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In vitro maturation in synthetic oviductal fluid increases gene expression associated with quality and lipid metabolism in bovine oocytes

Published online by Cambridge University Press:  13 November 2023

Adriano Felipe Mendes
Affiliation:
University of Western São Paulo (UNOESTE), Presidente Prudente, São Paulo, Brazil
Raquel Zaneti Puelker
Affiliation:
São Paulo State University (UNESP), Botucatu, São Paulo, Brazil
Lilian Francisco Arantes de Souza
Affiliation:
University of Western São Paulo (UNOESTE), Presidente Prudente, São Paulo, Brazil Federal Rural University of Pernambuco (UFRPE), Recife, Pernambuco, Brazil
Andréa Renesto Coimbra Jacintho
Affiliation:
University of Western São Paulo (UNOESTE), Presidente Prudente, São Paulo, Brazil
Priscila Helena dos Santos
Affiliation:
São Paulo State University (UNESP), Botucatu, São Paulo, Brazil
Ines Cristina Giometti
Affiliation:
University of Western São Paulo (UNOESTE), Presidente Prudente, São Paulo, Brazil
Sheila Merlo Firetti
Affiliation:
University of Western São Paulo (UNOESTE), Presidente Prudente, São Paulo, Brazil
Anthony César de Souza Castilho
Affiliation:
University of Western São Paulo (UNOESTE), Presidente Prudente, São Paulo, Brazil São Paulo State University (UNESP), Botucatu, São Paulo, Brazil
Marilice Zundt
Affiliation:
University of Western São Paulo (UNOESTE), Presidente Prudente, São Paulo, Brazil
Claudia Maria Bertan Membrive
Affiliation:
São Paulo State University (UNESP), Dracena, São Paulo, Brazil
Caliê Castilho*
Affiliation:
University of Western São Paulo (UNOESTE), Presidente Prudente, São Paulo, Brazil
*
Corresponding author: Caliê Castilho; Email: calie@unoeste.br

Summary

Traditionally, in vitro oocyte and embryo culture progresses through a series of varying culture medium. To investigate simplifying the in vitro production of bovine cumulus–oocyte complexes (COCs), this study used synthetic oviductal fluid (SOF) supplemented with conjugated linoleic acid (CLA). Special interest was placed on gene expression linked to lipid metabolism and oocyte maturation. COCs were matured in different media: Medium 199 (M199 group), M199 with 100 μM CLA (M199 + CLA group), SOF (SOF group), and SOF with 100 μM CLA (SOF + CLA group). COCs matured with SOF showed a higher relative abundance of mRNA of quality indicators gremlin 1 (GREM1) and prostaglandin-endoperoxide synthase 2 (PTGS2) in oocytes, and GREM1 in cumulus cells compared with in the M199 group. SOF medium COCs had a higher relative abundance of fatty acid desaturase 2 (FADS2) compared with the M199 group, which is essential for lipid metabolism in oocytes. Furthermore, the abundance of stearoyl-coenzyme A desaturase 1 (SCD1) in oocytes matured with SOF was not influenced by the addition of CLA, whereas the relative abundance of SCD1 was reduced in M199 medium with CLA. We concluded that maturation in SOF medium results in a greater abundance of genes linked to quality and lipidic metabolism in oocytes, regardless of the addition of CLA.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Aardema, H., Van Tol, H. T. A., Wubbolts, R. W., Brouwers, J. F. H. M., Gadella, B. M. and Roelen, B. A. J. (2017). Stearoyl-CoA desaturase activity in bovine cumulus cells protects the oocyte against saturated fatty acid stress. Biology of Reproduction, 96(5), 982992. doi: 10.1095/BIOLREPROD.116.146159 CrossRefGoogle ScholarPubMed
Abe, H., Yamashita, S., Satoh, T. and Hoshi, H. (2002). Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media. Molecular Reproduction and Development, 61(1), 5766. doi: 10.1002/MRD.1131 CrossRefGoogle ScholarPubMed
Brookheart, R. T., Michel, C. I. and Schaffer, J. E. (2009). As a matter of fat. Cell Metabolism, 10(1), 912. https://doi.org/10.1016/J.CMET.2009.03.011 CrossRefGoogle ScholarPubMed
