Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Linoleic (LA) and linolenic (ALA) acid concentrations in follicular fluid of prepubertal goats and their effect on oocyte in vitro maturation and embryo development

Montserrat Roura A , María G. Catalá A , Sandra Soto-Heras A , Sondes Hammami A , Dolors Izquierdo A , Ali Fouladi-Nashta B and Maria-Teresa Paramio A C
+ Author Affiliations
- Author Affiliations

A Departament de Ciència Animal i dels Aliments, Facultat de Veterinària, Universitat Autònoma de Barcelona (UAB), Travessera dels Turons s/n, 08193, Bellaterra, Barcelona, Catalonia, Spain.

B Reproduction Genes and Development Group, Department of Veterinary Basic Sciences, The Royal Veterinary College, Hawkshead Lane Hatfield, Herts AL97TA, UK.

C Corresponding author. Email: teresa.paramio@uab.cat

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17174
Submitted: 7 February 2017  Accepted: 7 June 2017   Published online: 6 July 2017

Abstract

In this study we assessed the concentration of linoleic acid (LA) and linolenic acid (ALA) in follicular fluid of prepubertal goats according to follicle size (<3 mm or ≥3 mm) by gas chromatography and tested the addition of different LA and ALA (LA : ALA) concentration ratios (50 : 50, 100 : 50 and 200 : 50 µM) to the IVM medium on embryo development, mitochondrial activity, ATP concentration and relative gene expression (RPL19, ribosomal protein L19; SLC2A1, facilitated glucose transporter 1; ATF4, activating transcription factor 4; GPX1, glutathione peroxidase 1; HSPA5, heat-shock protein family A 70 kDa; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; DNMT1, DNA methyltransferase 1; GCLC, glutamate–cysteine ligase catalytic subunit; SOD1, superoxide dismutase 1). Oocytes were in vitro matured, fertilised or parthenogenetically activated and zygotes were cultured following conventional protocols. LA concentration ranged from 247 to 319 µM and ALA concentration from 8.39 to 41.19 µM without any effect of follicle size. Blastocyst production from the different groups was: control FCS (22.33%) and BSA (19.63%), treatments 50 : 50 (22.58%), 100 : 50 (21.01%) and 200 : 50 (9.60%). Oocytes from the 200 : 50 group presented higher polyspermy and mitochondrial activity compared with controls and the rest of the treatment groups. No differences were observed in ATP concentration or relative expression of the genes measured between treatment groups. In conclusion, the low number of blastocysts obtained in the 200 : 50 group was caused by a high number of polyspermic zygotes, which could suggest that high LA concentration impairs oocyte membranes.

Additional keywords: blastocysts, embryo production, omega-3 and omega-6 PUFAs, oocyte membrane.


References

Alves, J. P. M., Bertolini, M., Bertolini, L. R., Silva, C. M. G., and Rondina, D. (2015). Lipotoxicity : impact on oocyte quality and reproductive efficiency in mammals. Anim. Reprod. 12, 291–297. open url image1

Amini, E., Asadpour, R., Roshangar, L., and Jafari-joozani, R. (2016). Effect of linoleic acid supplementation on in vitro maturation, embryo development and apoptotic related gene expression in ovine. Int. J Reprod Biomed (Yazd) 14, 255–262. open url image1

Armstrong, D. T. (2001). Effects of maternal age on oocyte developmental competence. Theriogenology 55, 1303–1322.
Effects of maternal age on oocyte developmental competence.CrossRef | 1:CAS:528:DC%2BD3MXjsFSis78%3D&md5=008097b7bf4f49287a60b4a5873b57b4CAS | open url image1

Bender, K., Walsh, S., Evans, A. C. O., Fair, T., and Brennan, L. (2010). Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows. Reproduction 139, 1047–1055.
Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows.CrossRef | 1:CAS:528:DC%2BC3cXns12qsbs%3D&md5=5820a9bf4f70fa1593967d87490f0874CAS | open url image1

Brevini, T. A. L. (2005). Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes. Biol. Reprod. 72, 1218–1223.
Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes.CrossRef | 1:CAS:528:DC%2BD2MXjslSntrc%3D&md5=c6961018cf067bf1cb0bd715ed318c17CAS | open url image1

