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Time course of the meiotic arrest in sheep cumulus–oocyte complexes treated with roscovitine

Published online by Cambridge University Press:  14 July 2015

Letícia Ferrari Crocomo ,
Wolff Camargo Marques Filho ,
Camila Louise Ackermann ,
Daniela Martins Paschoal ,
Midyan Daroz Guastali ,
Rosiára Rosária Dias Maziero ,
Mateus José Sudano ,
Fernanda da Cruz Landim-Alvarenga  and
Sony Dimas Bicudo
Letícia Ferrari Crocomo*
Affiliation:
Rua dos Girassóis, n.278 – Bairro Convívio – CEP: 18605–240 Botucatu – S.P., Brazil. Department of Animal Reproduction and Veterinary Radiology - School of Veterinary Medicine and Animal Science (FMVZ), São Paulo State University (UNESP) - Botucatu, Brazil.
Wolff Camargo Marques Filho
Affiliation:
Department of Animal Reproduction and Veterinary Radiology - School of Veterinary Medicine and Animal Science (FMVZ), São Paulo State University (UNESP) - Botucatu, Brazil.
Camila Louise Ackermann
Affiliation:
Department of Animal Reproduction and Veterinary Radiology - School of Veterinary Medicine and Animal Science (FMVZ), São Paulo State University (UNESP) - Botucatu, Brazil.
Daniela Martins Paschoal
Affiliation:
Department of Animal Reproduction and Veterinary Radiology - School of Veterinary Medicine and Animal Science (FMVZ), São Paulo State University (UNESP) - Botucatu, Brazil.
Midyan Daroz Guastali
Affiliation:
Department of Animal Reproduction and Veterinary Radiology - School of Veterinary Medicine and Animal Science (FMVZ), São Paulo State University (UNESP) - Botucatu, Brazil.
Rosiára Rosária Dias Maziero
Affiliation:
Department of Animal Reproduction and Veterinary Radiology - School of Veterinary Medicine and Animal Science (FMVZ), São Paulo State University (UNESP) - Botucatu, Brazil.
Mateus José Sudano
Affiliation:
Laboratory of Genetics and Animal Breeding, Federal University of Pampa, Uruguaiana, RS, Brazil.
Fernanda da Cruz Landim-Alvarenga
Affiliation:
Department of Animal Reproduction and Veterinary Radiology - School of Veterinary Medicine and Animal Science (FMVZ), São Paulo State University (UNESP) - Botucatu, Brazil.
Sony Dimas Bicudo
Affiliation:
Department of Animal Reproduction and Veterinary Radiology - School of Veterinary Medicine and Animal Science (FMVZ), São Paulo State University (UNESP) - Botucatu, Brazil.
*
All correspondence to: Letícia Ferrari Crocomo. Rua dos Girassóis, n.278 – Bairro Convívio – CEP: 18605–240 Botucatu – S.P., Brazil. Tel: + 55 14 3882–4743. E-mail: leticia.crocomo@gmail.com
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Summary

Temporary meiosis arrest with cyclin-dependent kinases inhibitors has been proposed in order to improve the quality of in vitro matured oocytes. In sheep, however, this phenomenon has been rarely investigated. Therefore, the present study aimed to evaluate the effect of different incubation times with roscovitine on nuclear maturation and cumulus cell expansion of sheep cumulus–oocyte complexes (COCs). For this, COCs were cultured for 0, 6, 12 or 20 h in basic maturation medium (Control) containing 75 μM roscovitine (Rosco). After, they were in vitro matured (IVM) for 18 h in the presence of luteinizing hormone (LH) and follicle-stimulating hormone (FSH). At the end of each treatment, cumulus cell expansion and nuclear maturation were assessed under a stereomicroscope and by Hoechst 33342 staining, respectively. In the Control and Rosco groups, the absence of cumulus cell expansion prevailed at 0, 6, 12 and 20 h. After IVM for 18 h, total cumulus cell expansion in the Rosco treatments was dependent on the exposure time to roscovitine. A significantly high percentage of oocytes treated with roscovitine for 6 h (87%), 12 h or 20 h (65%) were arrested at the germinal vesicle (GV) stage. In contrast, 23% GVBD, 54% metaphase I (MI) and 61% MII oocytes were observed in the Control groups at 6, 12 and 20 h, respectively. In all treatments, a significant percentage of oocytes reached MII after IVM for 18 h. Therefore, roscovitine reversibly arrested the meiosis of sheep oocytes during different culture times with the maximal efficiency of meiotic inhibition reached at 6 h. In addition, reversibility of its inhibitory action on cumulus cells was exposure-time dependent.

