Hostname: page-component-55f67697df-zpzq9 Total loading time: 0 Render date: 2025-05-18T00:08:32.594Z Has data issue: false hasContentIssue false
  • English
  • Français

Messenger RNAs in metaphase II oocytes correlate with successful embryo development to the blastocyst stage

Published online by Cambridge University Press:  10 October 2012

Fernando Henrique Biase ,
Robin Edward Everts ,
Rosane Oliveira ,
Weruska Karyna Freitas Santos-Biase ,
Giovana Krempel Fonseca Merighe ,
Lawrence Charles Smith ,
Lúcia Martelli ,
Harris Lewin  and
Flávio Vieira Meirelles
Fernando Henrique Biase
Affiliation:
Departamento de Genética, Faculdade de Medicina de Ribeirão Preto–Universidade de São Paulo, Ribeirão Preto, São Paulo, Brasil. Department of Animal Sciences, University of Illinois at Urbana-Champaign, USA.
Robin Edward Everts
Affiliation:
Department of Animal Sciences, University of Illinois at Urbana-Champaign, USA.
Rosane Oliveira
Affiliation:
Department of Animal Sciences, University of Illinois at Urbana-Champaign, USA.
Weruska Karyna Freitas Santos-Biase
Affiliation:
Departamento de Ciências Básicas, Faculdade de Zootecnia e Engenharia de Alimentos–Universidade de São Paulo, Pirassununga, São Paulo, Brasil.
Giovana Krempel Fonseca Merighe
Affiliation:
Departamento de Ciências Básicas, Faculdade de Zootecnia e Engenharia de Alimentos–Universidade de São Paulo, Pirassununga, São Paulo, Brasil.
Lawrence Charles Smith
Affiliation:
Centre de Recherche en Reproducion Animale, Faculté de Médicine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Quebec, Canada.
Lúcia Martelli
Affiliation:
Departamento de Genética, Faculdade de Medicina de Ribeirão Preto–Universidade de São Paulo, Ribeirão Preto, São Paulo, Brasil.
Harris Lewin
Affiliation:
Department of Animal Sciences, University of Illinois at Urbana-Champaign, USA.
Flávio Vieira Meirelles*
Affiliation:
Departamento de Ciências Básicas, Faculdade de Zootecnia e Engenharia de Alimentos–Universidade de São Paulo, Pirassununga, São Paulo, Brasil.
*
All correspondence to: Flávio Meirelles. Departamento de Ciências Básicas, Faculdade de Zootecnia e Engenharia de Alimentos–Universidade de São Paulo, Pirassununga, São Paulo, Brasil. Tel: +55 19 3565 4112; Fax: +55 19 3565 4117. e-mail: meirellf@usp.br
Get access Rights & Permissions [Opens in a new window]

Summary

The mRNAs accumulated in oocytes provide support for embryo development until embryo genomic activation. We hypothesized that the maternal mRNA stock present in bovine oocytes is associated with embryo development until the blastocyst stage. To test our hypothesis, we analyzed the transcriptome of the oocyte and correlated the results with the embryo development. Our goal was to identify genes expressed in the oocyte that correlate with its ability to develop to the blastocyst stage. A fraction of oocyte cytoplasm was biopsied using micro-aspiration and stored for further expression analysis. Oocytes were activated chemically, cultured individually and classified according to their capacity to develop in vitro to the blastocyst stage. Microarray analysis was performed on mRNA extracted from the oocyte cytoplasm fractions and correlated with its ability to develop to the blastocyst stage (good quality oocyte) or arrest at the 8–16-cell stage (bad quality oocyte). The expression of 4320 annotated genes was detected in the fractions of cytoplasm that had been collected from oocytes matured in vitro. Gene ontology classification revealed that enriched gene expression of genes was associated with certain biological processes: ‘RNA processing’, ‘translation’ and ‘mRNA metabolic process’. Genes that are important to the molecular functions of ‘RNA binding’ and ‘translation factor activity, RNA binding’ were also enriched in oocytes. We identified 29 genes with differential expression between the two groups of oocytes compared (good versus bad quality). The content of mRNAs expressed in metaphase II oocytes influences the activation of the embryonic genome and enables further develop to the blastocyst stage.

