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Effect of antioxidants on preimplantation embryo development in vitro: a review

Published online by Cambridge University Press:  14 January 2021

Sam Zarbakhsh Open the ORCID record for Sam Zarbakhsh [Opens in a new window]
Sam Zarbakhsh*
Affiliation:
1Nervous System Stem Cells Research Center, Semnan University of Medical Sciences, Semnan, Iran 2Department of Anatomy, Faculty of Medicine, Semnan University of Medical Sciences, Semnan, Iran
*
Author for correspondence: Sam Zarbakhsh. Nervous System Stem Cells Research Center, Semnan University of Medical Sciences, Semnan, Iran. E-mail: [email protected]
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Summary

In vitro culture of the embryo is a useful method to treat infertility that shows embryo potential for selecting the best one to transfer and successfully implantation. However, embryo development in vitro is affected by oxidative stresses such as reactive oxygen species that may damage embryo development. Antioxidants are molecules found in fruits, vegetables, and fish that play an important role in reducing oxidative processes. In the natural environment, there is a physiological antioxidant system that protects embryos against oxidative damage. This antioxidant system does not exist in vitro. Antioxidants act as free radical scavengers and protect cells or repair damage done by free radicals. Various studies have shown that adding antioxidants into embryo culture medium improves embryo development in vitro. This review article emphasizes different aspects of various antioxidants, including types, functions and mechanisms, on the growth improvement of different species of embryos in vitro.

Keywords

AntioxidantsEmbryo developmentIn vitroOxidative stress
Type
Review Article
Information
Zygote , Volume 29 , Issue 3 , June 2021 , pp. 179 - 193
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Abdelrazik, H, Sharma, R, Mahfouz, R and Agarwal, A (2009). l-Carnitine decreases DNA damage and improves the in vitro blastocyst development rate in mouse embryos. Fertil Steril 91, 589–96.CrossRefGoogle ScholarPubMed
Abe, T, Kawahara-Miki, R, Hara, T, Noguchi, T, Hayashi, T, Shirasuna, K, Kuwayama, T and Iwata, H (2017). Modification of mitochondrial function, cytoplasmic lipid content and cryosensitivity of bovine embryos by resveratrol. J Reprod Dev 63, 455–61.CrossRefGoogle ScholarPubMed
Abramov, JP and Wells, PG (2011). Embryoprotective role of endogenous catalase in acatalasemic and human catalase-expressing mouse embryos exposed in culture to developmental and phenytoin-enhanced oxidative stress. Toxicol Sci 120, 428–38.CrossRefGoogle ScholarPubMed
Agarwal, A, Aponte-Mellado, A, Premkumar, BJ, Shaman, A and Gupta, S (2012). The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol 10, 49.CrossRefGoogle ScholarPubMed
Agarwal, A, Said, TM, Bedaiwy, MA, Banerjee, J and Alvarez, JG (2006). Oxidative stress in an assisted reproductive techniques setting. Fertil Steril 86, 503–12.CrossRefGoogle Scholar
Ainsworth, AJ, Fredrickson, JR and Morbeck, DE (2017). Improved detection of mineral oil toxicity using an extended mouse embryo assay. J Assist Reprod Genet 34, 391–7.CrossRefGoogle ScholarPubMed
Aitken, RJ and Clarkson, JS (1988). Significance of reactive oxygen species and antioxidants in defining the efficacy of sperm preparation techniques. J Androl 9, 367–76.CrossRefGoogle ScholarPubMed
Aitken, RJ, Finnie, JM, Muscio, L, Whiting, S, Connaughton, HS, Kuczera, L, Rothkirch, TB and De Iuliis, GN (2014). Potential importance of transition metals in the induction of DNA damage by sperm preparation medium. Hum Reprod 29, 2136–47.CrossRefGoogle Scholar
Ali, I, Liu, HX, Zhong-Shu, L, Dong-Xue, M, Xu, L, Shah, SZA, Ullah, O and Nan-Zhu, F (2018). Reduced glutathione alleviates tunicamycin-induced endoplasmic reticulum stress in mouse preimplantation embryos. J Reprod Dev 64, 15–24.CrossRefGoogle ScholarPubMed
Anjos, JC, Aguiar, FLN, Sa, NAR, Souza, JF, Cibin, FWS, Alves, BG, Santos, RR and Figueiredo, JR (2019). Anethole improves blastocysts rates together with antioxidant capacity when added during bovine embryo culture rather than in the in vitro maturation medium. Zygote 27, 382–5.CrossRefGoogle ScholarPubMed
Arenas, J, Rubio, JC, Martin, MA and Campos, Y (1998). Biological roles of l-carnitine in perinatal metabolism. Early Hum Dev 53(Suppl), S43–50.CrossRefGoogle ScholarPubMed
Asgari, Z, Ghasemian, F, Ramezani, M and Bahadori, MH (2012). The effect of melatonin on the developmental potential and implantation rate of mouse embryos. Cell J 14, 203–8.Google ScholarPubMed
Augustyniak, A, Bartosz, G, Cipak, A, Duburs, G, Horakova, L, Luczaj, W, Majekova, M, Odysseos, AD, Rackova, L, Skrzydlewska, E, Stefek, M, Strosova, M, Tirzitis, G, Venskutonis, PR, Viskupicova, J, Vraka, PS and Zarkovic, N (2010). Natural and synthetic antioxidants: an updated overview. Free Radic Res 44, 1216–62.CrossRefGoogle Scholar
Baek, IJ, Yon, JM, Lee, BJ, Yun, YW, Yu, WJ, Hong, JT, Ahn, B, Kim, YB, Kim, DJ, Kang, JK and Nam, SY (2005). Expression pattern of cytosolic glutathione peroxidase (cGPx) mRNA during mouse embryogenesis. Anat Embryol (Berl) 209, 315–21.CrossRefGoogle ScholarPubMed
Barbonetti, A, Castellini, C, Di Giammarco, N, Santilli, G, Francavilla, S and Francavilla, F (2016). In vitro exposure of human spermatozoa to bisphenol A induces pro-oxidative/apoptotic mitochondrial dysfunction. Reprod Toxicol 66, 61–7.CrossRefGoogle ScholarPubMed
Bazinet, L and Doyen, A (2017). Antioxidants, mechanisms, and recovery by membrane processes. Crit Rev Food Sci Nutr 57, 677–700.CrossRefGoogle ScholarPubMed
Beckman, JS and Koppenol, WH (1996). Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271, C1424–37.CrossRefGoogle ScholarPubMed
Bell, EL and Chandel, NS (2007). Mitochondrial oxygen sensing: regulation of hypoxia-inducible factor by mitochondrial generated reactive oxygen species. Essays Biochem 43, 17–27.Google ScholarPubMed
