Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-26T00:59:01.913Z Has data issue: false hasContentIssue false
  • English
  • Français

Global poly(A) mRNA expression profile measured in individual bovine oocytes and cleavage embryos

Published online by Cambridge University Press:  01 February 2008

F.H. Biase ,
G. Krempel Fonseca Merighe ,
W. Karyna Freitas Santos Biase ,
L. Martelli  and
F. Vieira Meirelles
F.H. Biase
Affiliation:
Universidade de São Paulo – Faculdade de Zootecnia e Engenharia de Alimentos Departamento de Ciências Básicas, Rua Duque de Caxias Norte 225, Pirassununga–SP, Brasil. Departamento de Genética, Faculdade de Medicina de Ribeirão Preto–Universidade de São Paulo, Ribeirão Preto, São Paulo, Brasil.
G. Krempel Fonseca Merighe
Affiliation:
Universidade de São Paulo – Faculdade de Zootecnia e Engenharia de Alimentos Departamento de Ciências Básicas, Rua Duque de Caxias Norte 225, Pirassununga–SP, Brasil.
W. Karyna Freitas Santos Biase
Affiliation:
Universidade de São Paulo – Faculdade de Zootecnia e Engenharia de Alimentos Departamento de Ciências Básicas, Rua Duque de Caxias Norte 225, Pirassununga–SP, Brasil.
L. Martelli
Affiliation:
Departamento de Genética, Faculdade de Medicina de Ribeirão Preto–Universidade de São Paulo, Ribeirão Preto, São Paulo, Brasil.
F. Vieira Meirelles*
Affiliation:
Universidade de São Paulo – Faculdade de Zootecnia e Engenharia de Alimentos Departamento de Ciências Básicas, Rua Duque de Caxias Norte 225, Pirassununga–SP, Brasil.
*
All correspondence to: Flávio Vieira Meirelles. Universidade de São Paulo – Faculdade de Zootecnia e Engenharia de Alimentos Departamento de Ciências Básicas, Rua Duque de Caxias Norte 225, Pirassununga–SP, Brasil. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The objective of this article was to estimate quantitative differences for GAPDH transcripts and poly(A) mRNA: (i) between oocytes collected from cumulus–oocyte complexes (COCs) qualified morphologically as grades A and B; (ii) between grade A oocytes before and after in vitro maturation (IVM); and (iii) among in vitro-produced embryos at different developmental stages. To achieve this objective a new approach was developed to estimate differences between poly(A) mRNA when using small samples. The approach consisted of full-length cDNA amplification (acDNA) monitored by real-time PCR, in which the cDNA from half of an oocyte or embryo was used as a template. The GAPDH gene was amplified as a reverse transcription control and samples that were not positive for GAPDH transcripts were discarded. The fold differences between two samples were estimated using delta Ct and statistical analysis and were obtained using the pairwise fixed reallocation randomization test. It was found that the oocytes recovered from grade B COCs had quantitatively less poly(A) mRNA (p < 0.01) transcripts compared with grade A COCs (1 arbitrary unit expression rate). In the comparison with immature oocytes (1 arbitrary unit expression rate), the quantity of poly(A) mRNA did not change during IVM, but declined following IVF and varied with embryo culture (p < 0.05). Amplification of cDNA by real-time PCR was an efficient method to estimate differences in the amount of poly(A) mRNA between oocytes and embryos. The results obtained from individual oocytes suggested an association between poly(A) mRNA abundance and different morphological qualities of oocytes from COCs. In addition, a poly(A) mRNA profile was characterized from oocytes undergoing IVM, fertilization and blastocyst heating.

Keywords

CattlecDNA amplificationCumulus–oocyte complexEmbryoOocyteReal-time PCR
Type
Research Article
Information
Zygote , Volume 16 , Issue 1 , February 2008 , pp. 29 - 38
Copyright
Copyright © Cambridge University Press 2008

