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Protective Effects of Coenzyme Q10 on Developmental Competence of Porcine Early Embryos

Published online by Cambridge University Press:  07 June 2017

Shuang Liang ,
Ying Jie Niu ,
Kyung-Tae Shin  and
Xiang-Shun Cui
Shuang Liang
Affiliation:
Department of Animal Science, Chungbuk National University, Cheongju, Chungbuk, 361-763, Republic of Korea
Ying Jie Niu
Affiliation:
Department of Animal Science, Chungbuk National University, Cheongju, Chungbuk, 361-763, Republic of Korea
Kyung-Tae Shin
Affiliation:
Department of Animal Science, Chungbuk National University, Cheongju, Chungbuk, 361-763, Republic of Korea
Xiang-Shun Cui*
Affiliation:
Department of Animal Science, Chungbuk National University, Cheongju, Chungbuk, 361-763, Republic of Korea
*
*Corresponding author.xscui@cbnu.ac.kr
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Abstract

Coenzyme Q10 (Q10) plays an important role in the cellular antioxidant system by protecting the cells from free-radical oxidative damage and apoptosis. In the present study, we have investigated the effect of Q10 on the preimplantation development of porcine parthenogenetic embryos, as well as the underlying mechanism. The results showed that 100 μM was the optimal concentration of Q10, which resulted in significantly increased cleavage and blastocyst formation rates and improvement of blastocyst quality. Q10 improved the blastocyst hatching rate and cellular proliferation rate in hatching blastocysts and increased the expression of hatching-related genes. Furthermore, Q10 not only decreased reactive oxygen species production, DNA damage levels, and apoptosis in the blastocysts from H2O2-induced oxidative injury, but also maintained mitochondrial function. Taken together, these results indicate that Q10 has beneficial effects on the development of porcine parthenogenetic embryos by preventing oxidative damage and apoptosis.

Keywords

Q10embryonic developmentoxidative damageimmunofluorescence histochemistry
Type
Biological Science Applications
Information
Microscopy and Microanalysis , Volume 23 , Issue 4 , August 2017 , pp. 849 - 858
Copyright
© Microscopy Society of America 2017 

