Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Polydatin improves the developmental competence of bovine embryos in vitro via induction of sirtuin 1 (Sirt1)

Imran Khan A , Sung Woo Kim C , Kyung-Lim Lee A , Seok-Hwan Song A , Ayman Mesalam A , M. M. R. Chowdhury A , Zia Uddin D , Ki Hun Park B D and Il-Keun Kong A B E
+ Author Affiliations
- Author Affiliations

A Department of Animal Science, Division of Applied Life Science (BK21 Plus), Gyeongsang National University, Jinju 52828, Gyeongnam Province, Republic of Korea.

B Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 52828, Gyeongnam Province, Republic of Korea.

C Animal Genetic Resources Research Center, National Institute of Animal Science, Rural Development Administration, Namwon 55717, Republic of Korea.

D Division of Applied Life Science (BK21 Plus), Gyeongsang National University, Jinju 52828, Gyeongnam Province, Republic of Korea.

E Corresponding author. Email: ikong7900@gmail.com

Reproduction, Fertility and Development 29(10) 2011-2020 https://doi.org/10.1071/RD16302
Submitted: 4 August 2016  Accepted: 5 December 2016   Published: 14 February 2017

Abstract

The aim of the present study was to investigate the beneficial effect of polydatin (PD), the glycoside form of resveratrol, on embryo development in vitro. Oocytes were aspirated from ovaries of Korean Hanwoo cows and cultured until Day 8 in a humidified atmosphere of 5% CO2 in air at 38.5°C. Protein and gene expression levels were determined through confocal microscopy and reverse transcription–polymerase chain reaction respectively, whereas the number of total and apoptotic cells in Day 8 blastocysts was determined using Hoechst 33342 staining and terminal deoxyribonucleotidyl transferase-mediated dUTP–digoxigenin nick end-labelling. Of the different concentrations of PD (0.5, 1.0 and 2.0 µM) added to the IVM medium, only 1.0 µM PD significantly improved blastocyst development. Immunofluorescence analysis confirmed that protein levels of sirtuin 1 (Sirt1) increased significantly (P < 0.05) after PD treatment, whereas levels of reactive oxygen species (ROS) were significantly (P < 0.05) decreased, as evidenced by reductions in 8-oxoguanine immunoreactivity. Similarly, protein levels of nuclear factor (NF)-κB and cyclo-oxygenase (COX)-2  were significantly (P < 0.05) lower in the PD-treated group than in the control group. Treatment with 1.0 µM PD reduced gene expression of BCL2-associated X protein, inducible nitric oxide synthase, COX2 and Nfkb, but increased the expression of Sirt1, supporting the immunofluorescence data. PD possesses antioxidant activity and is useful for embryo development in vitro. We conclude that supplementation of IVM medium with PD improves embryo developmental competence via Sirt1.

Additional keywords: apoptosis, blastocyst, oocyte, oxidative stress.


References

Agarwal, A., and Allamaneni, S. S. (2004). Role of free radicals in female reproductive diseases and assisted reproduction. Reprod. Biomed. Online 9, 338–347.
Role of free radicals in female reproductive diseases and assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotFWrtLc%3D&md5=1f41d0468a95e1081bad9aac1760535aCAS |

Alvarez, J. G., and Storey, B. T. (1983). Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility. Biol. Reprod. 29, 548–555.
Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlslShtL4%3D&md5=8dd6e87545ef1f438eef4c2d61ca15ebCAS |

Balaban, R. S., Nemoto, S., and Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483–495.
Mitochondria, oxidants, and aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitVWnurg%3D&md5=63303f199bde0108d1555389dc19a1bbCAS |

Barceló-Fimbres, M., and Seidel, G. E. (2007). Effects of either glucose or fructose and metabolic regulators on bovine embryo development and lipid accumulation in vitro. Mol. Reprod. Dev. 74, 1406–1418.
Effects of either glucose or fructose and metabolic regulators on bovine embryo development and lipid accumulation in vitro.Crossref | GoogleScholarGoogle Scholar |