Bryan, D. L., Hart, P., Forsyth, K., and Gibson, R. (2001). Incorporation of alpha-linolenic acid and linoleic acid into human respiratory epithelial cell lines. Lipids 36, 713–717.
Incorporation of alpha-linolenic acid and linoleic acid into human respiratory epithelial cell lines.CrossRef | 1:CAS:528:DC%2BD3MXmtFKltL4%3D&md5=4a58879e204dcffdedb307919b647251CAS | open url image1

Carro, M., Buschiazzo, J., Ríos, G. L., Oresti, G. M., and Alberio, R. H. (2013). Linoleic acid stimulates neutral lipid accumulation in lipid droplets of maturing bovine oocytes. Theriogenology 79, 687–694.
Linoleic acid stimulates neutral lipid accumulation in lipid droplets of maturing bovine oocytes.CrossRef | 1:CAS:528:DC%2BC38XhvFWgsr3L&md5=626ee0f4297fd49a455af27d3e6177d0CAS | open url image1

Cole, M. A., Murray, A. J., Cochlin, L. E., Heather, L. C., McAleese, S., Knight, N. S., Sutton, E., Jamil, A. A., Parassol, N., and Clarke, K. (2011). A high fat diet increases mitochondrial fatty acid oxidation and uncoupling to decrease efficiency in rat heart. Basic Res. Cardiol. 106, 447–457.
A high fat diet increases mitochondrial fatty acid oxidation and uncoupling to decrease efficiency in rat heart.CrossRef | 1:CAS:528:DC%2BC3MXkt12rtLY%3D&md5=0d139f77dcc99e5e46c39944d73dec63CAS | open url image1

Colell, A., Ricci, J., Green, D. R., and Ricci, J. (2009). Novel roles for GAPDH in cell death and carcinogenesis. Cell Death Differ. 16, 1573–1581.
Novel roles for GAPDH in cell death and carcinogenesis.CrossRef | 1:CAS:528:DC%2BD1MXhsVWlsrzF&md5=17cc075bf168eabac5f767302e898bd3CAS | open url image1

Childs, S., Hennessy, A. A., Sreenan, J. M., Wathes, D. C., Cheng, Z., Stanton, C., Diskin, M. G., and Kenny, D. A. (2008). Effect of level of dietary n-3 polyunsaturated fatty acid supplementation on systemic and tissue fatty acid concentrations and on selected reproductive variables in cattle. Theriogenology 70, 595–611.
Effect of level of dietary n-3 polyunsaturated fatty acid supplementation on systemic and tissue fatty acid concentrations and on selected reproductive variables in cattle.CrossRef | 1:CAS:528:DC%2BD1cXpsVCrtbs%3D&md5=4efa3a8205bf509dc40293657faf47adCAS | open url image1

Dickinson, D. A., Levonen, A. L., Moellering, D. R., Arnold, E. K., Zhang, H., Darley-Usmar, V. M., and Forman, H. J. (2004). Human glutamate cysteine ligase gene regulation through the electrophile response element. Free Radic. Biol. Med. 37, 1152–1159.
Human glutamate cysteine ligase gene regulation through the electrophile response element.CrossRef | 1:CAS:528:DC%2BD2cXnvFaitbo%3D&md5=c6bb6f6bd419cb612d9768cacc6d9786CAS | open url image1

Dumesic, D. A., Meldrum, D. R., Katz-Jaffe, M. G., Krisher, R. L., and Schoolcraft, W. B. (2015). Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health. Fertil. Steril. 103, 303–316.
Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health.CrossRef | open url image1

Dunham, W. R., Klein, S. B., Rhodes, L. M., and Marcelo, C. L. (1996). Oleic acid and linoleic acid are the major determinants of changes in keratinocyte plasma membrane viscosity. J. Invest. Dermatol. 107, 332–335.
Oleic acid and linoleic acid are the major determinants of changes in keratinocyte plasma membrane viscosity.CrossRef | 1:CAS:528:DyaK28XlvVOgu7c%3D&md5=e8b4eaedb80044e79bffae2fced45392CAS | open url image1

