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Antioxidant and developmental capacity of retinol on the in vitro culture of rabbit embryos

  • Ahmed M. Elomda (a1), Mohamed F. Saad (a1), Ayman M. Saeed (a1), Ashraf Elsayed (a2), Ahmed O. Abass (a2), Hosam M. Safaa (a2) (a3) and Gamal M. K. Mehaisen (a2)...

Summary

Oxidative stress is a major cause of defective embryo development during in vitro culture. Retinoids are recognized as non-enzymatic antioxidants and may have an important role in the regulation of cell differentiation and vertebrate development. However, there are not enough reports discussing the antioxidant and developmental capacity of retinoids, including retinol (RT), on the in vitro development of embryos recovered from livestock animals, particularly in rabbit species. Therefore, morula embryos obtained from nulliparous Red Baladi rabbit does were cultured for 48 h in TCM199 medium in the absence of RT (control group) or in the presence of RT at concentrations of 10, 100 and 1000 nM. The developmental capacity to the hatched blastocyst stage, the antioxidant biomarker assay and the expression of several selected genes were analyzed in each RT group. The data show that RT significantly (P<0.001) promoted the embryo hatchability rate at the concentration of 1000 nM to 69.44% versus 29.71% for the control. The activity of malondialdehyde (MDA) level was significantly (P<0.05) lower in the RT groups than in the control group, while the total antioxidant capacity (TAC), superoxide dismutase (SOD) and glutathione peroxidase (GPx) activities were significantly (P<0.05) higher following treatment with RT. Furthermore, RT treatment considerably upregulated the relative expression of gap junction protein alpha 1 (GJA1), POU class 5 homeobox 1 (POU5F1) and superoxide dismutase 1 (SOD1) genes compared with the control group. The current study highlights the potential effects of RT as antioxidant in the culture medium on the in vitro development of rabbit embryos.

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Corresponding author

Author for correspondence: Gamal M.K. Mehaisen. Department of Animal Production, Faculty of Agriculture, Cairo University, 7 Gamaa Street, 12613 Giza, Egypt. Tel: +201226797270. Fax: +20235717355. E-mail: gamoka@cu.edu.eg

