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Eugenol influences the expression of messenger RNAs for superoxide dismutase and glutathione peroxidase 1 in bovine secondary follicles cultured in vitro

Published online by Cambridge University Press:  18 February 2021

E.M. Vasconcelos ,
F.C. Costa ,
A.V.N. Azevedo ,
P.A.A. Barroso ,
E.I.T. de Assis ,
L.R.F.M. Paulino ,
B.R. Silva ,
A.W.B. Silva ,
A.L.P. Souza  and
J.R.V. Silva Open the ORCID record for J.R.V. Silva [Opens in a new window]
E.M. Vasconcelos
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
F.C. Costa
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
A.V.N. Azevedo
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
P.A.A. Barroso
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
E.I.T. de Assis
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
L.R.F.M. Paulino
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
B.R. Silva
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
A.W.B. Silva
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
A.L.P. Souza
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
J.R.V. Silva*
Affiliation:
Postgraduate Programme in Biotechnology, Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceará, Av. Comandante Mauricélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
*
Author for correspondence: J. R. V. Silva. Biotechnology Nucleus of Sobral – NUBIS, Federal University of Ceará, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil. Tel:/Fax: +55 88 36118000. E-mail jrvsilva@ufc.br
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Summary

This study aimed to investigate the effects of eugenol on growth, viability, antrum formation and mRNA expression of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase 1 (GPX1) and peroxiredoxin 6 (PRDX6) in bovine secondary follicles cultured in vitro. To this end, bovine ovaries were collected from a local slaughterhouse and in the laboratory the follicles were isolated from the ovarian cortex. The follicles were then cultured in TCM-199+ alone or supplemented with different concentrations of eugenol (0.5, 5.0 and 50.0 μM). Follicular diameters and antrum formation were evaluated on days 0, 6, 12 and 18. Viability analysis was performed using calcein and ethidium homodimer. Real-time PCR was used to quantify mRNA levels for SOD, CAT, GPX1 and PRDX6 in cultured follicles. Follicular diameters and mRNA levels in follicles cultured in vitro were compared using analysis of variance and Kruskal–Wallis tests, while follicular survival and antrum formation were compared using the chi-squared test (P < 0.05). The results showed that secondary follicles cultured with eugenol maintained similar morphology and viability to follicles cultured in the control group. A progressive increase in follicular diameter was observed between days 0 and 12 for all treatments, except for follicles cultured with 50 µM eugenol. Eugenol (5.0 and 50.0 μM) increased mRNA levels for GPX1 in cultured follicles, but 0.5 μM eugenol reduced mRNA levels for SOD. The addition of eugenol did not influence mRNA expression for CAT and PRDX6. In conclusion, eugenol supplementation reduces mRNA levels for SOD and increases mRNA levels of GPX1 in bovine secondary follicles cultured in vitro.