Cunnane, S. C. (2003). Problems with essential fatty acids: Time for a new paradigm? Progress in Lipid Research, 42(6), 544568. doi: 10.1016/s0163-7827(03)00038-9 CrossRefGoogle ScholarPubMed
del Collado, M., Saraiva, N. Z., Lopes, F. L., Gaspar, R. C., Padilha, L. C., Costa, R. R., Rossi, G. F., Vantini, R. and Garcia, J. M. (2015). Influence of bovine serum albumin and fetal bovine serum supplementation during in vitro maturation on lipid and mitochondrial behaviour in oocytes and lipid accumulation in bovine embryos. Reproduction, Fertility, and Development, 28(11), 17211732. doi: 10.1071/RD15067 CrossRefGoogle Scholar
Duque, P., Hidalgo, C. O., Gómez, E., Pintado, B., Facal, N. and Díez, C. (2003). Macromolecular source as dependent on osmotic pressure and water source: Effects on bovine in vitro embryo development and quality. Reproduction, Nutrition, Development, 43(6), 487496. doi: 10.1051/RND:2004007 CrossRefGoogle ScholarPubMed
Fayezi, S., Ghaffari Novin, M., Darabi, M., Norouzian, M., Nouri, M., Farzadi, L. and Darabi, M. (2018). Primary culture of human cumulus cells requires stearoyl-coenzyme A desaturase 1 activity for steroidogenesis and enhancing oocyte in vitro maturation. Reproductive Sciences, 25(6), 844853. doi: 10.1177/1933719117698578 CrossRefGoogle ScholarPubMed
Gandhi, A. P., Lane, M., Gardner, D. K. and Krisher, R. L. (2000). A single medium supports development of bovine embryos throughout maturation, fertilization and culture. Human Reproduction, 15(2), 395401. doi: 10.1093/HUMREP/15.2.395 CrossRefGoogle ScholarPubMed
Goldrat, O., van den Steen, G., Gonzalez-Merino, E., Dechène, J., Gervy, C., Delbaere, A., Devreker, F., de Maertelaer, V. and Demeestere, I. (2019). Letrozole-associated controlled ovarian hyperstimulation in breast cancer patients versus conventional controlled ovarian hyperstimulation in infertile patients: Assessment of oocyte quality related biomarkers. Reproductive Biology and Endocrinology: RB&E, 17(1), 3. doi: 10.1186/s12958-018-0443-x CrossRefGoogle ScholarPubMed
González-Serrano, A. F., Pirro, V., Ferreira, C. R., Oliveri, P., Eberlin, L. S., Heinzmann, J., Lucas-Hahn, A., Niemann, H. and Cooks, R. G. (2013). Desorption electrospray ionization mass spectrometry reveals lipid metabolism of individual oocytes and embryos. PLOS ONE, 8(9), e74981. doi: 10.1371/JOURNAL.PONE.0074981 CrossRefGoogle ScholarPubMed
Hosseini, S. M., Moulavi, F., Hajian, M., Abedi, P., Forouzanfar, M., Ostad Hosseini, S., Hosseini, L., Pirestani, A., Ghasemzadeh Nava, H., Tajik, P., Shahverdi, A. H. and Nasr-Esfahani, M. H. (2008). Highly efficient in vitro production of bovine blastocyst in cell-free sequential synthetic oviductal fluid vs. TCM199 vero cell co-culture system. International Journal of Fertility and Sterility, 2(2), 6673. doi: 10.22074/IJFS.2008.45712 Google Scholar
Khurana, N. K. and Niemann, H. (2000). Energy metabolism in preimplantation bovine embryos derived in vitro or in vivo . Biology of Reproduction, 62(4), 847856. doi: 10.1095/BIOLREPROD62.4.847 CrossRefGoogle ScholarPubMed
Lapa, M., Marques, C. C., Alves, S. P., Vasques, M. I., Baptista, M. C., Carvalhais, I., Silva Pereira, M., Horta, A. E. M., Bessa, R. J. P. and Pereira, R. M. (2011). Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition. Reproduction in Domestic Animals, 46(5), 904910. doi: 10.1111/j.1439-0531.2011.01762.x CrossRefGoogle ScholarPubMed
Leão, B. C. S., Rocha-Frigoni, N. A. S., Cabral, E. C., Coelho, M. B., Ferreira, C. R., Eberlin, M. N., Accorsi, M. F., Nogueira, É. and Mingoti, G. Z. (2015). Improved embryonic cryosurvival observed after in vitro supplementation with conjugated linoleic acid is related to changes in the membrane lipid profile. Theriogenology, 84(1), 127136. doi: 10.1016/J.THERIOGENOLOGY.2015.02.023 CrossRefGoogle ScholarPubMed
