The antioxidative effect of gamma-oryzanol on ovine embryo development in vitro

Document Type : Original Article

Authors
Saeed Musapoor 1
Najmeh Davoodian 2
Ali kadivar 3
Ebrahimٍ Ahmadi 2
Hassan Nazari 4
1 Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord- Iran
2 Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran
3 Department of Clinical Sciences, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran
4 Research Institute of Animal Embryo Technology
10.22034/ijvcs.2023.14472.1057
Abstract
The researches of the past two decades in the field of laboratory embryo production in ruminants tried to maximize the number of developed embryos and increase the quality of produced blastocysts. The present study addresses the effect of gamma-oryzanol in the culture medium of ovine oocytes using embryo development evaluation. For this purpose, ovine ovaries were collected from the slaughterhouse, and then the oocytes were aspirated from 2 to 6 mm follicles subjected to washing, maturation and fertilization in vitro, then cultured in drops of medium enriched with or without 5 μM of gamma-oryzanol. Assessment of embryo development showed that the cleavage and total blastocyst rate was higher in treatment than control (P < 0.05), however, there was no difference between early, expanded, and hatched blastocysts as well as total cell number. The results showed downregulation of BAX, and Caspase-9 transcripts however no modulation was observed in the expression of BCL-2, NRF2, SOD, and CAT transcripts in treatment group compared to control. In conclusion, gamma-oryzanol improves the efficiency of ovine embryo production through an antiapoptotic pathway.
Keywords
sheep
embryo
gamma-oryzanol
antioxidant
Subjects
 1-      Agarwal, A; Durairajanayagam, D. and Du-Plessis, SS; Utility of antioxidants during assisted reproductive techniques: an evidence based review. Reprod.Biol.Endocrinol; 2014;12:1-19.
2-      Anjos, J; Aguiar, F; Sá, N; Souza, J; Cibin, F. and Alves, B; Anethole improves blastocysts rates together with antioxidant capacity when added during bovine embryo culture rather than in the in vitro maturation medium. Zygote; 2019;27:382-5.
3-      Aruoma, O; Halliwell, B; Laughton, M; Quinlan, G. and Gutteridge, J; The mechanism of initiation of lipid peroxidation. Evidence against a requirement for an iron (II)-iron (III) complex. Biochem.J; 1989;258:617-20.
4-      Chanapiwat, P. and Kaeoket, K; Breed of boar influences the optimal concentration of gamma‐oryzanol needed for semen cryopreservation. Reprod.Domes.Anim; 2015;50:221-6.
5-      Cicero, A. and Gaddi, A; Rice bran oil and γ‐oryzanol in the treatment of hyperlipoproteinaemias and other conditions. Phyto.Res; 2001;15:277-89.
6-      Cognie, Y, Baril G; Poulin, N. and Mermillod, P; Current status of embryo technologies in sheep and goat. Theriogenology; 2003;59:171-88.
7-      De-Oliveira, L.R.M; de-Aquino, L.V.C; de-Oliveira, S.M.V; Figueirêdo-Freitas, V.J; Bertini, L.M. and Pereira, A.F; Effects of different concentrations of eugenol in maturation medium on bovine oocytes, oxidative status and preimplantation embryos. Anim.Prod.Sci; 2021;62:142-51.
8-      Gad, A; Hoelker, M; Besenfelder, U; Havlicek, V; Cinar, U. and Rings, F; Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol.Reprod; 2012;87-98.
9-      Guemra, S; Monzani, P; Santos, E; Zanin, R; Ohashi, O. and Miranda, M; In vitro maturation of bovine oocytes in medium supplemented with quercetin, and its effect on embryonic development. Arq.Bras.Med.Vet.Zoo; 2013;65:1616-24.
10-  Guerin, P.E.l; Mouatassim, S. and Menezo, Y; Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum.Reprod.Upd; 2001;7:175-89.
11-  Huang, D; Ou, B; Hampsch-Woodill, M; Flanagan, J.A. and Deemer, E.K; Development and validation of oxygen radical absorbance capacity assay for lipophilic antioxidants using randomly methylated β-cyclodextrin as the solubility enhancer. J.Agri.Food.Chem; 2002;50:1815-21.
12-  Huang, L; Jiang, W; Zhu, L; Ma, C; Ou, Z. and Luo, C; γ-Oryzanol suppresses cell apoptosis by inhibiting reactive oxygen species-mediated mitochondrial signaling pathway in H2O2-stimulated L02 cells. Biomed.Pharmaco; 2020;121:109554.
13-  Ismail, N; Ismail, M; Imam, M.U; Azmi, N.H; Fathy, S.F. and Foo, J.B; Mechanistic basis for protection of differentiated SH-SY5Y cells by oryzanol-rich fraction against hydrogen peroxide-induced neurotoxicity. Complem.Altern.Medi; 2014;14:1-11.
14-  Juliano, C; Cossu, M; Alamanni, M.C. and Piu, L; Antioxidant activity of gamma-oryzanol: mechanism of action and its effect on oxidative stability of pharmaceutical oils. Inter.J.Pharma; 2005;299:146-54.
15-  Krisher, R. and Bavister, B; Responses of oocytes and embryos to the culture environment. Theriogenology; 1998;49:103-14.
