Effect of the acidified extract of Moringa oleifera leaves as a supplement in the in vitro culture medium of sheep preantral follicles
DOI:
https://doi.org/10.5433/1679-0359.2023v44n6p1991Keywords:
Phenolic compound, Moringa oleifera, Oocyte, Ovine, Preantral follicle.Abstract
This study was conducted to evaluate the effects of the acidified extract of M. oleifera leaves as a supplement into the base medium for in vitro culture of sheep isolated secondary follicles. Follicles were isolated and cultured for 12 days in α-MEM+(supplemented with bovine serum albumin, insulin, glutamine, hypoxanthine, transferrin, selenium, and ascorbic acid) with or without 0.1; 0.2 or 0.4 mg/ml of the acidified extract of M. oleifera. Follicle morphology, antral cavity formation, follicular and oocyte diameter, glutathione (GSH) concentration, mitochondrial activity and meiotic resumption were evaluated. After 12 days of culture, there was no significant difference among treatments in relation to follicular morphology, antral cavity formation, diameter and mitochondrial activity. Nevertheless, oocytes from follicles cultured in α-MEM+ showed greater GSH concentration than media containing M. oleifera extract. Furthermore, the concentration of 0.4 mg/ml M. oleifera extract significantly increased the percentage of fully grown oocyte (≥ 110 µm) when compared to the other treatments. In conclusion, the concentration of 0.4 mg/ml M. oleifera extract as a supplement of the culture medium, maintained the survival, and increased the percentage of fully grown oocytes.
Downloads
References
Ajagun‐Ogunleye, M. O., & Ebuehi, O. A. T. (2020). Evaluation of the anti‐aging and antioxidant action of Ananas sativa and Moringa oleifera in a fruit fly model organism. Journal of Food Biochemistry, 44(11), e13426. doi: 10.1111/jfbc.13426 DOI: https://doi.org/10.1111/jfbc.13426
Almansa-Ordonez, A., Bellido, R., Vassena, R., Barragan, M., & Zambelli, F. (2020). Oxidative stress in reproduction: a mitochondrial perspective. Biology, 9(269) 1-22. doi: 10.3390/biology9090269 DOI: https://doi.org/10.3390/biology9090269
Amelia, D., Santoso, B., Purwanto, B., Miftahussurur, M., & Joewono, H. T. (2018). Effects of Moringa oleifera on insulin levels and folliculogenesis in polycystic ovary syndrome model with insulin resistance. Immunology, Endocrine & Metabolic Agents in Medicinal Chemistry (Formerly Current Medicinal Chemistry-Immunology, Endocrine and Metabolic Agents), 18(1), 22-30. doi: 10.2174/1871522218666180426100754 DOI: https://doi.org/10.2174/1871522218666180426100754
Araújo, V. R., Chaves, R. N., Duarte, A. B. G., Hollanda Celestino, J. J. de, Silva, G. M. da, Fernandes, D. D., & Figueiredo, J. R. de. (2011). Effect of culture medium replacement protocol on the in vitro development of isolated caprine secondary follicles. Small Ruminant Research, 95(2-3), 139-143. doi: 10.1016/j.smallrumres.2010.09.014 DOI: https://doi.org/10.1016/j.smallrumres.2010.09.014
Asgari-Kafrani, A., Fazilati, M., & Nazem, H. (2020). Hepatoprotective and antioxidant activity of aerial parts of Moringa oleifera in prevention of non-alcoholic fatty liver disease in Wistar rats. South African Journal of Botany, 129 (1), 82-90. doi: 10.1016/j.sajb.2019.01.014 DOI: https://doi.org/10.1016/j.sajb.2019.01.014