Bell, EL, Emerling, BM and Chandel, NS (2005). Mitochondrial regulation of oxygen sensing. Mitochondrion 5, 322–32.CrossRefGoogle ScholarPubMed
Benov, L, Sztejnberg, L and Fridovich, I (1998). Critical evaluation of the use of hydroethidine as a measure of superoxide anion radical. Free Radic Biol Med 25, 826–31.CrossRefGoogle ScholarPubMed
Betts, DH and Madan, P (2008). Permanent embryo arrest: molecular and cellular concepts. Mol Hum Reprod 14, 445–53.CrossRefGoogle ScholarPubMed
Biggers, JD, Summers, MC and McGinnis, LK (1997). Polyvinyl alcohol and amino acids as substitutes for bovine serum albumin in culture medium for mouse preimplantation embryos. Hum Reprod Update 3, 125–35.CrossRefGoogle ScholarPubMed
Bing, YZ, Hirao, Y, Takenouchi, N, Che, LM, Nakamura, H, Yodoi, J and Nagai, T (2003). Effects of thioredoxin on the preimplantation development of bovine embryos. Theriogenology 59, 863–73.CrossRefGoogle ScholarPubMed
Boadi, WY, Amartey, PK and Lo, A (2016). Effect of quercetin, genistein and kaempferol on glutathione and glutathione-redox cycle enzymes in 3T3-L1 preadipocytes. Drug Chem Toxicol 39, 239–47.CrossRefGoogle ScholarPubMed
Bontekoe, S, Mantikou, E, van Wely, M, Seshadri, S, Repping, S and Mastenbroek, S (2012). Low oxygen concentrations for embryo culture in assisted reproductive technologies. Cochrane Database Syst Rev CD008950.CrossRefGoogle Scholar
Bungum, M, Humaidan, P and Bungum, L (2002). Recombinant human albumin as protein source in culture medium used for IVF: a prospective randomized study. Reprod Biomed Online 4, 233–6.CrossRefGoogle ScholarPubMed
Burton, GJ, Hempstock, J and Jauniaux, E (2003). Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed Online 6, 84–96.CrossRefGoogle ScholarPubMed
Canella, R, Benedusi, M, Martini, M, Cervellati, F, Cavicchio, C and Valacchi, G (2018). Role of Nrf2 in preventing oxidative stress induced chloride current alteration in human lung cells. J Cell Physiol 233, 6018–27.CrossRefGoogle ScholarPubMed
Chen, B, Lu, Y, Chen, Y and Cheng, J (2015). The role of Nrf2 in oxidative stress-induced endothelial injuries. J Endocrinol 225, R83–99.CrossRefGoogle ScholarPubMed
Chen, HW, Jiang, WS and Tzeng, CR (2001). Nitric oxide as a regulator in preimplantation embryo development and apoptosis. Fertil Steril 75, 1163–71.CrossRefGoogle ScholarPubMed
Chen, R, Lai, UH, Zhu, L, Singh, A, Ahmed, M and Forsyth, NR (2018). Reactive oxygen species formation in the brain at different oxygen levels: the role of hypoxia inducible factors. Front Cell Dev Biol 6, 132.CrossRefGoogle Scholar
Chen, X, Xuan, B, Xu, D, Wang, Q, Cheng, M and Jin, Y (2019). Crocin supplementation during oocyte maturation enhances antioxidant defence and subsequent cleavage rate. Reprod Domest Anim 54, 300–8.Google ScholarPubMed
Chowdhury, MMR, Choi, BH, Khan, I, Lee, KL, Mesalam, A, Song, SH, Xu, L, Joo, MD, Afrin, F and Kong, IK (2017). Supplementation of lycopene in maturation media improves bovine embryo quality in vitro . Theriogenology 103, 173–84.CrossRefGoogle ScholarPubMed
Dannenmann, B, Lehle, S, Hildebrand, DG, Kubler, A, Grondona, P, Schmid, V, Holzer, K, Froschl, M, Essmann, F, Rothfuss, O and Schulze-Osthoff, K (2015). High glutathione and glutathione peroxidase-2 levels mediate cell-type-specific DNA damage protection in human induced pluripotent stem cells. Stem Cell Reports 4, 886–98.CrossRefGoogle ScholarPubMed
De Geyter, C, Calhaz-Jorge, C, Kupka, MS, Wyns, C, Mocanu, E, Motrenko, T, Scaravelli, G, Smeenk, J, Vidakovic, S, Goossens, V, European IVFmCftESoHR and Embryology (2018). ART in Europe, 2014: results generated from European registries by ESHRE: The European IVF-monitoring Consortium (EIM) for the European Society of Human Reproduction and Embryology (ESHRE). Hum Reprod 33, 1586–601.CrossRefGoogle Scholar
De Giusti, VC, Caldiz, CI, Ennis, IL, Perez, NG, Cingolani, HE and Aiello, EA (2013). Mitochondrial reactive oxygen species (ROS) as signaling molecules of intracellular pathways triggered by the cardiac renin-angiotensin II-aldosterone system (RAAS). Front Physiol 4, 126.CrossRefGoogle Scholar
De Iuliis, GN, Wingate, JK, Koppers, AJ, McLaughlin, EA and Aitken, RJ (2006). Definitive evidence for the nonmitochondrial production of superoxide anion by human spermatozoa. J Clin Endocrinol Metab 91, 1968–75.CrossRefGoogle ScholarPubMed
de Waal, E, Mak, W, Calhoun, S, Stein, P, Ord, T, Krapp, C, Coutifaris, C, Schultz, RM and Bartolomei, MS (2014). In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies. Biol Reprod 90, 22.CrossRefGoogle ScholarPubMed
Dickinson, BC and Chang, CJ (2011). Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 7, 504–11.CrossRefGoogle ScholarPubMed
Dos Santos, EC, Varchetta, R, de Lima, CB, Ispada, J, Martinho, HS, Fontes, PK, Nogueira, MFG, Gasparrini, B and Milazzotto, MP (2019). The effects of crocetin supplementation on the blastocyst outcome, transcriptomic and metabolic profile of in vitro produced bovine embryos. Theriogenology 123, 30–6.CrossRefGoogle ScholarPubMed
Dumoulin, JC, Bergers-Janssen, JM, Pieters, MH, Enginsu, ME, Geraedts, JP and Evers, JL (1994). The protective effects of polymers in the cryopreservation of human and mouse zonae pellucidae and embryos. Fertil Steril 62, 793–8.CrossRefGoogle ScholarPubMed
Dumoulin, JC, Vanvuchelen, RC, Land, JA, Pieters, MH, Geraedts, JP and Evers, JL (1995). Effect of oxygen concentration on in vitro fertilization and embryo culture in the human and the mouse. Fertil Steril 63, 115–9.CrossRefGoogle ScholarPubMed
Elomda, AM, Saad, MF, Saeed, AM, Elsayed, A, Abass, AO, Safaa, HM and Mehaisen, GMK (2018). Antioxidant and developmental capacity of retinol on the in vitro culture of rabbit embryos. Zygote 26, 326–32.CrossRefGoogle ScholarPubMed
Eshtiyaghi, M, Deldar, H, Pirsaraei, ZA and Shohreh, B (2016). Royal jelly may improve the metabolism of glucose and redox state of ovine oocytes matured in vitro and embryonic development following in vitro fertilization. Theriogenology 86, 2210–21.CrossRefGoogle Scholar
