Addition of MitoTEMPO to the maturation medium improves in vitro ‎maturation competence of bovine oocytes

Document Type : Original Article

Authors

Department of Animal Science, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran

Abstract

The effects of MitoTEMPO, a mitochondria-targeted antioxidant, and its non-targeted parent, TEMPO, on bovine oocyte maturation competence have not been determined so far. Hence, our study was aimed to investigate the effects of supplementing maturation medium with different concentrations of MitoTEMPO (0.00, 0.10, 1.00 and 10.00 µM) or TEMPO (0.00, 5.00, 10.00 and 15.00 mM) on in vitro maturation (IVM) and fertilization (IVF) of bovine oocytes. The oocytes after IVM and IVF were evaluated for the signs of nuclear maturation and normal fertilization. The average number of spermatozoa penetrated per oocyte and the level of intracellular reactive oxygen species (ROS) were also evaluated. The results showed that percentages of bovine oocytes reached the metaphase II stage of meiosis were significantly higher in the 1.00 µM MitoTEMPO group compared to the control group (without antioxidant supplementation). The normal fertilization rate also tended to be greater in this group than the control group. In comparison with the control group, the medium supplementation with 1.00 µM MitoTEMPO led to a significant decrease in the intracellular ROS level. The average number of spermatozoa penetrated per oocyte was not significantly different among the antioxidant-treated and the non-treated groups. The TEMPO addition to the maturation medium affected neither the rate of maturation/fertilization nor the level of intracellular ROS in bovine oocytes. Based on these results, we concluded that MitoTEMPO at a concentration of 1.00 µM had beneficial effects on the quality and fertilization potential of bovine oocytes.

Keywords


  1.  

