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
Maite del Collado A B F , Naiara Z. Saraiva C , Flavia L. Lopes D , Roberta C. Gaspar B , Luciana C. Padilha B , Roberta R. Costa E , Guilherme F. Rossi B , Roberta Vantini B and Joaquim M. Garcia BA Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, USP, Avenida Duque de Caxias Norte, 225, 13635-900, Pirassununga, SP, Brazil.
B Departamento de Medicina Veterinária Preventiva e Reprodução Animal, Faculdade de Ciências Agrárias e Veterinárias, UNESP, Via de Acesso Prof. Paulo D. Castellane SN, 14884-900, Jaboticabal, SP, Brazil.
C Empresa Brasileira de Pesquisa Agropecuária, Embrapa Amazônia Oriental, Travessa Dr. Enéas Pinheiro s/n, 66095-100, Belém, PA, Brazil.
D Departamento de Apoio, Produção e Saúde Animal, Faculdade de Medicina Veterinária de Araçatuba, UNESP, Rua Clóvis Pestana, 793, 16050-680, Araçatuba, SP, Brazil.
E Departamento de Biologia Celular e Molecular e de Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, USP, Avenida Bandeirantes, 3900, 14049-900, Ribeirão Preto, SP, Brazil.
F Corresponding author. Email: delcollado@hotmail.com
Reproduction, Fertility and Development 28(11) 1721-1732 https://doi.org/10.1071/RD15067
Submitted: 19 February 2015 Accepted: 2 April 2015 Published: 19 May 2015
Abstract
Proper oocyte maturation is crucial for subsequent embryo development; however, oocyte mitochondrial and lipid-droplet behaviour are still poorly understood. Although excessive lipid accumulation during in vitro production (IVP) of bovine embryos has been linked with impaired cryotolerance, lipid oxidation is essential for adequate energy supply. Fetal bovine serum (FBS) and bovine serum albumin (BSA) are supplements used during IVP, containing high and low lipid content, respectively. This study aimed to understand how these supplements influence oocyte mitochondrial and lipid behaviour during in vitro maturation (IVM) in comparison to in vivo maturation, as well as their influence on development rates and embryo lipid accumulation during IVP. We demonstrate that only in vivo-matured oocytes maintained correlation between lipid content and active mitochondria. IVM media containing FBS increased total lipid content 18-fold and resulted in higher lipid accumulation in oocytes when compared with media with BSA. IVM using a lower FBS concentration combined with BSA resulted in satisfactory maturation and embryo development and also reduced lipid accumulation in blastocysts. In conclusion, IVM causes changes in mitochondrial and lipid dynamics, which may have negative effects on oocyte development rates and embryo lipid accumulation. Moreover, decreasing FBS concentrations during IVM may reduce embryo lipid accumulation without affecting production rates.
Additional keywords: in vitro production (IVP), lipid droplet, mitochondria, reproduction.
References
Aardema, H., Vos, P. L., Lolicato, F., Roelen, B. A., Knijn, H. M., Vaandrager, A. B., Helms, J. B., and Gadella, B. M. (2011). Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol. Reprod. 85, 62–69.| Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFOls74%3D&md5=91c35c1502e6480acc58b76f6a2faff4CAS | 21311036PubMed |
Abd El Razek, I. M., Charpigny, G., Kodja, S., Marquant-Leguienne, B., Mermillod, P., Guyader-Joly, C., and Humblot, P. (2000). Difference in lipid composition between in vivo- and in vitro-produced bovine embryos. Theriogenology 54, 346.
