Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T01:31:08.780Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  05 October 2018

Ahmed M. Elomda ,
Mohamed F. Saad ,
Ayman M. Saeed ,
Ashraf Elsayed ,
Ahmed O. Abass ,
Hosam M. Safaa  and
Gamal M. K. Mehaisen Open the ORCID record for Gamal M. K. Mehaisen [Opens in a new window]
Ahmed M. Elomda
Affiliation:
Department of Animal Biotechnology, Animal Production Research Institute, Dokki, Giza, Egypt
Mohamed F. Saad
Affiliation:
Department of Animal Biotechnology, Animal Production Research Institute, Dokki, Giza, Egypt
Ayman M. Saeed
Affiliation:
Department of Animal Biotechnology, Animal Production Research Institute, Dokki, Giza, Egypt
Ashraf Elsayed
Affiliation:
Department of Animal Production, Faculty of Agriculture, Cairo University, Giza, Egypt
Ahmed O. Abass
Affiliation:
Department of Animal Production, Faculty of Agriculture, Cairo University, Giza, Egypt
Hosam M. Safaa
Affiliation:
Department of Animal Production, Faculty of Agriculture, Cairo University, Giza, Egypt Bisha University, Bisha, Saudi Arabia
Gamal M. K. Mehaisen*
Affiliation:
Department of Animal Production, Faculty of Agriculture, Cairo University, Giza, Egypt
*
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: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Antioxidant biomarkersGene expressionIn vitro developmentRabbit embryoRetinol
Type
Research Article
Information
Zygote , Volume 26 , Issue 4 , August 2018 , pp. 326 - 332
Copyright
© Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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, 68–71.Google Scholar
Aebi, H (1984) [13] Catalase in vitro . Methods Enzymol 105, 121–126.Google Scholar
Agarwal, A, Saleh, RA Bedaiwy, MA (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79, 829–843.Google Scholar
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, 1375–1404.Google Scholar
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, 365–373.Google Scholar
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, 483–489.Google Scholar
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, e68–e72.Google Scholar
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, 116–124.Google Scholar
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, 234–242.Google Scholar
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, 808–813.Google Scholar
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, 1355–1367.Google Scholar
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, 2706–2714.Google Scholar
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.Google Scholar
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, 607–614.Google Scholar
Gornall, AG, Bardawill, CJ David, MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177, 751–766.Google Scholar
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, 175–189.Google Scholar
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, 1403–1412.Google Scholar
Ikeda, S, Kitagawa, M, Imai, H Yamada, M (2005) The roles of vitamin A for cytoplasmic maturation of bovine oocytes. J Reprod Dev 51, 23–35.Google Scholar
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, 342–350.Google Scholar
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, 735–742.Google Scholar
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, 849–856.Google Scholar
Kei, S (1978) Serum lipid peroxide in cerebrovascular disorders determined by a new colorimetric method. Clin Chim Acta 90, 37–43.Google Scholar
Khalil, M (2002) The Baladi Rabbits (Egypt) Options Méditerranéennes Série B: Etudes et Recherches (CIHEAM).Google Scholar
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, 193–202.Google Scholar
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, 1698–1705.Google Scholar
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, 356–361.Google Scholar
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, 55–64.Google Scholar
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.Google Scholar
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, 356–360.Google Scholar
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, 184–192.Google Scholar
Livak, KJ Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.Google Scholar
Livingston, T, Eberhardt, D, Edwards, JL Godkin, J (2004) Retinol improves bovine embryonic development in vitro . Reprod Biol Endocrinol 2, 83.Google Scholar
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 Google Scholar
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, 314–323.Google Scholar
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.Google Scholar
Mehaisen, GMK Saeed, AM (2015) In vitro development rate of preimplantation rabbit embryos cultured with different levels of melatonin. Zygote 23, 111–115.Google Scholar
Nishikimi, M, Roa, N Yogi, K (1972) Determination of superoxide dismutase in tissue homogenate. Biochem Bioph Res Commun 46, 849–854.Google Scholar
Noy, N (2010) Between death and survival: retinoic acid in regulation of apoptosis. Annu Revi Nutr 30, 201–217.Google Scholar
Ovitt, C Schöler, H (1998) The molecular biology of Oct-4 in the early mouse embryo. Mol Hum Reprod 4, 1021–1031.Google Scholar
Paglia, DE Valentine, WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70, 158–169.Google Scholar
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, 116–122.Google Scholar
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, 973–976.Google Scholar
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, 105–113.Google Scholar
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, 592–607.Google Scholar
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, 833–839.Google Scholar
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, 1884–1890.Google Scholar
Rhinn, M Dollé, P (2012) Retinoic acid signalling during development. Development 139, 843–858.Google Scholar
SAS (2004) STAT User Guide Version 912 SAS Institute Inc., Cary NC, USA.Google Scholar
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. 65–87.Google Scholar
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, 1058–1066.Google Scholar
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, 720–726.Google Scholar
Vahedi, V, Zeinoaldini, S, Kohram, H Farahavar, A (2009) Retinoic acid effects on nuclear maturation of bovine oocytes in vitro . African J Biotechnol 8, 3974–3978.Google Scholar
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 Google Scholar
Yan, H Harding, JJ (1997) Glycation-induced inactivation and loss of antigenicity of catalase and superoxide dismutase. Biochem J 328, 599.Google Scholar
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, 337–349.Google Scholar
Zidane, M (2017) Epigenetic and Exosome-mediated Cell–Cell Communication in Follicular Cells and Preimplantation Embryos. Universitäts- und Landesbibliothek Bonn.Google Scholar