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

Influence of follicle size on bovine oocyte lipid composition, follicular metabolic and stress markers, embryo development and blastocyst lipid content

Kelly Annes A B , Diego B. Müller A , Jorge A. P. Vilela A , Roniele S. Valente A , Diana P. Caetano A , Francielli W. S. Cibin A , Marcella P. Milazzotto B , Fernando S. Mesquita A , Katia R. A. Belaz C D , Marcos N. Eberlin C and Mateus J. Sudano orcid.org/0000-0002-7699-4449 A B E
+ Author Affiliations
- Author Affiliations

A School of Veterinary Medicine, Federal University of Pampa, BR 472 – KM 592, PO Box 118, 97501-970, Uruguaiana, RS, Brazil.

B Centre of Natural and Human Sciences, Federal University of ABC, Av. dos Estados, 5001, 09210-580, Santo André, São Paulo, Brazil.

C ThoMSon Mass Spectrometry Laboratory, Institute of Chemistry, University of Campinas, UNICAMP PO Box 6154, 13083–970, Distrito de Barão Geraldo, Campinas, São Paulo, Brazil.

D Institute of Chemistry, Federal University of Uberlândia (UFU), 38408-144, Uberlândia, Minas Gerais, Brazil.

E Corresponding author. Email: mjsudano@gmail.com

Reproduction, Fertility and Development 31(3) 462-472 https://doi.org/10.1071/RD18109

Abstract

This study assessed the lipid composition of oocytes from different follicle sizes and compared the expression of lipid-related genes and follicular fluid (FF) molecules between groups. We also investigated the functional consequences of differences on embryo development and blastocyst lipid deposits. Oocytes and FF were recovered from different follicle sizes. Oocytes from small (≤5 mm) and large (≥6mm) bovine follicles were used to produce Day 7 expanded blastocysts (Day7Ex) and blastocysts that only became expanded at Day 8 (Day8Ex) after insemination. Oocytes from >8 mm follicles had the highest lipid content. Few oocyte phospholipid variations were identified between groups. Very long chain fatty acid elongase 6 (ELOVL6) mRNA abundance was reduced in larger follicle-derived oocytes compared with the ≤2mm group. Increased levels of glucose, reactive oxygen species, glutathione and superoxide dismutase activity were also identified in FF from larger follicles. Large follicle-derived embryo development and lipid content of Day7Ex were greater than those derived from small follicles. Day8Ex had greater lipid deposition than Day7Ex. Oocytes and blastocysts exhibited follicle size-specific lipids. Large-follicle oocytes had increased lipid content and became Day7Ex with greater lipid deposition whereas delayed blastocoel expansion associated with a prolonged period of culture determined the lipid accumulation of Day8Ex. The FF microenvironment of large follicles seems to favour embryo development.

Additional keywords: follicular fluid microenvironment, in vitro production, lipid metabolism, mammalian egg, mass spectrometry.


References

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 |

Al Darwich, A., Perreau, C., Petit, M. H., Papillier, P., Dupont, J., Guillaume, D., Mermillod, P., and Guignot, F. (2010). Effect of PUFA on embryo cryoresistance, gene expression and AMPKα phosphorylation in IVF-derived bovine embryos. Prostaglandins Other Lipid Mediat. 93, 30–36.
Effect of PUFA on embryo cryoresistance, gene expression and AMPKα phosphorylation in IVF-derived bovine embryos.Crossref | GoogleScholarGoogle Scholar |

Assey, R. J., Hyttel, P., Greve, T., and Purwantara, B. (1994). Oocyte morphology in dominant and subordinate follicles. Mol. Reprod. Dev. 37, 335–344.
Oocyte morphology in dominant and subordinate follicles.Crossref | GoogleScholarGoogle Scholar |

Attaran, M., Pasqualotto, E., Falcone, T., Goldberg, J. M., Miller, K. F., Agarwal, A., and Sharma, R. K. (2000). The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int. J. Fertil. Womens Med. 45, 314–320.

Belaz, K. R. A., Tata, A., França, M. R., Santos da Silva, M. I., Vendramini, P. H., Fernandes, A. A., D’Alexandri, F. L., Eberlin, M. N., and Binelli, M. (2016). Phospholipid profile and distribution in the receptive oviduct and uterus during early diestrus in cattle. Biol. Reprod. 95, 127.
Phospholipid profile and distribution in the receptive oviduct and uterus during early diestrus in cattle.Crossref | GoogleScholarGoogle Scholar |

Blondin, P., and Sirard, M. A. (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev. 41, 54–62.
Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes.Crossref | GoogleScholarGoogle Scholar |

Blondin, P., Vigneault, C., Nivet, A., and Sirard, M. (2012). Improving oocyte quality in cows and heifers - what are we learned so far? Anim. Reprod. 9, 281–289.