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References

Aitken, R.J., De Iuliis, G.N., Finnie, J.M., Hedges, A. & McLachlan, R.I. (2010). Analysis of the relationships between oxidative stress, DNA damage and sperm vitality in a patient population: development of diagnostic criteria. Hum Reprod 25(10), 2415–2426.CrossRefGoogle Scholar
Anand, V., Singh, K., Palta, P., Manik, R., Singla, S. & Chauhan, M. (2010). Apoptosis and effect of cysteamine supplementation in IVM and IVC media during in vitro development of buffalo (Bubalus bubalis) embryos. Rev Vet 21(1), 822–825.Google Scholar
Balercia, G., Mancini, A., Paggi, F., Tiano, L., Pontecorvi, A., Boscaro, M., Lenzi, A. & Littarru, G.P. (2009). Coenzyme Q10 and male infertility. J Endocrinol Invest 32(7), 626–632.Google Scholar
Bentov, Y., Hannam, T., Jurisicova, A., Esfandiari, N. & Casper, R.F. (2014). Coenzyme Q10 supplementation and oocyte aneuploidy in women undergoing IVF–ICSI treatment. Clin Med Insights Reprod Health 8, 31.Google Scholar
Bhagavan, H.N. & Chopra, R.K. (2006). Coenzyme Q10: absorption, tissue uptake, metabolism and pharmacokinetics. Free Radic Res 40(5), 445–453.Google Scholar
Bohrer, R.C., Che, L., Gonçalves, P.B., Duggavathi, R. & Bordignon, V. (2013). Phosphorylated histone H2A. x in porcine embryos produced by IVF and somatic cell nuclear transfer. Reproduction 146(4), 325–333.Google Scholar
Boiani, M., Gambles, V. & Schöler, H. (2004). ATP levels in clone mouse embryos. Cytogenet Genome Res 105(2–4), 270–278.Google Scholar
Burstein, E., Perumalsamy, A., Bentov, Y., Esfandiari, N., Jurisicova, A. & Casper, R. (2009). Co-enzyme Q10 supplementation improves ovarian response and mitochondrial function in aged mice. Fertil Steril 92(3), S31.Google Scholar
Choi, J., Park, S.M., Lee, E., Kim, J.H., Jeong, Y.I., Lee, J.Y., Park, S.W., Kim, H.S., Hossein, M.S. & Jeong, Y.W. (2008). Anti‐apoptotic effect of melatonin on preimplantation development of porcine parthenogenetic embryos. Mol Reprod Dev 75(7), 1127–1135.Google Scholar
Dai, J., Wu, C., Muneri, C.W., Niu, Y., Zhang, S., Rui, R. & Zhang, D. (2015). Changes in mitochondrial function in porcine vitrified MII-stage oocytes and their impacts on apoptosis and developmental ability. Cryobiology 71(2), 291–298.CrossRefGoogle ScholarPubMed
Favetta, L.A., John, E.J.S., King, W.A. & Betts, D.H. (2007). High levels of p66 shc and intracellular ROS in permanently arrested early embryos. Free Radic Biol Med 42(8), 1201–1210.Google Scholar
Ferris, J., Mahboubi, K., MacLusky, N., King, W.A. & Favetta, L.A. (2016). BPA exposure during in vitro oocyte maturation results in dose-dependent alterations to embryo development rates, apoptosis rate, sex ratio and gene expression. Reprod Toxicol 59, 128–138.Google Scholar
Forsmark-Andrée, P., Lee, C.-P., Dallner, G. & Ernster, L. (1997). Lipid peroxidation and changes in the ubiquinone content and the respiratory chain enzymes of submitochondrial particles. Free Radic Biol Med 22(3), 391–400.Google Scholar
Funahashi, H. (2003). Polyspermic penetration in porcine IVM–IVF systems. Reprod Fertil Dev 15(3), 167–177.Google Scholar
Gardner, D.K., Lane, M., Stevens, J., Schlenker, T. & Schoolcraft, W.B. (2000). Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertil Steril 73(6), 1155–1158.Google Scholar
Goossens, K., Van Soom, A., Van Zeveren, A., Favoreel, H. & Peelman, L.J. (2009). Quantification of fibronectin 1 (FN1) splice variants, including two novel ones, and analysis of integrins as candidate FN1 receptors in bovine preimplantation embryos. BMC Dev Biol 9(1), 1.Google Scholar
Goto, Y., Noda, Y., Mori, T. & Nakano, M. (1993). Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic Biol Med 15(1), 69–75.Google Scholar
Gualtieri, R., Barbato, V., Fiorentino, I., Braun, S., Rizos, D., Longobardi, S. & Talevi, R. (2014). Treatment with zinc, d-aspartate, and coenzyme Q10 protects bull sperm against damage and improves their ability to support embryo development. Theriogenology 82(4), 592–598.Google Scholar
