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Chromatin dynamics in Triturus cristatus oogenesis: an epigenetic approach

Published online by Cambridge University Press:  01 November 2008

Liliana Burlibaşa ,
Otilia Zărnescu ,
Natalia Cucu  and
Lucian Gavrilă
Liliana Burlibaşa*
Affiliation:
University of Bucharest, Faculty of Biology, Genetics Department, No. 1–3 Aleea Portocalilor, Sector 6, 060101, Bucharest, Romania. Institute of Genetics, Faculty of Biology, University of Bucharest, No. 1–3 Aleea Portocalilor, Sector 6, 060101, Bucharest, Romania.
Otilia Zărnescu
Affiliation:
Developmental Biology Department, University of Bucharest, Faculty of Biology, No. 91–95 Splaiul Independenţei, Sector 5, 050095, Bucharest, Romania
Natalia Cucu
Affiliation:
Institute of Genetics, Faculty of Biology, University of Bucharest, No. 1–3 Aleea Portocalilor, Sector 6, 060101, Bucharest, Romania.
Lucian Gavrilă
Affiliation:
Institute of Genetics, Faculty of Biology, University of Bucharest, No. 1–3 Aleea Portocalilor, Sector 6, 060101, Bucharest, Romania.
*
All correspondence to Liliana Burlibasa. University of Bucharest, Faculty of Biology, Genetics Department, No. 1–3 Aleea Portocalilor, Sector 6, 060101, Bucharest, Romania. Tel:/Fax: +40213181565. e-mail: [email protected]
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Summary

Oogenesis is a critical event in the formation of female gametes, whose role in development is to transfer genomic information to the next generation. During this process, the gene expression pattern changes dramatically concomitant with genome remodelling, while genomic information is stably maintained. The aim of the present study was to investigate the chromatin architecture in newt oocytes. Using fluorescence microscopy, as well as transmission electron microscopy (TEM), immunohistochemical method and RE-ChIP assay, some peculiar aspects of chromatin and chromosome organization and evolution in crested newt oogenesis were investigated. We focussed our investigations on detection of certain epigenetic modifications (H4 hyperacetylation, H2A ubiquitinylation and cytosine methylation) at the rRNA gene (18S–5.8S–28S) promoter region. Our findings suggest that there is an involvement of some epigenetic modifications as well as of linker histone variants in chromatin architecture dynamics during crested newt oogenesis.

Keywords

Chromatin remodellingEpigenetic modificationsLinker histonesOogenesisrRNA gene promoter
Type
Research Article
Information
Zygote , Volume 16 , Issue 4 , November 2008 , pp. 315 - 326
Copyright
Copyright © Cambridge University Press 2008