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 | 1:CAS:528:DC%2BC3cXhsFahurfN&md5=548d00de5e7460a39941122d18d3ff0fCAS | open url image1

Ghaffarilaleh, V., Fouladi-Nashta, A., and Paramio, M.-T. (2014). Effect of α-linolenic acid on oocyte maturation and embryo development of prepubertal sheep oocytes. Theriogenology 82, 686–696.
Effect of α-linolenic acid on oocyte maturation and embryo development of prepubertal sheep oocytes.CrossRef | 1:CAS:528:DC%2BC2cXhtFentb%2FP&md5=35ec793f84da397562b39d2877384e30CAS | open url image1

Heinzmann, J., Hansmann, T., Herrmann, D., Wrenzycki, C., Zechner, U., Haaf, T., and Niemann, H. (2011). Epigenetic profile of developmentally important genes in bovine oocytes. Mol. Reprod. Dev. 78, 188–201.
Epigenetic profile of developmentally important genes in bovine oocytes.CrossRef | 1:CAS:528:DC%2BC3MXjsVKmsL8%3D&md5=ceda4ca68f6096f6889a60f69688c730CAS | open url image1

Holm, P., Booth, P. J., Schmidt, M. H., Greve, T., and Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683–700.
High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins.CrossRef | 1:STN:280:DC%2BD3c7pvVGnsw%3D%3D&md5=4b5bf1ef366000f0c309b3ada47205f5CAS | open url image1

Homa, S. T., and Brown, C. A. (1992). Changes in linoleic-acid during follicular development and inhibition of spontaneous breakdown of germinal vesicles in cumulus-free bovine oocytes. J. Reprod. Fertil. 94, 153–160.
Changes in linoleic-acid during follicular development and inhibition of spontaneous breakdown of germinal vesicles in cumulus-free bovine oocytes.CrossRef | 1:CAS:528:DyaK38XhslWjtLs%3D&md5=e4940c76fbd562d9801ff7757a2e88ceCAS | open url image1

Hong, M., Kim, H., and Kim, I. (2014). Ribosomal protein L19 overexpression activates the unfolded protein response and sensitizes MCF7 breast cancer cells to endoplasmic reticulum stress-induced cell death. Biochem. Biophys. Res. Commun. 450, 673–678.
Ribosomal protein L19 overexpression activates the unfolded protein response and sensitizes MCF7 breast cancer cells to endoplasmic reticulum stress-induced cell death.CrossRef | 1:CAS:528:DC%2BC2cXhtVKhtb7E&md5=d818ad9862446356c6a08102ac460bbdCAS | open url image1

Hou, Y.-J., Zhu, C.-C., Duan, X., Liu, H.-L., Wang, Q., and Sun, S.-C. (2016). Both diet and gene mutation induced obesity affect oocyte quality in mice. Sci. Rep. 6, 18858.
Both diet and gene mutation induced obesity affect oocyte quality in mice.CrossRef | 1:CAS:528:DC%2BC28XltFGhtg%3D%3D&md5=08da72d40f0d74f34db701cb9c77a8c3CAS | open url image1

Jansen, R. P. S., and Burton, G. J. (2004). Mitochondrial dysfunction in reproduction. Mitochondrion 4, 577–600.
Mitochondrial dysfunction in reproduction.CrossRef | 1:CAS:528:DC%2BD2cXhtVCgs7nL&md5=a2301e35e12e4ec9db49443acb6bc30eCAS | open url image1

Jeseta, M., Ctvrtlikova Knitlova, D., Hanzalova, K., Hulinska, P., Hanulakova, S., Milakovic, I., Nemcova, L., Kanka, J., and Machatkova, M. (2014). Mitochondrial patterns in bovine oocytes with different meiotic competence related to their in vitro maturation. Reprod. Domest. Anim. 49, 469–475.
Mitochondrial patterns in bovine oocytes with different meiotic competence related to their in vitro maturation.CrossRef | 1:CAS:528:DC%2BC2cXns12lsbg%3D&md5=5b1667e557f6ea232f5004485195173bCAS | open url image1

