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Production of in vitro bovine embryos supplemented with l-carnitine in different oxygen tensions and the relation to nitric oxide

Published online by Cambridge University Press:  23 July 2020

Daniela Moraes Pereira ,
Christopher Junior Tavares Cardoso ,
Wilian Aparecido Leite da Silva ,
Mirela Brochado Souza-Cáceres ,
Mariana Santos Open the ORCID record for Mariana Santos [Opens in a new window] ,
Ralf Pöhland ,
Allan Motta Couto ,
Iluska Senna Bonfá Moslaves ,
Mônica Cristina Toffoli Kadri  and
Fabiana de Andrade Melo Sterza Open the ORCID record for Fabiana de Andrade Melo Sterza [Opens in a new window]
Daniela Moraes Pereira
Affiliation:
State University of Mato Grosso do Sul, Animal Science, Aquidauana, Mato Grosso do Sul, Brazil
Christopher Junior Tavares Cardoso
Affiliation:
Federal University of Mato Grosso do Sul, Veterinary Science, Campo Grande, Mato Grosso do Sul, Brazil
Wilian Aparecido Leite da Silva
Affiliation:
Federal University of Mato Grosso do Sul, Animal Science, Campo Grande, Mato Grosso do Sul, Brazil
Mirela Brochado Souza-Cáceres
Affiliation:
State University of Londrina, Animal Science, Londrina, Paraná, Brazil
Mariana Santos
Affiliation:
State University of Mato Grosso do Sul, Animal Science, Aquidauana, Mato Grosso do Sul, Brazil
Ralf Pöhland
Affiliation:
State University of Londrina, Animal Science, Londrina, Paraná, Brazil
Allan Motta Couto
Affiliation:
State University of Mato Grosso do Sul, Animal Science, Aquidauana, Mato Grosso do Sul, Brazil
Iluska Senna Bonfá Moslaves
Affiliation:
Federal University of Mato Grosso do Sul, Pharmacology and Inflammation Laboratory, Campo Grande, Mato Grosso do Sul, Brazil
Mônica Cristina Toffoli Kadri
Affiliation:
Federal University of Mato Grosso do Sul, Pharmacology and Inflammation Laboratory, Campo Grande, Mato Grosso do Sul, Brazil
Fabiana de Andrade Melo Sterza*
Affiliation:
State University of Mato Grosso do Sul, Animal Science, Aquidauana, Mato Grosso do Sul, Brazil Federal University of Mato Grosso do Sul, Veterinary Science, Campo Grande, Mato Grosso do Sul, Brazil Leibniz Institute for Farm Animal Biology, Institute of Reproductive Biology, Dummerstorf, Germany
*
Author for correspondence: Fabiana de Andrade Melo Sterza. Universidade Estadual de Mato Grosso do Sul – Aquidauana/MS. 25 Rodovia Graziela Maciel Barrozo, Km 12 Zona Rural, Aquidauana – MS, CEP: 79200-000, Brazil. Tel: +55 67 39042242. E-mail: [email protected]
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Summary

The aim of this study was to evaluate the production of bovine embryos in vitro when supplemented with l-carnitine for 24 h beginning on day 5 (d 5) under two different oxygen tensions (20% or 5%) and the relationship of nitric oxide (NO) in in vitro culture (IVC) medium to embryo development. Cumulus–oocyte complexes (COC; n = 837) were matured in vitro for 24 h and fertilization was performed for 18 h. Zygotes were cultured in vitro for 9 days after in vitro fertilization in synthetic oviductal fluid (SOF) medium with 5% fetal calf serum. At d 5 the plates were assigned to one of four treatment groups: high (20%) or low (5%) O2 tension either with or without the addition of 3.03 mM l-carnitine (High-Cont, High-Lcar, Low-Cont, Low-Lcar). The concentration of NO in the culture medium was evaluated on d 5, d 6 and d 9. On d 7, parts of the embryos were submitted for evaluation of intracellular lipid droplets. The cleavage rate was similar (P > 0.05) between high and low O2 tension and the blastocyst rate was similar in all conditions evaluated. The hatching rate was higher (P < 0.05) for Low-Cont. The NO concentration was higher at d 9 under low O2 tension (P < 0.1). The addition of 3.03 mM l-carnitine between d 5 and d 6 of IVC was not efficient in reducing cytoplasmic lipid content of bovine embryos. Additionally, IVC at a low oxygen tension without l-carnitine promoted better conditions for embryo development. A higher concentration of NO in medium was observed under low O2 tension.

