oocyte IVM on embryo development.
Additional keywords: assisted reproduction, blastocyst, developmental competence, intracytoplasmic sperm injection (ICSI), oocyte maturation.
References
Abdel-Ghani, M. A., Sakaguchi, K., Kanno, C., Yanagawa, Y., Katagiri, S., and Nagano, M. (2018). Effects of pre-maturational culture duration on developmental competence of bovine small-sized oocytes. J. Reprod. Dev. 64, 365–369.| Effects of pre-maturational culture duration on developmental competence of bovine small-sized oocytes.Crossref | GoogleScholarGoogle Scholar | 29798966PubMed |
Adona, P. R., Pires, P. R., Quetglas, M. D., Schwarz, K. R., and Leal, C. L. (2008a). Nuclear maturation kinetics and in vitro embryo development of cattle oocytes prematured with butyrolactone I combined or not combined with roscovitine. Anim. Reprod. Sci. 104, 389–397.
| Nuclear maturation kinetics and in vitro embryo development of cattle oocytes prematured with butyrolactone I combined or not combined with roscovitine.Crossref | GoogleScholarGoogle Scholar | 17644285PubMed |
Adona, P. R., Pires, P. R., Quetglas, M. D., Schwarz, K. R., and Leal, C. L. (2008b). Prematuration of bovine oocytes with butyrolactone I: effects on meiosis progression, cytoskeleton, organelle distribution and embryo development. Anim. Reprod. Sci. 108, 49–65.
| Prematuration of bovine oocytes with butyrolactone I: effects on meiosis progression, cytoskeleton, organelle distribution and embryo development.Crossref | GoogleScholarGoogle Scholar | 17692479PubMed |
Albuz, F. K., Sasseville, M., Lane, M., Armstrong, D. T., Thompson, J. G., and Gilchrist, R. B. (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum. Reprod. 25, 2999–3011.
| Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 20870682PubMed |
Alm, H., and Hinrichs, K. (1996). Effect of cycloheximide on nuclear maturation of horse oocytes and its relation to initial cumulus morphology. J. Reprod. Fertil. 107, 215–220.
| Effect of cycloheximide on nuclear maturation of horse oocytes and its relation to initial cumulus morphology.Crossref | GoogleScholarGoogle Scholar | 8882287PubMed |
Alm, H., Torner, H., Kanitz, W., Becker, F., and Hinrichs, K. (1997). Comparison of different methods for the recovery of horse oocytes. Equine Vet. J. Suppl. 25, 47–50.
Azari-Dolatabad, N., Rahmani, H. R., Hajian, M., Ostadhosseini, S., Hosseini, S. M., and Nasr-Esfahani, M. H. (2016). Effects of cilostamide and/or forskolin on the meiotic resumption and development competence of growing ovine oocytes selected by brilliant cresyl blue staining. Theriogenology 85, 1483–1490.
| Effects of cilostamide and/or forskolin on the meiotic resumption and development competence of growing ovine oocytes selected by brilliant cresyl blue staining.Crossref | GoogleScholarGoogle Scholar | 26879998PubMed |
Barretto, L. S. S., Castro, V. S., Garcia, J. M., and Mingoti, G. Z. (2011). Meiotic inhibition of bovine oocytes in medium supplemented with a serum replacer and hormones: effects on meiosis progression and developmental capacity. Zygote 19, 107–116.
| Meiotic inhibition of bovine oocytes in medium supplemented with a serum replacer and hormones: effects on meiosis progression and developmental capacity.Crossref | GoogleScholarGoogle Scholar |
Choi, Y. H., Love, L. B., Varner, D. D., and Hinrichs, K. (2004). Factors affecting developmental competence of equine oocytes after intracytoplasmic sperm injection. Reproduction 127, 187–194.
| Factors affecting developmental competence of equine oocytes after intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 15056784PubMed |
Choi, Y. H., Love, L. B., Varner, D. D., and Hinrichs, K. (2006a). Blastocyst development in equine oocytes with low meiotic competence after suppression of meiosis with roscovitine prior to in vitro maturation. Zygote 14, 1–8.