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References

Agalioti, T., Chen, G. & Thanos, D. (2002). Deciphering the transcriptional histone acetylation code for a human gene. Cell 111, 381–92.CrossRefGoogle ScholarPubMed
Allfrey, V., Faulkner, R.M. & Mirsky, A.E. (1964). Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl. Acad. Sci. USA 51, 786–94.CrossRefGoogle ScholarPubMed
Ausio, J. (1992). Structure and dynamics of transcriptionally active chromatin J. Cell. Sci. 102, 1–5.CrossRefGoogle ScholarPubMed
Ausio, J. & van Holde, K.E. (1986). Histone hyperacetylation: its effect on nucleosome conformation and stability. Biochemistry 25, 1421–8.CrossRefGoogle ScholarPubMed
Ayer, D.E. (1999). Histone deacetylases, transcriptional repression with SINers and NuRDs. Trends Cell Biol. 9, 193–8.CrossRefGoogle ScholarPubMed
Baarends, W.M., Hoogerbrugge, J.W., Roest, H.P., Jan Vreeburg, M.O., Hoeijnakers, H.J. & Grootegoed, J.A. (1999). Histone ubiquitination and chromatin remodelling in mouse spermatogenesis. Dev. Biol. 207, 322–33.CrossRefGoogle Scholar
Barsacchi, G., Bussoti, L. & Mancino, G. (1970). The maps of the lampbrush chromosomes of Triturus (Amphibia, Urodela). IV Triturus vulgaris meridionalis. Chromosoma 31, 255–78.CrossRefGoogle ScholarPubMed
Bird, A.P. (1996). The relationship of DNA methylation to cancer. Cancer Surv. 28, 87–101.Google ScholarPubMed
Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6–21.CrossRefGoogle ScholarPubMed
Bird, A. & Wolffe, A.P. (1999). Methylation-induced repression—belts, braces and chromatin. Cell 99, 451–4.CrossRefGoogle ScholarPubMed
Brown, D. & Dawid, J.B. (1970). Specific gene amplification in oocyte. Science 160, 272.CrossRefGoogle Scholar
Brown, D.T., Gunjan, A., Alexander, B.T. & Sittman, D.B. (1997). Differential effect of H1 variant overproduction on gene expression is due to differences in the central globular domain. Nucl. Acids Res. 15, 5003–9.CrossRefGoogle Scholar
Burlibasa, L. & Gavrila, L. (2005). Molecular and ultrastructural studies of the sperm chromatin from Triturus cristatus. Zygote 13, 197–205.CrossRefGoogle ScholarPubMed
Carruthers, L.M., Bednary, J., Woodcock, C.L. & Hansen, J.C. (1998). Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays, mechanistic ramifications for higher-order chromatin folding. Biochemistry 37, 14776–87.CrossRefGoogle ScholarPubMed
Conconi, A., Widmer, R.M., Koller, T. & Sojo, Y.M. (1989). Two different chromatin structure coexist in ribosomal RNA genes throughout the cell cycle. Cell 57, 753–61.CrossRefGoogle ScholarPubMed
Garcia-Ramirez, M., Rocchini, C. & Ausio, J. (1995). Modulation of chromatin folding by histone acetylation. J. Biol. Chem. 270, 17920–8.CrossRefGoogle ScholarPubMed
Grant, A.P. (2001). A tale of histone modifications. Genome Biol. 2 (4), 0003.1–6.CrossRefGoogle ScholarPubMed
Grummt, I. & Pikaard, C.S. (2003). Epigenetic silencing of RNA polymerase I transcription. Nat. Rev. Mol. Cell. Biol. 4, 641–9.CrossRefGoogle ScholarPubMed
Grunstein, M. (1990). Histone function in transcription. Ann. Rev. Cell. Biol. 6, 643–78.CrossRefGoogle ScholarPubMed
Gunjan, A. & Brown, D.T. (1999). Overproduction of histone H1 variants in vivo increases basal and induced activity of the mouse mammary tumor virus promoter. Nucleic Acids Res. 27, 3355–63.CrossRefGoogle ScholarPubMed
Gunjan, A., Sittman, D. & Brown, D. (2001). Core histone acetylation is regulated by linker histone stoichiometry in vivo. J. Biol. Chem. 276 (5), 3635–40.CrossRefGoogle ScholarPubMed