Keywords

Blastocyst developmentDevelopmental competenceOocyte
Type
Research Article
Information
Zygote , Volume 22 , Issue 1 , February 2014 , pp. 69 - 79
Copyright
Copyright © Cambridge University Press 2012 

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.)

Article purchase

Temporarily unavailable

References

Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T., Harris, M.A., Hill, D.P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J.C., Richardson, J.E., Ringwald, M., Rubin, G.M. & Sherlock, G. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25–9.Google Scholar
Benjamini, Y. & Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Statist. Soc. B. 57, 289–300.Google Scholar
Biase, F.H., Fonseca Merighe, G.K., Santos Biase, W.K., 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., Merighe, G.K., Santos Biase, W.K., Miranda, M., Smith, L.C. & Meirelles, F.V. (2009). A retrospective model of oocyte competence: global mRNA and housekeeping transcripts are not associated with in vitro developmental outcome. Zygote 17, 289–95.CrossRefGoogle Scholar
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
Bilodeau-Goeseels, S. & Panich, P. (2002). Effects of oocyte quality on development and transcriptional activity in early bovine embryos. Anim. Reprod. Sci. 71, 143–55.Google Scholar
Blondin, P. & Sirard, M.A. (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev. 41, 54–62.Google Scholar
Brad, A.M., Hendricks, K.E. & Hansen, P.J. (2007). The block to apoptosis in bovine two-cell embryos involves inhibition of caspase-9 activation and caspase-mediated DNA damage. Reproduction 134, 789–97.Google Scholar
Caixeta, E.S., Ripamonte, P., Franco, M.M., Junior, J.B. & Dode, M.A. (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.Google Scholar
Calder, M.D., Caveney, A.N., Westhusin, M.E. & Watson, A.J. (2001). Cyclooxygenase-2 and prostaglandin E2 (PGE2) receptor messenger RNAs are affected by bovine oocyte maturation time and cumulus–oocyte complex quality, and PGE2 induces moderate expansion of the bovine cumulus in vitro. Biol. Reprod. 65, 135–40.Google Scholar
Carambula, S.F., Oliveira, L.J. & Hansen, P.J. (2009). Repression of induced apoptosis in the 2-cell bovine embryo involves DNA methylation and histone deacetylation. Biochem. Biophys. Res. Commun. 388, 418–21.Google Scholar
Carolan, C., Lonergan, P., Khatir, H. & Mermillod, P. (1996). In vitro production of bovine embryos using individual oocytes. Mol. Reprod. Dev. 45, 145–50.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Chen, L., Wang, D., Wu, Z., Ma, L. & Daley, G.Q. (2010). Molecular basis of the first cell fate determination in mouse embryogenesis. Cell Res. 20, 982–93.CrossRefGoogle ScholarPubMed
Cui, X.S., Li, X.Y., Yin, X.J., Kong, I.K., Kang, J.J. & Kim, N.H. (2007). Maternal gene transcription in mouse oocytes: genes implicated in oocyte maturation and fertilization. J. Reprod. Dev. 53, 405–18.Google Scholar
Dalbies-Tran, R. & Mermillod, P. (2003). Use of heterologous complementary DNA array screening to analyze bovine oocyte transcriptome and its evolution during in vitro maturation. Biol. Reprod. 68, 252–61.Google Scholar
Donnison, M. & Pfeffer, P.L. (2004). Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development. Biol. Reprod. 71, 1813–21.Google Scholar