Keywords

Cumulus cell expansionInhibitorMeiosisNuclear maturationOvine
Type
Research Article
Information
Zygote , Volume 24 , Issue 2 , April 2016 , pp. 310 - 318
Copyright
Copyright © Cambridge University Press 2015 

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References

Accardo, C., Dattena, M., Pilichi, S., Mara, L., Chessa, B. & Cappai, P. (2004). Effect of recombinant human FSH and LH on in vitro maturation of sheep oocytes; embryo development and viability. Anim. Reprod. Sci. 81, 77–86.CrossRefGoogle ScholarPubMed
Barretto, L.S.S., Castro, V.S.D.C., Garcia, J.M. & 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, 107–16.CrossRefGoogle Scholar
Berg, D.K., Thompson, J.G. & Asher, G.W. (2002). Development of in vitro embryo production systems for red deer (Cervus elaphus). Part 2. The timing of in vitro nuclear oocyte maturation. Anim. Reprod. Sci. 70, 77–84 Google Scholar
Cotterill, M., Catt, S. L. & Picton, H. M. (2012). Characterisation of the cellular and molecular responses of ovine oocytes and their supporting somatic cells to pre-ovulatory levels of LH and FSH during in vitro maturation. Reproduction 144, 195–207.CrossRefGoogle ScholarPubMed
Coy, P., Romar, R., Ruiz, S., Cánovas, S., Gadea, J., Vázquez, F.G. & Matás, C. (2005). Birth of piglets after transferring of in vitro-produced embryos pre-matured with R-roscovitine. Reproduction 129, 747–55.Google Scholar
Crocomo, L.F., Marques Filho, W.C., Sudano, M.J., Paschoal, D.M., Alvarenga, F.C.L. & Bicudo, S.D. (2013). Effect of roscovitine and cycloheximide on ultrastructure of sheep oocytes. Small Rum. Res. 109, 156–62.Google Scholar
Crocomo, L.F., Marques Filho, W.C., Ulian, C.M.V., Branchini, N.S., Silva, D.T., Ackermann, C.L., Landim-Alvarenga, F.C. & Bicudo, S.D. (2015). Effect of oil overlay on inhibition potential of roscovitine in sheep cumulus–oocyte complexes. Reprod. Domest. Anim. 50, 410–6.CrossRefGoogle ScholarPubMed
Dekel, N., Lawrence, T.S., Gilula, N.B. & Beers, W.H. (1981). Modulation of cell-to-cell communication in the cumulus–oocyte complex and the regulation of oocyte maturation by LH. Dev. Biol. 86, 356–92.Google Scholar
Donnay, I., Faerge, I., Grøndahl, C., Verhaeghe, B., Sayoud, H., Ponderato, N., Galli, C. & Lazzari, G. (2004). Effect of prematuration, meiosis activating sterol and enriched maturation medium on the nuclear maturation and competence to development of calf oocytes. Theriogenology 62, 1093–107.CrossRefGoogle ScholarPubMed
Ferreira, E.M., Vireque, A.A., Adona, P.R., Meirelles, F.V., Ferriani, R.A. & Navarro, P.A.A.S. (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–48.Google Scholar
Franz, L.C., Choi, Y.H., Squires, E.L., Seidel, G.E. & 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.Google Scholar
Gharibi, S.H., Hajian, M., Ostadhosseini, S., Hosseini, S.M., Forouzanfar, M. & Nasr-Esfahani, M.H. (2013). Effect of phosphodiesterase type 3 inhibitor on nuclear maturation and in vitro development of ovine oocytes. Theriogenology 80, 302–12.Google Scholar
Han, D., Lan, G., Wu, Y., Han, Z., Wang, H. & Tan, J. (2006). Factors affecting the efficiency and reversibility of roscovitine (ros) block on the meiotic resumption of goat oocytes. Mol. Reprod. Dev. 73, 238–46.Google Scholar
Heidari Amale, M., Zare Shahne, A., Abavisani, A. & Nasrollahi, S. (2011). Effects of inhibiting nitric oxide synthase on cumulus expansion and nuclear maturation of sheep oocytes. Czech J. Anim. Sci. 56, 284–91.CrossRefGoogle Scholar
Hyttel, P., Xu, K. P., Smith, S. & Greve, T. (1986). Ultrastructure of in vitro oocyte maturation in cattle. J. Reprod. Fert. 78, 615–25.CrossRefGoogle ScholarPubMed
Kito, S. & Bavister, B.D. (1997). Gonadotropins, serum, and amino acids alter nuclear maturation, cumulus expansion, and oocyte morphology in hamster cumulus–oocyte complexes in vitro. Biol. Reprod. 56, 1281–9.CrossRefGoogle Scholar
Krisher, R.L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, E14–E23.Google ScholarPubMed
Lagutina, I., Ponderato, N., Lazzari, G. & Galli, C. (2002). Kinetics of oocyte maturation and subsequent development of IVF, parthenogenetic, and NT bovine embryos after meiotic inhibition with roscovitine. Cloning Stem Cells 4, 113–9.Google Scholar
