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The protective effect of melatonin on the in vitro development of yak embryos against hydrogen peroxide-induced oxidative injury

Published online by Cambridge University Press:  23 April 2019

Wei Peng ,
Mengtong Lei ,
Jun Zhang  and
Yong Zhang Open the ORCID record for Yong Zhang [Opens in a new window]
Wei Peng*
Affiliation:
College of Veterinary Medicine, Northwest A&F University, Yangling 712100, Shaanxi, China
Mengtong Lei
Affiliation:
College of Veterinary Medicine, Northwest A&F University, Yangling 712100, Shaanxi, China
Jun Zhang*
Affiliation:
Institute of Veterinary Medicine, Qinghai Academy of Animal Science and Veterinary Medicine, Xining, Qinghai, China
Yong Zhang
Affiliation:
College of Veterinary Medicine, Northwest A&F University, Yangling 712100, Shaanxi, China
*
*Author for correspondence: Jun Zhang. Institute of Veterinary Medicine, Qinghai Academy of Animal Science and Veterinary Medicine, Xining, Qinghai, China. Tel:/Fax: +86 29 87080092. E-mail: zhangjunxn2003@163.com; Yong Zhang. College of Veterinary Medicine, Northwest A&F University, Yangling 712100, Shaanxi, China. E-mail: zhangy712100@yeah.net
*Author for correspondence: Jun Zhang. Institute of Veterinary Medicine, Qinghai Academy of Animal Science and Veterinary Medicine, Xining, Qinghai, China. Tel:/Fax: +86 29 87080092. E-mail: zhangjunxn2003@163.com; Yong Zhang. College of Veterinary Medicine, Northwest A&F University, Yangling 712100, Shaanxi, China. E-mail: zhangy712100@yeah.net
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Summary

Melatonin plays a critical role in several types of cells as an antioxidant to protect intracellular molecules from oxidative stress. The anti-oxidation effect of melatonin in yak embryos is largely unknown. We report that melatonin can protect the development of yak preimplantation embryos against oxidative stress induced by hydrogen peroxide (H2O2). Therefore, the quality of blastocysts developed from zygotes exposed to H2O2 was promoted. In addition, we observed that melatonin reduced H2O2-induced intracellular reactive oxygen species (ROS) levels and prevented mitochondrial dysfunction in zygotes. These phenomena revealed the effective antioxidant activity of melatonin to prevent oxidative stress in yak embryos. To determine the underlying mechanism, we further demonstrated that melatonin protected preimplantation embryos from oxidative damage by preserving antioxidative enzymes. Collectively, these results confirmed the anti-oxidation effect of melatonin in yak embryos that significantly improved the quantity and quality of blastocysts in the in vitro production of embryos in yaks.

Keywords

EmbryoOxidative stressReproductionYakZygote
Type
Research Article
Information
Zygote , Volume 27 , Issue 3 , June 2019 , pp. 118 - 125
Copyright
© Cambridge University Press 2019 

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Footnotes

†

These authors contributed equally to this study.

