In vitro maturation of bovine oocytes: the role of ROS, oxidative stress, and the impact of natural antioxidant supplementation
Palavras-chave:
Reactive Oxygen Species, In vitro embryo production, Oocyte nuclear maturation, Oocyte cytoplasmic maturation, Moringa oleiferaResumo
According to available data in the literature, Brazil has one of the largest cattle herds in the world and is one of the leading embryo producers, with a clear predominance of embryos produced in vitro. These data influence the ongoing pursuit of optimizing the results obtained in IVEP (in vitro embryo production). In this technique, in vitro maturation (IVM) is such a crucial stage that it justifies studies involving components that, when added to the media, can lead to improved cleavage rates and blastocyst development. It is well known that oocyte quality is influenced by oxidative stress, and in this context, the inclusion of antioxidants in the IVM medium may enhance these outcomes. Thus, the present study aimed to review oocyte maturation, the impact of oxidative stress, and the addition of antioxidants, such as Moringa oleifera, to the IVM media.
Downloads
Referências
Aboulthana, WM; Shousha, WG; Essawy, EAR; Saleh, MH; Salama, AH. Assessment of the anti-cancer efficiency of silver Moringa oleifera leaves nano-extract against colon cancer induced chemically in rats. Asian Pacific Journal of Cancer Prevention, v.22, p. 3267-3286, 2021.
Aitken, RJ. Impact of oxidative stress on male and female germ cells: implications for fertility. Reproduction, v.159, p. 189-201, 2020.
Agarwal, A. Oxidative stress and its implications in female infertility- a clinician´s perspective. Reproductive BioMedicine Online, v.11, n.5, p. 641-650, 2005.
Ahumada, CJ; Salvador, I; Cebrian-Serrano, A; Lopera, R; Silvestre, MA. Effect of supplementation of different growth factors in embryo culture medium with a small number of bovine embryos on in vitro embryo development and quality. Animal, v.7, n.3, p. 455-462, 2012.
Ajantha, A; Kathirvelan, C; Purushothaman, MR; Visha P. Study on nutrients, mineral and vitamin profile of Moringa oleífera leaf meal. International Journal of Current Microbiology and Applied Sciences, v.7, n. 5, 2018.
Alegbeleye, OO. How functional in Moringa oleífera? A review of its nutritive, medicinal, and socioeconomic potential. Food and Nutrition Bulletin, v.39, n.1, 149-170, 2018.
Almansa-Ordonez, A; Bellido, R; Vanessa, R; Barragan, M; Zambelli, F. Oxidative stress in reproduction: a mitochondrial perspective. Biology, v.269, p. 1-22, 2020.
Almubarak, A; Yu, IJ; Jeon, Y. Antioxidants as alleviating agents of in vitro embryo production oxidative stress. Journal of Animal Reproduction and Biotechnology, v.38, p. 47-53, 2023.
Anguita, B; Jimenez-Macedo, AR; Izquierdo, D; Mogas, T; Paramio, MT. Effect of oocyte diameter on meiotic competence, embryo development, p34 (cdc2) expression and MPF activity in prepubertal goat oocytes. Theriogenology, v.67, p.526-536, 2007.
Aquino, LVA; Santos, MVO; Oliveira, LRM; Moura, YBF; Nascimento, TL; Bertini, LM; Pereira, AF. Antioxidant effects of Citrus sinensis peel essential oil in a bovine oocyte model. Livestock Science, v.276, 105324, 2023.
Barros, FDA; Adona, PR; Guemra, S; Damião, BCM. Oxidative homeostasis in oocytes competence for in vitro embryo development. Animal Science Journal, v.90, p. 1343-1349, 2019.
Baruselli, PS; Catussi, BLC; Abreu, LA; Elliff, FM; Silva, LG; Batista, EOS. Challenges to increase the AI and ET markets Brazil. Proceedings of the 33rd Annual Meeting of the Brazilian Embryo Technology Society (SBTE), p. 1-12, 2019.
Belin, S; Kaya, F; Burtey, S; Fontes, M. Ascorbic acid and gene expression: another example of regulation of gene expression by small molecules. Current Genomics, v.11, p. 52-57, 2010.
Blerkom, JV. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion, v.11, p. 797-813, 2011.