Espinosa-Diez, C, Miguel, V, Mennerich, D, Kietzmann, T, Sanchez-Perez, P, Cadenas, S and Lamas, S (2015). Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol 6, 183–97.CrossRefGoogle ScholarPubMed
Fan, AQ, Feng, JQ, Liu, W, Zhang, MJ, Liu, T, Zhou, YL and Xu, YJ (2017). [Antagonistic effect of quercetin on PM2.5 toxicity in the rat’s embryonic development in vitro]. Beijing Da Xue Bao Yi Xue Ban 49, 388–93.Google Scholar
Feng, C (2012). Mechanism of Nitric oxide synthase regulation: electron transfer and interdomain interactions. Coord Chem Rev 256, 393–411.CrossRefGoogle ScholarPubMed
Fukai, T and Ushio-Fukai, M (2011). Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 15, 1583–606.CrossRefGoogle Scholar
Gad, A, Hoelker, M, Besenfelder, U, Havlicek, V, Cinar, U, Rings, F, Held, E, Dufort, I, Sirard, MA, Schellander, K and Tesfaye, D (2012). Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol Reprod 87, 100.CrossRefGoogle ScholarPubMed
Gomes, A, Fernandes, E and Lima, JL (2005). Fluorescence probes used for detection of reactive oxygen species. J Biochem Biophys Methods 65, 45–80.CrossRefGoogle ScholarPubMed
Guerin, P, El Mouatassim, S and Menezo, Y (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 7, 175–89.CrossRefGoogle ScholarPubMed
Guo, Q, Xuan, MF, Luo, ZB, Wang, JX, Jin, SS, Yin, XJ and Kang, JD (2019). Baicalin improves IVM of pig oocytes and subsequent preimplantation embryo development by inhibiting apoptosis. Reprod Fertil Dev 31, 983–92.CrossRefGoogle ScholarPubMed
Haida, Z and Hakiman, M (2019). A comprehensive review on the determination of enzymatic assay and nonenzymatic antioxidant activities. Food Sci Nutr 7, 1555–63.CrossRefGoogle ScholarPubMed
Hajian, M, Hosseini, SM, Ostadhosseini, S and Nasr-Esfahani, MH (2017). Comparative stepwise pattern of reactive oxygen species production during in vitro development of fertilized and nuclear transferred goat embryos. Int J Fertil Steril 11, 93–8.Google ScholarPubMed
Halliwell, B (1988). Albumin–an important extracellular antioxidant? Biochem Pharmacol 37, 569–71.CrossRefGoogle ScholarPubMed
Halliwell, B (2012). Free radicals and antioxidants: updating a personal view. Nutr Rev, 70, 257–65.CrossRefGoogle ScholarPubMed
Hamman, R, Thompson, PN, Smuts, MP, Tshuma, T and Holm, DE (2019). Oocyte quality and viability in Nguni and Hereford cows exposed to different levels of dietary protein. Trop Anim Health Prod 51, 1187–94.CrossRefGoogle ScholarPubMed
Handy, DE and Loscalzo, J (2012). Redox regulation of mitochondrial function. Antioxid Redox Signal 16, 1323–67.CrossRefGoogle ScholarPubMed
Hansen, JM (2012). Thioredoxin redox status assessment during embryonic development: the redox western. Methods Mol Biol 889, 305–13.CrossRefGoogle ScholarPubMed
Hara, T, Kin, A, Aoki, S, Nakamura, S, Shirasuna, K, Kuwayama, T and Iwata, H (2018). Resveratrol enhances the clearance of mitochondrial damage by vitrification and improves the development of vitrified-warmed bovine embryos. PLoS One 13, e0204571.CrossRefGoogle ScholarPubMed
Hayashi, T, Ueda, S, Mori, M, Baba, T, Abe, T and Iwata, H (2018). Influence of resveratrol pretreatment on thawed bovine embryo quality and mitochondrial DNA copy number. Theriogenology 106, 271–8.CrossRefGoogle ScholarPubMed
Hughes, PM, Morbeck, DE, Hudson, SB, Fredrickson, JR, Walker, DL and Coddington, CC (2010). Peroxides in mineral oil used for in vitro fertilization: defining limits of standard quality control assays. J Assist Reprod Genet 27, 87–92.CrossRefGoogle ScholarPubMed
Hybertson, BM, Gao, B, Bose, SK and McCord, JM (2011). Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation. Mol Aspects Med 32, 234–46.CrossRefGoogle ScholarPubMed
Iwayama, K, Kusakabe, A, Ohtsu, K, Nawano, T, Tatsunami, R, Ohtaki, KI, Tampo, Y and Hayase, N (2017). Long-Term treatment of clarithromycin at a low concentration improves hydrogen peroxide-induced oxidant/antioxidant imbalance in human small airway epithelial cells by increasing Nrf2 mRNA expression. BMC Pharmacol Toxicol 18, 15.CrossRefGoogle Scholar
Jeeva, JS, Sunitha, J, Ananthalakshmi, R, Rajkumari, S, Ramesh, M and Krishnan, R (2015). Enzymatic antioxidants and its role in oral diseases. J Pharm Bioallied Sci 7, S331–3.Google ScholarPubMed
Jeong, SG, Lee, SE, Park, YG, Son, YJ, Shin, MY, Kim, EY and Park, SP (2017). Treatment of allicin improves maturation of immature oocytes and subsequent developmental ability of preimplantation embryos. Zygote 25, 480–8.CrossRefGoogle ScholarPubMed
Jeong, WJ, Cho, SJ, Lee, HS, Deb, GK, Lee, YS, Kwon, TH and Kong, IK (2009). Effect of cytoplasmic lipid content on in vitro developmental efficiency of bovine IVP embryos. Theriogenology 72, 584–9.CrossRefGoogle ScholarPubMed
Joo, BS, Kim, MK, Na, YJ, Moon, HS, Lee, KS and Kim, HD (2001). The mechanism of action of coculture on embryo development in the mouse model: direct embryo-to-cell contact and the removal of deleterious components. Fertil Steril 75, 193–9.CrossRefGoogle ScholarPubMed
Kannan, K and Jain, SK (2000). Oxidative stress and apoptosis. Pathophysiology 7, 153–63.CrossRefGoogle ScholarPubMed
Karimian, M, Zandi, M, Sanjabi, MR, Masoumian, M and Ofoghi, H (2018). Effects of grape seed extract, quercetin and vitamin C on ovine oocyte maturation and subsequent embryonic development. Cell Mol Biol (Noisy-le-grand) 64, 98–102.CrossRefGoogle ScholarPubMed
Kelm, M (1999). Nitric oxide metabolism and breakdown. Biochim Biophys Acta 1411, 273–89.CrossRefGoogle ScholarPubMed
Kepka, A, Chojnowska, S, Okungbowa, OE and Zwierz, K (2014). The role of carnitine in the perinatal period. Dev Period Med 18, 417–25.Google ScholarPubMed
Khan, I, Chowdhury, MMR, Song, SH, Mesalam, A, Zhang, S, Khan Khalil, AA, Jung, EH, Kim, JB, Jafri, L, Mirza, B and Kong, IK (2018). Lupeol supplementation improves the developmental competence of bovine embryos in vitro . Theriogenology 107, 203–10.CrossRefGoogle ScholarPubMed
Khan, I, Kim, SW, Lee, KL, Song, SH, Mesalam, A, Chowdhury, MMR, Uddin, Z, Park, KH and Kong, IK (2017). Polydatin improves the developmental competence of bovine embryos in vitro via induction of sirtuin 1 (Sirt1). Reprod Fertil Dev 29, 2011–20.CrossRefGoogle Scholar