Everts, R.E., Chavatte-Palmer, P., Razzak, A., Hue, I., Green, C.A., Oliveira, R., Vignon, X., Rodriguez-Zas, S.L., Tian, X.C., Yang, X., Renard, J.P. & Lewin, H.A. (2008). Aberrant gene expression patterns in placentomes are associated with phenotypically normal and abnormal cattle cloned by somatic cell nuclear transfer. Physiol. Genomics 33, 65–77.Google Scholar
Fair, T., Gutierrez-Adan, A., Murphy, M., Rizos, D., Martin, F., Boland, M.P. & Lonergan, P. (2004a). Search for the bovine homolog of the murine ped gene and characterization of its messenger RNA expression during bovine preimplantation development. Biol. Reprod. 70, 488–94.Google Scholar
Fair, T., Murphy, M., Rizos, D., Moss, C., Martin, F., Boland, M.P. & Lonergan, P. (2004b). Analysis of differential maternal mRNA expression in developmentally competent and incompetent bovine two-cell embryos. Mol. Reprod. Dev. 67, 136–44.Google Scholar
Fair, T., Carter, F., Park, S., Evans, A.C. & Lonergan, P. (2007). Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology 68 Suppl 1, S91–7.Google Scholar
Fear, J.M. & Hansen, P.J. (2011). Developmental changes in expression of genes involved in regulation of apoptosis in the bovine preimplantation embryo. Biol. Reprod. 84, 43–51.Google Scholar
Gardner, R.L. (2001). The initial phase of embryonic patterning in mammals. Int. Rev. Cytol. 203, 233–90.Google Scholar
Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., Hornik, K., Hothorn, T., Huber, W., Iacus, S., Irizarry, R., Leisch, F., Li, C., Maechler, M., Rossini, A.J., Sawitzki, G., Smith, C., Smyth, G., Tierney, L., Yang, J.Y. & Zhang, J. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.Google Scholar
Grondahl, M.L., Yding Andersen, C., Bogstad, J., Nielsen, F.C., Meinertz, H. & Borup, R. (2010). Gene expression profiles of single human mature oocytes in relation to age. Hum. Reprod. 25, 957–68.Google Scholar
Gutierrez-Adan, A., Rizos, D., Fair, T., Moreira, P.N., Pintado, B., de la Fuente, J., Boland, M.P. & Lonergan, P. (2004). Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro. Mol. Reprod. Dev. 68, 441–8.Google Scholar
Hamatani, T., Falco, G., Carter, M.G., Akutsu, H., Stagg, C.A., Sharov, A.A., Dudekula, D.B., VanBuren, V. & Ko, M.S. (2004). Age-associated alteration of gene expression patterns in mouse oocytes. Hum. Mol. Genet. 13, 2263–78.Google Scholar
Hellemans, J., Mortier, G., De Paepe, A., Speleman, F. & Vandesompele, J. (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.Google Scholar
Ihaka, R. & Gentleman, R. (1996). R: a language for data analysis and graphics. J. Comp. Graph. Stat. 5, 299–314.Google Scholar
Janny, L. & Menezo, Y. J. (1996). Maternal age effect on early human embryonic development and blastocyst formation. Mol. Reprod. Dev. 45, 31–7.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Jeanmougin, M., de Reynies, A., Marisa, L., Paccard, C., Nuel, G. & Guedj, M. (2010). Should we abandon the t-test in the analysis of gene expression microarray data: a comparison of variance modeling strategies. PLoS One 5, e12336.Google Scholar
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
Koo, D.H., McFadden, C., Huang, Y., Abdulhussein, R., Friese-Hamim, M. & Vogel, W.F. (2006). Pinpointing phosphotyrosine-dependent interactions downstream of the collagen receptor DDR1. FEBS Lett. 580, 15–22.Google Scholar
Kues, W.A., Sudheer, S., Herrmann, D., Carnwath, J.W., Havlicek, V., Besenfelder, U., Lehrach, H., Adjaye, J. & Niemann, H. (2008). Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo. Proc. Natl. Acad. Sci. USA 105, 19768–73.CrossRefGoogle ScholarPubMed
Lequarre, A.S., Traverso, J.M., Marchandise, J. & Donnay, I. (2004). Poly(A) RNA is reduced by half during bovine oocyte maturation but increases when meiotic arrest is maintained with CDK inhibitors. Biol. Reprod. 71, 425–31.Google Scholar
Lighten, A.D., Hardy, K., Winston, R.M. & Moore, G.E. (1997). Expression of mRNA for the insulin-like growth factors and their receptors in human preimplantation embryos. Mol. Reprod. Dev. 47, 134–9.Google Scholar
Lonergan, P., Khatir, H., Piumi, F., Rieger, D., Humblot, P. & Boland, M.P. (1999). Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos. J. Reprod. Fertil. 117, 159–67.Google Scholar
Lonergan, P., Gutierrez-Adan, A., Pintado, B., Fair, T., Ward, F., Fuente, J.D. & Boland, M. (2000). Relationship between time of first cleavage and the expression of IGF-I growth factor, its receptor, and two housekeeping genes in bovine two-cell embryos and blastocysts produced in vitro. Mol. Reprod. Dev. 57, 146–52.Google Scholar
Loor, J.J., Everts, R.E., Bionaz, M., Dann, H.M., Morin, D.E., Oliveira, R., Rodriguez-Zas, S.L., Drackley, J.K. & Lewin, H.A. (2007). Nutrition-induced ketosis alters metabolic and signaling gene networks in liver of periparturient dairy cows. Physiol. Genomics 32, 105–16.Google Scholar
Medina, I., Carbonell, J., Pulido, L., Madeira, S.C., Goetz, S., Conesa, A., Tarraga, J., Pascual-Montano, A., Nogales-Cadenas, R., Santoyo, J., Garcia, F., Marba, M., Montaner, D. & Dopazo, J. (2010). Babelomics: an integrative platform for the analysis of transcriptomics, proteomics and genomic data with advanced functional profiling. Nucleic Acids Res. 38 Suppl, W210–3.Google Scholar
Memili, E. & First, N. L. (2000). Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.Google Scholar
Misirlioglu, M., Page, G.P., Sagirkaya, H., Kaya, A., Parrish, J.J., First, N.L. & Memili, E. (2006). Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. Proc. Natl. Acad. Sci. USA 103, 18905–10.Google Scholar
Mourot, M., Dufort, I., Gravel, C., Algriany, O., Dieleman, S. & Sirard, M.A. (2006). The influence of follicle size, FSH-enriched maturation medium, and early cleavage on bovine oocyte maternal mRNA levels. Mol. Reprod. Dev. 73, 1367–79.Google Scholar
O'Doherty, A.M., O'Shea, L.C. & Fair, T. (2012). Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biol. Reprod. 86, 67.Google Scholar
Palacios, I.M. & St Johnston, D. (2001). Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. Annu. Rev. Cell Dev. Biol. 17, 569–614.Google Scholar
Pan, H., O'Brien, M.J., Wigglesworth, K., Eppig, J.J. & Schultz, R.M. (2005). Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev. Biol. 286, 493–506.Google Scholar
Patel, O.V., Bettegowda, A., Ireland, J.J., Coussens, P.M., Lonergan, P. & Smith, G.W. (2007). Functional genomics studies of oocyte competence: evidence that reduced transcript abundance for follistatin is associated with poor developmental competence of bovine oocytes. Reproduction 133, 95–106.Google Scholar
Revel, F., Mermillod, P., Peynot, N., Renard, J.P. & Heyman, Y. (1995). Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows. J. Reprod. Fertil. 103, 115–20.Google Scholar
