Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-23T07:36:23.640Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of cyanocobalamin on oocyte maturation, in vitro fertilization, and embryo development in mice

Published online by Cambridge University Press:  17 December 2020

Tamana Rostami ,
Fardin Fathi ,
Vahideh Assadollahi ,
Javad Hosseini ,
Mohamad Bagher Khadem Erfan ,
Asrin Rashidi ,
Golzar Amiri ,
Omid Banafshi  and
Masoud Alasvand Open the ORCID record for Masoud Alasvand [Opens in a new window]
Tamana Rostami
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Fardin Fathi
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Vahideh Assadollahi
Affiliation:
Cancer and Immunology Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Javad Hosseini
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Mohamad Bagher Khadem Erfan
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Asrin Rashidi
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Golzar Amiri
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Omid Banafshi
Affiliation:
Cellular and Molecular Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
Masoud Alasvand*
Affiliation:
Cancer and Immunology Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran
*
Author for correspondence: Masoud Alasvand. Kurdistan University of Medical Sciences, Pasdaran St, Sanandaj 6617713446, Iran. Tel: +98 8733235445. Fax: +98 8733233600. E-mail: alasvand1100@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

The aim of this study was to investigate the effect of cyanocobalamin supplementation on in vitro maturation (IVM), in vitro fertilization (IVF), and subsequent embryonic development competence to the blastocyst stage, and in vitro development of mouse 2-cell embryos. Cumulus cells were prepared from mouse cumulus–oocyte complexes (COCs) and incubated for 24 h in an in vitro culture (IVC) medium that contained different concentrations of cyanocobalamin (100, 200, 300 or 500 pM). We collected 2-cell embryos from superovulated NMRI mice and cultured them in the same concentrations of cyanocobalamin (100, 200, 300 or 500 pM). After 42 h of IVM, we observed significantly increased oocyte maturation in the 200 pM cyanocobalamin-treated group compared with the control group (P < 0.0001). Mature oocytes cultured in 200 pM cyanocobalamin were fertilized and cultured in IVC medium with cyanocobalamin (100, 200, 300 or 500 pM) during early embryogenesis. The matured oocytes that were cultured in 200 pM cyanocobalamin had significantly higher 2-cell development rates compared with the control oocytes (P < 0.01). Embryos obtained from in vitro mature oocytes and in vivo fertilized oocytes that were cultured in 200 pM cyanocobalamin had significantly greater frequencies of development to the blastocyst stage and a significant reduction in 2-cell blocked and degenerated embryos compared with the control embryos (P < 0.0001). Embryos derived from oocytes fertilized in vivo with 200 pM cyanocobalamin had a higher percentage of blastocyst embryos compared with those derived from matured oocytes cultured in vitro (P < 0.0001). These finding demonstrated that the effects of cyanocobalamin on oocyte maturation, fertilization, and embryo development in mice depend on the concentration used in IVC medium.

