Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-26T13:43:14.508Z Has data issue: false hasContentIssue false
  • English
  • Français

Treatment of allicin improves maturation of immature oocytes and subsequent developmental ability of preimplantation embryos

Published online by Cambridge University Press:  17 July 2017

Sang-Gi Jeong ,
Seung-Eun Lee ,
Yun-Gwi Park ,
Yeo-Jin Son ,
Min-Young Shin ,
Eun-Young Kim  and
Se-Pill Park
Sang-Gi Jeong
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Stem Cell Research Center, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea.
Seung-Eun Lee
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Stem Cell Research Center, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea.
Yun-Gwi Park
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Stem Cell Research Center, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea.
Yeo-Jin Son
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Stem Cell Research Center, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea.
Min-Young Shin
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Stem Cell Research Center, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea.
Eun-Young Kim*
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Stem Cell Research Center, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Mirae Cell Bio, 288 Achasan-ro, Gwangjin-gu, Seoul, 05066, Korea.
Se-Pill Park*
Affiliation:
Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Stem Cell Research Center, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Mirae Cell Bio, 288 Achasan-ro, Gwangjin-gu, Seoul, 05066, Korea.
*
Eun-Young Kim. Mirae Cell Bio, 288 Achasan-ro, Gwangjin-gu, Seoul, 05066, Korea. Tel: +82 2 457 8758. E-mail: [email protected]
All correspondence to: Se-Pill Park. Faculty of Biotechnology, College of Applied Life Sciences, Jeju National University, 102 Jejudaehak-ro, Jeju-si, Jeju Special Self-Governing Province, 63243, Korea. Tel: +82 64 754 4650. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Allicin (AL) regulates the cellular redox, proliferation, viability, and cell cycle of different cells against extracellular-derived stress. This study investigated the effects of allicin treatment on porcine oocyte maturation and developmental competence. Porcine oocytes were cultured in medium supplemented with 0 (control), 0.01, 0.1, 1, 10 or 100 μM AL, respectively, during in vitro maturation (IVM). The rate of polar body emission was higher in the 0.1 AL-treated group (74.5% ± 2.3%) than in the control (68.0% ± 2.6%) (P < 0.1). After parthenogenetic activation, the rates of cleavage and blastocyst formation were significantly higher in the 0.1 AL-treated group than in the control (P < 0.05). The reactive oxygen species level at metaphase II did not significantly differ among all groups. In matured oocytes, the expression of both BAK and CASP3, and BIRC5 was significantly lower and higher, respectively, in the 0.1 AL-treated group than in the control. Similarly, the expression of BMP15 and CCNB1, and the activity of phospho-p44/42 mitogen-activated protein kinase (MAPK), significantly increased. These results indicate that supplementation of oocyte maturation medium with allicin during IVM improves the maturation of oocytes and the subsequent developmental competence of porcine oocytes.

Keywords

AllicinEmbryo developmentIn vitro maturationOocyte maturationPig
Type
Research Article
Information
Zygote , Volume 25 , Issue 4 , August 2017 , pp. 480 - 488
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

5

These authors contributed equally to this work.