| Blastocyst development in equine oocytes with low meiotic competence after suppression of meiosis with roscovitine prior to in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 16700969PubMed |
Choi, Y. H., Love, L. B., Varner, D. D., and Hinrichs, K. (2006b). Holding immature equine oocytes in the absence of meiotic inhibitors: effect on germinal vesicle chromatin and blastocyst development after intracytoplasmic sperm injection. Theriogenology 66, 955–963.
| Holding immature equine oocytes in the absence of meiotic inhibitors: effect on germinal vesicle chromatin and blastocyst development after intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 16574209PubMed |
Choi, Y. H., Love, L. B., Varner, D. D., and Hinrichs, K. (2007). Effect of holding technique and culture drop size in individual or group culture on blastocyst development after ICSI of equine oocytes with low meiotic competence. Anim. Reprod. Sci. 102, 38–47.
| Effect of holding technique and culture drop size in individual or group culture on blastocyst development after ICSI of equine oocytes with low meiotic competence.Crossref | GoogleScholarGoogle Scholar | 17088030PubMed |
Colleoni, S., Luciano, A. M., and Gandolfi, F. (2004). Cumulus–oocyte communications in the horse: role of the breeding season and of the maturation medium. Reprod. Domest. Anim. 39, 70–75.
| Cumulus–oocyte communications in the horse: role of the breeding season and of the maturation medium.Crossref | GoogleScholarGoogle Scholar | 15065986PubMed |
Colonna, R., and Mangia, F. (1983). Mechanisms of amino acid uptake in cumulus-enclosed mouse oocytes. Biol. Reprod. 28, 797–803.
| Mechanisms of amino acid uptake in cumulus-enclosed mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 6860738PubMed |
Conti, M., Andersen, C. B., Richard, F. J., Shitsukawa, K., and Tsafriri, A. (1998). Role of cyclic nucleotide phosphodiesterases in resumption of meiosis. Mol. Cell. Endocrinol. 145, 9–14.
| Role of cyclic nucleotide phosphodiesterases in resumption of meiosis.Crossref | GoogleScholarGoogle Scholar | 9922093PubMed |
Conti, M., Hsieh, M., Zamah, A. M., and Oh, J. S. (2012). Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol. Cell. Endocrinol. 356, 65–73.
| Novel signaling mechanisms in the ovary during oocyte maturation and ovulation.Crossref | GoogleScholarGoogle Scholar | 22101318PubMed |
Dell’Aquila, M. E., Albrizio, M., Guaricci, A. C., De Santis, T., Maritato, F., Tremoleda, J. L., Colenbrander, B., Guerra, L., Casavola, V., and Minoia, P. (2008). Expression and localization of the mu-opioid receptor (MOR) in the equine cumulus–oocyte complex and its involvement in the seasonal regulation of oocyte meiotic competence. Mol. Reprod. Dev. 75, 1229–1246.
| Expression and localization of the mu-opioid receptor (MOR) in the equine cumulus–oocyte complex and its involvement in the seasonal regulation of oocyte meiotic competence.Crossref | GoogleScholarGoogle Scholar | 18213645PubMed |
Diaw, M., Salgado, R. M., Canesin, H. S., Gridley, N., and Hinrichs, K. (2018). Effect of different shipping temperatures (~22°C vs. ~7°C) and holding media on blastocyst development after overnight holding of immature equine cumulus–oocyte complexes. Theriogenology 111, 62–68.
| Effect of different shipping temperatures (~22°C vs. ~7°C) and holding media on blastocyst development after overnight holding of immature equine cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 29428846PubMed |
Dieci, C., Lodde, V., Franciosi, F., Lagutina, I., Tessaro, I., Modina, S. C., Albertini, D. F., Lazzari, G., Galli, C., and Luciano, A. M. (2013). The effect of cilostamide on gap junction communication dynamics, chromatin remodeling, and competence acquisition in pig oocytes following parthenogenetic activation and nuclear transfer. Biol. Reprod. 89, 68.
| The effect of cilostamide on gap junction communication dynamics, chromatin remodeling, and competence acquisition in pig oocytes following parthenogenetic activation and nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 23926281PubMed |
Dieci, C., Lodde, V., Labreque, R., Dufort, I., Tessaro, I., Sirard, M. A., and Luciano, A. M. (2016). Differences in cumulus cell gene expression indicate the benefit of a pre-maturation step to improve in-vitro bovine embryo production. Mol. Hum. Reprod. 22, 882–897.