Keywords

CyanocobalaminEmbryo developmentIn vitro cultureIn vitro fertilizationIn vitro maturationMouse
Type
Research Article
Information
Zygote , Volume 29 , Issue 2 , April 2021 , pp. 161 - 168
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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

Agarwal, A and Gupta, S (2005). Role of reactive oxygen species in female reproduction. Part I. Oxidative stress: a general overview. Agro Food Ind Hi-Tech 16, 21–5.Google Scholar
Agarwal, A, Saleh, RA and Bedaiwy, MA (2003). Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79, 829–43.CrossRefGoogle ScholarPubMed
Agarwal, A, Gupta, S and Sikka, S (2006a). The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol 18, 325–32.CrossRefGoogle ScholarPubMed
Agarwal, A, Said, TM, Bedaiwy, MA, Banerjee, J and Álvarez, JG (2006b). Oxidative stress in an assisted reproductive techniques setting. Fertil Steril 86, 503–12.CrossRefGoogle Scholar
Askoxylaki, M, Siristatidis, C, Chrelias, C, Vogiatzi, P, Creatsa, M, Salamalekis, G, Vrantza, T, Vrachnis, N and Kassanos, D (2013). Reactive oxygen species in the follicular fluid of subfertile women undergoing in vitro fertilization: a short narrative review. J Endocrinol Invest 36, 1117–20.Google ScholarPubMed
Assadollahi, V, Mohammadi, E, Fathi, F, Hassanzadeh, K, Erfan, MBK, Soleimani, F, Banafshi, O, Yousefi, F and Allahvaisi, O (2019). Effects of cigarette smoke condensate on proliferation and pluripotency gene expression in mouse embryonic stem cells. J Cell Biochem 120, 4071–80.CrossRefGoogle ScholarPubMed
Attaran, M, Pasqualotto, E, Falcone, T, Goldberg, JM, Miller, KF, Agarwal, A and Sharma, RK (2000). The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int J Fertil Womens Med 45, 314–320.Google ScholarPubMed
Betts, D and Madan, P (2008). Permanent embryo arrest: molecular and cellular concepts. Mol Human Reprod 14, 445–53.CrossRefGoogle ScholarPubMed
Biggers, JD (2004). Reflections on the culture of the preimplantation embryo. Int J Dev Biol 42, 879–84.Google Scholar
Burton, GJ, Hempstock, J and Jauniaux, E (2003). Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed Online 6, 84–96.CrossRefGoogle ScholarPubMed
Cagnone, G and Sirard, M-A (2016). The embryonic stress response to in vitro culture: insight from genomic analysis. Reproduction 152, R247–61.CrossRefGoogle ScholarPubMed
Crespo, I, García-Mediavilla, MV, Almar, M, González, P, Tuñón, MJ, Sánchez-Campos, S and González-Gallego, J (2008). Differential effects of dietary flavonoids on reactive oxygen and nitrogen species generation and changes in antioxidant enzyme expression induced by proinflammatory cytokines in Chang liver cells. Food Chem Toxicol 46, 1555–69.CrossRefGoogle ScholarPubMed
Farin, P, Crosier, A and Farin, C (2001). Influence of in vitro systems on embryo survival and fetal development in cattle. Theriogenology 55, 151–70.CrossRefGoogle ScholarPubMed
Gardiner, CS and Reed, DJ (1994). Status of glutathione during oxidant-induced oxidative stress in the preimplantation mouse embryo. Biol Reprod 51, 1307–14.CrossRefGoogle ScholarPubMed
Gaskins, AJ, Chiu, Y-H, Williams, PL, Ford, JB, Toth, TL, Hauser, R, Chavarro JE and the Earth Study Team (2015). Association between serum folate and vitamin B-12 and outcomes of assisted reproductive technologies. Am J Clin Nutr 102, 943–50.CrossRefGoogle ScholarPubMed
Green, R, Allen, LH, Bjørke-Monsen, AL, Brito, A, Guéant, JL, Miller, JW, Molloy, AM, Nexo, E, Stabler, S, Toh, BH, Ueland, PM and Yajnik, C (2017). Vitamin B12 deficiency. Nat Reviews Dis Primers 3, 1–20.Google ScholarPubMed
Gupta, S, Banerjee, J and Agarwal, A (2006). The impact of reactive oxygen species on early human embryos: A systematic review of the literature. Embryo Talk 1, 87–98.Google Scholar