Ritchie, M.E., Silver, J., Oshlack, A., Holmes, M., Diyagama, D., Holloway, A. & Smyth, G.K. (2007). A comparison of background correction methods for two-colour microarrays. Bioinformatics 23, 2700–7.Google Scholar
Robert, C., Barnes, F.L., Hue, I. & Sirard, M.A. (2000). Subtractive hybridization used to identify mRNA associated with the maturation of bovine oocytes. Mol. Reprod. Dev. 57, 167–75.Google Scholar
Roberts, R.M., Katayama, M., Magnuson, S.R., Falduto, M.T. & Torres, K.E. (2011). Transcript profiling of individual twin blastomeres derived by splitting two-cell stage murine embryos. Biol. Reprod. 84, 487–94.CrossRefGoogle ScholarPubMed
Romar, R., De Santis, T., Papillier, P., Perreau, C., Thelie, A., Dell'aquila, M., Mermillod, P. & Dalbies-Tran, R. (2011). Expression of maternal transcripts during bovine oocyte in vitro maturation is affected by donor age. Reprod. Domest. Anim. 46, e23–30.Google Scholar
Schmittgen, T.D. & Livak, K.J. (2008). Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101–8.Google Scholar
Smyth, G. (2003). Normalization of cDNA microarray data. Methods. 31, 265–273.Google Scholar
Smyth, G.K. (2004). Linear models and empirical Bayes methods for assessing differencial expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, 3.Google Scholar
Smyth, G.K. (2005). Limma: Linear Models for Microarray Data. Springer: New York, pp. 397–420.Google Scholar
Smyth, G.K., Michaud, J. & Scott, H.S. (2005). Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21, 2067–75.CrossRefGoogle ScholarPubMed
Steuerwald, N.M., Bermudez, M.G., Wells, D., Munne, S. & Cohen, J. (2007). Maternal age-related differential global expression profiles observed in human oocytes. Reprod. Biomed. Online 14, 700–8.Google Scholar
Sutovsky, P., Flechon, J.E. & Pavlok, A. (1995). F-actin is involved in control of bovine cumulus expansion. Mol. Reprod. Dev. 41, 521–9.Google Scholar
Tang, F., Barbacioru, C., Nordman, E., Bao, S., Lee, C., Wang, X., Tuch, B.B., Heard, E., Lao, K. & Surani, M.A. (2011). Deterministic and stochastic allele specific gene expression in single mouse blastomeres. PLoS One. 6, e21208.Google Scholar
Tervit, H.R., Whittingham, D.G. & Rowson, L.E. (1972). Successful culture in vitro of sheep and cattle ova. J. Reprod. Fertil. 30, 493–7.Google Scholar
Vogel, W.F., Abdulhussein, R. & Ford, C.E. (2006). Sensing extracellular matrix: an update on discoidin domain receptor function. Cell Signal 18, 1108–16.Google Scholar
Wang, L.M., Feng, H.L., Ma, Y.Z., Cang, M., Li, H.J., Yan, Z., Zhou, P., Wen, J.X., Bou, S. & Liu, D.J. (2009). Expression of IGF receptors and its ligands in bovine oocytes and preimplantation embryos. Anim. Reprod. Sci. 114, 99–108.Google Scholar
Warzych, E., Wrenzycki, C., Peippo, J. & Lechniak, D. (2007). Maturation medium supplements affect transcript level of apoptosis and cell survival related genes in bovine blastocysts produced in vitro. Mol. Reprod. Dev. 74, 280–9.Google Scholar
Yaseen, M.A., Wrenzycki, C., Herrmann, D., Carnwath, J.W. & Niemann, H. (2001). Changes in the relative abundance of mRNA transcripts for insulin-like growth factor (IGF-I and IGF-II) ligands and their receptors (IGF-IR/IGF-IIR) in preimplantation bovine embryos derived from different in vitro systems. Reproduction. 122, 601–10.Google Scholar
Yuan, J.S., Reed, A., Chen, F. & StewartC.N., Jr. C.N., Jr. (2006). Statistical analysis of real-time PCR data. BMC Bioinformatics 7, 85.Google Scholar