Brackett, BG; Bousquet, D; Boice, ML; Donawick, WJ; Evans, JF; Dressel, MA. Normal development following in vitro fertilization in the cow. Biology of Reproduction, v.27, p. 147-158, 1982.
Budani, MC; Tiboni, GM. Effects of supplementation with natural antioxidants on oocyte and preimplantation embryos. Antioxidants, v.9, n. 612, p. 1-25, 2020.
Cajas, YN; Beltrán, KC; Guevara, ML; Blanca, MGM; Ramos-Ibeas, P; Gutiérrez-Adán, A; Rizos, D; González, EM. Antioxidant nobiletin enhances oocytes maturation and subsequent embryo development and quality. International Journal of Molecular Sciences, v.21, p. 1-18, 2020.
Catala, MG; Roura, M; Soto-Heras, S; Menéndez, I; Contreras-Solis, I; Paramio, MT; Izquierdo. 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, v.168, p. 82-86, 2018.
Chen, X; Xuan, B; Xu, D; Wang, Q; Cheng, M; Jin, Y. Crocin supplementation during oocyte maturation enhances antioxidant defence and subsequent cleavage rate. Reproduction in Domestic Animals, v.54, p. 300-308, 2019.
Chowdhury, MMR; Choi, BH; Khan, I; Lee, KL; Mesalam, A; Song, SH; Xu, L; Joo, MD; Afrin, F; Kong, IK. Supplementation of lycopene in maturation media improves bovine embryo quality in vitro. Theriogenology, v.103, p. 173-184, 2017.
Dalvit, G; Lllanes, SP; Descalzo, A; Insani, M; Beconi, M; Cetica, P. Effect of alpha-tocopherol and ascorbic acid on bovine oocyte in vitro maturation. Reproduction in Domestic Animals, v.40, p. 93-97, 2005.
Das, S; Chattopadhyay, R; Ghosh, S; Gosh, S; Goswami, SK; Chakravarty, BN; Chaudhury, K. Reactive oxygen species level in follicular fluid- embryo quality marker in IVF? Human Reproduction, v.21, n.9, p. 2403-2407, 2006.
Davoodian, N; Kadivar, A; Mehrban, H. Supplementation of media with gamma-oryzanol as a novel antioxidant to overcome redox imbalance during bovine oocyte maturation in vitro. Reproduction in Domestic Animals, v.59, n.1, e14503, 2024.
Denicol, AC; Siqueira, LGB. Maternal contribuitions to pregnancy success: from gamete quality to uterine environment. Animal Reproduction, v.20, n.2, p. 1-16, 2023.
Dode, MAN; Rumpf, R. Produção in vitro de embriões- eficiência, limitações e perspectivas futuras: visão da Embrapa Recursos Genéticos e Biotecnologia. In: Anais do Workshop sobre embriões bovinos produzidos in vitro: perspectivas de utilização e possíveis impactos na pecuária brasileira. Ministério da Agricultura, Pecuária e abastecimento. p. 13-26, 2002.
Dröge, W. Free radicals in the physiological control of cell function. American Physiological Society, v.82, p. 47-95, 2002.
Dumollard, R; Duchen, M; Carroll, J. The role of mitochondrial function in the oocyte and embryo. Current Topics in Developmental Biology, v.77, p. 21-48, 2007.
Eini, F; Bidadkosh, A; Nazarian, H; Piryaei, A; Novin, MG; Joharchi, K. Thymoquinone reduces intracytoplasmic oxidative stress and improves epigenetic modification in polycystic ovary syndrome mice oocytes, during in vitro maturation. Molecular Reproduction & Development, p. 1-14, 2019.
Fair, T; Hyttel, P; Greve, T. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Molecular Reproduction and Development, v.42, p. 437-442, 1995.
Ferré, LB, Kjelland, ME; Strobech, LB; Hyttel, P; Mermillod, P; Ross, PJ. Review: Recent advances in bovine in vitro embryo production: reproductive biotechnology history and methods. Animal, v.14, n.5, 2020.
Ferreira, EM; Vireque, AA; Adona, PR; Meirelles, FV; Ferriani, RA; Navarro, PAAS. Cytoplasmic maturation of bovine oocytes: Structural and biochemical modification and acquisition of developmental competence. Theriogenology, v.71, p. 836-848, 2009.