References

Albarracin, J.L., Morato, R., Izquierdo, D. & Mogas, T. (2005). Vitrification of calf oocytes: effects of maturation stage and prematuration treatment on the nuclear and cytoskeletal components of oocytes and their subsequent development. Mol. Reprod. Dev. 72, 239–49.CrossRefGoogle ScholarPubMed
Borlinghaus, J., Albrecht, F., Gruhlke, M.C., Nwachukwu, I.D. & Slusarenko, A.J. (2014). Allicin: chemistry and biological properties. Molecules 19, 12591–618.CrossRefGoogle ScholarPubMed
Cai, Y., Wang, R., Pei, F. & Liang, B.B. (2007). Antibacterial activity of allicin alone and in combination with β-lactams against Staphylococcus spp. and Pseudomonas aeruginosa . J. Antibiotics 60, 335–8.CrossRefGoogle ScholarPubMed
Chan, J.Y., Yuen, A.C., Chan, R.Y. & Chan, S.W. (2013). A review of the cardiovascular benefits and antioxidant properties of allicin. Phytother. Res. PTR 27, 637–46.CrossRefGoogle ScholarPubMed
Chen, S., Tang, Y., Qian, Y., Chen, R., Zhang, L., Wo, L. & Chai, H. (2014). Allicin prevents H2O2-induced apoptosis of HUVECs by inhibiting an oxidative stress pathway. BMC Complement. Altern. Med. 14, 321.CrossRefGoogle ScholarPubMed
Choi, J.Y., Kang, J.T., Park, S.J., Kim, S.J., Moon, J.H., Saadeldin, I.M., Jang, G. & Lee, B.C. (2013). Effect of 7,8-dihydroxyflavone as an antioxidant on in vitro maturation of oocytes and development of parthenogenetic embryos in pigs. J. Reprod. Dev. 59, 450–456.CrossRefGoogle ScholarPubMed
Chu, Y.L., Ho, C.T., Chung, J.G., Rajasekaran, R. & Sheen, L.Y. (2012). Allicin induces p53-mediated autophagy in Hep G2 human liver cancer cells. J. Agric. Food Chem. 60, 8363–71.CrossRefGoogle ScholarPubMed
Craig, J., Zhu, H., Dyce, P.W., Petrik, J. & Li, J. (2004). Leptin enhances oocyte nuclear and cytoplasmic maturation via the mitogen-activated protein kinase pathway. Endocrinology 145, 5355–63.CrossRefGoogle ScholarPubMed
Dedieu, T., Gall, L., Crozet, N., Sevellec, C. & Ruffini, S. (1996). Mitogen-activated protein kinase activity during goat oocyte maturation and the acquisition of meiotic competence. Mol. Reprod. Dev. 45, 351–8.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Duan, X., Wang, Q.C., Chen, K.L., Zhu, C.C., Liu, J. & Sun, S.C. (2015). Acrylamide toxic effects on mouse oocyte quality and fertility in vivo . Sci. Rep. 5, 11562.CrossRefGoogle ScholarPubMed
Fathi, M., Seida, A.A., Sobhy, R.R., Darwish, G.M., Badr, M.R. & Moawad, A.R. (2014). Caffeine supplementation during IVM improves frequencies of nuclear maturation and preimplantation development of dromedary camel oocytes following IVF. Theriogenology 81, 1286–92.CrossRefGoogle ScholarPubMed
Gupta, M.K., Uhm, S.J. & Lee, H.T. (2010). Effect of vitrification and β-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertil. Steril. 93, 2602–7.CrossRefGoogle ScholarPubMed
Hussein, T.S., Thompson, J.G. & Gilchrist, R.B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–21.CrossRefGoogle ScholarPubMed
Jeon, Y., Kwak, S.S., Cheong, S.A., Seong, Y.H. & Hyun, S.H. (2013). Effect of trans-epsilon-viniferin on in vitro porcine oocyte maturation and subsequent developmental competence in preimplantation embryos. J. Vet Med. Sci. 75, 1277–86.CrossRefGoogle ScholarPubMed
Kang, J.T., Koo, O.J., Kwon, D.K., Park, H.J., Jang, G., Kang, S.K. & Lee, B.C. (2009). Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells. J. Pineal Res. 46, 22–8.CrossRefGoogle ScholarPubMed
Kere, M., Siriboon, C., Lo, N.W., Nguyen, N.T. & Ju, J.C. (2013). Ascorbic acid improves the developmental competence of porcine oocytes after parthenogenetic activation and somatic cell nuclear transplantation. J. Reprod. Dev. 59, 78–84.CrossRefGoogle ScholarPubMed
Kim, Y.S., Kim, K.S., Han, I., Kim, M.H., Jung, M.H. & Park, H.K. (2012). Quantitative and qualitative analysis of the antifungal activity of allicin alone and in combination with antifungal drugs. PLoS One 7, e38242.CrossRefGoogle ScholarPubMed
Lee, S.E., Kim, E.Y., Choi, H.Y., Moon, J.J., Park, M.J., Lee, J.B., Jeong, C.J. & Park, S.P. (2014). Rapamycin rescues the poor developmental capacity of aged porcine oocytes. Asian-Aust. J. Anim. Sci. 27, 635–47.CrossRefGoogle ScholarPubMed
Liang, C.G., Su, Y.Q., Fan, H.Y., Schatten, H. & Sun, Q.Y. (2007). Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. Mol. Endocrinol. 21, 2037–55.CrossRefGoogle ScholarPubMed
