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Gene expression in the in vitro-produced preimplantation bovine embryos

Published online by Cambridge University Press:  01 November 2007

H. Badr
Istituto Sperimentale Italiano “Lazzaro Spallanzani”, Località La Quercia, Rivolta D'Adda 26027 (Cremona), Italy.
G. Bongioni
Istituto Sperimentale Italiano “Lazzaro Spallanzani”, Località La Quercia, Rivolta D'Adda 26027 (Cremona), Italy.
A.S.S. Abdoon
Department of Animal Reproduction & A.I, National Research Centre, Dokki 12311, Cairo, Egypt.
O. Kandil
Department of Animal Reproduction & A.I, National Research Centre, Dokki 12311, Cairo, Egypt.
R. Puglisi*
Istituto Sperimentale Italiano “Lazzaro Spallanzani”, Località La Quercia, Rivolta D'Adda 26027 (Cremona), Italy.
All correspondence to: Roberto Puglisi, Istituto Sperimentale Italiano “Lazzaro Spallanzani”, Località La Quercia, Rivolta D'Adda 26027 (Cremona), Italy. Tel: +39 0363 78883. Fax: +39 0363 37047981. e-mail:


Recent studies have demonstrated the relevance of a gene expression profile as a clinically important key feature determining embryo quality during the in vitro preimplantation period. Although the oocyte origin can play a crucial role in blastocyst yield, the postfertilization culture period has a profound effect in determining the blastocyst quality with particular regard to the relative abundance of many developmentally and clinically important candidate genes. During the preimplantation period, the embryo undergoes several morphogenetic developmental events including oocyte maturation, minor and major forms of embryonic genome activation and transition of transcription from maternal to embryonic control. The effect of an altered gene expression pattern on the in vitro-produced bovine embryos, particularly when cultured under suboptimal conditions, was reflected by the occurrence of clinically important phenomena like apoptosis and the large offspring syndrome. This review attempts to focus on the morphogenetic embryo development and gene expression profile in the in vitro-produced bovine embryos, with special emphasis on the different parameters that may alter gene expression pattern during the critical period of in vitro culture. The effect of the in vitro system, as reflected by some clinically important phenomena like apoptosis, is also discussed.

Research Article
Zygote , Volume 15 , Issue 4 , November 2007 , pp. 355 - 367
Copyright © Cambridge University Press 2007

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Barnes, F.L. & Eyestone, W.H. (1990). Early cleavage and maternal zygotic transition in bovine embryos. Theriogenology 33, 141–52.CrossRefGoogle Scholar
Barnes, F.L. & First, N.L. (1991). Embryonic transcription in in vitro cultured bovine embryos. Mol. Reprod. Dev. 29, 117–23.CrossRefGoogle ScholarPubMed
Bashirulla, A., Halsell, S.R., Cooperstock, R.L., Kloc, M., Karaiskakis, A., Fisher, W.W., Fu, W., Hamilton, J.K., Etkin, L.D. & Lipshitz, H.D. (1999). Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J. 18, 2610–20.CrossRefGoogle Scholar
Bavister, B.D. (2002). Early history of in vitro fertilisation. Reproduction 124, 181–96.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, β-glucuronidase, glyceraldehyde 3 phosphate dehydrogenase, β-actin and histone H2A during bovine oocyte maturation and early embryogenesis in vitro. Mol. Reprod. Dev. 73, 267–78.CrossRefGoogle ScholarPubMed
Betteridge, K.J. & Flechon, J.E. (1988). The anatomy and physiology of pre-attachment bovine embryos. Theriogenology 29, 155–87.CrossRefGoogle Scholar
Betts, D.H. & King, W.A. (2001). Genetic regulation of embryo death and senescence. Theriogenology 55, 171–91.CrossRefGoogle ScholarPubMed
Bilodeau-Goeseels, S. (2003). Effect of oocyte quality on the relative abundance of specific gene transcripts in bovine mature oocytes and 16-cell embryos. Cana. J. Vet. Res. 67, 151–6.Google 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.CrossRefGoogle ScholarPubMed
