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Effect of zinc chloride and sodium selenite supplementation on in vitro maturation, oxidative biomarkers, and gene expression in buffalo (Bubalus bubalis) oocytes

Published online by Cambridge University Press:  26 March 2021

Wael A. Khalil ,
Chun-Yan Yang ,
Mostafa M. El-Moghazy ,
Mohamed S. El-Rais ,
Jiang-Hua Shang  and
Ashraf El-Sayed Open the ORCID record for Ashraf El-Sayed [Opens in a new window]
Wael A. Khalil*
Affiliation:
Animal Production Department, Faculty of Agriculture, Mansoura University, Mansoura, Egypt
Chun-Yan Yang
Affiliation:
Key Laboratory of Buffalo Genetics, Breeding and Reproduction Technology, Ministry of Agriculture and Guangxi, Buffalo Research Institute, Chinese Academy of Agricultural Sciences, Nanning, 530001, China
Mostafa M. El-Moghazy
Affiliation:
Animal Production Department, Faculty of Agriculture, Damietta University, Damietta, Egypt
Mohamed S. El-Rais
Affiliation:
Animal Production Department, Faculty of Agriculture, Damietta University, Damietta, Egypt
Jiang-Hua Shang
Affiliation:
Key Laboratory of Buffalo Genetics, Breeding and Reproduction Technology, Ministry of Agriculture and Guangxi, Buffalo Research Institute, Chinese Academy of Agricultural Sciences, Nanning, 530001, China
Ashraf El-Sayed
Affiliation:
Animal Production Department, Faculty of Agriculture, Cairo University, Giza, Egypt King Abdulaziz University, Jeddah, Kingdom of Saudi Arabia
*
Author for correspondence: Wael A. Khalil. Animal Production Department, Faculty of Agriculture, Mansoura University, Mansoura, Egypt. E-mail: [email protected]
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Summary

This study examined the effects of zinc chloride (ZnCl2) and sodium selenite (Na2SeO3) supplementation in maturation medium on in vitro maturation (IVM) rate, oxidative biomarkers and gene expression in buffalo oocytes. Ovaries from a slaughterhouse were aspirated and good quality cumulus–oocyte complexes (COCs) with at least four layers of compact cumulus cells and evenly granulated dark ooplasm were selected. COCs were randomly allocated during IVM (22 h) to one of four treatment groups: (1) control maturation medium (basic medium), or basic medium supplemented with (2) ZnCl2 (1.5 µg/ml), (3) Na2SeO3 (5 µg/l), or (4) ZnCl2 + Na2SeO3 (1.5 µg/ml + 5 µg/l, respectively). Oocytes were denuded after 22 h of IVM in the first four replicates. Specimens were fixed and stained to evaluate the stage of nuclear maturation. The spent medium was collected for biochemical assays of total antioxidant capacity (TAC), malondialdehyde (MDA) and hydrogen peroxide concentrations. A second four replicates were used for COCs for RNA extraction. The expression levels of antioxidant (SOD1, GPX4, CAT and PRDX1), antiapoptotic (BCL2 and BCL-XL) and proapoptotic (BAX and BID) genes were measured. Supplementation with ZnCl2 and Na2SeO3 during IVM increased the ratio of oocytes reaching metaphase II at 22 h, increased TAC and decreased MDA and H2O2 concentrations in the maturation medium (P < 0.05). Moreover, beneficial effects were associated with complementary changes in expression patterns of antioxidative, antiapoptotic and proapoptotic genes, suggesting lower oxidative stress and apoptosis. Supplementation medium with zinc chloride and sodium selenite improves the maturation rate, reduces oxidative stress and increases expression levels of antioxidative and antiapoptotic genes.

