Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-24T16:37:47.605Z Has data issue: false hasContentIssue false
  • English
  • Français

Supplementation of kaempferol to in vitro maturation medium regulates oxidative stress and enhances subsequent embryonic development in vitro

Published online by Cambridge University Press:  30 October 2019

Yuhan Zhao Open the ORCID record for Yuhan Zhao [Opens in a new window] ,
Yongnan Xu ,
Yinghua Li ,
Qingguo Jin ,
Jingyu Sun ,
Zhiqiang E  and
Qingshan Gao
Yuhan Zhao
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000 China; and Engineering Research Centre of Yanbian Yellow Cattle Resources Reservation, Yanji, 133000China
Yongnan Xu
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000 China; and Engineering Research Centre of Yanbian Yellow Cattle Resources Reservation, Yanji, 133000China
Yinghua Li
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000 China; and Engineering Research Centre of Yanbian Yellow Cattle Resources Reservation, Yanji, 133000China
Qingguo Jin
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000 China; and Engineering Research Centre of Yanbian Yellow Cattle Resources Reservation, Yanji, 133000China
Jingyu Sun
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000 China; and Engineering Research Centre of Yanbian Yellow Cattle Resources Reservation, Yanji, 133000China
Zhiqiang E
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000 China; and Engineering Research Centre of Yanbian Yellow Cattle Resources Reservation, Yanji, 133000China
Qingshan Gao*
Affiliation:
College of Agriculture, Yanbian University, Yanji, 133000 China; and Engineering Research Centre of Yanbian Yellow Cattle Resources Reservation, Yanji, 133000China
*
Author for correspondence: Qingshan Gao, College of Agriculture, Yanbian University, Yanji City, Jilin Province, China. Tel: +86 0433 2436435. Fax: +86 433 243 5638. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Kaempferol (KAE) is one of the most common dietary flavonols possessing biological activities such as anticancer, anti-inflammatory and antioxidant effects. Although previous studies have reported the biological activity of KAE on a variety of cells, it is not clear whether KAE plays a similar role in oocyte and embryo in vitro culture systems. This study investigated the effect of KAE addition to in vitro maturation on the antioxidant capacity of embryos in porcine oocytes after parthenogenetic activation. The effects of kaempferol on oocyte quality in porcine oocytes were studied based on the expression of related genes, reactive oxygen species, glutathione and mitochondrial membrane potential as criteria. The rate of blastocyst formation was significantly higher in oocytes treated with 0.1 µm KAE than in control oocytes. The mRNA level of the apoptosis-related gene Caspase-3 was significantly lower in the blastocysts derived from KAE-treated oocytes than in the control group and the mRNA expression of the embryo development-related genes COX2 and SOX2 was significantly increased in the KAE-treated group compared with that in the control group. Furthermore, the level of intracellular reactive oxygen species was significantly decreased and that of glutathione was significantly increased after KAE treatment. Mitochondrial membrane potential (ΔΨm) was increased and the activity of Caspase-3 was significantly decreased in the KAE-treated group compared with that in the control group. Taken together, these results suggested that KAE is beneficial for the improvement of embryo development by inhibiting oxidative stress in porcine oocytes.

Keywords

AntioxidantEmbryonic developmentKaempferolParthenogeneticPorcine
Type
Research Article
Information
Zygote , Volume 28 , Issue 1 , February 2020 , pp. 59 - 64
Copyright
© Cambridge University Press 2019 

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.)