References

Abe, Y, Sakairi, T, Beeson, C Kopp, JB (2013) TGF-β1 stimulates mitochondrial oxidative phosphorylation and generation of reactive oxygen species in cultured mouse podocytes, mediated in part by the mTOR pathway. Am J Physiol Renal Physiol 305, F1477–f1490.Google Scholar
Areti, A, Komirishetty, P, Akuthota, M, Malik, RA Kumar, A (2017) Melatonin prevents mitochondrial dysfunction and promotes neuroprotection by inducing autophagy during oxaliplatin-evoked peripheral neuropathy. J Pineal Res 62, doi: 10.1111/jpi.12393.Google Scholar
Asghari, MH, Abdollahi, M, de Oliveira, MR Nabavi, SM (2017) A review of the protective role of melatonin during phosphine-induced cardiotoxicity: focus on mitochondrial dysfunction, oxidative stress and apoptosis. J Pharm Pharmacol 69, 236–243.Google Scholar
Avdesh, A, Wong, P, Martins, RN Martin-Iverson, MT (2011) Memory function in a mouse genetic model of Alzheimer’s disease. J Alzheimers Dis 25, 433–444.Google Scholar
Barbato, V, Talevi, R, Braun, S, Merolla, A, Sudhakaran, S, Longobardi, S Gualtieri, R (2017) Supplementation of sperm media with zinc, d-aspartate and co-enzyme Q10 protects bull sperm against exogenous oxidative stress and improves their ability to support embryo development. Zygote 25, 168–175.Google Scholar
Cheng, NH, Zhang, W, Chen, WQ, Jin, J, Cui, X, Butte, NF, Chan, L Hirschi, KD (2011) A mammalian monothiol glutaredoxin, Grx3, is critical for cell cycle progression during embryogenesis. FEBS J 278, 2525–2539.Google Scholar
Chowdhury, SR, Ray, U, Chatterjee, BP Roy, SS (2017) Targeted apoptosis in ovarian cancer cells through mitochondrial dysfunction in response to Sambucus nigra agglutinin. Cell Death Dis 8, e2762.Google Scholar
Czechowska, G, Celinski, K, Korolczuk, A, Wojcicka, G, Dudka, J, Bojarska, A Reiter, RJ (2015) Protective effects of melatonin against thioacetamide-induced liver fibrosis in rats. J Physiol Pharmacol 66, 567–579.Google Scholar
Delwing-de Lima, D, Sasso, S, Dalmedico, L, Delwing-Dal Magro, D, Pereira, EM Wyse, ATS (2017) Argininic acid alters markers of cellular oxidative damage in vitro: Protective role of antioxidants. Exp Toxicol Pathol 69, 605–611.Google Scholar
Do, GY, Kim, JW, Park, HJ, Yoon, SB, Park, JY, Yang, SG, Jung, BD, Kwon, YS, Kang, MJ, Song, BS, Kim, SU, Chang, KT Koo, DB (2017) Native plants (Phellodendron amurense and Humulus japonicus) extracts act as antioxidants to support developmental competence of bovine blastocysts. Asian-Australas J Anim Sci 30, 1245–1252.Google Scholar
Goswami, S Haldar, C (2014) UVB irradiation severely induces systemic tissue injury by augmenting oxidative load in a tropical rodent: efficacy of melatonin as an antioxidant. J Photochem Photobiol B 141, 84–192.Google Scholar
Hamdy, SM, Shabaan, AM, Abdel Latif, AKM, Abdel-Aziz, AM Amin, AM (2017) Protective effect of hesperidin and tiger nut against acrylamide toxicity in female rats. Exp Toxicol Pathol 69, 580–588.Google Scholar
Huo, X, Liu, C, Gao, L, Xu, X, Zhu, N Cao, L (2017) Hepatoprotective effect of aqueous extract from the seeds of Orychophragmus violaceus against liver injury in mice and HepG2 cells. Int J Mol Sci 18, pii E1197.Google Scholar
Kim, MG, Kim, DH, Lee, HR, Lee, JS, Jin, SJ Lee, HT (2017) Sirtuin inhibition leads to autophagy and apoptosis in porcine preimplantation blastocysts. Biochem Biophys Res Commun 488, 603–608.Google Scholar
Liu, LF, Qin, Q, Qian, ZH, Shi, M, Deng, QC, Zhu, WP, Zhang, H, Tao, XM Liu, Y (2014) Protective effects of melatonin on ischemia-reperfusion induced myocardial damage and hemodynamic recovery in rats. Eur Rev Med Pharmacol Sci 18, 3681–3686.Google Scholar
Liu, J, Zhang, Y, Chen, L, Yu, F, Li, X, Dan, T, Zhao, J Zhou, S (2017) Polyphyllin I induces G2/M phase arrest and apoptosis in U251 human glioma cells via mitochondrial dysfunction and the JNK signaling pathway. Acta Biochim Biophys Sin (Shanghai) 49, 479–486.Google Scholar
