Effects of different concentrations of eugenol in maturation medium on bovine oocytes, oxidative status and preimplantation embryos
Lhara Ricarliany Medeiros de Oliveira A , Leonardo Vitorino Costa de Aquino A , Maria Valéria de Oliveira Santos A , Vicente José de Figueirêdo Freitas B , Luciana Medeiros Bertini C and Alexsandra Fernandes Pereira
A *
+ Author Affiliations
- Author Affiliations
A Laboratory of Animal Biotechnology, Federal Rural University of Semi-Arid, Mossoró, RN, Brazil.
B Laboratory of Physiology and Control of Reproduction, Ceará State University, Fortaleza, CE, Brazil.
C Federal Institute of Rio Grande do Norte, Apodi, RN, Brazil.
Animal Production Science 62(2) 142-151 https://doi.org/10.1071/AN21197
Submitted: 12 April 2021 Accepted: 30 August 2021 Published: 22 October 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Eugenol is a bioactive compound with defined attributes, including a role in reducing oxidative stress. Therefore, it is an interesting candidate for in vitro embryo production that has an environment that favours the formation of reactive oxygen species.
Aim: The objective of the study was to evaluate different concentrations of eugenol in bovine oocytes during in vitro maturation to observe the oxidative status and embryonic development.
Methods: Oocytes were allocated into five groups: control (without antioxidant), 100 μM cysteamine, 83 μM eugenol (E83), 100 μM eugenol and 120 μM eugenol. Three experiments were performed with 23 replicates. Oocytes were evaluated for metaphase II, first polar body, cytoplasmic maturation, cumulus cell expansion and viability. Oxidative status was measured by mitochondrial membrane potential, reactive oxygen species and glutathione. Oocytes were artificially activated and cultured in vitro.
Key results: The presence of eugenol at 83 μM improved the metaphase II rate compared with all treatments (P < 0.05). E83 and 100 μM cysteamine improved first polar body extrusion, cumulus cell expansion, viability and mitochondrial aggregation rates (P < 0.05). All antioxidant treatments resulted in increased cytoplasmic maturation and decreased mitochondrial membrane potential (P < 0.05). Reactive oxygen species levels decreased, and glutathione levels increased with E83 and 100 μM cysteamine treatments (P < 0.05). Finally, the E83 group increased the cleavage rates, embryo development, number of expanded blastocysts and number of blastomeres (P < 0.05).
Conclusions: A low concentration of eugenol (83 μM) is sufficient to generate a significant effect, attenuating the oxidative status and optimising in vitro maturation and embryo development.
Implications: This study provides information of a new natural antioxidant with defined concentration, 83 μM eugenol, representing a lower cost alternative capable of improving the efficiency of in vitro embryo production in cattle.
Keywords: antioxidant activity, blastocyst, bioactive, cattle, oocyte maturation, parthenogenetic embryos, phenolic compound, Syzygium aromaticum.
References
Abd El-Aziz AH, Mahrous UE, Kamel SZ, Sabek AA (2016) Factors influencing in vitro production of bovine embryos: a review. Asian Journal of Animal and Veterinary Advances 11, 737–756.| Factors influencing in vitro production of bovine embryos: a review.Crossref | GoogleScholarGoogle Scholar |
Adams RP (2007) ‘Identification of essential oils components by gas chromatography mass spectroscopy.’, 4th edn. (Allured Publishing Corporation: Carol Stream, IL)
Adefegha SA, Okeke BM, Oboh G (2021) Antioxidant properties of eugenol, butylated hydroxylanisole, and butylated hydroxyl toluene with key biomolecules relevant to Alzheimer’s diseases—In vitro. Journal of Food Biochemistry 45, e13276
| Antioxidant properties of eugenol, butylated hydroxylanisole, and butylated hydroxyl toluene with key biomolecules relevant to Alzheimer’s diseases—In vitro.Crossref | GoogleScholarGoogle Scholar | 32458455PubMed |
Ambrogi M, Dall’Acqua PC, Rocha‐Frigoni NAS, Leão BCS, Mingoti GZ (2017) Transporting bovine oocytes in a medium supplemented with different macromolecules and antioxidants: effects on nuclear and cytoplasmic maturation and embryonic development in vitro. Reproduction in Domestic Animals 52, 409–421.