Marchal, R., Tomanek, M., Terqui, M. & Mermillod, P (2001). Effects of cell cycle dependent kinases inhibitor on nuclear amd cytoplasmic maturation of porcine oocytes. Mol. Reprod. Dev. 60, 65–73.Google Scholar
Marshall, V.S., Wilton, L.J. & Moore, R.D.M. (1998). Parthenogenetic activation of marmoset (callithrix jacchus) oocytes and the development of marmoset parthenogenones in vitro and in vivo . Biol. Reprod. 59, 1491–7.CrossRefGoogle ScholarPubMed
Mattioli, M., Bacci, M.L., Galeati, G. & Seren, E. (1991). Effects of LH and FSH on the maturation of pig oocytes in vitro . Theriogenology 36, 95–105.CrossRefGoogle ScholarPubMed
Máximo, D.M., Martins da Silva, I.G., Mondadori, R.G., Neves, J. P. & Lucci, C.M. (2012). Ultrastructural characteristics of sheep oocytes during in vitro maturation (IVM). Small Rumin. Res. 105, 210–5.Google Scholar
Mehlmann, L. M., 2005. Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791–9.CrossRefGoogle ScholarPubMed
Meijer, L., Borgne, A., Mulner, O., Chong, J.P.J., Blow, J.J., Inagaki, N., Inagaki, M., Delcros, J.G. & Moulinoux, J.P. (1997). Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur. J. Biochem. 243, 527–36.Google Scholar
Mermillod, P., Tomanek, M., Marchal, R. & Meijer, L. (2000). High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 h in culture by specific inhibition of MPF kinase activity. Mol. Reprod. Dev. 55, 89–95.3.0.CO;2-M>CrossRefGoogle Scholar
Mermillod, P., Dalbies-Tran, R., Uzbekova, S., Thelie, A., Traverso, J.M., Perreau, C., Papillier, P. & Monget, P. (2008). Factors affecting oocyte quality: who is driving the follicle? Reprod. Dom. Anim. 43, 393–400.CrossRefGoogle ScholarPubMed
Moor, R. M. & Crosby, I.M. (1985). Temperature-induced abnormalities in sheep oocytes during maturation. J. Reprod. Fert. 75, 467–73.Google Scholar
Natsuyama, S., Noda, Y., Narimoto, K. & Mori, T. (1993). Role of protein supplements in the culture of mouse embryos. Theriogenology 40,149–57.Google Scholar
Pincus, G. & Enzmann, E.V. (1935).The comparative behavior of mammalian eggs in vivo and in vitro. J. Exp. Med. 62, 665–75.Google Scholar
Rizos, D., Lonergan, P., Ward, F., Duffy, P. & Boland, M.P. (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: Implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234–48.Google Scholar
Sananmuang, T., Techakumphu, M. & Tharasanit, T. (2010). The effects of roscovitine on cumulus cell apoptosis and the developmental competence of domestic cat oocytes. Theriogenology 73, 199–207.CrossRefGoogle ScholarPubMed
Sanbuissho, A. & Threlfall, W.R. (1990). The influence of serum and gonadotropins on in vitro maturation and fertilization of bovine oocytes. Theriogenology 34, 341–8.CrossRefGoogle ScholarPubMed
Schoevers, E.J., Bevers, M.M., Roelen, B.A.J. & Colenbrander, B. (2005). Nuclear and cytoplasmatic maturation of sow oocytes are not synchronized by specific meiotic inhibition with roscovitine during in vitro maturation. Theriogenology 63, 1111–30.CrossRefGoogle Scholar
Shirazi, A., Bahiraee, A., Ahmadi, E., Nazari, H., Heidari, B. & Borjian, S. (2009). The effect of the duration of in vitro maturation (IVM) on parthenogenetic development of ovine oocytes. Avicenna J. Med. Biotechnol. 1, 181–91.Google Scholar
Shirazi, A., Shams-Esfandabadi, N., Ahmadi, E. & Heidari, B. (2010). Effects of growth hormone on nuclear maturation of ovine oocytes and embryo. Reprod. Dom. Anim. 45, 530–6.Google Scholar
Sirard, M.A., Parrish, J.J., Ware, C.B., Leibfried-Rutledge, M.L. & First, N.L. (1988). Culture of bovine oocytes to obtain developmentally competent embryos. Biol. Reprod. 39, 546–52.Google Scholar
Souza-Fabjan, J.M.G., Panneau, B., Duffard, N., Locatelli, Y., Figueiredo, J.R., Freitas, V.J.F. & Mermillod, P. (2014). In vitro production of small ruminant embryos: Late improvements and further research. Theriogenology 81, 1149–62.CrossRefGoogle ScholarPubMed
Tanghe, S., Soom, A.V., Nauwynck, H., Coryn, M. & De Kruif, A. (2002). Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation and fertilization. Mol. Reprod. Dev. 61, 414–24.Google Scholar
Watson, A.J. (2007). Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J. Anim. Sci. 85, E1–3.Google Scholar