Guerin, P., El Mouatassim, S. & Menezo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 7(2), 175–189.Google Scholar
Guo, J., Zhao, M.-H., Liang, S., Choi, J.-W., Nam-Hyung, K. & Cui, X.-S. (2016). Liver receptor homolog 1 influences blastocyst hatching in pigs. J Reprod Dev 62(3), 297–303.CrossRefGoogle Scholar
Huang, J.-C., Wun, W.-S.A., Goldsby, J.S., Matijevic-Aleksic, N. & Wu, K.K. (2004). Cyclooxygenase-2-derived endogenous prostacyclin enhances mouse embryo hatching. Hum Reprod 19(12), 2900–2906.Google Scholar
Johnson, M.H. & Nasresfahani, M.H. (1994). Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? Bioessays 16(1), 31–38.CrossRefGoogle ScholarPubMed
Kitagawa, Y., Suzuki, K., Yoneda, A. & Watanabe, T. (2004). Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62(7), 1186–1197.Google Scholar
Liang, S., Yuan, B., Kwon, J.-W., Ahn, M., Cui, X.-S., Bang, J.K. & Kim, N.-H. (2016). Effect of antifreeze glycoprotein 8 supplementation during vitrification on the developmental competence of bovine oocytes. Theriogenology 86(2), 485–494.e481.Google Scholar
Liang, S., Zhao, M.H., Ock, S.A., Kim, N.H. & Cui, X.S. (2015). Fluoride impairs oocyte maturation and subsequent embryonic development in mice. Environ Toxicol 31(11), 1486–1495.Google Scholar
McEvoy, T., Coull, G., Broadbent, P., Hutchinson, J. & Speake, B. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil 118(1), 163–170.Google Scholar
McManus, K.J. & Hendzel, M.J. (2005). ATM-dependent DNA damage-independent mitotic phosphorylation of H2AX in normally growing mammalian cells. Mol Biol Cell 16(10), 5013–5025.Google Scholar
Nasr-Esfahani, M.H., Aitken, J.R. & Johnson, M.H. (1990). Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109(2), 501–507.Google Scholar
Orsi, N.M. & Leese, H.J. (2001). Protection against reactive oxygen species during mouse preimplantation embryo development: role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Mol Reprod Dev 59(1), 44–53.Google Scholar
Pakrasi, P.L. & Jain, A.K. (2007). Evaluation of cyclooxygenase 2 derived endogenous prostacyclin in mouse preimplantation embryo development in vitro. Life Sci 80(16), 1503–1507.Google Scholar
Ptak, G., Zacchini, F., Czernik, M., Fidanza, A., Palmieri, C., Della Salda, L., Scapolo, P.A. & Loi, P. (2012). A short exposure to polychlorinated biphenyls deregulates cellular autophagy in mammalian blastocyst in vitro. Hum Reprod 27(4), 1034–1042.Google Scholar
Quiles, J.L., Ochoa, J.J., Huertas, J.R. & Mataix, J. (2004). Coenzyme Q supplementation protects from age-related DNA double-strand breaks and increases lifespan in rats fed on a PUFA-rich diet. Exp Gerontol 39(2), 189–194.Google Scholar
Schultz, J.F., Mayernik, L., Rout, U.K. & Armant, D.R. (1997). Integrin trafficking regulates adhesion to fibronectin during differentiation of mouse peri-implantation blastocysts. Dev Genet 21(1), 31–43.Google Scholar
Small, D.M., Coombes, J.S., Bennett, N., Johnson, D.W. & Gobe, G.C. (2012). Oxidative stress, anti‐oxidant therapies and chronic kidney disease. Nephrology 17(4), 311–321.CrossRefGoogle ScholarPubMed
Turi, A., Giannubilo, S.R., Brugè, F., Principi, F., Battistoni, S., Santoni, F., Tranquilli, A.L., Littarru, G. & Tiano, L. (2012). Coenzyme Q10 content in follicular fluid and its relationship with oocyte fertilization and embryo grading. Arch Gynecol Obstet 285(4), 1173–1176.CrossRefGoogle ScholarPubMed
Valko, M., Leibfritz, D., Moncol, J., Cronin, M.T., Mazur, M. & Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1), 44–84.Google Scholar
Van Blerkom, J., Davis, P. & Alexander, S. (2003). Inner mitochondrial membrane potential (ΔΨm), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes. Hum Reprod 18(11), 2429–2440.CrossRefGoogle ScholarPubMed
Van Thuan, N., Harayama, H. & Miyake, M. (2002). Characteristics of preimplantational development of porcine parthenogenetic diploids relative to the existence of amino acids in vitro. Biol Reprod 67(6), 1688–1698.Google Scholar