Burnum, K. E., Cornett, D. S., Puolitaival, S. M., Milne, S. B., Myers, D. S., Tranguch, S., Brown, H. A., Dey, S. K., and Caprioli, R. M. (2009). Spatial and temporal alterations of phospholipids determined by mass spectrometry during mouse embryo implantation. J. Lipid Res. 50, 2290–2298.
Spatial and temporal alterations of phospholipids determined by mass spectrometry during mouse embryo implantation.Crossref | GoogleScholarGoogle Scholar |

Caixeta, E. S., Machado, M. F., Ripamonte, P., Price, C., and Buratini, J. (2013). Effects of FSH on the expression of receptors for oocyte-secreted factors and members of the EGF-like family during in vitro maturation in cattle. Reprod. Fertil. Dev. 25, 890–899.
Effects of FSH on the expression of receptors for oocyte-secreted factors and members of the EGF-like family during in vitro maturation in cattle.Crossref | GoogleScholarGoogle Scholar |

Cantley, L. C. (2002). The phosphoinositide 3-kinase pathway. Science 296, 1655–1657.
The phosphoinositide 3-kinase pathway.Crossref | GoogleScholarGoogle Scholar |

Chen, Q., Vazquez, E. J., Moghaddas, S., Hoppel, C. L., and Lesnefsky, E. J. (2003). Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 278, 36027–36031.
Production of reactive oxygen species by mitochondria: central role of complex III.Crossref | GoogleScholarGoogle Scholar |

Cognie, Y., Benoit, F., Poulin, N., Khatir, H., and Driancourt, M. A. (1998). Effect of follicle size and of the FecB Booroola gene on oocyte function in sheep. J. Reprod. Fertil. 112, 379–386.
Effect of follicle size and of the FecB Booroola gene on oocyte function in sheep.Crossref | GoogleScholarGoogle Scholar |

Combelles, C. M., Holick, E. A., Paolella, L. J., Walker, D. C., and Wu, Q. (2010). Profiling of superoxide dismutase isoenzymes in compartments of the developing bovine antral follicles. Reproduction 139, 871–881.
Profiling of superoxide dismutase isoenzymes in compartments of the developing bovine antral follicles.Crossref | GoogleScholarGoogle Scholar |

Dadarwal, D., Honparkhe, M., Dias, F. C., Alce, T., Lessard, C., and Singh, J. (2015). Effect of superstimulation protocols on nuclear maturation and distribution of lipid droplets in bovine oocytes. Reprod. Fertil. Dev. 27, 1137–1146.
Effect of superstimulation protocols on nuclear maturation and distribution of lipid droplets in bovine oocytes.Crossref | GoogleScholarGoogle Scholar |

del Collado, M., da Silveira, J. C., Sangalli, J. R., Andrade, G. M., Sousa, L. R. D. S., Silva, L. A., Meirelles, F. V., and Perecin, F. (2017). Fatty acid binding protein 3 and transzonal projections are involved in lipid accumulation during in vitro maturation of bovine oocytes. Sci. Rep. 7, 2645.
Fatty acid binding protein 3 and transzonal projections are involved in lipid accumulation during in vitro maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar |

Dubey, A. K., Wang, H. A., Duffy, P., and Penzias, A. S. (1995). The correlation between follicular measurements, oocyte morphology, and fertilization rates in an in vitro fertilization program. Fertil. Steril. 64, 787–790.
The correlation between follicular measurements, oocyte morphology, and fertilization rates in an in vitro fertilization program.Crossref | GoogleScholarGoogle Scholar |

Dunning, K. R., Russell, D. L., and Robker, R. L. (2014). Lipids and oocyte developmental competence: the role of fatty acids and β-oxidation. Reproduction 148, R15–R27.
Lipids and oocyte developmental competence: the role of fatty acids and β-oxidation.Crossref | GoogleScholarGoogle Scholar |

Fair, T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 78, 203–216.
Follicular oocyte growth and acquisition of developmental competence.Crossref | GoogleScholarGoogle Scholar |

Ferreira, C. R., Saraiva, S. A., Catharino, R. R., Garcia, J. S., Gozzo, F. C., Sanvido, G. B., Santos, L. F., Lo Turco, E. G., Pontes, J. H., Basso, A. C., Bertolla, R. P., Sartori, R., Guardieiro, M. M., Perecin, F., Meirelles, F. V., Sangalli, J. R., and Eberlin, M. N. (2010). Single embryo and oocyte lipid fingerprinting by mass spectrometry. J. Lipid Res. 51, 1218–1227.
Single embryo and oocyte lipid fingerprinting by mass spectrometry.Crossref | GoogleScholarGoogle Scholar |