Jaenish, R. & Bird, A. (2003). Epigenetic regulation of gene expression, how the genome integrates intrinsic and environmental signals. Nat. Genet. 33, 245–54.CrossRefGoogle Scholar
Jasencakova, Z., Meister, A., Walter, J., Turner, B.M. & Schubert, I. (2000). Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Plant Cell 12, 2087–100.CrossRefGoogle ScholarPubMed
Jenuwein, T. & Allis, C D. (2001). Translating the histone code. Science 293, 1074–80.CrossRefGoogle ScholarPubMed
Jones, P.A. & Baylin, S.B. (2002). The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3, 415–28.CrossRefGoogle ScholarPubMed
Juan, L.J., Utley, R.T., Adams, C.C., Vetesse-Dadey, M. & Workman, J.L. (1994). Differential repression of transcription factor binding by histone H1 is regulated by the core histone amino termini. EMBO J. 13, 6031–40.CrossRefGoogle ScholarPubMed
Kandolf, H. (1994). The H1A histone variant is an in vivo repressor of oocyte-type 5S gene transcription in Xenopus laevis embryos. Proc. Natl. Acad. Sci. USA 91, 7257–61.CrossRefGoogle Scholar
Kaplan, L.J., Bauer, R., Morrison, E., Langan, T.A. & Fosman, G.D. (1984). The structure of chromatin reconstituted with phosphorylated H1. Circular dichroism and thermal denaturation studies. J. Biol. Chem. 259, 8777–85.CrossRefGoogle ScholarPubMed
Karpen, G.H., Schaefer, J.E. & Laird, C.D. (1998). A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation. Genes Dev. 2, 1745–63.CrossRefGoogle Scholar
Kim, J.M., Liu, H., Tazaki, M., Nagata, M. & Aoki, F. (2003). Changes in histone acetylation during mouse oocyte meiosis. J. Cell Biol. 162 (1), 37–46.CrossRefGoogle ScholarPubMed
Kuo, M.H., Zhou, J., Jambeck, P., Churchill, M.E. & Allis, C.D. (1998). Histone acetyltransferase activity of yeast Gcn5p is required for the activation of target genes in vivo. Genes Dev. 12, 627–39.CrossRefGoogle ScholarPubMed
Lawrence, R.J., Early, K., Pontes, O., Silva, M., Chen, Z.J., Neves, N., Viegas, W. & Pikaard, C.S. (2004). A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol. Cells 13, 599–609.CrossRefGoogle ScholarPubMed
Long, E.O. & Dawid, I.B. (1980). Repeated genes in eukaryotes. Ann. Rev. Biochem. 4, 727–64.CrossRefGoogle Scholar
Lusser, A. (2002). Acetylated, methylated, remodelled, chromatin states for gene regulation. Curr. Opin. Plant. Biol. 5, 437–43.CrossRefGoogle ScholarPubMed
Macgregor, H.C. (1993). An Introduction to Animal Cytogenetics. London: Chapman & Hall.Google Scholar
Macleod, D. & Bird, A. (1983). Transcription in oocytes of highly methylated rDNA from Xenopus laevis sperm. Nature 306, 200–3.CrossRefGoogle ScholarPubMed
Magnaghi-Jaulin, L. & Jaulin, C. (2006). Histone deacetylase activity is necessary for chromosome condensation during meiotic maturation in Xenopus laevis. Chromosome Res. 14, 319–32.CrossRefGoogle ScholarPubMed
McStay, B. (2006). Nucleolar dominance, a model for rRNA gene silencing. Genes Dev. 20, 1207–14.CrossRefGoogle Scholar
Nan, X., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N. & Bird, A. (1998). Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386–9.CrossRefGoogle ScholarPubMed
Peng, J.C. & Karpen, G.H. (2007). H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nat. Cell. Biol. 9 (1), 25–35.CrossRefGoogle ScholarPubMed
Pennock, D.G. & Reeder, R.H. (1984). In vitro methylation of HpaII sites in Xenopus laevis rDNA does not affect its transcription in oocytes. Nucleic Acids Res. 12, 2225–32.CrossRefGoogle Scholar
Polach, K.J. & Widom, J. (1999). Restriction enzymes as probes of nucleosome stability, Methods Enzymol. 304, 278–98.CrossRefGoogle ScholarPubMed