Bedaiwy, M. A., Falcone, T., Mohamed, M. S., Aleem, A. A. N., Sharma, R. K., Worley, S. E., Thornton, J., and Agarwal, A. (2004). Differential growth of human embryos in vitro: role of reactive oxygen species. Fertil. Steril. 82, 593–600.
Differential growth of human embryos in vitro: role of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFOjs7o%3D&md5=6773f4948262792e000a5991411b0defCAS |

De Maria, S., Scognamiglio, I., Lombardi, A., Amodio, N., Caraglia, M., Cartenì, M., Ravagnan, G., and Stiuso, P. (2013). Polydatin, a natural precursor of resveratrol, induces cell cycle arrest and differentiation of human colorectal Caco-2 cell. J. Transl. Med. 11, 264.
Polydatin, a natural precursor of resveratrol, induces cell cycle arrest and differentiation of human colorectal Caco-2 cell.Crossref | GoogleScholarGoogle Scholar |

Deb, G. K., Dey, S. R., Bang, J. I., Cho, S. J., Park, H. C., Lee, J. G., and Kong, I. K. (2011). 9-Cis retinoic acid improves developmental competence and embryo quality during in vitro maturation of bovine oocytes through the inhibition of oocyte tumor necrosis factor-α gene expression. J. Anim. Sci. 89, 2759–2767.
9-Cis retinoic acid improves developmental competence and embryo quality during in vitro maturation of bovine oocytes through the inhibition of oocyte tumor necrosis factor-α gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFWqtrjE&md5=69e86ee65914f21e1c2e5752bbe6ea7cCAS |

Doherty, A. S., Mann, M. R. W., Tremblay, K. D., Bartolomei, M. S., and Schultz, R. M. (2000). Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62, 1526–1535.
Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsF2hsrc%3D&md5=e5f2b402dfaafa7b724002d82ed29ed3CAS |

Floyd, R. A. (1990). The role of 8-hydroxyguanine in carcinogenesis. Carcinogenesis 11, 1447–1450.
The role of 8-hydroxyguanine in carcinogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmt1Grsbs%3D&md5=47a41eface3c4999454efcc95fdcdc8fCAS |

Fujitani, Y., Kasai, K., Ohtani, S., Nishimura, K., Yamada, M., and Utsumi, K. (1997). Effect of oxygen concentration and free radicals on in vitro development of in vitro-produced bovine embryos. J. Anim. Sci. 75, 483–489.
Effect of oxygen concentration and free radicals on in vitro development of in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsVGks70%3D&md5=13134544281b4dfb64dbb304010e6490CAS |

Gjørret, J. O., Knijn, H. M., Dieleman, S. J., Avery, B., Larsson, L. I., and Maddox-Hyttel, P. (2003). Chronology of apoptosis in bovine embryos produced in vivo and in vitro. Biol. Reprod. 69, 1193–1120.
Chronology of apoptosis in bovine embryos produced in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar |

Gordon, I. (2003). Recovering the bovine oocyte. In ‘Laboratory Production of Cattle Embryos’. 2nd edn. (Eds I. Gabrielle.) pp. 79–111. (CABI: Cambridge, UK.)

Goto, Y., Noda, Y., Mori, T., and Nakano, M. (1993). Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic. Biol. Med. 15, 69–75.
Increased generation of reactive oxygen species in embryos cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlvFOnsL8%3D&md5=18bbe1c29bbf8a3d860bceb33e9f8469CAS |

Guérin, P., El Mouatassim, S., and Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–189.
Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings.Crossref | GoogleScholarGoogle Scholar |

Haddad, J. J. (2002). Antioxidant and prooxidant mechanisms in the regulation of redox(y)-sensitive transcription factors. Cell. Signal. 14, 879–897.
Antioxidant and prooxidant mechanisms in the regulation of redox(y)-sensitive transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVCkurk%3D&md5=ecbd05a9c83d58968b17defa67f71bc8CAS |

Hardy, K., and Spanos, S. (2002). Growth factor expression and function in the human and mouse preimplantation embryo. J. Endocrinol. 172, 221–236.
Growth factor expression and function in the human and mouse preimplantation embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVejt78%3D&md5=5bc8fa11f2497757355c76560b69b23dCAS |

