Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-23T16:53:19.997Z Has data issue: false hasContentIssue false
  • English
  • Français

Developmental competence and expression of the MATER and ZAR1 genes in immature bovine oocytes selected by brilliant cresyl blue

Published online by Cambridge University Press:  26 November 2009

Gustavo Bruno Mota ,
Ribrio Ivan Tavares Pereira Batista ,
Raquel Varella Serapião ,
Mariana Cortes Boité ,
João Henrique Moreira Viana ,
Ciro Alexandre Alves Torres  and
Luiz Sergio de Almeida Camargo
Gustavo Bruno Mota
Affiliation:
Departamento de Zootecnia, Universidade Federal de Viçosa, Av. P H Rolfs s/n, Viçosa, MG, 36571–000, Brazil.
Ribrio Ivan Tavares Pereira Batista
Affiliation:
Embrapa Gado de Leite, Juiz de Fora, MG, 36038–330, Brazil.
Raquel Varella Serapião
Affiliation:
Embrapa Gado de Leite, Juiz de Fora, MG, 36038–330, Brazil.
Mariana Cortes Boité
Affiliation:
Embrapa Gado de Leite, Juiz de Fora, MG, 36038–330, Brazil.
João Henrique Moreira Viana
Affiliation:
Embrapa Gado de Leite, Juiz de Fora, MG, 36038–330, Brazil.
Ciro Alexandre Alves Torres
Affiliation:
Departamento de Zootecnia, Universidade Federal de Viçosa, Av. P H Rolfs s/n, Viçosa, MG, 36571–000, Brazil.
Luiz Sergio de Almeida Camargo*
Affiliation:
Embrapa Gado de Leite, Juiz de Fora, MG, 36038–330, Brazil.
*
All correspondence to: Luiz S. A. Camargo. Embrapa Gado de Leite, Juiz de Fora, MG, 36038–330, Brazil. Tel: +55 32 32494800. Fax: +55 32 32494701. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The objective of this work was to evaluate the selection of immature bovine oocytes by brilliant cresyl blue dye (BCB) and expression of transcripts MATER and ZAR1. Cumulus–oocyte complexes (COCs) from slaughterhouse ovaries were exposed to BCB diluted in mDPBS and incubated for 60 min at 38.5 °C in humidified air. After exposure those COCs were distributed in two groups, according to their cytoplasm colour: BCB+ (coloured cytoplasm) or BCB− (colourless cytoplasm). The control group was submitted to in vitro maturation (IVM) immediately after morphological selection and holding control group COCs were exposed to mDPBS without BCB but in the same incubation conditions of BCB+ and BCB− group. The COCs of all groups were submitted to IVM, in vitro fertilization (IVF) and in vitro culture (IVC). Cleavage rate (72 h post-insemination) was similar between control (65.3%) and BCB+ (64.4%) groups, but greater than (p < 0.05) holding control (49.8%) and BCB− (51.3%) groups. Blastocyst rate (192 h post-insemination) was not different between BCB+ (18.5%) and control (16.3%) groups, but greater (p < 0.05) than BCB− (8.4%) group. No difference was found for blastocyst rate between holding control group (14.2%), control and BCB+ groups. The relative expression of MATER and ZAR1 genes was evaluated by real-time PCR in immature oocytes collected from the control, holding control, BCB+ and BCB− groups. Despite the relative expression of MATER in holding control, BCB+ and BCB− were down regulated in comparison to control group there was no statistical difference (p > 0.05) in the relative expression of MATER and ZAR1 transcripts among groups. The results indicate that the BCB dye detects immature oocyte populations with different developmental competence, although no improvement in in vitro embryo production using oocytes exposed or not to BCB was observed. Development competence of immature oocytes exposed to BCB does not seem to be associated with variations in the expression of MATER and ZAR1 transcripts.