Keywords

BovineEmbryo developmentNile RedReactive nitrogen species
Type
Research Article
Information
Zygote , Volume 28 , Issue 5 , October 2020 , pp. 403 - 408
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Abbas, K, Breton, J, Planson, AG, Bouton, C, Bignon, J, Seguin, C, Riquier, S, Toledano, MB and Drapier, JC (2011). Nitric oxide activates an nrf2/sulfiredoxin antioxidant pathway in macrophages. Free Radic Biol Med 51, 107–14.CrossRefGoogle ScholarPubMed
Abdelrazik, H, Sharma, R, Mahfouz, R and Agarwal, A (2009). l-Carnitine decreases DNA damage and improves the in vitro blastocyst development rate in mouse embryos. Fertil Steril 91, 589–96.CrossRefGoogle ScholarPubMed
Agarwal, A, Said, TM, Bedaiwy, MA, Banerjee, J and Alvarez, JG (2006). Oxidative stress in an assisted reproductive technique setting. Fertil Steril 86, 503–12.CrossRefGoogle Scholar
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, 314–20.Google ScholarPubMed
Bagheri, D, Kazemi, P, Sarmadi, F, Shamsara, M, Hashemi, E, Joupari, MD and Dashtizad, M (2018). Low oxygen tension promotes invasive ability and embryo implantation rate. Reprod Biol 18, 295–300.CrossRefGoogle ScholarPubMed
Bu, S, Xia, G, Tao, Y, Lei, L and Zhou, B (2003). Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol Cell Endocrinol 207, 21–30.CrossRefGoogle ScholarPubMed
Corrêa, GA, Rumpf, R, Mundim, TCD, Franco, MM and Dode, MAN (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim Reprod Sci 104, 132–42.CrossRefGoogle ScholarPubMed
Dias, LRO, Leme, LO, Sprícigo, JFW, Pivato, I, Dode, MAN (2020). Effect of delipidant agents during in vitro culture on the development, lipid content, gene expression and cryotolerance of bovine embryos. Reprod Domest Anim 55(1), 11–20.CrossRefGoogle ScholarPubMed
Ding, AH, Nathan, CF and Stuehr, D (1988). Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 141, 2407–12.Google ScholarPubMed
Dubey, PK, Tripathi, V, Singh, RP, Saikumar, G, Nath, A, Pratheesh, MD, Gade, N and Sharma, GT (2012). Expression of nitric oxide synthase isoforms in different stages of buffalo (Bubalus bubalis) ovarian follicles: effect of nitric oxide on in vitro development of preantral follicle. Theriogenology 77, 280–91.CrossRefGoogle ScholarPubMed
Finkel, T and Holbrook, NJ (2000). Oxidants, oxidative stress and the biology of ageing. Nature 408, 239–47.CrossRefGoogle ScholarPubMed
Ghanem, N, Ha, AN, Fakruzzaman, M, Bang, JI, Lee, SC and Kong, IK (2014). Differential expression of selected candidate genes in bovine embryos produced in vitro and cultured with chemicals modulating lipid metabolism. Theriogenology 82, 238–50.CrossRefGoogle ScholarPubMed
Guerin, P, El Mouatassim, S and Menezo, Y (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 7, 175–89.CrossRefGoogle ScholarPubMed
Held-Hoelker, E, Klein, SL, Rings, F, Salilew-Wondim, D, Saeed-Zidane, M, Neuhoff, C, Tesfaye, D, Schellander, K and Hoelker, M (2017). Cryosurvival of in vitro produced bovine embryos supplemented with l-carnitine and concurrent reduction of fatty acids. Theriogenology 96, 145–52.CrossRefGoogle ScholarPubMed
Inoue, M, Sato, EF, Park, AM, Nishikawa, M, Kasahara, E, Miyoshi, M, Ochi, A and Utsumi, K (2000). Cross-talk between NO and oxyradicals, a supersystem that regulates energy metabolism and survival of animals. Free Radic Res 33, 757–70.CrossRefGoogle ScholarPubMed