Keywords

AntioxidantBovineEugenolGene expressionPreantral follicles
Type
Research Article
Information
Zygote , Volume 29 , Issue 4 , August 2021 , pp. 301 - 306
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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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
Alves, JCO, Ferreira, GF, Santos, JR, Silva, LCN, Rodrigues, JFS, Neto, WRN, Farah, EI, Santos, ARC, Mendes, BS, Sousa, LVNF, Monteiro, AS, Dos Santos, VL, Santos, DA, Perez, AC, Romero, TRL, Denadai, AML and Guzzo, LS (2017). Eugenol induces phenotypic alterations and increases the oxidative burst in Cryptococcus . Front Microbiol 8, 2419.CrossRefGoogle ScholarPubMed
Arevalo, JA and Vázquez-Medina, JP (2018). The role of peroxiredoxin 6 in cell signaling. Antioxidants 24, 1–13.Google Scholar
Barberino, RS, Barros, VRP, Menezes, VG, Santos, LP, Araújo, VR, Queiroz, MAA, Almeida, JRGS, Palheta, RC and Matos, MHT (2015). Amburana cearensis leaf extract maintains survival and promotes in vitro development of ovine secondary follicles. Zygote 24, 277–85.CrossRefGoogle ScholarPubMed
Britt, JH (1991). Impacts of early postpartum metabolism on follicular development and fertility. The Bovine Practitioner Proceeding 24, 39–43.Google Scholar
Calder, MD, Caveney, AN, Westhusin, ME and Watson, AJ (2001). Cyclooxygenase-2 and prostaglandin E2 (PGE2) receptor messenger RNAs are affected by bovine oocyte maturation time and cumulus–oocyte complex quality, and PGE2 induces moderate expansion of the bovine cumulus in vitro . Biol Reprod 65, 135–40.CrossRefGoogle ScholarPubMed
Ceko, MJ, Hummitzsch, K, Hatzirodos, N, Bonner, WM, Aitken, JB, Russell, DL, Lane, M, Rodgers, RJ and Harris, HH (2015). X-ray fluorescence imaging and other analyses identify selenium and GPX1 as important in female reproductive function. Metallomics 7, 71–82.CrossRefGoogle ScholarPubMed
De Matos, DG, Furnus, CC and Moses, DF (1997). Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol Reprod 57, 1420–5.CrossRefGoogle ScholarPubMed
Elvin, JA, Yan, C and Matzuk, MM (2000). Growth differentiation factor-9 stimulates progesterone synthesis in granulosa cells via a prostaglandin E2/EP2 receptor pathway. Proc Natl Acad Sci USA 97, 10288–93.CrossRefGoogle Scholar
Figueiredo, JR, Cadenas, J, Lima, LF and Santo, RR (2019). Advances in in vitro folliculogenesis in domestic animal ruminants. Anim Reprod 16, 52–65.CrossRefGoogle Scholar
Fernandez, MC, Yu, A, Moawad, AR and O’Flaherty, C (2019). Peroxiredoxin 6 regulates the phosphoinositide 3-kinase/AKT pathway to maintain human sperm viability. Mol Hum Reprod 25, 787–96.Google ScholarPubMed
Fouad, AA and Yacoubi, MT (2011). Mechanisms underlying the protective effect of eugenol in rats with acute doxorubicin cardiotoxicity. Arch Pharm Res 4, 821–8.CrossRefGoogle Scholar
Gallelli, C.A, Calcagnini, S, Romano, A, Koczwara, JB, de Ceglia, M, Dante, D, Villani, R, Giudetti, AM, Cassano, T and Gaetani, S (2018). Modulation of the oxidative stress and lipid peroxidation by endocannabinoids and their lipid analogues. Antioxidants 7, 2–44.CrossRefGoogle ScholarPubMed
Halliwell, B (2014). Cell culture, oxidative stress, and antioxidants: avoiding pitfalls. Biomed J 37, 99–105.Google ScholarPubMed
Harvey, AJ, Kind, KL and Thompson, JG (2002). REDOX regulation of early embryo development. Reproduction 123, 479–86.CrossRefGoogle ScholarPubMed
Hsueh, AJ, Kawamura, K, Cheng, Y and Fauser, BC (2015). Intraovarian control of early folliculogenesis. Endocr Ver 36, 1–24.Google ScholarPubMed
Kashka, RH, Zavareh, S and Lashkarbolouki, T (2016). Augmenting effect of vitrification on lipid peroxidation in mouse preantral follicle during cultivation: modulation by coenzyme Q10. Syst Biol Reprod Med 62, 404–14.CrossRefGoogle ScholarPubMed
Kurutas, EB (2016). The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutr J 15, 171.Google ScholarPubMed
