Oxidative stress is one of the most detrimental factors that affect oocyte developmental competence and embryo development in vitro. The impact of anethole supplementation to in vitro maturation (IVM) media on oocyte maturation and further bovine in vitro embryo production was investigated. Oocytes of slaughterhouse-derived bovine ovaries were placed in IVM with anethole at different concentrations of 30 (AN30), 300 (AN300), and 2000 μg/mL (AN2000), or without (control treatment). The oocytes were assessed for maturation rates, and for reactive oxygen species (ROS) and ferric reducing antioxidant power (FRAP) levels, and mitochondrial membrane potential. Embryo development was assessed by cleavage and blastocyst rates, and embryo cell number. The percentage of metaphase II oocytes were similar among the treatments (range, 77%-96%). Anethole at 300 µg/mL was the only treatment that yielded higher cleavage and embryo development (morula and blastocyst) rates compared to the control treatment. The ROS production in the oocytes after maturation did not differ among treatments. However, oocytes treated with anethole at 300 µg/mL had higher (P < .05) FRAP and mitochondrial membrane potential compared to the control treatment. Furthermore, AN300 treatment increased (P < .05) the average number of total cells in blastocysts compared to the control and AN30 treatments. The use of anethole at 300 μg/mL during IVM is suggested to improve the quantity and quality of bovine embryos produced in vitro. The beneficial effects of anethole on embryonic developmental competence in vitro seems to be related to its capacity to regulate the redox balance and improve mitochondrial function in oocytes and embryos.
Arias-AlvarezMBermejo-AlvarezPGutierrez-AdanARizosDLorenzoPLLonerganP. Effect of leptin supplementation during in vitro oocyte maturation and embryo culture on bovine embryo development and gene expression patterns. Theriogenology. 2011;75(5):887–896.
2.
LonerganPFairT. Maturation of oocytes in vitro. Annu Rev Anim Biosci. 2016;4:255–268.
3.
ChowdhuryMMRMesalamAKhanI. Improved developmental competence in embryos treated with lycopene during in vitro culture system. Mol Reprod Dev. 2018;85(1):46–61.
4.
ZhuJMoawadARWangCYLiHFRenJYDaiYF. Advances in in vitro production of sheep embryos. Int J Vet Sci Med. 2018;6:15–26.
5.
FigueiraRCSSettiASBragaDPAFIaconelliAJrBorgesEJr. Blastocyst morphology holds clues concerning the chromosomal status of the embryo. Int J Fertil Steril. 2015;9(2):215–220.
6.
CombellesCMGuptaSAgarwalA. Could oxidative stress influence the in vitro maturation of oocytes?Reprod Biomed Online. 2009;18(6):864–880.
7.
MurrayAASwalesAKSmithREMolinekMDHillierSGSpearsN. Follicular growth and oocyte competence in the in vitro cultured mouse follicle: effects of gonadotrophins and steroids. Mol Hum Reprod. 2008;14(2):75–83.
8.
TillyJLTillyKI. Inhibitors of oxidative stress mimic the ability of follicle stimulating hormone to suppress apoptosis in cultured rat ovarian follicles. Endocrinology. 1995;136(1):242–252.
9.
HovattaOSilyeRAbirRKrauszTWinstonRM. Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum Reprod. 1997;12(5):1032–1036.
10.
AgarwalASaidTMBedaiwyMABanerjeeJAlvarezJG. Oxidative stress in an assisted reproductive technique setting. Fertil Steril. 2006;86(3):503–512.
11.
FinkelTHolbrookNJ. Oxidants, oxidative stress and the biology of ageing. Nature. 2000;408(6809):239–247.
12.
AitkenRJHarkissDBuckinghamD. Relationship between iron catalysed lipid peroxidation potential and human sperm function. J Reprod Fertil. 1993;98(1):257–265.
13.
TakahashiTIgarashiHAmitaMHaraSMatsuoKKurachiH. Molecular mechanism of poor embryo development in postovulatory aged oocytes: mini review. J Obstet Gynaecol Res. 2013;39(10):1431–1439.
14.
HeLHeTFarrarSJiLLiuTMaX. Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol Biochem. 2017;44(2):532–553.
15.
AndradeERvan den HurkRLisboaLA. Effects of ascorbic acid on in vitro culture of bovine preantral follicles. Zygote. 2012;20(4):379–388.
16.
Cebrian-SerranoASalvadorIRagaEDinnyesASilvestreMA. Beneficial effect of melatonin on blastocyst in vitro production from heat-stressed bovine oocytes. Reprod Domest Anim. 2013;48(5):738–746.
17.
da CostaNNBritoKNSantanaPD. Effect of cortisol on bovine oocyte maturation and embryo development in vitro. Theriogenology. 2016;85(2):323–329.
18.
WangZFuCYuS. Green tea polyphenols added to IVM and IVC media affect transcript abundance, apoptosis, and pregnancy rates in bovine embryos. Theriogenology. 2013;79(1):186–192.
19.
SáNARAraújoVRCorreiaHHV. Anethole improves the in vitro development of isolated caprine secondary follicles. Theriogenology. 2017;89:226–234.
20.
Leal-CardosoJHFontelesMC. Pharmacological effects of essential oils plants of the Northeast of Brazil. An Acad Bras Cienc. 1999;71(2):207–213.
21.