Inoue, M, Sato, EF, Nishikawa, M, Park, AM, Kira, Y, Imada, I and Utsumi, K (2003). Cross talk of nitric oxide, oxygen radicals, and superoxide dismutase regulates the energy metabolism and cell death and determines the fates of aerobic life. Antioxid Redox Sign 5, 475–84.CrossRefGoogle ScholarPubMed
Jablonka-Shariff, A and Olson, LM (1998). The role of nitric oxide in oocyte meiotic maturation and ovulation: Meiotic abnormalities of endothelial nitric oxide synthase knock-out mouse oocytes. Endocrinology 139, 2944–54.CrossRefGoogle ScholarPubMed
Jiang, W, Li, Y, Zhao, Y, Gao, Q, Jin, Q, Yan, C, Xu, Y (2020). l-Carnitine supplementation during in vitro culture regulates oxidative stress in embryos from bovine aged oocytes. Theriogenology 143, 64–73.CrossRefGoogle ScholarPubMed
Kitagawa, Y, Suzuki, K, Yoneda, A and Watanabe, T (2004). Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62, 1186–97.CrossRefGoogle Scholar
Liu, Y, Fiskum, G and Schubert, D (2002). Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80, 780–7.CrossRefGoogle ScholarPubMed
Ma, YY, Chen, HW and Tzeng, CR (2017). Low oxygen tension increases mitochondrial membrane potential and enhances expression of antioxidant genes and implantation protein of mouse blastocyst cultured in vitro. J Ova Res 10, 47.CrossRefGoogle ScholarPubMed
Matta, SG, Caldas-Bussiere, MC, Viana, KS, Faes, MR, Paes de Carvalho, CS, Dias, BL and Quirino, CR (2009). Effect of inhibition of synthesis of inducible nitric oxide synthase-derived nitric oxide by aminoguanidine on the in vitro maturation of oocyte–cumulus complexes of cattle. Anim Reprod Sci 111, 189–201.CrossRefGoogle ScholarPubMed
Mingoti, GZ, Caiado Castro, VS, Méo, SC, Barretto, LS and Garcia, JM (2009). The effect of interaction between macromolecule supplement and oxygen tension on bovine oocytes and embryos cultured in vitro. Zygote 17, 321–8.CrossRefGoogle ScholarPubMed
Morado, SA, Cetica, PD, Beconi, MT and Dalvit, GC (2009). Reactive oxygen species in bovine oocyte maturation in vitro. Reprod Fertil Dev. 21, 608–14.CrossRefGoogle ScholarPubMed
Parrish, J, Krogenaes, A and Susko-Parrish, J (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44, 859–69.CrossRefGoogle ScholarPubMed
Pasqualotto, EB, Agarwal, A, Sharma, RK, Izzo, VM, Pinotti, JA, Joshi, NJ and Rose, BI (2004). Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril 81, 973–6.CrossRefGoogle ScholarPubMed
Pires, PRL, Santos, NP, Adona, PR, Natori, MM, Schwarz KRL de Bem THC and Leal CLV (2009). Endothelial and inducible nitric oxide synthases in oocytes of cattle. Anim Reprod Sci 116, 233–43.CrossRefGoogle ScholarPubMed
Ricart-Jane, D, Llobera, M, and Lopez-Tejero, MD (2002). Anticoagulants and other preanalytical factors interfere in plasma nitrate/nitrite quantification by the Griess method. Nitric Oxide 6, 178–85.CrossRefGoogle ScholarPubMed
Robertson, I and Nelson, R (1998). Certification and identification of the embryo. In: Stringfellow, DA and Seidel, SM (eds), Manual of the International Embryo Transfer Society, 3rd edn. International Embryo Transfer Society, Savoy, IL, USA, pp. 103–34.Google Scholar