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

Alizadeh, Z., Kageyama, S. & Aoki, F. (2005). Degradation of maternal mRNA in mouse embryos., selective degradation of specific mRNAs after fertilization. Mol. Reprod. Dev. 72, 281–90.CrossRefGoogle ScholarPubMed
Aoki, F., Hara, K.T. & Schultz, R.M. (2003). Acquisition of transcriptional competence in the 1-cell mouse embryo, requirement for recruitment of maternal mRNAs. Mol. Reprod. Dev. 64, 270–4.CrossRefGoogle ScholarPubMed
Bachvarova, R. & De Leon, V. (1980). Polyadenylated RNA of mouse ova and loss of maternal RNA in early development. Dev. Biol. 74, 1–8.CrossRefGoogle ScholarPubMed
Barnes, F.L. & Eyestone, W.H. (1990). Early cleavage and the maternal zygotic transition in bovine embryos. Theriogenology 33, 141–9.CrossRefGoogle Scholar
Bettegowda, A., Patel, O.V., Ireland, J.J. & Smith, G.W. (2006). Quantitative analysis of messenger RNA abundance for ribosomal protein L-15, cyclophilin-A, phosphoglycerokinase, B-glucuronidase, glyceraldehyde 3-phosphate dehydrogenase, B-actin and histone H2A during bovine oocyte maturation and early embryogenesis in vitro. Mol. Reprod. Dev. 73, 267–78.CrossRefGoogle Scholar
Bilodeau-Goeseels, S. & Panich, P. (2002). Effects of oocyte quality on development and transcriptional activity in early bovine embryos. Anim. Reprod. Sci. 71, 143.CrossRefGoogle ScholarPubMed
Blondin, P. & Sirard, M.A. (1995). Oocyte and follicular morphology as determined characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev. 41, 54–62.CrossRefGoogle ScholarPubMed
Brevini, T.A., Lonergan, P., Cillo, F., Francisci, C., Favetta, L.A., Fair, T. & Gandolfi, F. (2002). Evolution of mRNA polyadenylation between oocyte maturation and first embryonic cleavage in cattle and its relation with developmental competence. Mol. Reprod. Dev. 63, 510–7.CrossRefGoogle ScholarPubMed
Brevini-Gandolfi, T.A., Favetta, L.A., Maurri, L., Luciano, A.M., Cillo, F. & Gandolfi, F. (1999). Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. Mol. Reprod. Dev. 52, 427–33.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Deprez, R.H.L., Fijnvandraat, A.C., Ruijter, J.M. & Moorman, A.F.M. (2002). Sensitivity and accuracy of quantitative real-time polymerase chain reaction using SYBR green I depend on cDNA synthesis conditions. Anal. Biochem. 307, 63–9.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Eichenlaub-Ritter, U. & Peschke, M. (2002). Expression in in-vivo and in-vitro grown and maturing oocytes, focus on regulation of expression at the translational level. Human Reprod. Update 8, 21–41.CrossRefGoogle Scholar
Fair, T., Hyttel, P. & Greve, T. (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437–42.CrossRefGoogle ScholarPubMed
Fair, T., Murphy, M., Rizos, D., Moss, C., Martin, F., Boland, MP. & Lonergan, P. (2004). Analysis of differential maternal mRNA expression in developmentally competent and incompetent bovine two-cell embryos. Mol. Reprod. Dev. 67, 136–44.CrossRefGoogle ScholarPubMed
Gordon, I. (1994). Laboratory Production of Cattle Embryos, p. 640. Oxon: CAB International.Google Scholar
Hamatani, T., Carter, M.G., Sharov, A.A. & Ko, M.S. (2004). Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117–31.CrossRefGoogle ScholarPubMed
Han, D., Song, S., Uhum, S.J., Do, J., Kim, N., Chung, K. & Lee, H.T. (2003). Expression of IGF2 and IGF receptor mRNA in bovine nuclear transferred embryos. Zygote 11, 245–52.CrossRefGoogle ScholarPubMed
Hawk, H.W. & Wall, R.J. (1994). Improved yields of bovine blastocysts from in vitro-produced oocytes. II. Media and co-culture cells. Theriogenology 41, 1585.CrossRefGoogle Scholar
Hyttel, P., Fair, T., Callesen, H. & Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.CrossRefGoogle Scholar
Iscove, N.N., Barbara, M., Gu, M., Gibson, M., Modi, C. & Winegarden, N. (2002). Representation is faithfully preserved in global cDNA amplified exponentially from sub-picogram quantities of mRNA. Nat. Biotechnol. 20, 940–3.CrossRefGoogle ScholarPubMed
