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Comparison of three antioxidants in chemical and biological assays on porcine oocytes during ageing in vitro

Published online by Cambridge University Press:  21 April 2022

Chan-Oh Park ,
Seung-Eun Lee ,
Jae-Wook Yoon ,
Hyo-Jin Park ,
So-Hee Kim ,
Seung-Hwan Oh ,
Do-Geon Lee ,
Da-Bin Pyeon ,
Eun-Young Kim  and
Se-Pill Park Open the ORCID record for Se-Pill Park [Opens in a new window]
Chan-Oh Park
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea
Seung-Eun Lee
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea
Jae-Wook Yoon
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea
Hyo-Jin Park
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea
So-Hee Kim
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea
Seung-Hwan Oh
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea
Do-Geon Lee
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea
Da-Bin Pyeon
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea
Eun-Young Kim
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Mirae Cell Bio, Seongdong-gu, Seoul, Korea
Se-Pill Park*
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Stem Cell Research Center, Jeju National University, Jeju-si, Jeju Special Self-Governing Province, Korea Mirae Cell Bio, Seongdong-gu, Seoul, Korea
*
Author for correspondence: Se-Pill Park. Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Tel: +82 64 754 4650. Email: sppark@jejunu.ac.kr
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Summary

Our previous studies have already revealed that β-cryptoxanthin (BCX), hesperetin (HES), and icariin (ICA) antioxidants are effective for in vitro maturation (IVM) of porcine oocytes. In this study, we investigated which of BCX, HES, or ICA was more effective for IVM of porcine oocytes. The antioxidant properties were assessed with aged porcine oocytes and embryos by comparing 2,2-diphenyl-1-(2,4,6-trinitrophenyl)hydrazyl (DPPH), reducing power, and H2O2 scavenging activity assays. The chemical assay results demonstrated that BCX had a greater DPPH scavenging activity and reducing power than HES and ICA, compared with controls. However, the H2O2 scavenging activity of the antioxidants was similar when tested at the optimal concentrations of 1 μM BCX (BCX-1), 100 μM HES (HES-100), and 5 μM ICA (ICA-5). The biological assay results showed that BCX-1 treatment was more effective in inducing a significant reduction in reactive oxygen species (ROS), improving glutathione levels, and increasing the expression of antioxidant genes. In addition, BCX-1 inhibited apoptosis by increasing the expression of anti-apoptotic genes and decreasing pro-apoptotic genes in porcine parthenogenetic blastocysts. BCX-1 also significantly increased the blastocyst formation rate compared with the ageing control group, HES-100 and ICA-5. This study demonstrates that damage from ROS produced during oocyte ageing can be prevented by supplementing antioxidants into the IVM medium, and BCX may be a potential candidate to improve assisted reproductive technologies.

Keywords

β-CryptoxanthinHesperetinIcariinIn vitro ageingPorcine oocyte
Type
Research Article
Information
Zygote , Volume 30 , Issue 4 , August 2022 , pp. 561 - 570
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Al-Amiery, AA, Al-Majedy, YK, Kadhum, AAH and Mohamad, AB (2015). Hydrogen peroxide scavenging activity of novel coumarins synthesized using different approaches. PLoS One 10, e0132175.CrossRefGoogle ScholarPubMed
Blois, MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181, 1199–200.CrossRefGoogle Scholar
Boerjan, ML and De Boer, P (1990). First cell cycle of zygotes of the mouse derived from oocytes aged postovulation in vivo and fertilized in vivo . Mol Reprod Dev 25, 155–63.CrossRefGoogle ScholarPubMed