Rocha-Frigoni, NA, Leão, BC, Nogueira, É, Accorsi, MF and Mingoti, GZ (2013). Effects of gaseous atmosphere and antioxidants on the development and cryotolerance of bovine embryos at different periods of in vitro culture. Zygote 23, 159–68.CrossRefGoogle ScholarPubMed
Stojkovic, M, Machado, SA, Stojkovic, P, Zakhartchenko, V, Hutzler, P, Gonçalves, P.B and Wolf, E (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol Reprod 64, 904–9.CrossRefGoogle ScholarPubMed
Sudano, MJ, Rascado, TD, Tata, A, Belaz, KR, Santos, VG, Valente, RS, Mesquita, FS, Ferreira, CR, Araújo, JP, Eberlin, MN and Landim-Alvarenga, FD (2016). Lipidome signatures in early bovine embryo development. Theriogenology 86, 472–84.CrossRefGoogle ScholarPubMed
Sutton-McDowall, ML, Feil, D, Robker, RL, Thompson, JG and Dunning, KR (2012). Utilization of endogenous fatty acid stores for energy production in bovine preimplantation embryos. Theriogenology 77, 1632–41.CrossRefGoogle ScholarPubMed
Takahashi, M, Keicho, K, Takahashi, H, Ogawa, H, Schulte, R and Okano, A (2000). Effect of oxidative stress on development and DNA damage in in-vitro cultured bovine embryos by comet assay. Theriogenology 54, 137–45.CrossRefGoogle ScholarPubMed
Takahashi, T, Inaba, Y, Somfai, T, Kaneda, M, Geshi, M, Nagai, T and Manabe, N (2013). Supplementation of culture medium with l-carnitine improves development and cryotolerance of bovine embryos produced in vitro. Reprod Fertil Dev 25, 589–99.CrossRefGoogle ScholarPubMed
Tejero, J, Shiva, S and Gladwin, MT (2019). Sources of vascular nitric oxide and reactive oxygen species and their regulation. Physiol Rev 99, 311–79.CrossRefGoogle ScholarPubMed
Tesfaye, D, Kadanga, A, Rings, F, Bauch, K, Jennen, D, Nganvongpanit, K, Holker, M, Tholen, E, Ponsuksili, S, Wimmers, K, Montag, M, Gilles, M, Kirfel, G, Herzog, V and Schellander, K (2006). The effect of nitric oxide inhibition and temporal expression patterns of the mRNA and protein products of nitric oxide synthase genes during in vitro development of bovine pre-implantation embryos. Reprod Domest Anim 41, 501–509.CrossRefGoogle ScholarPubMed
Tranguch, S, Steuerwald, N and Huet-Hudson, YM (2003). Nitric oxide synthase production and nitric oxide regulation of preimplantation embryo development. Biol Reprod 68, 1538–44.CrossRefGoogle ScholarPubMed
Viana, J (2018). Statistics of embryo production and transfer in domestic farm animals Is it a turning point? In 2017 more in vitro-produced than in vivo-derived embryos were transferred worldwide. Embryo Technology Newsletter 36, 8–25.Google Scholar
Viana, KS, Caldas-Bussiere, MC, Matta, SG, Faes, MR, de Carvalho, CS and Quirino, CR (2007). Effect of sodium nitroprusside, a nitric oxide donor, on the in vitro maturation of bovine oocytes. Anim Reprod Sci 102, 217–27.CrossRefGoogle ScholarPubMed
Zheng, K, Sulieman, FJ, Li, J, Wei, Q, Xu, M and Shi, F (2015). Nitric oxide and thyroid hormone receptor (1 contribute to ovarian follicular development in immature hyper- and hypo-thyroid rats. Reprod Biol 15, 27–33.CrossRefGoogle ScholarPubMed
Zolini, AM, Carrascal-Triana, E, Ruiz de King, A, Hansen, PJ, Alves Torres, CA and Block, J (2019). Effect of addition of l-carnitine to medium for oocyte maturation and embryo culture on development and cryotolerance of bovine embryos produced in vitro. Theriogenology 133, 135–43.CrossRefGoogle ScholarPubMed