References

Aiyer, HS, Bouker, KB, Cook, KL, Facey, CO, Hu, R, Schwartz, JL, Shajahan, AN, Hilakivi-Clarke, L and Clarke, R (2012) Interaction of dietary polyphenols with molecular signaling pathways of antiestrogen resistance: possible role in breast cancer recurrence. Horm Mol Biol Clin Investig 9, 127–41.Google ScholarPubMed
Chappel, S (2013) The role of mitochondria from mature oocyte to viable blastocyst. Obstet Gynecol Int 18, 3024.Google Scholar
Cheong, SA, Kim, E, Kwak, SS, Jeon, Y and Hyun, SH (2015) Improvement in the blastocyst quality and efficiency of putative embryonic stem cell line derivation from porcine embryos produced in vitro using a novel culturing system. Mol Med Rep 12, 2140–8.CrossRefGoogle ScholarPubMed
Choi, EM (2011) Kaempferol protects MC3T3-E1 cells through antioxidant effect and regulation of mitochondrial function. Food Chem Toxicol 49, 1800–5.CrossRefGoogle ScholarPubMed
Cimen, H, Han, MJ, Yang, Y, Tong, Q, Koc, H and Koc, EC (2010) Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria. Biochemistry 49, 304–11.CrossRefGoogle ScholarPubMed
Czarny, P, Wigner, P, Galecki, P and Sliwinski, T (2018) The interplay between inflammation, oxidative stress, DNA damage, DNA repair and mitochondrial dysfunction in depression. Prog Neuropsychopharmacol Biol Psychiatry 80, 309–21.CrossRefGoogle ScholarPubMed
de Souza-Fabjan, JM, Panneau, B, Duffard, N, Locatelli, Y, de Figueiredo, JR, Freitas, V.J and Mermillod, P (2014) In vitro production of small ruminant embryos: late improvements and further research. Theriogenology 81, 1149–62.CrossRefGoogle ScholarPubMed
Gilchrist, RB, Luciano, AM, Richani, D, Zeng, HT, Wang, X, Vos, MD, Sugimura, S, Smitz, J, Richard, FJ and Thompson, JG (2016) Oocyte maturation and quality: role of cyclic nucleotides. Reproduction 152, R143–57.CrossRefGoogle ScholarPubMed
Guo, Z, Liao, Z, Huang, L, Liu, D, Yin, D and He, M (2015) Kaempferol protects cardiomyocytes against anoxia/reoxygenation injury via mitochondrial pathway mediated by SIRT1. Eur J Pharmacol 761, 245–53.CrossRefGoogle ScholarPubMed
Kala, M, Shaikh, MV and Nivsarkar, M (2017) Equilibrium between anti-oxidants and reactive oxygen species: a requisite for oocyte development and maturation. Reprod Med Biol 16, 28–35.CrossRefGoogle ScholarPubMed
Khazaei, M and Aghaz, F (2017) Reactive oxygen species generation and use of antioxidants during in vitro maturation of oocytes. Int J Fertil Steril 11, 63–70.Google ScholarPubMed
Kim, E, Jeon, Y, Kim, DY, Lee, E and Hyun, SH (2015) Antioxidative effect of carboxyethylgermanium sesquioxide (Ge-132) on IVM of porcine oocytes and subsequent embryonic development after parthenogenetic activation and IVF. Theriogenology 84, 226–36.CrossRefGoogle ScholarPubMed
Kim, SH, Park, JG, Lee, J, Yang, WS, Park, GW, Kim, HG, Yi, YS, Baek, KS, Sung, NY, Hossen, MJ, Lee, MN, Kim, JH and Cho, JY (2015b) The dietary flavonoid kaempferol mediates anti-inflammatory responses via the Src, Syk, IRAK1 and IRAK4 molecular targets. Mediators Inflamm 90, 41–2.CrossRefGoogle Scholar
Kim, SJ, Koo, OJ, Kwon, DK, Kang, JT, Park, SJ, Gomez, MN, Atikuzzaman, M, Jang, G and Lee, BC (2014) Replacement of glutamine with the dipeptide derivative alanyl-glutamine enhances in vitro maturation of porcine oocytes and development of embryos. Zygote 22, 286–9.CrossRefGoogle ScholarPubMed
Li, HS, Zhou, YN, Li, L, Li, SF, Long, D, Chen, XL, Zhang, JB, Feng, L and Li, YP (2019) HIF-1α protects against oxidative stress by directly targeting mitochondria. Redox Biol 14, 101109.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–8.CrossRefGoogle Scholar
Lonergan, P and Fair, T (2016) Maturation of oocytes in vitro . Annu Rev Anim Biosci 4, 255–68.CrossRefGoogle ScholarPubMed
Mata, A, Marques, D, Martinez-Burgos, MA, Silveira, J, Marques, J, Mesquita, MF, Pariente, JA, Salido, GM and Singh, J (2008) Effect of hydrogen peroxide on secretory response, calcium mobilisation and caspase-3 activity in the isolated rat parotid gland. Mol Cell Biochem 319, 23–31.CrossRefGoogle ScholarPubMed
Miao, Y, Zhou, C, Bai, Q, Cui, Z, ShiYang, X, Lu, Y, Zhang, M, Dai, X and Xiong, B (2018) The protective role of melatonin in porcine oocyte meiotic failure caused by the exposure to benzo(a)pyrene. Hum Reprod 33, 116–27.CrossRefGoogle ScholarPubMed
Mishra, A, Reddy, IJ, Gupta, PS and Mondal, S (2017) Expression of apoptotic and antioxidant enzyme genes in sheep oocytes and in vitro produced embryos. Anim Biotechnol 28, 18–25.CrossRefGoogle ScholarPubMed
Ondricek, AJ, Kashyap, AK, Thamake, SI and Vishwanatha, JK (2012) A comparative study of phytoestrogen action in mitigating apoptosis induced by oxidative stress. In vivo 26, 765–75.Google ScholarPubMed
Prasad, S, Tiwari, M, Pandey, AN, Shrivastav, TG and Chaube, SK (2016) Impact of stress on oocyte quality and reproductive outcome. J Biomed Sci 23, 36.CrossRefGoogle ScholarPubMed
Qiu, W, Lin, J, Zhu, Y, Zhang, J, Zeng, L, Su, M and Tian, Y (2017) Kaempferol modulates DNA methylation and downregulates DNMT3B in bladder cancer. Cell Physiol Biochem 41, 1325–35.CrossRefGoogle ScholarPubMed
Ramalho-Santos, J, Amaral, S and Oliveira, PJ (2008) Diabetes and the impairment of reproductive function: possible role of mitochondria and reactive oxygen species. Curr Diabetes Rev 4, 46–54.CrossRefGoogle Scholar
Saw, CL, Guo, Y, Yang, AY, Paredes-Gonzalez, X, Ramirez, C, Pung, D and Kong, AN (2014) The berry constituents quercetin, kaempferol and pterostilbene synergistically attenuate reactive oxygen species: involvement of the Nrf2-ARE signaling pathway. Food Chem Toxicol 72, 303–11.CrossRefGoogle ScholarPubMed
Sinha, K, Das, J, Pal, PB and Sil, PC (2013) Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 87, 1157–80.CrossRefGoogle Scholar
Spinaci, M, Bucci, D, Muccilli, V, Cardullo, N, Nerozzi, C and Galeati, G (2019) A polyphenol-rich extract from an oenological oak-derived tannin influences in vitro maturation of porcine oocytes. Theriogenology 129, 82–9.CrossRefGoogle ScholarPubMed
Wang, FX, Liang, JH, Zhang, H, Wang, ZH, Wan, Q, Tan, CP, Ji, LN and Mao, Z (2019) Mitochondria-accumulating rhenium (I) tricarbonyl complexes induce cell death via irreversible oxidative stress and glutathione metabolism disturbance. ACS Appl Mater Interfaces 11, 13123–33.CrossRefGoogle ScholarPubMed
Wang, Z, Figueiredo-Pereira, C, Oudot, C, Vieira, HL and Brenner, C (2017) Mitochondrion: a common organelle for distinct cell deaths? Int Rev Cell Mol Biol 331, 245–87.CrossRefGoogle ScholarPubMed
Wei, S, Shen, X, Gong, Z, Deng, Y, Lai, L and Liang, H (2017) FSHR and LHR expression and signaling as well as maturation and apoptosis of cumulus–oocyte complexes following treatment with FSH receptor binding inhibitor in sheep. Cell Physiol Biochem 43, 660–9.CrossRefGoogle Scholar
White, MD, Angiolini, JF, Alvarez, YD, Kaur, G, Zhao, ZW, Mocskos, E, Bruno, L, Bissiere, S, Levi, V and Plachta, N (2016) Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo. Cell 165, 75–87.CrossRefGoogle ScholarPubMed
Wongsrikeao, P, Nagai, T, Agung, B, Taniguchi, M, Kunishi, M, Suto, S and Otoi, T (2007) Improvement of transgenic cloning efficiencies by culturing recipient oocytes and donor cells with antioxidant vitamins in cattle. Mol Reprod Dev 74, 694–702.CrossRefGoogle ScholarPubMed
Yang, QS, He, LP, Zhou, XL, Zhao, Y, Shen, J, Xu, P and Ni, SZ (2015) Kaempferol pretreatment modulates systemic inflammation and oxidative stress following hemorrhagic shock in mice. Chin Med 10, 6.CrossRefGoogle ScholarPubMed
Yang, S, Si, L, Jia, Y, Jian, W, Yu, Q, Wang, M and Lin, R (2019) Kaempferol exerts anti-proliferative effects on human ovarian cancer cells by inducing apoptosis, G0/G1 cell cycle arrest and modulation of MEK/ERK and STAT3 pathways. J BUON 24, 975–81.Google ScholarPubMed
Yao, X, Jiang, H, Liang, S, Shen, X, Gao, Q, Xu, YN and Kim, NH (2018) Laminarin enhances the quality of aged pig oocytes by reducing oxidative stress. J Reprod Dev 64, 489–94.CrossRefGoogle ScholarPubMed
Zhang, G, Yang, W, Jiang, F, Zou, P, Zeng, Y, Ling, X, Zhou, Z, Cao, J and Ao, L (2019) PERK regulates Nrf2/ARE antioxidant pathway against dibutyl phthalate-induced mitochondrial damage and apoptosis dependent of reactive oxygen species in mouse spermatocyte-derived cells. Toxicol Lett 308, 24–33.CrossRefGoogle ScholarPubMed