References

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Abouzaripour, M, Fathi, F, Daneshi, E, Mortezaee, K, Rezaie, MJ Abdi, M (2018) Combined effect of retinoic acid and basic fibroblast growth factor on maturation of mouse oocyte and subsequent fertilization and development. Int J Fertil Steril 12, 6871.
Aebi, H (1984) [13] Catalase in vitro . Methods Enzymol 105, 121126.
Agarwal, A, Saleh, RA Bedaiwy, MA (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79, 829843.
Agarwal, A, Gupta, S, Sekhon, L Shah, R (2008) Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications. Antioxid Redox Signal 10, 13751404.
Ahmed, JA, Dutta, D Nashiruddullah, N (2016) Comparative efficacy of antioxidant retinol melatonin and zinc during in vitro maturation of bovine oocytes under induced heat stress. Turk J Vet Anim Sci 40, 365373.
Alminana, C, Gil, M, Cuello, C, Caballero, I, Roca, J, Vazquez, J, Gomez, E Martinez, E (2008) In vitro maturation of porcine oocytes with retinoids improves embryonic development. Reprod Fertil Dev 20, 483489.
Chiamenti, A, Aguiar Filho, C, Freitas Neto, L, Chaves, R, Paula‐Lopes, F, Lima, P, Goncalves, P Oliveira, M (2010) Effects of retinoids on the in vitro development of Capra hircus embryos to blastocysts in two different culture systems. Reprod Domest Anim 45, e68e72.
Chiamenti, A, Filho, C, Moura, M, Paula-Lopes, F, Neves, J, Neto, C, Gonçalves, P, Lima, P Oliveira, M (2012) Use of retinyl acetate retinoic acid and insulin-like growth factor-I (IGF-I) to enhance goat embryo production. Acta Vet Hung 61, 116124.
Conceição, JC, Moura, MT, Ferreira-Silva, JC, Ramos-Deus, P, Silva, PG, Cantanhêde, LF, Chaves, RM, Lima, PF Oliveira, MA (2015) Use of retinoids during oocyte maturation diminishes apoptosis in caprine embryos. Acta Vet Hung 63, 234242.
Conceição, JC, Moura, MT, Ferreira-Silva, JC, Cantanhêde, LF, Chaves, RM, Lima, PF Oliveira, MA (2016) Incidence of apoptosis after retinoids and insulin-like growth factor-I (IGF-I) supplementation during goat in vitro embryo production. Zygote 24, 808813.
De Sousa, PA, Valdimarsson, G, Nicholson, BJ Kidder, GM (1993) Connexin trafficking and the control of gap junction assembly in mouse preimplantation embryos. Development 117, 13551367.
Duque, P, Diez, C, Royo, L, Lorenzo, P, Carneiro, G, Hidalgo, C, Facal, N Gomez, E (2002a) Enhancement of developmental capacity of meiotically inhibited bovine oocytes by retinoic acid. Hum Reprod 17, 27062714.
Duque, P, Gómez, E, Hidalgo, C, Facal, N, Fernández, I Diez, C (2002b) Retinoic acid during in vitro maturation of bovine oocytes promotes embryonic development and early differentiation. Theriogenology 57, 364.
Gomez, E, Caamano, JN, Bermejo-Alvarez, P, Diez, C, Munoz, M, Martin, D, Carrocera, S Gutierrez-Adan, A (2009) Gene expression in early expanded parthenogenetic and in vitro fertilized bovine blastocysts. J Reprod Dev 55, 607614.
Gornall, AG, Bardawill, CJ David, MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177, 751766.
Guerin, P, El Mouatassim, S Menezo, Y (2001) Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 7, 175189.
Houghton, F, Barr, K, Walter, G, Gabriel, H-D, Grummer, R, Traub, O, Leese, H, Winterhager, E Kidder, G (2002) Functional significance of gap junctional coupling in preimplantation development. Biol Reprod 66, 14031412.
Ikeda, S, Kitagawa, M, Imai, H Yamada, M (2005) The roles of vitamin A for cytoplasmic maturation of bovine oocytes. J Reprod Dev 51, 2335.
Kawasumi, M, Unno, Y, Matsuoka, T, Nishiwaki, M, Anzai, M, Amano, T, Mitani, T, Kato, H, Saeki, K Hosoi, Y (2009) Abnormal DNA methylation of the Oct‐4 enhancer region in cloned mouse embryos. Mol Reprod Dev 76, 342350.
Kazemi, P, Dashtizad, M, Shamsara, M, Mahdavinezhad, F, Hashemi, E, Fayazi, S Hajarian, H (2016) Effect of blastocoel fluid reduction before vitrification on gene expression in mouse blastocysts. Mol Reprod Dev 83, 735742.
Keefer, C, Baldassarre, H, Keyston, R, Wang, B, Bhatia, B, Bilodeau, A, Zhou, J, Leduc, M, Downey, B Lazaris, A (2001) Generation of dwarf goat (Capra hircus) clones following nuclear transfer with transfected and nontransfected fetal fibroblasts and in vitro-matured oocytes. Biol Reprod 64, 849856.
Kei, S (1978) Serum lipid peroxide in cerebrovascular disorders determined by a new colorimetric method. Clin Chim Acta 90, 3743.
Khalil, M (2002) The Baladi Rabbits (Egypt) Options Méditerranéennes Série B: Etudes et Recherches (CIHEAM).
Kim, Y-S, Kim, E-Y, Moon, J, Yoon, T-K, Lee, W-S Lee, K-A (2011) Expression of interferon regulatory factor-1 in the mouse cumulus–oocyte complex is negatively related with oocyte maturation. Clin Exp Reprod Med 38, 193202.
Kirchhof, N, Carnwath, J, Lemme, E, Anastassiadis, K, Scholer, H Niemann, H (2000) Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 63, 16981705.
Koracevic, D, Koracevic, G, Djordjevic, V, Andrejevic, S Cosic, V (2001) Method for the measurement of antioxidant activity in human fluids. J Clin Pathol 54, 356361.
Lasota, B, Ogonski, T, Blaszczyk, P, Seremak, B, Ligocki, M, Telesinski, A Kopczynski, P (2011) Activity of antioxidant enzymes and concentration of Mn, Cu, Zn, and protein in porcine follicular fluid. Acta Sci Pol Zootech 10, 5564.