Matos, J. E., Marques, C. C., Moura, T. F., Baptista, M. C., Horta, A. E., Soveral, G. and Pereira, R. M. (2015). Conjugated linoleic acid improves oocyte cryosurvival through modulation of the cryoprotectants influx rate. Reproductive Biology and Endocrinology: RB&E, 13, 60. doi: 10.1186/s12958-015-0059-3 CrossRefGoogle ScholarPubMed
McKenzie, L. J., Pangas, S. A., Carson, S. A., Kovanci, E., Cisneros, P., Buster, J. E., Amato, P. and Matzuk, M. M. (2004). Human cumulus granulosa cell gene expression: A predictor of fertilization and embryo selection in women undergoing IVF. Human Reproduction, 19(12), 28692874. doi: 10.1093/HUMREP/DEH535 CrossRefGoogle ScholarPubMed
Pandey, S., Somal, A., Parmar, M. S., Gupta, S., Bharti, M. K., Bhat, I. A., Indu, B., Chandra, V., Kumar, G. S. and Sharma, G. T. (2018). Effect of roscovitine on developmental competence of small follicle-derived buffalo oocytes. Indian Journal of Medical Research, 148(Suppl.), S140S150. doi: 10.4103/ijmr.IJMR_2068_17 Google ScholarPubMed
Pangas, S. A., Jorgez, C. J. and Matzuk, M. M. (2004). Growth differentiation factor 9 regulates expression of the bone morphogenetic protein antagonist gremlin. Journal of Biological Chemistry, 279(31), 3228132286. doi: 10.1074/jbc.M403212200 CrossRefGoogle ScholarPubMed
Pereira, R. M., Baptista, M. C., Vasques, M. I., Horta, A. E. M., Portugal, P. V., Bessa, R. J. B., Silva, J. C., Pereira, M. S. and Marques, C. C. (2007). Cryosurvival of bovine blastocysts is enhanced by culture with trans-10 cis-12 conjugated linoleic acid (10t,12c CLA). Animal Reproduction Science, 98(3–4), 293301. doi: 10.1016/J.ANIREPROSCI.2006.03.015 CrossRefGoogle Scholar
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Research, 29(9), e45. doi: 10.1093/nar/29.9.e45 CrossRefGoogle ScholarPubMed
Russell, D. F., Baqir, S., Bordignon, J. and Betts, D. H. (2006). The impact of oocyte maturation media on early bovine embryonic development. Molecular Reproduction and Development, 73, 12551270. https://doi.org/10.1002/mrd.20553 CrossRefGoogle ScholarPubMed
Shao, L., Chian, R. C., Xu, Y., Yan, Z, Zhang, Y., Gao, C., Gao, L., Liu, J., Cui, Y. (2015). Genomic expression profiles in cumulus cells derived from germinal vesicle and MII mouse oocytes. Reproduction Fertility and Development, 5 (20). doi: 10.1071/RD15077.Google Scholar
Shimada, M., Hernandez-Gonzalez, I., Gonzalez-Robayna, I. and Richards, J. S. (2006). Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: Key roles for prostaglandin synthase 2 and progesterone receptor. Molecular Endocrinology, 20(6), 13521365. doi: 10.1210/me.2005-0504 CrossRefGoogle ScholarPubMed
Stoffel, W., Holz, B., Jenke, B., Binczek, E., Günter, R. H., Kiss, C., Karakesisoglou, I., Thevis, M., Weber, A. A., Arnhold, S. and Addicks, K. (2008). Δ6-Desaturase (FADS2) deficiency unveils the role of ω3- and ω6-polyunsaturated fatty acids. EMBO Journal, 27(17), 22812292. doi: 10.1038/EMBOJ.2008.156 CrossRefGoogle ScholarPubMed
Sugimura, S., Ritter, L. J., Rose, R. D., Thompson, J. G., Smitz, J., Mottershead, D. G. and Gilchrist, R. B. (2015). Promotion of EGF receptor signaling improves the quality of low developmental competence oocytes. Developmental Biology, 403: 139149. https://doi.org/10.1016/j.ydbio.2015.05.008 CrossRefGoogle ScholarPubMed
Warzych, E., Pawlak, P., Pszczola, M., Cieslak, A., Madeja, Z. E. and Lechniak, D. (2017). Interactions of bovine oocytes with follicular elements with respect to lipid metabolism. Animal Science Journal = Nihon Chikusan Gakkaiho, 88(10), 14911497. doi: 10.1111/ASJ.12799 Google ScholarPubMed
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