He, Y. D., Liu, Y. T., Lin, Q. X., Zhu, J., Zhang, Y., Wang, L. Y., Ren, X. L., and Ye, X. Y. (2012). Polydatin suppresses UVB-induced cyclooxygenase-2 expression in vitro and in vivo via reduced production of reactive oxygen species. Br. J. Dermatol. 167, 941–944.
Polydatin suppresses UVB-induced cyclooxygenase-2 expression in vitro and in vivo via reduced production of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVSnsL3P&md5=411221956cf2e1dad7ed3476ea7dbe35CAS |

Houtkooper, R. H., Pirinen, E., and Auwerx, J. (2012). Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 13, 225–238.
Sirtuins as regulators of metabolism and healthspan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtlOktbw%3D&md5=c37ac34f07611d6a4e01d6efb98d0d39CAS |

Huang, K., Chen, C., Hao, J., Huang, J., Wang, S., Liu, P., and Huang, H. (2015). Polydatin promotes Nrf2-ARE anti-oxidative pathway through activating Sirt1 to resist AGEs-induced upregulation of fibronetin and transforming growth factor-β1 in rat glomerular messangial cells. Mol. Cell. Endocrinol. 399, 178–189.
Polydatin promotes Nrf2-ARE anti-oxidative pathway through activating Sirt1 to resist AGEs-induced upregulation of fibronetin and transforming growth factor-β1 in rat glomerular messangial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFWgsLrI&md5=d756e6d72cc22b53c09c1e668c853c69CAS |

Jang, M., Cai, L., Udeani, G. O., Slowing, K. V., Thomas, C. F., Beecher, C. W., Fong, H. H., Farnsworth, N. R., Kinghorn, A. D., Mehta, R. G., Moon, R. C., and Pezzuto, J. M. (1997). Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275, 218–220.
Cancer chemopreventive activity of resveratrol, a natural product derived from grapes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXks1Sjtw%3D%3D&md5=fe2027a8d0412b0d1bab1f70a3e35a8eCAS |

Jeong, W. J., Cho, S. J., Lee, H. S., Deb, G. K., Lee, Y. S., Kwon, T. H., and Kong, I. K. (2009). Effect of cytoplasmic lipid content on in vitro developmental efficiency of bovine IVP embryos. Theriogenology 72, 584–589.
Effect of cytoplasmic lipid content on in vitro developmental efficiency of bovine IVP embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptl2ns7s%3D&md5=5687ebf830375b8ed044554abf0ae366CAS |

Ji, H., Zhang, X., Du, Y., Liu, H., and Li, S. (2012). Polydatin modulates inflammation by decreasing NF-kB activation and oxidative stress by increasing Gli1, Ptch1, SOD1 expression and ameliorates blood–brain barrier permeability for its neuroprotective effect in pMCAO rat brain. Brain Res. Bull. 87, 50–59.
Polydatin modulates inflammation by decreasing NF-kB activation and oxidative stress by increasing Gli1, Ptch1, SOD1 expression and ameliorates blood–brain barrier permeability for its neuroprotective effect in pMCAO rat brain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs12gsrrM&md5=7a3ba246186180f4cab815868877a7baCAS |

Jin, W. J., Chen, S. Y., Qian, Z. X., and Shi, X. H. (1993). Effects of polydatin IV on inhibiting respiratory burst of PMNS and scavenging oxygen free radicals. Chin. Pharmacol. Bull 9, 355–357.
| 1:CAS:528:DyaK2MXotVCisb0%3D&md5=d7487bf3fa7752a269bb098f04a5bf3eCAS |

Khan, I., Lee, K. L., Fakruzzaman, M., Song, S. H., Ihsan-ul-Haq, , Mirza, B., Yan, C. G., and Kong, I. K. (2016). Coagulansin-A has beneficial effects on the development of bovine embryos in vitro via HSP70 induction. Biosci. Rep. 36, e00310.
Coagulansin-A has beneficial effects on the development of bovine embryos in vitro via HSP70 induction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XntlOktb0%3D&md5=a6ab1d73623a7d782fb307501917e366CAS |

Li, T., Liu, Y., Li, G., Wang, X., Zeng, Z., Cai, S., Li, F., and Chen, Z. (2014). Polydatin attenuates ipopolysaccharide-induced acute lung injury in rats. Int. J. Clin. Exp. Pathol. 7, 8401–8410.