Liu, S., Jiang, L., Zhong, T., Kong, S., Zheng, R., Kong, F., Zhang, C., Zhang, L. & An, L. (2015). Effect of acrylamide on oocyte nuclear maturation and cumulus cells apoptosis in mouse in vitro . PLoS One 10, e0135818.CrossRefGoogle ScholarPubMed
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25, 402–8.CrossRefGoogle Scholar
O'Doherty, A.M., O'Gorman, A., al Naib, A., Brennan, L., Daly, E., Duffy, P. & Fair, T. (2014). Negative energy balance affects imprint stability in oocytes recovered from postpartum dairy cows. Genomics 104, 177–85.CrossRefGoogle ScholarPubMed
Ogawa, B., Ueno, S., Nakayama, N., Matsunari, H., Nakano, K., Fujiwara, T., Ikezawa, Y. & Nagashima, H. (2010). Developmental ability of porcine in vitro matured oocytes at the meiosis II stage after vitrification. J. Reprod. Dev. 56, 356–61.CrossRefGoogle ScholarPubMed
Phongnimitr, T., Liang, Y., Srirattana, K., Panyawai, K., Sripunya, N., Treetampinich, C. & Parnpai, R. (2013). Effect of l-carnitine on maturation, cryo-tolerance and embryo developmental competence of bovine oocytes. Nihon chikusan Gakkaiho [Anim. Sci. J.] 84, 719–25.Google ScholarPubMed
Pu, Y., Wang, Z., Bian, Y., Zhang, F., Yang, P., Li, Y., Zhang, Y., Liu, Y., Fang, F., Cao, H. & Zhang, X. (2014). All-trans retinoic acid improves goat oocyte nuclear maturation and reduces apoptotic cumulus cells during in vitro maturation. Nihon chikusan Gakkaiho [Anim. Sci. J.] 85, 833–9.Google ScholarPubMed
Sanchez, F. & Smitz, J. (2012). Molecular control of oogenesis. Biochim. Biophys. Acta 1822, 1896–912.CrossRefGoogle ScholarPubMed
SAS Institute Inc. (2013). Base SASȼç 9.4 Procedures Guide: Statistical Procedures, Second Edition. Cary, North Carolina, USA: SAS Institute Inc.Google Scholar
Shamas-Din, A., Kale, J., Leber, B. & Andrews, D.W. (2013). Mechanisms of action of Bcl-2 family proteins. Cold Spring Harb. Perspect. Biol. 5, a008714.CrossRefGoogle ScholarPubMed
Siffroi-Fernandez, S., Dulong, S., Li, X.M., Filipski, E., Grechez-Cassiau, A., Peteri-Brunback, B., Meijer, L., Levi, F., Teboul, M. & Delaunay, F. (2014). Functional genomics identify Birc5/survivin as a candidate gene involved in the chronotoxicity of cyclin-dependent kinase inhibitors. Cell Cycle 13, 984–91.CrossRefGoogle ScholarPubMed
Sun, S.C., Xiong, B., Lu, S.S. & Sun, Q.Y. (2008). MEK1/2 is a critical regulator of microtubule assembly and spindle organization during rat oocyte meiotic maturation. Mol. Reprod. Dev. 75, 1542–8.CrossRefGoogle ScholarPubMed
Tang, D.W., Fang, Y., Liu, Z.X., Wu, Y., Wang, X.L., Zhao, S., Han, G.C. & Zeng, S.M. (2013). The disturbances of endoplasmic reticulum calcium homeostasis caused by increased intracellular reactive oxygen species contributes to fragmentation in aged porcine oocytes. Biol. Reprod. 89, 124.CrossRefGoogle ScholarPubMed
Terret, M.E., Lefebvre, C., Djiane, A., Rassinier, P., Moreau, J., Maro, B. & Verlhac, M.H. (2003). DOC1R: a MAP kinase substrate that control microtubule organization of metaphase II mouse oocytes. Development 130, 5169–77.CrossRefGoogle ScholarPubMed
Tu, G., Zhang, Y.F., Wei, W., Li, L., Zhang, Y., Yang, J. & Xing, Y. (2016). Allicin attenuates H2O2-induced cytotoxicity in retinal pigmented epithelial cells by regulating the levels of reactive oxygen species. Mol. Med. Rep. 13, 2320–6.CrossRefGoogle ScholarPubMed
Ueno, S., Kurome, M., Ueda, H., Tomii, R., Hiruma, K. & Nagashima, H. (2005). Effects of maturation conditions on spindle morphology in porcine MII oocytes. J. Reprod. Dev. 51, 405–10.CrossRefGoogle ScholarPubMed
Wang, W., Du, Z., Nimiya, Y., Sukamtoh, E., Kim, D. & Zhang, G. (2016). Allicin inhibits lymphangiogenesis through suppressing activation of vascular endothelial growth factor (VEGF). receptor. J. Nutri. Biochem. 29, 83–9.CrossRefGoogle ScholarPubMed
Yan, L., Luo, H., Gao, X., Liu, K. & Zhang, Y. (2012). Vascular endothelial growth factor-induced expression of its receptors and activation of the MAPK signaling pathway during ovine oocyte maturation in vitro . Theriogenology 78, 1350–60.CrossRefGoogle ScholarPubMed
Zhang, W. & Liu, H.T. (2002). MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 12, 9–18.CrossRefGoogle ScholarPubMed