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Reduction in cytoplasmic lipid content in bovine embryos cultured in vitro with linoleic acid in semi-defined medium is correlated with increases in cryotolerance

Published online by Cambridge University Press:  09 September 2015

Mônica F. Accorsi ,
Beatriz Caetano da Silva Leão ,
Nathália Alves de Souza Rocha-Frigoni ,
Silvia Helena Venturoli Perri  and
Gisele Zoccal Mingoti
Mônica F. Accorsi
Affiliation:
School of Veterinary Medicine, Laboratory of Reproductive Physiology, UNESP–Universidade Estadual Paulista, Araçatuba, SP 16050–680, Brazil.
Beatriz Caetano da Silva Leão
Affiliation:
School of Veterinary Medicine, Laboratory of Reproductive Physiology, UNESP–Universidade Estadual Paulista, Araçatuba, SP 16050–680, Brazil. School of Agrarian and Veterinarian Sciences, Departament of Animal Reproduction, UNESP–Universidade Estadual Paulista, Jaboticabal, SP 16050–680, Brazil.
Nathália Alves de Souza Rocha-Frigoni
Affiliation:
School of Veterinary Medicine, Laboratory of Reproductive Physiology, UNESP–Universidade Estadual Paulista, Araçatuba, SP 16050–680, Brazil. School of Agrarian and Veterinarian Sciences, Departament of Animal Reproduction, UNESP–Universidade Estadual Paulista, Jaboticabal, SP 16050–680, Brazil.
Silvia Helena Venturoli Perri
Affiliation:
School of Veterinary Medicine, Laboratory of Reproductive Physiology, UNESP–Universidade Estadual Paulista, Araçatuba, SP 16050–680, Brazil.
Gisele Zoccal Mingoti*
Affiliation:
School of Veterinary Medicine, Department of Animal Health, UNESP–Universidade Estadual Paulista, Araçatuba 16050–680, São Paulo, Brazil. School of Agrarian and Veterinarian Sciences, Departament of Animal Reproduction, UNESP–Universidade Estadual Paulista, Jaboticabal, SP 16050–680, Brazil.
*
All correspondence to: G.Z. Mingoti, School of Veterinary Medicine, Department of Animal Health, UNESP–Universidade Estadual Paulista, Araçatuba 16050–680, São Paulo, Brazil. Tel: +55 18 3636 1375. Fax: +55 18 3636 1352. E-mail: gmingoti@fmva.unesp.br
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Summary

We examined whether culturing embryos with linoleic acid (LA) in semi-defined medium reduces lipid accumulation and improves cryosurvival after vitrification. Embryos were cultured with LA (100 μM) and a semi-defined medium was used during in vitro culture (IVC), in which the fetal calf serum was substituted by bovine serum albumin (BSA). There was a reduction (P < 0.05) in the embryonic development rate (Control: 25.8% versus LA: 18.5%), but the proposed system was effective in promoting the decrease (P = 0.0130) in the intracellular lipid content (Control: 27.3 ± 0.7 versus LA: 24.6 ± 0.7 arbitrary fluorescence units of embryos stained with the fluorescent dye Nile Red), consequently increasing (P = 0.0490) the embryo survival after 24h of culture post-warming (Control: 50.0% versus LA: 71.7%). The results question the criteria used to evaluate the efficiency of an in vitro production system specifically with relation to the maximum number of blastocysts produced and suggest that might be more appropriate to improve the desired characteristics of embryos generated in accordance with the specific purpose of in vitro embryo production, commercial or scientific. In conclusion, supplying LA to serum-free culture medium was found to adversely affect the rates of embryo development to the blastocyst stage, but significantly reduced embryo lipid accumulation and improved cryopreservation survival.