Gonçalves, R. F., Ferreira, M. S., de Oliveira, D. N., Canevarolo, R., Achilles, M. A., D’Ercole, D. L., Bols, P. E., Visintin, J. A., Killian, G. J., and Catharino, R. R. (2016). Analysis and characterisation of bovine oocyte and embryo biomarkers by matrix-assisted desorption ionisation mass spectrometry imaging. Reprod. Fertil. Dev. 28, 293–301.
Analysis and characterisation of bovine oocyte and embryo biomarkers by matrix-assisted desorption ionisation mass spectrometry imaging.Crossref | GoogleScholarGoogle Scholar |

Gupta, S., Choi, A., Yu, H. Y., Czerniak, S. M., Holick, E. A., Paolella, L. J., Agarwal, A., and Combelles, C. M. (2011). Fluctuations in total antioxidant capacity, catalase activity and hydrogen peroxide levels of follicular fluid during bovine folliculogenesis. Reprod. Fertil. Dev. 23, 673–680.
Fluctuations in total antioxidant capacity, catalase activity and hydrogen peroxide levels of follicular fluid during bovine folliculogenesis.Crossref | GoogleScholarGoogle Scholar |

Hennet, M. L., and Combelles, C. M. (2012). The antral follicle: a microenvironment for oocyte differentiation. Int. J. Dev. Biol. 56, 819–831.
The antral follicle: a microenvironment for oocyte differentiation.Crossref | GoogleScholarGoogle Scholar |

Hennet, M. L., Yu, H. Y., and Combelles, C. M. (2013). Follicular fluid hydrogen peroxide and lipid hydroperoxide in bovine antral follicles of various size, atresia, and dominance status. J. Assist. Reprod. Genet. 30, 333–340.
Follicular fluid hydrogen peroxide and lipid hydroperoxide in bovine antral follicles of various size, atresia, and dominance status.Crossref | GoogleScholarGoogle Scholar |

Hissin, P. J., and Hilf, R. (1976). A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 74, 214–226.
A fluorometric method for determination of oxidized and reduced glutathione in tissues.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar |

Huwiler, A., Kolter, T., Pfeilschifter, J., and Sandhoff, K. (2000). Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim. Biophys. Acta 1485, 63–99.
Physiology and pathophysiology of sphingolipid metabolism and signaling.Crossref | GoogleScholarGoogle Scholar |

Hyttel, P., Fair, T., Callesen, H., and Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.
Oocyte growth, capacitation and final maturation in cattle.Crossref | GoogleScholarGoogle Scholar |

Hyttel P., Sinowatz F., Vejlsted M., and Betteridge, K. (2011). ‘Essentials of Domestic Animal Embryology.’ (Elsevier: Amsterdam.)

Jung, J., Shin, H., Bang, S., Mok, H. J., Suh, C. S., Kim, K. P., and Lim, H. J. (2014). Analysis of the phospholipid profile of metaphase II mouse oocytes undergoing vitrification. PLoS One 9, e102620.
Analysis of the phospholipid profile of metaphase II mouse oocytes undergoing vitrification.Crossref | GoogleScholarGoogle Scholar |

Ka, H. H., Sawai, K., Wang, W. H., Im, K. S., and Niwa, K. (1997). Amino acids in maturation medium and presence of cumulus cells at fertilization promote male pronuclear formation in porcine oocytes matured and penetrated in vitro. Biol. Reprod. 57, 1478–1483.
Amino acids in maturation medium and presence of cumulus cells at fertilization promote male pronuclear formation in porcine oocytes matured and penetrated in vitro.Crossref | GoogleScholarGoogle Scholar |

Katso, R., Okkenhaug, K., Ahmadi, K., White, S., Timms, J., and Waterfield, M. D. (2001). Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 17, 615–675.
Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer.Crossref | GoogleScholarGoogle Scholar |

Khatir, H., Anouassi, A., and Tibary, A. (2007). Effect of follicular size on in vitro developmental competence of oocytes and viability of embryos after transfer in the dromedary (Camelus dromedarius). Anim. Reprod. Sci. 99, 413–420.
Effect of follicular size on in vitro developmental competence of oocytes and viability of embryos after transfer in the dromedary (Camelus dromedarius).Crossref | GoogleScholarGoogle Scholar |

