Skip to main content Accessibility help
×
Home

Protective effects of ethanol extracts of Artemisia asiatica Nakai ex Pamp. on ageing-induced deterioration in mouse oocyte quality

  • Hyuk-Joon Jeon (a1), Seung Yeop You (a1), Dong Hyun Kim (a1) (a2), Hong Bae Jeon (a2) and Jeong Su Oh (a3)...

Summary

Following ovulation, oocytes undergo a time-dependent deterioration in quality referred to as post-ovulatory ageing. Although various factors influence the post-ovulatory ageing of oocytes, oxidative stress is a key factor involved in deterioration of oocyte quality. Artemisia asiatica Nakai ex Pamp. has been widely used in East Asia as a food ingredient and traditional medicine for the treatment of inflammation, cancer, and microbial infections. Recent studies have shown that A. asiatica exhibits antioxidative effects. In this study, we investigated whether A. asiatica has the potential to attenuate deterioration in oocyte quality during post-ovulatory ageing. Freshly ovulated mouse oocytes were cultured with 0, 50, 100 or 200 μg/ml ethanol extracts of A. asiatica Nakai ex Pamp. After culture for up to 24 h, various ageing-induced oocyte abnormalities, including morphological changes, reactive oxygen species (ROS) accumulation, apoptosis, chromosome and spindle defects, and mitochondrial aggregation were determined. Treatment of oocytes with A. asiatica extracts reduced ageing-induced morphological changes. Moreover, A. asiatica extracts decreased ROS generation and the onset of apoptosis by preventing elevation of the Bax/Bcl-2 expression ratio during post-ovulatory ageing. Furthermore, A. asiatica extracts attenuated the ageing-induced abnormalities including spindle defects, chromosome misalignment and mitochondrial aggregation. Our results demonstrate that A. asiatica can relieve deterioration in oocyte quality and delay the onset of apoptosis during post-ovulatory ageing.

Copyright

Corresponding author

All correspondence to: Jeong Su Oh. Department of Genetic Engineering, College of Biotechnology and Bioengineering, Sungkyunkwan University, Suwon, Korea. Tel.: +82 31 290 7865. Fax: +82 31 290 7870. E-mail: ohjs@skku.edu