Burri, BJ, La Frano, MR and Zhu, C (2016). Absorption, metabolism, and functions of beta-cryptoxanthin. Nutr Rev 74, 69–82.CrossRefGoogle ScholarPubMed
Chen, F and Huang, G (2019). Antioxidant activity of polysaccharides from different sources of ginseng. Int J Biol Macromol 125, 906–8.CrossRefGoogle ScholarPubMed
Del Río, LA, Sevilla, F, Gómez, M, Yañez, J and López, J (1978). Superoxide dismutase: An enzyme system for the study of micronutrient interactions in plants. Planta 140, 221–5.CrossRefGoogle Scholar
El Mouatassim, S, Guérin, P and Ménézo, Y (1999). Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation. Mol Hum Reprod 5, 720–5.CrossRefGoogle ScholarPubMed
Francenia Santos Sánchez, N, Salas Coronado, R, Villanueva Cañongo, C and Hernández Carlos, B (2019). Antioxidant compounds and their antioxidant mechanism. Antioxidants doi: 10.5772/intechopen.85270 CrossRefGoogle Scholar
Goc, A, Kochuparambil, ST, Al-Husein, B, Al-Azayzih, A, Mohammad, S and Somanath, PR (2012). Simultaneous modulation of the intrinsic and extrinsic pathways by simvastatin in mediating prostate cancer cell apoptosis. BMC Cancer 12, 409.CrossRefGoogle ScholarPubMed
Gülçın, İ, Oktay, M, Kıreçcı, E and Küfrevıoğlu, Öİ (2003). Screening of antioxidant and antimicrobial activities of anise (Pimpinella anisum L.) seed extracts. Food Chem 83, 371–82.CrossRefGoogle Scholar
Gupta, N, Srivastava, N and Bhagyawant, SS (2018). Vicilin-A major storage protein of mungbean exhibits antioxidative potential, antiproliferative effects and ACE inhibitory activity. PLoS One 13, e0191265.CrossRefGoogle ScholarPubMed
Halliwell, B (1991) Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am J Med 91(3C), 14S–22S.CrossRefGoogle ScholarPubMed
Haoujar, I, Cacciola, F, Abrini, J, Mangraviti, D, Giuffrida, D, Oulad El Majdoub, Y, Kounnoun, A, Miceli, N, Fernanda Taviano, M, Mondello, L, Rigano, F and Skali Senhaji, N (2019). The contribution of carotenoids, phenolic compounds, and flavonoids to the antioxidative properties of marine microalgae isolated from Mediterranean Morocco. Molecules 24, 4037.CrossRefGoogle Scholar
Hara, K, Someya, T, Sano, K, Sagane, Y, Watanabe, T and Wijesekara, RGS (2018). Antioxidant activities of traditional plants in Sri Lanka by DPPH free radical-scavenging assay. Data Brief 17, 870–5.CrossRefGoogle 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
Kikuzaki, H, Hisamoto, M, Hirose, K, Akiyama, K and Taniguchi, H (2002). Antioxidant properties of ferulic acid and its related compounds. J Agric Food Chem 50, 2161–8.CrossRefGoogle ScholarPubMed
Kim, HK, Jeong, TS, Lee, MK, Park, YB and Choi, MS (2003). Lipid-lowering efficacy of hesperetin metabolites in high-cholesterol fed rats. Clin Chim Acta 327, 129–37.CrossRefGoogle ScholarPubMed
Kim, WJ, Lee, SE, Park, YG, Jeong, SG, Kim, EY and Park, SP (2019). Antioxidant hesperetin improves the quality of porcine oocytes during aging in vitro . Mol Reprod Dev 86, 32–41.CrossRefGoogle ScholarPubMed
Kwak, SS, Cheong, SA, Jeon, Y, Lee, E, Choi, KC, Jeung, EB and Hyun, SH (2012). The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology 78, 86–101.CrossRefGoogle ScholarPubMed
Lee, SE, Sun, SC, Choi, HY, Uhm, SJ and Kim, NH (2012). mTOR is required for asymmetric division through small GTPases in mouse oocytes. Mol Reprod Dev 79, 356–66.CrossRefGoogle ScholarPubMed
Lee, SE, Kim, EY, Choi, HY, Moon, JJ, Park, MJ, Lee, JB, Jeong, CJ and Park, SP (2014). Rapamycin rescues the poor developmental capacity of aged porcine oocytes. Asian-Australas J Anim Sci 27, 635–47.CrossRefGoogle ScholarPubMed
