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Meiotic arrest as an alternative to increase the production of bovine embryos by somatic cell nuclear transfer

Published online by Cambridge University Press:  26 October 2016

F.M.C. Caixeta ,
R.V. Sousa ,
A.L. Guimarães ,
L.O. Leme ,
J.F.W. Sprícigo ,
S.B. Senna Netto ,
I. Pivato  and
M.A.N. Dode
F.M.C. Caixeta
Affiliation:
School of Agriculture and Veterinary Medicine, University of Brasilia, Brasília-DF, Brazil.
R.V. Sousa
Affiliation:
EMBRAPA Genetic Resources and Biotechnology, Brasília-DF, Brazil.
A.L. Guimarães
Affiliation:
School of Agriculture and Veterinary Medicine, University of Brasilia, Brasília-DF, Brazil.
L.O. Leme
Affiliation:
School of Agriculture and Veterinary Medicine, University of Brasilia, Brasília-DF, Brazil.
J.F.W. Sprícigo
Affiliation:
School of Agriculture and Veterinary Medicine, University of Brasilia, Brasília-DF, Brazil.
S.B. Senna Netto
Affiliation:
School of Agriculture and Veterinary Medicine, University of Brasilia, Brasília-DF, Brazil.
I. Pivato
Affiliation:
School of Agriculture and Veterinary Medicine, University of Brasilia, Brasília-DF, Brazil.
M.A.N. Dode*
Affiliation:
EMBRAPA Genetic Resources and Biotechnology, Parque Estação Biológica, Final Av. W5/N, Prédio PBI, 70770-900, Brasília-DF, Brazil. EMBRAPA Genetic Resources and Biotechnology, Brasília-DF, Brazil.
*
All correspondence to: Margot Alves Nunes Dode, EMBRAPA Genetic Resources and Biotechnology, Parque Estação Biológica, Final Av. W5/N, Prédio PBI, 70770–900, Brasília-DF, Brazil. Tel: +55 61 34484659. Fax: +55 61 3340 3658. E-mail: margot.dode@embrapa.br
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Summary

This study aimed to evaluate the effect of meiotic arrest using phosphodiesterase type 3A (PDE 3A) inhibitors, cilostamide and C-type natriuretic peptide (NPPC), on pre-maturation (PM) of oocytes to be used in the production of cloned embryos. Nuclear maturation, in vitro embryo production (IVP), somatic cell nuclear transfer (SCNT) and parthenogenetic activation (PA), and total cells number of cloned embryos were evaluated. The results were analysed by chi-squared and Kruskal–Wallis test with a P-value <0.05 considered to be significant. Approximately 87.8% of the oocytes remained at germinal vesicle stage (GV) after 6 h of PM with 5 μM of cilostamide, confirming the meiotic block. Embryo development in IVP was similar (P > 0.05) between control and PM, both for cleavage (78.2% and 76.9%) and blastocyst (35.5% and 29.3%) rates. After SCNT, cleavage rate was also similar (P > 0.05) between control and PM (66% and 51.9%) however, blastocyst rate was lower (P < 0.05) in the PM group than in the control group (7.4% and 30.2%). After 6 h of PM with 100 nM of NPPC, approximately 84.9% of the oocytes remained at GV. No difference was found between control and PM in cleavage (69.2% and 76.1%) and blastocyst rates (37,4% and 35%) after IVP. Similarly, no differences between PM and control groups were observed for cleavage (69.2% and 68.4%) and blastocyst (24.4% and 21.5%) rates. SCNT and PA embryos from control or PM oocytes had similar total cell number. It can be concluded that PM for 6 h with 100 nM NPPC is feasible for cloned embryo production without affecting embryo outcome.

Keywords

CilostamideNPPCOocytePre-maturationSCNT
Type
Research Article
Information
Zygote , Volume 25 , Issue 1 , February 2017 , pp. 32 - 40
Copyright
Copyright © Cambridge University Press 2016 