Keywords

Bovine embryoIn Vitro ProductionLinoleic acidLipidVitrification
Type
Research Article
Information
Zygote , Volume 24 , Issue 4 , August 2016 , pp. 485 - 494
Copyright
Copyright © Cambridge University Press 2015 

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References

Abe, H., Yamashita, S., Satoh, T. & 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.CrossRefGoogle ScholarPubMed
Al Darwich, A., Perreau, C., Petit, M.H., Papillier, P., Dupont, J., Guillaume, D., Mermillod, P. & Guignot, . (2010). Effect of PUFA on embryo cryoresistence, gene expression and AMPKα phosphorylation in IVF-derived bovine embryos. Prostag. Oth. Lipid M. 93, 30–6.CrossRefGoogle Scholar
Alasnier, C., Berdeaux, O., Chardigny, J.M. & Sebedio, J.L. (2002). Fatty acid composition and conjugated linoleic acid content the different tissues in rats fed individual conjugated linoleic acid isomers given as triacylglycerols small star, filled. J. Nutr. Biochem. 13, 337–345.CrossRefGoogle ScholarPubMed
Andreoli, M.F., Gonzalez, M.A., Martinelli, M.I., Mocchiutti, N.O. & Bernal, C.A. (2009). Effects of dietary conjugated linoleic acid at high-fat levels on triacylglycerol regulation in mice. Nutrition 25, 445–452.CrossRefGoogle ScholarPubMed
Bain, N.T., Madan, P. & Betts, D.H. (2011). The early embryo to intracellular reactive oxygen species is developmentally regulate. Reprod. Fertil. Dev. 23, 561–575.CrossRefGoogle Scholar
Baumgard, L.H., Corl, B.A., Dwyer, D.A. & Bauman, D.E. (2000). Identification of the conjugated linoleic acid isomer that inhibits milk fat synthesis. Am. J. Physiol. Reg. I. 278, 179–84.Google ScholarPubMed
Baumgard, L.H., Corl, B.A., Dwyer, D.A. & Bauman, D.E. (2002). Effects of conjugates linoleic acids (CLA) on tissue response to homeostatic signals and plasma variables associated with lipid metabolism in lactating dairy cows. J. Anim. Sci. 80, 1285–1293.CrossRefGoogle Scholar
Brown, J.M., Halvorsen, Y.D., Lea-Currie, Y.R., Geigerman, C. & Mcintosh, M. (2001). Trans-10cis-12 but not cis-9trans-11 conjugated linoleic acid attenuates lipidogenesis in primary cultures of stromal vascular cells from human adipose tissue. J. Nutr. 131, 2316–2321.CrossRefGoogle ScholarPubMed
Corrêa, G.A., Rumpf, R., Mundim, T.C.D., Franco, M.M. & Dode, M.A.N. (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim. Reprod. Sci. 104, 132–142.CrossRefGoogle ScholarPubMed
Dinnyes, A. & Nedambal, T.L. (2009). Cryopreservation of manipulated embryos: tackling the double jeopardy. Reprod. Fertil. Dev. 21, 45–59.CrossRefGoogle ScholarPubMed
Fagali, N. & Catalá, A. (2008). Antioxidant activity of conjugated linoleic acid isomers, linoleic acid and its methyl ester determined by photoemission and DPPH techniques. Biophys. Chem. 137, 56–62.CrossRefGoogle ScholarPubMed
Ferreira, C.R., Eberlin, L.S., Hallett, J.E. & Cooks, R.G. (2012). Single oocyte and single embryo lipid analysis by desorption electrospray ionization mass spectrometry. J. Mass Spectrom. 47, 29–33.CrossRefGoogle ScholarPubMed
Feugang, J.M., Van Langendonckt, A., Sayoud, H., Rees, J.F., Pampfer, S., Moens, A., Dessy, F. & Donnay, I. (2003). Effect of prooxidant agents added at the morula/blastocyst stage on bovine embryo development, cell death and glutathione contente. Zygote 11, 107–118.CrossRefGoogle Scholar