16-  Kozuka, C; Yabiku, K; Takayama, C; Matsushita, M; Shimabukuro, M. and Masuzaki, H; Natural food science based novel approach toward prevention and treatment of obesity and type 2 diabetes: Recent studies on brown rice and γ-oryzanol. bes.Res.Clin.Pract;2013;7:65-72.
17-  Kensler, T.W; Wakabayashi, N. and Biswal, S; Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol; 2007;47:89-116.
18-  Lopes, S; Jurisicova, A; Sun, J.G. and Casper, R.F; Reactive oxygen species: potential cause for DNA fragmentation in human spermatozoa. Hum.Reprod; 1998;13:896-900.
19-  Madan, M; Singla, S; Chauhan, M. and Manik, R; In vitro production and transfer of embryos in buffaloes. Theriogenology; 1994;41:139-143.
20-  Mishra, A; Reddy, I; Dhali, A. and Javvaji, P; l-Ergothioneine improves the developmental potential of in vitro sheep embryos without influencing OCTN1-mediated cross-membrane transcript expression. Zygote; 2018;26:149-61.
21-  Moon, S.H; Kim, D; Shimizu, N; Okada, T; Hitoe, S. and Shimoda, H; Ninety-day oral toxicity study of rice-derived γ-oryzanol in Sprague-Dawley rats. Toxicolo.Repor; 2017;4:9-18.
22-  Noda, Y; Matsumoto, H; Umaoka, Y; Tatsumi, K; Kishi, J. and Mori, T; Involvement of superoxide radicals in the mouse two‐cell block. Molecul. Reprod. Develop; 1991;28:356-60.
23-  Pérez-Marín, C.C; Requena, F.D; Arando, A; Ortiz-Villalón, S; Requena, F. and Agüera, E.I; Effect of trehalose- and sucrose-based extenders on equine sperm quality after vitrification. Cryobiol; 2018;80:62-9.
24-  Rodrigues-Cunha, M.C; Mesquita, L.G; Bressan, F; Del-Collado, M; Balieiro, J.C. and Schwarz, K.R; Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development. Theriogenology; 2016; 86: 1685-1694.
25- Rungratanawanich, W; Abate, G; Serafini, M.M; Guarienti, M; Catanzaro, M. and Marziano, M; Characterization of the Antioxidant Effects of γ-Oryzanol: Involvement of the Nrf2 Pathway. Oxid.Med.Cell.Long; 2018:2987249.
26-  Rungratanawanich, W; Abate, G. and Uberti, D; Pharmacological profile of γ-oryzanol: Its antioxidant mechanisms and its effects in age-related diseases; P.V.R. and P.V.B, 2ndEd. Academic Press, 2020; pp:201-208.
27-  Sá, N.A; Vieira, L.A; Ferreira, A.C.A; Cadenas, J; Bruno, J.B. and Maside, C; Anethole supplementation during oocyte maturation improves in vitro production of bovine embryos. Reprod.Sci; 2020; 27:1602-8.
28-  Tian, X; Wang, F; He, C; Zhang, L; Tan, D. and Reiter, R.J; Beneficial effects of melatonin on bovine oocytes maturation: a mechanistic approach. J.Pin.Res; 2014; 57:239-47.
29-  Ullah, O; Li, Z; Ali, I; Xu, L; Liu, H. and Shah, S.Z.A; Pterostilbene alleviates hydrogen peroxide-induced oxidative stress via nuclear factor erythroid 2 like 2 pathway in mouse preimplantation embryos. J.Reprod.Dev; 2019;65:73-81.
30-  Wang, X; Falcone, T; Attaran, M; Goldberg, J.M; Agarwal, A. and Sharma, R.K; Vitamin C and Vitamin E supplementation reduce oxidative stress–induced embryo toxicity and improve the blastocyst development rate. Fertil.steril; 2002;78:1272-7.
31-  Wang, F; Tian, X; Zhang, L; He, C; Ji, P. and Li, Y; Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Fertil.Steril; 2014;101:577-86.
32-  Wilson, T.A; Nicolosi, R.J; Woolfrey, B. and Kritchevsky, D; Rice bran oil and oryzanol reduce plasma lipid and lipoprotein cholesterol concentrations and aortic cholesterol ester accumulation to a greater extent than ferulic acid in hypercholesterolemic hamsters. J. Nutr. Biochem; 2007; 18:105-12.
33-  Xu, Z. and Godber, J.S; Antioxidant activities of major components of γ‐oryzanol from rice bran using a linoleic acid model. J.Amer.O.Chem.Soc; 2001; 78(6):645
34- Xu, Z; Hua, N. and Godber, J.S; Antioxidant activity of tocopherols, tocotrienols, and γ-oryzanol components from rice bran against cholesterol oxidation accelerated by 2, 2 ‘-azobis (2-methylpropionamidine) dihydrochloride. J.Agri.Food.Chem; 2001;49: 2077-2081.
35- Yasukawa, K; Akihisa, T; Kimura, Y; Tamura, T. and Takido, M; Inhibitory effect of cycloartenol ferulate, a component of rice bran, on tumor promotion in two-stage carcinogenesis in mouse skin. Biolo.Pharmaceut.Bullet; 1998;21:1072-1076.
Iranian Journal of Veterinary Clinical Sciences
Volume 17, Issue 1 - Serial Number 28
Spring & Summer 2023
September 2023
Pages 103-111