Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
Shopping Cart: ( empty )
You are here: Home > Journals > RD > RD08198
RESEARCH ARTICLE
Contents Vol 21(4)

Reactive oxygen species in bovine oocyte maturation in vitro

Sergio A. Morado A B , Pablo D. Cetica A , Martha T. Beconi A and Gabriel C. Dalvit A
+ Author Affiliations
- Author Affiliations

A Area of Biochemistry, Institute of Research and Technology in Animal Reproduction (INITRA), School of Veterinary Sciences, University of Buenos Aires, Chorroarín 280, C1427CWO, Buenos Aires, Argentina.

B Corresponding author. Email: smorado@fvet.uba.ar

Reproduction, Fertility and Development 21(4) 608-614 https://doi.org/10.1071/RD08198
Submitted: 10 September 2008  Accepted: 26 January 2009   Published: 17 April 2009

Abstract

The role of reactive oxygen species (ROS) in the in vitro maturation (IVM) of oocytes remains controversial. The aim of the present study was to determine possible fluctuations in ROS production during bovine oocyte IVM in the presence of different modulators of ROS generation. Cumulus–oocyte complexes were cultured in medium 199 (control) in the absence or presence of 0.6 mm cysteine, 1mm 1-choro-2,4-dinitro benzene (CDNB), 2μm diphenyliodonium, 0.5 mm N-nitro-l-arginine methyl ester or 10 μm sodium nitroprusside (SNP) at 39°C, in 5% CO2 in humidified air for 22 h. In addition, the respiratory chain effectors potassium cyanide (KCN; 1 mm) and carbonyl cyanide m-chlorophenylhydrazone (0.42 μm) were used. Meiotic maturation was determined by the presence of MII. ROS production was evaluated in denuded oocytes at different time points as the ratio of 2′,7′-dichlorodihydrofluorescein diacetate (DCHF-DA) to fluorescein diacetate (FDA). ROS levels, expressed as DCHF-DA : FDA, fluctuated throughout the 22 h of maturation depending on the treatment applied. At 12 h incubation in the presence of KCN and SNP, ROS levels were increased, whereas ROS levels after 12 h in the presence of cysteine were reduced (P < 0.05). Both CDNB and SNP impaired meiotic progression. The higher metabolic activity demand during bovine oocyte maturation coincides with a concomitant reduction in ROS generation. These results suggest that 12 h would be a critical point for bovine oocyte IVM because it is closely related to the production of ROS at this time.


Acknowledgements

This work was supported by a grant from the University of Buenos Aires. The authors thank the Japanese International Cooperation Agency (JICA) for technology transfer and equipment, Astra Laboratories for ultrapure water, Deltacar abbatoir for providing ovaries and Fernando Delicia for recovering the ovaries.


References

Antunes, F. , Boveris, A. , and Cadenas, E. (2004). On the mechanism and biology of cytochrome oxidase by nitric oxide. Proc. Natl Acad. Sci. USA 101, 16 774–16 779.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Boveris A., and Cadenas E. (1982) Production of superoxide radicals and hydrogen peroxide in mitochondria. In ‘Superoxide dismutase’. (Ed. L. W. Oberley.) pp. 15–30. (CRC Press: Boca Raton.)

Bu, S. , Xie, H. , Tao, Y. , Wang, J. , and Xia, G. (2004). Nitric oxide influences the maturation of cumulus cell-enclosed mouse oocytes cultured in spontaneous maturation medium and hypoxanthine-supplemented medium through different pathways. Mol. Cell. Endocrinol. 223, 85–93.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Buhimschi, I. A. , Kramer, W. B. , Buhimschi, C. S. , Thompson, L. P. , and Weiner, C. P. (2000). Reduction–oxidation (redox) state regulation of matrix metalloproteinase activity in human fetal membranes. Am. J. Obstet. Gynecol. 182, 458–464.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Calabrese, V. , Boyd-Kimball, D. , Scapagnini, G. , and Butterfield, D. A. (2004). Nitric oxide and cellular stress response in brain aging and neurodegenerative disorders: the role of vitagenes. In Vivo 18, 245–267.
| PubMed |  CAS |

Cetica, P. D. , Dalvit, G. C. , and Beconi, M. T. (1999). Study of evaluation criteria used for in vitro bovine oocyte selection and maturation. Biocell 23, 125–133.
| PubMed |  CAS |

Cetica, P. D. , Pintos, L. N. , Dalvit, G. C. , and Beconi, M. T. (2001). Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life 51, 57–64.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Chance, B. , Sies, H. , and Boveris, A. (1979). Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59, 527–605.
| PubMed |  CAS |

