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Combined inhibitory effects of low temperature and N-acetyl-l-cysteine on the postovulatory aging of mouse oocytes

Published online by Cambridge University Press:  24 March 2015

Qian Li  and
Long-Bo Cui
Qian Li*
Affiliation:
College of Life Science, Yantai University, YanTai, Shandong 264005, China.
Long-Bo Cui
Affiliation:
College of Life Science, Yantai University, YanTai, Shandong 264005, China.
*
All correspondence to: Qian Li. College of Life Science, Yantai University, YanTai, Shandong 264005, China. Tel: +86 5356900638. Fax: +86 5356900638. E-mail: [email protected]
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Summary

The postovulatory aging of oocytes eventually affects the development of oocytes and embryos. Oxidative stress is known to accelerate the onset of apoptosis in oocytes and influence their capacity for fertilisation. This study aimed to reveal the roles of temperature and the antioxidant N-acetyl-l-cysteine in preventing the aging of postovulatory mouse oocytes. First, newly ovulated mouse oocytes were cultured at various temperature and time combinations in HCZB medium with varying concentrations of N-acetyl-l-cysteine to assess signs of aging and developmental potential. When cultured in HCZB with 300 μM N-acetyl-l-cysteine at different temperature and incubation time combinations (namely 25°C for 12 h, 15°C for 24 h and 5°C for 12 h), the increase in the susceptibility of oocytes to activating stimuli was efficiently prevented, and the developmental potential was maintained following Sr2+ activation or in vitro fertilisation. After incubation at either 15°C for 36 h or 5°C for 24 h, oocytes that had decreased blastocyst rates displayed unrecoverable abnormal cortical granule distribution together with decreased BCL2 levels, total glutathione concentrations and glutathione/glutathione disulphide (GSH/GSSG) ratios. In conclusion, postovulatory oocyte aging could be effectively inhibited by appropriate N-acetyl-l-cysteine addition at low temperatures. In addition, a simple method for the temporary culture of mature oocytes was established.

Keywords

AgingAntioxidantLow temperatureN-acetyl-l-cysteineOxidative stress
Type
Research Article
Information
Zygote , Volume 24 , Issue 2 , April 2016 , pp. 195 - 205
Copyright
Copyright © Cambridge University Press 2015 

