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Brilliant cresyl blue staining negatively affects mitochondrial functions in porcine oocytes

Published online by Cambridge University Press:  20 December 2013

E.C.S. Santos ,
D. Sato ,
T. Lucia Jr  and
H. Iwata
E.C.S. Santos
Affiliation:
Centro de Desenvolvimento Tecnológico, Universidade Federal de Pelotas, Campus Capão do Leão s/n, 96010-900, Pelotas-RS, Brazil.
D. Sato
Affiliation:
Tokyo University of Agriculture, Funako 1737 Atsugi City, 243-0037 Japan.
T. Lucia Jr
Affiliation:
Centro de Desenvolvimento Tecnológico, Universidade Federal de Pelotas, Campus Capão do Leão s/n, 96010-900, Pelotas-RS, Brazil.
H. Iwata*
Affiliation:
Tokyo University of Agriculture, Funako 1737 Atsugi City, 243-0037 Japan. Tokyo University of Agriculture, Funako 1737 Atsugi City, 243-0037 Japan.
*
All correspondence to: H. Iwata. Tokyo University of Agriculture, Funako 1737 Atsugi City, 243-0037Japan. e-mail: [email protected]
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Summary

The aim of the present study was to examine the effects of brilliant cresyl blue (BCB) staining on mitochondrial functions in porcine oocytes. Cumulus–oocyte complexes (COCs) collected from slaughterhouse-derived porcine ovaries were cultured with (13 μM) or without (0 μM, control) BCB for 60 min. Mitochondrial functions in oocytes were examined immediately after staining or after in vitro maturation. The BCB-stained oocytes produced reactive oxygen species (ROS) at higher levels than control oocytes immediately after staining (2.2-fold, P < 0.001) and after maturation (1.7-fold, P < 0.001). The adenosine triphosphate (ATP) content and mitochondrial membrane potential (MMP) in oocytes were similar for the two groups immediately after staining. However, ATP and relative MMP levels were significantly (P < 0.05) lower in BCB-treated oocytes than in the control (2.18 versus 2.83 pM and 0.82 versus 1.0, respectively). There was no difference in mitochondrial DNA copy number between the two groups after maturation. The ATP content in early developmental stage embryos (3 days after parthenogenetic activation) was lower in the BCB-stained group than that in the control group but the difference was not significant. In conclusion, BCB staining of oocytes at the immature stage compromises mitochondrial functions throughout oocyte maturation, but function is restored during early embryo development.

Keywords

BCB stainingMitochondriaOocytePig
Type
Research Article
Information
Zygote , Volume 23 , Issue 3 , June 2015 , pp. 352 - 359
Copyright
Copyright © Cambridge University Press 2013 

