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Analysis of transcription factor expression during oogenesis and preimplantation development in mice

Published online by Cambridge University Press:  01 May 2007

S. Kageyama
Affiliation:
Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8562, Japan.
W. Gunji
Affiliation:
Department of Biological Science and Technology, Faculty of Industrial Science and Technology, Tokyo University of Science, Chiba 278-8510, Japan.
M. Nakasato
Affiliation:
Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8562, Japan.
Y. Murakami
Affiliation:
Department of Biological Science and Technology, Faculty of Industrial Science and Technology, Tokyo University of Science, Chiba 278-8510, Japan.
M. Nagata
Affiliation:
Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8562, Japan.
F. Aoki*
Affiliation:
Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8562, Japan.
*
All correspondence to: Fugaku Aoki, Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Shinryoiki-Seimei Building 302, Kashiwa-no-ha 5–1-5, Kashiwa, Chiba 277-8562, Japan. Tel: +81 4-7136 5424. Fax: +81 4-7136 3698. e-mail: aokif@k.u-tokyo.ac.jp

Summary

The transition from a differentiated germ cell into a totipotent zygote during oogenesis and preimplantation development is critical to the creation of a new organism. During this period, cell characteristics change dynamically, suggesting that a global alteration of gene expression patterns occurs, which is regulated by global changes in various epigenetic factors. Among these, transcription factors (TFs) are essential in the direct regulation of transcription and also play important roles in determining cell characteristics. However, no comprehensive analysis of TFs from germ cells to embryos had been undertaken. We used mRNA amplification systems and microarrays to conduct a genomewide analysis of TFs at various stages of oogenesis and preimplantation development. The greatest alteration in TFs occurred between the 1- and 2-cell stages, at which time zygotic genome activation (ZGA) occurs. Our analysis of TFs classified by structure and function revealed several specific patterns of change. Basic transcription factors, which are the general components of transcription, increased transiently at the 2-cell stage, while homeodomain (HD) TFs were expressed specifically in the oocyte. TFs containing the Rel homology region (RHR) and Ets domains were expressed at a high level in 2-cell and blastocyst embryos. Thus, the global TF dynamics that occur during oogenesis and preimplantation development seem to regulate the transition from germ-cell-type to embryo-type gene expression.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2007