| Transporting bovine oocytes in a medium supplemented with different macromolecules and antioxidants: effects on nuclear and cytoplasmic maturation and embryonic development in vitro.Crossref | GoogleScholarGoogle Scholar | 28120355PubMed |
Barros FDA, Adona PR, Guemra S, Damião BCM (2019) Oxidative homeostasis in oocyte competence for in vitro embryo development. Animal Science Journal 90, 1343–1349.
| Oxidative homeostasis in oocyte competence for in vitro embryo development.Crossref | GoogleScholarGoogle Scholar | 31469477PubMed |
Bezerra DP, Gadelha Militão GC, Castro de Morais M, Pergentino de Sousa D (2017) The dual antioxidant/prooxidant effect of eugenol and its action in cancer development and treatment. Nutrients 9, 1367
| The dual antioxidant/prooxidant effect of eugenol and its action in cancer development and treatment.Crossref | GoogleScholarGoogle Scholar |
Budani MC, Tiboni GM (2020) Effects of supplementation with natural antioxidants on oocytes and preimplantation embryos. Antioxidants 9, 612
| Effects of supplementation with natural antioxidants on oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar |
Catala M-G, Roura M, Soto-Heras S, Menéndez I, Contreras-Solis I, Paramio M-T, Izquierdo D (2018) Effect of season on intrafollicular fatty acid concentrations and embryo production after in vitro fertilization and parthenogenic activation of prepubertal goat oocytes. Small Ruminant Research 168, 82–86.
| Effect of season on intrafollicular fatty acid concentrations and embryo production after in vitro fertilization and parthenogenic activation of prepubertal goat oocytes.Crossref | GoogleScholarGoogle Scholar |
Chen X, Xuan B, Xu D, Wang Q, Cheng M, Jin Y (2019) Crocin supplementation during oocyte maturation enhances antioxidant defence and subsequent cleavage rate. Reproduction in Domestic Animals 54, 300–308.
| Crocin supplementation during oocyte maturation enhances antioxidant defence and subsequent cleavage rate.Crossref | GoogleScholarGoogle Scholar | 30325531PubMed |
Conti M, Franciosi F (2018) Acquisition of oocyte competence to develop as an embryo: integrated nuclear and cytoplasmic events. Human Reproduction Update 24, 245–266.
| Acquisition of oocyte competence to develop as an embryo: integrated nuclear and cytoplasmic events.Crossref | GoogleScholarGoogle Scholar | 29432538PubMed |
de Oliveira Santos MV, Azevedo Borges A, Bento de Queiroz Neta L, Medeiros Bertini L, Pereira AF (2018) Use of natural antioxidants in in vitro mammalian embryo production. Semina: Ciências Agrárias 39, 431–444.
| Use of natural antioxidants in in vitro mammalian embryo production.Crossref | GoogleScholarGoogle Scholar |
Elomda AM, Saad MF, Saeed AM, Elsayed A, Abass AO, Safaa HM, Mehaisen GMK (2018) Antioxidant and developmental capacity of retinol on the in vitro culture of rabbit embryos. Zygote 26, 326–332.
| Antioxidant and developmental capacity of retinol on the in vitro culture of rabbit embryos.Crossref | GoogleScholarGoogle Scholar | 30289099PubMed |
Fang Y, Zhang J, Li Y, Guo X, Li J, Zhong R, Zhang X (2019) Melatonin-induced demethylation of antioxidant genes increases antioxidant capacity through RORα in cumulus cells of prepubertal lambs. Free Radical Biology and Medicine 131, 173–183.
| Melatonin-induced demethylation of antioxidant genes increases antioxidant capacity through RORα in cumulus cells of prepubertal lambs.Crossref | GoogleScholarGoogle Scholar | 30472366PubMed |
Gad A, Abu Hamed S, Khalifa M, Amin A, El-Sayed A, Swiefy SA, El-Assal S (2018) Retinoic acid improves maturation rate and upregulates the expression of antioxidant-related genes in in vitro matured buffalo (Bubalus bubalis) oocytes. International Journal of Veterinary Science and Medicine 6, 279–285.