Latham, K. E. (2016). Stress signaling in mammalian oocytes and embryos: a basis for intervention and improvement of outcomes. Cell Tissue Res. 363, 159–167.
Stress signaling in mammalian oocytes and embryos: a basis for intervention and improvement of outcomes.CrossRef | 1:CAS:528:DC%2BC2MXkt1Ogsb8%3D&md5=ab0f62d7c59a457fcc0368939e067e81CAS | open url image1

Leoni, G. G., Palmerini, M. G., Satta, V., Succu, S., Pasciu, V., Zinellu, A., Carru, C., Macchiarelli, G., Nottola, S. A., Naitana, S., and Berlinguer, F. (2015). Differences in the kinetic of the first meiotic division and in active mitochondrial distribution between prepubertal and adult oocytes mirror differences in their developmental competence in a sheep model. PLoS One 10, e0124911.
Differences in the kinetic of the first meiotic division and in active mitochondrial distribution between prepubertal and adult oocytes mirror differences in their developmental competence in a sheep model.CrossRef | open url image1

Li, X., Higashida, K., Kawamura, T., and Higuchi, M. (2016). Alternate-day high-fat diet induces an increase in mitochondrial enzyme activities and protein content in rat skeletal muscle. Nutrients 8, 203.
Alternate-day high-fat diet induces an increase in mitochondrial enzyme activities and protein content in rat skeletal muscle.CrossRef | open url image1

Liu, L., Trimarchi, J. R., and Keefe, D. L. (2000). Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes. Biol. Reprod. 62, 1745–1753.
Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes.CrossRef | 1:CAS:528:DC%2BD3cXjsF2hsbg%3D&md5=5388951edb83c29c7c59ace6280ac832CAS | open url image1

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. 408, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method.CrossRef | open url image1

Luderer, U., Diaz, D., Faustman, E. M., and Kavanagh, T. J. (2003). Localization of glutamate cysteine ligase subunit mRNA within the rat ovary and relationship to follicular apoptosis. Mol. Reprod. Dev. 65, 254–261.
Localization of glutamate cysteine ligase subunit mRNA within the rat ovary and relationship to follicular apoptosis.CrossRef | 1:CAS:528:DC%2BD3sXksVOitLc%3D&md5=f20bc1bf0eb00273f76f5c5ad8d22fe3CAS | open url image1

Marei, W. F., Wathes, D. C., and Fouladi-Nashta, A. A. (2009). The effect of linolenic acid on bovine oocyte maturation and development. Biol. Reprod. 81, 1064–1072.
The effect of linolenic acid on bovine oocyte maturation and development.CrossRef | 1:CAS:528:DC%2BD1MXhsV2lt7vL&md5=c394981d0786b60f609596a194155ec4CAS | open url image1

Marei, W. F., Wathes, D. C., and Fouladi-Nashta, A. A. (2010). Impact of linoleic acid on bovine oocyte maturation and embryo development. Reproduction 139, 979–988.
Impact of linoleic acid on bovine oocyte maturation and embryo development.CrossRef | 1:CAS:528:DC%2BC3cXns12qsLY%3D&md5=49e049e7699f3bbe6ac521c184f81ee8CAS | open url image1

Marei, W. F., Wathes, D. C., and 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, 679–690.
Differential effects of linoleic and alpha-linolenic fatty acids on spatial and temporal mitochondrial distribution and activity in bovine oocytes.CrossRef | 1:CAS:528:DC%2BC38XnvFehu74%3D&md5=e026593a30d2e6aa87361044f6fdc93eCAS | open url image1

Matoba, S., Bender, K., Fahey, A. G., Mamo, S., Brennan, L., Lonergan, P., and Fair, T. (2014). Predictive value of bovine follicular components as markers of oocyte developmental potential. Reprod. Fertil. Dev. 26, 337–345.
Predictive value of bovine follicular components as markers of oocyte developmental potential.CrossRef | 1:CAS:528:DC%2BC2cXjtFCmtg%3D%3D&md5=96f083dbb5602e1c88c763d7bee518eeCAS | open url image1