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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.Google Scholar
Adona, P.R., Pires, P.R., Quetglas, M.D., Schwarz, K.R. & Leal, C.L. (2008). Prematuration of bovine oocytes with butyrolactone I: effects on meiosis progression, cytoskeleton, organelle distribution and embryo development. Anim. Reprod. Sci. 108, 49–65.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.Google Scholar
Barretto, L.S.S., Caiado Castro, V.S.D., 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.Google Scholar
Buell, M., Chitwood, J.L. & Ross, P.J. (2015). cAMP modulation during sheep in vitro oocyte maturation delays progression of meiosis without affecting oocyte parthenogenetic developmental competence. Anim. Reprod. Sci. 154, 16–24.Google Scholar
Campbell, K.H., Fisher, P., Chen, W.C., Choi, I., Kelly, R.D., Lee, J.H. & Xhu, J. (2007). Somatic cell nuclear transfer: Past, present and future perspectives. Theriogenology 68 (Suppl. 1), S214–31.Google Scholar
Chen, J., Chi, M.M., Moley, K.H. & Downs, S.M. (2009). cAMP pulsing of denuded mouse oocytes increases meiotic resumption via activation of AMP-activated protein kinase. Reproduction 138, 759–70.Google Scholar
De Bem, T.H., Chiaratti, M.R., Rochetti, R., Bressan, F.F., Sangalli, J.R., Miranda, M.S., Pires, P.R., Schwartz, K.R., Sampaio, R.V., Fantinato-Neto, P., Pimentel, J.R., Perecin, F., Smith, L.C., Meirelles, F.V., Adona, P.R. & Leal, C.L. (2011). Viable calves produced by somatic cell nuclear transfer using meiotic-blocked oocytes. Cell Reprogram. 13, 419–29.Google Scholar
De Cesaro, M.P., Macedo, M.P., Santos, J.T., Rosa, P.R., Ludke, C.A., Rissi, V.B., Gasperin, B.G. & Goncalves, P.B. (2015). Natriuretic peptides stimulate oocyte meiotic resumption in bovine. Anim. Reprod. Sci. 159, 52–9.CrossRefGoogle ScholarPubMed
Dieci, C., Lodde, V., Franciosi, F., Lagutina, I., Tessaro, I., Modina, S.C., Albertini, D.F., Lazzari, G., Galli, C. & 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.CrossRefGoogle ScholarPubMed
Dode, M.A.N. & Adona, P.R. (2001). Developmental capacity of Bos indicus oocytes after inhibition of meiotic resumption by 6-dimethylaminopurine. Anim. Reprod. Sci. 65, 171–80.Google Scholar
Farghaly, T., Khalifa, E., Mostafa, S., Hussein, M., Bedaiwy, M. and Ahmady, A. (2015). The effect of temporary meiotic attenuation on the in vitro maturation outcome of bovine oocytes. In Vitro Cell. Dev. Biol. Anim. 51, 662–71.Google Scholar
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.Google Scholar
Gilchrist, R.B. & Thompson, J.G. (2007). Oocyte maturation: emerging concepts and technologies to improve development potential in vitro . Theriogenology 67, 6–15.Google Scholar
Guimaraes, A.L., Pereira, S.A., Kussano, N.R. & Dode, M.A. (2015). Evaluation of the simulated physiological oocyte maturation system for improving bovine in vitro embryo production. Theriogenology 83, 52–7.Google Scholar
Guimaraes, A.L., Pereira, S.A., Kussano, N.R. & Dode, M.A. (2016). The effect of pre-maturation culture using phosphodiesterase type 3 inhibitor and insulin, transferrin and selenium on nuclear and cytoplasmic maturation of bovine oocytes. Zygote 24, 219–29.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Hendriksen, P.J.M., Vos, P.L.A.M., Steenweg, W.N.M., Bevers, M.M. & Dieleman, S.J. (2000). Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology 53, 11–20.CrossRefGoogle ScholarPubMed
Hiradate, Y., Hoshino, Y., Tanemura, K. & Sato, E. (2014). C-type natriuretic peptide inhibits porcine oocyte meiotic resumption. Zygote 22, 372–7.CrossRefGoogle ScholarPubMed
Holm, P., Booth, P.J., Schmidt, M.H., Greve, T. & Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using sofaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683–700.Google Scholar
Hosseini, S.M., Dufort, I., Nieminen, J., Moulavi, F., Ghanaei, H.R., Hajian, M., Jafarpour, F., Forouzanfar, M., Gourbai, H., Shahverdi, A.H., Nasr-Esfahani, M.H. & Sirard, M.A. (2016). Epigenetic modification with trichostatin A does not correct specific errors of somatic cell nuclear transfer at the transcriptomic level; highlighting the non-random nature of oocyte-mediated reprogramming errors. BMC Genomics 17, 16.Google Scholar