| Retinoic acid improves maturation rate and upregulates the expression of antioxidant-related genes in in vitro matured buffalo (Bubalus bubalis) oocytes.Crossref | GoogleScholarGoogle Scholar | 30564610PubMed |
Guo N, Deng T, Jiang H, Gong Y, Yin L, Ren X, Jin L, Li Y (2020) Association between blastocyst morphology and live birth rate following frozen–thawed single blastocyst transfer: results from a 5‐year retrospective analysis of 2593 cryopreserved blastocysts. Journal of Obstetrics and Gynaecology Research 46, 2314–2322.
| Association between blastocyst morphology and live birth rate following frozen–thawed single blastocyst transfer: results from a 5‐year retrospective analysis of 2593 cryopreserved blastocysts.Crossref | GoogleScholarGoogle Scholar |
Huang Z, Pang Y, Hao H, Du W, Zhao X, Zhu H (2018) Effects of epigallocatechin-3-gallate on bovine oocytes matured in vitro. Asian-Australasian Journal of Animal Sciences 31, 1420–1430.
| Effects of epigallocatechin-3-gallate on bovine oocytes matured in vitro.Crossref | GoogleScholarGoogle Scholar | 29531187PubMed |
Kaabi AM, Barakat IAH, Alajmi RA, Abdel-Daim MM (2020) Use of black seed (Nigella sativa) honey bee to improve sheep oocyte maturation medium. Environmental Science and Pollution Research 27, 33872–33881.
| Use of black seed (Nigella sativa) honey bee to improve sheep oocyte maturation medium.Crossref | GoogleScholarGoogle Scholar | 32535822PubMed |
Khalil AA, Rahman U, Khan MR, Sahar A, Mehmood T, Khan M (2017) Essential oil eugenol: sources, extraction techniques and nutraceutical perspectives. RSC Advances 7, 32669–32681.
| Essential oil eugenol: sources, extraction techniques and nutraceutical perspectives.Crossref | GoogleScholarGoogle Scholar |
Khan I, Chowdhury MMR, Song S-H, Mesalam A, Zhang S, Khalil AAK, Jung E-H, Kim J-B, Jafrim L, Mirza B, Kong IK (2018) Lupeol supplementation improves the developmental competence of bovine embryos in vitro. Theriogenology 107, 203–210.
| Lupeol supplementation improves the developmental competence of bovine embryos in vitro.Crossref | GoogleScholarGoogle Scholar | 29172177PubMed |
Kim HJ, Park JK, Eum JH, Song H, Lee WS, Lyu SW (2021) Embryo selection based on morphological parameters in a single vitrified-warmed blastocyst transfer cycle. Reproductive Sciences 28, 1060–1068.
| Embryo selection based on morphological parameters in a single vitrified-warmed blastocyst transfer cycle.Crossref | GoogleScholarGoogle Scholar | 33051819PubMed |
Kim W-J, Lee S-E, Park Y-G, Jeong S-G, Kim E-Y, Park S-P (2019) Antioxidant hesperetin improves the quality of porcine oocytes during aging in vitro. Molecular Reproduction and Development 86, 32–41.
| Antioxidant hesperetin improves the quality of porcine oocytes during aging in vitro.Crossref | GoogleScholarGoogle Scholar | 30358012PubMed |
Kong X, Yang S, Gong F, Lu C, Zhang S, Lu G, Lin G (2016) The relationship between cell number, division behavior and developmental potential of cleavage stage human embryos: a time-lapse study. PLoS One 11, e0153697
| The relationship between cell number, division behavior and developmental potential of cleavage stage human embryos: a time-lapse study.Crossref | GoogleScholarGoogle Scholar | 27077739PubMed |
Maside C, Martinez CA, Cambra JM, Lucas X, Martinez EA, Gil MA, Rodriguez-Martinez H, Parrilla I, Cuello C (2019) Supplementation with exogenous coenzyme Q10 to media for in vitro maturation and embryo culture fails to promote the developmental competence of porcine embryos. Reproduction in Domestic Animals 54, 72–77.