Li, Y, Huang, TT, Carlson, EJ, Melov, S, Ursell, PC, Olson, JL, Noble, LJ, Yoshimura, MP, Berger, C, Chan, PH, Wallace, DC and Epstein, CJ (1995). Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11, 376–81.CrossRefGoogle ScholarPubMed
Lim, JY and Wang, XD (2020). Mechanistic understanding of beta-cryptoxanthin and lycopene in cancer prevention in animal models. Biochim Biophys Acta Mol Cell Biol Lipids 1865, 158652.CrossRefGoogle ScholarPubMed
Liu, C, Bronson, RT, Russell, RM and Wang, X-D (2011). β-Cryptoxanthin supplementation prevents cigarette smoke-induced lung inflammation, oxidative damage, and squamous metaplasia in ferrets. Cancer Prev Res (Phila) 4, 1255–66.CrossRefGoogle ScholarPubMed
Liu, JJ, Li, SP and Wang, YT (2006). Optimization for quantitative determination of four flavonoids in Epimedium by capillary zone electrophoresis coupled with diode array detection using central composite design. J Chromatogr A 1103, 344–9.CrossRefGoogle ScholarPubMed
Liu, J, Liu, L, Sun, J, Luo, Q, Yan, C, Zhang, H, Liu, F, Wei, Y and Dong, J (2019). Icariin protects hippocampal neurons from endoplasmic reticulum stress and NF-kappaB mediated apoptosis in fetal rat hippocampal neurons and asthma rats. Front Pharmacol 10, 1660.CrossRefGoogle ScholarPubMed
Liu, XR, Wang, YY, Dan, XG, Kumar, A, Ye, TZ, Yu, YY and Yang, LG (2016). Anti-inflammatory potential of β-cryptoxanthin against LPS-induced inflammation in mouse Sertoli cells. Reprod Toxicol 60, 148–55.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–DDCT method. Methods 25, 402–8.CrossRefGoogle Scholar
López-Martínez, LM, Santacruz-Ortega, H, Navarro, RE, Sotelo-Mundo, RR and González-Aguilar, GA (2015). A 1H NMR Investigation of the interaction between phenolic acids found in mango (Manguifera indica cv ataulfo) and papaya (Carica papaya cv maradol) and 1,1-diphenyl-2-picrylhydrazyl (DPPH) free radicals. PLoS One 10, e0140242.CrossRefGoogle ScholarPubMed
Lord, T and Aitken, RJ (2013). Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction 146, R217–27.CrossRefGoogle ScholarPubMed
Luna, M, Copperman, AB, Duke, M, Ezcurra, D, Sandler, B and Barritt, J (2008). Human blastocyst morphological quality is significantly improved in embryos classified as fast on day 3 (≥10 cells), bringing into question current embryological dogma. Fertil Steril 89, 358–63.CrossRefGoogle Scholar
Mehaisen, GMK, 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
Miceli, N, Marino, A, Köroğlu, A, Cacciola, F, Dugo, P, Mondello, L and Taviano, MF (2020). Comparative study of the phenolic profile, antioxidant and antimicrobial activities of leaf extracts of five Juniperus L. (Cupressaceae) taxa growing in Turkey. Nat Prod Res 34, 1636–41.CrossRefGoogle ScholarPubMed
Muhammad, T, Ikram, M, Ullah, R, Rehman, SU and Kim, MO (2019). Hesperetin, a citrus flavonoid, attenuates LPS-induced neuroinflammation, apoptosis and memory impairments by modulating TLR4/NF-kB signaling. Nutrients 11, 648.CrossRefGoogle Scholar
Moldogazieva, NT, Mokhosoev, IM, Feldman, NB and Lutsenko, SV (2018). ROS and RNS signalling: adaptive redox switches through oxidative/nitrosative protein modifications. Free Radic Res 52, 507–43.CrossRefGoogle ScholarPubMed
Nasheed Hamad Almohammed, Z, Moghani-Ghoroghi, F, Ragerdi-Kashani, I, Fathi, R, Tahaei, LS, Naji, M and Pasbakhsh, P (2019). The effect of melatonin on mitochondrial function and autophagy in in vitro matured oocytes of aged mice. Cell J 22, 9–16.Google ScholarPubMed
Němeček, D, Dvořáková, M, Heroutová, I, Chmelíková, E and Sedmíková, M (2017). Anti-apoptotic properties of carbon monoxide in porcine oocyte during in vitro aging. Peer J 5, e3876.CrossRefGoogle ScholarPubMed