Chen, Q. , Vazquez, E. J. , Moghaddas, S. , Hoppel, C. L. , and Lesnefsky, E. J. (2003). Production of reactive oxygen species by mitochondria. J. Biol. Chem. 278, 36 027–36 031.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Dalvit, G. C. , Cetica, P. D. , and Beconi, M. T. (1998). Effect of alpha-tocopherol and ascorbic acid on bovine in vitro fertilization. Theriogenology 49, 619–627.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Dalvit, G. , Llanes, S. P. , Descalzo, A. , Insani, M. , Beconi, M. , and Cetica, P. (2005). Effect of alpha-tocopherol and ascorbic acid on bovine oocyte in vitro maturation. Reprod. Domest. Anim. 40, 93–97.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

de Matos, G. D. , and Furnus, C. C. (2000). The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development: effect of β-mercaptoethanol, cysteine and cystine. Theriogenology 53, 761–771.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

de Matos, G. D. , Furnus, C. C. , and Moses, D. F. (1997). Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol. Reprod. 57, 1420–1425.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Dumollard, R. , Marangos, P. , Fitzharris, G. , Swann, K. , Duchen, M. , and Carroll, J. (2004). Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 131, 3057–3067.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Finkel, T. (1998). Oxygen radicals and signalling. Curr. Opin. Cell Biol. 10, 248–253.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Forman, H. J. , and Torres, M. (2002). Reactive oxygen species and cell signalling: respiratory burst in macrophages signalling. Am. J. Respir. Crit. Care Med. 166, S4–S8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Gouge, R. C. , Marshburn, P. , Gordon, B. E. , Nunley, W. , and Huet-Hudson, Y. M. (1998). Nitric oxide as a regulator of embryonic development. Biol. Reprod. 58, 875–879.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Hashimoto, S. , Minami, N. , Yamada, M. , and Imai, H. (2000). Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Mol. Reprod. Dev. 56, 520–526.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Hattori, M. , and Tabata, S. (2006). Nitric oxide and ovarian function. Anim. Sci. J. 77, 275–284.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Heales, S. J. , Davies, S. E. , Bates, T. E. , and Clark, J. B. (1995). Depletion of brain glutathione is accompanied by impaired mitochondrial function and decreased N-acetyl aspartate concentration. Neurochem. Res. 20, 31–38.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Ho, Y. S. , Dey, M. S. , and Crapo, J. D. (1996). Antioxidant enzyme expression in rat lungs during hypoxia. Am. J. Physiol. 270, L810–L818.
| PubMed |  CAS |

Hsu, M. , Srinivas, B. , Kumar, J. , Subramanian, R. , and Andersen, J. (2005). Glutathione depletion resulting in selective mitochondrial complex I inhibition in dopaminergic cells is via an NO-mediated pathway not involving peroxynitrite: implications for Parkinson’s disease. J. Neurochem. 92, 1091–1103.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Ignarro, L. J. (1999). Nitric oxide: a unique endogenous signalling molecule in vascular biology. Biosci. Rep. 19, 51–71.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Irani, K. , Xia, Y. , Zweier, J. L. , Sollott, S. J. , Der, C. J. , Fearon, E. R. , Sundaresan, M. , Finkel, T. , and Goldschmidt-Clermont, P. J. (1997). Mitogenic signalling mediated by oxidants in Ras-transformed fibroblasts. Science 275, 1649–1652.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Jablonka-Shariff, A. , and Olson, L. M. (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, 2944–2954.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Jablonka-Shariff, A. , and Olson, L. M. (2000). Nitric oxide is essential for optimal meiotic maturation of murine cumulus–oocyte complexes in vitro. Mol. Reprod. Dev. 55, 412–421.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Johnson, M. H. , and Nasr-Esfahani, M. H. (1994). Radical solutions and culture problems: could free oxygen-radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? Bioessays 16, 31–38.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Kissner, R. , Nauser, T. , Bugnon, P. , Lye, P. G. , and Koppenol, W. H. (1997). Formation and properties of peroxynitrite as studied by laser flash protolysis, high pressure stopped-flow technique, and pulse radiolysis. Chem. Res. Toxicol. 10, 1285–1292.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Kuo, R. C. , Baxter, G. T. , Thompson, S. H. , Stricker, S. A. , Patton, C. , Bonaventura, J. , and Epel, D. (2000). NO is necessary and sufficient for egg activation at fertilization. Nature 406, 633–636.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Lane, M. , Maybach, J. M. , and Gardner, D. K. (2002). Addition of ascorbate during cryopreservation stimulates subsequent embryo development. Hum. Reprod. 17, 2686–2693.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

LeBel, C. P. , Ischiropoulos, H. , and Bondy, S. C. (1992). Evaluation of the probe 2′,7′-dichlorofluorescein as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 5, 227–231.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Li, N. , and Karin, M. (1999). Is NF-κB the sensor of oxidative stress? FASEB J. 13, 1137–1143.
| PubMed |  CAS |

Li, N. , Ragheb, K. , Lawler, G. , Sturgis, J. , Rajwa, B. , Melendez, J. A. , and Robinson, J. P. (2003). DPI induces mitochondrial superoxide-mediated apoptosis. Free Radic. Biol. Med. 34, 465–477.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Luberda, Z. (2005). The role of glutathione in mammalian gametes. Reprod. Biol. 5, 5–17.
| PubMed |