Keywords

BuffaloGene expressionIn vitro maturationOxidative biomarkersSodium seleniteZinc chloride
Type
Research Article
Information
Zygote , Volume 29 , Issue 5 , October 2021 , pp. 393 - 400
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Abedelahi, A, Salehnia, M, Allameh, AA and Davoodi, D (2010). Sodium selenite improves the in vitro follicular development by reducing the reactive oxygen species level and increasing the total antioxidant capacity and glutathione peroxide activity. Hum Reprod 25, 977–85.CrossRefGoogle ScholarPubMed
Aebi, H (1984). Catalase in vitro . Methods Enzymol 105, 121–6.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
Aghaz, F and Khazaei, M (2017). Reactive oxygen species generation and use of antioxidants during in vitro maturation of oocytes. Int J Fertil Steril 11, 63–70.Google Scholar
Anchordoquy, JM, Anchordoquy, JP, Sirini, MA, Picco, SJ, Peral-García, P and Furnus, CC (2014). The importance of having zinc during in vitro maturation of cattle cumulus–oocyte complex: role of cumulus cells. Reprod Domest Anim 49, 865–74.CrossRefGoogle ScholarPubMed
Anchordoquy, JM, Picco, SJ, Seoane, A, Anchordoquy, JP, Ponzinibbio, MV, Mattioli, GA, Peral-García, P and Furnus, CC (2011). Analysis of apoptosis and DNA damage in bovine cumulus cells after exposure in vitro to different zinc concentrations. Cell Biol Int 35, 593–7.CrossRefGoogle ScholarPubMed
Baruselli, PS, Soares, JG, Bayeux, BM, Silva, JCB, Mingoti, RD and Carvalho, NAT (2018). Assisted reproductive technologies (ART) in water buffaloes. Anim Reprod 15, 971–83.CrossRefGoogle Scholar
Bosse, AC, Pallauf, J, Hommel, B, Sturm, M, Fischer, S, Wolf, NM and Mueller, AS (2010). Impact of selenite and selenate on differentially expressed genes in rat liver examined by microarray analysis. Biosci Rep 30, 293–306.CrossRefGoogle ScholarPubMed
Branca, JJV, Morucci, G, Maresca, M, Tenci, B, Cascella, R, Paternostro, F, Ghelardini, C, Gulisano, M, Mannelli, LD-C and Pacini, A (2018). Selenium and zinc: two key players against cadmium-induced neuronal toxicity. Toxicol In Vitro 48, 159–69.CrossRefGoogle ScholarPubMed
Cathomen, T and Joung, JK (2008). Zinc-finger nucleases: the next generation emerges. Mol Ther 16, 1200–7.CrossRefGoogle ScholarPubMed
Chai, F, Truong-Tran, AQ, Ho, LH and Zalewski, PD (1999). Regulation of caspase activation and apoptosis by cellular zinc fluxes and zinc deprivation: a review. Immunol Cell Biol 77, 272–8.CrossRefGoogle ScholarPubMed
Demyda, S and Genero, E (2011). Developmental competence of in vivo and in vitro matured oocytes: a review. Biotechnol Mol Biol Rev 6, 155–65.Google Scholar
Duncan, BD (1955). Multiple range and multiple F-test. Biometrics 11, 1–42.CrossRefGoogle Scholar
Duprez, J, Roma, LP, Close, A-F and Jonas, J-C (2012). Protective antioxidant and antiapoptotic effects of ZnCl2 in rat pancreatic islets cultured in low and high glucose concentrations. PLoS One 7, 1–11.CrossRefGoogle ScholarPubMed
Ebert, R, Ulmer, M, Zeck, S, Meissner-Weigl, J, Schneider, D, Stopper, H, Schupp, N, Kassem, M and Jakob, F (2006). Selenium supplementation restores the antioxidative capacity and prevents cell damage in bone marrow stromal cells in vitro. Stem Cells 24, 1226–35.CrossRefGoogle ScholarPubMed