References

Hide All
Agarwal, A., Gupta, S., Sekhon, L. & Shah, R. (2008). Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications. Antioxid. Redox Signal. 10, 1375–403.
Chaube, S.K., Prasad, P.V., Thakur, S.C. & Shrivastav, T.G. (2005). Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro . Apoptosis 10, 863–74.
Choi, W.J., Banerjee, J., Falcone, T., Bena, J., Agarwal, A. & Sharma, R.K. (2007). Oxidative stress and tumour necrosis factor-α-induced alterations in metaphase II mouse oocyte spindle structure. Fertil. Steril. 88, 1220–31.
de Matos, D.G. & 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, 761–71.
Dodson, M.G., Minhas, B.S., Curtis, S.K., Palmer, T.V. & Robertson, J.L. (1989). Spontaneous zona reaction in the mouse as a limiting factor for the time in which an oocyte may be fertilized. J. In Vitro Fert. Embryo. Transf. 6, 101–6.
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.
Duranthon, V. & Renard, J.P. (2001). The developmental competence of mammalian oocytes: a convenient but biologically fuzzy concept. Theriogenology 55, 1277–89.
Eppig, J.J., Hosoe, M., O'Brien, M.J., Pendola, F.M., Requena, A. & Watanabe, S. (2000). Conditions that affect acquisition of developmental competence by mouse oocytes in. vitro: FSH, insulin, glucose and ascorbic acid. Mol. Cell. Endocrinol. 163, 109–16.
Fissore, R.A., Kurokawa, M., Knott, J., Zhang, M. & Smyth, J. (2002). Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 124, 745–54.
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.
Hahm, K.B., Kim, J.H., You, B.M., Kim, Y.S., Cho, S.W., Yim, H., Ahn, B.O. & Kim, W.B. (1998). Induction of apoptosis with an extract of Artemisia. asiatica attenuates the severity of cerulein-induced pancreatitis in rats. Pancreas 17, 153–7.
Huh, K., Kwon, T.H., Shin, U.S., Kim, W.B., Ahn, B.O., Oh, T.Y. & Kim, J.A. (2003). Inhibitory effects of DA-9601 on ethanol-induced gastrohemorrhagic lesions and gastric xanthine oxidase activity in rats. J. Ethnopharmacol. 88, 269–73.
Longo, F.J. (1981). Changes in the zones pellucidae and plasmalemma of aging mouse eggs. Biol. Reprod. 25, 399411.
Lord, T. & Aitken, R.J. (2013). Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction 146, R217–27.
Luberda, Z. (2005). The role of glutathione in mammalian gametes. Reprod. Biol. 5, 517.
Martin, S.J., Reutelingsperger, C.P., McGahon, A.J., Rader, J.A., van Schie, R.C., LaFace, D.M. & Green, D.R. (1995). Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl . J. Exp. Med. 182, 1545–56.
Miao, Y.L., Kikuchi, K., Sun, Q.Y. & Schatten, H. (2009). Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum. Reprod. Update 15, 573–85.
Nagai, S., Mabuchi, T., Hirata, S., Shoda, T., Kasai, T., Yokota, S., Shitara, H., Yonekawa, H. & Hoshi, K. (2006). Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J. Exp. Med. 210, 137–44.
Oh, T.Y., Ahn, G.J., Choi, S.M., Ahn, B.O. & Kim, W.B. (2005). Increased susceptibility of ethanol-treated gastric mucosa to naproxen and its inhibition by DA-9601, an Artemisia asiatica extract. World J. Gastroenterol. 11, 7450–6.
Oh, T.Y., Lee, J.S., Ahn, B.O., Cho, H., Kim, W.B., Kim, Y.B., Surh, Y.J., Cho, S.W., Lee, K.M. & Hahm, K.B. (2001). Oxidative stress is more important than acid in the pathogenesis of reflux oesophagitis in rats. Gut 49, 364–71.
Perez, G.I., Jurisicova, A., Matikainen, T., Moriyama, T., Kim, M.R., Takai, Y., Pru, J.K., Kolesnick, R.N. & Tilly, J.L. (2005). A central role for ceramide in the age-related acceleration of apoptosis in the female germline. FASEB J. 19, 860862.
Premkumar, K.V. & Chaube, S.K. (2013). An insufficient increase of cytosolic free calcium level results postovulatory aging-induced abortive spontaneous egg activation in rat. J. Assist. Reprod. Genet. 30, 117–23.
Ryu, B.K., Ahn, B.O., Oh, T.Y., Kim, S.H., Kim, W.B. & Lee, E.B. (1998). Studies on protective effect of DA-9601, Artemisia asiatica extract, on acetaminophen- and CCl4-induced liver damage in rats. Arch. Pharm. Res. 21, 508–13.
Seo, H.J., Park, K.K., Han, S.S., Chung, W.Y., Son, M.W., Kim, W.B. & Surh, Y.J. (2002). Inhibitory effects of the standardized extract (DA-9601) of Artemisia asiatica Nakai on phorbol ester-induced ornithine decarboxylase activity, papilloma formation, cyclooxygenase-2 expression, inducible nitric oxide synthase expression and nuclear transcription factor kappa B activation in mouse skin. Int. J. Cancer 100, 456–62.
Seol, S.Y., Kim, M.H., Ryu, J.S., Choi, M.G., Shin, D.W. & Ahn, B.O. (2004). DA-9601 for erosive gastritis: results of a double-blind placebo-controlled phase III clinical trial. World J. Gastroenterol. 10, 2379–82.
Song, H.J., Shin, C.Y., Oh, T.Y. & Sohn, U.D. (2008). The protective effect of eupatilin on indomethacin-induced cell damage in cultured feline ileal smooth muscle cells: involvement of HO-1 and ERK. J. Ethnopharmacol. 118, 94101.
Steuerwald, N.M., Steuerwald, M.D. & Mailhes, J.B. (2005). Post-ovulatory aging of mouse oocytes leads to decreased MAD2 transcripts and increased frequencies of premature centromere separation and anaphase. Mol. Hum. Reprod. 11, 623–30.
Szollosi, D. (1971). Morphological changes in mouse eggs due to aging in the fallopian tube. Am. J .Anat. 130, 209–25.
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.
Tao, Y., Zhou, B., Xia, G., Wang, F., Wu, Z. & Fu, M. (2004). Exposure to l-ascorbic acid or α-tocopherol facilitates the development of porcine denuded oocytes from metaphase I to metaphase II and prevents cumulus cells from fragmentation. Reprod. Domest. Anim. 39, 52–7.
Tarin, J.J., Perez-Albala, S., Aguilar, A., Minarro, J., Hermenegildo, C. & Cano, A. (1999). Long-term effects of postovulatory aging of mouse oocytes on offspring: a two-generational study. Biol. Reprod. 61, 1347–55.
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.
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.
Winston, N.J., Braude, P.R. & Johnson, M.H. (1993). Are failed-fertilized human oocytes useful? Hum. Reprod. 8, 503–7.
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.
Zhang, N., Wakai, T. & Fissore, R.A. (2011). Caffeine alleviates the deterioration of Ca2+ release mechanisms and fragmentation of in vitro-aged mouse eggs. Mol. Reprod. Dev. 78, 684701.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed