Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-23T09:10:40.031Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro maturation alters gene expression in bovine oocytes

Published online by Cambridge University Press:  17 February 2016

Paulo R. Adona ,
Cláudia L.V. Leal ,
Fernando H. Biase ,
Tiago H. De Bem ,
Lígia G. Mesquita ,
Flávio V. Meirelles ,
André L. Ferraz ,
Luiz R. Furlan ,
Paulo S. Monzani  and
Samuel Guemra
Paulo R. Adona*
Affiliation:
Agropecuária Laffranchi. PO box 45. Zip Code: 86125-000 – Tamarana, Paraná. Brazil. Escola de Medicina Veterinária, Universidade Norte do Paraná, Arapongas, PR, Brazil. Departamento de Ciências Básicas, Universidade de São Paulo, Pirassununga, SP, Brazil.
Cláudia L.V. Leal
Affiliation:
Departamento de Ciências Básicas, Universidade de São Paulo, Pirassununga, SP, Brazil.
Fernando H. Biase
Affiliation:
Department of Animal Sciences, Auburn University, Auburn, AL, USA.
Tiago H. De Bem
Affiliation:
Departamento de Ciências Básicas, Universidade de São Paulo, Pirassununga, SP, Brazil.
Lígia G. Mesquita
Affiliation:
Departamento de Ciências Básicas, Universidade de São Paulo, Pirassununga, SP, Brazil.
Flávio V. Meirelles
Affiliation:
Departamento de Ciências Básicas, Universidade de São Paulo, Pirassununga, SP, Brazil.
André L. Ferraz
Affiliation:
Escola de Zootecnia, Universidade estadual de Mato Grosso do Sul, Aquidauana, MS, Brazil.
Luiz R. Furlan
Affiliation:
Departamento de Tecnologia, Universidade Estadual Paulista, Botucatu, SP, Brazil.
Paulo S. Monzani
Affiliation:
Escola de Medicina Veterinária, Universidade Norte do Paraná, Arapongas, PR, Brazil. Laboratório de Reprodução Animal, Agropecuária Laffranchi, Tamarana, PR, Brazil.
Samuel Guemra
Affiliation:
Escola de Medicina Veterinária, Universidade Norte do Paraná, Arapongas, PR, Brazil. Laboratório de Reprodução Animal, Agropecuária Laffranchi, Tamarana, PR, Brazil.
*
All correspondence to: Paulo R. Adona. Agropecuária Laffranchi. PO box 45. Zip Code: 86125-000 – Tamarana, Paraná. Brazil. Tel: +55 43 33994700. E-mail: paulo_adona@yahoo.com.br
Get access Rights & Permissions [Opens in a new window]

Summary

Gene expression profiling of in vivo- and in vitro-matured bovine oocytes can identify transcripts related to the developmental potential of oocytes. Nonetheless, the effects of in vitro culturing oocytes are yet to be fully understood. We tested the effects of in vitro maturation on the transcript profile of oocytes collected from Bos taurus indicus cows. We quantified the expression of 1488 genes in in vivo- and in vitro-matured oocytes. Of these, 51 genes were up-regulated, whereas 56 were down-regulated (≥2-fold) in in vivo-matured oocytes in comparison with in vitro-matured oocytes. Quantitative real-time polymerase chain reaction (PCR) of nine genes confirmed the microarray results of differential expression between in vivo- and in vitro-matured oocytes (EZR, EPN1, PSEN2, FST, IGFBP3, RBBP4, STAT3, FDPS and IRS1). We interrogated the results for enrichment of Gene Ontology categories and overlap with protein–protein interactions. The results revealed that the genes altered by in vitro maturation are mostly related to the regulation of oocyte metabolism. Additionally, analysis of protein–protein interactions uncovered two regulatory networks affected by the in vitro culture system. We propose that the differentially expressed genes are candidates for biomarkers of oocyte competence. In vitro oocyte maturation can affect the abundance of specific transcripts and are likely to deplete the developmental competence.

Type
Research Article
Information
Zygote , Volume 24 , Issue 4 , August 2016 , pp. 624 - 633
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ayres, M., Ayres, J.M., Ayres, D.L. & Santos, A.S. (2007). BioEstat 5.0. Statistical Applications in Biological and Medical Sciences. Sociedade Civil Mamirauá, Brasília, CNPq, 138 pp.Google Scholar
Belli, M., Cimadomo, D., Merico, V., Redi, C.A., Garagna, S. & Zuccotti, M. (2013). The NOBOX protein becomes undetectable in developmentally competent antral and ovulated oocytes. Int. J. Dev. Biol. 57, 35–9.CrossRefGoogle ScholarPubMed
Beltman, M.E., Forde, N., Furney, P., Carter, F., Roche, J.F., Lonergan, P. & Crowe, M.A. (2010). Characterisation of endometrial gene expression and metabolic parameters in beef heifers yielding viable or non-viable embryos on day 7 after insemination. Reprod. Fertil. Dev. 22, 987–99.CrossRefGoogle ScholarPubMed
Benjamini, Y. & Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. Annals Stat. 29, 1165–88.CrossRefGoogle Scholar
Bessa, I.R., Nishimura, R.C., Franco, M.M. & Dode, M.A.N. (2013). Transcription profile of candidate genes for the acquisition of competence during oocyte growth in cattle. Reprod. Domest. Anim. 48, 781–9.CrossRefGoogle ScholarPubMed
Biase, F.H., Fonseca Merighe, G.K., Santos-Biase, W., Martelli, L. & Meirelles, F.V. (2008). Global poly(A) mRNA expression profile measured in individual bovine oocytes and cleavage embryos. Zygote 16, 29–38.CrossRefGoogle ScholarPubMed
Biase, F.H., Martelli, L., Puga, R., Giuliatti, S., Santos-Biase, W.K., Fonseca Merighe, G.K. & Meirelles, F.V. (2010). Messenger RNA expression of Pabpnl1 and Mbd3l2 genes in oocytes and cleavage embryos. Fertil. Steril. 93, 2507–12.CrossRefGoogle ScholarPubMed
Biase, F.H., Everts, R.E., Oliveira, R., Santos-Biase, W.K., Fonseca Merighe, G.K., Smith, L.C., Martelli, L., Lewin, H. & Meirelles, F.V. (2014). Messenger RNAs in metaphase II oocytes correlate with successful embryo development to the blastocyst stage. Zygote 22, 69–79.CrossRefGoogle Scholar
Bonnet, A., Bevilacqua, C., Benne, F., Bodin, L., Cotinot, C., Liaubet, L., Sancristobal, M., Sarry, J., Terenina, E. & Martin, P. (2011). Transcriptome profiling of sheep granulosa cells and oocytes during early follicular development obtained by laser capture microdissection. BMC Genomics 12, 417.CrossRefGoogle ScholarPubMed
Bower, N.I., Moser, R.J., Hill, J.R., Lehnert, S.A. (2007). Universal reference method for real-time PCR gene expression analysis of preimplantation embryos. Biotechniques 42, 199–206.CrossRefGoogle ScholarPubMed
Brunet, S., Dumont, J., Lee, K.W., Kinoshita, K., Hikal, P., Gruss, O.J., Maro, B. & Verlhac, M.-H. (2008). Meiotic regulation of TPX2 protein levels governs cell cycle progression in mouse oocytes. PLoS One 3, e3338.CrossRefGoogle ScholarPubMed
Caixeta, E.S., Ripamonte, P., Franco, M.M., Junior, J.B. & Dode, M.A.N. (2009). Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence. Reprod. Fertil. Dev. 21, 655–64.CrossRefGoogle ScholarPubMed
Caixeta, E.S., Sutton-McDowall, M.L., Gilchrist, R.B., Thompson, J.G., Price, C.A., Machado, M.F., Lima, P.F. & Buratini, J. (2013). Bone morphogenetic protein 15 and fibroblast growth factor 10 enhance cumulus expansion, glucose uptake, and expression of genes in the ovulatory cascade during in vitro maturation of bovine cumulus–oocyte complexes. Reproduction 146, 27–35.CrossRefGoogle ScholarPubMed
Chatr-Aryamontri, A., Breitkreutz, B.J., Heinicke, S., Boucher, L., Winter, A., Stark, C., Nixon, J., Ramage, L., Kolas, N., O’Donnell, L., Reguly, T., Breitkreutz, A., Sellam, A., Chen, D., Chang, C., Rust, J., Livstone, M., Oughtred, R., Dolinski, K. & Tyers, M. (2013). The BioGRID interaction database: 2013 update. Nucleic Acids Res. 41, D816–23.CrossRefGoogle ScholarPubMed
Corcoran, D., Rizos, D., Fair, T., Evans, A.C. & Lonergan, P. (2007). Temporal expression of transcripts related to embryo quality in bovine embryos cultured from the two-cell to blastocyst stage in vitro or in vivo . Mol. Reprod. Dev. 74, 972–977.CrossRefGoogle ScholarPubMed
Fair, T., Carter, F., Park, S., Evans, A.C.O. & Lonergan, P. (2007). Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology 68, S91–7.CrossRefGoogle ScholarPubMed
Ferreira, E.M., Vireque, A.A., Adona, P.R., Meirelles, F.V., Ferriani, R.A. & Navarro, P.A.A.S. (2009). Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71, 836–48.CrossRefGoogle ScholarPubMed
Gandolfi, T.A. & Gandolfi, F. (2001). The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology 55, 1255–76.CrossRefGoogle Scholar
Gasca, S., Pellestor, F., Assou, S., Loup, V., Anahory, T., Dechaud, H., De Vos, J. & Hamamah, S. (2008). Identifying new human oocyte marker genes: a microarray approach. Reprod. Biomed. Online 14, 175–83.CrossRefGoogle Scholar
Hao, Z., Stoler, M.H., Sen, B., Shore, A., Westbrook, A., Flickinger, C.J., Herr, J.C. & Coonrod, S.A. (2002). TACC3 expression and localization in the murine egg and ovary. Mol. Reprod. Dev. 63, 291–9.CrossRefGoogle ScholarPubMed
Heng, S., Cervero, A., Simon, C., Stephens, A.N., Li, Y., Zhang, J., Paule, S., Rainczuk, A., Singh, H. & Quinonero, A. (2011). Proprotein convertase 5/6 is critical for embryo implantation in women: regulating receptivity by cleaving EBP50, modulating ezrin binding, and membrane-cytoskeletal interactions. Endocrinology 152, 5041–52.CrossRefGoogle ScholarPubMed
Huang, D.W., Sherman, B.T. & Lempicki, R.A. (2009). Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat. Protoc. 4, 44–57.CrossRefGoogle ScholarPubMed
Jiang, J.-Y., Xiong, H., Cao, M., Xia, X., Sirard, M.-A. & Tsang, B.K. (2010). Mural granulosa cell gene expression associated with oocyte developmental competence. J. Ovarian Res. 3, 6.CrossRefGoogle ScholarPubMed
Kanka, J., Nemcova, L., Toralova, T., Vodickova-Kepkova, K., Vodicka, P., Jeseta, M. & Machatkova, M. (2012). Association of the transcription profile of bovine oocytes and embryos with developmental potential. Anim. Reprod. Sci. 134, 29–35.CrossRefGoogle ScholarPubMed
Katz-Jaffe, M.G., McCallie, B.R., Preis, K.A., Filipovits, J. & Gardner, D.K. (2009). Transcriptome analysis of in vivo and in vitro matured bovine MII oocytes. Theriogenology 71, 939–46.CrossRefGoogle ScholarPubMed
Knijn, H.M., Gjørret, J.O., Vos, P.L., Hendriksen, P.J., van der Weijden, B.C., Maddox-Hyttel, P. & Dieleman, S.J. (2003). Consequences of in vivo development and subsequent culture on apoptosis, cell number, and blastocyst formation in bovine embryos. Biol. Reprod. 69, 1371–8.CrossRefGoogle ScholarPubMed
Kolano, A., Brunet, S., Silk, A.D., Cleveland, D.W. & Verlhac, M.-H. (2012). Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. Proc. Natl. Acad. Sci. 109, E1858–67.CrossRefGoogle ScholarPubMed
Labrecque, R., Vigneault, C., Blondin, P. & Sirard, M.A. (2013). Gene expression analysis of bovine oocytes with high developmental competence obtained from FSH-stimulated animals. Mol. Reprod. Dev. 80, 428–40.CrossRefGoogle ScholarPubMed
Li, Y., Ray, D. & Ye, P. (2013). Identification of germ cell-specific genes in mammalian meiotic prophase. BMC Bioinform. 14, 1–13.CrossRefGoogle ScholarPubMed
Lisboa, L.A., Bordignon, V. & Seneda, M.M. (2012). Immunolocalization of BRG1–SWI/SNF protein during folliculogenesis in the porcine ovary. Zygote 20, 243–8.CrossRefGoogle ScholarPubMed
Liu, Z. & Zheng, Y. (2009). A requirement for epsin in mitotic membrane and spindle organization. J. Cell Biol. 186, 473–80.CrossRefGoogle ScholarPubMed
Liu, W., Yin, J., Zhao, G., Yun, Y., Wu, S., Jones, K.T. & Lei, A. (2012). Differential regulation of cyclin B1 degradation between the first and second meiotic divisions of bovine oocytes. Theriogenology 78, 1171–81.CrossRefGoogle ScholarPubMed
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–8.CrossRefGoogle Scholar