Fulka Jr, J; First, NL; Moor, RM. Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation. Molecular Human Reproduction, v.4, n.1, p. 41-48, 1998.
Gandolfi, BTAL; Gandolfi, F. The maternal legacy to the embryo: Cytoplasmic components and their effects on early development. Theriogenology, v.55, p. 1255-1276, 2001.
Ge, H; Tollner, TL; Hu, Z; Dai, M; Li, X; Guan, H; Shan, D; Zhang, X; LV, J; Huang, C; Dong, Q. The importance of mitochondrial metabolic activity and mitochondrial DNA replication during oocyte maturation in vitro on oocyte quality and subsequent embryo developmental competence. Molecular Reproduction & Development, v.79, p. 392-401, 2012.
Goto, Y; Noda, Y; Mori, T; Nakano, M. Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radical Biology & Medicine, v.15, p. 69-75, 1993.
Guemra, S; Monzani, PS; Santos, ES; Zanin, R; Ohashi, OM; Miranda, MS; Adona, PR. Maturação in vitro de oócitos bovinos em meios suplementados com quercetina e seu efeito sobre o desenvolvimento embrionário. Arquivo Brasileiro de Medicina Veternária e Zootecnia, v.65, n.6, p. 1616-1624, 2013.
Harris, SE; Leese, HJ; Gosden, RG; Picton, HM. Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Molecular Reproduction & Development, v.76, p. 231-238, 2009.
Hyttel, P; Xu, KP; Smith, S; Greve, T. Ultrastructure of in vitro oocyte maturation in cattle. Journals of Reproduction & Fertility, v.78, 615-625, 1986.
IBGE- INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Rebanho de Bovinos (Bois e Vacas). Rio de Janeiro: IBGE, 2022.
IETS. 2021 Statistics of embryo production and transfer in domestic farm animals. In: Embryo Technology Newsletter, v.40, n.4, p. 01-19, 2022.
Khan, I; Chowdhury, MMR; Song, SH; Mesalam, A; Zhang, S; Khalil, AAK; Jung, EH; Kim, JB; Jafri, L; Mirza, B; Kong, IK. Lupeol supplementation improves the developmental competence of bovine embryos in vitro. Theriogenology, v.107, p. 203-210, 2018.
Khazaei, M; Aghaz, F. Reactive oxygen species generation and use of antioxidants during in vitro maturation of oocytes. International Journal of Fertility and Sterility, v.11, n.2, p. 63-70, 2017.
Krisher, RL. The effect of oocyte quality on development. Journal of Animal Science, v.82, p. 14-23, 2004.
Kruip, TAM; Cran, DG; Beneden, TH; Dieleman, SJ. Structural changes in bovine oocytes during final maturation in vitro. Gamete Research, v.8, p. 29-47, 1983.
Kubelka, M; Motlík, J; Schultz, RM; Pavlok, A. Butyrolactone I reversibly inhibits meiotic maturation of bovine oocytes, without influencing chromosome condensation activity. Biology of Reproduction, v.62, p. 292-302, 2000.
Lalan, G; Thirumal, M; Ankul, SS; Anant, N. Phytochemical screening and in vitro evaluation of antibacteriala antioxidant properties of Moringa oleífera linn leaf extract. Research Journal of Pharmacy and Technology, v.16, p. 4512-4518, 2023.
Landim-Alvarenga, FC, Maziero, RRD. Controlo f oocyte maturation. Animal Reproduction, v.11, n.3, p.150-158, 2014.
Lee, Y; Shim, J; Ko, N; Kim, HJ; Park, JK; Kwak, K; Kim, H; Choi, K. Effect of alanine supplementation during in vitro maturation on oocyte maturation and embryonic development after parthenogenesis and somatic cell nuclear transfer in pigs. Theriogenology, v.127, p. 80-87, 2019.
Leone, A; Spada, A; Battezzati, A; Schiraldi, A; Aristil, J; Bertoli, S. Cultivation, genetic, ethnoparmacology, phytochemistry and pharmacology of Moringa oleífera leaves: An overview. International Journal of Molecular Sciences, v.16, p. 12791-12835, 2015.
Leone, A; Spada, A; Battezzati, A; Schiraldi, A; Aristil, J; Bertoli, S. Moringa oleífera seeds and oil: Characteristics and uses for human health. International Journal of Molecular Sciences, v.17, p. 1-14, 2016.
