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Delaying meiotic resumption during transportation of bovine cumulus–oocyte complexes: effects on development, apoptosis and caspases activity of in vitro-produced embryos

Published online by Cambridge University Press:  27 November 2017

Priscila Chediek Dall'Acqua ,
Beatriz Caetano da Silva Leão ,
Nathália Alves de Souza Rocha-Frigoni ,
Fernanda Patrícia Gottardi  and
Gisele Zoccal Mingoti
Priscila Chediek Dall'Acqua
Affiliation:
Universidade Estadual Paulista (UNESP), School of Veterinary Medicine, Laboratory of Reproductive Physiology, Araçatuba, SP 16050–680, Brazil. Universidade Estadual Paulista (UNESP), School of Agricultural and Veterinarian Sciences, Graduate Program in Veterinary Medicine, Jaboticabal, SP 16050–680, Brazil.
Beatriz Caetano da Silva Leão
Affiliation:
Universidade Estadual Paulista (UNESP), School of Veterinary Medicine, Laboratory of Reproductive Physiology, Araçatuba, SP 16050–680, Brazil. Universidade Estadual Paulista (UNESP), School of Agricultural and Veterinarian Sciences, Graduate Program in Veterinary Medicine, Jaboticabal, SP 16050–680, Brazil.
Nathália Alves de Souza Rocha-Frigoni
Affiliation:
Universidade Estadual Paulista (UNESP), School of Veterinary Medicine, Laboratory of Reproductive Physiology, Araçatuba, SP 16050–680, Brazil. Universidade Estadual Paulista (UNESP), School of Agricultural and Veterinarian Sciences, Graduate Program in Veterinary Medicine, Jaboticabal, SP 16050–680, Brazil.
Fernanda Patrícia Gottardi
Affiliation:
Federal University of Piauí (UFPI), Bom Jesus, PI, Brazil.
Gisele Zoccal Mingoti*
Affiliation:
Universidade Estadual Paulista (UNESP), School of Veterinary Medicine, Department of Animal Health, Araçatuba 16050–680, São Paulo, Brazil. Universidade Estadual Paulista (UNESP), School of Agricultural and Veterinarian Sciences, Graduate Program in Veterinary Medicine, Jaboticabal, SP 16050–680, Brazil.
*
All correspondence to: G.Z. Mingoti. Universidade Estadual Paulista (UNESP), School of Veterinary Medicine, Department of Animal Health, Araçatuba 16050–680, São Paulo, Brazil. Tel: +55 18 3636 1375. Fax: +55 18 3636 1352. E-mail: gmingoti@fmva.unesp.br
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Summary

This study examined the effects of meiosis inhibition during bovine oocyte transportation on developmental competence and quality of produced embryos. The transportation medium was supplemented with: 100 μM butyrolactone I (BL), 500 μM IBMX + 100 μM forskolin (mSPOM), 100 μM milrinone (MR) or follicular fluid (bFF), and was carried out in a portable incubator for 6 h. Next, oocytes were in vitro matured (IVM) for 18 h, without the meiotic inhibitors, with the exception of mSPOM group, in which was added 20 μM cilostamide. The three control groups were IVM with 10% fetal calf serum (FCS) (Control Lab FCS) or 0.6% bovine serum albumin (BSA) (Control Lab BSA) in a CO2 in air incubator or in the portable incubator with 0.6% BSA (Control Transp BSA). Higher cleavage rates (P < 0.05) were obtained in the Control Lab FCS group (84.5 ± 5.3%) compared with the other groups (59.6 ± 3.4% to 70.9 ± 2.3%). Embryonic development was higher (P < 0.05) in the Control Lab FCS group (39.8 ± 4.7%) than in the Control Transp BSA (22.7 ± 3.4%) and MR (21.6 ± 2.3%) groups. However, they were similar (P > 0.05) to the other groups (23.6 ± 3.3% to 28.8 ± 2.7%). The total number of blastomeres was higher (P < 0.05) in the Control Lab FCS group (85.2 ± 5.6) than in Control Lab BSA (53.6 ± 2.9), Control Transp BSA (55.5 ± 4.4), BL (58.2 ± 3.0), mSPOM (57.9 ± 4.9) and MR (59.2 ± 3.9), but all these treatments did not differ (P > 0.05) from bFF (67.7 ± 4.2). No differences (P > 0.05) were found in apoptosis by the activity of caspases (139.0 ± 3.2 to 152.4 ± 6.5, expressed in fluorescence intensity) as well as the percentage of TUNEL-positive cells (12.3 ± 2.0% to 15.7 ± 1.7%). In conclusion, the transportation of oocytes over 6 h with BL, mSPOM or bFF enabled the acquisition of developmental competence at similar rates to the Control Lab FCS group.