Khanmohammadi, N, Movahedin, M, Safari, M, Sameni, HR, Yousefi, B, Jafari, B and Zarbakhsh, S (2016). Effect of l-carnitine on in vitro developmental rate, the zona pellucida and hatching of blastocysts and their cell numbers in mouse embryos. Int J Reprod Biomed (Yazd) 14, 649–56.Google ScholarPubMed
Khatun, H, Egashira, J, Sakatani, M, Takenouchi, N, Tatemoto, H, Wada, Y and Yamanaka, KI (2018). Sericin enhances the developmental competence of heat-stressed bovine embryos. Mol Reprod Dev 85, 696–708.CrossRefGoogle ScholarPubMed
Khera, A, Vanderlelie, JJ, Holland, O and Perkins, AV (2017). Overexpression of endogenous anti-oxidants with selenium supplementation protects trophoblast cells from reactive oxygen species-induced apoptosis in a Bcl-2-dependent manner. Biol Trace Elem Res 177, 394–403.CrossRefGoogle Scholar
Khera, A, Vanderlelie, JJ and Perkins, AV (2013). Selenium supplementation protects trophoblast cells from mitochondrial oxidative stress. Placenta 34, 59498.CrossRefGoogle ScholarPubMed
Kim, EH, Kim, GA, Taweechaipaisankul, A, Lee, SH, Qasim, M, Ahn, C and Lee, BC (2019). Melatonin enhances porcine embryo development via the Nrf2/ARE signaling pathway. J Mol Endocrinol 63, 175–85.CrossRefGoogle ScholarPubMed
Kim, MK, Park, JK, Paek, SK, Kim, JW, Kwak, IP, Lee, HJ, Lyu, SW and Lee, WS (2018). Effects and pregnancy outcomes of l-carnitine supplementation in culture media for human embryo development from in vitro fertilization. J Obstet Gynaecol Res 44, 2059–66.CrossRefGoogle ScholarPubMed
Kirby, RS (2018). Assisted reproductive technology and developmental outcomes. Pediatrics 142, e20183072.CrossRefGoogle ScholarPubMed
Kohler, M, Kundig, A, Reist, HW and Michel, C (1994). Modification of in vitro mouse embryogenesis by X-rays and fluorochromes. Radiat Environ Biophys 33, 341–51.CrossRefGoogle ScholarPubMed
Kotwicka, M, Skibinska, I, Jendraszak, M and Jedrzejczak, P (2016). 17beta-estradiol modifies human spermatozoa mitochondrial function in vitro . Reprod Biol Endocrinol 14, 50.CrossRefGoogle ScholarPubMed
Krisher, RL and Prather, RS (2012). A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation. Mol Reprod Dev 79, 311–20.CrossRefGoogle ScholarPubMed
Kumar, S, Sharma, S and Vasudeva, N (2017). Review on antioxidants and evaluation procedures. Chin J Integr Med 2017, doi: 10.1007/s11655-017-2414-z.CrossRefGoogle Scholar
Kundu, JK and Surh, YJ (2010). Nrf2-Keap1 signaling as a potential target for chemoprevention of inflammation-associated carcinogenesis. Pharm Res 27, 999–1013.CrossRefGoogle ScholarPubMed
Kwon, DH, Cha, HJ, Lee, H, Hong, SH, Park, C, Park, SH, Kim, GY, Kim, S, Kim, HS, Hwang, HJ and Choi, YH (2019). Protective effect of glutathione against oxidative stress-induced cytotoxicity in RAW 264.7 macrophages through activating the nuclear factor erythroid 2-related factor-2/heme oxygenase-1 pathway. Antioxidants (Basel) 8, 82.CrossRefGoogle ScholarPubMed
Labied, S, Jouan, C, Wenders, F, Ravet, S, Gaspard, O, Thonon, F, Gridelet, V, Henry, L, Perrier d’Hauterive, S and Nisolle, M (2019). Comparison between paraffin and mineral oil covering on early human embryo culture: a prospective randomized study. Syst Biol Reprod Med 65, 81–6.CrossRefGoogle ScholarPubMed
Lagoa, R, Graziani, I, Lopez-Sanchez, C, Garcia-Martinez, V and Gutierrez-Merino, C (2011). Complex I and cytochrome c are molecular targets of flavonoids that inhibit hydrogen peroxide production by mitochondria. Biochim Biophys Acta 1807, 1562–72.CrossRefGoogle ScholarPubMed
Lan, KC, Lin, YC, Chang, YC, Lin, HJ, Tsai, YR and Kang, HY (2019). Limited relationships between reactive oxygen species levels in culture media and zygote and embryo development. J Assist Reprod Genet 36, 325–34.CrossRefGoogle ScholarPubMed
Ledesma-Osuna, AI, Ramos-Clamont, G and Vazquez-Moreno, L (2008). Characterization of bovine serum albumin glycated with glucose, galactose and lactose. Acta Biochim Pol 55, 491–7.CrossRefGoogle ScholarPubMed
Lee, S, Jin, JX, Taweechaipaisankul, A, Kim, GA and Lee, BC (2018). Synergistic effects of resveratrol and melatonin on in vitro maturation of porcine oocytes and subsequent embryo development. Theriogenology 114, 191–8.CrossRefGoogle ScholarPubMed
Lee, SK, Oh, KH, Chung, AY, Park, HC, Lee, SH, Kwon, SY and Choi, J (2015). Protective role of quercetin against cisplatin-induced hair cell damage in zebrafish embryos. Hum Exp Toxicol 34, 1043–52.CrossRefGoogle ScholarPubMed
Lee, TH, Lee, MS, Liu, CH, Tsao, HM, Huang, CC and Yang, YS (2012). The association between microenvironmental reactive oxygen species and embryo development in assisted reproduction technology cycles. Reprod Sci 19, 725–32.CrossRefGoogle ScholarPubMed
Li, F, Cui, L, Yu, D, Hao, H, Liu, Y, Zhao, X, Pang, Y, Zhu, H and Du, W (2019). Exogenous glutathione improves intracellular glutathione synthesis via the γ-glutamyl cycle in bovine zygotes and cleavage embryos. J Cell Physiol 234, 7384–94.CrossRefGoogle ScholarPubMed
Li, R Wu, H Zhuo, WW Mao, QF Lan, H Zhang, Y and Hua, S (2015). Astaxanthin normalizes epigenetic modifications of bovine somatic cell cloned embryos and decreases the generation of lipid peroxidation. Reprod Domest Anim 50, 793–9.CrossRefGoogle ScholarPubMed
Li, XX, Lee, KB, Lee, JH, Kim, KJ, Kim, EY, Han, KW, Park, KS, Yu, J and Kim, MK (2014). Glutathione and cysteine enhance porcine preimplantation embryo development in vitro after intracytoplasmic sperm injection. Theriogenology 81, 309–14.CrossRefGoogle ScholarPubMed
Liu, Z, Ren, Z, Zhang, J, Chuang, CC, Kandaswamy, E, Zhou, T and Zuo, L (2018). Role of ROS and nutritional antioxidants in human diseases. Front Physiol 9, 477.CrossRefGoogle ScholarPubMed
Ma, YY, Chen, HW and Tzeng, CR (2017). Low oxygen tension increases mitochondrial membrane potential and enhances expression of antioxidant genes and implantation protein of mouse blastocyst cultured in vitro . J Ovarian Res 10, 47.CrossRefGoogle ScholarPubMed
Maarman, GJ (2017). Natural antioxidants as potential therapy, and a promising role for melatonin against pulmonary hypertension. Adv Exp Med Biol 967, 161–78.CrossRefGoogle Scholar