ChainyGBMannaSKChaturvediMMAggarwalBB. Anethole blocks both early and late cellular responses transduced by tumor necrosis factor: effect on NF-kappaB, AP-1, JNK, MAPKK and apoptosis. Oncogene. 2000;19(25):2943–2950.
22.
SáNARBrunoJBGuerreiroDD. Anethole reduces oxidative stress and improves in vitro survival and activation of primordial follicles. Braz J Med Biol Res. 2018;51(8):7129–7137.
23.
FreireRSMoraisSMCatunda-JuniorFEPinheiroDC. Synthesis and antioxidant, anti-inflammatory and gastroprotector activities of anethole and related compounds. Bioorg Med Chem. 2005;13(13):4353–4358.
24.
KhanAAhmadAAkhtarF. Induction of oxidative stress as a possible mechanism of the antifungal action of three phenylpropanoids. FEMS Yeast Res. 2011;11(1):114–122.
25.
TakahashiYHishinumaMMatsuiMTanakaHKanagawaH. Development of in vitro matured/fertilized bovine embryos in a chemically defined medium: influence of oxygen concentration in the gas atmosphere. J Vet Med Sci. 1996;58(9):897–902.
26.
PapaPMPapaFOOliveiraLAGuastiPNCastilhoCGiomettiIC. Different extenders in the cryopreservation of bovine epididymal spermatozoa. Anim Reprod Sci. 2015;161:58–63.
27.
GordonI. Laboratory Production of Cattle Embryos. Wallingford, England: CAB International; 1994.
28.
LoetchutinatSKothanSDechsupaJMeesungnoenJJay-GerinSM. Spectrofluorometric determination of intracellular levels of reactive oxygen species in drug-sensitive and drug-resistant cancer cells using the 20,70-dichlorofluorescein diacetate assay. Radiat Phys Chem. 2005;72(2-3):323–331.
29.
BenzieIFFStrainsJJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem. 1996;239(1):70–76.
30.
PerrySWNormanJPBarbieriJBrownEBGelbardHA. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotechniques. 2011;50(2):98–115.
31.
FabbriRVicentiRMartinoNA. Confocal laser scanning microscopy analysis of bioenergetic potential and oxidative stress in fresh and frozen-thawed human ovarian tissue from oncologic patients. Fertil Steril. 2014;101(3):795–804.
32.
ChankitisakulVSomfaiTInabaYTechakumphuMNagaiT. Supplementation of maturation medium with L-carnitine improves cryo-tolerance of bovine in vitro matured oocytes. Theriogenology. 2013;79(4):590–598.
33.
FurnusCCde MatosDGPiccoS. Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes. Anim Reprod Sci. 2008;109(1-4):88–99.
34.
CliftDSchuhM. Restarting life: fertilization and the transition from meiosis to mitosis. Nat Rev Mol Cell Biol. 2013;14(9):549–562.
35.
SoaresPMLimaRFde Freitas PiresASouzaEPAssreuyAMCriddleDN. Effects of anethole and structural analogues on the contractility of rat isolated aorta: involvement of voltage-dependent Ca2+-channels. Life Sci. 2007;81(13):1085–1093.
36.
DumollardRWardZCarrollJDuchenMR. Regulation of redox metabolism in the mouse oocyte and embryo. Development. 2007;134(3):455–465.
37.
PamplonaRCostantiniD. Molecular and structural antioxidant defenses against oxidative stress in animals. Am J Physiol Regul Integr Comp Physiol. 2011;301(4):843–863.
38.
DongareVKulkarniCKondawarMMagdumCHaldavnekarVArvindekarA. Inhibition of aldose reductase and anti-cataract action of trans-anethole isolated from Foeniculum vulgare Mill. fruits. Food Chem. 2012;132(1):385–390.
39.
BrandMDOrrALPerevoshchikovaIVQuinlanCL. The role of mitochondrial function and cellular bioenergetics in ageing and disease. Br J Dermatol. 2013;169(2):1–8.
40.
EgerszegiIAlmHRátkyJHeleilBBrüssowKPTornerH. Meiotic progression, mitochondrial features and fertilisation characteristics of porcine oocytes with different G6PDH activities. Reprod Fertil Dev. 2010;22(5):830–838.
41.
Van BlerkomJDavisPMathwigVAlexanderS. Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum Reprod. 2002;17(2):393–406.
42.
TarazonaAMRodríguezJIRestrepoLFOlivera-AngelM. Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro. Reprod Domest Anim. 2006;41(1):5–11.
43.
GotoYNodaYMoriTNakanoM. Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic Biol Med. 1993;15(1):69–75.
44.
YuYDumollardRRossbachALaiFASwannK. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol. 2010;224(3):672–680.
45.
NoseK. Role of reactive oxygen species in the regulation of physiological functions. Biol Pharm Bull. 2000;23(8):897–903.
BenkhalifaMFerreiraYJChahineH. Mitochondria: participation to infertility as source of energy and cause of senescence. Int J Biochem Cell Biol. 2014;55:60–64.
48.
PangWZhangYZhaoNDarwicheSSFuXXiangW. Low expression of Mfn2 is associated with mitochondrial damage and apoptosis in the placental villi of early unexplained miscarriage. Placenta. 2013;34(7):613–618.
49.
Vander HeidenMGCantleyLCThompsonCB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930):1029–1033.