Loren, P, Sanchez, R, Arias, ME, Felmer, R, Risopatron, J Cheuqueman, C (2017) Melatonin scavenger properties against oxidative and nitrosative stress: impact on gamete handling and in vitro embryo production in humans and other mammals. Int J Mol Sci 18, pii E1119.Google Scholar
Maarman, GJ, Andrew, BM, Blackhurst, DM Ojuka, EO (2017) Melatonin protects against uric acid-induced mitochondrial dysfunction, oxidative stress, and triglyceride accumulation in C2C12 myotubes. J Appl Physiol 122, 1003–1010.Google Scholar
Marinho, LS, Sanches, BV, Rosa, CO, Tannura, JH, Rigo, AG, Basso, AC, Pontes, JH Seneda, MM (2015) Pregnancy rates to fixed embryo transfer of vitrified IVP Bos indicus, Bos taurus or Bos indicus × Bos taurus embryos. Reprod Domest Anim 50, 807–811.Google Scholar
Mata-Campuzano, M, Alvarez-Rodriguez, M, del Olmo, E, Fernandez-Santos, MR, Garde, JJ Martinez-Pastor, F (2012) Quality, oxidative markers and DNA damage (DNA) fragmentation of red deer thawed spermatozoa after incubation at 37°C in presence of several antioxidants. Theriogenology 78, 1005–1019.Google Scholar
Mehrzadi, S, Safa, M, Kamrava, SK, Darabi, R, Hayat, P Motevalian, M (2016) Protective mechanisms of melatonin against hydrogen-peroxide-induced toxicity in human bone-marrow-derived mesenchymal stem cells. Can J Physiol Pharmacol 95, 773–786.Google Scholar
Moreno, D, Neira, A, Dubreil, L, Liegeois, L, Destrumelle, S, Michaud, S, Thorin, C, Briand-Amirat, L, Bencharif, D Tainturier, D (2015) In vitro bovine embryo production in a synthetic medium: embryo development, cryosurvival, and establishment of pregnancy. Theriogenology 84, 1053–1060.Google Scholar
Nikseresht, M, Toori, MA, Rahimi, HR, Fallahzadeh, AR, Kahshani, IR, Hashemi, SF, Bahrami, S Mahmoudi, R (2017) Effect of antioxidants (β-mercaptoethanol and cysteamine) on assisted reproductive technology in vitro. J Clin Diagn Res 11, BC10–BC14.Google Scholar
Pan, Y, Cui, Y, Baloch, AR, Fan, J, He, J, Li, G, Zheng, H, Zhang, Y, Lv, P Yu, S (2015) Insulinlike growth factor I improves yak (Bos grunniens) spermatozoa motility and the oocyte cleavage rate by modulating the expression of Bax and Bcl-2. Theriogenology 84, 756–762.Google Scholar
Rahman, M, Halade, GV, Bhattacharya, A Fernandes, G (2009) The fat-1 transgene in mice increases antioxidant potential, reduces pro-inflammatory cytokine levels, and enhances PPAR-γ and SIRT-1 expression on a calorie restricted diet. Oxid Med Cell Longev 2, 307–316.Google Scholar
Sharafati-Chaleshtori, R, Shirzad, H, Rafieian-Kopaei, M Soltani, A (2017) Melatonin and human mitochondrial diseases. J Res Med Sci 22, 2.Google Scholar
Sirard, MA (2017) The influence of in vitro fertilization and embryo culture on the embryo epigenetic constituents and the possible consequences in the bovine model. J Dev Orig Health Dis 8, 411–417.Google Scholar
Song, C, Peng, W, Yin, S, Zhao, J, Fu, B, Zhang, J, Mao, T, Wu, H Zhang, Y (2016) Melatonin improves age-induced fertility decline and attenuates ovarian mitochondrial oxidative stress in mice. Sci Rep 6, 35165.Google Scholar
Takahashi, M (2012) Oxidative stress and redox regulation on in vitro development of mammalian embryos. J Reprod Dev 58, 1–9.Google Scholar
Takahashi, T, Inaba, Y, Somfai, T, Kaneda, M, Geshi, M, Nagai, T Manabe, N (2013) Supplementation of culture medium with l-carnitine improves development and cryotolerance of bovine embryos produced in vitro . Reprod Fertil Dev 25, 589–599.Google Scholar
Tian, X, Wang, F, He, C, Zhang, L, Tan, D, Reiter, RJ, Xu, J, Ji, P Liu, G (2014) Beneficial effects of melatonin on bovine oocytes maturation: a mechanistic approach. J Pineal Res 57, 239–247.Google Scholar
Tian, X, Wang, F, Zhang, L, Ji, P, Wang, J, Lv, D, Li, G, Chai, M, Lian, Z Liu, G (2017) Melatonin promotes the in vitro development of microinjected pronuclear mouse embryos via its anti-oxidative and anti-apoptotic effects. Int J Mol Sci 18, pii E988.Google Scholar
Zhou, L, Zhao, D, An, H, Zhang, H, Jiang, C Yang, B (2015) Melatonin prevents lung injury induced by hepatic ischemia-reperfusion through anti-inflammatory and anti-apoptosis effects. Int Immunopharmacol 29, 462–467.Google Scholar