Liu, Y., Zhang, X. J., Yang, C. H., and Fan, H. G. (2009). Oxymatrine protects rat brains against permanent focal ischemia and downregulates NF-kappaB expression. Brain Res. 1268, 174–180.
Oxymatrine protects rat brains against permanent focal ischemia and downregulates NF-kappaB expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVansrs%3D&md5=8e833918c89ca29db07d346fbf516a7bCAS |

Lonergan, P., Rizos, D., Gutierrez-Adan, A., Fair, T., and Boland, M. P. (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod. Domest. Anim. 38, 259–267.
Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3svis1SrsA%3D%3D&md5=908969d519d8f5d1540979fa2b53df15CAS |

Lou, T., Jiang, W., Xu, D., Chen, T., and Fu, Y. (2015). Inhibitory effects of polydatin on lipopolysaccharide-stimulated RAW 264.7 cells. Inflammation 38, 1213–1220.
Inhibitory effects of polydatin on lipopolysaccharide-stimulated RAW 264.7 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosFamug%3D%3D&md5=0943ea378afbd2115cb66962a6b546f5CAS |

Mancini, A. D., and Di Battista, J. A. (2011). The cardinal role of the phospholipase A(2)/cyclooxygenase-2/prostaglandin E synthase/prostaglandin E(2) (PCPP) axis in inflammostasis. Inflamm. Res. 60, 1083–1092.
The cardinal role of the phospholipase A(2)/cyclooxygenase-2/prostaglandin E synthase/prostaglandin E(2) (PCPP) axis in inflammostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFSju7rM&md5=b84d194f7fd0cfd07e7deeb5a5305ec3CAS |

Matheus, A. S., Coelho, A. M. M., Sampietre, S., Patzina, R., Jukemura, J., Cunha, J. E. M., and Machado, M. C. C. (2007). Effect of inhibition of prostaglandin E2 production on pancreatic infection in experimental acute pancreatitis. HPB (Oxford) 9, 392–397.
Effect of inhibition of prostaglandin E2 production on pancreatic infection in experimental acute pancreatitis.Crossref | GoogleScholarGoogle Scholar |

Mello Filho, A. C., Hoffmann, M. E., and Meneghini, R. (1984). Cell killing and DNA damage by hydrogen peroxide are mediated by intracellular iron. Biochem. J. 218, 273–275.
Cell killing and DNA damage by hydrogen peroxide are mediated by intracellular iron.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhtVSktbk%3D&md5=e7c17e671c23a63875937d1faf8e4aebCAS |

Merton, S. (2000). Morphological evaluation of embryos in domestic species. In ‘Assessment of Mammalian Embryo Quality, Invasive and Non-Invasive Techniques’. (Eds A. V. Soom and M. Boerjan.) pp. 233–255. (Kluwer Academic Press.)

Merton, J. S., de Roos, A. P., Mullaart, E., de Ruigh, L., Kaal, L., Vos, P. L., and Dieleman, S. J. (2003). Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry. Theriogenology 59, 651–674.
Factors affecting oocyte quality and quantity in commercial application of embryo technologies in the cattle breeding industry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38jjslKrtA%3D%3D&md5=ebe38a9f7b6b70b66141266c946fee53CAS |

Michan, S., and Sinclair, D. (2007). Sirtuins in mammals: insights into their biological function. Biochem. J. 404, 1–13.
Sirtuins in mammals: insights into their biological function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXks1ansr4%3D&md5=81b5dfef6659d51cbe49a267bfeb0a6dCAS |