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References

Almeida, P.A. & Bolton, V.N. (1995). The effect of temperature fluctuations on the cytoskeletal organisation and chromosomal constitution of the human oocyte. Zygote 3, 357–65.Google Scholar
Aman, R.R. & Parks, J.E. (1994). Effects of cooling and rewarming on the meiotic spindle and chromosomes of in vitro-matured bovine oocytes. Biol. Reprod. 50, 103–10.CrossRefGoogle ScholarPubMed
Arrigo, A.P. (1999). Gene expression and the thiol redox state. Free Radical Bio. Med. 27, 936–44.CrossRefGoogle ScholarPubMed
Atkuri, K.R., Mantovani, J.J. & Herzenberg, L.A. (2007). N-Acetylcysteine—a safe antidote for cysteine/glutathione deficiency. Curr. Opin. Pharmacol. 7, 355–9.Google Scholar
Azambuja, R.M., Kraemer, D.C. & Westhusin, M.E. (1998). Effect of low temperatures on in-vitro matured bovine oocytes. Theriogenology 49, 1155–64.CrossRefGoogle ScholarPubMed
Bavister, B.D. (1989). A consistently successful procedure for in vitro fertilization of golden hamster eggs. Gamete Res. 23, 139–58.CrossRefGoogle ScholarPubMed
Boerjan, M.L. & de Boer, P. (1990). First cell cycle of zygotes of the mouse derived from oocytes aged postovulation in vivo and fertilized in vivo . Mol. Reprod. Dev. 25, 155–63.Google Scholar
Cha, S.K., Kim, B.Y., Kim, M.K., Kim, Y.S., Lee, W.S., Yoon, T.K. & Lee, D.R. (2011). Effects of various combinations of cryoprotectants and cooling speed on the survival and further development of mouse oocytes after vitrification. Clin. Exp. Reprod. Med. 38, 24–30.Google Scholar
Chang, M.C. (1953). Storage of unfertilized rabbit ova; subsequent fertilization and the probability of normal development. Nature 172, 353–4.Google Scholar
Chip, S., Zelmer, A., Ogunshola, O.O., Felderhoff-Mueser, U., Nitsch, C., Buhrer, C. & Wellmann, S. (2011). The RNA-binding protein RBM3 is involved in hypothermia induced neuroprotection. Neurobiol. Dis. 43, 388–96.CrossRefGoogle ScholarPubMed
Dickinson, D.A., Moellering, D.R., Iles, K.E., Patel, R.P., Levonen, A.L., Wigley, A., Darley-Usmar, V.M. & Forman, H.J. (2003). Cytoprotection against oxidative stress and the regulation of glutathione synthesis. Biol. Chem. 384, 527–37.Google Scholar
Ducibella, T., Duffy, P., Reindollar, R. & Su, B. (1990). Changes in the distribution of mouse oocyte cortical granules and ability to undergo the cortical reaction during gonadotropin-stimulated meiotic maturation and aging in vivo . Biol. Reprod. 43, 870–6.Google Scholar
Fissore, R.A. & Robl, J.M. (1992). Intracellular response of rabbit oocytes to electrical stimulation. Mol. Reprod. Dev. 32, 9–16.Google Scholar
Fujino, Y., Ozaki, K., Yamamasu, S., Ito, F., Matsuoka, I., Hayashi, E., Nakamura, H., Ogita, S., Sato, E. & Inoue, M. (1996). DNA fragmentation of oocytes in aged mice. Hum. Reprod. 11, 1480–3.CrossRefGoogle ScholarPubMed
Funahashi, H., Cantley, T.C., Stumpf, T.T., Terlouw, S.L. & Day, B.N. (1994). Use of low-salt culture medium for in vitro maturation of porcine oocytes is associated with elevated oocyte glutathione levels and enhanced male pronuclear formation after in vitro fertilization. Biol. Reprod. 51, 633–9.Google Scholar
Gordo, A.C., Wu, H., He, C.L. & Fissore, R.A. (2000). Injection of sperm cytosolic factor into mouse metaphase II oocytes induces different developmental fates according to the frequency of [Ca2+](i) oscillations and oocyte age. Biol. Reprod. 62, 1370–19.Google Scholar
Gordo, A.C., Rodrigues, P., Kurokawa, M., Jellerette, T., Exley, G.E., Warner, C. & Fissore, R. (2002). Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol. Reprod. 66, 1828–37.Google Scholar
Goto, Y., Noda, Y., Mori, T. & Nakano, M. (1993). Increased generation of reactive oxygen species in embryos cultured in vitro . Free Radical Bio. Med. 15, 69–75.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, 175–89.Google Scholar
Kikuchi, K., Izaike, Y., Noguchi, J., Furukawa, T., Daen, F.P., Naito, K. & Toyoda, Y. (1995). Decrease of histone H1 kinase activity in relation to parthenogenetic activation of pig follicular oocytes matured and aged in vitro . J. Reprod. Fertil. 105, 325–30.Google Scholar
Kikuchi, K., Naito, K., Noguchi, J., Shimada, A., Kaneko, H., Yamashita, M., Aoki, F., Tojo, H. & Toyoda, Y. (2000). Maturation/M-phase promoting factor: a regulator of aging in porcine oocytes. Biol. Reprod. 63, 715–22.CrossRefGoogle ScholarPubMed