| 27559149PubMed |
Dieleman, S. J., Hendriksen, P. J., Viuff, D., Thomsen, P. D., Hyttel, P., Knijn, H. M., Wrenzycki, C., Kruip, T. A., Niemann, H., Gadella, B. M., Bevers, M. M., and Vos, P. L. (2002). Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos. Theriogenology 57, 5–20.
| Effects of in vivo prematuration and in vivo final maturation on developmental capacity and quality of pre-implantation embryos.Crossref | GoogleScholarGoogle Scholar | 11775980PubMed |
Dini, P., Bogado Pascottini, O., Ducheyne, K., Hostens, M., and Daels, P. (2016). Holding equine oocytes in a commercial embryo-holding medium: new perspective on holding temperature and maturation time. Theriogenology 86, 1361–1368.
| Holding equine oocytes in a commercial embryo-holding medium: new perspective on holding temperature and maturation time.Crossref | GoogleScholarGoogle Scholar | 27268297PubMed |
Eppig, J. J. (1996). Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod. Fertil. Dev. 8, 485–489.
| Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals.Crossref | GoogleScholarGoogle Scholar | 8870074PubMed |
Ferreira, E. M., Vireque, A. A., Adona, P. R., Ferriani, R. A., and Navarro, P. A. (2009). Prematuration of bovine oocytes with butyrolactone I reversibly arrests meiosis without increasing meiotic abnormalities after in vitro maturation. Eur. J. Obstet. Gynecol. Reprod. Biol. 145, 76–80.
| Prematuration of bovine oocytes with butyrolactone I reversibly arrests meiosis without increasing meiotic abnormalities after in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 19403233PubMed |
Foss, R., Ortis, H., and Hinrichs, K. (2013). Effect of potential oocyte transport protocols on blastocyst rates after intracytoplasmic sperm injection in the horse. Equine Vet. J. Suppl. 45, 39–43.
| Effect of potential oocyte transport protocols on blastocyst rates after intracytoplasmic sperm injection in the horse.Crossref | GoogleScholarGoogle Scholar |
Franciosi, F., Lodde, V., Goudet, G., Duchamp, G., Deleuze, S., Douet, C., Tessaro, I., and Luciano, A. M. (2012). Changes in histone H4 acetylation during in vivo versus in vitro maturation of equine oocytes. Mol. Hum. Reprod. 18, 243–252.
| Changes in histone H4 acetylation during in vivo versus in vitro maturation of equine oocytes.Crossref | GoogleScholarGoogle Scholar | 22155671PubMed |
Franciosi, F., Coticchio, G., Lodde, V., Tessaro, I., Modina, S. C., Fadini, R., Dal Canto, M., Renzini, M. M., Albertini, D. F., and Luciano, A. M. (2014). Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol. Reprod. 91, 61.
| Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes.Crossref | GoogleScholarGoogle Scholar | 25078681PubMed |
Franz, L. C., Choi, Y. H., Squires, E. L., Seidel, G. E., and Hinrichs, K. (2003). Effects of roscovitine on maintenance of the germinal vesicle in horse oocytes, subsequent nuclear maturation, and cleavage rates after intracytoplasmic sperm injection. Reproduction 125, 693–700.
| Effects of roscovitine on maintenance of the germinal vesicle in horse oocytes, subsequent nuclear maturation, and cleavage rates after intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 12713432PubMed |
Galli, C., Colleoni, S., Turini, P., Crotti, G., Dieci, C., Lodde, V., Luciano, A. M., and Lazzari, G. (2014). Holding equine oocytes at room temperature for 18 hours prior to in vitro maturation maintains their developmental competence. J. Equine Vet. Sci. 34, 174–175.
| Holding equine oocytes at room temperature for 18 hours prior to in vitro maturation maintains their developmental competence.Crossref | GoogleScholarGoogle Scholar |
García-Roselló, E., Coy, P., Garcia Vazquez, F. A., Ruiz, S., and Matas, C. (2006). Analysis of different factors influencing the intracytoplasmic sperm injection (ICSI) yield in pigs. Theriogenology 66, 1857–1865.
| Analysis of different factors influencing the intracytoplasmic sperm injection (ICSI) yield in pigs.Crossref | GoogleScholarGoogle Scholar | 16769105PubMed |
Gharibi, S., Hajian, M., Ostadhosseini, S., Hosseini, S. M., Forouzanfar, M., and Nasr-Esfahani, M. H. (2013). Effect of phosphodiesterase type 3 inhibitor on nuclear maturation and in vitro development of ovine oocytes. Theriogenology 80, 302–312.