Keywords

Developmental competenceIn vitro maturationMeiotic blockOocyteTransport
Type
Research Article
Information
Zygote , Volume 25 , Issue 6 , December 2017 , pp. 740 - 750
Copyright
Copyright © Cambridge University Press 2017 

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References

Adona, P.R. & Leal, C.L.V. (2004). Meiotic inhibition with different cyclin-dependent kinase inhibitors in bovine oocytes and its effects on maturation and embryo development. Zygote 12, 197–204.CrossRefGoogle ScholarPubMed
Albuz, F.K., Sasseville, M., Lane, M., Armstrong, D.T., Thompson, J.G. & 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.CrossRefGoogle ScholarPubMed
Ali, A., Coenen, K., Bousquet, D. & Sirard, M.A. (2004). Origin of bovine follicular fluid and its effect during in vitro maturation on the developmental competence of bovine oocytes. Theriogenology 62, 1596–606.CrossRefGoogle ScholarPubMed
Ambrogi, M., Dall'Acqua, P.C., Rocha-Frigoni, N.A.S., Leão, B.C.S. & Mingoti, G.Z. (2017). Transporting bovine oocytes in a medium supplemented with different macromolecules and antioxidants: effects on nuclear and cytoplasmic maturation and embryonic development in vitro . Reprod. Dom. Anim. 52, 409–21.Google Scholar
Barceló-Fimbres, M., Campos-Chillón, L.F., Mtango, N.R., Altermatt, J., Bonilla, L., Koppang, R. & Verstegen, J.P. (2015). Improving in vitro maturation and pregnancy outcome in cattle using a novel oocyte shipping and maturation system not requiring a CO2 gas phase. Theriogenology 84, 109–17.CrossRefGoogle Scholar
Barretto, L.S.S., Caiado Castro, V.S.D., Garcia, J.M. & Mingoti, G.Z. (2007). Role of roscovitine and IBMX on kinetics of nuclear and cytoplasmic maturation of bovine oocytes in vitro . Anim. Reprod. Sci. 99, 202–7.CrossRefGoogle ScholarPubMed
Bender, K., Walsh, S., Evans, A.C.O., Fair, T. & Brennan, L. (2010). Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows. Reproduction 139, 1047–55.Google Scholar
Bilodeau-Goeseels, S. (2012). Bovine oocyte meiotic inhibition before in vitro maturation and its value to in vitro embryo production: Does it improve developmental competence? Reprod. Dom. Anim. 47, 687–93.CrossRefGoogle ScholarPubMed
Byrne, A.T., Southgate, J., Brison, D.R. & Leese, H.J. (1999). Analysis of apoptosis in the preimplantation bovine embryos using TUNEL. J. Reprod. Fertil. 117, 97–105.CrossRefGoogle ScholarPubMed
Combelles, M.H.C., Gupta, S. & Agarwal, A. (2009). Could oxidative stress influence the in-vitro maturation of oocytes? Reprod. BioMed. Online 18, 864–80.CrossRefGoogle ScholarPubMed
Del Collado, M., Saraiva, NZ., Lopes, F.L., Gaspar, R.C., Padilha, L.C., Costa, R.R., Rossi, G.F., Vantini, R. & Garcia, J.M. (2015). Influence of bovine serum albumin and fetal bovine serum supplementation during in vitro maturation on lipid and mitochondrial behaviour in oocytes and lipid accumulation in bovine embryos. Reprod. Fertil. Dev. 28, 1721–32.CrossRefGoogle Scholar
Downs, S.M., Daniel, S.A.J., Bomslaeger, E.A., Hoppe, P.C. & Eppig, J.J. (1989). Maintenance of meiotic arrest in mouse oocytes by purines: Modulation of cAMP levels and cAMP phosphodiesterase activity. Gamete Res. 23, 323–34.CrossRefGoogle ScholarPubMed