Feugang, J.M., De Roover, R., Moens, A., Leonard, S., Dessy, F. & Donnay, I. (2004). Addition of b-mercaptoethanol or trolox at the morula/blastocyst stage improves the quality of bovine blastocysts and prevents induction of apoptosis and degeneration by prooxidants agents. Theriogenology 61, 71–90.CrossRefGoogle ScholarPubMed
Genicot, G., Leroy, J.L.M.R., Van Soom, A. & Donnay, I. (2005). The use of a fluorescent dye, Nile Red, to evaluate the lipid content of single mammalian oocytes. Theriogenology 63, 1181–1194.CrossRefGoogle ScholarPubMed
Gervais, R., McFadden, J.W., Lengi, A.J., Corl, B.A. & Chouinard, P.Y. (2009). Effects of intravenous infusion of trans-10, cis-12 18:2 on mammary lipid metabolism in lactating dairy cows. J. Dairy Sci. 92, 5167–5177.CrossRefGoogle Scholar
Gomes, A., Fernandes, E. & Lima, J.L.F.C. (2006). Use of fluorescence probes for detection of reactive oxygen species: a review. J. Fluoresc. 16, 119–139.CrossRefGoogle Scholar
Gómez, E., Rodríguez, A., Muñoz, M., Caamaño, J.N., Hidalgo, C.O., Morán, E., Facal, N. & Díez, C. (2008). Serum free embryo culture medium improves in vitro survival of bovine blastocysts to vitrification. Theriogenology 69, 1013–1021.CrossRefGoogle ScholarPubMed
Goto, Y., Noda, Y., Mori, T. & Nakano, M. (1993). Increased generation of reactive oxygen species in embryo cultured in vitro . Free. Radic. Biol. Med. 15, 69–75.CrossRefGoogle ScholarPubMed
Guérin, P., Mouatassin, S. & Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–189.CrossRefGoogle ScholarPubMed
Gupta, M.K., Uhm, S.J. & Lee, H.T. (2010). Effect of vitrification and beta-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertil. Steril. 8, 2602–2607.CrossRefGoogle Scholar
Gutiérrez-Adán, A., Lonergan, P., Rizos, D., Ward, F.A., Boland, M.P., Pintado, B. & De La Fuente, J. (2001). Effect of the in vitro culture system on the kinetics of blastocyst development and sex ratio of bovine embryo. Theriogenology 15, 1117–1126.CrossRefGoogle Scholar
Haggarty, P., Wood, M., Ferguson, E., Hoad, G., Srikantharajah, A., Milne, E., Hamilton, M. & Bhattacharya, S. (2006). Fatty acid metabolism in human preimplantation embryos. Hum. Reprod. 21, 766–773.CrossRefGoogle ScholarPubMed
Halliwell, B. & Gutteridge, J.M.C. (1999). Free Radicals in Biology and Medicine 3rd edn. New York: Oxford University Press, 936 pp.Google Scholar
Harvey, A. J. (2007). The role the oxygen in ruminant preimplantation embryo development and metabolism. Anim. Reprod. Sci. 98, 113–128.CrossRefGoogle ScholarPubMed
Hochi, S., Kimura, K. & Hanada, A. (1999). Effect of linoleic acid-albumin in the culture medium on freezing sensitivity of in vitro-produced bovine morulae. Theriogenology 52, 497–504.CrossRefGoogle ScholarPubMed
Kim, J.Y., Kinoshita, M., Ohnishi, M. & Fukui, Y. (2001). Lipid and fatty acid analysis of fresh and frozen-thawed immature and in vitro matured bovine oocytes. Reproduction 122, 131–8.CrossRefGoogle ScholarPubMed
Koba, K., Belury, M.A. & Sugano, M. (2007). Potential health benefits of conjugated trienoic acids. Lipid Technol. 19, 200–3.CrossRefGoogle Scholar
Leão, B.C., Rocha-Frigoni, N.A.S., Cabral, E.C., Coelho, M.B., Ferreira, C.R, Eberlin, M.N., Accorsi, M.F., Nogueira, É. & 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, 127–36.CrossRefGoogle ScholarPubMed