McKeegan, P. J., and Sturmey, R. G. (2012). The role of fatty acids in oocyte and early embryo development. Reprod. Fertil. Dev. 24, 59–67.
The role of fatty acids in oocyte and early embryo development.CrossRef | open url image1

Montgomery, M. K., and Turner, N. (2015). Mitochondrial dysfunction and insulin resistance: an update. Endocr. Connect. 4, R1–R15.
Mitochondrial dysfunction and insulin resistance: an update.CrossRef | open url image1

Morton, K. M., Catt, S. L., Maxwell, W. M. C., and Evans, G. (2005). Effects of lamb age, hormone stimulation and response to hormone stimulation on the yield and in vitro developmental competence of prepubertal lamb oocytes. Reprod. Fertil. Dev. 17, 593–601.
Effects of lamb age, hormone stimulation and response to hormone stimulation on the yield and in vitro developmental competence of prepubertal lamb oocytes.CrossRef | 1:CAS:528:DC%2BD2MXms1yhtLc%3D&md5=fcc298d1793a4967f5b71e6de8ef5609CAS | open url image1

Parrish, J. J., Susko-Parrish, J. L., Leibfried-Rutledge, M. L., Crister, E. S., Eyeston, W. H., and First, N. L. (1986). Bovine in vitro fertilization with frozen thawed semen. Theriogenology 25, 591–600.
Bovine in vitro fertilization with frozen thawed semen.CrossRef | 1:STN:280:DC%2BD283pvV2itQ%3D%3D&md5=c238a263d539c324481592d69c9c168bCAS | open url image1

Renaville, B., Bacciu, N., Comin, A., Motta, M., Poli, I., Vanini, G., and Prandi, A. (2010). Plasma and follicular fluid fatty acid profiles in dairy cows. Reprod. Domest. Anim. 45, 118–121.
Plasma and follicular fluid fatty acid profiles in dairy cows.CrossRef | 1:CAS:528:DC%2BC3cXislagu7w%3D&md5=83e09c378e6d16ad0d9fb05cf9dbde6dCAS | open url image1

Romaguera, R., Casanovas, A., Morato, R., Izquierdo, D., Catala, M., Jimenez-Macedo, A. R., Mogas, T., and Paramio, M. T. (2010). Effect of follicle diameter on oocyte apoptosis, embryo development and chromosomal ploidy in prepubertal goats. Theriogenology 74, 364–373.
Effect of follicle diameter on oocyte apoptosis, embryo development and chromosomal ploidy in prepubertal goats.CrossRef | 1:STN:280:DC%2BC3cnntVGltA%3D%3D&md5=c3591e02426a526e2664683385c4513bCAS | open url image1

Romaguera, R., Moll, X., Morató, R., Roura, M., Palomo, M. J., Catalá, M. G., Jiménez-Macedo, A. R., Hammami, S., Izquierdo, D., Mogas, T., and Paramio, M. T. (2011). Prepubertal goat oocytes from large follicles result in similar blastocyst production and embryo ploidy than those from adult goats. Theriogenology 76, 1–11.
Prepubertal goat oocytes from large follicles result in similar blastocyst production and embryo ploidy than those from adult goats.CrossRef | 1:STN:280:DC%2BC3MrntlCqtA%3D%3D&md5=4eb7da323c0fe79f508bbe24a2e6d92dCAS | open url image1

Salavati, M., Ghafari, F., Zhang, T., and Fouladi-Nashta, A. A. (2012). Effects of oxygen concentration on in vitro maturation of canine oocytes in a chemically defined serum-free medium. Reproduction 144, 547–556.
Effects of oxygen concentration on in vitro maturation of canine oocytes in a chemically defined serum-free medium.CrossRef | 1:CAS:528:DC%2BC38XhslClt73F&md5=128481142c1993f2e900a44164094e66CAS | open url image1

Schatten, H., Sun, Q.-Y., and Prather, R. (2014). The impact of mitochondrial function/dysfunction on IVF and new treatment possibilities for infertility. Reprod. Biol. Endocrinol. 12, 111.
The impact of mitochondrial function/dysfunction on IVF and new treatment possibilities for infertility.CrossRef | open url image1