Downs, S.M., Mosey, J.L. & Klinger, J. (2009). Fatty acid oxidation and meiotic resumption in mouse oocytes. Mol. Reprod. Dev. 76, 844–53.CrossRefGoogle ScholarPubMed
Ducolomb, Y., González-Márquez, H., Fierro, R., Jiménez, I., Casas, E., Flores, D., Bonilla, E., Salazar, Z. & Betancourt, M. (2013). Effect of porcine follicular fluid proteins and peptides on oocyte maturation and their subsequent effect on in vitro fertilization. Theriogenology 79, 896–904.CrossRefGoogle ScholarPubMed
Dunning, K.R., Cashman, K., Russell, D.L., Thompson, J.G., Norman, R.J. & Robker, R.L. (2010). β-Oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol. Reprod. 83, 909–18.CrossRefGoogle ScholarPubMed
Franciosi, F., Coticchio, G., Lodde, V., Tessaro, I., Modina, S.C., Fadini, R., Dal Canto, M., Renzini, M.M., Albertini, D.F. & 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.CrossRefGoogle ScholarPubMed
Gilchrist, R.B. (2011). Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod. Fertil. Dev. 23, 23–31.CrossRefGoogle ScholarPubMed
Gilchrist, R.B. & Thompson, J.G. (2007). Oocyte maturation: Emerging concepts and technologies to improve developmental potential in vitro . Theriogenology 67, 6–15.CrossRefGoogle ScholarPubMed
Guemra, S., Santos, ES., Zanin, R., Monzani, P.S., Sovernigo, T.C., Ohashi, O.M., Leal, C.L.V. & 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, 982–7.Google Scholar
Guérin, P., Mouatassim, S.E.L. & Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–89.Google Scholar
Hashimoto, S., Minami, N., Takakura, R. & Imai, H. (2002). Bovine immature oocytes acquire developmental competence during meiotic arrest in vitro . Biol. Reprod. 66, 1696–701.Google Scholar
Homa, S.T. & Brown, C.A. (1992). Changes in linoleic acid during follicular development and inhibition of spontaneous breakdown of germinal vesicles in cumulus-free bovine oocytes. J. Reprod. Fertil. 94, 153–60.CrossRefGoogle ScholarPubMed
Krisher, R.L., Lane, M. & Bavister, B.D. (1999). Developmental competence and metabolism of bovine embryos cultured in semi-defined and defined culture media. Biol. Reprod. 60, 1345–52.CrossRefGoogle ScholarPubMed
Kubelka, M., Motlik, J., Schultz, R.M. & Pavlok, A. (2000). Butyrolactone I reversibly inhibits meiotic maturation of bovine oocyte, without influencing chromosome condensation activity. Biol. Reprod. 62, 292–302.CrossRefGoogle ScholarPubMed
Lonergan, P., Carolan, C., Van Langendonckt, A., Donnay, I., Khatir, H. & Mermillod, P. (1996). Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro . Biol. Reprod. 54, 1420–9.CrossRefGoogle ScholarPubMed
Mingoti, G.Z., Castro, V.S.D.C., Méo, S.C., Barretto, L.S.S. & Garcia, J.M. (2011). The effects of macromolecular and serum supplements and oxygen tension during bovine in vitro procedures on kinetics of oocyte maturation and embryo development. In Vitro Cell Dev. Biol. Anim. 47, 361–7.Google Scholar
Naruse, K., Iga, K., Shimizu, M., Takenouchi, N., Akagi, S., Somfai, T. & Hirao, Y. (2012). Milrinone treatment of bovine oocytes during in vitro maturation benefits production of nuclear transfer embryos by improving enucleation rate and developmental competence. J. Reprod. Dev. 58, 476–83.CrossRefGoogle ScholarPubMed
Paczkowski, M., Silva, E., Schoolcraft, W.B. & Krisher, R.L. (2013). Comparative importance of fatty-acid β-oxidation to nuclear maturation, gene expression and glucose metabolism in mouse, bovine and porcine cumulus–oocyte complexes. Biol. Reprod. 88, 111.CrossRefGoogle ScholarPubMed