| Effect of phosphodiesterase type 3 inhibitor on nuclear maturation and in vitro development of ovine oocytes.Crossref | GoogleScholarGoogle Scholar | 23683693PubMed |
Gilchrist, R. B., Luciano, A. M., Richani, D., Zeng, H. T., Wang, X., Vos, M. D., Sugimura, S., Smitz, J., Richard, F. J., and Thompson, J. G. (2016). Oocyte maturation and quality: role of cyclic nucleotides. Reproduction 152, R143–R157.
| Oocyte maturation and quality: role of cyclic nucleotides.Crossref | GoogleScholarGoogle Scholar | 27422885PubMed |
Gilula, N. B., Epstein, M. L., and Beers, W. H. (1978). Cell-to-cell communication and ovulation. A study of the cumulus–oocyte complex. J. Cell Biol. 78, 58–75.
| Cell-to-cell communication and ovulation. A study of the cumulus–oocyte complex.Crossref | GoogleScholarGoogle Scholar | 670298PubMed |
Guemra, S., da Silva Santo, E., Zanin, R., Monzani, P. S., Sovernigo, T. C., Ohashi, O. M., Verde Leal, C. L., and Adona, P. R. (2014). Effect of temporary meiosis block during prematuration of bovine cumulus–oocyte complexes on pregnancy rates in a commercial setting for in vitro embryo production. Theriogenology 81, 982–987.
| Effect of temporary meiosis block during prematuration of bovine cumulus–oocyte complexes on pregnancy rates in a commercial setting for in vitro embryo production.Crossref | GoogleScholarGoogle Scholar | 24576716PubMed |
Hendriksen, P. J., Vos, P. L., Steenweg, W. N., Bevers, M. M., and Dieleman, S. J. (2000). Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology 53, 11–20.
| Bovine follicular development and its effect on the in vitro competence of oocytes.Crossref | GoogleScholarGoogle Scholar | 10735058PubMed |
Hinrichs, K. (2010). The equine oocyte: factors affecting meiotic and developmental competence. Mol. Reprod. Dev. 77, 651–661.
| The equine oocyte: factors affecting meiotic and developmental competence.Crossref | GoogleScholarGoogle Scholar | 20652997PubMed |
Hinrichs, K. (2018). Assisted reproductive techniques in mares. Reprod. Domest. Anim. 53, 4–13.
| Assisted reproductive techniques in mares.Crossref | GoogleScholarGoogle Scholar | 30238661PubMed |
Hinrichs, K., and Schmidt, A. L. (2000). Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season. Biol. Reprod. 62, 1402–1408.
| Meiotic competence in horse oocytes: interactions among chromatin configuration, follicle size, cumulus morphology, and season.Crossref | GoogleScholarGoogle Scholar | 10775193PubMed |
Hinrichs, K., Choi, Y. H., Norris, J. D., Love, L. B., Bedford-Guaus, S. J., Hartman, D. L., and Velez, I. C. (2012). Evaluation of foal production following intracytoplasmic sperm injection and blastocyst culture of oocytes from ovaries collected immediately before euthanasia or after death of mares under field conditions. J. Am. Vet. Med. Assoc. 241, 1070–1074.
| Evaluation of foal production following intracytoplasmic sperm injection and blastocyst culture of oocytes from ovaries collected immediately before euthanasia or after death of mares under field conditions.Crossref | GoogleScholarGoogle Scholar | 23039983PubMed |
Huang, W., Nagano, M., Kang, S. S., Yanagawa, Y., and Takahashi, Y. (2013). Effects of in vitro growth culture duration and prematuration culture on maturational and developmental competences of bovine oocytes derived from early antral follicles. Theriogenology 80, 793–799.
| Effects of in vitro growth culture duration and prematuration culture on maturational and developmental competences of bovine oocytes derived from early antral follicles.Crossref | GoogleScholarGoogle Scholar | 23953693PubMed |
Huang, W., Nagano, M., Kang, S. S., Yanagawa, Y., and Takahashi, Y. (2014). Prematurational culture with 3-isobutyl-1-methylxanthine synchronizes meiotic progression of the germinal vesicle stage and improves nuclear maturation and embryonic development in in vitro-grown bovine oocytes. J. Reprod. Dev. 60, 9–13.