| Supplementation with exogenous coenzyme Q10 to media for in vitro maturation and embryo culture fails to promote the developmental competence of porcine embryos.Crossref | GoogleScholarGoogle Scholar | 31625244PubMed |
Menéndez-Blanco I, Soto-Heras S, Catalá MG, Roura M, Izquierdo D, Paramio MT (2020) Effect of crocetin added to IVM medium for prepubertal goat oocytes on blastocyst outcomes after IVF, intracytoplasmic sperm injection and parthenogenetic activation. Theriogenology 155, 70–76.
| Effect of crocetin added to IVM medium for prepubertal goat oocytes on blastocyst outcomes after IVF, intracytoplasmic sperm injection and parthenogenetic activation.Crossref | GoogleScholarGoogle Scholar | 32623132PubMed |
Mesalam A, Khan I, Lee KL, Song SH, Chowdhury MMR, Uddin Z, Kong IK (2017) 2-Methoxystypandrone improves in vitro-produced bovine embryo quality through inhibition of IKBKB. Theriogenology 99, 10–20.
| 2-Methoxystypandrone improves in vitro-produced bovine embryo quality through inhibition of IKBKB.Crossref | GoogleScholarGoogle Scholar | 28708489PubMed |
Mohammadi NS, Özgüneş H, Başaran N (2017) Pharmacological and toxicological properties of eugenol. Turkish Journal of Pharmaceutical Sciences 14, 201–206.
| Pharmacological and toxicological properties of eugenol.Crossref | GoogleScholarGoogle Scholar |
Montag M, Koll B, Holmes P, Ven HVD (2000) Significance of the number of embryonic cells and the state of the zona pellucida for hatching of mouse blastocysts in vitro versus in vivo. Biology of Reproduction 62, 1738–1744.
| Significance of the number of embryonic cells and the state of the zona pellucida for hatching of mouse blastocysts in vitro versus in vivo.Crossref | GoogleScholarGoogle Scholar | 10819778PubMed |
Nie J, Yan K, Sui L, Zhang H, Zhang H, Yang X, Lu S, Lu K, Liang X (2020) Mogroside V improves porcine oocyte in vitro maturation and subsequent embryonic development. Theriogenology 141, 35–40.
| Mogroside V improves porcine oocyte in vitro maturation and subsequent embryonic development.Crossref | GoogleScholarGoogle Scholar | 31518726PubMed |
Nikoloff N, Campagna A, Luchetti C, Carranza-Martín AC, Pascua AM, Anchordoquy JM, Furnus CC (2020) Effects of EPA on bovine oocytes matured in vitro with antioxidants: impact on the lipid content of oocytes and early embryo development. Theriogenology 146, 152–161.
| Effects of EPA on bovine oocytes matured in vitro with antioxidants: impact on the lipid content of oocytes and early embryo development.Crossref | GoogleScholarGoogle Scholar | 31787466PubMed |
Oliveira LRM, Santos MVO, Bertini LM, Pereira AF (2020) Bioguided isolation of compounds with antioxidant activity to improve the in vitro maturation of mammalian oocytes. Research, Society and Development 9, e117985137
| Bioguided isolation of compounds with antioxidant activity to improve the in vitro maturation of mammalian oocytes.Crossref | GoogleScholarGoogle Scholar |
Piras A-R, Menendez-Blanco I, Soto-Heras S, Catala M-G, Izquierdo D, Bogliolo L, Paramio M-T (2019) Resveratrol supplementation during in vitro maturation improves embryo development of prepubertal goat oocytes selected by brilliant cresyl blue staining. Journal of Reproduction and Development 65, 113–120.