Barakat, I. A. H., Khalil, W. K. B., & Al-Himaidi, A. R. (2015). Moringa oleífera extract modulates the expression of fertility related genes and elevation of calcium ions in sheep oocytes. Small Ruminant Research, 130(1), 67-75. doi: 10.1016/j.smallrumres.2015.06.011 DOI: https://doi.org/10.1016/j.smallrumres.2015.06.011
Bergamo, L. Z., Bonato, D. V., Bizarro-Silva, C., Bonato, F. G. C., Sanches, T. K., Cerezetti, M. B., Rossaneis, A. C., Verri, W. A., Morotti, F., & Seneda, M. M. (2021). Follicular development, morphological integrity, and oxidative stress in bovine preantral follicles cultured in vitro with ascorbic acid. Zygote, 1(3), 1-7. doi: 10.1017/S0967199421000903 DOI: https://doi.org/10.1017/S0967199421000903
Bogapathi, S. K., Shetty, R. H. S., Sumanta, N., & Venkataswamy, G. K. (2021). Effect of the Murraya koenigii and Moringa oleifera leaf extracts on the ovarian follicular population and other organ weights in rats (Rattus norvegicus). Indian Journal of Veterinary Sciences and Biotechnology, 17(3), 23-26. doi: 10.21887/ijvsbt.17.3.5
Cadenas, J., Maside, C., Ferreira, A. C. A., Vieira, L. A., Leiva-Revilla, J., Paes, V. M., Alves, B. G., Brandão, F. Z., Rodrigues, A. P. R., Wheeler, M. B., & Figueiredo, J. R. (2018). Relationship between follicular dynamics and oocyte maturation during in vitro culture as a non-invasive sign of caprine oocyte meiotic competence. Theriogenology, 107(1), 95-103. doi: 10.1016/j.theriogenology.2017.10.038 DOI: https://doi.org/10.1016/j.theriogenology.2017.10.038
Carvalho, F. A. L. de, Munekata, P. E. S., Lopes de Oliveira, A., Pateiro, M., Domínguez, R., Trindade, M. A., & Lorenzo, J. M. (2020a). Turmeric (Curcuma longa L.) extract on oxidative stability, physicochemical and sensory properties of fresh lamb sausage with fat replacement by tiger nut (Cyperus esculentus L.) oil. Food Research International, 136(1), 109487. doi: 10.1016/j.foodres.2020.109487 DOI: https://doi.org/10.1016/j.foodres.2020.109487
Carvalho, K. F., Machado, T. S., Garcia, B. M., Zangirolamo, A. F., Macabelli, C. H., Sugiyama, F. H. C., Grejo, M. P., Augusto, J. D., Neto, Tostes, K., Ribeiro, F. K. S., Sarapião, F. D., Pandey, A. K., Nociti, R. P., Tizioto, P., Coutinho, L. L., Meirelles, F. V., Guimarães, F. E. G., Pernas, L., Seneda, M. M., & Chiaratti, M. R. (2020b). Mitofusin 1 is required for oocyte growth and communication with follicular somatic cells. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 34(6), 76447660. doi: 10.1096/fj.201901761R DOI: https://doi.org/10.1096/fj.201901761R
Cavalcante, A. Y. P., Lins, T. L. B. G., Santos, J. M. S., Barros, V. R. P., Monte, A. P. O., Barberino, R. S., & Matos, M. H. T. (2018). Supplemented Morus nigra extract‐based medium associated with FSH enables the survival and growth of isolated ovine secondary ovarian follicles. Reproduction in Domestic Animals, 53(2), 423-432. doi: 10.1111/rda.13122. DOI: https://doi.org/10.1111/rda.13122
Cavilla, J. L., Kennedy, C. R., Byskov, A. G., & Hartshorne, G. M. (2008). Human immature oocytes grow during culture for IVM. Human Reproduction, 23(1), 37-45. doi: 10.1093/humrep/dem178 DOI: https://doi.org/10.1093/humrep/dem178