| Prematurational culture with 3-isobutyl-1-methylxanthine synchronizes meiotic progression of the germinal vesicle stage and improves nuclear maturation and embryonic development in in vitro-grown bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 24212477PubMed |
Huang, W., Kang, S. S., Nagai, K., Yanagawa, Y., Takahashi, Y., and Nagano, M. (2016). Mitochondrial activity during pre-maturational culture in in vitro-grown bovine oocytes is related to maturational and developmental competences. Reprod. Fertil. Dev. 28, 349–356.
| Mitochondrial activity during pre-maturational culture in in vitro-grown bovine oocytes is related to maturational and developmental competences.Crossref | GoogleScholarGoogle Scholar | 25029376PubMed |
Hyttel, P., Fair, T., Callesen, H., and Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.
| Oocyte growth, capacitation and final maturation in cattle.Crossref | GoogleScholarGoogle Scholar |
Lazzari, G., Wrenzycki, C., Herrmann, D., Duchi, R., Kruip, T., Niemann, H., and Galli, C. (2002). Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol. Reprod. 67, 767–775.
| Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome.Crossref | GoogleScholarGoogle Scholar | 12193383PubMed |
Leroy, J. L., Van Hoeck, V., Clemente, M., Rizos, D., Gutierrez-Adan, A., Van Soom, A., Uytterhoeven, M., and Bols, P. E. (2010). The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality. Hum. Reprod. 25, 768–778.
| The effect of nutritionally induced hyperlipidaemia on in vitro bovine embryo quality.Crossref | GoogleScholarGoogle Scholar | 20007613PubMed |
Li, H. J., Sutton-McDowall, M. L., Wang, X., Sugimura, S., Thompson, J. G., and Gilchrist, R. B. (2016a). Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Hum. Reprod. 31, 810–821.
| Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions.Crossref | GoogleScholarGoogle Scholar | 26908844PubMed |
Li, Q. Y., Lou, J., Yang, X. G., Lu, Y. Q., Lu, S. S., and Lu, K. H. (2016b). Effect of the meiotic inhibitor cilostamide on resumption of meiosis and cytoskeletal distribution in buffalo oocytes. Anim. Reprod. Sci. 174, 37–44.
| Effect of the meiotic inhibitor cilostamide on resumption of meiosis and cytoskeletal distribution in buffalo oocytes.Crossref | GoogleScholarGoogle Scholar | 27616355PubMed |
Love, L. B., Choi, Y. H., Love, C. C., Varner, D. D., and Hinrichs, K. (2003). Effect of ovary storage and oocyte transport method on maturation rate of horse oocytes. Theriogenology 59, 765–774.
| Effect of ovary storage and oocyte transport method on maturation rate of horse oocytes.Crossref | GoogleScholarGoogle Scholar | 12517380PubMed |
Luciano, A. M., and Lodde, V. (2013). Changes of large-scale chromatin configuration during mammalian oocyte differentiation. In ‘Oogenesis’. (Eds G. Coticchio, D. Albertini, and L. De Santis.) pp. 93–108. (Springer: London.)
Luciano, A. M., Goudet, G., Perazzoli, F., Lahuec, C., and Gerard, N. (2006). Glutathione content and glutathione peroxidase expression in in vivo and in vitro matured equine oocytes. Mol. Reprod. Dev. 73, 658–666.
| Glutathione content and glutathione peroxidase expression in in vivo and in vitro matured equine oocytes.Crossref | GoogleScholarGoogle Scholar | 16493673PubMed |
Luciano, A. M., Franciosi, F., Modina, S. C., and Lodde, V. (2011). Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol. Reprod. 85, 1252–1259.
| Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s).Crossref | GoogleScholarGoogle Scholar | 21816847PubMed |
Luciano, A. M., Lodde, V., Franciosi, F., Tessaro, I., Corbani, D., and Modina, S. (2012). Large-scale chromatin morpho-functional changes during mammalian oocyte growth and differentiation. Eur. J. Histochem. 56, e37.