Reeder, R.H. (1985). Mechanisms of nucleolar dominance in animals and plants. J. Cell Biol. 101, 2013–6.CrossRefGoogle ScholarPubMed
Santoro, R. (2005). The silence of the ribosomal RNA genes. Cell Mol. Life Sci. 62, 2067–79.CrossRefGoogle ScholarPubMed
Santoro, R. & Grummt, I. (2005). Epigenetic mechanism of rRNA gene silencing, temporal order of NoRC-mediated histone modification, chromatin remodelling and DNA methylation. Mol. Cell. Biol. 25, 2539–46.CrossRefGoogle ScholarPubMed
Santoro, R., Li, J. & Grummt, I. (2002). The nucleolar remodelling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat. Gen. 32, 393–6.CrossRefGoogle ScholarPubMed
Shaw, P.J., Highett, M.I., Beven, A.F. & Jordan, E.G. (1995). The nucleolar architecture of polymerase I transcription and processing. EMBO J. 14, 2896–906.CrossRefGoogle ScholarPubMed
Shen, W. & Gorovsky, M.A. (1996). Linker histone H1 regulates specific gene expression but not global transcription in vivo. Cell 86 (3), 475–83.CrossRefGoogle Scholar
Shertakova, E., Bandu, M.T., Doly, J. & Bonnefoy, E. (2001). Inhibition of histone induces constitutive depression of the b interferon promoter and confers antiviral activity. J. Virol. 75, 3444–52.CrossRefGoogle Scholar
Sommerville, J., Baird, J. & Turner, B. (1993). Histone H4 acetylation and transcription in amphibian chromatin. J. Cell Biol. 120 (2), 277–90.CrossRefGoogle ScholarPubMed
Steopoe, I., Gavrilă, L., Mihăescu, Gr & Comşa, D. (1985). The study of the lampbrush chromosomes in relation with the ribosomal gene amplification in oocytes of Triturus cristatus and Salamandra salamandra. Annals of Buch. Univ. XXXIV, 3–9.Google Scholar
Strahl, B.D. & Allis, C.D. (2000). The language of covalent histone modifications. Nature 403, 41–5.CrossRefGoogle ScholarPubMed
Turner, B.M. (1991). Histone acetylation and control of gene expression. J. Cell. Sci. 99, 13–20.CrossRefGoogle ScholarPubMed
Turner, B.M. (1993). Decoding the nucleosome. Cell 75, 5–8.CrossRefGoogle ScholarPubMed
Ura, K., Hayes, J.J. & Wolffe, A.P. (1995). A positive role for nucleosome mobility in the transcriptional activity of chromatin templates, restriction by linker histones. EMBO J. 14, 3752–65.CrossRefGoogle ScholarPubMed
Utley, R.T., Ikeda, K., Grant, P.A., Cote, J., Steger, D.J., Eberharter, A., John, S. & Workman, J.L. (1998). Transcriptional activators direct histone acetyltransferase complexes to nucleosomes. Nature 394, 498–502.CrossRefGoogle ScholarPubMed
Wang, L., Liu, L. & Berger, S.L. (1998). Critical residues for histone acetylation by Gcn5, functioning in Ada and SAGA complexes, are also required for transcriptional function in vivo. Genes Dev. 12, 640–53.CrossRefGoogle ScholarPubMed
Wolffe, A.P. (1992). Chromatin, Structure and Function. London: Academic Press.Google Scholar
Workman, J.L. (2006). Nucleosome displacement in transcription, Genes Dev. 20, 2009–17.CrossRefGoogle ScholarPubMed
Zărnescu, O. (2007). Immunohistochemical distribution of hyperacetylated histone H4 in testis of paddlefish Polyodon spathula, ultrastructural correlation with chromatin condensation. Cell Tissue Res. DOI 10.1007/s00441-006-0373-3.CrossRefGoogle Scholar
Zhao, J., Herrera-Diaz, J. & Gross, D.S. (2005). Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density. Mol. Cell. Biol. 25, 8985–99.CrossRefGoogle Scholar
Zlatanova, J. (1990). Histone H1 and regulation of transcription of eukaryotic genes. Trends Biochem. Sci. 15, 2.CrossRefGoogle ScholarPubMed