Majima, E. , Ikawa, K. , Takeda, M. , Hashimoto, M. , Shinohara, Y. , and Terada, H. (1995). Translocation of loops regulates transport activity of mitochondrial ADP/ATP carrier deduced from formation of a specific intermolecular disulfide bridge catalyzed by copper-o-phenanthroline. J. Biol. Chem. 270, 29 548–29 554.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Marshall, H. E. , Merchant, K. , and Stamler, J. S. (2000). Nitrosation and oxidation in the regulation of gene expression. FASEB J. 14, 1889–1900.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Meyer, M. , Schreck, R. , and Bauerle, P. A. (1993). H2O2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J. 12, 2005–2015.
| PubMed |  CAS |

Muller, F. L. , Liu, Y. , and Vam Remmen, H. (2004). Complex III releases superoxide to both sides of the inner mitochondrial membrane. J. Biol. Chem. 279, 49 064–49 073.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Muzyamba, M. C. , Speake, P. F. , and Gibson, J. S. (2000). Oxidants and regulation of K–Cl cotransport in equine red blood cells. Am. J. Physiol. Cell Physiol. 279, C981–C989.
| PubMed |  CAS |

O’Flaherty, C. , Breininger, E. , Beorlegui, N. , and Beconi, M. T. (2005). Acrosome reaction in bovine spermatozoa: role of reactive oxygen species and lactate dehydrogenase C4. Biochim. Biophys. Acta 1726, 96–101.
| PubMed |  CAS |

Petr, J. , Rajmon, R. , Rozinek, J. , Sedmíkova, M. , Jeseta, M. , Chmelíkova, E. , Svetskova, D. , and Jílek, F. (2005). Activation of pig oocytes using nitric oxide donors. Mol. Reprod. Dev. 71, 115–122.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Poderoso, J. J. , Carreras, M. C. , Lisdero, C. L. , Riobó, N. A. , Schöpfer, F. , and Boveris, A. (1996). Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch. Biochem. Biophys. 328, 85–92.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Riley, J. C. , and Behrman, H. R. (1991). Oxygen radicals and reactive oxygen species in reproduction. Proc. Soc. Exp. Biol. Med. 198, 781–791.
| PubMed |  CAS |

Schreck, R. , Rieber, P. , and Bauerle, P. A. (1991). Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO J. 10, 2247–2258.
| PubMed |  CAS |

Sengoku, K. , Takuma, N. , Horikawa, M. , Tsuchiya, K. , Komoro, H. , Sharifa, D. , Tamate, K. , and Ishikawa, M. (2001). Requirement of nitric oxide for murine oocyte maturation, embryo development, and trophoblast outgrowth in vitro. Mol. Reprod. Dev. 58, 262–268.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Seyfried, J. , Soldner, F. , Schulz, J. B. , Klockgether, T. , Kovar, K. A. , and Wülner, U. (1999). Differential effects of l-buthionine sulfoximine and ethacrynic acid on glutathione levels and mitochondrial function in PC12 cells. Neurosci. Lett. 264, 1–4.
| Crossref | l-buthionine sulfoximine and ethacrynic acid on glutathione levels and mitochondrial function in PC12 cells.&journal=Neurosci. Lett.&volume=264&pages=1-4&publication_year=1999&author=J%2E%20Seyfried&hl=en&doi=10.1016/S0304-3940(99)00107-X" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed | CAS |

Sirard, M. A. , Florman, H. M. , Leibfried-Rutledge, M. L. , Barnes, F. L. , Sims, M. L. , and First, N. L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–1263.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Sutton, M. L. , Cetica, P. D. , Beconi, M. T. , Kind, K. L. , Gilchrist, R. B. , and Thompson, J. G. (2003). Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126, 27–34.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Takami, M. , Preston, S. L. , Toyloy, V. A. , and Behrman, H. R. (1999). Antioxidants reversibly inhibit the spontaneous resumption of meiosis. Am. J. Physiol. 276, 684–688.


Tarkowski, A. K. (1966). An air-drying method for chromosome preparations from mouse eggs. Cytogenetics 5, 394–400.
| Crossref | GoogleScholarGoogle Scholar |

Vesce, S. , Jekabsons, M. B. , Johnson-Caldwell, L. I. , and Nicholls, D. G. (2005). Acute glutathione depletion restricts mitochondrial ATP export in cerebellar granule neurons. J. Biol. Chem. 280, 38 720–38 728.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Wang, Y. X. , Zheng, Y. M. , Abdullaev, I. , and Kotlikoff, M. (2003). Metabolic inhibition with cyanide induces calcium release in pulmonary artery myocytes and Xenopus oocytes. Am. J. Physiol. Cell Physiol. 284, C378–C388.
| PubMed |  CAS |

Yang, H. W. , Hwang, K. J. , Kwon, H. C. , Kim, H. S. , Choi, K. W. , and Oh, K. S. (1998). Detection of reactive oxygen species (ROS) and apoptosis in human fragmentated embryos. Hum. Reprod. 13, 998–1002.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Zuelke, K. A. , Jones, D. P. , and Perreault, S. D. (1997). Glutathione oxidation is associated with altered microtubule function and disrupted fertilization in mature hamster oocytes. Biol. Reprod. 57, 1413–1419.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |