Baicalin improves IVM of pig oocytes and subsequent preimplantation embryo development by inhibiting apoptosis
Qing Guo A * , Mei-Fu Xuan A * , Zhao-Bo Luo A , Jun-Xia Wang A , Song-Shan Jin A , Xi-Jun Yin
A B and Jin-Dan Kang A B
+ Author Affiliations
- Author Affiliations
A Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, No. 977 Gongyuan Street, Yanji, Jilin 133002, China.
B Corresponding authors. Emails: yinxj33@msn.com; kangjindan@hotmail.com
Reproduction, Fertility and Development 31(5) 983-992 https://doi.org/10.1071/RD18333
Submitted: 20 August 2018 Accepted: 25 December 2018 Published: 1 March 2019
Abstract
Baicalin, a monomer of flavonoids extracted from dried roots of Scutellaria baicalensis, is used to treat female infertility. However, the effect of baicalin on oocyte maturation is unknown. In this study we investigated the effects of baicalin on the IVM of pig oocytes and subsequent embryo development following parthenogenetic activation (PA). We found that 0.1 µg mL−1 baicalin significantly (P < 0.05) increased the IVM rate of oocytes compared with the non-treatment (control) group by reducing levels of reactive oxygen species (ROS). In addition, the mRNA expression of genes related to nuclear maturation and cumulus cell expansion, mitochondrial membrane potential and ATP content was significantly (P < 0.05) higher in baicalin-treated than control oocytes. To determine whether baicalin treatment during IVM of pig oocytes improves subsequent development of PA embryos, we measured the cleavage and blastocyst formation rates, as well as the number of cells per blastocyst. All these parameters were significantly (P < 0.05) higher in the baicalin-treated than control group. In conclusion, this study demonstrates that baicalin improves pig oocyte maturation and subsequent embryo development in vitro by inhibiting production of ROS and reducing apoptosis in oocytes.
Additional keywords: parthenogenetic activation, reactive oxygen species.
References
Abdulhasan, M. K., Li, Q., Dai, J., Abu-Soud, H. M., Puscheck, E. E., and Rappolee, D. A. (2017). CoQ10 increases mitochondrial mass and polarization, ATP and Oct4 potency levels, and bovine oocyte MII during IVM while decreasing AMPK activity and oocyte death. J. Assist. Reprod. Genet. 34, 1595–1607.| CoQ10 increases mitochondrial mass and polarization, ATP and Oct4 potency levels, and bovine oocyte MII during IVM while decreasing AMPK activity and oocyte death.Crossref | GoogleScholarGoogle Scholar | 28900834PubMed |
Agarwal, S., Sharma, S., Agrawal, V., and Roy, N. (2005). Caloric restriction augments ROS defense in S. cerevisiae, by a Sir2p independent mechanism. Free Radic. Res. 39, 55–62.
| Caloric restriction augments ROS defense in S. cerevisiae, by a Sir2p independent mechanism.Crossref | GoogleScholarGoogle Scholar | 15875812PubMed |
Dou, J., Wang, Z., Ma, L., Peng, B., Mao, K., Li, C., Su, M., Zhou, C., and Peng, G. (2018). Baicalein and baicalin inhibit colon cancer using two distinct fashions of apoptosis and senescence. Oncotarget 9, 20089–20102.
| Baicalein and baicalin inhibit colon cancer using two distinct fashions of apoptosis and senescence.Crossref | GoogleScholarGoogle Scholar | 29732005PubMed |
Fissore, R. A., Kurokawa, M., Knott, J., Zhang, M., and Smyth, J. (2002). Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 124, 745–754.
| Mechanisms underlying oocyte activation and postovulatory ageing.Crossref | GoogleScholarGoogle Scholar | 12530912PubMed |
Guo, M., Cao, Y., Wang, T., Song, X., Liu, Z., Zhou, E., Deng, X., Zhang, N., and Yang, Z. (2014). Baicalin inhibits Staphylococcus aureus-induced apoptosis by regulating TLR2 and TLR2-related apoptotic factors in the mouse mammary glands. Eur. J. Pharmacol. 723, 481–488.
| Baicalin inhibits Staphylococcus aureus-induced apoptosis by regulating TLR2 and TLR2-related apoptotic factors in the mouse mammary glands.Crossref | GoogleScholarGoogle Scholar | 24211786PubMed |
Guo, Q., Jin, L., Zhu, H. Y., Xing, X. X., Xuan, M. F., Luo, Q. R., Zhang, G. L., Luo, Z. B., Wang, J. X., and Yin, X. J. (2018). The cyclin-dependent kinase inhibitor, JNJ-7706621, improves in vitro developmental competence of porcine parthenogenetic activation and somatic cell nuclear transfer embryos. Reprod. Fertil. Dev. 30, 1002–1010.
| The cyclin-dependent kinase inhibitor, JNJ-7706621, improves in vitro developmental competence of porcine parthenogenetic activation and somatic cell nuclear transfer embryos.Crossref | GoogleScholarGoogle Scholar |
Harvey, A. J., Gibson, T. C., Quebedeaux, T. M., and Brenner, C. A. (2007). Impact of assisted reproductive technologies: a mitochondrial perspective of cytoplasmic transplantation. Curr. Top. Dev. Biol. 77, 229–249.
| Impact of assisted reproductive technologies: a mitochondrial perspective of cytoplasmic transplantation.Crossref | GoogleScholarGoogle Scholar | 17222706PubMed |
Hassold, T., and Hunt, P. (2001). To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2, 280–291.
| To err (meiotically) is human: the genesis of human aneuploidy.Crossref | GoogleScholarGoogle Scholar | 11283700PubMed |
Holt, J. E., Lane, S. I. R., and Jones, K. T. (2013). Chapter seven – the control of meiotic maturation in mammalian oocytes. Curr. Top. Dev. Biol. 102, 207–226.
| Chapter seven – the control of meiotic maturation in mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 23287034PubMed |
Hou, J., Wang, J., Zhang, P., Li, D., Zhang, C., Zhao, H., Fu, J., Wang, B., and Liu, J. (2012). Baicalin attenuates proinflammatory cytokine production in oxygen–glucose deprived challenged rat microglial cells by inhibiting TLR4 signaling pathway. Int. Immunopharmacol. 14, 749–757.
| Baicalin attenuates proinflammatory cytokine production in oxygen–glucose deprived challenged rat microglial cells by inhibiting TLR4 signaling pathway.Crossref | GoogleScholarGoogle Scholar | 23116637PubMed |
Huang, W. H., Lee, A. R., and Yang, C. H. (2006). Antioxidative and anti-inflammatory activities of polyhydroxyflavonoids of Scutellaria baicalensis GEORGI. Biosci. Biotechnol. Biochem. 70, 2371–2380.
| 17031041PubMed |
Iwata, H., Goto, H., Tanaka, H., Sakaguchi, Y., Kimura, K., Kuwayama, T., and Monji, Y. (2011). Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev. 23, 424–432.
| Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 21426860PubMed |
Jin, J. X., Lee, S., Khoirinaya, C., Oh, A., Kim, G. A., and Lee, B. C. (2016). Supplementation with spermine during in vitro maturation of porcine oocytes improves early embryonic development after parthenogenetic activation and somatic cell nuclear transfer. J. Anim. Sci. 94, 963–970.
| Supplementation with spermine during in vitro maturation of porcine oocytes improves early embryonic development after parthenogenetic activation and somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 27065258PubMed |
Jin, J. X., Lee, S., Taweechaipaisankul, A., Kim, G. A., and Lee, B. C. (2017). Melatonin regulates lipid metabolism in porcine oocytes. J. Pineal Res. 62, e12388.
| Melatonin regulates lipid metabolism in porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 28095627PubMed |
Jin, J. X., Lee, S., Emn, S., Taweechaipaisankul, A., Kim, G. A., Han, H. J., Ahn, C., and Lee, B. C. (2018). A potential role of knockout serum replacement as a porcine follicular fluid substitute for in vitro maturation: lipid metabolism approach. J. Cell. Physiol. 233, 6984–6995.
| A potential role of knockout serum replacement as a porcine follicular fluid substitute for in vitro maturation: lipid metabolism approach.Crossref | GoogleScholarGoogle Scholar | 29345310PubMed |
Lee, S., Jin, J. X., Khoirinaya, C., Kim, G. A., and Lee, B. C. (2016). Lanosterol influences cytoplasmic maturation of pig oocytes in vitro and improves preimplantation development of cloned embryos. Theriogenology 85, 575–584.
| Lanosterol influences cytoplasmic maturation of pig oocytes in vitro and improves preimplantation development of cloned embryos.Crossref | GoogleScholarGoogle Scholar | 26494176PubMed |
Lee, S., Jin, J. X., Taweechaipaisankul, A., Kim, G. A., Ahn, C., and Lee, B. C. (2017). Melatonin influences the sonic hedgehog signaling pathway in porcine cumulus oocyte complexes. J. Pineal Res. 63, e12424.
| Melatonin influences the sonic hedgehog signaling pathway in porcine cumulus oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 28658519PubMed |
Luo, Z. B., Jin, L., Guo, Q., Wang, J. X., Xing, X. X., Xuan, M. F., Luo, Q. R., Zhang, G. L., Yin, X. J., and Kang, J. D. (2018). Cotreatment with RepSox and LBH589 improves the in vitro developmental competence of porcine somatic cell nuclear transfer embryos. Reprod. Fertil. Dev. 30, 1342–1351.
| Cotreatment with RepSox and LBH589 improves the in vitro developmental competence of porcine somatic cell nuclear transfer embryos.Crossref | GoogleScholarGoogle Scholar |
Ma, A. T., Zhong, X. H., Liu, Z. M., Shi, W. Y., Du, J., Zhai, X. H., Zhang, T., and Meng, L. G. (2009). Protective effects of baicalin against bromocriptine induced abortion in mice. Am. J. Chin. Med. 37, 85–95.
| Protective effects of baicalin against bromocriptine induced abortion in mice.Crossref | GoogleScholarGoogle Scholar | 19222114PubMed |
Martin, J., and Dusek, J. (2002). [The Baikal scullcap (Scutellaria baicalensis Georgi) – a potential source of new drugs.] Ceska Slov. Farm. 51, 277–283.
| 12501487PubMed |
Nagano, M., and Katagiri, S. Y. (2006). ATP content and maturational/developmental ability of bovine oocytes with various cytoplasmic morphologies. Zygote 14, 299–304.
| ATP content and maturational/developmental ability of bovine oocytes with various cytoplasmic morphologies.Crossref | GoogleScholarGoogle Scholar | 17266788PubMed |
Park, H. J., Park, J. Y., Kim, J. W., Yang, S. G., Jung, J. M., Kim, M. J., Kang, M. J., Cho, Y. H., Wee, G., and Yang, H. Y. (2018). Melatonin improves the meiotic maturation of porcine oocytes by reducing endoplasmic reticulum stress during in vitro maturation. J. Pineal Res. 64, e12458.
| Melatonin improves the meiotic maturation of porcine oocytes by reducing endoplasmic reticulum stress during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 29149522PubMed |
Qi, X., Li, H., Cong, X., Wang, X., Jiang, Z., Cao, R., and Tian, W. (2016). Baicalin increases developmental competence of mouse embryos in vitro by inhibiting cellular apoptosis and modulating HSP70 and DNMT expression. J. Reprod. Dev. 62, 561–569.
| Baicalin increases developmental competence of mouse embryos in vitro by inhibiting cellular apoptosis and modulating HSP70 and DNMT expression.Crossref | GoogleScholarGoogle Scholar | 27478062PubMed |
Shi, L., Hao, Z., Zhang, S., Wei, M., Lu, B., Wang, Z., and Ji, L. (2018a). Baicalein and baicalin alleviate acetaminophen-induced liver injury by activating Nrf2 antioxidative pathway: the involvement of ERK1/2 and PKC. Biochem. Pharmacol. 150, 9–23.
| Baicalein and baicalin alleviate acetaminophen-induced liver injury by activating Nrf2 antioxidative pathway: the involvement of ERK1/2 and PKC.Crossref | GoogleScholarGoogle Scholar | 29338970PubMed |
Shi, M., Cheng, J., He, Y., Jiang, Z., Bodinga, B. M., Liu, B., Chen, H., and Li, Q. (2018b). Effect of FH535 on in vitro maturation of porcine oocytes by inhibiting WNT signaling pathway. Anim. Sci. J. 89, 631–639.
| Effect of FH535 on in vitro maturation of porcine oocytes by inhibiting WNT signaling pathway.Crossref | GoogleScholarGoogle Scholar | 29284185PubMed |
Sommer, C. A., Stadtfeld, M., Murphy, G. J., Hochedlinger, K., Kotton, D. N., and Mostoslavsky, G. (2009). Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 27, 543–549.
| Induced pluripotent stem cell generation using a single lentiviral stem cell cassette.Crossref | GoogleScholarGoogle Scholar | 19096035PubMed |
Su, Y. Q., Wu, X., O’Brien, M. J., Pendola, F. L., Denegre, J. N., Matzuk, M. M., and Eppig, J. J. (2004). Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte–cumulus cell complex in mice: genetic evidence for an oocyte–granulosa cell regulatory loop. Dev. Biol. 276, 64–73.
| Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte–cumulus cell complex in mice: genetic evidence for an oocyte–granulosa cell regulatory loop.Crossref | GoogleScholarGoogle Scholar | 15531364PubMed |
Tian, X. Y., Cheung, L. M., Leung, K., Qi, C., Deng, B., Deng, P. X., and Xu, M. (2009). The effects of Scutellaria baicalensis extract on embryonic development in mice. Birth Defects Res. B Dev. Reprod. Toxicol. 86, 79–84.
| The effects of Scutellaria baicalensis extract on embryonic development in mice.Crossref | GoogleScholarGoogle Scholar | 19283861PubMed |
Van Blerkom, J. (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.
| Mitochondrial function in the human oocyte and embryo and their role in developmental competence.Crossref | GoogleScholarGoogle Scholar | 20933103PubMed |
Wallace, D. C., Fan, W., and Procaccio, V. (2010). Mitochondrial energetics and therapeutics. Annu. Rev. Pathol. 5, 297–348.