Keywords

Brilliant cresyl blueBovineGene expressionIn vitro fertilizationOocytes
Type
Research Article
Information
Zygote , Volume 18 , Issue 3 , August 2010 , pp. 209 - 216
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alm, H., Torner, H., Löhrke, B., Viergutz, T., Ghoneim, I.M. & Kanitz, W. (2005). Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brilliant cresyl blue staining before IVM as indicator for glucose-6-phosphate dehydrogenase activity. Theriogenology 63, 2194–205.CrossRefGoogle ScholarPubMed
Bhojwani, S., Alm, H., Torner, H., Kanitz, W. & Poehland, R. (2007). Selection of developmentally competent oocytes through brilliant cresyl blue stain enhances blastocyst development rate after bovine nuclear. Theriogenology 67, 341–5.CrossRefGoogle ScholarPubMed
Camargo, L.S.A., Viana, J.H.M., Ramos, A.A., Serapião, R.V., de Sa, W.F., Ferreira, A.M., Guimarães, M.F.M. & do Vale Filho, V.R. (2007). Developmental competence and expression of the Hsp 70.1 gene in oocytes obtained from Bos indicus and Bos taurus dairy cows in a tropical environment. Theriogenology 68, 626–32.CrossRefGoogle Scholar
Conover, J.C., Temeles, G.L., Zimmermann, J.W., Burke, B. & Schultz, R.M. (1991). Stage-specific expression of a family of proteins that are major products of zygotic gene activation in the mouse embryo. Dev. Biol. 144, 392–404.CrossRefGoogle ScholarPubMed
Crozet, N., Kanka, J., Motlik, J. & Fulka, J. (1986). Nucleolar fine structure and RNA synthesis in bovine oocytes from antral follicles. Gamete Res. 14, 65–73.CrossRefGoogle Scholar
Dean, J. (2002). Oocyte-specific genes regulate follicle formation, fertility and early mouse development. J. Reprod. Immunol. 53, 171–80.CrossRefGoogle ScholarPubMed
El Shourbagy, S.H., Spikings, E.C., Freitas, M. & St John, J.C. (2006). Mitochondria directly influence fertilization outcome in pig. Reproduction 131, 233–45.CrossRefGoogle ScholarPubMed
Ericsson, S.A., Boice, M.L., Funahashi, H. & Day, B.N. (1993). Assessment of porcine oocytes using brilliant cresyl blue (abstract). Theriogenology 39, 214.CrossRefGoogle Scholar
Fair, T. & Hyttel, P. (1999). Nucleolar proteins in bovine oocytes (abstract). Theriogenology 51, 371.CrossRefGoogle Scholar
Fair, T., Hyttel, P. & Greve, T. (1995). Bovine oocyte size in relationship to follicular diameter, maturational competence and rna synthesis (abstract). Theriogenology 43, 209.CrossRefGoogle Scholar
Gandolfi, F. (1996). Intra-ovarian regulation of oocyte development competence in cattle. Zygote 4, 323–6.CrossRefGoogle ScholarPubMed
Gandolfi, T.A.L.B. & Gandolfi, F. (2001). The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology 55, 1255–76.CrossRefGoogle Scholar
Ghanem, N., Hölker, M., Rings, F., Jennen, D., Tholen, E., Sirard, M.A., Torner, H., Kanitz, W., Schellander, K. & Tesfaye, D. (2007). Alterations in transcript abundance of bovine oocytes recovered at growth and dominance phases of the first follicular wave. BMC Dev. Biol. 7, 90.CrossRefGoogle ScholarPubMed
Gordon, I. (1994). Laboratory Production of Cattle Embryo. London: CAB International. Cambridge University Press.Google Scholar
Hyttel, P., Fair, T., Callesen, H. & Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.CrossRefGoogle Scholar
Ishizaki, C., Watanabe, H., Bhuiyan, M.M.U. & Fukui, Y. (2009). Developmental competence of porcine oocytes selected by brilliant cresyl blue and matured individually in a chemically defined culture medium. Theriogenology 72, 72–80.CrossRefGoogle Scholar