El-Sayed, A, Salem, SM, El-Garhy, AA, Rahman, ZA and Kandil, AM (2013). Protective effect of zinc against cadmium toxicity on pregnant rats and their fetuses at morphological, physiological and molecular level. African J Biotechnol 12, 2110–9.Google Scholar
Ferreira, EM, Vireque, AA, Adona, PR, Meirelles, FV, Ferriani, RA and Navarro, PAAS (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–48.CrossRefGoogle ScholarPubMed
Ghorbanmehr, N, Salehnia, M and Amoushahi, M (2018). The effects of sodium selenite on mitochondrial DNA copy number and reactive oxygen species levels of in vitro matured mouse oocytes. Cell J 20, 396–402.Google ScholarPubMed
Hewitt, DA, Watson, PF and England, GCW (1998). Nuclear staining and culture requirements for in vitro maturation of domestic bitch oocytes. Theriogenology 49, 1083–101.CrossRefGoogle ScholarPubMed
Imed, M, Fatima, H and Abdelhamid, K (2009). Protective effects of selenium (Se) and zinc (Zn) on cadmium (Cd) toxicity in the liver of the rat: effects on the oxidative stress. Ecotoxicol Environ Safety 72, 1559–64.Google Scholar
Jeon, Y, Yoon, JD, Cai, L, Hwang, SU, Kim, E, Zheng, Z, Lee, E, Kim, DY and Hyun, SH (2014). Supplementation of zinc on oocyte in vitro maturation improves preimplantation embryonic development in pigs. Theriogenology 82, 866–74.CrossRefGoogle Scholar
Kakkassery, MP, Vijayakumaran, V and Sreekumaran, T (2010). Effect of cumulus–oocyte complex morphology on in vitro maturation of bovine oocytes. J Vet Anim Sci 41, 12–7.Google Scholar
Kala, M, Shaikh, MV and Nivsarkar, M (2017). Equilibrium between anti-oxidants and reactive oxygen species: a requisite for oocyte development and maturation. Reprod Med Biol 16, 28–35.CrossRefGoogle ScholarPubMed
Khoudja, RY, Xu, Y, Li, T and Zhou, C (2013). Better IVF outcomes following improvements in laboratory air quality. J Assist Reprod Genet 30, 69–76.CrossRefGoogle ScholarPubMed
Kloubert, V and Rink, L (2015). Zinc as a micronutrient and its preventive role of oxidative damage in cells. Food Function 6, 3195–204.CrossRefGoogle ScholarPubMed
Koracevic, D, Koracevic, G, Djordjevic, V, Andrejevic, S and Cosic, V (2001). Method for the measurement of antioxidant activity in human fluids. J Clin Pathol 54, 356–61.CrossRefGoogle ScholarPubMed
Leoni, GG, Rosati, I, Succu, S, Bogliolo, L, Bebbere, D, Berlinguer, F, Ledda, S and Naitana, S (2007). A low oxygen atmosphere during IVF accelerates the kinetic of formation of in vitro produced ovine blastocysts. Reprod Domest Anim 42, 299–304.CrossRefGoogle ScholarPubMed
Liebel, F, Kaur, S, Ruvolo, E, Kollias, N and Southall, MD (2012). Irradiation of skin with visible light induces reactive oxygen species and matrix-degrading enzymes. J Invest Dermatol 132, 1901–7.CrossRefGoogle ScholarPubMed
Lockshin, RA and Zakeri, Z (2007). Cell death in health and disease. J Cell Mol Med 11, 1214–24.CrossRefGoogle ScholarPubMed
Mahmoud, KGM and El-Naby, A (2013). Factors affecting buffalo oocyte maturation. Glob Vet 11, 497–510.Google Scholar
Menezo, YJ, Silvestris, E, Dale, B and Elder, K (2016). Oxidative stress and alterations in DNA methylation: two sides of the same coin in reproduction. Reprod Biomed Online 33, 668–83.CrossRefGoogle ScholarPubMed
Ohkawa, H, Ohishi, N and Yagi, K (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95, 351–8.CrossRefGoogle ScholarPubMed
Oltval, ZN, Milliman, CL and Korsmeyer, SJ (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death. Cell 74, 609–19.CrossRefGoogle Scholar