Maciazek-Jurczyk, M, Szkudlarek, A, Chudzik, M, Pozycka, J and Sulkowska, A (2018). Alteration of human serum albumin binding properties induced by modifications: a review. Spectrochim Acta A Mol Biomol Spectrosc 188, 675–83.CrossRefGoogle ScholarPubMed
Madrid Gaviria, S, Lopez-Herrera, A, Urrego, R, Restrepo Betancur, G and Echeverri Zuluaga, JJ (2019). Effect of resveratrol on vitrified in vitro produced bovine embryos: recovering the initial quality. Cryobiology 89, 42–50.CrossRefGoogle ScholarPubMed
Mari, M, Morales, A, Colell, A, Garcia-Ruiz, C and Fernandez-Checa, JC (2009). Mitochondrial glutathione, a key survival antioxidant. Antioxid Redox Signal 11, 2685–700.CrossRefGoogle ScholarPubMed
Marques, TC, da Silva Santos, EC, Diesel, TO, Leme, LO, Martins, CF, Dode, M, Alves, BG, Costa, F, de Oliveira, EB and Gambarini, ML (2018). Melatonin reduces apoptotic cells, SOD2 and HSPB1 and improves the in vitro production and quality of bovine blastocysts. Reprod Domest Anim 53, 226–36.CrossRefGoogle ScholarPubMed
Martin-Romero, FJ, Miguel-Lasobras, EM, Dominguez-Arroyo, JA, Gonzalez-Carrera, E and Alvarez, IS (2008). Contribution of culture media to oxidative stress and its effect on human oocytes. Reprod Biomed Online 17, 652–61.CrossRefGoogle ScholarPubMed
Martinez, CA, Nohalez, A, Ceron, JJ, Rubio, CP, Roca, J, Cuello, C, Rodriguez-Martinez, H, Martinez, EA and Gil, MA (2017). Peroxidized mineral oil increases the oxidant status of culture media and inhibits in vitro porcine embryo development. Theriogenology 103, 17–23.CrossRefGoogle ScholarPubMed
Marzo, I, Susin, SA, Petit, PX, Ravagnan, L, Brenner, C, Larochette, N, Zamzami, N and Kroemer, G (1998). Caspases disrupt mitochondrial membrane barrier function. FEBS Lett 427, 198–202.CrossRefGoogle ScholarPubMed
Maside, C, Martinez, CA, Cambra, JM, Lucas, X, Martinez, EA, Gil, MA, Rodriguez-Martinez, H, Parrilla, I and Cuello, C (2019). Supplementation with exogenous coenzyme Q10 to media for in vitro maturation and embryo culture fails to promote the developmental competence of porcine embryos. Reprod Domest Anim 54 Suppl 4, 72–7.CrossRefGoogle ScholarPubMed
Mehaisen, GM, Saeed, AM, Gad, A, Abass, AO, Arafa, M and El-Sayed, A (2015). Antioxidant capacity of melatonin on preimplantation development of fresh and vitrified rabbit embryos: morphological and molecular aspects. PLoS One 10, e0139814.CrossRefGoogle ScholarPubMed
Menezo, Y, Dale, B and Cohen, M (2010). DNA damage and repair in human oocytes and embryos: a review. Zygote 18, 357–65.CrossRefGoogle ScholarPubMed
Miller-Pinsler, L and Wells, PG (2015). Embryonic catalase protects against ethanol embryopathies in acatalasemic mice and transgenic human catalase-expressing mice in embryo culture. Toxicol Appl Pharmacol 287, 232–9.CrossRefGoogle ScholarPubMed
Miranda-Vizuete, A, Damdimopoulos, AE and Spyrou, G (2000). The mitochondrial thioredoxin system. Antioxid Redox Signal 2, 801–10.CrossRefGoogle ScholarPubMed
Mishra, A, Reddy, IJ, Dhali, A and Javvaji, PK (2018). l-Ergothioneine improves the developmental potential of in vitro sheep embryos without influencing OCTN1-mediated cross-membrane transcript expression. Zygote 26, 149–61.CrossRefGoogle ScholarPubMed
Mishra, A, Reddy, IJ, Gupta, PS and Mondal, S (2017). Expression of apoptotic and antioxidant enzyme genes in sheep oocytes and in vitro produced embryos. Anim Biotechnol 28, 18–25.CrossRefGoogle ScholarPubMed
Morel, Y and Barouki, R (1999). Repression of gene expression by oxidative stress. Biochem J 342(Pt 3), 481–96.CrossRefGoogle ScholarPubMed
Movafagh, S, Crook, S and Vo, K (2015). Regulation of hypoxia-inducible factor-1a by reactive oxygen species: new developments in an old debate. J Cell Biochem 116, 696–703.CrossRefGoogle Scholar
Muratori, M, Tarozzi, N, Carpentiero, F, Danti, S, Perrone, FM, Cambi, M, Casini, A, Azzari, C, Boni, L, Maggi, M, Borini, A and Baldi, E (2019). Sperm selection with density gradient centrifugation and swim up: effect on DNA fragmentation in viable spermatozoa. Sci Rep 9, 7492.CrossRefGoogle ScholarPubMed
Nasrollahzadeh, F, Varidi, M, Koocheki, A and Hadizadeh, F (2017). Effect of microwave and conventional heating on structural, functional and antioxidant properties of bovine serum albumin-maltodextrin conjugates through Maillard reaction. Food Res Int 100, 289–97.CrossRefGoogle ScholarPubMed
Nguyen, TV, Tanihara, F, Do, L, Sato, Y, Taniguchi, M, Takagi, M, Van Nguyen, T and Otoi, T (2017). Chlorogenic acid supplementation during in vitro maturation improves maturation, fertilization and developmental competence of porcine oocytes. Reprod Domest Anim 52, 969–75.CrossRefGoogle ScholarPubMed
Niu, YJ, Zhou, W, Guo, J, Nie, ZW, Shin, KT, Kim, NH, Lv, WF and Cui, XS (2017). C-Phycocyanin protects against mitochondrial dysfunction and oxidative stress in parthenogenetic porcine embryos. Sci Rep 7, 16992.CrossRefGoogle ScholarPubMed
Nohalez, A, Martinez, CA, Parrilla, I, Roca, J, Gil, MA, Rodriguez-Martinez, H, Martinez, EA and Cuello, C (2018). Exogenous ascorbic acid enhances vitrification survival of porcine in vitro-developed blastocysts but fails to improve the in vitro embryo production outcomes. Theriogenology 113, 113–9.CrossRefGoogle ScholarPubMed
Nonogaki, T, Noda, Y, Narimoto, K, Umaoka, Y and Mori, T (1992). Effects of superoxide dismutase on mouse in vitro fertilization and embryo culture system. J Assist Reprod Genet 9, 274–80.CrossRefGoogle ScholarPubMed
Orsi, NM and Leese, HJ (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, 44–53.CrossRefGoogle ScholarPubMed
Osman, N, Abd El-Maqsoud, NMR and El Gelany, SAA (2015). Correlation of NQO1 and Nrf2 in female genital tract cancer and their precancerous lesions (cervix, endometrium and ovary). World J Oncol 6, 364–74.CrossRefGoogle Scholar
Otsuki, J, Nagai, Y and Chiba, K (2007). Peroxidation of mineral oil used in droplet culture is detrimental to fertilization and embryo development. Fertil Steril 88, 741–3.CrossRefGoogle ScholarPubMed