    1. Lopera-Vásquez R, Hamdi M, Fernandez-Fuertes B, et al. Extracellular vesicles from BOEC in in vitro embryo development and quality. PLoS One 2016; 11(2): e0148083. doi:10.1371/journal.pone.0148083.
    2. Ali AA, Bilodeau JF, Sirard MA. Antioxidant requirements for bovine oocytes varies during in vitro maturation, fertilization and development. Theriogenology 2003; 59(3-4): 939-949.
    3. Sovernigo TC, Adona PR, Monzani PS, et al. Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reprod Domest Anim 2017; 52(4): 561-569.
    4. Guérin P, El Mouatassim S, Ménézo Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 2001; 7(2): 175-189.
    5. Yu S, Long H, Lyu Q-F, et al. Protective effect of quercetin on the development of preimplantation mouse embryos against hydrogen peroxide-induced oxidative injury. PloS One 2014; 9(2): e89520. doi:10.1371/journal.pone.0089520.
    6. Aitken RJ, Clarkson JS, Fishel S. Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod 1989; 41(1): 183-197.
    7. Halliwell B, Aruoma OI. DNA damage by oxygen‐ derived species. Its mechanism and measurement in mammalian systems. FEBS Lett 1991; 281(1-2): 9-19.
    8. Prastowo S, Amin A, Rings F, et al. Fateful triad of reactive oxygen species, mitochondrial dysfunction and lipid accumulation is associated with expression outline of the AMP-activated protein kinase pathway in bovine blastocysts. Reprod Fertil Dev 2017; 29(5): 890-905.
    9. Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil 1987; 81(2): 459-469.
    10. Downs SM, Mastropolo AM. The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev Biol 1994; 162(1): 154-168.
    11. Dalvit G, Llanes SP, Descalzo A, et al. Effect of alpha‐ tocopherol and ascorbic acid on bovine oocyte in vitro maturation. Reprod Domest Anim 2005; 40(2): 93-97.
    12. de Matos DG, Furnus CC. The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development effect of β-mercaptoethanol, cysteine and cystine. Theriogenology 2000; 53(3): 761-771.
    13. de Matos DG, Herrera C, Cortvrindt R, et al. Cysteamine supplementation during in vitro maturation and embryo culture: a useful tool for increasing the efficiency of bovine in vitro embryo production. Mol Reprod Dev 2002; 62(2): 203-209.
    14. de Matos DG, Furnus CC, Moses DF, et al. Effect of cysteamine on glutathione level and developmental capacity of bovine oocyte matured in vitro. Mol Reprod Dev 1995; 42(4): 432-436.
    15. Papis K, Poleszczuk O, Wenta‐Muchalska E, et al. Melatonin effect on bovine embryo development in vitro in relation to oxygen concentration. J Pineal Res 2007; 43(4): 321-326.
    16. Rodrigues-Cunha MC, Mesquita LG, Bressan F, et al. Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development. Theriogenology 2016; 86(7): 1685-1694.
    17. Tian X, Wang F, He C, et al. Beneficial effects of melatonin on bovine oocytes maturation: a mechanistic approach. J Pineal Res 2014; 57(3): 239-247.
    18. Ambrogi M, Dall'Acqua PC, Rocha‐Frigoni NA, et al. Transporting bovine oocytes in a medium supplemented with different macromolecules and antioxidants: Effects on nuclear and cytoplasmic maturation and embryonic development in vitro. Reprod Domest Anim 2017; 52(3): 409-421.
    19. Rocha-Frigoni NA, Leão BC, Dall'Acqua PC, et al. Improving the cytoplasmic maturation of bovine oocytes matured in vitro with intracellular and/or extracellular antioxidants is not associated with increased rates of embryo development. Theriogenology 2016; 86(8): 1897-1905.
    20. Rocha-Frigoni NA, Leão BC, Nogueira É, et al. Reduced levels of intracellular reactive oxygen species and apoptotic status are not correlated with increases in cryotolerance of bovine embryos produced in vitro in the presence of antioxidants. Reprod Fertil Dev 2014; 26(6): 797-805.
    21. Sudano MJ, Mattos MCC, Fernandes CB, et al. In vitro production of bovine embryos using Sigma antioxidant supplement®, α-tocopherol and L-ascorbic acid. Anim Reprod 2010; 7(1): 42-48.
    22. Ramis MR, Esteban S, Miralles A, et al. Protective effects of melatonin and mitochondria-targeted antioxidants against oxidative stress: a review. Curr Med Chem 2015; 22(22): 2690-2711.
    23. Smith RAJ, Murphy MP. Mitochondria-targeted antioxidants as therapies. Discov Med 2011; 11(57): 106-114.
    24. Ni R, Cao T, Xiong S, et al. Therapeutic inhibition of mitochondrial reactive oxygen species with mito-TEMPO reduces diabetic cardiomyopathy. Free Radic Biol Med 2016; 90: 12-23.
    25. Yang SG, Park HJ, Kim JW, et al. Mito-TEMPO improves development competence by reducing superoxide in preimplantation porcine embryos. Sci Rep 2018; 8(1): 10130. doi: 10.1038/s41598-018-28497-5.
    26. Uhde K, van Tol HTA, Stout TAE, et al. Metabolomic profiles of bovine cumulus cells and cumulus-oocyte-complex-conditioned medium during maturation in vitro. Sci Rep 2018; 8(1): 9477. doi:10.1038/s41598-018-27829-9.
    27. de Castro E Paula LA, Hansen PJ. Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro Theriogenology 2007; 68(5): 763-770.
    28. Dumollard R, Ward Z, Carroll J, et al. Regulation of redox metabolism in the mouse oocyte and embryo. Development 2007; 134(3): 455-465.
    29. Roth Z, Hansen PJ. Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 2005; 129(2): 235-244.
    30. Pavlok A, Lucas‐Hahn A, Niemann H. Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol Reprod Dev 1992; 31(1): 63-67.
    31. Remião MH, Lucas CG, Domingues WB, et al. Melatonin delivery by nanocapsules during in vitro bovine oocyte maturation decreased the reactive oxygen species of oocytes and embryos. Reprod Toxicol 2016; 63: 70-81.
    32. Balcerczyk A, Łuczak K, Soszyński M, et al. Prooxidative effects of TEMPO on human erythrocytes. Cell Biol Int 2004; 28(8‐9): 585-591.
    33. Gordon I. Laboratory production of cattle embryos. 2nd Cambridge, USA: CABI Publishing 2003; 79-111.
    34. Gilchrist RB, Thompson Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 2007; 67(1): 6-15.
    35. Goud AP, Goud PT, Diamond MP, et al. Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid. Free Radic Biol Med 2008; 44(7): 1295-1304.
    36. Curnow EC, Ryan J, Saunders D, et al. Bovine in vitro oocyte maturation as a model for manipulation of the gamma-glutamyl cycle and intraoocyte glutathione. Reprod Fertil Dev 2008; 20(5): 579-588.
    37. Lu X, Zhang Y, Bai H, et al. Mitochondria-targeted antioxidant MitoTEMPO improves the post-thaw sperm quality. Cryobiology 2018; 80: 26-29.
    38. You J, Kim J, Lim J, et al. Anthocyanin stimulates in vitro development of cloned pig embryos by increasing the intracellular glutathione level and inhibiting reactive oxygen species. Theriogenology 2010; 74(5): 777-785.
    39. Zhang X, Wu XQ, Lu S, et al. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res 2006; 16(10): 841-850.
    40. de Vantéry C, Stutz A, Vassalli JD, et al. Acquisition of meiotic competence in growing mouse oocytes is controlled at both translational and posttranslational levels. Dev Biol 1997; 187(1): 43-54.
    41. Picton H, Briggs D, Gosden R. The molecular basis of oocyte growth and development. Mol Cell Endocrinol 1998; 145(1-2): 27-37.
    42. Chowdhury MMR, Choi B-H, Khan I, et al. Supplementation of lycopene in maturation media improves bovine embryo quality in vitro. Theriogenology 2017; 103: 173-184.
    43. Ghaleno LR, Valojerdi MR, Hassani F, et al. High level of intracellular sperm oxidative stress negatively influences embryo pronuclear formation after intracytoplasmic sperm injection treatment. Andrologia 2014; 46(10): 1118-1127.
    44. Curnow EC, Ryan JP, Saunders DM, et al. Developmental potential of bovine oocytes following IVM in the presence of glutathione ethyl ester. Reprod Fertil Dev 2010; 22(4): 597-605.
    45. Wang ZG, Yu SD, Xu ZR. Improvement in bovine embryo production in vitro by treatment with green tea polyphenols during in vitro maturation of oocytes. Anim Reprod Sci 2007; 100(1-2): 22-31.
    46. Zhao XM, Wang N, Hao HS, et al. Melatonin improves the fertilization capacity and developmental ability of bovine oocytes by regulating cytoplasmic maturation events. J Pineal Res 2018; 64(1): e12445. doi:10.1111/jpi.12445.
    47. Sutovsky P, Schatten G. Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod 1997; 56(6): 1503-1512.
Volume 13, Issue 1
March 2022
Pages 71-78
  • Receive Date: 10 October 2019
  • Revise Date: 18 December 2019
  • Accept Date: 08 January 2020
  • First Publish Date: 15 December 2021