Leoni, GG; Palmerini, MG; Satta, V; Succu, S; Pasciu, V; Zinellu, A; Carru, C; Macchiarelli, G; Nottola, AS; Naitana, Salvatore; Berlinguer, F. Differences in the kinetic of the first meiotic division and active mitochondrial distribution between prepubertal and adult oocytes mirror differences in their developmental competence in a sheep. PloS ONE, v.10, n.4, p. 1-5, 2015.
Lin, J; Wang, L. Oxidative stress in oocyte and embryo development: implications for in vitro systems. Antioxidants and Redox Signaling, p. 1-38, 2020.
Liu, L; Trimarchi, JR; Keefe, DL. Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes. Biology of Reproduction, v.62, p. 1745-17553, 2000.
Liu, Y; Wang, X; Wei, X; Gao, Z. Values, properties and utility of different parts of Moringa oleifera: an overview. Chinese Herbal Medicines, v.10, p. 371-378, 2018.
Lonergan, P; Khatir, H; Carolan, C; Mermillod, P. Bovine blastocyst production in vitro after inhibition of oocyte meiotic resumption for 24h. Journal of Reproduction and Fertility, v.109, p. 355-365, 197.
Magata, F; Ideta, A; Okubo, H; Matsuda, F; Urakawa, M; Oono, Y. Growth potential of bovine embryos presenting abnormal cleavage observed through time lapse cinematography. Theriogenology, v.133, p. 119-124, 2019.
Maillo, V; Lopera-Vasquez, R; Hamdi, M; Gutierrez-Adan, A; Lonergan, P; Rizos, D. Maternal-embryo interaction in the bovine oviduct: Evidence from in vivo and in vitro studies. Theriogenology, v.86, p. 443-450, 2016.
Matos, L; Stevenson, D; Gomes, F; Silva-Carvalho, JL; Almeida, H. Superoxide dismutase expression. In human cumulus oophorus cells. Molecular Human Reproduction, v.15, n.7, p. 411-419, 2009.
Oliveira, LRM; Aquino, LVC; Santos, MVO; Freitas, VJF; Bertini, LM; Pereira, A. Antioxidant effect of bioactive compounds isolated from Syzygium aromaticum essential oil on the in vitro developmental potential of bovine oocytes. Livestock Science, v.260, 104932, 2022.
Paikra, BK; Dhongade, HKJ; Gidwani, B. Phytochemistry and pharmacology of Moringa oleifera Lam. Journal of Pharmacopunture, v.20, n.3, p. 194-200, 2017.
Piras, AR; Menéndez-Blanco, I; Soto-Heras, S; Catalá, MG; Izquierdo, D; Bogliolo, L; Paramio, MT. Resveratron supplementation during in vitro maturation improves embryos development of prepubertal goat oocytes selected by brilliant cresyl blue staining. Journal of Reproduction and Development, v.65, n.2, p. 113-120, 2019.
Pollini, L; Tringaniello, C; Ianni, F; Blasi, F; Manes, J; Cossignani, L. Impact of ultrasound extraction parameters on the antioxidant properties of Moringa oleífera leaves. Antioxidants, v.277, n.9, p. 1-14, 2020.
Procházková, D; Bousová, I; Wilhelmová, N. Antioxidants and prooxidant properties of flavonoids. Fitoterapia, v.82, p. 513-523, 2011.
Rani, NZA; Husain, K; Kumolosasi, E. Moringa Genus: A review of phytochemistry and Pharmacology. Frontiers in Pharmacology, p. 1-26, 2018.
Rasheed, A; Azeez, RFA. Chapter- A review on natural antioxidants. Traditional and Complementary Medicine, p. 1-24, 2019.
Rizos, D; Ward, F; Duffy, P; Boland, MP; Lonergan, P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: Implications for blastocyst yield and blastocyst quality. Molecular Reproduction and Development, v.61, p. 234-248, 2002.
Rodrigues-Cunha, MC; Mesquita, LG; Bressan, F; Collado, M; Balieiro, JCC; Schwarz, KRL; Castro, FC; Watanabe, OY; Watanabe, YF. Effects of melatonin during IVM in defined medium on oocyte meiosis, oxidative stress, and subsequent embryo development. Theriogenology, v.86, n.7, p. 1685-1694, 2016.