Boni, R., Tosti, E., Roviello, S. & Dale, B. (1999). Intercellular communication in in vivo-produced and in vitro-produced bovine embryos. Biol. Reprod. 61, 1050–5.CrossRefGoogle Scholar
Brackett, B.G. & Zuelke, K.A. (1993). Analysis of factors involved in the in vitro production of bovine embryos. Theriogenology 39, 4364.CrossRefGoogle Scholar
Brackett, B.G., Bousquet, D., Boice, M.L., Donawick, W.J., Evans, J.F. & Dressel, M.A. (1982). Normal development following in vitro fertilization in the cow. Biol. Reprod. 27, 147–58.CrossRefGoogle ScholarPubMed
Brevini-Gandolfi, T.A.L., Favetta, L.A., Mauri, 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
Brill, A., Torchinsky, A., Carp, H. & Toder, V. (1999). The role of apoptosis in normal and abnormal embryonic development. J. Assi. Reprod. Gene 16, 512–9.CrossRefGoogle ScholarPubMed
Brison, D.R. & Schultz, R.M. (1997). Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor α1. Biol. Reprod. 56, 1088–96.CrossRefGoogle Scholar
Byrne, A.T., Southgate, J., Brison, D.R. & Leese, H.J. (1999). Analysis of apoptosis in the pre-implantation bovine embryo using TUNEL. J. Reprod. Fertil. 117, 97105.CrossRefGoogle Scholar
Chan, A.W.S., Homan, E.J., Ballou, L.U., Burns, J.C. & Bremel, R.D. (1998). Transgenic cattle produced by reverse-transcribed gene transfer in oocytes. Proc. Natl. Acad. Sci. USA 95, 14028–33.CrossRefGoogle ScholarPubMed
Chandolia, R.K., Peltier, M.R., Tian, W. & Hansen, P.J. (1999). Transcriptional control of development, protein synthesis and heat-induced heat shock protein 70 synthesis in 2-cell bovine embryos. Biol. Reprod. 61, 1644–8.CrossRefGoogle ScholarPubMed
Corcoran, D., Fair, T. & Lonergan, P. (2005). Predicting embryo quality: mRNA expression and the pre-implantation embryo. Reprod. BioMed. Online 11, 340–8.CrossRefGoogle Scholar
Cotter, T.G., Lennon, S.V., Glynn, J.G. & Martin, S.J. (1990). Cell death via apoptosis and its relationship to growth, development and differentiation of both tumour and normal cells. Antican. Res. 10, 1153–9.Google 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
De La Fuente, R, Hahnel, A., Basrur, P.K. & King, W.A. (1999). X inactive-specific transcript (Xist) expression and X chromosome inactivation in the pre-attachment bovine embryo. Biol. Reprod. 60, 769–75.CrossRefGoogle Scholar
de Oliveira, A.T.D., Lopes, R.F.F. & Rodrigues, J.L (2006). Gene expression and developmental competence of bovine embryos produced in vitro with different serum concentrations. Reprod. Dom. Anim. 41, 129–36.CrossRefGoogle Scholar
De Sousa, P.A., Caveney, A., Westhusin, M.E. & Watson, A.J. (1998). Temporal patterns of embryonic gene expression and their dependence on oogenetic factors. Theriogenology 49, 115–28.CrossRefGoogle ScholarPubMed
Dieleman, S.J., Hendriksen, P.J.M., Viuff, D., Thomsen, P.D., Hyttel, P., Knijn, H.M., Wrenzycki, C., Kruip, T.A.M., Niemann, H., Gadella, B.M., Bevers, M.M. & Vos, P.L.A.M. (2002). Effects of in vivo pre-maturation and in vivo final maturation on developmental capacity and quality of pre-implantation embryos. Theriogenology 57, 520.CrossRefGoogle Scholar
Dode, M.A.N., Dufort, I., Massicotte, L. & Sirard, M-A. (2006). Quantitative expression of candidate genes for developmental competence in bovine two-cell embryos. Mol. Reprod. Dev. 73, 288–97.CrossRefGoogle ScholarPubMed
Edwards, R.G. (1965). Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208, 349–51.CrossRefGoogle ScholarPubMed
Ellis, R.E., Yuan, J.Y. & Horvits, H.R. (1991). Mechanisms and functions of cell death. Annu. Rev. Cell Bio. 7, 663–98.CrossRefGoogle ScholarPubMed
Enright, B.P., Lonergan, P., Dinnyes, A., Fair, T., Ward, F.A., Yang, X. & Boland, M.P. (2000). Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality. Theriogenology 54, 659–73.CrossRefGoogle ScholarPubMed
Farin, C.E., Farin, P.W. & Piedrahita, J.A. (2004). Development of fetuses from in vitro-produced and cloned bovine embryos. J. Anim Sci. 82, E53E62.Google ScholarPubMed