Otsuki, J, Nagai, Y and Chiba, K (2009). Damage of embryo development caused by peroxidized mineral oil and its association with albumin in culture. Fertil Steril 91, 1745–9.CrossRefGoogle ScholarPubMed
Otsuki, J, Nagai, Y, Matsuyama, Y, Terada, T and Era, S (2013). The redox state of recombinant human serum albumin and its optimal concentration for mouse embryo culture. Syst Biol Reprod Med 59, 48–52.CrossRefGoogle ScholarPubMed
Ou, B, Hampsch-Woodill, M, Flanagan, J, Deemer, EK, Prior, RL and Huang, D (2002). Novel fluorometric assay for hydroxyl radical prevention capacity using fluorescein as the probe. J Agric Food Chem 50, 2772–7.CrossRefGoogle ScholarPubMed
Pang, YW, Sun, YQ, Jiang, XL, Huang, ZQ, Zhao, SJ, Du, WH, Hao, HS, Zhao, XM and Zhu, HB (2016). Protective effects of melatonin on bovine sperm characteristics and subsequent in vitro embryo development. Mol Reprod Dev 83, 993–1002.CrossRefGoogle ScholarPubMed
Park, DJ, Kang, JB, Shah, FA, Jin, YB and Koh, PO (2020). Quercetin attenuates decrease of thioredoxin expression following focal cerebral ischemia and glutamate-induced neuronal cell damage. Neuroscience 428, 38–49.CrossRefGoogle ScholarPubMed
Park, YG, Lee, SE, Son, YJ, Jeong, SG, Shin, MY, Kim, WJ, Kim, EY and Park, SP (2018). Antioxidant (-cryptoxanthin enhances porcine oocyte maturation and subsequent embryo development in vitro . Reprod Fertil Dev 30, 1204–13.CrossRefGoogle ScholarPubMed
Parveen, A, Akash, MS, Rehman, K and Kyunn, WW (2016). Recent investigations for discovery of natural antioxidants: a comprehensive review. Crit Rev Eukaryot Gene Expr 26, 143–60.CrossRefGoogle ScholarPubMed
Paszkowski, T and Clarke, RN (1996). Antioxidative capacity of preimplantation embryo culture medium declines following the incubation of poor quality embryos. Hum Reprod 11, 2493–5.CrossRefGoogle ScholarPubMed
Patenaude, A, Ven Murthy, MR and Mirault, ME (2004). Mitochondrial thioredoxin system: effects of TrxR2 overexpression on redox balance, cell growth, and apoptosis. J Biol Chem 279, 27302–14.CrossRefGoogle Scholar
Perez-Pasten, R, Martinez-Galero, E and Chamorro-Cevallos, G (2010). Quercetin and naringenin reduce abnormal development of mouse embryos produced by hydroxyurea. J Pharm Pharmacol 62, 1003–9.CrossRefGoogle ScholarPubMed
Pey, AL, Megarity, CF, Medina-Carmona, E and Timson, DJ (2016). Natural small molecules as stabilizers and activators of cancer-associated NQO1 polymorphisms. Curr Drug Targets 17, 1506–14.CrossRefGoogle ScholarPubMed
Pirson, M, Debrulle, S, Clippe, A, Clotman, F and Knoops, B (2015). Thioredoxin-2 modulates neuronal programmed cell death in the embryonic chick spinal cord in basal and target-deprived conditions. PLoS One 10, e0142280.CrossRefGoogle ScholarPubMed
Pool, TB and Martin, JE (1994). High continuing pregnancy rates after in vitro fertilization-embryo transfer using medium supplemented with a plasma protein fraction containing alpha- and beta-globulins. Fertil Steril 61, 714–9.CrossRefGoogle ScholarPubMed
Rincon, JAA, Pradiee, J, Remiao, MH, Collares, TV, Mion, B, Gasperin, BG, Tomazele Rovani, M, Correa, MN, Pegoraro, LMC and Schneider, A (2019). Effect of high-density lipoprotein on oocyte maturation and bovine embryo development in vitro . Reprod Domest Anim 54, 445–55.CrossRefGoogle ScholarPubMed
Rozoy, E, Simard, S, Liu, Y, Kitts, D, Lessard, J and Bazinet, L (2012). The use of cyclic voltammetry to study the oxidation of l-5-methyltetrahydrofolate and its preservation by ascorbic acid. Food Chem 132, 1429–35.CrossRefGoogle Scholar
Safari, M, Parsaie, H, Sameni, HR, Aldaghi, MR and Zarbakhsh, S (2018). Anti-Oxidative and anti-apoptotic effects of apigenin on number of viable and apoptotic blastomeres, zona pellucida thickness and hatching rate of mouse embryos. Int J Fertil Steril 12, 257–62.Google ScholarPubMed
Sameni, HR, Javadinia, SS, Safari, M, Tabrizi Amjad, MH, Khanmohammadi, N, Parsaie, H and Zarbakhsh, S (2018). Effect of quercetin on the number of blastomeres, zona pellucida thickness, and hatching rate of mouse embryos exposed to actinomycin D: an experimental study. Int J Reprod Biomed (Yazd) 16, 101–8.Google ScholarPubMed
Santos, MVO, Nascimento, LE, Praxedes, EA, Borges, AA, Silva, AR, Bertini, LM and Pereira, AF (2019). Syzygium aromaticum essential oil supplementation during in vitro bovine oocyte maturation improves parthenogenetic embryonic development. Theriogenology 128, 74–80.CrossRefGoogle ScholarPubMed
Sariozkan, S, Turk, G, Canturk, F, Yay, A, Eken, A and Akcay, A (2013). The effect of bovine serum albumin and fetal calf serum on sperm quality, DNA fragmentation and lipid peroxidation of the liquid stored rabbit semen. Cryobiology 67, 1–6.CrossRefGoogle ScholarPubMed
Schwarzer, C, Esteves, TC, Araúzo-Bravo, MJ, Le Gac, S, Nordhoff, V, Schlatt, S and Boiani, M (2012). ART culture conditions change the probability of mouse embryo gestation through defined cellular and molecular responses. Hum Reprod 27, 2627–40.CrossRefGoogle ScholarPubMed
Scialo, F, Fernandez-Ayala, DJ and Sanz, A (2017). Role of mitochondrial reverse electron transport in ROS signaling: potential roles in health and disease. Front Physiol 8, 428.CrossRefGoogle ScholarPubMed
Shafiei, G, Almasi, M, Nikzad, H, Miyan, J, Mahabadi, JA and Moshkdanian, G (2020). l-Carnitine reduces the adverse effects of ROS and up-regulates the expression of implantation related genes in in vitro developed mouse embryos. Theriogenology 145, 59–66.CrossRefGoogle ScholarPubMed
Sharma, V, Mishra, M, Ghosh, S, Tewari, R, Basu, A, Seth, P and Sen, E (2007). Modulation of interleukin-1beta mediated inflammatory response in human astrocytes by flavonoids: implications in neuroprotection. Brain Res Bull 73, 55–63.CrossRefGoogle ScholarPubMed
Shih, YF, Lee, TH, Liu, CH, Tsao, HM, Huang, CC and Lee, MS (2014). Effects of reactive oxygen species levels in prepared culture media on embryo development: a comparison of two media. Taiwan J Obstet Gynecol 53, 504–8.CrossRefGoogle ScholarPubMed