Kątska-Książkiewicz, L., Opiela, J. & Ryńska, B. (2007). Effects of oocyte quality, semen donor and embryo co-culture system on the efficiency of blastocyst production in goats. Theriogenology 68, 736–44.CrossRefGoogle ScholarPubMed
Liu, Z. & Foote, R.H. (1997). Effects of amino acids and alpha-amanitin on bovine embryo development in a simple protein-free medium. Mol. Reprod. Dev. 46, 278–85.3.0.CO;2-M>CrossRefGoogle Scholar
Lonergan, P., Monaghan, P., Rizos, D., Boland, M.P. & Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization and culture in vitro. Mol. Reprod. Dev. 37, 48–53.CrossRefGoogle ScholarPubMed
Machatkova, M., Krausova, K., Jokesova, E. & Tomanek, M. (2004). Developmental competence of bovine oocytes: effects of follicle size and the phase of follicular wave on in vitro embryo production. Theriogenology 61, 329–35.CrossRefGoogle ScholarPubMed
Mangia, F. & Epstein, C.J. (1975). Biochemical studies of growing mouse oocytes: preparation of oocytes and analysis of glucose-6-phosphate dehydrogenase and lactate dehydrogenase activities. Dev. Biol. 45, 211–20.CrossRefGoogle ScholarPubMed
Manjunatha, B.M., Gupta, P.S.P., Devaraj, M., Ravindra, J.P. & Nandi, S. (2007). Selection of developmentally competent buffalo oocytes by brilliant cresyl blue staining before IVM. Theriogenology 68, 1299–304.CrossRefGoogle ScholarPubMed
Minami, N., Suzuki, T. & Tsukamoto, S. (2007). Zygotic gene activation and maternal factors in mammals. J. Reprod. Dev. 53, 707–15.CrossRefGoogle ScholarPubMed
Opiela, J., Kątska-Książkiewicz, L., Lipiński, D., Słomski, R., Bzowska, M. & Ryńska, B. (2008). Interactions among activity of glucose-6-phosphate dehydrogenase in immature oocytes, expression of apoptosis-related genes Bcl-2 and Bax and developmental competence following IVP in cattle. Theriogenology 69, 546–55.CrossRefGoogle ScholarPubMed
Pennetier, S., Perreau, C., Uzbekova, S., Thélie, A., Delaleu, B., Mermillod, P. & Dalbiès-Tran, R. (2006). MATER protein expression and intracellular localization throughout folliculogenesis and preimplantation embryo development in the bovine. BMC Dev. Biol. 6, 26.CrossRefGoogle ScholarPubMed
Pennetier, S., Uzbekova, S., Perreau, C., Papillier, P., Mermillod, P. & Tran, P.R. (2004). Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15 and VASA in adult bovine tissues, oocytes and preimplantation embryos. Biol. Repr. 71, 1359–66.CrossRefGoogle ScholarPubMed
Pujol, M., López-Béjar, M. & Paramio, M.T. (2004). Developmental competence of heifer oocytes selected using the brilliant cresyl blue (BCB) test. Theriogenology 61, 735–44.CrossRefGoogle ScholarPubMed
Ramakers, C., Ruijter, J.M., Deprez, R.H. & Moorman, A.F.M. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–6.CrossRefGoogle ScholarPubMed
Roca, J., Martinez, E., Vazquez, J.M. & Lucas, X. (1998). Selection of immature pig oocytes for homologous in vitro penetration assays with the brilliant cresyl blue test. Reprod. Fert. Dev. 10, 479–85.CrossRefGoogle ScholarPubMed
Rodríguez-González, E., López-Béjar, M., Velilla, E. & Paramio, M.T. (2002). Selection of prepubertal goat oocytes using the brilliant cresyl blue test. Theriogenology 57, 1397–409.CrossRefGoogle ScholarPubMed
Schultz, R.M. (2002). The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum. Reprod. Up. 8, 323–31.CrossRefGoogle ScholarPubMed
Seshagiri, P.B., McKenzie, D.I., Bavister, B.D., Williamson, J.L. & Aiken, J.M. (1992). Golden hamster embryonic genome activation occurs at the two-cell stage: correlation with major developmental changes. Mol. Reprod. Dev. 32, 229–35.CrossRefGoogle ScholarPubMed