Hamedani, M, Tahmasbi, AM and Ahangari, Y (2013). Effects of vitamin B 12 supplementation on the quality of ovine spermatozoa. Open Vet J 3, 140–4.Google Scholar
Hannibal, L, Lysne, V, Bjørke-Monsen, AL, Behringer, S, Grünert, SC, Spiekerkoetter, U, Jacobsen, DW, and Blom, HJ (2016). Biomarkers and algorithms for the diagnosis of vitamin B12 deficiency. Front Mol Biosci 3, 27.CrossRefGoogle ScholarPubMed
Hayes, D (2007). Nutritional hormesis. Eur J Clin Nutr 61, 147–59.CrossRefGoogle ScholarPubMed
Kendig, EL, Le, HH and Belcher, SM (2010). Defining hormesis: evaluation of a complex concentration response phenomenon. Int J Toxicol 29, 235–246.CrossRefGoogle ScholarPubMed
Kimura, N, Tsunoda, S, Iuchi, Y, Abe, H, Totsukawa, K and Fujii, J (2010). Intrinsic oxidative stress causes either 2-cell arrest or cell death depending on developmental stage of the embryos from SOD1-deficient mice. Mol Human Reprod 16, 441–51.CrossRefGoogle ScholarPubMed
Kwong, WY, Adamiak, S, Gwynn, A, Singh, R and Sinclair, KD (2010). Endogenous folates and single-carbon metabolism in the ovarian follicle, oocyte and pre-implantation embryo. Reproduction 139, 705.CrossRefGoogle ScholarPubMed
Lan, K-C, Lin, Y-C, Chang, Y-C, Lin, H-J, Tsai, Y-R and Kang, H-Y (2019). Limited relationships between reactive oxygen species levels in culture media and zygote and embryo development. J Assist Reprod Genet 36, 325–34.CrossRefGoogle ScholarPubMed
Lopes, A, Lane, M and Thompson, J (2010). Oxygen consumption and ROS production are increased at the time of fertilization and cell cleavage in bovine zygotes. Hum Reprod 25, 2762–73.CrossRefGoogle ScholarPubMed
Luberda, Z (2005). The role of glutathione in mammalian gametes. Reprod Biol 5, 5–17.Google ScholarPubMed
Martín-Romero, FJ, Miguel-Lasobras, EM, Domínguez-Arroyo, JA, González-Carrera, E and Álvarez, IS (2008). Contribution of culture media to oxidative stress and its effect on human oocytes. Reprod Biomed Online 17, 652–61.CrossRefGoogle ScholarPubMed
Mello, A, Hyde, A, Elsea, L and Whitaker, B (2018). The effects of cyanocobalamin supplementation during the thawing of frozen boar semen on spermatozoa, in vitro fertilization, and embryonic development. Anim Reprod 10, 119–23.Google Scholar
Nakamura, BN, Fielder, TJ, Hoang, YD, Lim, J, McConnachie, LA, Kavanagh, TJ and Luderer, U (2011). Lack of maternal glutamate cysteine ligase modifier subunit (Gclm) decreases oocyte glutathione concentrations and disrupts preimplantation development in mice. Endocrinology 152, 2806–15.CrossRefGoogle ScholarPubMed
Nasr-Esfahani, MH, Aitken, JR and Johnson, MH (1990). Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo . Development 109, 501–7.Google ScholarPubMed
Noda, Y, Matsumoto, H, Umaoka, Y, Tatsumi, K, Kishi, J and Mori, T (1991). Involvement of superoxide radicals in the mouse two-cell block. Mol Reprod Dev 28, 356–60.CrossRefGoogle ScholarPubMed
Pereira, DC, Dode, MAN and Rumpf, R (2005). Evaluation of different culture systems on the in vitro production of bovine embryos. Theriogenology 63, 1131–41.CrossRefGoogle ScholarPubMed
Reese Pepper, M and Black, MM (2011). B12 in fetal development. Semin Cell Dev Biol 22, 619–23.CrossRefGoogle Scholar
Riley, JC and Behrman, HR (1991). Oxygen radicals and reactive oxygen species in reproduction. Proc Soc Exp Biol Med 198, 781–91.CrossRefGoogle ScholarPubMed
Rizos, D, Ward, F, Duffy, P, Boland, MP and Lonergan, P (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev 61, 234–48.CrossRefGoogle ScholarPubMed