Iwamoto, D., Yamagata, K., Kishi, M., Hayashi-Takanaka, Y., Kimura, H., Wakayama, T. & Saeki, K. (2015). Early development of cloned bovine embryos produced from oocytes enucleated by fluorescence metaphase II imaging using a conventional halogen-lamp microscope. Cell Reprogram. 17, 106–14.Google Scholar
Jee, B.C., Chen, H.Y. & Chian, R.C. (2009). Effect of a phosphodiesterase type 3 inhibitor in oocyte maturation medium on subsequent mouse embryo development. Fertil. Steril. 91, 2037–42.Google Scholar
Jeong, Y.I., Park, C.H., Kim, H.S., Jeong, Y.W., Lee, J.Y., Park, S.W., Lee, S.Y., Hyun, S.H., Kim, Y.W., Shin, T. & Hwang, W.S. (2013). Effects of trichostatin A on in vitro development of porcine embryos derived from somatic cell nuclear transfer. Asian-Australas J. Anim. Sci. 26, 1680–8.CrossRefGoogle ScholarPubMed
Kato, Y., Tani, T. & Tsunoda, Y. (2000). Cloning of calves from various somatic cell types of male and female adult, newborn and fetal cows. J. Reprod. Fertil. 120, 231–237.Google Scholar
Keefer, C.L. (2015). Artificial cloning of domestic animals. Proc. Natl. Acad. Sci. USA 112, 8874–8.CrossRefGoogle ScholarPubMed
Latham, K.E. (2005). Early and delayed aspects of nuclear reprogramming during cloning. Biol. Cell 97, 119–32.Google Scholar
Lodde, V., Franciosi, F., Tessaro, I., Modina, S.C. & Luciano, A.M. (2013). Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte. J. Assist. Reprod. Genet. 30, 1219–26.CrossRefGoogle ScholarPubMed
Luciano, A.M., Franciosi, F., Modina, S.C. & Lodde, V. (2011). Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol. Reprod. 85, 1252–9.Google Scholar
Marques, M.G., Nascimento, A.B., Gerger, R.P., Goncalves, J.S., Coutinho, A.R., Simoes, R., Assumpcao, M.E. & Visintin, J.A. (2011). Effect of culture media on porcine embryos produced by in vitro fertilization or parthenogenetic activation after oocyte maturation with cycloheximide. Zygote 19, 331–7.CrossRefGoogle ScholarPubMed
Mayes, M.A. & Sirard, M.-A. (2002). Effect of type 3 and type 4 phosphodiesterase inhibitors on the maintenance of bovine oocytes in meiotic arrest. Biol. Reprod. 66, 180–184.Google Scholar
Niemann, H., Tian, X.C., King, W.A. & Lee, R.S. (2008). Epigenetic reprogramming in embryonic and foetal development upon somatic cell nuclear transfer cloning. Reproduction 135, 151–63.Google Scholar
Santos, F., Zakhartchenko, V., Stojkovic, M., Peters, A., Jenuwein, T., Wolf, E., Reik, W. & Dean, W. (2003). Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr. Biol. 13, 1116–21.Google Scholar
Sasseville, M., Albuz, F.K., Cote, 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. (2001). Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–54.Google Scholar
Smith, L.C.B.V., Babkine, M., Fecteau, G. & Keefer, C. (2000). Benefits and problems with cloning animals. Can. Vet. J. 41, 6.Google Scholar
Smith, L.C., Suzuki, J. Jr., Goff, A.K., Filion, F., Therrien, J., Murphy, B.D., Kohan-Ghadr, H.R., Lefebvre, R., Brisville, A.C., Buczinski, S., Fecteau, G., Perecin, F. & Meirelles, F.V. (2012). Developmental and epigenetic anomalies in cloned cattle. Reprod. Domest. Anim. 47 (Suppl. 4), 107–14.CrossRefGoogle ScholarPubMed
Song, Z., Cong, P., Ji, Q., Chen, L., Nie, Y., Zhao, H., He, Z. & Chen, Y. (2015). Establishment, differentiation, electroporation and nuclear transfer of porcine mesenchymal stem cells. Reprod. Domest. Anim. 50, 840–8.Google Scholar
Ulloa, S.M., Heinzmann, J., Herrmann, D., Timmermann, B., Baulain, U., Grossfeld, R., Diederich, M., Lucas-Hahn, A. & Niemann, H. (2015). Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote 23, 367–77.Google Scholar
Vanhoutte, L., Nogueira, D., Gerris, J., Dhont, M. & De Sutter, P. (2008). Effect of temporary nuclear arrest by phosphodiesterase 3-inhibitor on morphological and functional aspects of in vitro matured mouse oocytes. Mol. Reprod. Dev. 75, 1021–30.CrossRefGoogle ScholarPubMed
Zhang, M., Su, Y.-Q., Sugiura, K., Xia, G. & Eppig, J.J. (2010). Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330, 366–9.Google Scholar
Zhong, Y., Lin, J., Liu, X., Hou, J., Zhang, Y. & Zhao, X. (2015). C-Type natriuretic peptide maintains domestic cat oocytes in meiotic arrest. Reprod. Fertil. Dev. doi: 10.1071/RD14425. [Epub ahead of print]Google Scholar