Mohammadi-Sangcheshmeh, A., Held, E., Ghanem, N., Rings, F., Salilew-Wondim, D., Tesfaye, D., Sieme, H., Schellander, K. & Hoelker, M. (2011). G6PDH-activity in equine oocytes correlates with morphology, expression of candidate genes for viability, and preimplantative in vitro development. Theriogenology 76, 1215–26.CrossRefGoogle ScholarPubMed
Niemann, H., Carnwath, J.W. & Kues, W. (2007). Application of DNA array technology to mammalian embryos. Theriogenology 68, S165–77.CrossRefGoogle ScholarPubMed
Pocar, P., Brevini, T.A.L., Perazzoli, F., Cillo, F., Modina, S. & Gandolfi, F. (2001). Cellular and molecular mechanisms mediating the effects of polychlorinated biphenyls on oocyte developmental competence in cattle. Mol. Reprod. Dev. 60, 535–41.CrossRefGoogle ScholarPubMed
Powell, M.D., Manandhar, G., Spate, L., Sutovsky, M., Zimmerman, S., Sachdev, S.C., Hannink, M., Prather, R.S. & Sutovsky, P. (2010). Discovery of putative oocyte quality markers by comparative ExacTag proteomics. PROTEOMICS – Clinical Applications 4, 337–51.CrossRefGoogle ScholarPubMed
Sawai, K. (2009). Studies on gene expression in bovine embryos derived from somatic cell nuclear transfer. J. Reprod. Dev. 55, 11–6.CrossRefGoogle ScholarPubMed
Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B. & Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–504.CrossRefGoogle ScholarPubMed
Sirard, M.-A., Richard, F., Blondin, P. & Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–36.CrossRefGoogle ScholarPubMed
Smith, S.L., Everts, R.E., Sung, L.Y., Du, F., Page, R.L., Henderson, B., Rodriguez-Zas, S.L., Nedambale, T.L., Renard, J.P., Lewin, H.A., Yang, X., Tian, X.C. (2009). Gene expression profiling of single bovine embryos uncovers significant effects of in vitro maturation, fertilization and culture. Mol. Reprod. Dev. 76, 38–47.CrossRefGoogle ScholarPubMed
Smyth, G.K. (2005). Limma: linear models for microarray data. In Bioinformatics and computational biology solutions using R and Bioconductor (Gentleman, R., Carey, V., Huber, W., Irizarry, R. & Dudoit, S., eds), pp. 397–420. Springer.CrossRefGoogle Scholar
Smyth, G.K. & Speed, T. (2003). Normalization of cDNA microarray data. Methods 31, 265–273.CrossRefGoogle ScholarPubMed
Sun, S.-C., Liu, H.-L. & Sun, Q.-Y. (2012). Survivin regulates Plk1 localization to kinetochore in mouse oocyte meiosis. Biochem. Biophys. Res. Commun. 421, 797–800.CrossRefGoogle ScholarPubMed
Takahashi, H., Parmely, T.J., Sato, S., Tomomori-Sato, C., Banks, C.A., Kong, S.E., Szutorisz, H., Swanson, S.K., Martin-Brown, S., Washburn, M.P., Florens, L., Seidel, C.W., Lin, C., Smith, E.R., Shilatifard, A., Conaway, R.C. & Conaway, J.W. (2011). Human mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 146, 92–104.CrossRefGoogle ScholarPubMed
Tomek, W., Torner, H. & Kanitz, W. (2002). Comparative analysis of protein synthesis, transcription and cytoplasmic polyadenylation of mRNA during maturation of bovine oocytes in vitro . Reprod. Domest. Anim. 37, 86–91.CrossRefGoogle ScholarPubMed
Vigneault, C., McGraw, S. & Sirard, M.-A. (2009). Spatiotemporal expression of transcriptional regulators in concert with the maternal-to-embryonic transition during bovine in vitro embryogenesis. Reproduction 137, 13–21.CrossRefGoogle ScholarPubMed
Wolffe, A.P., Urnov, F.D. & Guschin, D. (2000). Co-repressor complexes and remodelling chromatin for repression. Biochem. Soc. Trans. 28, 379–86.CrossRefGoogle ScholarPubMed
Yamamoto-Honda, R., Honda, Z.I., Ueki, K., Tobe, K., Kaburagi, Y., Takahashi, Y., Tamemoto, H., Suzuki, T., Itoh, K. & Akanuma, Y. (1996). Mutant of insulin receptor substrate-1 incapable of activating phosphatidylinositol 3-kinase did not mediate insulin-stimulated maturation of Xenopus laevis oocytes. J. Biol. Chem. 271, 28677–81.CrossRefGoogle Scholar
Yu, J., Hecht, N.B. & Schultz, R.M. (2002). RNA-binding properties and translation repression in vitro by germ cell-specific MSY2 protein. Biol. Reprod. 67, 1093–8.CrossRefGoogle ScholarPubMed
Yuan, J.S., Reed, A., Chen, F. & Stewart, C.N. Jr (2006). Statistical analysis of real-time PCR data. BMC Bioinformatics 7, 85.CrossRefGoogle Scholar