Cerezetti, M. B., González, S. M., Ferraz, C. R., Verri, W. A., Jr., Rabelo, E. A., Seneda, M. M., & Morotti, F. (2021). Impact of the antioxidant quercetin on morphological integrity and follicular development in the in vitro culture of Bos indicus female ovarian fragments. In Vitro Cellular & Developmental Biology, 57 (1), 856-864. doi: 10.1007/s11626-021-00629-8 DOI: https://doi.org/10.1007/s11626-021-00629-8
Crozet, N., Dahirel, M., & Gall, L. (2000). Meiotic competence of in vitro grown goat oocytes. Journal of Reproduction and Fertility, 118(2), 367-374. doi: 10.1530/jrf.0.1180367 DOI: https://doi.org/10.1530/jrf.0.1180367
Davoodian, N., Kadivar, A., Ahmadi, E., Nazari, H., & Mehrban, H. (2021). Quercetin effect on the efficiency of ovine oocyte vitrification at GV stage. Theriogenology, 174(1), 53-59. doi: 10.1016/jtheriogeno-logy. 2021.07.027 DOI: https://doi.org/10.1016/j.theriogenology.2021.07.027
Ding, Y., Shi, Y., & Yang, S. (2020). Molecular regulation of plant responses to environmental temperatures. Molecular Plant, 13(4), 544-564. doi: 10.1016/j.molp.2020.02.004 DOI: https://doi.org/10.1016/j.molp.2020.02.004
Fahey, J. W. (2017). Moringa oleifera. A review of the medicinal potential. Acta Horticulturae, 1158, 209-224. doi: 10.17660/ActaHortic.2017.1158.25 DOI: https://doi.org/10.17660/ActaHortic.2017.1158.25
González-Burgos, E., Ureña-Vacas, I., Sánchez, M., & Gómez-Serranillos, M. P. (2021). Nutritional value of Moringa Oleifera Lam. leaf powder extracts and their neuroprotective effects via antioxidative and mitochondrial regulation. Nutrients, 13(7), 2203-2216. doi: 10.3390/nu13072203 DOI: https://doi.org/10.3390/nu13072203
Gouveia, B. B., Macedo, T. J. S., Santos, J. M. S., Barberino, R. S., Menezes, V. G., Müller, M. C., & Matos, M. H. T. (2016). Supplemented base medium containing Amburana cearensis associated with FSH improves in vitro development of isolated goat preantral follicles. Theriogenology, 86(5), 1275-1284. doi: 10.1016/j.theriogenology.2016.04.068 DOI: https://doi.org/10.1016/j.theriogenology.2016.04.068
Huang, W., Nagano, M., Kang, S. S., Yanagawa, Y., & Takahashi, Y. (2014). Prematurational culture with 3-isobutyl-1-methylxanthine synchronizes meiotic progression of the germinal vesicle stage and improves nuclear maturation and embryonic development in in vitro-grown bovine oocytes. Journal of Reproduction and Development, 60(1), 9-13.doi:10.1262/jrd.2013-082 DOI: https://doi.org/10.1262/jrd.2013-082
Khadrawy, O., Gebremedhn, S., Salilew-Wondim, D., Taqi, M.O., Neuhoff, C., Tholen, E., Hoelker, M., Schellander, K., Tesfaye, D. (2019). Modulação endógena e exógena da resposta ao estresse oxidativo mediada por Nrf2 em células da granulosa bovina: implicação potencial para a função ovariana. International Journal of Molecular Sciences, 20(7), 1635. doi: 10.3390/ijms20071635. DOI: https://doi.org/10.3390/ijms20071635
Kona, S. S. R., Kumar, A. S., Punyakumari, B., Kumar, R. S., & Rao, V. H. (2021). Influence of TCM 199B, α-MEM, Waymouth MB 752/1 culture media, VEGF, Estradiol-17β, GDF-9 and FGF on in vitro development of preantral follicles in sheep. Veterinary and Animal Science, 13(1), 100189-100194. doi: 10.1016/j.vas.2021.100189 DOI: https://doi.org/10.1016/j.vas.2021.100189
Lakshmidevamma, T. N., Ugalat, J., Apoorva, K. A., Suresh, S. P., Doddamani, M., Kadam, S., & Fakrudin, B. (2021). Genetic diversity of Moringa (Moringa Oleifera Lam). The Moringa Genome, 1(1), 57-65. doi: 10.1007/978-3-030-80956-0_7 DOI: https://doi.org/10.1007/978-3-030-80956-0_7