Leyens, G, Knoops, B and Donnay, I (2004). Expression of peroxiredoxins in bovine oocytes and embryos produced in vitro . Mol Reprod Dev 69, 243–51.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–8.CrossRefGoogle Scholar
Lopes, AA, da Fonseca, FN, Rocha, TM, de Freitas, LB, Araújo, EVO, Wong, DVT, Lima Júnior, RCP and Lea, LKAM (2018). Eugenol as a promising molecule for the treatment of dermatitis: antioxidant and anti-inflammatory activities and its nanoformulation. Oxid Med Cell Longev 2018, 1–13.CrossRefGoogle Scholar
Magalhães, CB, Casquilhoa, NV, Machado, MN, Riva, DR, Travassos, LH, Leal-Cardoso, JH, Fortunato, RS, Faffe, DS and Zina, WA (2018). The anti-inflammatory and anti-oxidative actions of eugenol improve lipopolysaccharide-induced lung injury. Resp Physiol Neurobiol 259, 1–7.Google ScholarPubMed
Nagababu, E and Lakshmaiah, N (1992). Efeito inibitório do eugenol na peroxidação lipídica não enzimática em mitocôndrias de fígado de ratos. Biochem Pharmacol 43, 2393–400.CrossRefGoogle Scholar
Nagababu, E and Lakshmaiah, N (1994). Inhibition of microsomal lipid peroxidation and monooxygenase activities by eugenol. Free Radic Res 20, 235–66.CrossRefGoogle ScholarPubMed
Nagababu, E, Rifkind, JM, Boindala, S and Nakka, L (2010). Assessment of antioxidant activity of eugenol in vitro and in vivo . Methods Mol Biol 610, 165–80.CrossRefGoogle ScholarPubMed
Park, YS, You, SY, Cho, S, Jeon, HJ, Lee, S, Cho, DH, Kim, JS and Oh, JS (2016). Eccentric localization of catalase to protect chromosomes from oxidative damages during meiotic maturation in mouse oocytes. Histochem Cell Biol 146, 281–8.CrossRefGoogle ScholarPubMed
Sá, NAR, Bruno, JB, Guerreiro, DD, Cadenas, J, Alves, BG, Cibin, FWS, Leal-Cardoso, Gastal EL and Figueiredo, JR (2018). Anethole reduces oxidative stress and improves in vitro survival and activation of primordial follicles. Braz J Med Biol Res 51, 8, e7129.CrossRefGoogle ScholarPubMed
Saeed-Zidane, M, Linden, L, Salilew-Wondim, D, Held, E, Neuhoff, C, Tholen, E, Hoelker, M, Schellander, K and Tesfaye, D (2017). Cellular and exosome mediated molecular defense mechanism in bovine granulosa cells exposed to oxidative stress. PLoS One 12, 1–24.CrossRefGoogle ScholarPubMed
Sies, H (2015). Oxidative stress: a concept in redox biology and medicine. Redox Biol 4, 180–3.CrossRefGoogle ScholarPubMed
Salah, A, Bouaziz, C, Amara, I, Abid-Essefi, S and Bacha, H (2019). Eugenol protects against citrinin-induced cytotoxicity and oxidative damages in cultured human colorectal HCT116 cells. Environ Sci Pollut Res 26, 31374–83.CrossRefGoogle ScholarPubMed
Salavati, M, Ghafari, F, Zhang, T and Fouladi-Nashta, AA (2012). Effects of oxygen concentration on in vitro maturation of canine oocytes in a chemically defined serum-free medium. Reproduction 144, 547–56.CrossRefGoogle Scholar
Slamenová, D, Horváthová, E, Wsólová, L, Sramková, M and Navarová, J (2009). Investigation of anti-oxidative, cytotoxic, DNA-damaging and DNA-protective effects of plant volatiles eugenol and borneol in human-derived HepG2, Caco-2 and VH10 cell lines. Mutat Res 677, 46–52.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
Tiku, AB, Abraham, SK and Kale, RK (2004). Eugenol as an in vivo radio protective agent. J Radiat Res 45, 435–40.CrossRefGoogle Scholar
Van Den Hurk, R, Spek, ER, Hage, WJ, Fair, T, Ralph, JH and Schotanus, K (1998). Ultrastructure and viability of isolated bovine preantral follicles. Hum Reprod Update 4, 833–41.CrossRefGoogle ScholarPubMed
Wang, F, Xu, SC, Zhou, Y, Wang, PM and Zhang, XM (2017). Trace element exposure of whooper swans (Cygnus cygnus) wintering in a marine lagoon (Swan Lake), northern China. Mar Pollut Bull 119, 60–7.CrossRefGoogle Scholar
Wang, Y, Phelan, SA, Manevich, Y, Feinstein, SI and Fisher, AB (2006). Transgenic mice overexpressing peroxiredoxin 6 show increased resistance to lung injury in hyperoxia. Am J Respir Cell Mol Biol 34, 481–6.CrossRefGoogle ScholarPubMed
Zhao, GR, Xiang, ZJ, Ye, TX, Yuan, YJ and Guo, ZX (2006). Antioxidant activities of Salvia miltiorrhiza and Panax notoginseng . Food Chem 99, 767–74.CrossRefGoogle Scholar