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References

Algul, H., Tando, Y., Schneider, G., Weidenbach, H., Adler, G. & Schmid, R.M. (2002). Acute experimental pancreatitis and NF-kappaB/Rel activation. Pancreatology 2, 503–9.CrossRefGoogle ScholarPubMed
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
Alonso, C.R. (2002). Hox proteins: sculpting body parts by activating localized cell death. Curr. Biol. 12, R7768.CrossRefGoogle ScholarPubMed
Aoki, F., Worrad, D.M. & Schultz, R.M. (1997). Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 181, 296307.CrossRefGoogle ScholarPubMed
Block, K.L., Shou, Y. & Poncz, M. (1996a). An Ets/Sp1 interaction in the 5′-flanking region of the megakaryocyte-specific alpha IIb gene appears to stabilize Sp1 binding and is essential for expression of this TATA-less gene. Blood 88, 2071–80.CrossRefGoogle ScholarPubMed
Block, K.L., Shou, Y., Thorton, M. & Poncz, M. (1996b). The regulated expression of a TATA-less, platelet-specific gene, alphaIIb. Stem Cells 14, 3847.CrossRefGoogle ScholarPubMed
Brand-Saberi, B. (2005). Genetic and epigenetic control of skeletal muscle development. Ann. Anat. 187, 199207.CrossRefGoogle ScholarPubMed
Choi, T., Aoki, F., Mori, M., Yamashita, M., Nagahama, Y. & Kohmoto, K. (1991). Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113, 789–95.CrossRefGoogle ScholarPubMed
Das, P.M. & Singal, R. (2004). DNA methylation and cancer. J. Clin. Oncol. 22, 4632–42.CrossRefGoogle ScholarPubMed
Davis, W., Jr., De Sousa, P.A. & Schultz, R.M. (1996). Transient expression of translation initiation factor eIF-4C during the 2-cell stage of the preimplantation mouse embryo: identification by mRNA differential display and the role of DNA replication in zygotic gene activation. Dev. Biol. 174, 190201.CrossRefGoogle ScholarPubMed
De Pamphilis, M.L. (1993). Origins of DNA replication in metazoan chromosomes. J. Biol. Chem. 268, 14.CrossRefGoogle ScholarPubMed
Doherty, A.S., Bartolomei, M.S. & Schultz, R.M. (2002). Regulation of stage-specific nuclear translocation of Dnmt10 during preimplantation mouse development. Dev. Biol. 242, 255–66.CrossRefGoogle ScholarPubMed
Ehrlich, M. (2002). DNA methylation in cancer: too much, but also too little. Oncogene 21, 5400–13.CrossRefGoogle ScholarPubMed
FitzGerald, P.C., Shlyakhtenko, A., Mir, A.A. & Vinson, C. (2004). Clustering of DNA sequences in human promoters. Genome Res. 14, 1562–74.CrossRefGoogle ScholarPubMed
Fuchimoto, D., Mizukoshi, A., Schultz, R.M., Sakai, S. & Aoki, F. (2001). Posttranscriptional regulation of cyclin A1 and cyclin A2 during mouse oocyte meiotic maturation and preimplantation development. Biol. Reprod. 65, 986–93.CrossRefGoogle ScholarPubMed
Gehring, W.J. (1992). The homeobox in perspective. Trends Biochem. Sci. 17, 277–80.CrossRefGoogle Scholar
Gunji, W., Kai, T., Sameshima, E., Iizuka, N., Katagi, H., Utsugi, T., Fujimori, F. & Murakami, Y. (2004). Global analysis of the expression patterns of transcriptional regulatory factors in formation of embryoid bodies using sensitive oligonucleotide microarray systems. Biochem Biophys. Res. Commun. 325, 265–75.CrossRefGoogle ScholarPubMed
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
Howell, C.Y., Bestor, T.H., Ding, F., Latham, K.E., Mertineit, C., Trasler, J.M. & Chaillet, J.R. (2001). Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104, 829–38.CrossRefGoogle ScholarPubMed
Howlett, S.K. & Reik, W. (1991). Methylation levels of maternal and paternal genomes during preimplantation development. Development 113, 119–27.CrossRefGoogle ScholarPubMed
Iwamori, N., Naito, K., Sugiura, K. & Tojo, H. (2002). Preimplantation-embryo-specific cell cycle regulation is attributed to the low expression level of retinoblastoma protein. FEBS Lett. 526, 119–23.CrossRefGoogle Scholar
Johnson, J., Canning, J., Kaneko, T., Pru, J.K. & Tilly, J.L. (2004). Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428, 145–50.CrossRefGoogle ScholarPubMed
Kabrun, N. & Enrietto, P.J. (1994). The Rel family of proteins in oncogenesis and differentiation. Semin. Cancer Biol. 5, 103–12.Google ScholarPubMed
Kafri, T., Ariel, M., Brandeis, M., Shemer, R., Urven, L., McCarrey, J., Cedar, H. & Razin, A. (1992). Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev. 5, 705–14.CrossRefGoogle Scholar
Kageyama, R., Ohtsuka, T., Hatakeyama, J. & Ohsawa, R. (2005). Roles of bHLH genes in neural stem cell differentiation. Exp. Cell Res. 306, 343–8.CrossRefGoogle ScholarPubMed
Kageyama, S.I., Nagata, M. & Aoki, F. (2004). Isolation of nascent messenger RNA from mouse preimplantation embryos. Biol. Reprod. 30, 1948–55.CrossRefGoogle Scholar
Kaneko, K.J., Cullinan, E.B., Latham, K.E. & DePamphilis, M.L. (1997). Transcription factor mTEAD-2 is selectively expressed at the beginning of zygotic gene expression in the mouse. Development 124, 1963–73.CrossRefGoogle ScholarPubMed
Kotaja, N., De Cesare, D., Macho, B., Monaco, L., Brancorsini, S., Goossens, E., Tournaye, H., Gansmuller, A. & Sassone-Corsi, P. (2004). Abnormal sperm in mice with targeted deletion of the act (activator of cAMP-responsive element modulator in testis) gene. Proc. Natl. Acad. Sci. USA 101, 10620–5.CrossRefGoogle ScholarPubMed