| Large-scale chromatin morpho-functional changes during mammalian oocyte growth and differentiation.Crossref | GoogleScholarGoogle Scholar | 23027353PubMed |
Luciano, A. M., Franciosi, F., Dieci, C., and Lodde, V. (2014). Changes in large-scale chromatin structure and function during oogenesis: a journey in company with follicular cells. Anim. Reprod. Sci. 149, 3–10.
| Changes in large-scale chromatin structure and function during oogenesis: a journey in company with follicular cells.Crossref | GoogleScholarGoogle Scholar | 25028181PubMed |
Martino, N. A., Dell’Aquila, M. E., Filioli Uranio, M., Rutigliano, L., Nicassio, M., Lacalandra, G. M., and Hinrichs, K. (2014). Effect of holding equine oocytes in meiosis inhibitor-free medium before in vitro maturation and of holding temperature on meiotic suppression and mitochondrial energy/redox potential. Reprod. Biol. Endocrinol. 12, 99.
| Effect of holding equine oocytes in meiosis inhibitor-free medium before in vitro maturation and of holding temperature on meiotic suppression and mitochondrial energy/redox potential.Crossref | GoogleScholarGoogle Scholar | 25306508PubMed |
Mermillod, P., and Marchal, R. (1999). Oocyte of domestic mammals: a model for the study of in vitro maturation. Contracept. Fertil. Sex. 27, 440–448.
| 10431450PubMed |
Mermillod, P., Lonergan, P., Carolan, C., Khatir, H., Poulin, N., and Cognie, Y. (1996). In vitro oocyte maturation in domestic ruminants. Contracept. Fertil. Sex. 24, 552–558.
| 8924955PubMed |
Mermillod, P., Tomanek, M., Marchal, R., and Meijer, L. (2000). High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity. Mol. Reprod. Dev. 55, 89–95.
| High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 hours in culture by specific inhibition of MPF kinase activity.Crossref | GoogleScholarGoogle Scholar | 10602278PubMed |
Motlík, J., and Kubelka, M. (1990). Cell-cycle aspects of growth and maturation of mammalian oocytes. Mol. Reprod. Dev. 27, 366–375.
| Cell-cycle aspects of growth and maturation of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 2264998PubMed |
Nogueira, D., Ron-El, R., Friedler, S., Schachter, M., Raziel, A., Cortvrindt, R., and Smitz, J. (2006). Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development. Biol. Reprod. 74, 177–184.
| Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development.Crossref | GoogleScholarGoogle Scholar | 16207840PubMed |
Oberstein, N., O’Donovan, M. K., Bruemmer, J. E., Seidel, G. E., Carnevale, E. M., and Squires, E. L. (2001). Cryopreservation of equine embryos by open pulled straw, cryoloop, or conventional slow cooling methods. Theriogenology 55, 607–613.
| Cryopreservation of equine embryos by open pulled straw, cryoloop, or conventional slow cooling methods.Crossref | GoogleScholarGoogle Scholar | 11233786PubMed |
Pandey, S., Somal, A., Parmar, M. S., Gupta, S., Bharti, M. K., Bhat, I. A., Indu, B., Chandra, V., Kumar, G. S., and Sharma, G. T. (2018). Effect of roscovitine on developmental competence of small follicle-derived buffalo oocytes. Indian J. Med. Res. 148, S140–S150.
| 30964092PubMed |
Park, B., Lee, H., Lee, Y., Elahi, F., Lee, J., Lee, S. T., Park, C. K., Hyun, S. H., and Lee, E. (2016). Cilostamide and forskolin treatment during pre-IVM improves preimplantation development of cloned embryos by influencing meiotic progression and gap junction communication in pigs. Theriogenology 86, 757–765.
| Cilostamide and forskolin treatment during pre-IVM improves preimplantation development of cloned embryos by influencing meiotic progression and gap junction communication in pigs.Crossref | GoogleScholarGoogle Scholar | 27056415PubMed |
Pedersen, H. G., Watson, E. D., and Telfer, E. E. (2004). Effect of ovary holding temperature and time on equine granulosa cell apoptosis, oocyte chromatin configuration and cumulus morphology. Theriogenology 62, 468–480.
| Effect of ovary holding temperature and time on equine granulosa cell apoptosis, oocyte chromatin configuration and cumulus morphology.Crossref | GoogleScholarGoogle Scholar | 15226003PubMed |
Pomar, F. J., Teerds, K. J., Kidson, A., Colenbrander, B., Tharasanit, T., Aguilar, B., and Roelen, B. A. (2005). Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species: a comparative study. Theriogenology 63, 2254–2268.
| Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species: a comparative study.Crossref | GoogleScholarGoogle Scholar | 15826688PubMed |
Ponderato, N., Lagutina, I., Crotti, G., Turini, P., Galli, C., and Lazzari, G. (2001). Bovine oocytes treated prior to in vitro maturation with a combination of butyrolactone I and roscovitine at low doses maintain a normal developmental capacity. Mol. Reprod. Dev. 60, 579–585.
| Bovine oocytes treated prior to in vitro maturation with a combination of butyrolactone I and roscovitine at low doses maintain a normal developmental capacity.Crossref | GoogleScholarGoogle Scholar | 11746969PubMed |
Ponderato, N., Crotti, G., Turini, P., Duchi, R., Galli, C., and Lazzari, G. (2002). Embryonic and foetal development of bovine oocytes treated with a combination of butyrolactone I and roscovitine in an enriched medium prior to IVM and IVF. Mol. Reprod. Dev. 62, 513–518.
| Embryonic and foetal development of bovine oocytes treated with a combination of butyrolactone I and roscovitine in an enriched medium prior to IVM and IVF.Crossref | GoogleScholarGoogle Scholar | 12112585PubMed |
Ribeiro, B. I., Love, L. B., Choi, Y. H., and Hinrichs, K. (2008). Transport of equine ovaries for assisted reproduction. Anim. Reprod. Sci. 108, 171–179.
| Transport of equine ovaries for assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 17888596PubMed |
Romero, S., Sánchez, F., Lolicato, F., Van Ranst, H., and Smitz, J. (2016). Immature oocytes from unprimed juvenile mice become a valuable source for embryo production when using C-type natriuretic peptide as essential component of culture medium. Biol. Reprod. 95, 64.
| Immature oocytes from unprimed juvenile mice become a valuable source for embryo production when using C-type natriuretic peptide as essential component of culture medium.Crossref | GoogleScholarGoogle Scholar | 27488026PubMed |
Salgado, R. M., Brom-de-Luna, J. G., Resende, H. L., Canesin, H. S., and Hinrichs, K. (2018). Lower blastocyst quality after conventional vs. Piezo ICSI in the horse reflects delayed sperm component remodeling and oocyte activation. J. Assist. Reprod. Genet. 35, 825–840.
| Lower blastocyst quality after conventional vs. Piezo ICSI in the horse reflects delayed sperm component remodeling and oocyte activation.Crossref | GoogleScholarGoogle Scholar | 29637506PubMed |
Sánchez, F., Lolicato, F., Romero, S., De Vos, M., Van Ranst, H., Verheyen, G., Anckaert, E., and Smitz, J. E. J. (2017). An improved IVM method for cumulus-oocyte complexes from small follicles in polycystic ovary syndrome patients enhances oocyte competence and embryo yield. Hum. Reprod. 32, 2056–2068.
| An improved IVM method for cumulus-oocyte complexes from small follicles in polycystic ovary syndrome patients enhances oocyte competence and embryo yield.Crossref | GoogleScholarGoogle Scholar | 28938744PubMed |
Santiquet, N. W., Greene, A. F., Becker, J., Barfield, J. P., Schoolcraft, W. B., and Krisher, R. L. (2017). A pre-in vitro maturation medium containing cumulus oocyte complex ligand-receptor signaling molecules maintains meiotic arrest, supports the cumulus oocyte complex and improves oocyte developmental competence. Mol. Hum. Reprod. 23, 594–606.
| A pre-in vitro maturation medium containing cumulus oocyte complex ligand-receptor signaling molecules maintains meiotic arrest, supports the cumulus oocyte complex and improves oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 28586460PubMed |
Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 22930834PubMed |
Soto-Heras, S., Paramio, M. T., and Thompson, J. G. (2019). Effect of pre-maturation with C-type natriuretic peptide and 3-isobutyl-1-methylxanthine on cumulus-oocyte communication and oocyte developmental competence in cattle. Anim. Reprod. Sci. 202, 49–57.