Jakobsen, A.S., Avery, B., Dieleman, S.J., Knijn, H.M., Vos, P.L. & Thomsen, P.D. (2006). Transcription of ribosomal RNA genes is initiated in the third cell cycle of bovine embryos. Mol. Reprod. Dev. 73, 196–205.CrossRefGoogle ScholarPubMed
Kastrop, P.M., Bevers, M.M., Destree, O.H. & Kruip, T.A. (1991). Protein synthesis and phosphorylation patterns of bovine oocytes maturing in vivo. Mol. Reprod. Dev. 29, 271–5.CrossRefGoogle ScholarPubMed
Kulpa, D., Topping, R. & Telesnitsky, A. (1997). Determination of the site of first strand transfer during Moloney murine leukemia virus reverse transcription and identification of strand transfer-associated reverse transcriptase errors. EMBO J. 16, 856–65.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.CrossRefGoogle ScholarPubMed
Liss, B. (2002). Improved quantitative real-time RT-PCR for expression profiling of individual cells. Nucleic Acid Res. 30, e89.CrossRefGoogle ScholarPubMed
Lonergan, P., Rizos, D., Ward, F. & Boland, M.P. (2001). Factors influencing oocyte and embryo quality in cattle. Reprod. Nutr. Dev. 41, 427–37.CrossRefGoogle ScholarPubMed
Lonergan, P., Rizos, D., Gutiérrez-Adán, A., Moreira, P.M., Pintado, B., de la Fuente, J. & Boland, M.P. (2003). Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol. Reprod. 69, 1424–31.CrossRefGoogle ScholarPubMed
Meirelles, F.V., Caetano, A.R., Watanabe, Y.F., Ripamonte, P., Carambula, S.F., Merighe, G.K. & Garcia, S.M. (2004). Genome activation and developmental block in bovine embryos. Anim. Reprod. Sci. 82–3, 13–20.CrossRefGoogle Scholar
Memili, E. & First, N.L. (1999). Control of gene expression at the onset of bovine embryonic development. Biol. Reprod. 61, 1198–207.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 oocytes maternal mRNA levels. Mol. Reprod. Dev. 73, 1367–79.CrossRefGoogle ScholarPubMed
Nagy, Z.B., Kelemen, J.Z., Fehér, L.Z., Zvara, A., Juház, K. & Puskás, L.G. (2005). Real time polymerase chain reaction-based exponential sample amplification for microarray gene expression profiling 337, 76–83.Google ScholarPubMed
Neilson, L., Andalibi, A., Kang, D., Coutifaris, C., Strauss, J.F., 3rd, Stanton, J.A. & Green, D.P. (2000). Molecular phenotype of the human oocyte by PCR–SAGE. Genomics 63, 13–24.CrossRefGoogle ScholarPubMed
Parrish, J.J., Susku-Parrish, J., Winer, M.A. & First, N.L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–80.CrossRefGoogle ScholarPubMed
Pavlok, A., Lucas-Hahn, A. & Niemann, H. (1992). Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol. Reprod. Dev. 31, 63–7.CrossRefGoogle ScholarPubMed
Payton, B.V., Rempel, R. & Bachvarova, R. (1988). Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse. Dev. Biol. 129, 304–24.CrossRefGoogle Scholar
Pennetier, S., Uzbekova, S., Perreau, C., Papillier, P., Mermillod, P. & Dalbies-Tran, R. (2004). Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, and VASA in adult bovine tissues, oocytes and preimplantation embryos. Biol. Reprod. 71, 1359–66.CrossRefGoogle ScholarPubMed
Perez, G.I., Tao, X.J. & Tilly, J.L. (1999). Fragmentation and death (a.k.a. apoptosis) of ovulated oocytes. Mol. Hum. Reprod. 5, 414–20.CrossRefGoogle ScholarPubMed
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acid Res. 29, 2002–7.CrossRefGoogle ScholarPubMed
Pfaffl, M.W., Horgan, G.W. & Dempfle, L. (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acid Res. 30, e36.CrossRefGoogle Scholar
Piccioni, F., Zappavigna, V. & Verrotti, A.Translational regulation during oogenesis and early development, the cap-poly(A) tail relationship. C R Biol. (2005). 328, 863–81.CrossRefGoogle ScholarPubMed
Picton, H., Briggs, D. & Gosden, R. (1998). The molecular basis of oocyte growth and development. Mol. Cell. Endocrinol. 145, 27–37.CrossRefGoogle ScholarPubMed
Pikó, L. & Clegg, K.B. (1982). Quantitative changes in total RNA, total poly(A) and ribosomes in early mouse embryos. Dev. Biol. 89, 362–78.CrossRefGoogle ScholarPubMed
Plante, L., Plante, C., Shepherd, D.L. & King, W.A. (1994). Cleavage and 3H-uridine incorporation in bovine embryos of high in vitro developmental potential. Mol. Reprod. Dev. 39, 375–83.CrossRefGoogle ScholarPubMed