Lievre, V., Becuwe, P., Bianchi, A., Bossenmeyer-Pourie, C., Koziel, V., Franco, P., Nicolas, M.B., Dauça, M., Vert, P., & Daval, J. L. (2001). Intracellular generation of free radicals and modifications of detoxifying enzymes in cultured neurons from the developing rat forebrain in response to transient hypoxia. Neuroscience, 105(2), 287-297. doi: 10.1016/S0306-4522(01)00189-0 DOI: https://doi.org/10.1016/S0306-4522(01)00189-0
Lins, T. L. B. G., Barberino, R. S., Monte, A. P. O., Pinto, J. G. C., Campinho, D. S. P., Palheta, R. C., Jr., Matos, M. H. T. (2021). Rutin promotes activation and reduces apoptosis of primordial follicles by regulating Akt phosphorylation after in vitro culture of ovine ovarian tissue. Theriogenology, 173, 64-72. doi: 10.1016/j.theriogenology.2021.07.018 DOI: https://doi.org/10.1016/j.theriogenology.2021.07.018
Lins, T. L. B. G., Cavalcante, A. Y. P., Santos, J. M. S., Menezes, V. G., Barros, V. R. P., Barberino, R. S., Bezerra, M.E.S., Macedo, T.J.S., Matos, M. H. T. (2017). Rutin can replace the use of three other antioxidants in the culture medium, maintaining the viability of sheep isolated secondary follicles. Theriogenology, 89(1), 263-270. doi: 10.1016/j.theriogenology.2016.11.019 DOI: https://doi.org/10.1016/j.theriogenology.2016.11.019
Luqman, S., Srivastava, S., Kumar, R., Maurya, A. K., & Chanda, D. (2012). Experimental assessment of Moringa oleifera leaf and fruit for its antistress, antioxidant, and scavenging potential using in vitro and in vivo assays. Evidence-based Complementary and Alternative Medicine, 2012(1), 51. doi: 10.1155/2012/519084 DOI: https://doi.org/10.1155/2012/519084
Macedo, T. J. S., Santos, J. M. S., Bezerra, M. É. S., Menezes, V. G., Gouveia, B. B., Barbosa, L. M. R., Lins, T. L. B. G., Monte, A. P. O., Barberino, R. S., Batista, A.M., Barros, V.R.P., Wischral, A., Queiroz, M. A. A., Araújo, G. G. L., & Matos, M .H. T. (2019). Immunolocalization of leptin and its receptor in the sheep ovary and in vitro effect of leptin on follicular development and oocyte maturation. Molecular and Cellular Endocrinology, 495(15), 110506-11513. doi: 10.1016/j.mce.2019.110506 DOI: https://doi.org/10.1016/j.mce.2019.110506
Martono, Y., Yanuarsih, F. F., Aminu, N. R., & Muninggar, J. (2019). Fractionation and determination of phenolic and flavonoid compound from Moringa oleifera leaves. Journal of Physics: Conference Series, 1307(1), 12014-12021. doi: 10.1088/1742-6596/1307/1/012014 DOI: https://doi.org/10.1088/1742-6596/1307/1/012014
Mbemya, G. T., Cadenas, J., Ribeiro de Sá, N. A., Damasceno Guerreiro, D., Donfack, N. J., Alberto Vieira, L., & Rodrigues, A. P. R. (2018). Supplementation of in vitro culture medium with FSH to grow follicles and mature oocytes can be replaced by extracts of Justicia insularis. PloS One, 13(12), 1-21. doi: 10.1371/journal.pone.0208760 DOI: https://doi.org/10.1371/journal.pone.0208760
Menezes, V. G. S., Barberino, R. S., Gouveia, B. B., Gonçalves, R. J., Almeida, J. R. G. S., & Matos, M. H. T. (2017). Extract of Amburana cearensis maintains the survival of ovine preantral follicles during long-term ovarian tissue transport and promotes primordial follicle activation after in vitro culture. Semina: Ciências Agrárias, 39(5), 2001-2016. doi: 10.5433/1679-0359.2018v39n5p2001 DOI: https://doi.org/10.5433/1679-0359.2018v39n5p2001