| Effect of pre-maturation with C-type natriuretic peptide and 3-isobutyl-1-methylxanthine on cumulus-oocyte communication and oocyte developmental competence in cattle.Crossref | GoogleScholarGoogle Scholar | 30772104PubMed |
Sugimura, S., Yamanouchi, T., Palmerini, M. G., Hashiyada, Y., Imai, K., and Gilchrist, R. B. (2018). Effect of pre-in vitro maturation with cAMP modulators on the acquisition of oocyte developmental competence in cattle. J. Reprod. Dev. 64, 233–241.
| Effect of pre-in vitro maturation with cAMP modulators on the acquisition of oocyte developmental competence in cattle.Crossref | GoogleScholarGoogle Scholar | 29503399PubMed |
Tan, J. H., Wang, H. L., Sun, X. S., Liu, Y., Sui, H. S., and Zhang, J. (2009). Chromatin configurations in the germinal vesicle of mammalian oocytes. Mol. Hum. Reprod. 15, 1–9.
| Chromatin configurations in the germinal vesicle of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 19019837PubMed |
Vanhoutte, L., Nogueira, D., and De Sutter, P. (2008). Prematuration of human denuded oocytes in a three-dimensional co-culture system: effects on meiosis progression and developmental competence. Hum. Reprod. 24, 658–669.
| Prematuration of human denuded oocytes in a three-dimensional co-culture system: effects on meiosis progression and developmental competence.Crossref | GoogleScholarGoogle Scholar | 19056772PubMed |
Vanhoutte, L., Nogueira, D., Dumortier, F., and De Sutter, P. (2009). Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor. Hum. Reprod. 24, 1946–1959.
| Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor.Crossref | GoogleScholarGoogle Scholar | 19395363PubMed |
Xiong, X. R., Lan, D. L., Li, J., Lin, Y. Q., and Li, M. Y. (2017). Supplementation of cilostazol during in vitro maturation enhances the meiosis and developmental competence of yak oocytes by influencing cAMP content and mRNA expression. Anim. Reprod. Sci. 186, 21–30.
| Supplementation of cilostazol during in vitro maturation enhances the meiosis and developmental competence of yak oocytes by influencing cAMP content and mRNA expression.Crossref | GoogleScholarGoogle Scholar | 28935242PubMed |
Zeng, H. T., Ren, Z., Guzman, L., Wang, X., Sutton-McDowall, M. L., Ritter, L. J., De Vos, M., Smitz, J., Thompson, J. G., and Gilchrist, R. B. (2013). Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Hum. Reprod. 28, 1536–1545.
| Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence.Crossref | GoogleScholarGoogle Scholar | 23559189PubMed |
Zeng, H. T., Richani, D., Sutton-McDowall, M. L., Ren, Z., Smitz, J. E., Stokes, Y., Gilchrist, R. B., and Thompson, J. G. (2014). Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes. Biol. Reprod. 91, 47.
| Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 24966394PubMed |
Zhang, J., Wei, Q., Cai, J., Zhao, X., and Ma, B. (2015). Effect of C-type natriuretic peptide on maturation and developmental competence of goat oocytes matured in vitro. PLoS One 10, e0132318.
| Effect of C-type natriuretic peptide on maturation and developmental competence of goat oocytes matured in vitro.Crossref | GoogleScholarGoogle Scholar | 26716983PubMed |
Zhang, Y., Wang, H., Liu, W., Yang, Y., Wang, X., Zhang, Z., Guo, Q., Wang, C., and Xia, G. (2017). Natriuretic peptides improve the developmental competence of in vitro cultured porcine oocytes. Reprod. Biol. Endocrinol. 15, 41.
| Natriuretic peptides improve the developmental competence of in vitro cultured porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 28558842PubMed |
Zuccotti, M., Giorgi Rossi, P., Martinez, A., Garagna, S., Forabosco, A., and Redi, C. A. (1998). Meiotic and developmental competence of mouse antral oocytes. Biol. Reprod. 58, 700–704.
| Meiotic and developmental competence of mouse antral oocytes.Crossref | GoogleScholarGoogle Scholar | 9510956PubMed |
Zuccotti, M., Ponce, R. H., Boiani, M., Guizzardi, S., Govoni, P., Scandroglio, R., Garagna, S., and Redi, C. A. (2002). The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote 10, 73–78.
| The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst.Crossref | GoogleScholarGoogle Scholar | 11964094PubMed |