Lavara, R, Lavara, F, Vicente, J Mocé, E (2000) Use of different diluents with a low number of spermatozoa by insemination dose in rabbit. In Proceedings of the 7th World Rabbit Congress, Valencia, pp. 173–7.
Lima, P, Oliveira, M, Goncalves, P, Montagner, M, Reichenbach, HD, Weppert, M, Neto, CC, Pina, V Santos, M (2004) Effects of retinol on the in vitro development of Bos indicus embryos to blastocysts in two different culture systems. Reprod Domest Anim 39, 356360.
Lima, P, Oliveira, M, Santos, M, Reichenbach, H-D, Weppert, M, Paula-Lopes, F, Neto, CC Gonçalves, P (2006) Effect of retinoids and growth factor on in vitro bovine embryos produced under chemically defined conditions. Anim Reprod Sci 95, 184192.
Livak, KJ Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.
Livingston, T, Eberhardt, D, Edwards, JL Godkin, J (2004) Retinol improves bovine embryonic development in vitro . Reprod Biol Endocrinol 2, 83.
Livingston, TE (2003) The Effects of Retinol During In Vivo and In Vitro Oocyte Maturation and Embryonic Development. PhD diss., University of Tennessee, 2003. http://trace.tennessee.edu/utk_graddiss/2109
Maity, P, Bindu, S, Dey, S, Goyal, M, Alam, A, Pal, C, Reiter, R Bandyopadhyay, U (2009) Melatonin reduces indomethacin‐induced gastric mucosal cell apoptosis by preventing mitochondrial oxidative stress and the activation of mitochondrial pathway of apoptosis. J Pineal Res 46, 314323.
Mehaisen, GM, Saeed, AM, Gad, A, Abass, AO, Arafa, M 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.
Mehaisen, GMK Saeed, AM (2015) In vitro development rate of preimplantation rabbit embryos cultured with different levels of melatonin. Zygote 23, 111115.
Nishikimi, M, Roa, N Yogi, K (1972) Determination of superoxide dismutase in tissue homogenate. Biochem Bioph Res Commun 46, 849854.
Noy, N (2010) Between death and survival: retinoic acid in regulation of apoptosis. Annu Revi Nutr 30, 201217.
Ovitt, C Schöler, H (1998) The molecular biology of Oct-4 in the early mouse embryo. Mol Hum Reprod 4, 10211031.
Paglia, DE Valentine, WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70, 158169.
Panda, BS, Pandey, S, Somal, A, Parmar, MS, Bhat, IA, Baiju, I, Bharti, MK, Kumar, GS, Chandra, V Sharma, GT (2017) Leptin supplementation in vitro improved developmental competence of buffalo oocytes and embryos. Theriogenology 98, 116122.
Pasqualotto, EB, Agarwal, A, Sharma, RK, Izzo, VM, Pinotti, JA, Joshi, NJ Rose, BI (2004) Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril 81, 973976.
Peippo, J, Kurkilahti, M Bredbacka, P (2001) Developmental kinetics of in vitro produced bovine embryos: the effect of sex glucose and exposure to time-lapse environment. Zygote 9, 105113.
Poprac, P, Jomova, K, Simunkova, M, Kollar, V, Rhodes, CJ Valko, M (2017) Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol Sci 38, 592607.
Pu, Y, Wang, Z, Bian, Y, Zhang, F, Yang, P, Li, Y, Zhang, Y, Liu, Y, Fang, F Cao, H (2014) All‐trans retinoic acid improves goat oocyte nuclear maturation and reduces apoptotic cumulus cells during in vitro maturation. Anim Sci J 85, 833839.
Rajesh, N, Shankar, M Deecaraman, M (2010) Effect of vitamin A supplementation at different gaseous environments on in vitro development of pre-implantation sheep embryos to the blastocyst stage. Animal 4, 18841890.
Rhinn, M Dollé, P (2012) Retinoic acid signalling during development. Development 139, 843858.
SAS (2004) STAT User Guide Version 912 SAS Institute Inc., Cary NC, USA.
Sharma, R, Roychoudhury, S, Alsaad, R Bamajbuor, F (2017) Negative effects of oxidative stress (OS) on reproductive system at cellular level. In Agarwal A et al., (eds) Oxidative Stress in Human Reproduction. Springer, pp. 6587.
Succu, S, Pasciu, V, Manca, ME, Chelucci, S, Torres-Rovira, L, Leoni, GG, Zinellu, A, Carru, C, Naitana, S Berlinguer, F (2014) Dose-dependent effect of melatonin on postwarming development of vitrified ovine embryos. Theriogenology 81, 10581066.
Suzuki, T, Sugino, N, Fukaya, T, Sugiyama, S, Uda, T, Takaya, R, Yajima, A Sasano, H (1999) Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization. Fertil Steril 72, 720726.
Vahedi, V, Zeinoaldini, S, Kohram, H Farahavar, A (2009) Retinoic acid effects on nuclear maturation of bovine oocytes in vitro . African J Biotechnol 8, 39743978.
Wang, F (2012) Low reactive oxygen species and high glycolysis in glioblastoma stem cells: mechanisms and therapeutic implications. UT GSBS Dissertations and Theses (Open Access). 279. http://digitalcommons.library.tmc.edu/utgsbs_dissertations/279
Yan, H Harding, JJ (1997) Glycation-induced inactivation and loss of antigenicity of catalase and superoxide dismutase. Biochem J 328, 599.
Zelko, IN, Mariani, TJ Folz, RJ (2002) Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1) Mn-SOD (SOD2) and EC-SOD (SOD3) gene structures evolution and expression. Free Radical Biol Med 33, 337349.
Zidane, M (2017) Epigenetic and Exosome-mediated Cell–Cell Communication in Follicular Cells and Preimplantation Embryos. Universitäts- und Landesbibliothek Bonn.

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