Galli, C. & Lazzari, G. (1996). Practical aspects of IVM/IVF in cattle. Anim. Reprod. Sci. 42, 371–9.CrossRefGoogle Scholar
Gasparrini, B. (2002). In vitro embryo production in buffalo species: state of the art. Theriogenology 57, 237–56.CrossRefGoogle ScholarPubMed
Gjorret, J.O., Avery, B., Larsson, L-I., Schellander, K. & Hyttel, P. (2001). Apoptosis in bovine blastocysts produced in vivo and in vitro. Theriogenology 55, 321 (abstract).Google Scholar
Gjorret, J.O., Knijn, H.M., Dieleman, S.J., Avery, B., Larsson, L-I. & Maddox-Hyttel, P. (2003). Chronology of apoptosis in bovine embryos produced in vivo and in vitro. Biol. Reprod. 69, 1193–200.CrossRefGoogle ScholarPubMed
Gordon, I. & Lu, K.H. (1990). Production of embryos in vitro and its impact on livestock production. Theriogenology 33, 7787.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Hall, V.J., Ruddock, N.T. & French, A.J. (2005). Expression profiling of genes crucial for placental and pre-implantation development in bovine in vivo, in vitro and nuclear transfer blastocysts. Mol. Reprod. Dev. 72, 1624.CrossRefGoogle Scholar
Handyside, A.H. & Hunter, S. (1986). Cell division and death in the mouse blastocyst before implantation. Roux's Archi. Dev. Biol. 195, 519–26.CrossRefGoogle ScholarPubMed
Hardy, K. (1997). Cell death in the mammalian blastocyst. Mol. Hum. Reprod. 3, 919925.CrossRefGoogle ScholarPubMed
Hardy, K. (1999). Apoptosis in the human embryo. Rev. Reprod. 4, 125–34.CrossRefGoogle ScholarPubMed
Harvey, M.P., Arcellana-Panlilio, M.Y., Zhang, X., Schultz, G.A. & Watson, A.J. (1995). Expression of genes encoding antioxidant enzymes in pre-implantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biol. Reprod. 53, 532–40.CrossRefGoogle Scholar
Holm, P., Booth, P.J. & Callesen, H. (2002). Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media. Reproduction 123, 553–65.CrossRefGoogle ScholarPubMed
Hyttel, P., Viuff, D., Avery, B., Laurincik, J. & Greve, T. (1996). Transcription and cell cycle-dependent development of intranuclear bodies and granules in two-cell bovine embryos. J. Reprod. Fertil. 108, 263–70.CrossRefGoogle ScholarPubMed
Hyttel, P., Fair, T., Callesen, H. & Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 2332.CrossRefGoogle Scholar
Hyttel, P., Laurincik, J., Viuff, D., Fair, T., Zakhartchenko, V., Rosenkranz, C., Avery, B., Rath, D., Niemann, H., Thomsen, P.D., Schellander, K., Callesen, H., Wolf, E., Ochs, R.L. & Greve, T. (2000). Activation of ribosomal RNA genes in pre-implantation cattle and swine embryos. Anim. Reprod. Sci. 60–61, 4960.CrossRefGoogle Scholar
Hyttel, P., Viuff, D., Fair, T., Laurincik, J., Thomsen, P.D., Callesen, H., Vos, P.L.A.M., Hendriksen, P.J.M., Dieleman, S.J., Schellander, K., Besenfelder, U. & Greve, T. (2001). Ribosomal RNA gene expression and chromosome aberrations in bovine oocytes and pre-implantation embryos. Reproduction 122, 2130.CrossRefGoogle Scholar
Jurisicova, A. & Acton, B.M. (2004). Deadly decisions: the role of genes regulating programmed cell death in human pre-implantation embryo development, Reproduction 128, 281–91.CrossRefGoogle Scholar
Kanka, J. (2003). Gene expression and chromatin structure in the pre-implantation embryo. Theriogenology 59, 319.CrossRefGoogle ScholarPubMed
Khurana, N. & Niemann, H. (2000). Energy metabolism in pre-implantation bovine embryos derived in vitro or in vivo. Biol. Reprod. 62, 847–56.CrossRefGoogle ScholarPubMed
Knijn, H.M. (2004). Gene expression and apoptosis in bovine embryos during in vitro culture and in vivo development. Ph.D. Thesis, Faculty of Veterinary Medicine, Utrecht University, Netherlands.Google Scholar
Knijn, H.M., Wrenzycki, C., Hendriksen, P.J.M., Vos, P.L.A.M, Herrmann, D., Van Der Weijden, G.C., Niemann, H. & Dieleman, S.J. (2002). Effect of oocyte maturation regimen on the relative abundance of gene transcripts in bovine blastocysts derived in vitro or in vivo. Reproduction 124, 365–75.CrossRefGoogle ScholarPubMed