Ramakers, C., Ruijter, J., Deprez, R.H.L. & Moorman, A.F.M. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letts. 339, 62–6.CrossRefGoogle ScholarPubMed
Robert, C., McGraw, S., Massicotte, L., Pravetoni, M., Gandolfi, F. & Sirard, M.A. (2002). Quantification of housekeeping transcript levels during the development of bovine preimplantation embryos. Biol. Reprod. 67, 1465–72.CrossRefGoogle ScholarPubMed
Roller, R.J., Kinloch, R.A., Hiraoka, B.Y., Li, S.S. & Wassarman, P.M. (1989). Gene expression during mammalian oogenesis and early embryogenesis, quantification of three messenger RNAs abundant in fully grown mouse oocytes. Development 106, 251–61.CrossRefGoogle ScholarPubMed
Sakurai, T., Sato, M. & Kimura, M. (2005). Diverse patterns of poly(A) tail elongation and shortening of murine maternal mRNAs from fully grown oocyte to 2-cell embryo stages. Biochem. Biophys. Res. Commun. 336, 1181–9.CrossRefGoogle ScholarPubMed
Salamone, D.F., Adams, G.P. & Mapletoft, R.J. (1999). Changes in the cumulus–oocyte complex of subordinate follicles relative to follicular wave status in cattle. Theriogenology 52, 549–61.CrossRefGoogle ScholarPubMed
Seth, D., Gorrell, M.D., McGuiness, P.H., Leo, M.A., Lieber, C.S., McCaughan, G.W. & Haber, P.S. (2003). SMART amplification maintains representation of relative gene expression., quantitative validation by real time PCR and application to studies of alcoholic liver disease in primates. J. Biochem. Biophys. Methods 55, 53–66.CrossRefGoogle ScholarPubMed
Seveg, H., Memili, E. & First, N.L. (2001). Expression patterns of histone deacetylases in bovine oocytes and early embryos and the effect of their inhibition on embryo development. Zygote 9, 123–33.Google Scholar
Sirard, M.A., Florman, H.M., Leibfried-Rutledge, M.L., Barnes, F.L. & Sims, M.L. & First, N.L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–63.CrossRefGoogle ScholarPubMed
Sirard, M.A., Dufort, I., Vallee, M., Massicotte, L., Gravel, C., Reghenas, H., Watson, A.J., King, W.A. & Robert, C. (2005). Potential and limitations of bovine-specific arrays for the analysis of mRNA levels in early development., preliminary analysis using a bovine embryonic array. Reprod. Fertil. Dev. 17, 47–57.CrossRefGoogle ScholarPubMed
Sirard, M-A., Richard, F., Blondin, P. & Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126.CrossRefGoogle ScholarPubMed
Telford, N.A., Watson, A.J. & Schultz, G.A. (1990). Transition from maternal to embryonic control in early mammalian development. A comparison of several species. Mol. Reprod. Dev. 26, 90–100.CrossRefGoogle ScholarPubMed
Tesfaye, D., Ponsuksili, S., Wimmers, K., Gilles, M. & Schellander, K. (2003). Identification and quantification of differentially expressed transcripts in in vitro-produced bovine preimplantation stage embryos. Mol. Reprod. Dev. 66, 105–14.CrossRefGoogle ScholarPubMed
Van Blerkom, J. & Davis, P.W. (1998). DNA strand breaks and phosphatidylserine redistribution in newly ovulated and cultured mouse and human oocytes., occurrence and relationship to apoptosis. Hum. Reprod. 13, 1317–24.CrossRefGoogle ScholarPubMed
Vigneault, C., McGraw, S., Massicotte, L. & Sirard, M.A. (2004). Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal-zygotic transition. Biol. Reprod. 70, 1701–9.CrossRefGoogle ScholarPubMed
Yuan, Y.Q., Van Soom, A., Leroy, J.L., Dewulf, J., Van Zeveren, A., de Kruif, A. & Peelman, L.J. (2005). Apoptosis in cumulus cells., but not in oocytes., may influence bovine embryonic developmental competence. Theriogenology 63, 2147–63.CrossRefGoogle Scholar
Zeng, F., Baldwin, D.A. & Schultz, R.M. (2004). Transcript profiling during preimplantation mouse development. Dev. Biol. 272, 483–96.CrossRefGoogle ScholarPubMed
Zhu, Y.Y., Machleder, E.M., Chenchik, A., Li, R. & Siebert, P.D. (2001). Reverse transcriptase template switching, a SMART approach for full-length cDNA library construction. Biotechniques 30, 892–7.CrossRefGoogle Scholar