Kil, H.Y., Zhang, J. & Piantadosi, C.A. (1996). Brain temperature alters hydroxyl radical production during cerebral ischemia/reperfusion in rats. J. Cerebr. Blood F. Met. 16, 100–6.Google Scholar
Kimura, Y. & Yanagimachi, R. (1995). Intracytoplasmic sperm injection in the mouse. Biol. Reprod. 52, 709–20.Google Scholar
Kubiak, J.Z. (1989). Mouse oocytes gradually develop the capacity for activation during the metaphase II arrest. Dev. Biol. 136, 537–45.CrossRefGoogle ScholarPubMed
Lan, G.C., Ma, S.F., Wang, Z.Y., Luo, M.J., Chang, Z.L. & Tan, J.H. (2004). Effects of post-treatment with 6-dimethylaminopurine (6-DMAP) on ethanol activation of mouse oocytes at different ages. J. Exp. Zool. 301, 837–43.CrossRefGoogle ScholarPubMed
Li, Q., Wang, G., Zhang, J., Zhou, P., Wang, T. Y., Cui, W., Luo, M. J. & Tan, J. H. (2012). Combined inhibitory effects of pyruvate and low temperature on postovulatory aging of mouse oocytes. Biol. Reprod. 87, 105.Google Scholar
Liu, N., Wu, Y.G., Lan, G.C., Sui, H.S., Ge, L., Wang, J.Z., Liu, Y., Qiao, T.W. & Tan, J. H. (2009). Pyruvate prevents aging of mouse oocytes. Reproduction 138, 223–34.Google Scholar
Liu, J., Liu, M., Ye, X., Liu, K., Huang, J., Wang, L., Ji, G., Liu, N., Tang, X., Baltz, J.M., Keefe, D.L. & Liu, L. (2012). Delay in oocyte aging in mice by the antioxidant N-acetyl-L-cysteine (NAC). Hum. Reprod. 27, 1411–20.Google Scholar
Longo, F.J. (1974). Ultrastructural changes in rabbit eggs aged in vivo . Biol. Reprod. 11, 22–39.Google Scholar
Lord, T. & Aitken, R.J. (2013). Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction 146, R217–27.Google Scholar
Lord, T., Nixon, B., Jones, K.T. & Aitken, R.J. (2013). Melatonin prevents postovulatory oocyte aging in the mouse and extends the window for optimal fertilization in vitro . Biol. Reprod. 88, 67.Google Scholar
Ma, W., Zhang, D., Hou, Y., Li, Y.H., Sun, Q.Y., Sun, X.F. & Wang, W.H. (2005). Reduced expression of MAD2, BCL2, and MAP kinase activity in pig oocytes after in vitro aging are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation. Biol. Reprod. 72, 373–83.Google Scholar
Maas, D.H., Storey, B.T. & Mastroianni, L. Jr. (1976). Oxygen tension in the oviduct of the rhesus monkey (Macaca mulatta). Fertil. Steril. 27, 1312–7.Google Scholar
Magistrini, M. & Szollosi, D. (1980). Effects of cold and of isopropyl-N-phenylcarbamate on the second meiotic spindle of mouse oocytes. Eur. J. Cell Biol. 22, 699–707.Google Scholar
Marston, J.H. & Chang, M.C. (1964). The fertilizable life of ova and their morphology following delayed insemination in mature and immature mice. J. Exp. Zool. 155, 237–51.Google Scholar
Martino, A., Pollard, J.W. & Leibo, S.P. (1996). Effect of chilling bovine oocytes on their developmental competence. Mol. Reprod. Dev. 45, 503–12.Google Scholar
Meister, A. & Anderson, M.E. (1983). Glutathione. Annu. Rev. Biochem. 52, 711–60.Google Scholar
Moor, R.M. & Crosby, I.M. (1985). Temperature-induced abnormalities in sheep oocytes during maturation. J. Reprod. Fertil. 75, 467–73.Google Scholar
Nagai, T. (1987). Parthenogenetic activation of cattle follicular oocytes in vitro with ethanol. Gamete Res. 16, 243–9.Google Scholar
O’Neil, L., Paynter, S.J. & Fuller, B.J. (1997). Vitrification of mature mouse oocytes: improved results following addition of polyethylene glycol to a dimethyl sulfoxide solution. Cryobiology 34, 295–301.Google Scholar
Ojha, A. & Srivastava, N. (2012). Redox imbalance in rat tissues exposed with organophosphate pesticides and therapeutic potential of antioxidant vitamins. Ecotoxicol. Environ. Safety 75, 230–41.Google Scholar
Pickering, S.J. & Johnson, M.H. (1987). The influence of cooling on the organization of the meiotic spindle of the mouse oocyte. Hum. Reprod. 2, 207–16.CrossRefGoogle ScholarPubMed
Shao, Z.H., Sharp, W.W., Wojcik, K.R., Li, C.Q., Han, M., Chang, W.T., Ramachandran, S., Li, J., Hamann, K.J. & Van den Hoek, T.L. (2010). Therapeutic hypothermia cardioprotection via Akt- and nitric oxide-mediated attenuation of mitochondrial oxidants. Am. J. Physiol.–Heart C. 298, H2164–73.Google Scholar
Sies, H. (1999). Glutathione and its role in cellular functions. Free Radical Bio. Med. 27, 916–21.Google Scholar