Sirard, M.A., Richard, F., Blondin, P. & Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–36.CrossRefGoogle ScholarPubMed
Thélie, A., Papillier, P., Pennetier, S., Perreau, C., Traverso, J.M., Uzbekova, S., Mermillod, P., Joly, C., Humblot, P. & Dalbiès-Tran, R. (2007). Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev. Biol. 7, 125.CrossRefGoogle ScholarPubMed
Tian, W.N., Braunstein, L.D., Pang, J., Stuhlmeier, K.M., Xi, Q.C., Tian, X. & Stanton, R.C. (1998). Importance of glucose-6-phosphate dehydrogenase activity for cell growth. J. Biol. Chem. 273, 10609–17.CrossRefGoogle ScholarPubMed
Tong, Z-B., Gold, L., Pfeifer, K.E., Dorward, H., Lee, E., Bondy, C.A., Dean, J. & Nelson, L.M. (2000). Mater, a maternal effect gene required for early embryonic development in mice. Nat. Genet. 26, 267–8.CrossRefGoogle Scholar
Torner, H., Ghanem, N., Ambros, C., Hölker, M., Tomek, W., Phatsara, C., Alm, H., Sirard, M.A., Kanitz, W., Schellander, K. & Tesfaye, D. (2008). Molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity. Reproduction 135, 197–212.CrossRefGoogle ScholarPubMed
Tsutsumi, O., Satoh, K., Taketani, Y. & Kato, T. (1992). Determination of enzyme activities of energy metabolism in the maturing rat oocyte. Mol. Reprod. Dev. 33, 333–7.CrossRefGoogle ScholarPubMed
Urdaneta, A., Jiménez-Macedo, A.R., Izquierdo, D. & Paramio, M.T. (2003). Supplementation with cysteamine during maturation and embryo culture on embryo development of prepubertal goat oocytes selected by the brilliant cresyl blue test. Zygote 11, 347–54.CrossRefGoogle ScholarPubMed
Urner, F. & Sakkas, D. (2005). Involvement of the pentose phosphate pathway and redox regulation in fertilization in the mouse. Mol. Reprod. Dev. 70, 494–503.CrossRefGoogle ScholarPubMed
Uzbekova, S., Roy-Sabau, M., Dalbiès-Tran, R., Perreau, C., Papillier, P., Mompart, F., Thelie, A., Pennetier, S., Cognie, J., Cadoret, V., Royere, D., Monget, P. & Mermillod, P. (2006). Zygote arrest 1 gene in pig, cattle and human: evidence of different transcript variants in male and female germ cells. Reprod. Biol. Endocrinol. 4, 12.CrossRefGoogle ScholarPubMed
Viana, J.H.M. & Camargo, L.S.A. (2007). Bovine embryo production in Brazil: a new scenario. Acta Sci. Vet. 35, 920–4.Google Scholar
Viana, J.H.M., Camargo, L.S.A., Ferreira, A.M., de Sa, W.F., Fernandes, C.A.C. & Marques Junior, A.P. (2004). Short intervals between ultrasonographically guided follicle aspiration improve oocyte quality but do not prevent establishment of dominant follicles in the Gir breed (Bos indicus) of cattle. Anim. Reprod. Sci. 84, 1–12.CrossRefGoogle Scholar
Wongsrikeao, P., Otoi, T., Yamasaki, H., Agung, B., Taniguchi, M., Naoi, H., Shimizu, R. & Nagai, T. (2006). Effects of single and double exposure to brilliant cresyl blue on the selection of porcine oocytes for in vitro production of embryos. Theriogenology 66, 366–72.CrossRefGoogle ScholarPubMed
Wood, J.R., Dumesic, D.A., Abbott, D.H. & Strauss, J.F. (2007). Molecular abnormalities in oocytes from women with polycystic ovary syndrome revealed by microarray analysis. J. Clin. Endocrinol. Metab. 92, 705–13.CrossRefGoogle ScholarPubMed
Wu, Y-G., Liu, Y., Zhou, P., Lan, G-C., Han, D., Miao, D-Q. & Tan, J-H. (2007). Selection of oocytes for in vitro maturation by brilliant cresyl blue staining: a study using the mouse model. Cell Res. 17, 722–31.CrossRefGoogle ScholarPubMed
Wu, X., Viveiros, M.M., Eppig, J.J., Bai, Y., Fitzpatrick, S.L. & Matzuk, M.M. (2003). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat. Genet. 33, 187–91.CrossRefGoogle ScholarPubMed