Seifert, E. L., Estey, C., Xuan, J. Y., and Harper, M. E. (2010). Electron transport chain-dependent and -independent mechanisms of mitochondrial H2O2 emission during long-chain fatty acid oxidation. J. Biol. Chem. 285, 5748–5758.
Electron transport chain-dependent and -independent mechanisms of mitochondrial H2O2 emission during long-chain fatty acid oxidation.CrossRef | 1:CAS:528:DC%2BC3cXhvFCru70%3D&md5=7f08a5ab7e2b8584e580769ac225d621CAS | open url image1

Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Goncalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.CrossRef | 1:CAS:528:DC%2BD3MXhsVKjtrk%3D&md5=8b7cf000f9af1a1d5cf28bb11a06283eCAS | open url image1

Subbaiah, P. V., Gould, I. G., Lal, S., and Aizezi, B. (2011). Incorporation profiles of conjugated linoleic acid isomers in cell membranes and their positional distribution in phospholipids. Biochim. Biophys. Acta 1811, 17–24.
Incorporation profiles of conjugated linoleic acid isomers in cell membranes and their positional distribution in phospholipids.CrossRef | 1:CAS:528:DC%2BC3cXhsFanu77E&md5=e632cf1ced07bb6eb4ee2f1b3cfa0990CAS | open url image1

Sukhija, P. S., and Palmquist, D. L. (1988). Rapid method for determination of total fatty acid content and composition of feedstuffs and feces. J. Agric. Food Chem. 36, 1202–1206.
Rapid method for determination of total fatty acid content and composition of feedstuffs and feces.CrossRef | 1:CAS:528:DyaL1cXlvVyrtbY%3D&md5=15d4ee91c773f083f272942aa0e60523CAS | open url image1

Sutton-McDowall, M. L., Wu, L. L. Y., Purdey, M., Abell, A. D., Ewa, M., Macmillan, K. L., Thompson, J. G., and Robker, R. L. (2016). Nonesterified fatty acid-induced endoplasmic reticulum stress in cattle cumulus oocyte complexes alters cell metabolism and developmental competence. Biol. Reprod. 94, 23.
Nonesterified fatty acid-induced endoplasmic reticulum stress in cattle cumulus oocyte complexes alters cell metabolism and developmental competence.CrossRef | open url image1

Sviderskaya, E. V., Jazrawi, E., Baldwin, S. A., Widnell, C. C., and Pasternak, C. A. (1996). Cellular stress causes accumulation of the glucose transporter at the surface of cells independently of their insulin sensitivity. J. Membr. Biol. 149, 133–140.
Cellular stress causes accumulation of the glucose transporter at the surface of cells independently of their insulin sensitivity.CrossRef | 1:CAS:528:DyaK28XpvV2jug%3D%3D&md5=53c21bc62c6c7637b048e10a85367fbcCAS | open url image1

Thouas, G. A., Korfiatis, N. A., French, A. J., Jones, G. M., and Trounson, A. O. (2001). Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. Biomed. Online 3, 25–29.
Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts.CrossRef | open url image1

Turner, N., Bruce, C. R., Beale, S. M., Hoehn, K. L., So, T., Rolph, M. S., and Cooney, G. J. (2007). Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56, 2085–2092.
Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents.CrossRef | 1:CAS:528:DC%2BD2sXos12qsL0%3D&md5=32287e0591432ffbbd744e8e402e0912CAS | open url image1

Van Blerkom, J., and Runner, M. N. (1984). Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte. Am. J. Anat. 171, 335–355.
Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte.CrossRef | 1:STN:280:DyaL2M%2FpsVWhuw%3D%3D&md5=b9bed4819f80a6e9a19fc05d27d15953CAS | open url image1

Van Blerkom, J., Davis, P. W., and Lee, J. (1995). ATP content of human oocytes and developmental potential and outcome after in vitro fertilization and embryo transfer. Hum. Reprod. 10, 415–424.
ATP content of human oocytes and developmental potential and outcome after in vitro fertilization and embryo transfer.CrossRef | 1:STN:280:DyaK2M3os1OrtQ%3D%3D&md5=3e7957ec8d671ddb5394acb50620c419CAS | open url image1