Picco, SJ, Anchordoquy, JM, De Matos, DG, Anchordoquy, JP, Seoane, A, Mattioli, GA, Errecalde, AL and Furnus, CC (2010). Effect of increasing zinc sulphate concentration during in vitro maturation of bovine oocytes. Theriogenology 74, 1141–8.CrossRefGoogle ScholarPubMed
Rice, JM, Zweifach, A and Lynes, MA (2016). Metallothionein regulates intracellular zinc signaling during CD4+ T cell activation. BMC Immunol 17, 1–14.CrossRefGoogle ScholarPubMed
SAS (2007). Statistical analysis System. Stat User’s Guide. Release 9.1.3. SAS Institute. Cary, NC, USA.Google Scholar
Schnabel, R, Lubos, E, Messow, CM, Sinning, CR, Zeller, T, Wild, PS, Peetz, D, Handy, DE, Munzel, T and Loscalzo, J (2008). Selenium supplementation improves antioxidant capacity in vitro and in vivo in patients with coronary artery disease: the selenium therapy in coronary artery disease patients (SETCAP) study. Am Heart J 156, 1–20.CrossRefGoogle ScholarPubMed
Szuster-Ciesielska, A, Stachura, A, Słotwińska, M, Kamińska, T, Śnieżko, R, Paduch, R, Abramczyk, D, Filar, J and Kandefer-Szerszeń, M (2000). The inhibitory effect of zinc on cadmium-induced cell apoptosis and reactive oxygen species (ROS) production in cell cultures. Toxicology 145, 159–71.CrossRefGoogle ScholarPubMed
Tareq, KMA, Akter, QS, Khandoker, MA and Tsujii, H (2012). Selenium and vitamin E improve the in vitro maturation, fertilization and culture to blastocyst of porcine oocytes. J Reprod Dev 58, 621–8.CrossRefGoogle ScholarPubMed
Tariba, B, Živković, T, Gajski, G, Gerić, M, Gluščić, V, Garaj-Vrhovac, V, Peraica, M and Pizent, A (2017). In vitro effects of simultaneous exposure to platinum and cadmium on the activity of antioxidant enzymes and DNA damage and potential protective effects of selenium and zinc. Drug Chem Toxicol 40, 228–34.CrossRefGoogle ScholarPubMed
Tiwari, M, Prasad, S, Tripathi, A, Pandey, AN, Singh, AK, Shrivastav, TG and Chaube, SK (2016). Involvement of reactive oxygen species in meiotic cell cycle regulation and apoptosis in mammalian oocytes. Reactive Oxygen Species 1, 110–6.CrossRefGoogle Scholar
Truong-Tran, AQ, Carter, J, Ruffin, RE and Zalewski, PD (2001). The role of zinc in caspase activation and apoptotic cell death. In Maret, W (eds). Zinc Biochemistry, Physiology, and Homeostasis. Springer, Dordrecht, pp. 129–44.CrossRefGoogle Scholar
Xiong, X, Lan, D, Li, J, Lin, Y and Li, M (2018a). Selenium supplementation during in vitro maturation enhances meiosis and developmental capacity of yak oocytes. Anim Sci J 89, 298–306.CrossRefGoogle ScholarPubMed
Xiong, X, Lan, D, Li, J, Lin, Y and Zi, X (2018b). Effects of zinc supplementation during in vitro maturation on meiotic maturation of oocytes and developmental capacity in Yak. Biol Trace Element Res 185, 89–97.CrossRefGoogle ScholarPubMed
Yadav, A, Singh, KP, Singh, MK, Saini, N, Palta, P, Manik, RS, Singla, SK, Upadhyay, RC and Chauhan, MS (2013). Effect of physiologically relevant heat shock on development, apoptosis and expression of some genes in buffalo (Bubalus bubalis) embryos produced in vitro . Reprod Domest Anim 48, 858–65.CrossRefGoogle ScholarPubMed
Yeo, JE and Kang, SK (2007). Selenium effectively inhibits ROS-mediated apoptotic neural precursor cell death in vitro and in vivo in traumatic brain injury. Biochim Biophys Acta 1772, 1199–210.CrossRefGoogle ScholarPubMed