Mosharov, E., Cranford, M. R., & Banerjee, R. (2000). The quantitatively important relationship between homocysteine metabolism and glutathione synthesis by the transsulfuration pathway and its regulation by redox changes. Biochemistry, 39(42), 13005-13011. doi: 10.1021/bi001088w DOI: https://doi.org/10.1021/bi001088w
Mukherjee, A., Malik, H., Saha, A. P., Dubey, A., Singhal, D. K., Boateng, S., & Malakar, D. (2014). Resveratrol treatment during goat oocytes maturation enhances developmental competence of parthenogenetic and hand-made cloned blastocysts by modulating intracellular glutathione level and embryonic gene expression. Journal of Assisted Reproduction and Genetics, 31(1), 229-239. doi: 10.1007/s10815-013-0116-9 DOI: https://doi.org/10.1007/s10815-013-0116-9
Nascimento, T. S., Silva, I. S., Alves, M. C. M., Gouveia, B. B., Barbosa, L. M. R., Macedo, T. J., Santos, J. M. S., Monte, A. P. O., Matos, M. H. T., Padilha, F. F., Lima-Verde, I. B. (2019). Effect of red propolis extract isolated or encapsulated in nanoparticles on the in vitro culture of sheep preantral follicle: impacts on antrum formation, mitochondrial activity and glutathione levels. Reproduction in Domestic Animals, 54(1), 31-38. doi: 10.1111/rda.13347 DOI: https://doi.org/10.1111/rda.13347
Oldoni, T. L. C., Merlin, N., Bicas, T. C., Prasniewsk, A., Carpes, S. T., Ascari, J., & Thomé, G. (2021). Antihyperglycemic activity of crude extract and isolation of phenolic compounds with antioxidant activity from Moringa oleifera Lam. leaves grown in Southern Brazil. Food Research International, 141(1), 110082-110094. doi: 10.1016/j.foodres.2020.110082 DOI: https://doi.org/10.1016/j.foodres.2020.110082
Paulino, L. R., Assis, E. I. de, Azevedo, V. A., Silva, B. R., Cunha, E. V. da, & Silva, J. R. (2022). Why is it so difficult to have competent oocytes from in vitro cultured preantral follicles?. Reproductive Sciences, 29(12), 1-14. doi: 10.1007/s43032-021-00840-8 DOI: https://doi.org/10.1007/s43032-021-00840-8
Piovesana, A., & Noreña, C. P. Z. (2019). Study of acidified aqueous extraction of phenolic compounds from Hibiscus sabdariffa L. calyces. The Open Food Science Journal, 11(1), 25-34. doi: 10.2174/1874256401911010025 DOI: https://doi.org/10.2174/1874256401911010025
Qwele, K., Hugo, A., Oyedemi, S. O., Moyo, B., Masika, P. J., & Muchenje, V. (2013). Chemical composition, fatty acid content and antioxidant potential of meat from goats supplemented with Moringa (Moringa oleifera) leaves, sunflower cake and grass hay. Meat Science, 93(3), 455-462. doi: 10.1016/j.meatsci.2012.11.009 DOI: https://doi.org/10.1016/j.meatsci.2012.11.009
Sá, N. A., Ferreira, A. C., Sousa, F. G., Duarte, A. B., Paes, V. M., Cadenas, J., & Figueiredo, J. R. (2020). First pregnancy after in vitro culture of early antral follicles in goats: positive effects of anethole on follicle development and steroidogenesis. Molecular Reproduction and Development, 87(9), 966-977. doi: 10.1002/mrd.23410 DOI: https://doi.org/10.1002/mrd.23410