Newman, B and Dai, Y (1996). Transcription of c-mos protooncogene in the pig involves both tissue-specific promoters and alternative polyadenylation sites. Mol Reprod Dev 44, 275–88.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Nguyen, T, Nioi, P and Pickett, CB (2009). The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284, 13291–5.CrossRefGoogle ScholarPubMed
Niu, YJ, Zhou, W, Nie, ZW, Zhou, D, Xu, YN, Ock, SA, Yan, CG and Cui, XS (2020). Ubiquinol-10 delays postovulatory oocyte aging by improving mitochondrial renewal in pigs. Aging (Albany New York) 12, 1256–71.Google ScholarPubMed
Ochota, M, Wojtasik, B and Niżański, W (2016). Total cell number and its allocation to trophectoderm and inner cell mass in in vitro obtained cats’ blastocysts. Reprod Domest Anim 51, 339–45.CrossRefGoogle ScholarPubMed
Park, YG, Lee, SE, Son, YJ, Jeong, SG, Shin, MY, Kim, WJ, Kim, EY and Park, SP (2018). Antioxidant beta-cryptoxanthin enhances porcine oocyte maturation and subsequent embryo development in vitro . Reprod Fertil Dev 30, 1204–13.CrossRefGoogle ScholarPubMed
Piras, AR, Menéndez-Blanco, I, Soto-Heras, S, Catalá, MG, Izquierdo, D, Bogliolo, L and Paramio, MT (2019). Resveratrol supplementation during in vitro maturation improves embryo development of prepubertal goat oocytes selected by brilliant cresyl blue staining. J Reprod Dev 65, 113–20.CrossRefGoogle ScholarPubMed
Roman, P, Budziński, G, Suszka-Świtek, A, Caban, A, Oczkowicz, G, Czech, E, Ryszka, F, Wiaderkiewicz, R, Smorąg, Z and Cierpka, L (2016). Caspase-3 expression and ALT, AST, and GGT activity after 24 hours of porcine liver cold storage, depending on the type of transgenesis. Transplant Proc 48, 1829–32.CrossRefGoogle ScholarPubMed
Ruch, RJ, Cheng, SJ and Klaunig, JE (1989). Prevention of cytotoxicity and inhibition of intercellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis 10, 1003–8.CrossRefGoogle ScholarPubMed
Schroeder, A and Johnson, EA (1993). Antioxidant role of carotenoids in Phaffia rhodozyma . J Gen Microbiol 139, 907–12.CrossRefGoogle Scholar
Sebaugh, JL (2011). Guidelines for accurate EC50/IC50 estimation. Pharm Stat 10, 128–34.CrossRefGoogle ScholarPubMed
Sugiura, M Ogawa, K and Yano, M (2013). Absorption, storage and distribution of β-cryptoxanthin in rat after chronic administration of satsuma mandarin (Citrus unshiu MARC.) juice. Biol Pharm Bull 36, 147–51.CrossRefGoogle ScholarPubMed
Takahashi, M (2012). Oxidative stress and redox regulation on in vitro development of mammalian embryos. J Reprod Dev 58, 1–9.CrossRefGoogle ScholarPubMed
Taviano, MF, Filocamo, A, Ragusa, S, Cacciola, F, Dugo, P, Mondello, L, Paterniti Mastrazzo, G, De Rose, RF, Celano, M, Lombardo, GE, Melchini, A and Miceli, N (2018). Phenolic profile, antioxidant and cytotoxic properties of polar extracts from leaves and flowers of Isatis tinctoria L. (Brassicaceae) growing in Sicily. Plant Biosyst 152, 795–803.CrossRefGoogle Scholar
Teshima, TH, Ianez, RC, Coutinho-Camillo, CM, Tucker, AS and Lourenço, SV (2016). Apoptosis-associated protein expression in human salivary gland morphogenesis. Arch Oral Biol 69, 71–81.CrossRefGoogle ScholarPubMed
Wang, Y, Branicky, R, Noë, A and Hekimi, S (2018). Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling. J Cell Biol 217, 1915–28.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
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
Yoon, JW, Lee, SE, Park, YG, Kim, WJ, Park, HJ, Park, CO, Kim, SH, Oh, SH, Lee, DG, Pyeon, DB, Kim, EY and Park, SP (2021) The antioxidant icariin protects porcine oocytes from age-related damage in vitro. Anim Biosci, 34, 546–57.CrossRefGoogle ScholarPubMed
You, J, Kim, J, Lim, J and Lee, E (2010). Anthocyanin stimulates in vitro development of cloned pig embryos by increasing the intracellular glutathione level and inhibiting reactive oxygen species. Theriogenology 74, 777–85.CrossRefGoogle ScholarPubMed