Minami, N., Sasaki, K., Aizawa, A., Miyamoto, M., and Imai, H. (2001). Analysis of gene expression in mouse 2-cell embryos using fluorescein differential display: comparison of culture environments. Biol. Reprod. 64, 30–35.
Analysis of gene expression in mouse 2-cell embryos using fluorescein differential display: comparison of culture environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFCnug%3D%3D&md5=afbe73164c72e14989a4693fe210aa25CAS |

Niemann, H., and Wrenzycki, C. (2000). Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology 53, 21–34.
Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvVyqug%3D%3D&md5=5874eb3ab0e04aa5887cfa57d61b63b4CAS |

Palsamy, P., and Subramanian, S. (2008). Resveratrol, a natural phytoalexin, normalizes hyperglycemia in streptozotocin–nicotinamide induced experimental diabetic rats. Biomed. Pharmacother. 62, 598–605.
Resveratrol, a natural phytoalexin, normalizes hyperglycemia in streptozotocin–nicotinamide induced experimental diabetic rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12ns7vF&md5=0b8983fcceb16480d83bf38a7397bcccCAS |

Pang, Y. W., Sun, Y. Q., Sun, W. J., Du, W. H., Hao, H. S., Zhao, S. J., and Zhu, H. B. (2016). Melatonin inhibits paraquat-induced cell death in bovine preimplantation embryos. J. Pineal Res. 60, 155–166.
Melatonin inhibits paraquat-induced cell death in bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvFegug%3D%3D&md5=e7466b9859fd9074196728f7b66556b6CAS |

Powers, S. K., and Jackson, M. J. (2008). Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol. Rev. 88, 1243–1276.
Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGgtbnP&md5=3cfd81e09d0b5c409287f57a72d3d95bCAS |

Price, N. L., Gomes, A. P., Ling, A. J. Y., Duarte, F. V., Martin-Montalvo, A., North, B. J., Agarwal, B., Ye, L., Ramadori, G., Teodoro, J. S., Hubbard, B. P., Varela, A. T., Davis, J. G., Varamini, B., Hafner, A., Moaddel, R., Rolo, A. P., Coppari, R., Palmeira, C. M., De Cabo, R., Baur, J. A., and Sinclair, D. A. (2012). SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 15, 675–690.
SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmsVCit7w%3D&md5=05b9aab990d0c0568295c2d997088294CAS |

Qiao, H., Chen, H., Dong, Y., Ma, H., Zhao, G., Tang, F., and Li, Z. (2016). Polydatin attenuates H2O2-induced oxidative stress via PKC pathway. Oxid. Med. Cell. Longev. 2016, 5139458.
Polydatin attenuates H2O2-induced oxidative stress via PKC pathway.Crossref | GoogleScholarGoogle Scholar |

Rahman, S., and Islam, R. (2011). Mammalian Sirt1: insights on its biological functions. Cell Commun. Signal. 9, 11.
Mammalian Sirt1: insights on its biological functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsV2gsrg%3D&md5=42e8700b54097b32d7e5489b09f5c1edCAS |

Rosenkrans, C. F., Zeng, G. Q., McNamara, G. T., Schoff, P. K., and First, N. L. (1993). Development of bovine embryos in vitro as affected by energy substrates. Biol. Reprod. 49, 459–462.
Development of bovine embryos in vitro as affected by energy substrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFWk&md5=7cb2253873f40f5f3fe0aa54fac3fdf9CAS |

Sharma, R. K., and Agarwal, A. (1996). Role of reactive oxygen species in male infertility. Urology 48, 835–850.
Role of reactive oxygen species in male infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s7ivFWhtw%3D%3D&md5=75c3884e2182580983f14ff833eb313dCAS |

Sikka, S. C. (2004). Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. J. Androl. 25, 5–18.
Role of oxidative stress and antioxidants in andrology and assisted reproductive technology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslCguw%3D%3D&md5=a52f45a1de06f9a0d7988ac0b0922e41CAS |

Stroud, B. (2011). IETS 2011 Statistics and Data Retrieval Committee report. The year 2010 worldwide statistics of embryo transfer in domestic farm animals. Available at http://www.iets.org/pdf/comm_data/December2011.pdf [verified 13 December 2016].