Sireesh, D, Ganesh, MR, Dhamodharan, U, Sakthivadivel, M, Sivasubramanian, S, Gunasekaran, P and Ramkumar, KM (2017). Role of pterostilbene in attenuating immune mediated devastation of pancreatic beta cells via Nrf2 signaling cascade. J Nutr Biochem 44, 11–21.CrossRefGoogle ScholarPubMed
Somfai, T, Kaneda, M, Akagi, S, Watanabe, S, Haraguchi, S, Mizutani, E, Dang-Nguyen, TQ, Geshi, M, Kikuchi, K and Nagai, T (2011). Enhancement of lipid metabolism with l-carnitine during in vitro maturation improves nuclear maturation and cleavage ability of follicular porcine oocytes. Reprod Fertil Dev 23, 912–20.CrossRefGoogle ScholarPubMed
Soto-Heras, S, Catala, MG, Roura, M, Menendez-Blanco, I, Piras, AR, Izquierdo, D and Paramio, MT (2019). Effects of melatonin on oocyte developmental competence and the role of melatonin receptor 1 in juvenile goats. Reprod Domest Anim 54, 381–90.CrossRefGoogle ScholarPubMed
Sovernigo, TC, Adona, PR, Monzani, PS, Guemra, S, Barros, F, Lopes, FG and Leal, C (2017). Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reprod Domest Anim 52, 561–9.CrossRefGoogle ScholarPubMed
Sun, WJ, Pang, YW, Liu, Y, Hao, HS, Zhao, XM, Qin, T, Zhu, HB and Du, WH (2015). Exogenous glutathione supplementation in culture medium improves the bovine embryo development after in vitro fertilization. Theriogenology 84, 716–23.CrossRefGoogle ScholarPubMed
Sunderam, S, Kissin, DM, Crawford, SB, Folger, SG, Jamieson, DJ, Barfield, WD, Centers for Disease C and Prevention (2014). Assisted reproductive technology surveillance--United States, 2011. MMWR Surveill Summ, 63, 1–28.Google ScholarPubMed
Sunderam, S, Kissin, DM, Zhang, Y, Folger, SG, Boulet, SL, Warner, L, Callaghan, WM and Barfield, WD (2019). Assisted Reproductive Technology Surveillance – United States, 2016. MMWR Surveill Summ 68, 1–24.CrossRefGoogle ScholarPubMed
Susin, SA, Zamzami, N and Kroemer, G (1998). Mitochondria as regulators of apoptosis: doubt no more. Biochim Biophys Acta 1366, 151–65.CrossRefGoogle ScholarPubMed
Swain, JE, Carrell, D, Cobo, A, Meseguer, M, Rubio, C and Smith, GD (2016). Optimizing the culture environment and embryo manipulation to help maintain embryo developmental potential. Fertil Steril 105, 571–87.CrossRefGoogle ScholarPubMed
Talebi, A, Hayati Roodbari, N, Reza Sameni, H and Zarbakhsh, S (2020). Impact of coadministration of apigenin and bone marrow stromal cells on damaged ovaries due to chemotherapy in rat: an experimental study. Int J Reprod Biomed (Yazd) 18, 551–60.Google ScholarPubMed
Tanihara, F, Hirata, M, Nhien, NT, Hirano, T, Kunihara, T and Otoi, T (2018). Effect of ferulic acid supplementation on the developmental competence of porcine embryos during in vitro maturation. J Vet Med Sci 80, 1007–11.CrossRefGoogle ScholarPubMed
Tarazona, AM, Rodriguez, JI, Restrepo, LF and Olivera-Angel, M (2006). Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro . Reprod Domest Anim 41, 5–11.CrossRefGoogle ScholarPubMed
Taverne, YJ, Bogers, AJ, Duncker, DJ and Merkus, D (2013). Reactive oxygen species and the cardiovascular system. Oxid Med Cell Longev 2013, 862423.CrossRefGoogle ScholarPubMed
Taweechaipaisankul, A, Jin, JX, Lee, S, Kim, GA and Lee, BC (2016). The effects of canthaxanthin on porcine oocyte maturation and embryo development in vitro after parthenogenetic activation and somatic cell nuclear transfer. Reprod Domest Anim 51, 870–6.CrossRefGoogle ScholarPubMed
Tebboub, I and Kechrid, Z (2019). Effect of curcuma on zinc, lipid profile and antioxidants levels in blood and tissue of streptozotocin-induced diabetic rats fed zinc deficiency diet. Arch Physiol Biochem 19, 1–8.Google Scholar
Tengan, CH and Moraes, CT (2017). NO control of mitochondrial function in normal and transformed cells. Biochim Biophys Acta Bioenerg 1858, 573–81.CrossRefGoogle ScholarPubMed
Tian, X, Wang, F, Zhang, L, Ji, P, Wang, J, Lv, D, Li, G, Chai, M, Lian, Z and 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, 988.CrossRefGoogle ScholarPubMed
Tonissen, KF and Di Trapani, G (2009). Thioredoxin system inhibitors as mediators of apoptosis for cancer therapy. Mol Nutr Food Res 53, 87–103.CrossRefGoogle ScholarPubMed
Torres, V, Hamdi, M, Maillo, V, Urrego, R, Echeverri, JJ, Lopez-Herrera, A, Gutierrez-Adan, A, Rizos, D and Sanchez-Calabuig, MJ (2019). Ascorbic acid-cyclodextrin complex alters the expression of genes associated with lipid metabolism in bovine in vitro produced embryos. Reprod Domest Anim 54, 55–62.CrossRefGoogle ScholarPubMed
Tranguch, S, Steuerwald, N and Huet-Hudson, YM (2003). Nitric oxide synthase production and nitric oxide regulation of preimplantation embryo development. Biol Reprod 68, 1538–44.CrossRefGoogle ScholarPubMed
Truong, T and Gardner, DK (2017). Antioxidants improve IVF outcome and subsequent embryo development in the mouse. Hum Reprod 32, 2404–13.CrossRefGoogle ScholarPubMed
Truong, TT and Gardner, DK (2020). Antioxidants increase blastocyst cryosurvival and viability post-vitrification. Hum Reprod 35, 12–23.CrossRefGoogle ScholarPubMed
Truong, TT, Soh, YM and Gardner, DK (2016). Antioxidants improve mouse preimplantation embryo development and viability. Hum Reprod 31, 1445–54.CrossRefGoogle ScholarPubMed
Twigg, J, Irvine, DS, Houston, P, Fulton, N, Michael, L and Aitken, RJ (1998). Iatrogenic DNA damage induced in human spermatozoa during sperm preparation: protective significance of seminal plasma. Mol Hum Reprod 4, 439–45.CrossRefGoogle ScholarPubMed
Ullah, O, Li, Z, Ali, I, Xu, L, Liu, H, Shah, SZA and Fang, N (2019). Pterostilbene alleviates hydrogen peroxide-induced oxidative stress via nuclear factor erythroid 2 like 2 pathway in mouse preimplantation embryos. J Reprod Dev 65, 73–81.CrossRefGoogle ScholarPubMed
Uribe, P, Boguen, R, Treulen, F, Sanchez, R and Villegas, JV (2015). Peroxynitrite-Mediated nitrosative stress decreases motility and mitochondrial membrane potential in human spermatozoa. Mol Hum Reprod 21, 237–43.CrossRefGoogle ScholarPubMed
Valko, M, Leibfritz, D, Moncol, J, Cronin, MT, Mazur, M and Telser, J (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39, 44–84.CrossRefGoogle ScholarPubMed