Pandey, A.N., Tripathi, A., Premkumar, K.V., Shrivastav, T.G. & Chaube, S.K. (2010). Reactive oxygen and nitrogen species during meiotic resumption from diplotene arrest in mammalian oocytes. J. Cell. Biochem. 111, 521–8.CrossRefGoogle ScholarPubMed
Paula-Lopes, F.F. & Hansen, P.J. (2002). Apoptosis is an adaptive response in bovine preimplantation embryos that facilitates survival after heat shock. Biochem. Biophys. Res. Commun. 295, 37–42.CrossRefGoogle ScholarPubMed
Perry, G. (2015). 2013 Statistics of embryo collection and transfer in domestic farm animals. Embryo Transfer Newslett. 33, 14–26.Google Scholar
Pomar, F.J.R., Teerds, K.J., Kidson, A., Colenbrander, B., Tharasanit, T., Aguilar, B. & Roelen, B.A.J. (2005). Differences in the incidence of apoptosis between in vivo and in vitro produced blastocysts of farm animal species: a comparative study. Theriogenology 63, 2254–68.Google Scholar
Ponderato, N., Crotti, G., Turini, P., Duchi, R., Galli, C. & 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, 513–8.CrossRefGoogle Scholar
Rocha-Frigoni, N.A.S., Leão, B.C.S., Dall'Acqua, P.C. & Mingoti, G.Z. (2016). Improving the cytoplasmic maturation of bovine oocytes matured in vitro with intracellular and/or extracellular antioxidants is not associated with increased rates of embryo development. Theriogenology 86, 1897–905.CrossRefGoogle Scholar
Rocha-Frigoni, N.A., Leão, B.C., Nogueira, É., Accorsi, M.F. & Mingoti, G.Z. (2014). Reduced levels of intracellular reactive oxygen species and apoptotic status are not correlated with increases in cryotolerance of bovine embryos produced in vitro in the presence of antioxidants. Reprod. Fertil. Dev. 26, 797–805.CrossRefGoogle Scholar
Romero-Arredondo, A. & Seidel, GE. Jr (1996). Effects of follicular fluid during in vitro maturation of bovine oocytes on in vitro fertilization and early embryonic development. Biol. Reprod. 55, 1012–6.CrossRefGoogle ScholarPubMed
Russell, D.F., Baqir, S., Bordignon, J. & Betts, D.H. (2006). The impact of oocyte maturation media on early bovine embryonic development. Mol. Reprod. Dev. 73, 1255–70.CrossRefGoogle ScholarPubMed
Sasseville, M., Albuz, FK., Côté, N., Guillemette, C., Gilchrist, R.B. & Richard, F.J. (2009). Characterization of novel phosphodiesterases in the bovine ovarian follicle. Biol. Reprod. 81, 415–25.Google Scholar
Sirard, M.A., Richard, F. & Mayes, M. (1998). Controlling meiotic resumption in bovine oocytes: a review. Theriogenology 49, 483–97.CrossRefGoogle ScholarPubMed
Takahashi, M., Koide, S.S. & Donahoe, PK. (1986). Müllerian inhibiting substance as oocyte meiosis inhibitor. Mol. Cell. Endo. 47, 225–34.Google Scholar
Thomas, R.E., Armstrong, D.T. & Gilchrist, R.B. (2002). Differential effects of specific phosphodiesterase isoenzyme inhibitors on bovine oocyte meiotic maturation. Dev. Biol. 244, 215–25.Google Scholar
Tsafiri, A., Chun, SY., Zhang, R., Hsueh, A.J.W. & Conti, M. (1996). Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 178, 393–402.CrossRefGoogle Scholar
van den Hurk, R. & Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles, Theriogenology 63, 1717–51.CrossRefGoogle ScholarPubMed