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 |

Labrecque, R., Fournier, E., and Sirard, M. A. (2016). Transcriptome analysis of bovine oocytes from distinct follicle sizes: insights from correlation network analysis. Mol. Reprod. Dev. 83, 558–569.
Transcriptome analysis of bovine oocytes from distinct follicle sizes: insights from correlation network analysis.Crossref | GoogleScholarGoogle Scholar |

Leão, B. C., Rocha-Frigoni, N. A., Cabral, E. C., Franco, M. F., Ferreira, C. R., Eberlin, M. N., Filgueiras, P. R., and Mingoti, G. Z. (2015). Membrane lipid profile monitored by mass spectrometry detected differences between fresh and vitrified in vitro-produced bovine embryos. Zygote 23, 732–741.
Membrane lipid profile monitored by mass spectrometry detected differences between fresh and vitrified in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar |

Lonergan, P., Monaghan, P., Rizos, D., Boland, M. P., and Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol. Reprod. Dev. 37, 48–53.
Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro.Crossref | GoogleScholarGoogle Scholar |

Luberda, Z. (2005). The role of glutathione in mammalian gametes. Reprod. Biol. 5, 5–17.

McEvoy, T. G., Coull, G. D., Broadbent, P. J., Hutchinson, J. S., and 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.

Milne, S., Ivanova, P., Forrester, J., and Alex Brown, H. (2006). Lipidomics: an analysis of cellular lipids by ESI-MS. Methods 39, 92–103.
Lipidomics: an analysis of cellular lipids by ESI-MS.Crossref | GoogleScholarGoogle Scholar |

Misra, H. P., and Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. 247, 3170–3175.

Moon, Y. A., Hammer, R. E., and Horton, J. D. (2009). Deletion of ELOVL5 leads to fatty liver through activation of SREBP-1c in mice. J. Lipid Res. 50, 412–423.
Deletion of ELOVL5 leads to fatty liver through activation of SREBP-1c in mice.Crossref | GoogleScholarGoogle Scholar |

Mori, T., Amano, T., and Shimizu, H. (2000). Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro. Biol. Reprod. 62, 913–919.
Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro.Crossref | GoogleScholarGoogle Scholar |

Nagai, T. (2001). The improvement of in vitro maturation systems for bovine and porcine oocytes. Theriogenology 55, 1291–1301.
The improvement of in vitro maturation systems for bovine and porcine oocytes.Crossref | GoogleScholarGoogle Scholar |

Ohkawa, H., Ohishi, N., and Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95, 351–358.
Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction.Crossref | GoogleScholarGoogle Scholar |

Parrish, J. J., Krogenaes, A., and Susko-Parrish, J. L. (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44, 859–869.
Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development.Crossref | GoogleScholarGoogle Scholar |

Pasqualotto, E. B., Lara, L. V., Salvador, M., Sobreiro, B. P., Borges, E., and Pasqualotto, F. F. (2009). The role of enzymatic antioxidants detected in the follicular fluid and semen of infertile couples undergoing assisted reproduction. Hum. Fertil. 12, 166–171.
The role of enzymatic antioxidants detected in the follicular fluid and semen of infertile couples undergoing assisted reproduction.Crossref | GoogleScholarGoogle Scholar |

Paszkowski, T., Traub, A. I., Robinson, S. Y., and McMaster, D. (1995). Selenium dependent glutathione peroxidase activity in human follicular fluid. Clin. Chim. Acta 236, 173–180.
Selenium dependent glutathione peroxidase activity in human follicular fluid.Crossref | GoogleScholarGoogle Scholar |

Pavlok, A., Lucas-Hahn, A., and Niemann, H. (1992). Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol. Reprod. Dev. 31, 63–67.
Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles.Crossref | GoogleScholarGoogle Scholar |

Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 45e.
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar |

Prates, E. G., Nunes, J. T., and Pereira, R. M. (2014). A role of lipid metabolism during cumulus–oocyte complex maturation: impact of lipid modulators to improve embryo production. Mediators Inflamm. 2014, 692067.
A role of lipid metabolism during cumulus–oocyte complex maturation: impact of lipid modulators to improve embryo production.Crossref | GoogleScholarGoogle Scholar |

Stocco, C. (2008). Aromatase expression in the ovary: hormonal and molecular regulation. Steroids 73, 473–487.
Aromatase expression in the ovary: hormonal and molecular regulation.Crossref | GoogleScholarGoogle Scholar |

Sturmey, R. G., O’Toole, P. J., and Leese, H. J. (2006). Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte. Reproduction 132, 829–837.
Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte.Crossref | GoogleScholarGoogle Scholar |