Lim, K.T., Jang, G., Ko, K.H., Lee, W.W., Park, H.J., Kim, J.J., Lee, S.H., Hwang, W.S., Lee, B.C. & Kang, S.K. (2007). Improved in vitro bovine embryo development and increased efficiency in producing viable calves using defined media. Theriogenology 67, 293–302.CrossRefGoogle ScholarPubMed
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Farin, T. & Boland, M.P. (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod. Domest. Anim. 38, 259–67.CrossRefGoogle ScholarPubMed
Loor, J.J. & Herbein, J.H. (1998). Exogenous conjugated linoleic acid isomers reduce bovine milk fat concentration and yield by inhibiting de novo fatty acid synthesis. J. Nutr. 128, 2411–9.CrossRefGoogle ScholarPubMed
Marei, W.F., Wathes, D.C. & Fouladi-Nashta, A.A. (2012). Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes. Reprod. Fertil. Dev. 24, 679–90.CrossRefGoogle ScholarPubMed
Matwee, C., Betts, D.H. & King, W.A. (2000). Apoptosis in the early bovine embryo. Zygote 8, 57–68.CrossRefGoogle ScholarPubMed
McEvoy, T.G., Coull, G.D., Broadbent, P.J., Hutchinson, J.S.M. & Speake, B.K. (2000). Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J. Reprod. Fertil. 118, 163–170.CrossRefGoogle ScholarPubMed
Nagao, Y., Lijima, R. & Saeki, K. (2008). Interaction between embryos and culture conditions during in vitro development of bovine early embryos. Zygote 16, 127–133.CrossRefGoogle ScholarPubMed
Nedambale, T.L., Du, F., Yang, X. & Tian, X.C. (2006). Higher survival rate of vitrified and thawed in vitro produced bovine blastocyst following culture in defined medium supplemented with beta-mercaptoethanol. Anim. Reprod. Sci. 93, 61–75.CrossRefGoogle ScholarPubMed
Pariza, M.W., Park, Y. & Cook, M.E. (2001). The biologically active isomers of conjugated linoleic acid. Progr. Lipid Res. 40, 283–298.CrossRefGoogle ScholarPubMed
Park, Y., Storkson, J.M., Albright, K.J., Liu, W. & Pariza, M.W. (1999). Evidence that the trans-10, cis-12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids 34, 235–241.CrossRefGoogle ScholarPubMed
Parrish, J.J., Susko-Parrish, J., Winer, M.A. & First, N.L. (1988). Capacitation of bovine sperm by heparina. Biol. Reprod. 38, 1171–1180.CrossRefGoogle Scholar
Paula-Lopes, F.F. & Hansen, P.J. (2002). Heat shock-induced apoptosis in preimplantation bovine embryos is a developmental regulated phenomenon. Biol. Reprod. 66, 1169–77.CrossRefGoogle ScholarPubMed
Pereira, R.M., Baptista, M.C., Vasques, M.I., Horta, A.E.M., Portugal, P.V., Bessa, R.J.B., Chagas, J., Silva Pereira, M. & Marques, C.C. (2007). Cryo-survival of bovine blastocysts is enhanced by culture with trans-10, cis-12 conjugated linoleic acid (10t 12c CLA). Anim. Reprod. Sci. 98, 293–301.CrossRefGoogle Scholar
Pereira, R.M., Carvalhais, I., Pimenta, J., Baptista, M.C., Vasques, M.I., Horta, A.E.M., Santos, I.C., Marques, M.R., Reis, A., Silva Pereira, M. & Marques, C.C. (2008). Biopsied and vitrified bovine embryos viability is improve by trans10, cis12 conjugated linoleic acid supplementation during in vitro embryo culture. Anim. Reprod. Sci. 106, 322–32.CrossRefGoogle ScholarPubMed
Reis, A., Rooke, J.A., MacCallum, G.J., Staines, M.E., Ewen, M., Lomax, M.A. & McEvoy, T.G. (2003). Consequences of exposure to serum, with or without vitamin E supplementation, in terms of the fatty acid content and viability of bovine blastocysts produced in vitro . Reprod. Fertil. Dev. 15, 275–284.CrossRefGoogle ScholarPubMed
Reis, A., Maccallum, G.J. & Mcevoy, T.G. (2005). Accumulation and distribution of neural lipid droplets is nom-uniform in ovine blastocysts produced in vitro in either the presence or absence of serum. Reprod. Fertil. Dev. 17, 815–823.CrossRefGoogle ScholarPubMed
Rizos, D., Fair, T., Papadopoulos, S., Boland, M.P. & Lonergan, P. (2002). Developmental, qualitative, and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro . Mol. Reprod. Dev. 62, 320–322.CrossRefGoogle ScholarPubMed
Rizos, D., Gutierrez-Adan, A., Perez-Garnelo, S., De La Fuente, J., Boland, M.P. & Lonergan, P. (2003). Bovine embryo culture in the presence or the absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68, 236–43.CrossRefGoogle ScholarPubMed
Rizos, D., Clemente, M., Bermejo-Alvarez, P., De La Fuente, J., Lonergan, P. & Gutiérrez-Adán, A. (2008). Consequences of in vitro culture conditions on embryos development and quality. Reprod. Domest. Anim. 43, 44–50.CrossRefGoogle ScholarPubMed
Rybicka, M., Stachowska, E., Gutowska, I., Parczewski, M., Baśkiewicz, M., Machaliński, B., Boroń-Kaczmarska, A. & Chlubek, D. (2011). Comparative effects of conjugated linoleic acid (CLA) and linoleic acid (LA) on the oxidoreduction status in THP-1 macrophages. J. Agric. Food Chem. 27, 4095–103.CrossRefGoogle Scholar
Schmitz, G. & Ecker, J. (2008). The opposing effects of n-3 and n-6 fatty acids. Progr. Lipid Res. 47, 147–55.CrossRefGoogle ScholarPubMed
Sehat, N., Kramer, J.K., Mossoba, M.M., Yurawecz, M.P., Roach, J.A., Eulitz, K., Morehouse, K.M. & Ku, Y. (1998). Identification of conjugated linoleic acid isomers in cheese by gas chromatography, silver ion high performance liquid chromatography and mass spectral reconstructed ion profiles. Comparison of chromatographic elution sequences. Lipids 33, 963–71.CrossRefGoogle ScholarPubMed
Seidel, G.E. Jr (2006). Modifying oocytes and embryos to improve their cryopreservation. Theriogenology 65, 228–35.CrossRefGoogle ScholarPubMed
Sturmey, R.G., Reis, A., Leese, H.J. & Mcevoy, T.G. (2009). Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod. Domest. Anim. 44, 50–8.CrossRefGoogle ScholarPubMed
Sudano, M.J., Paschoal, D.M., Rascado, T.S., Magalhães, L.C.O., Crocomo, L.F., Lima-Neto, J.F. & Landim-Alvarenga, F.C. (2011). Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification. Theriogenology 75, 1211–20.CrossRefGoogle ScholarPubMed
Ufer, C., Wang, C.C., Borchert, B., Heydeck, D. & Kuh, H. (2010). Redox control in mammalian embryo development. Antioxid. Redox Signal. 13, 833–75.CrossRefGoogle ScholarPubMed
Vajta, G., Rindom, N., Peura, T.T., Holm, P., Greve, T. & Callesen, H. (1999). The effect of media, serum and temperature on in vitro survival of bovine blastocysts after open pulled straw (OPS) vitrification. Theriogenology 52, 939–48.CrossRefGoogle ScholarPubMed
Wilding, M., Dale, B., Marino, M., di Matteo, L., Alviggi, C., Pisaturo, M. L., Lombardi, L. & De Placido, G. (2001). Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16, 909–17.CrossRefGoogle ScholarPubMed