Sun, Q.Y. & Schatten, H. (2006). Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 131, 193–205.CrossRefGoogle ScholarPubMed
Szollosi, D. (1971). Morphological changes in mouse eggs due to aging in the fallopian tube. Am. J. Anat. 130, 209–25.CrossRefGoogle ScholarPubMed
Takahashi, T., Takahashi, E., Igarashi, H., Tezuka, N. & Kurachi, H. (2003). Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol. Reprod. Dev. 66, 143–52.Google Scholar
Takai, Y., Matikainen, T., Jurisicova, A., Kim, M.R., Trbovich, A.M., Fujita, E., Nakagawa, T., Lemmers, B., Flavell, R.A., Hakem, R., Momoi, T., Yuan, J., Tilly, J.L. & Perez, G.I. (2007). Caspase-12 compensates for lack of caspase-2 and caspase-3 in female germ cells. Apoptosis 12, 791–800.CrossRefGoogle ScholarPubMed
Tarin, J. J., Ten, J., Vendrell, F. J. & Cano, A. (1998). Dithiothreitol prevents age-associated decrease in oocyte/conceptus viability in vitro . Hum. Reprod. 13, 381–6.Google Scholar
Tatone, C., Di Emidio, G., Barbaro, R., Vento, M., Ciriminna, R. & Artini, P.G. (2011). Effects of reproductive aging and postovulatory aging on the maintenance of biological competence after oocyte vitrification: insights from the mouse model. Theriogenology 76, 864–73.Google Scholar
Tesarik, J. (1993). Subzonal sperm insertion with aged human oocytes from failed in-vitro fertilization attempts: fertilization results and some applications. Hum. Reprod. 8, 1245–50.Google Scholar
Tilly, J.L. & Tilly, K.I. (1995). Inhibitors of oxidative stress mimic the ability of follicle-stimulating hormone to suppress apoptosis in cultured rat ovarian follicles. Endocrinology 136, 242–52.Google Scholar
Wakayama, S., Thuan, N.V., Kishigami, S., Ohta, H., Mizutani, E., Hikichi, T., Miyake, M. & Wakayama, T. (2004). Production of offspring from one-day-old oocytes stored at room temperature. J. Reprod. Dev. 50, 627–37.Google Scholar
Wang, W.H., Meng, L., Hackett, R.J., Odenbourg, R. & Keefe, D.L. (2001). Limited recovery of meiotic spindles in living human oocytes after cooling-rewarming observed using polarized light microscopy. Hum. Reprod. 16, 2374–8.CrossRefGoogle ScholarPubMed
Wang, T.Y., Li, Q., Li, H., Zhu, J., Cui, W., Jiao, G.Z. & Tan, J.H. (2014). Non-frozen preservation protocols for mature mouse oocytes dramatically extend their developmental competence by reducing oxidative stress. Mol. Hum. Reprod. 20, 318–29.Google Scholar
Ware, C.B., Barnes, F.L., Maiki-Laurila, M. & First, N.L. (1989). Age dependence of bovine oocyte activation. Gamete Res. 22, 265–75.Google Scholar
Whittingham, D.G. & Siracusa, G. (1978). The involvement of calcium in the activation of mammalian oocytes. Exp. Cell Res. 113, 311–7.CrossRefGoogle ScholarPubMed
Winston, N.J., Braude, P.R. & Johnson, M.H. (1993). Are failed-fertilized human oocytes useful? Hum. Reprod. 8, 503–7.Google Scholar
Wu, B., Ignotz, G., Currie, W.B. & Yang, X. (1997). Dynamics of maturation-promoting factor and its constituent proteins during in vitro maturation of bovine oocytes. Biol. Reprod. 56, 253–9.Google Scholar
Xu, Z., Abbott, A., Kopf, G.S., Schultz, R.M. & Ducibella, T. (1997). Spontaneous activation of ovulated mouse eggs: time-dependent effects on M-phase exit, cortical granule exocytosis, maternal messenger ribonucleic acid recruitment, and inositol 1,4,5-trisphosphate sensitivity. Biol. Reprod. 57, 743–50.CrossRefGoogle ScholarPubMed
Yan, J., Suzuki, J., Yu, X.M., Qiao, J., Kan, F.W. & Chian, R.C. (2011). Effects of duration of cryo-storage of mouse oocytes on cryo-survival, fertilization and embryonic development following vitrification. J. Assist. Reprod. Gen. 28, 643–9.Google Scholar
Yanagimachi, R. & Chang, M.C. (1961). Fertilizable life of golden hamster ova and their morphological changes at the time of losing fertilizability. J. Exp. Zool. 148, 185–203.CrossRefGoogle ScholarPubMed
Yoshida, M., Ishigaki, K., Nagai, T., Chikyu, M. & Pursel, V.G. (1993). Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol. Reprod. 49, 89–94.Google Scholar
Zhou, P., Wu, Y.G., Wei, D.L., Li, Q., Wang, G., Zhang, J., Luo, M.J. & Tan, J.H. (2010). Mouse cumulus-denuded oocytes restore developmental capacity completely when matured with optimal supplementation of cysteamine, cystine, and cumulus cells. Biol. Reprod. 82, 759–68.Google Scholar