Van Hoeck, V., Sturmey, R. G., Bermejo-Alvarez, P., Rizos, D., Gutierrez-Adan, A., Leese, H. J., Bols, P. E. J., and Leroy, J. L. M. R. (2011). Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 6, e23183.
Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology.CrossRef | 1:CAS:528:DC%2BC3MXhtFKmsLjM&md5=e9fc8e01471a033adbaebf967955952eCAS | open url image1

Van Hoeck, V., Leroy, J. L. M. R., Alvarez, M. A., Rizos, D., Gutierrez-Adan, A., Schnorbusch, K., Bols, P. E. J., Leese, H. J., and Sturmey, R. G. (2013). Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: mechanistic insights. Reproduction 145, 33–44.
Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: mechanistic insights.CrossRef | 1:CAS:528:DC%2BC3sXhslGisb8%3D&md5=451b5a7b9c07dd9b3a281751d0ce2968CAS | open url image1

Veshkini, A., Asadi, H., Khadem, A. A., Mohammadi-Sangcheshmeh, A., Khazabi, S., Aminafshar, M., Deldar, H., Soleimani, M., and Cinar, M. U. (2015). Effect of linolenic acid during in vitro maturation of ovine oocytes: embryonic developmental potential and mRNA abundances of genes involved in apoptosis. J. Assist. Reprod. Genet. 32, 653–659.
Effect of linolenic acid during in vitro maturation of ovine oocytes: embryonic developmental potential and mRNA abundances of genes involved in apoptosis.CrossRef | open url image1

Veshkini, A., Khadem, A. A., Mohammadi-Sangcheshmeh, A., Alamouti, A. A., Soleimani, M., and Gastal, E. L. (2016). Linolenic acid improves oocyte developmental competence and decreases apoptosis of in vitro-produced blastocysts in goat. Zygote 24, 537–548.
Linolenic acid improves oocyte developmental competence and decreases apoptosis of in vitro-produced blastocysts in goat.CrossRef | 1:CAS:528:DC%2BC28XhtVOisb3K&md5=b655f018633dd9c1c98ddb704ce20ac4CAS | open url image1

Wathes, D. (2013). Polyunsaturated fatty acids and fertility in female mammals: an update. Perspect. Agric. Vet. Sci. Nutr. Nat. Resour. 8, .
Polyunsaturated fatty acids and fertility in female mammals: an update.CrossRef | open url image1

Wathes, D. C., Abayasekara, D. R. E., and Aitken, R. J. (2007). Polyunsaturated fatty acids in male and female reproduction. Biol. Reprod. 77, 190–201.
Polyunsaturated fatty acids in male and female reproduction.CrossRef | 1:CAS:528:DC%2BD2sXot1OnsL0%3D&md5=8d91c0ebdfe6625463b68e2bf9b4f2ccCAS | open url image1

Wonnacott, K. E., Kwong, W. Y., Hughes, J., Salter, A. M., Lea, R. G., Garnsworthy, P. C., and Sinclair, K. D. (2010). Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos. Reproduction 139, 57–69.
Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos.CrossRef | 1:CAS:528:DC%2BC3cXovVWnug%3D%3D&md5=82d980b8fb194b9c7cc725588d4470afCAS | open url image1

Wu, L. L. Y., Dunning, K. R., Yang, X., Russell, D. L., Lane, M., Norman, R. J., and Robker, R. L. (2010). High-fat diet causes lipotoxicity responses in cumulus–oocyte complexes and decreased fertilization rates. Endocrinology 151, 5438–5445.
High-fat diet causes lipotoxicity responses in cumulus–oocyte complexes and decreased fertilization rates.CrossRef | 1:CAS:528:DC%2BC3cXhsVKks7bL&md5=b1ae6d39b04fc855f4e8240fc618a4f9CAS | open url image1

Yu, Y., Dumollard, R., Rossbach, A., Lai, F. A., and Swann, K. (2010). Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J. Cell. Physiol. 224, 672–680.
Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation.CrossRef | 1:CAS:528:DC%2BC3cXosVWntLo%3D&md5=2923496255be92f6ea87ede66df0b247CAS | open url image1



Export Citation

View Altmetrics