Sudano, M. J., Santos, V. G., Tata, A., Ferreira, C. R., Paschoal, D. M., Machado, R., Buratini, J., Eberlin, M. N., and Landim-Alvarenga, F. D. (2012). Phosphatidylcholine and sphingomyelin profiles vary in Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts. Biol. Reprod. 87, 130.
Phosphatidylcholine and sphingomyelin profiles vary in Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts.Crossref | GoogleScholarGoogle Scholar |

Sudano, M. J., Paschoal, D. M., da Silva Rascado, T., Crocomo, L. F., Magalhães, L. C., Junior, A. M., Machado, R., and da Cruz Landim-Alvarenga, F. (2014). Crucial surviving aspects for vitrified in vitro-produced bovine embryos. Zygote 22, 124–131.
Crucial surviving aspects for vitrified in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar |

Sudano, M. J., Rascado, T. D., Tata, A., Belaz, K. R., Santos, V. G., Valente, R. S., Mesquita, F. S., Ferreira, C. R., Araújo, J. P., Eberlin, M. N., and Landim-Alvarenga, F. D. (2016). Lipidome signatures in early bovine embryo development. Theriogenology 86, 472–484.e1.
Lipidome signatures in early bovine embryo development.Crossref | GoogleScholarGoogle Scholar |

Sutton, M. L., Gilchrist, R. B., and Thompson, J. G. (2003). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Hum Reprod Updat. 9, 35–48.

Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–695.
The pivotal role of glucose metabolism in determining oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar |

Tata, A., Sudano, M. J., Santos, V. G., Landim-Alvarenga, F. D., Ferreira, C. R., and Eberlin, M. N. (2013). Optimal single-embryo mass spectrometry fingerprinting. J. Mass Spectrom. 48, 844–849.
Optimal single-embryo mass spectrometry fingerprinting.Crossref | GoogleScholarGoogle Scholar |

Thibault, C., Szöllösi, D., and Gérard, M. (1987). Mammalian oocyte maturation. Reprod. Nutr. Dev. 27, 865–896.
Mammalian oocyte maturation.Crossref | GoogleScholarGoogle Scholar |

Valdez, K. E., Cuneo, S. P., and Turzillo, A. M. (2005). Regulation of apoptosis in the atresia of dominant bovine follicles of the first follicular wave following ovulation. Reproduction 130, 71–81.
Regulation of apoptosis in the atresia of dominant bovine follicles of the first follicular wave following ovulation.Crossref | GoogleScholarGoogle Scholar |

Wang, Y., Botolin, D., Xu, J., Christian, B., Mitchell, E., Jayaprakasam, B., Nair, M. G., Nair, M., Peters, J. M., Busik, J. V., Busik, J., Olson, L. K., and Jump, D. B. (2006). Regulation of hepatic fatty acid elongase and desaturase expression in diabetes and obesity. J. Lipid Res. 47, 2028–2041.
Regulation of hepatic fatty acid elongase and desaturase expression in diabetes and obesity.Crossref | GoogleScholarGoogle Scholar |

Xia, J., Mandal, R., Sinelnikov, I. V., Broadhurst, D., and Wishart, D. S. (2012). MetaboAnalyst 2.0–a comprehensive server for metabolomic data analysis. Nucleic Acids Res. 40, W127–W133.
MetaboAnalyst 2.0–a comprehensive server for metabolomic data analysis.Crossref | GoogleScholarGoogle Scholar |

Yang, X., Dunning, K. R., Wu, L. L., Hickey, T. E., Norman, R. J., Russell, D. L., Liang, X., and Robker, R. L. (2010). Identification of perilipin-2 as a lipid droplet protein regulated in oocytes during maturation. Reprod. Fertil. Dev. 22, 1262–1271.
Identification of perilipin-2 as a lipid droplet protein regulated in oocytes during maturation.Crossref | GoogleScholarGoogle Scholar |

Yang, M., Hall, J., Fan, Z., Regouski, M., Meng, Q., Rutigliano, H. M., Stott, R., Rood, K. A., Panter, K. E., and Polejaeva, I. A. (2016). Oocytes from small and large follicles exhibit similar development competence following goat cloning despite their differences in meiotic and cytoplasmic maturation. Theriogenology 86, 2302–2311.
Oocytes from small and large follicles exhibit similar development competence following goat cloning despite their differences in meiotic and cytoplasmic maturation.Crossref | GoogleScholarGoogle Scholar |

Ye, X., Hama, K., Contos, J. J., Anliker, B., Inoue, A., Skinner, M. K., Suzuki, H., Amano, T., Kennedy, G., Arai, H., Aoki, J., and Chun, J. (2005). LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing. Nature 435, 104–108.
LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing.Crossref | GoogleScholarGoogle Scholar |