| Resveratrol supplementation during in vitro maturation improves embryo development of prepubertal goat oocytes selected by brilliant cresyl blue staining.Crossref | GoogleScholarGoogle Scholar |
Pirozzi AVA, Imbimbo P, D’Agostino A, Tirino V, Finamore R, Monti DM, Piccoli R, Schiraldi C (2021) Antioxidant and hypolipidemic activity of açai fruit makes it a valuable functional food. Antioxidants 10, 40
| Antioxidant and hypolipidemic activity of açai fruit makes it a valuable functional food.Crossref | GoogleScholarGoogle Scholar |
Pramod K, Ansari SH, Ali J (2010) Eugenol: a natural compound with versatile pharmacological actions. Natural Product Communications 5, 1934578X1000501236
| Eugenol: a natural compound with versatile pharmacological actions.Crossref | GoogleScholarGoogle Scholar |
Sá NA, Vieira LA, Ferreira ACA, Cadenas J, Bruno JB, Maside C, Sousa FGC, Cibin FWS, Alves BG, Rodrigues APR, Leal-Cardoso JH, Gastal EL, Figueiredo JR (2019) Anethole supplementation during oocyte maturation improves in vitro production of bovine embryos. Reproductive Sciences 1, 1933719119831783
| Anethole supplementation during oocyte maturation improves in vitro production of bovine embryos.Crossref | GoogleScholarGoogle Scholar |
Santos MVO, Nascimento LE, Praxedes ÉA, Borges AA, Silva AR, Bertini LM, Pereira AF (2019) Syzygium aromaticum essential oil supplementation during in vitro bovine oocyte maturation improves parthenogenetic embryonic development. Theriogenology 128, 74–80.
| Syzygium aromaticum essential oil supplementation during in vitro bovine oocyte maturation improves parthenogenetic embryonic development.Crossref | GoogleScholarGoogle Scholar | 30743106PubMed |
Santos-Sánchez NF, Salas-Coronado R, Villanueva-Cañongo C, Hernández-Carlos B (2019) Antioxidant compounds and their antioxidant mechanism. Antioxidants 10, 1–29.
| Antioxidant compounds and their antioxidant mechanism.Crossref | GoogleScholarGoogle Scholar |
Shi D, Xu J, Zhang M, Niu W, Shi H, Yao G, Li Y, Zhang N, Sun Y (2020) Association between the quality of inner cell mass and first trimester miscarriage after single blastocyst transfer. Reproductive Biology and Endocrinology 18, 43
| Association between the quality of inner cell mass and first trimester miscarriage after single blastocyst transfer.Crossref | GoogleScholarGoogle Scholar | 32398002PubMed |
Sovernigo TC, Adona PR, Monzani PS, Guemra S, Barros FDA, Lopes FG, Leal CLV (2017) Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reproduction in Domestic Animals 52, 561–569.
| Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production.Crossref | GoogleScholarGoogle Scholar | 28295710PubMed |
Viana da Silva M, Santos MRC, Alves Silva IR, Macedo Viana EB, Dos Anjos DA, Santos IA, Barbosa de Lima NG, Wobeto C, Jorge N, Lannes SCDS (2021) Synthetic and natural antioxidants used in the oxidative stability of edible oils: an overview. Food Reviews International 1, 1–24.
| Synthetic and natural antioxidants used in the oxidative stability of edible oils: an overview.Crossref | GoogleScholarGoogle Scholar |
Yu XX, Liu YH, Liu XM, Wang PC, Liu S, Miao JK, Yang CX (2018) Ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes. Scientific Reports 8, 6132
| Ascorbic acid induces global epigenetic reprogramming to promote meiotic maturation and developmental competence of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 29666467PubMed |
Zavareh S, Talebi A, Hasanzadeh H (2015) Amending in vitro culture condition to overcome oxidative stress in assisted reproduction techniques (ART). Archives of Advances in Biosciences 6, 135–148.
| Amending in vitro culture condition to overcome oxidative stress in assisted reproduction techniques (ART).Crossref | GoogleScholarGoogle Scholar |
Zeng Y, Shinada K, Hano K, Sui L, Yang T, Li X, Himaki T (2021) Effects of tris (2-carboxyethyl) phosphine hydrochloride treatment on porcine oocyte in vitro maturation and subsequent in vitro fertilized embryo developmental capacity. Theriogenology 162, 32–41.
| Effects of tris (2-carboxyethyl) phosphine hydrochloride treatment on porcine oocyte in vitro maturation and subsequent in vitro fertilized embryo developmental capacity.Crossref | GoogleScholarGoogle Scholar | 33444914PubMed |