Velez-Pardo, C., Morales, A. T., Rio, M. J. D., and Olivera-Angel, M. (2007). Endogenously generated hydrogen peroxide induces apoptosis via mitochondrial damage independent of NF-kB and p53 activation in bovine embryos. Theriogenology 67, 1285–1296.
Endogenously generated hydrogen peroxide induces apoptosis via mitochondrial damage independent of NF-kB and p53 activation in bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1OjsL4%3D&md5=d9d20f988fd23eeea4be819195db1925CAS |

Wang, F., Tian, X., Zhang, L., He, C., Ji, P., Li, Y., Tan, D., and Liu, G. (2014a). Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Fertil. Steril. 101, 577–586.e1.
Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVWjtbjN&md5=010898780e853ad8859975bf390a3b51CAS |

Wang, J., Liu, Y. T., Xiao, L., Zhu, L., Wang, Q., and Yan, T. (2014b). Anti-inflammatory effects of apigenin in lipopolysaccharide-induced inflammatory in acute lung injury by suppressing COX-2 and NF-kB pathway. Inflammation 37, 2085–2090.
Anti-inflammatory effects of apigenin in lipopolysaccharide-induced inflammatory in acute lung injury by suppressing COX-2 and NF-kB pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVKhtrzE&md5=a15262e47d6c7b60a147bcd4caba247dCAS |

Xie, X., Peng, J., Huang, K., Huang, J., Shen, X., Liu, P., and Huang, H. (2012). Polydatin ameliorates experimental diabetes-induced fibronectin through inhibiting the activation of NF-kB signaling pathway in rat glomerular mesangial cells. Mol. Cell. Endocrinol. 362, 183–193.
Polydatin ameliorates experimental diabetes-induced fibronectin through inhibiting the activation of NF-kB signaling pathway in rat glomerular mesangial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVCjtL%2FI&md5=8764be2db73650d607bdff0fc78f0eacCAS |

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 | 1:CAS:528:DC%2BD38Xis1egu7c%3D&md5=8d96aa3241e392c9db2199ed3bd2754bCAS |

Zeng, Z., Chen, Z., Xu, S., Song, R., Yang, H., and Zhao, K. S. (2015). Polydatin alleviates small intestine injury during hemorrhagic shock as a SIRT1 activator. Oxid. Med. Cell. Longev. 2015, 965961.
Polydatin alleviates small intestine injury during hemorrhagic shock as a SIRT1 activator.Crossref | GoogleScholarGoogle Scholar |

Zeng, Z., Yang, Y., Dai, X., Xu, S., Li, T., Zhang, Q., Zhao, K. S., and Chen, Z. (2016). Polydatin ameliorates injury to the small intestine induced by hemorrhagic shock via SIRT3 activation-mediated mitochondrial protection. Expert Opin. Ther. Targets 20, 645–652.
Polydatin ameliorates injury to the small intestine induced by hemorrhagic shock via SIRT3 activation-mediated mitochondrial protection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XmvFyrs7s%3D&md5=949d623d34919ebe96a7e5ba1a45b6a4CAS |

Zhang, P. W., Yu, C. L., Wang, Y. Z., Luo, S. F., Sun, L. S., and Li, R. S. (1995). Influence of 3,4′,5-trihydroxystibene-3-beta-mono-d-glucoside on vascular endothelial epoprostenol and platelet aggregation. Zhongguo Yao Li Xue Bao 16, 265–268.
| 1:CAS:528:DyaK2MXls12rtbs%3D&md5=20d3bdf30e9bf329f7ff5084f265f4eeCAS |

Zhang, H., Yu, C. H., Jiang, Y. P., Peng, C., He, K., Tang, J. Y., and Xin, H. L. (2012). Protective effects of polydatin from Polygonum cuspidatum against carbon tetrachloride-induced liver injury in mice. PLoS One 7, e46574.
Protective effects of polydatin from Polygonum cuspidatum against carbon tetrachloride-induced liver injury in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFSktrfJ&md5=742eb232529bbcbf35da896889567f10CAS |