Krajewski, S., Tanaka, S., Takayama, S., Schibler, M.J., Fenton, W. & Reed, J.C. (1993). Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum and outer mitochondrial membranes. Canc. Res. 53, 4701–14.Google ScholarPubMed
Lazzari, G., Wrenzycki, C., Herrmann, D., Duchi, R., Kruip, T., Niemann, H. & Galli, C. (2002). Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome. Biol. Reprod. 67, 767–75.CrossRefGoogle ScholarPubMed
Lequarre, A.S., Marchandise, J., Moreau, B., Massip, A. & Donnay, I. (2003). Cell cycle duration at the time of maternal zygotic transition for in vitro produced bovine embryos: effect of oxygen tension and transcription inhibition. Biol. Reprod. 69, 1707–13.CrossRefGoogle ScholarPubMed
Leunda-Casi, A., Genicot, G., Donnay, I., Pampfer, S. & De Hertogh, R. (2002). Increased cell death in mouse blastocysts exposed to high d-glucose in vitro: implications of an oxidative stress and alterations in glucose metabolism. Diabetologia 45, 571–9.CrossRefGoogle ScholarPubMed
Lonergan, P., Khatir, H., Puimi, F., Rieger, D., Humblot, P. & Boland, M.P. (1999). Effect of time interval from insemination to first cleavage on the developmental characteristics, sex and pregnancy rates following transfer of bovine pre-implantation embryos. J. Reprod. Fertil. 117, 159–67.CrossRefGoogle Scholar
Lonergan, P., Monaghan, P., Rizos, D., Boland, M.P. & 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, 4853.CrossRefGoogle ScholarPubMed
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Fair, T. & Boland, M.P. (2003a). Effect of culture environment on embryo quality and gene expression–experience from animal studies. Reprod. BioMed. Online 7, 657–63.CrossRefGoogle ScholarPubMed
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Fair, T. & Boland, M.P. (2003d). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod. Dom. Anim. 38, 259–67.CrossRefGoogle ScholarPubMed
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Moreira, P.M., Pintado, B. & de la Fuente, J. (2003c). 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
Lonergan, P., Rizos, D., Kanka, J., Nemcova, L., Mbaye, A.M., Kingston, M., Wade, M., Duffy, P. & Boland, M.P. (2003b). Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction 126, 337–46.CrossRefGoogle ScholarPubMed
Matwee, C., Kamaruddin, M., Betts, D.H., Basrur, P.K. & King, W.A. (2001). The effects of antibodies to heat shock protein 70 in fertilization and embryo development. Mol. Hum. Reprod. 7, 829–37.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. 82–83, 1320.CrossRefGoogle ScholarPubMed
Memili, E. & First, N.L. (1998). Developmental changes in RNA polymerase II in bovine oocytes, early embryos and effect of alpha-amanitin on embryo development. Mol. Reprod. Dev. 51, 381–9.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
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, 8796.CrossRefGoogle ScholarPubMed
Memili, E., Dominko, T. & First, N.L. (1998). Transcriptional activity of bovine oocytes and embryos. Theriogenology 49, 274 (abstract).CrossRefGoogle Scholar
Motlik, J. & Kubelka, M. (1990). Cell-cycle aspects of growth and maturation of mammalian oocytes. Mol. Reprod. Dev. 27, 366–75.CrossRefGoogle ScholarPubMed
Neglia, G., Gasparrini, B., di Brienza, V.C., Di Palo, R., Campanile, G., Presicce, G.A. & Zicarelli, L. (2003). Bovine and buffalo in vitro embryo production using oocytes derived from abattoir ovaries or collected by transvaginal follicle aspiration. Theriogenology 59, 1123–30.CrossRefGoogle ScholarPubMed
Niemann, H. & Wrenzycki, C. (2000). Alterations of expression of developmentally important genes in pre-implantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology 53, 2134.CrossRefGoogle Scholar
Niemann, H., Wrenzycki, C., Lucas-Hahn, A., Brambrink, T., Kues, W.A. & Carnwath, J.W. (2002). Gene expression patterns in bovine in vitro-produced and nuclear transfer-derived embryos and their implications for early development. Clon. Stem Cells 4, 2938.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