Romek, M; Gajda, B; Krzystofowicz, E; Kucia, M; Uzarowska, A; Smorag, Z. Improved quality of porcine embryos cultures with hyaluronan due to the modification of the mitochondrial membrane potential and reactive oxygen species level. Theriogenology, v.102, p. 1-9, 2017.
Sabatini, L; Wilson, C; Lower, A; Al- Shawaf, T; Grudzinskas, G. Superoxide dismutase activity in human follicular fluid after controlled ovarian hyperstimulation in women undergoing in vitro fertilization. Fertility and Sterility, v.72, n.6, p. 1027- 1034, 1999.
Saini, KR; Sivanesan, I; Keum, YS. Phytochemicals of Moringa oleífera: A review of their nutritional, therapeutic and industrial significance. 3 Biotech, v.203, n.6, p. 1-14, 2016.
Santos, TA; Shourbagy, SE; John, JCS. Mitochondrial content reflects oocyte variability and fertilization outcome. Fertility and Sterility, v.85, n.3, p. 1-8, 2006.
Santos, MVO; Borges, AA; Queiroz Neta, LB; Bertini, LM; Pereira, AF. Use of natural antioxidants in in vitro mammalian embryo production. Semina: Ciências Agrárias, v.39, n.1, p. 431-443, 2018.
Santos, MVO, Nascimento, LE; Praxedes, EA; Borges, AA; Silva, AR; Bertini, LM; Pereira, AF. Syzygium aromaticum essential oil supplementation during in vitro bovine oocytes maturation improves parthenogenetic embryonic development. Theriogenology, v.128, p. 74-80, 2019.
Segwatibe, MK; Cosa, S; Bassey, K. Antioxidant and antimicrobial evaluations of Moringa oleifera Lam leaves extract and isolates compounds. Molecules, v.28, n.2, p. 1-22, 2023.
Sharma, V; Paliwal, R; Pracheta, Sharma, S. Phytochemical analysis and evaluation of antioxidant activities of hydro-ethanolic extract of Moringa oleifera Lam. Pods. Journal of Pharmacy Research, v.4, n.2, p. 554-557, 2011.
Shu, Y; Zeng, H; Ren, Z; Zhuang, G; Liang, X; Shen, H; Yao, S; Ke, P; Wang, N. Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Human Reproduction, v.23, n.3, p. 504-513, 2008.
Sies, H. Oxidative stress: a concept in redoz biology and medicine. Redoz Biology, v.4, p. 180-183, 2015.
Sirard, MA; Richard, F; Blondin, P; Robert, C. Contribution of the oocyte to embryo quality. Theriogenology, v.65, p. 126-136, 2006.
Sirard, MA. 40 years of bovines IVF in the new genomic selection context. Reproduction, v.156, R1-R7, 2018.
Soto-Heras, S; Paramio, MT. Impacto f oxidative stress on oocyte competence for in vitro embryo production programs. Research in Veterinary Science, v.132, p. 342-350, 2020.
Sovernigo, TC, Adona, PR, Monzani, OS, Guemra, S; Barros, FDA, Lopes, FG; Leal, CLV. Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reproduction in Domestic Animals, p. 1-9, 2017.
Steptoe, PC; Edwards, RG. Birth after the reimplantation of a human embryo. The Lancet, p. 366, 1978.
Sugunabai, J; Jayaraj, M; Karpagam, T; Varalakshmi, B. Antidiabetic efficiency of Moringa oleifera and Solanum nigrum. International Journal of Pharmacy and Pharmaceutical Sciences, v.6, n.1, p. 40-42, 2014.
Sultana, S. Nutritional and functional properties of Moringa oleifera. Metabolism Open, v.8, p. 1-6, 2020.
Tesfay, SZ; Bertling, I; Odindo, AO; Workneh, TS; Mathaba, N. Levels of anti-oxidants in different parts of moringa (Moringa oleifera) seedling. African Journal of Agricultural Research, v.6, n.22, p. 5123-5132, 2011.
Tiloke, C; Anand, K; Gengan, RM; Chuturgoon, AA. Moringa oleifera and their phytonanoparticles: Potential antiproliferative agents against cancer. Biomedicine & Pharmacotherapy, v.108, p. 457-466, 2018.