Rizzo, P, Raffone, E and Benedetto, V (2010). Effect of the treatment with myo-inositol plus folic acid plus melatonin in comparison with a treatment with myo-inositol plus folic acid on oocyte quality and pregnancy outcome in IVF cycles. A prospective, clinical trial. Eur Rev Med Pharmacol Sci 14, 555–61.Google ScholarPubMed
Roy, PK, Fang, X, Hassan, BM, Shin, ST and Cho, JK (2017). Cobalamin supplementation during in vitro maturation improves developmental competence of porcine oocytes. 17th International Symposium on Developmental Biotechnology pp. 94–94. www.earticle.net/Article/A347362 Google Scholar
Sameni, HR, Javadinia, SS, Safari, M, Amjad, MHT, Khanmohammadi, N, Parsaie, H and Zarbakhsh, S (2018). Effect of quercetin on the number of blastomeres, zona pellucida thickness, and hatching rate of mouse embryos exposed to actinomycin D: an experimental study. Int J Reprod BioMed 16, 101.Google ScholarPubMed
Sellens, M, Stein, S and Sherman, M (1981). Protein and free amino acid content in preimplantation mouse embryos and in blastocysts under various culture conditions. Reproduction 61, 307–15.CrossRefGoogle ScholarPubMed
Shih, Y-F, Lee, T-H, Liu, C-H, Tsao, H-M, Huang, C-C and Lee, M-S (2014). Effects of reactive oxygen species levels in prepared culture media on embryo development: a comparison of two media. Taiwan J Obstet Gynecol 53, 504–8.CrossRefGoogle ScholarPubMed
Sinbad, OO, Folorunsho, AA, Olabisi, OL, Ayoola, OA and Temitope, EJ (2019). Vitamins as antioxidants. J Food Sci 2, 214–35.Google Scholar
Sinclair, KD, Allegrucci, C, Singh, R, Gardner, DS, Sebastian, S, Bispham, J, Thurston, A, Huntley, JF, Rees, WD and Maloney, CA (2007). DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA 104, 19351–6.CrossRefGoogle ScholarPubMed
Sugino, N (2005). Reactive oxygen species in ovarian physiology. Reprod Med Biol 4, 31–44.Google ScholarPubMed
Sugino, N (2006). Roles of reactive oxygen species in the corpus luteum. Anim Sci J 77, 556–65.CrossRefGoogle Scholar
Summers, MC and Biggers, JD (2003). Chemically defined media and the culture of mammalian preimplantation embryos: historical perspective and current issues. Hum Reprod Update 9, 557–82.CrossRefGoogle ScholarPubMed
Thiyagarajan, B and Valivittan, K (2009). Ameliorating effect of vitamin E on in vitro development of preimplantation buffalo embryos. J Assist Reprod Genet 26, 217–25.CrossRefGoogle ScholarPubMed
Tsunoda, S, Kimura, N and Fujii, J (2014). Oxidative stress and redox regulation of gametogenesis, fertilization, and embryonic development. Reprod Med Biol 13, 71–9.CrossRefGoogle ScholarPubMed
Van De Lagemaat, EE, De Groot, LC and Van Den Heuvel, EG (2019). Vitamin B12 in relation to oxidative stress: a systematic review. Nutrients 11, 482.CrossRefGoogle ScholarPubMed
Wiener-Megnazi, Z, Vardi, L, Lissak, A, Shnizer, S, Reznick, AZ, Ishai, D, Lahav-Baratz, S, Shiloh, H, Koifman, M and Dirnfeld, M (2004). Oxidative stress indices in follicular fluid as measured by the thermochemiluminescence assay correlate with outcome parameters in in vitro fertilization. Fertil Steril 82, 1171–6.CrossRefGoogle ScholarPubMed
Ye, R Xu, S Liu, Y Pang, L Lian, X Zhong, Y Su, Y and Wang, S (2017). Protective effect of icariin on the development of preimplantation mouse embryos against hydrogen peroxide-induced oxidative injury. Oxid Med Cell Longev 2017:2704532. doi: 10.1155/2017/2704532 CrossRefGoogle ScholarPubMed
Zacchini, F, Toschi, P and Ptak, GE (2017). Cobalamin supplementation during in vitro maturation improves developmental competence of sheep oocytes. Theriogenology 93, 55–61.CrossRefGoogle ScholarPubMed
Zuelke, KA, Jeffay, SC, Zucker, RM and Perreault, SD (2003). Glutathione (GSH) concentrations vary with the cell cycle in maturing hamster oocytes, zygotes, and pre-implantation stage embryos. Mol Reprod Dev 64, 106–12.CrossRefGoogle ScholarPubMed