Pavlok, A., Kopecny, V., Lucas-Hahn, A. & Niemann, H. (1993). Transcriptional activity and nuclear ultrastructure of 8-cell bovine embryos developed by in vitro maturation and fertilization of oocytes from different growth categories of antral follicles. Mol. Reprod. Dev. 35, 233–43.CrossRefGoogle ScholarPubMed
Pierce, G.B., Lewellyn, A.L. & Parchment, R.E. (1989). Mechanism of programmed cell death in the blastocyst. Proc. Natl. Acad. Sci. USA 86, 3654–8.CrossRefGoogle ScholarPubMed
Ponsuksili, S., Wimmers, K., Adjaye, J. & Schellander, K. (2002). A source of expression profile in single pre-implantation bovine embryos. Theriogenology 57, 1611–24.CrossRefGoogle Scholar
Reik, W., Santos, F. & Dean, W. (2003). Mammalian epigenomics: reprogramming the genome for development and therapy. Theriogenology 59, 2132.CrossRefGoogle ScholarPubMed
Rief, S., Sinowatz, F., Stojkovic, M., Einspanier, R., Wolf, E. & Prelle, K. (2002). Effects of co-culture system on development, metabolism and gene expression of bovine embryos produced in vitro. Reproduction 124, 543–56.CrossRefGoogle ScholarPubMed
Rizos, D., Lonergan, P., Boland, M.P., Arroyo-Garcia, R., Pintado, B., de la Fuente, J. & Gutierrez-Adan, A. (2002). Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality Biol. Reprod. 66, 589–95.CrossRefGoogle ScholarPubMed
Rizos, D., Gutierrez-Adan, A., Perez-Garnelo, S., de la Fuente, J., Boland, M.P. & Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum : implications for blastocyst development, cryotolerance and messenger RNA expression. Biol. Reprod. 68, 236–43.CrossRefGoogle ScholarPubMed
Rizos, D., Gutierrez-Adan, A., Moreira, P., O'Meara, C., Fair, T., Evans, A.C.O., Boland, M.P. & Lonergan, P. (2004). Species-related differences in blastocyst quality are associated with differences in relative mRNA transcription. Mol. Reprod. Dev. 69, 381–6.CrossRefGoogle ScholarPubMed
Sirard, M.A. & Blondin, P. (1996). Oocyte maturation and IVF in cattle. Anim. Reprod. Sci. 42, 417–26.CrossRefGoogle Scholar
Stice, S.L. & Rzucidlo, S.J. (2001). Increasing cloning efficiencies requires a better understanding of developmental abnormalities and gene expression in manipulated embryos. J. Anim. Sci. 79, E285E289.CrossRefGoogle Scholar
Surani, M.A. (1998). Imprinting and the initiation of gene silencing in the germ cell. Cell 93, 309–12.CrossRefGoogle Scholar
Tadros, W., Houston, S.A., Bashirullah, A., Cooperstock, R.L., Semotok, J.L., Reed, B.H. & Lipshitz, H.D. (2003). Regulation of maternal transcript destabilization during egg activation in Drosophila. Genetics 164, 9891001.Google 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, 90100.CrossRefGoogle ScholarPubMed
Tesfaye, D., Ponsuksili, S., Wimmers, K., Gilles, M. & Schellander, K. (2004). A comparative expression analysis of gene transcripts in post-fertilization developmental stages of bovine embryos produced in vitro or in vivo. Reprod. Dom. Anim. 39, 396404.CrossRefGoogle ScholarPubMed
Van Soom, A., Boerjan, M.L., Bols, P.E.J., Vanroose, G., Lein, A., Coryn, M. and de Kruif, A. (1997a). Timing of compaction and inner cell allocation in bovine embryos produced in vivo after superovulation. Biol. Reprod. 57, 1041–9.CrossRefGoogle ScholarPubMed
Van Soom, A., Ysebaert, M.T. & de Kruif, A. (1997b). Relationship between timing of development, morula morphology and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol. Reprod. Dev. 47, 4756.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Viuff, D., Avery, B., Greve, T., King, W.A. & Hyttel, P. (1996). Transcriptional activity in in vitro-produced bovine two- and four-cell embryos. Mol. Reprod. Dev. 43, 171–9.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Viuff, D., Hendriksen, P.J.M., Vos, P.L.a.m., Dieleman, S.J., Bibby, B.M., Greve, T., Hyttel, P. & Thomsen, P.D. (2001). Chromosomal abnormalities and developmental kinetics in in vivo-developed cattle embryos at days 2 to 5 after ovulation. Biol. Reprod. 65, 204–8.CrossRefGoogle ScholarPubMed