Tripathi, A; Kumar, KVP; Chaube, SK. Meiotic cell cycle arrest in mammalian oocytes. Journal of Cellular Physiology, v.233, p. 592-600, 2010.
Trounson, A; Anderiesz, C; Jones, G. Maturation of human oocytes in vitro and their developmental competence. Reproduction, v.121, p. 51-75, 2001.
Tomek, W; Torner, H; Kanitz, W. Comparative analysis of protein synthesis, transcription and cytoplasmic polyadenylation of mRNA during maturation of bovine oocytes in vitro. Reproduction in Domestic Animals, v.37, p. 86-91, 2002.
Turrens, JF. Mitochondrial formation of reactive oxygen species. Journal of Physiology, v.552, n.2, p.335-344, 2003.
Valdez-Solana, MA; Mejía-García, VY; Téllez-Valencia, A; García-Arenas, G; Salas-Pacheco, J; Alba-Romero, J; Sierra-Campos, E. Nutricional content and elemental and phytochemical analyses of Moringa oleífera Grow in Mexico. Journal of Chemistry, v.2015, p. 1-9, 2015.
Van Wagtendonk-de Leeuw, AM. Ovum pick up and in vitro production in the bovine after use in several generations: A 2005 status. Theriogenology, v.65, p. 914-925, 2006.
Varago, FC; Mendonça, LF; Lagares, MA. Produção in vitro de embriões bovinos: estado da arte e perspectiva de uma técnica em constante evolução. Revista Brasileira de Reprodução Animal. v.32, n.2, p. 100-109, 2008.
Vats, S; Gupta, T. Evaluation of bioactive compounds and antioxidant potential of hydroethanolic extract of Moringa oleifera Lam. From Rajasthan, India. Physiology and Molecular Biology of Plants, v.23, p.239-248, 2017.
Vergara-Jimenez, M; Almatrafi, MM; Fernandez, ML. Bioactive componentes in Moringa oleífera leaves protect against chronic disease. Antioxidants, v.6, n.91, p.1-13, 2017.
Viana, JHM. Produção de embriões bovinos in vivo (transferência de embriões - TE) e in vitro (Fecundação in vitro FIV) no Brasil: histórico, cenário atual e perspectivas. Anais do Simpósio de Reprodução de Bovinos, 1ª Ed., Pelotas, RS, Brasil, p. 48-55, 2008.
Wang, X; Falcone, T; Attaran, M; Goldberg, JM; Agarwal, A; Sharma, R. Vitamin C and vitamin E supplementation reduce oxidative stress-induced embryo toxicity and improve the blastocyst development rate. Fertility and Sterility, v.78, n.6, p. 1272-1277, 2002.
Wang, F; Tian, X; Zhang, L; He, C; Ji, P; Li, Y; Tan, D; Liu, G. Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Reproductive Science, v.101, n.2, p. 578-586, 2014.
Wang, S; He, G; Chen, M; Zuo, T; Xu, W; Liu, X. The role of antioxidant enzymes in the ovaries. Oxidative Medicine and Cellular Longevity, v.2017, p. 1-14, 2017.
Wang, Y; Gao, Y; Ding, H; Liu, S; Han, X; Gui, J; Liu, D. Subcritical ethanol extraction of flavonoids from Moringa oleifera leaf and evaluation of antioxidant activity. Food Chemistry, v.218, p. 152-158, 2017.
Watson, AJ. Oocyte cytoplasmatic maturation: A key mediator of oocyte and embryo developmental competence. Journal of Animal Science, v.85, E1-E3, 2007.
Yang, M; Tao, L; Kang, X; Wang, Z; Su, L; Li, L; Gu, F; Zhao, C; Sheng, J; Tian, Y. Moringa oleifera Lam. leaves as new raw food material: A review of its nutritional composition, functional properties and comprehensive application. Trends in Food Science & Technology, v.138, p.399-416, 2023.
Zhao, B; Ding, X; Wang, X; Sun, Y; Gao, S; Song, X; Zhang, B; Zhang, Y; Wang, Y. Supplementation with kaempferol relieves oxidative stress and enhances development of early bovine embryos in vitro. Reproduction in Domestic Animals, v.57, p. 1007-1015, 2022.