| Mitochondrial energetics and therapeutics.Crossref | GoogleScholarGoogle Scholar | 20078222PubMed |
Wang, X., Zhao, Y., and Zhong, X. (2014). Protective effects of baicalin on decidua cells of LPS-induced mice abortion. J. Immunol. Res. 2014, 859812.
| Protective effects of baicalin on decidua cells of LPS-induced mice abortion.Crossref | GoogleScholarGoogle Scholar | 25386564PubMed |
Wang, H., Zhang, Y., Bai, R., Wang, M., and Du, S. (2016). Baicalin attenuates alcoholic liver injury through modulation of hepatic oxidative stress, inflammation and sonic hedgehog pathway in rats. Cell. Physiol. Biochem. 39, 1129–1140.
| Baicalin attenuates alcoholic liver injury through modulation of hepatic oxidative stress, inflammation and sonic hedgehog pathway in rats.Crossref | GoogleScholarGoogle Scholar | 27576501PubMed |
Wen, Y. F., Zhao, J. Q., Bhadauria, M., and Nirala, S. K. (2013). Baicalin prevents cadmium induced hepatic cytotoxicity, oxidative stress and histomorphometric alterations. Exp. Toxicol. Pathol. 65, 189–196.
| Baicalin prevents cadmium induced hepatic cytotoxicity, oxidative stress and histomorphometric alterations.Crossref | GoogleScholarGoogle Scholar | 21924596PubMed |
Wigglesworth, K., Lee, K. B., O’Brien, M. J., Peng, J., Matzuk, M. M., and Eppig, J. J. (2013). Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes. Proc. Natl Acad. Sci. USA 110, E3723–E3729.
| Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 23980176PubMed |
Williams, J. B., Shin, T., Ling, L., Floresfoxworth, G., Romano, J., Bluemcclendon, A., Kraemer, D., and Westhusin, M. E. (2006). Cloning of exotic/endangered species: desert bighorn sheep. Methods Mol. Biol. 348, 169–181.
| Cloning of exotic/endangered species: desert bighorn sheep.Crossref | GoogleScholarGoogle Scholar | 16988379PubMed |
Wu, G. Q., Jia, B. Y., Li, J. J., Fu, X. W., Zhou, G. B., Hou, Y. P., and Zhu, S. E. (2011). l-Carnitine enhances oocyte maturation and development of parthenogenetic embryos in pigs. Theriogenology 76, 785–793.
| l-Carnitine enhances oocyte maturation and development of parthenogenetic embryos in pigs.Crossref | GoogleScholarGoogle Scholar | 21705056PubMed |
Xia, L., and Zhang, L. (2007). Mechanism underlying regualtion and role of maturation promoting factor during oocyte maturation. Chinese J. Dis. Control Prevent. 11, 614–617.
Yang, M. Y., and Rajamahendran, R. (2002). Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim. Reprod. Sci. 70, 159–169.
| Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 11943486PubMed |
Yang, J., Yang, X., and Li, M. (2012). Baicalin, a natural compound, promotes regulatory T cell differentiation. BMC Complement. Altern. Med. 12, 64.
| Baicalin, a natural compound, promotes regulatory T cell differentiation.Crossref | GoogleScholarGoogle Scholar | 22591709PubMed |
Zeng, J., Jiang, M., Wu, X., Diao, F., Qiu, D., Hou, X., Wang, H., Li, L., Li, C., and Ge, J. (2018). SIRT4 is essential for metabolic control and meiotic structure during mouse oocyte maturation. Aging Cell 17, e12789.
| SIRT4 is essential for metabolic control and meiotic structure during mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar |
Zhang, Y. M., Zhang, Y. Y., Bulbul, A., Shan, X., Wang, X. Q., and Yan, Q. (2015). Baicalin promotes embryo adhesion and implantation by upregulating fucosyltransferase IV (FUT4) via Wnt/beta-catenin signaling pathway. FEBS Lett. 589, 1225–1233.
| Baicalin promotes embryo adhesion and implantation by upregulating fucosyltransferase IV (FUT4) via Wnt/beta-catenin signaling pathway.Crossref | GoogleScholarGoogle Scholar | 25896022PubMed |
Zhong, X. H., Shi, W. Y., Ma, A. T., Gong, X. C., Zhai, X. H., Zhang, T., and Wang, X. D. (2008). Effects of Radix scutellariae and Rhizoma atractylodis on LPS-induced abortion and the uterine IL-10 contents in mice. Am. J. Chin. Med. 36, 141–148.
| Effects of Radix scutellariae and Rhizoma atractylodis on LPS-induced abortion and the uterine IL-10 contents in mice.Crossref | GoogleScholarGoogle Scholar | 18306457PubMed |