Van Blerkom, J (2008). Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod Biomed Online 16, 553–69.CrossRefGoogle ScholarPubMed
Van Blerkom, J (2009). Mitochondria in early mammalian development. Semin Cell Dev Biol 20, 354–64.CrossRefGoogle ScholarPubMed
Van Blerkom, J (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.CrossRefGoogle ScholarPubMed
Van Blerkom, J, Davis, PW and Lee, J (1995). ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum Reprod 10, 415–24.CrossRefGoogle ScholarPubMed
Wale, PL and Gardner, DK (2010). Time-Lapse analysis of mouse embryo development in oxygen gradients. Reprod Biomed Online 21, 402–10.CrossRefGoogle ScholarPubMed
Wale, PL and Gardner, DK (2016). The effects of chemical and physical factors on mammalian embryo culture and their importance for the practice of assisted human reproduction. Hum Reprod Update 22, 2–22.CrossRefGoogle ScholarPubMed
Walther, TC and Farese, RV, Jr (2012). Lipid droplets and cellular lipid metabolism. Annu Rev Biochem 81, 687–714.CrossRefGoogle ScholarPubMed
Wang, H and Joseph, JA (1999). Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 27, 612–6.CrossRefGoogle ScholarPubMed
Wang, HL, Liu, FT, Ding, AX, Ma, SF, He, L, Lin, L and Lu, ZL (2016). Water-Soluble Hantzsch ester as switch-on fluorescent probe for efficiently detecting nitric oxide. Spectrochim Acta A Mol Biomol Spectrosc 169, 1–6.CrossRefGoogle ScholarPubMed
Wang, Y, Zhang, M, Chen, ZJ and Du, Y (2018). Resveratrol promotes the embryonic development of vitrified mouse oocytes after in vitro fertilization. In Vitro Cell Dev Biol Anim 54, 430–8.CrossRefGoogle ScholarPubMed
Weathersbee, PS, Pool, TB and Ord, T (1995). Synthetic serum substitute (SSS): a globulin-enriched protein supplement for human embryo culture. J Assist Reprod Genet 12, 354–60.CrossRefGoogle ScholarPubMed
Weng, XG, Cai, MM, Zhang, YT, Liu, Y, Gao, ZL, Song, J and Liu, ZH (2018). Effect of Astragalus polysaccharide addition to thawed boar sperm on in vitro fertilization and embryo development. Theriogenology 121, 21–6.CrossRefGoogle ScholarPubMed
Xu, DP, Li, Y, Meng, X, Zhou, T, Zhou, Y, Zheng, J, Zhang, JJ and Li, HB (2017). Natural antioxidants in foods and medicinal plants: extraction, assessment and resources. Int J Mol Sci 18, 96.CrossRefGoogle ScholarPubMed
Yan, X, Fu, X, Jia, Y, Ma, X, Tao, J, Yang, T, Ma, H, Liang, X, Liu, X, Yang, J and Wei, J (2019). Nrf2/Keap1/ARE signaling mediated an antioxidative protection of human placental mesenchymal stem cells of fetal origin in alveolar epithelial cells. Oxid Med Cell Longev, 2019, 2654910.CrossRefGoogle ScholarPubMed
Yang, HW, Hwang, KJ, Kwon, HC, Kim, HS, Choi, KW and Oh, KS (1998). Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum Reprod 13, 998–1002.CrossRefGoogle ScholarPubMed
Yang, JC and Cortopassi, GA (1998). Induction of the mitochondrial permeability transition causes release of the apoptogenic factor cytochrome c . Free Radic Biol Med 24, 624–31.CrossRefGoogle ScholarPubMed
Yang, L, Gao, Z, Lei, L, Lv, Q, Zhao, Q, Li, L, Cao, X and Fu, W (2019). Lycium barbarum polysaccharide enhances development of previously-cryopreserved murine two-cell embryos via restoration of mitochondrial function and down-regulated generation of reactive oxygen species. J Reprod Dev 65, 163–70.CrossRefGoogle ScholarPubMed
Yang, SG, Park, HJ, Kim, JW, Jung, JM, Kim, MJ, Jegal, HG, Kim, IS, Kang, MJ, Wee, G, Yang, HY, Lee, YH, Seo, JH, Kim, SU and Koo, DB (2018). Mito-TEMPO improves development competence by reducing superoxide in preimplantation porcine embryos. Sci Rep 8, 10130.CrossRefGoogle ScholarPubMed
Yao, X, Jiang, H, NanXu, Y, Piao, X, Gao, Q and Kim, NH (2019). Kaempferol attenuates mitochondrial dysfunction and oxidative stress induced by H2O2 during porcine embryonic development. Theriogenology 135, 174–80.CrossRefGoogle ScholarPubMed
Yu, S, Long, H, Lyu, QF, Zhang, QH, Yan, ZG, Liang, HX, Chai, WR, Yan, Z, Kuang, YP and Qi, C (2014). Protective effect of quercetin on the development of preimplantation mouse embryos against hydrogen peroxide-induced oxidative injury. PLoS One 9, e89520.CrossRefGoogle ScholarPubMed
Zabihi, A, Shabankareh, HK, Hajarian, H and Foroutanifar, S (2019). Resveratrol addition to in vitro maturation and in vitro culture media enhances developmental competence of sheep embryos. Domest Anim Endocrinol 68, 25–31.CrossRefGoogle ScholarPubMed
Zarbakhsh, S, Safari, R, Sameni, HR, Yousefi, B, Safari, M, Khanmohammadi, N and Hayat, P (2019). Effects of co-administration of bone marrow stromal cells and l-carnitine on the recovery of damaged ovaries by performing chemotherapy model in rat. Int J Fertil Steril 13, 196–202.Google ScholarPubMed
Zare, Z, Abouhamzeh, B, Masteri Farahani, R, Salehi, M and Mohammadi, M (2017). Supplementation of l-carnitine during in vitro maturation of mouse oocytes affects expression of genes involved in oocyte and embryo competence: an experimental study. Int J Reprod Biomed (Yazd) 15, 779–86.Google ScholarPubMed
Zare, Z, Masteri Farahani, R, Salehi, M, Piryaei, A, Ghaffari Novin, M, Fadaei Fathabadi, F, Mohammadi, M and Dehghani-Mohammadabadi, M (2015). Effect of l-carnitine supplementation on maturation and early embryo development of immature mouse oocytes selected by brilliant cresyl blue staining. J Assist Reprod Genet 32, 635–43.CrossRefGoogle Scholar
Zhao, RZ, Jiang, S, Zhang, L and Yu, ZB (2019). Mitochondrial electron transport chain, ROS generation and uncoupling. Int J Mol Med 44, 3–15.Google ScholarPubMed
Zhao, Y, Xu, Y, Li, Y, Jin, Q, Sun, J, E Z and Gao, Q (2020). Supplementation of kaempferol to in vitro maturation medium regulates oxidative stress and enhances subsequent embryonic development in vitro . Zygote 28, 59–64.CrossRefGoogle ScholarPubMed
Zou, H, Chen, B, Ding, D, Gao, M, Chen, D, Liu, Y, Hao, Y, Zou, W, Ji, D, Zhou, P, Wei, Z, Cao, Y and Zhang, Z (2020). Melatonin promotes the development of immature oocytes from the COH cycle into healthy offspring by protecting mitochondrial function. J Pineal Res 68, e12621.CrossRefGoogle ScholarPubMed