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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.Google Scholar
Castaneda, C.A., Kaye, P., Pantaleon, M., Phillips, N., Norman, S., Fry, R. & D'Occhio, M.J. (2013). Lipid content, active mitochondria and brilliant cresyl blue staining in bovine oocytes. Theriogenology 79, 417–22.Google Scholar
Catalá, M.G., Izquierdo, D., Uzbekova, S., Morató, R., Roura, M., Romaguera, R., Papillier, P. & Paramio, M.T. (2011). Brilliant cresyl blue stain selects largest oocytes with highest mitochondrial activity, maturation-promoting factor activity and embryo developmental competence in prepubertal sheep. Reproduction 142, 517–27.Google Scholar
Catalá, M.G., Izquierdo, D., Rodríguez-Prado, M., Hammami, S. & Paramio, M.T. (2012). Effect of oocyte quality on blastocyst development after in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI) in a sheep model. Fertil. Steril. 97, 1004–8.CrossRefGoogle Scholar
Fujii, W. & Funahashi, H. (2009). Exogenous adenosine reduces the mitochondrial membrane potential of murine oocytes during the latter half of in vitro maturation and pronuclear formation following chemical activation. J. Reprod. Dev. 55, 187–93.Google Scholar
Ge, H., Tollner, T.L., Hu, Z., Da, M., Li, X., Guan, H., Shan, D., Lu, J., Huang, C. & Dong, Q. (2012). Impaired mitochondrial function in murine oocytes is associated with controlled ovarian hyperstimulation and in vitro maturation. Reprod. Fertil. Dev. 24, 945–52.Google Scholar
Ishizaki, C., Watanabe, H., Bhuiyan, M.M. & 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
Iwata, H., Goto, H., Tanaka, H., Sakaguchi, Y., Kimura, K., Kuwayama, T., Monji, Y. (2011). Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev. 23, 424–32.CrossRefGoogle ScholarPubMed
Janowski, D., Salilew-Wondim, D., Torner, H., Tesfaye, D., Ghanem, N., Tomek, W., El-Sayed, A., Schellander, K. & Hölker, M. (2012). Incidence of apoptosis and transcript abundance in bovine follicular cells is associated with the quality of the enclosed oocyte. Theriogenology 78, 656–69.CrossRefGoogle ScholarPubMed
Kang, J. & Pervaiz, S. (2012). Mitochondria: redox metabolism and dysfunction. Biochem. Res. Int. 2012, 896751.Google Scholar
Kempisty, B., Jackowska, M., Piotrowska, H., Antosik, P., Woźna, M., Bukowska, D., Brüssow, K. P. & Jaśkowski, J. M. (2011). Zona pellucida glycoprotein 3 (pZP3) and integrin β2 (ITGB2) mRNA and protein expression in porcine oocytes after single and double exposure to brilliant cresyl blue test. Theriogenology 75, 1525–35.Google Scholar
Mirshamsi, S.M., Karamishabankareh, H., Ahmadi-Hamedani, M., Soltani, L., Hajarian, H. & Abdolmohammadi, A.R. (2013). Combination of oocyte and zygote selection by brilliant cresyl blue (BCB) test enhanced prediction of developmental potential to the blastocyst in cattle. Anim. Reprod. Sci. 136, 245–51.Google Scholar
Mohammadi-Sangcheshmeh, A., Held, E., Ghanem, N., Rings, F., Salilew-Wondim, D., Tesfaye, D., Sieme, H., Schellander, K. & Hoelker, M. (2011). G6PDH-activity in equine oocytes correlates with morphology, expression of candidate genes for viability, and preimplantative in vitro development. Theriogenology 76, 1215–26.Google Scholar
Pawlak, P., Pers-Kamczyc, E., Renska, N., Kubickova, S. & Lechniak, D. (2011). Disturbances of nuclear maturation in BCB positive oocytes collected from peri-pubertal gilts. Theriogenology 75, 832–40.Google Scholar
Pereira, G.R., Lorenzo, P.L., Carneiro, G.F., Bilodeau-Goeseels, S., Kastelic, J.P., Esteller-Vico, A., Lopez-Bejar, M. & Liu, I.K. (2013). Selection of developmentally competent immature equine oocytes with brilliant cresyl blue stain prior to in vitro maturation with equine growth hormone. Zygote 1, 1–5.Google Scholar
Petters, R.M. & Wells, K.D. (1993). Culture of pig embryos. J. Reprod. Fertil. Suppl. 48, 61–73.Google Scholar
Silva, D.S., Rodriguez, P., Galuppo, A., Arruda, N.S. & Rodrigues, J.L. (2013). Selection of bovine oocytes by brilliant cresyl blue staining: effect on meiosis progression, organelle distribution and embryo development. Zygote 21, 250–5.CrossRefGoogle ScholarPubMed
Somfai, T., Inaba, Y., Watanabe, S., Geshi, M. & Nagai, T. (2012). Follicular fluid supplementation during in vitro maturation promotes sperm penetration in bovine oocytes by enhancing cumulus expansion and increasing mitochondrial activity in oocytes. Reprod. Fertil. Dev. 24, 743–52.Google Scholar
Stojkovic, M., Machado, S.A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, P.B. & Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–9.CrossRefGoogle ScholarPubMed
Sun, X. S., Liu, Y., Yue, K.Z., Ma, S.F. & Tan, J.H. (2004). Changes in germinal vesicle (GV) chromatin configurations during growth and maturation of porcine oocytes. Mol. Reprod. Dev. 69, 228–34.CrossRefGoogle ScholarPubMed
Van Blerkom, J. & Davis, P. (2007). Mitochondrial signaling and fertilization. Mol. Hum. Reprod. 13, 759–70.CrossRefGoogle ScholarPubMed
Wang, L., Lin, J., Huang, J., Wang, J., Zhao, Y. & Chen, T. (2012). Selection of ovine oocytes by brilliant cresyl blue staining. J. Biomed. Biotech. 2012, 161372.Google Scholar
Weber, T.A. & Reichert, A.S. (2010). Impaired quality control of mitochondria: aging from a new perspective. Exp. Gerontol. 45, 503–11.Google 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.Google Scholar
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I.M. & Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–9.Google Scholar
Zhang, W., Liu, Y., An, Z., Huang, D., Qi, Y. & Zhang, Y. (2011). Mediating effect of ROS on mtDNA damage and low ATP content induced by arsenic trioxide in mouse oocytes. Toxicol. In Vitro 25, 979–84.Google Scholar