Krausz, C. & Sassone-Corsi, P. (2005). Genetic control of spermiogenesis: insights from the CREM gene and implications for human infertility. Reprod. Biomed. Online 10, 6471.CrossRefGoogle ScholarPubMed
La Salle, S., Mertineit, C., Taketo, T., Moens, P.B., Bestor, T.H. & Trasler, J.M. (2004). Windows for sex-specific methylation marked by DNA methyltransferase expression profiles in mouse germ cells. Dev. Biol. 268, 403–15.CrossRefGoogle ScholarPubMed
Majumder, S., Miranda, M. & DePamphilis, M.L. (1993). Analysis of gene expression in mouse preimplantation embryos demonstrates that the primary role of enhancers is to relieve repression of promoters. EMBO J. 12, 1131–40.CrossRefGoogle ScholarPubMed
Monk, M., Boubelik, M. & Lehnert, S. (1987). Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99, 371–82.CrossRefGoogle ScholarPubMed
Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Scholer, H. & Smith, A. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379–91.CrossRefGoogle ScholarPubMed
Nothias, J.Y., Majumder, S., Kaneko, K.J. & DePamphilis, M.L. (1995). Regulation of gene expression at the beginning of mammalian development. J. Biol. Chem. 270, 22077–80.CrossRefGoogle ScholarPubMed
Oh, B., Hwang, S., McLaughlin, J., Solter, D. & Knowles, B.B. (2000). Timely translation during the mouse oocyte-to-embryo transition. Development 127, 3795–803.CrossRefGoogle ScholarPubMed
Oikawa, T. (2004). ETS transcription factors: possible targets for cancer therapy. Cancer Sci. 95, 626–33.CrossRefGoogle ScholarPubMed
Oikawa, T. & Yamada, T. (2003). Molecular biology of the Ets family of transcription factors. Gene 303, 1134.CrossRefGoogle ScholarPubMed
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, 493506.CrossRefGoogle ScholarPubMed
Rajkovic, A., Pangas, S.A., Ballow, D., Suzumori, N. & Matzuk, M.M. (2004). NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305, 1157–9.CrossRefGoogle ScholarPubMed
Reeves, R. (2000). Structure and function of the HMGI(Y) family of architectural transcription factors. Environ. Health Perspect. 108, 803–9.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
Santos, F., Hendrich, B., Reik, W. & Dean, W. (2002). Dynamic reprogramming of DNA methylation in the early mouse embryos. Dev. Biol. 241, 172–82.CrossRefGoogle Scholar
Santos, F., Zakhartchenko, V., Stojkovic, M., Peters, A., Jenuwein, T., Wolf, E., Reik, W. & Dean, W. (2003). Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr. Biol. 13, 1116–21.CrossRefGoogle ScholarPubMed
Schultz, R.M. (1993). Regulation of zygotic gene activation in the mouse. Bioessays 15, 531–8.CrossRefGoogle ScholarPubMed
Scott, M.P., Tamkun, J.W. & HartzellG.W., 3rd. G.W., 3rd. (1989). The structure and function of the homeodomain. Biochim. Biophys. Acta 989, 2548.Google ScholarPubMed
Soyal, S.M., Amleh, A. & Dean, J. (2000). FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development 127, 4645–54.CrossRefGoogle ScholarPubMed
Szyf, M., Pakneshan, P. & Rabbani, S.A. (2004). DNA methylation and breast cancer. Biochem. Pharmacol. 68, 1187–97.CrossRefGoogle ScholarPubMed
Tanaka, T.S., Kunath, T., Kimber, W.L., Jaradat, S.A., Stagg, C.A., Usuda, M., Yokota, T., Niwa, H., Rossant, J. & Ko, M.S. (2002). Gene expression profiling of embryo-derived stem cells reveals candidate genes associated with pluripotency and lineage specificity. Genome Res. 12, 1921–8.CrossRefGoogle ScholarPubMed
Telford, N.A., Hogan, A., Franz, C.R. & Schultz, G.A. (1990). Expression of genes for insulin and insulin-like growth factors and receptors in early postimplantation mouse embryos and embryonal carcinoma cells. Mol. Reprod. Dev. 27, 8192.CrossRefGoogle ScholarPubMed
Wang, Q. & Latham, K.E. (2000). Translation of maternal messenger ribonucleic acids encoding transcription factors during genome activation in early mouse embryos. Biol Reprod 62, 969–78.CrossRefGoogle ScholarPubMed
Wang, Q.T., Piotrowska, K., Ciemerych, M.A., Milenkovic, L., Scott, M.P., Davis, R.W. & Zernicka-Goetz, M. (2004). A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev. Cell 6, 133–44.CrossRefGoogle ScholarPubMed
Wasylyk, B., Hahn, S.L. & Giovane, A. (1993). The Ets family of transcription factors. Eur. J. Biochem. 211, 718.CrossRefGoogle ScholarPubMed
Whitten, W.K. (1971). Nutrient requirement for the culture of preimplantation embryos. Adv. Biosci. 6, 129139.Google Scholar
Worrad, D.M., Ram, P.T. & Schultz, R.M. (1994). Regulation of gene expression in the mouse oocyte and early preimplantation embryo: developmental changes in Sp1 and TATA box-binding protein, TBP. Development 120, 2347–57.CrossRefGoogle ScholarPubMed
Woychik, N.A. & Hampsey, M. (2002). The RNA polymerase II machinery: structure illuminates function. Cell 108, 453–63.CrossRefGoogle ScholarPubMed
Yu, S.H., Chiang, W.C., Shih, H.M. & Wu, K.J. (2004). Stimulation of c-Rel transcriptional activity by PKA catalytic subunit beta. J. Mol. Med. 9, 9.Google Scholar
Zeng, F., Baldwin, D.A. & Schultz, R.M. (2004). Transcript profiling during preimplantation mouse development. Dev. Biol. 272, 483–96.CrossRefGoogle ScholarPubMed
Zhou, M. & Ouyang, W. (2003). The function role of GATA-3 in Th1 and Th2 differentiation. Immunol. Res. 28, 2537.CrossRefGoogle ScholarPubMed