Watson, A.J. (1992). The cell biology of blastocyst development. Mol. Reprod. Dev. 33, 492504.CrossRefGoogle ScholarPubMed
Watson, A.J., Westhusin, M.E., De Sousa, P.A., Betts, D.H. & Barcroft, L.C. (1999). Gene expression regulating blastocyst formation. Theriogenology 51, 117–33.CrossRefGoogle ScholarPubMed
Watson, A.J., De Sousa, P., Caveney, A., Barcroft, L.C., Natale, D., Urquhart, J. & Westhusin, M.E. (2000). Impact of bovine oocyte maturation media on oocyte transcript levels, blastocyst development, cell number and apoptosis. Biol. Reprod. 62, 355–64.CrossRefGoogle ScholarPubMed
Watson, A.J., Natale, D.R. & Barcroft, L.C. (2004). Molecular regulation of blastocyst formation. Anim. Reprod. Sci. 82–83, 583592.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D., Carnwath, J.W. & Niemann, H. (1996). Expression of the gap junction gene connexin43 (Cx43) in pre-implantation bovine embryos derived in vitro or in vivo. J. Reprod. Fertil. 108, 1724.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D., Lemme, E., Eckert, J., Carnwath, J.W. & Niemann, H. (1997). Expression of developmentally important genes in pre-implantation bovine embryos generated in vitro. Theriogenology 47, 220 (abstract).CrossRefGoogle Scholar
Wrenzycki, C., Herrmann, D., Carnwath, J.W. & Niemann, H. (1999). Alterations in the relative abundance of gene transcripts in pre-implantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol. Reprod. Dev. 53, 818.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D., Korsawe, K., Hadeler, K-G. & Niemann, H. (2000). Relative abundance of specific mRNAS in bovine embryos produced in vivo or in vitro employing two different culture systems. Theriogenology 53, 415 (abstract).Google Scholar
Wrenzycki, C., Herrmann, D., Keskintepe, L., Martins, A.Jr., Sirisathien, S., Brackett, B. & Niemann, H. (2001). Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos. Hum. Reprod. 16, 893901.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Lucas-Hahn, A., Herrmann, D., Lemme, E., Korsawe, K. & Niemann, H. (2002). In vitro production and nuclear transfer affect dosage compensation of the X-linked gene transcripts G6PD, PGK and Xist in pre-implantation bovine embryos. Biol. Reprod. 66, 127–34.CrossRefGoogle Scholar
Wrenzycki, C., Herrmann, D. & Niemann, H. (2003). Timing of blastocyst expansion affects spatial messenger RNA expression patterns of genes in bovine blastocysts produced in vitro. Biol. Reprod. 68, 2073–80.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Herrmann, D., Lucas-Hahn, A., Lemme, E., Korsawe, K. & Niemann, H. (2004). Gene expression patterns in in vitro-produced and somatic nuclear transfer-derived pre-implantation bovine embryos: relationship to the large offspring syndrome. Anim. Reprod. Sci. 82–83, 593603.CrossRefGoogle Scholar
Yang, J., Liu, X. & Bhalla, K. (1997). Prevention of apoptosis by bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129–36.CrossRefGoogle ScholarPubMed
Yang, M.Y. & Rajamahendran, R. (1999). Involvement of apoptosis in bovine blastocysts produced in vitro. Theriogenology 51, 336 (abstract).CrossRefGoogle Scholar
Yang, M.Y. & Rajamahendran, R. (2002). Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim. Reprod. Sci. 70, 159–69.CrossRefGoogle ScholarPubMed
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 pre-implantation bovine embryos derived from different in vitro systems. Reproduction 122, 601–10.CrossRefGoogle Scholar
Young, L.E. & Fairburn, H.R. (2000). Improving the safety of embryo technologies: possible role of genomic imprinting. Theriogenology 53, 627–48.CrossRefGoogle ScholarPubMed
Young, L.E., Sinclair, K.D. & Wilmut, I. (1998). Large offspring syndrome in cattle and sheep. Rev. of Reprod. 3, 155–63.CrossRefGoogle ScholarPubMed
Zhang, D.Y., Lee, J. & Moor, R.M. (1998). Molecules involved in metaphase I to metaphase II transition in mammalian oocytes. Proceeding of Serono Symposium (Gametes: development and function), 50th International Congress on Animal Reproduction (ICAR), Rome, Italy.Google Scholar