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. Mol. Reprod. Dev. 61, 57–66.
| Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptVejur4%3D&md5=9f309a13a31a61fae851812e002e6e0eCAS | 11774376PubMed |
Adamiak, S. J., Powell, K., Rooke, J. A., Webb, R., and Sinclair, K. D. (2006). Body composition, dietary carbohydrates and fatty acids determine post-fertilisation development of bovine oocytes in vitro. Reproduction 131, 247–258.
| Body composition, dietary carbohydrates and fatty acids determine post-fertilisation development of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsL8%3D&md5=4387bb5a6237925289f117ee4a43d24fCAS | 16452718PubMed |
Ali, A., and Sirard, M. A. (2002). Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation. Biol. Reprod. 66, 901–905.
| Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCltLs%3D&md5=ea9f5bc0a8ea59174ce03559d241b944CAS | 11906907PubMed |
Auclair, S., Uzbekov, R., Elis, S., Sanchez, L., Kireev, I., Lardic, L., Dalbies-Tran, R., and Uzbekova, S. (2013). Absence of cumulus cells during in vitro maturation affects lipid metabolism in bovine oocytes. Am. J. Physiol. Endocrinol. Metab. 304, E599–E613.
| Absence of cumulus cells during in vitro maturation affects lipid metabolism in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVKnsb8%3D&md5=444c5c8ccde11181eaa8cee0ad69d510CAS | 23321473PubMed |
Bickel, P. E., Tansey, J. T., and Welte, M. A. (2009). PAT proteins, an ancient family of lipid-droplet proteins that regulate cellular lipid stores. Biochim. Biophys. Acta 1791, 419–440.
| PAT proteins, an ancient family of lipid-droplet proteins that regulate cellular lipid stores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntVKlsrc%3D&md5=a192103d0802ed82af26ed49d4494390CAS | 19375517PubMed |
Chen, J., Hudson, E., Chi, M. M., Chang, A. S., Moley, K. H., Hardie, D. G., and Downs, S. M. (2006). AMPK regulation of mouse oocyte meiotic resumption in vitro. Dev. Biol. 291, 227–238.
| AMPK regulation of mouse oocyte meiotic resumption in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1WisLk%3D&md5=b1e0e8c4db64fbed27491134f569c258CAS | 16443210PubMed |
Cherr, G. N., Drobnis, E. Z., and Katz, D. F. (1988). Localisation of cortical granule constituents before and after exocytosis in the hamster egg. J. Exp. Zool. 246, 81–93.
| Localisation of cortical granule constituents before and after exocytosis in the hamster egg.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktVCnu78%3D&md5=65b1e2ccbe127915d9445ec6d637812eCAS | 3133448PubMed |
Cummins, J. M. (2004). The role of mitochondria in the establishment of oocyte functional competence. Eur. J. Obstet. Gynecol. Reprod. Biol. 115, S23–S29.
| The role of mitochondria in the establishment of oocyte functional competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvVKlur8%3D&md5=048d7136df39cef0d5b465381783ed6dCAS | 15196712PubMed |
Downs, S. M., Mosey, J. L., and Klinger, J. (2009). Fatty-acid oxidation and meiotic resumption in mouse oocytes. Mol. Reprod. Dev. 76, 844–853.
| Fatty-acid oxidation and meiotic resumption in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptleht7c%3D&md5=3b14836c82b9bafe20052faa496b7360CAS | 19455666PubMed |
Dunning, K. R., Cashman, K., Russell, D. L., Thompson, J. G., Norman, R. J., and Robker, R. L. (2010). Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol. Reprod. 83, 909–918.
| Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFahurfN&md5=d2b87b938fd1b9207ccd0d890a41f1beCAS | 20686180PubMed |
Dunning, K. R., Anastasi, M. R., Zhang, V. J., Russell, D. L., and Robker, R. L. (2014). Regulation of fatty-acid oxidation in mouse cumulus–oocyte complexes during maturation and modulation by PPAR agonists. PLoS One 9, e87327.
| Regulation of fatty-acid oxidation in mouse cumulus–oocyte complexes during maturation and modulation by PPAR agonists.Crossref | GoogleScholarGoogle Scholar | 24505284PubMed |
Ferguson, E. M., and Leese, H. J. (1999). Triglyceride content of bovine oocytes and early embryos. J. Reprod. Fertil. 116, 373–378.