Santos, J. M. S., Monte, A. P. O., Lins, T. L. B. G., Barberino, R. S., Menezes, V. G., Gouveia, B. B., & Matos, M. H. T. (2019). Kaempferol can be used as the single antioxidant in the in vitro culture medium, stimulating sheep secondary follicle development through the phosphatidylinositol 3-kinase signaling pathway. Theriogenology, 136(1), 86-94. doi: 10.1016/j.theriogenology.2019.06.036 DOI: https://doi.org/10.1016/j.theriogenology.2019.06.036
Silva, G. A., Araújo, L. B., Silva, L. C., Gouveia, B. B., Barberino, R. S., Lins, T. L. B., Monte, A. P. O., Macedo, J.S., Santos, J. M. S, Menezes, V. G., Silva, R. L. S., &Matos, M. H. T. (2021a). Gallic acid promotes the in vitro development of sheep secondary isolated follicles involving the phosphatidylinositol 3-kinase pathway. Animal Reproduction Science, 230(1), 106767. doi: 10.1016/j.anireprosci.2021.106767 DOI: https://doi.org/10.1016/j.anireprosci.2021.106767
Silva, A. A. A., Silva, M. N. P., Figueiredo, L. B. F., Gonçalves, J. D., Silva, M. J. S., Loiola, M. L. G., Bastos, B. D. M., Oliveira, R. A., Ribeiro, L. G. M., Barberino, R. S., Gouveia, B. B., Monte, A. P. O., Nogueira, D. M., Cordeiro, M. F., Matos, M. H. T., & Lopes, E. S., Jr. (2018). Quercetin influences in vitro maturation, apoptosis and metabolically active mitochondria of goat oocytes. Zygote, 26(6), 465-470. doi: 10.1017/S0967199418000485 DOI: https://doi.org/10.1017/S0967199418000485
Silva, R. F., Lima, L. F., Rocha, R. M. P., Brito, I. R., Silva, G. M., Correia, H. H. V., Rodrigues, G. Q., Ferreira, A. C. A., Nunes-Pinheiro, D. C. S., Moura, A. A. A. N., Silveira, L. B. R., Lo Turco, E. G., Wheeler, M. B., Rodrigues, A. P. R., Campello, C. C., & Figueiredo, J. R. (2021b). In vitro long-term culture of isolated ovine preantral follicles: Influence of ethanol on steroid production, oocyte meiotic resumption, and metabolomic profile. Research in Veterinary Science, 135(1), 432-441. doi: 10.1016/j.rvsc.2020.10.029 DOI: https://doi.org/10.1016/j.rvsc.2020.10.029
Su, B., & Chen, X. (2020). Current status and potential of Moringa oleifera leaf as an alternative protein source for animal feeds. Frontiers in Veterinary Science, 7(53), 1-13. doi: 10.3389/fvets.2020.00053 DOI: https://doi.org/10.3389/fvets.2020.00053
Yang, H., Xie, Y., Yang, D., & Ren, D. (2017) A apoptose induzida por estresse oxidativo em células da granulosa envolve JNK, p53 e Puma. Oncotarget, 8(15), 25310-25322. doi: 10.18632/oncotarget.15813 DOI: https://doi.org/10.18632/oncotarget.15813
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Semina: Ciências Agrárias
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Semina: Ciências Agrárias adopts the CC-BY-NC license for its publications, the copyright being held by the author, in cases of republication we recommend that authors indicate first publication in this journal.
This license allows you to copy and redistribute the material in any medium or format, remix, transform and develop the material, as long as it is not for commercial purposes. And due credit must be given to the creator.
The opinions expressed by the authors of the articles are their sole responsibility.
The magazine reserves the right to make normative, orthographic and grammatical changes to the originals in order to maintain the cultured standard of the language and the credibility of the vehicle. However, it will respect the writing style of the authors. Changes, corrections or suggestions of a conceptual nature will be sent to the authors when necessary.