| Triglyceride content of bovine oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslOltbc%3D&md5=7dcf1ca4e4190921db5a3506b5f051d8CAS | 10615263PubMed |
Ferreira, C. R., Catharino, R. R., Saraiva, S. A., Fonsêca, M. F. R., Basso, A. C., Pontes, J. H. F., Ereno, J. C., and Eberlin, M. N. (2008). Perspectivas para aplicação da técnica de espectrometria de massas na caracterização do lipidoma de oócitos e embriões bovinos produzidos in vitro. Acta Clientage Veterinarian 36, 549.
Ferreira, C. R., Eberlin, L. S., Hallett, J. E., and Cooks, R. G. (2012). Single oocyte and single embryo lipid analysis by desorption electrospray ionisation mass spectrometry. J. Mass Spectrom. 47, 29–33.
| Single oocyte and single embryo lipid analysis by desorption electrospray ionisation mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yms7Y%3D&md5=beab83a6543a046a93a20e4cb8665636CAS | 22282086PubMed |
Gilbert, S. F. (2003). ‘Developmental Biology, 7th edn.’ (Sinauer Associates: Sunderland, MA.)
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 ionisation mass spectrometry reveals lipid metabolism of individual oocytes and embryos. PLoS One 8, e74981.
| Desorption electrospray ionisation mass spectrometry reveals lipid metabolism of individual oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 24073231PubMed |
Hyttel, P., Callesen, H., and Greve, T. (1986). Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J. Reprod. Fertil. 76, 645–656.
| Ultrastructural features of preovulatory oocyte maturation in superovulated cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL287pvFyrtQ%3D%3D&md5=8296c99176fa9ec87c0627ea5752db2eCAS | 3084771PubMed |
IETS (2012). ‘IETS 2012 Statistics and Data Retrieval Committee Report’. Available at http://www.iets.org/pdf/comm_data/December2012.pdf [Verified 24 April 2015]
Kim, J. Y., Kinoshita, M., Ohnishi, M., and Fukui, Y. (2001). Lipid and fatty-acid analysis of fresh and frozen–thawed immature and in vitro-matured bovine oocytes. Reproduction 122, 131–138.
| Lipid and fatty-acid analysis of fresh and frozen–thawed immature and in vitro-matured bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis70%3D&md5=2b5049110598d7946e58d5859cdefa02CAS | 11425337PubMed |
Kruip, T. A. M., Cran, D. G., Van Beneden, T. H., and Dieleman, S. J. (1983). Structural changes in bovine oocytes during final maturation in vivo. Gamete Res. 8, 29–47.
| Structural changes in bovine oocytes during final maturation in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlvVyisLc%3D&md5=fbb3ccdccd16f7d70416030d03e2d31cCAS |
Kuerschner, L., Moessinger, C., and Thiele, C. (2008). Imaging of lipid biosynthesis: how a neutral lipid enters lipid droplets. Traffic 9, 338–352.
| Imaging of lipid biosynthesis: how a neutral lipid enters lipid droplets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVakur4%3D&md5=a0740c033814877b42312840de38c1bbCAS | 18088320PubMed |
Leibfried-Rutledge, M. L., Critser, E. S., Eyestone, W. H., Northey, D. L., and Fiste, N. L. (1987). Development potential of bovine oocytes matured in vitro and in vivo. Biol. Reprod. 36, 376–383.
| Development potential of bovine oocytes matured in vitro and in vivo.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s3hsVemsQ%3D%3D&md5=89872d18703cc5de25018e6f9c1f7825CAS | 3580458PubMed |
Leroy, J. L., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., and Van Soom, A. (2005). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130, 485–495.
| Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rJ&md5=16ddfb8af1de3a55f051d7e88b361557CAS | 16183866PubMed |
Paczkowski, M., Silva, E., Schoolcraft, W. B., and Krisher, R. L. (2013). Comparative importance of fatty-acid beta-oxidation to nuclear maturation, gene expression and glucose metabolism in mouse, bovine and porcine cumulus–oocyte complexes. Biol. Reprod. 88, 111.
| Comparative importance of fatty-acid beta-oxidation to nuclear maturation, gene expression and glucose metabolism in mouse, bovine and porcine cumulus–oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 23536372PubMed |
Rizos, D., Fair, T., Papadopoulos, S., Boland, M. P., and Lonergan, P. (2002). Developmental, qualitative and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro. Mol. Reprod. Dev. 62, 320–327.
| Developmental, qualitative and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlWku7w%3D&md5=b3e5788f4300868e7080ccd01baf672fCAS | 12112595PubMed |
Rizos, D., Gutiérrez-Adán, A., Pérez-Garnelo, S., de la Fuente, J., Boland, M. P., and Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance and messenger RNA expression. Biol. Reprod. 68, 236–243.
| Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance and messenger RNA expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFWj&md5=7eac6d4191c91ddad2567e3bfaf367f2CAS | 12493719PubMed |
Romek, M., Gajda, B., Rolka, M., and Smorag, Z. (2011). Mitochondrial activity and morphology in developing porcine oocytes and pre-implantation non-cultured and cultured embryos. Reprod. Domest. Anim. 46, 471–480.
| Mitochondrial activity and morphology in developing porcine oocytes and pre-implantation non-cultured and cultured embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mvos1Gqsw%3D%3D&md5=6422a116dc531189a30faad2d31a2395CAS | 20955375PubMed |
Russell, D. F., Baqir, S., Bordignon, J., and Betts, D. H. (2006). The impact of oocyte maturation media on early bovine embryonic development. Mol. Reprod. Dev. 73, 1255–1270.
| The impact of oocyte maturation media on early bovine embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptlSnu7w%3D&md5=79bfe842c85872325ed306d27b454d57CAS | 16865717PubMed |
Sata, R., Tsujii, H., Abe, H., Yamashita, S., and Hoshi, H. (1999). Fatty-acid composition of bovine embryos cultured in serum-free and serum-containing medium during early embryonic development. J. Reprod. Dev. 45, 97–103.
| Fatty-acid composition of bovine embryos cultured in serum-free and serum-containing medium during early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFentb4%3D&md5=27a5a4a3ae762d43fedbebe15eeba240CAS |
Stone, S. J., Levin, M. C., Zhou, P., Han, J. Y., Walther, T. C., and Farese, R. V. (2009). The endoplasmic reticulum enzyme DGAT2 is found in mitochondria-associated membranes and has a mitochondrial targeting signal that promotes its association with mitochondria. J. Biol. Chem. 284, 5352–5361.
| The endoplasmic reticulum enzyme DGAT2 is found in mitochondria-associated membranes and has a mitochondrial targeting signal that promotes its association with mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVSntLk%3D&md5=d55dc043d0825b23d204a7c7c5640934CAS | 19049983PubMed |
Tarazona, A. M., Rodriguez, J. I., Restrepo, L. F., and Olivera-Angel, M. (2006). Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro. Reprod. Domest. Anim. 41, 5–11.
| Mitochondrial activity, distribution and segregation in bovine oocytes and in embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28%2FjsVWnuw%3D%3D&md5=038bd7348b9750f05387b04b8c268b62CAS | 16420320PubMed |
Tsujii, H., Yahia Khandoker, M. A. M., and Hamano, K. (2001). Lipid in mammalian embryo development. J. Mamm. Ova Res. 18, 73–80.
| Lipid in mammalian embryo development.Crossref | GoogleScholarGoogle Scholar |
Van Blerkom, J. (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.
| Mitochondrial function in the human oocyte and embryo and their role in developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWrsrzM&md5=d8fce630c456055ad27de96490482f43CAS | 20933103PubMed |