A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis

doi:10.1083/jcb.129.3.561

Quantitative Colocalization Analysis Software

This Article

Full Text (PDF, 5256K)

Alert me when this article is cited

Citation Map

Services

Email this article

Similar articles in this journal

Similar articles in PubMed

Alert me to new content in the JCB

Download to citation manager

Citing Articles

Citing Articles via HighWire

Citing Articles via CrossRef

Citing Articles via Google Scholar

Google Scholar

Articles by Weisenberger, D.

Articles by Scheer, U.

Search for Related Content

PubMed

PubMed Citation

Articles by Weisenberger, D.

Articles by Scheer, U.

Pubmed/NCBI databases

Substance via MeSH

Social Bookmarking

What's this?

ARTICLES

A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis

D Weisenberger and U Scheer
Department of Cell and Developmental Biology, Theodor-Boveri-Institute, University of Wurzburg, Germany.

When cells enter mitosis, RNA synthesis ceases. Yet the RNA polymerase I (pol I) transcription machinery involved in the production of pre- rRNA remains bound to the nucleolus organizing region (NOR), the chromosome site harboring the tandemly repeated rRNA genes. Here we examine whether rDNA transcription units are transiently blocked or "frozen" during mitosis. By using fluorescent in situ hybridization we were unable to detect nascent pre-rRNA chains on the NORs of mouse 3T3 and rat kangaroo PtK2 cells. Appropriate controls showed that our approach was sensitive enough to visualize, at the light microscopic level, individual transcriptionally active rRNA genes both in situ after experimental unfolding of nucleoli and in chromatin spreads ("Miller spreads"). Analysis of the cell cycle-dependent redistribution of transcript-associated components also revealed that most transcripts are released from the rDNA at mitosis. Upon disintegration of the nucleolus during mitosis, U3 small nucleolar RNA (snoRNA) and the nucleolar proteins fibrillarin and nucleolin became dispersed throughout the cytoplasm and were excluded from the NORs. Together, our data rule out the presence of "frozen Christmas-trees" at the mitotic NORs but are compatible with the view that inactive pol I remains on the rDNA. We propose that expression of the rRNA genes is regulated during mitosis at the level of transcription elongation, similarly to what is known for a number of genes transcribed by pol II. Such a mechanism may explain the decondensed state of the NOR chromatin and the immediate transcriptional reactivation of the rRNA genes following mitosis.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Sanij, E., Poortinga, G., Sharkey, K., Hung, S., Holloway, T. P., Quin, J., Robb, E., Wong, L. H., Thomas, W. G., Stefanovsky, V., Moss, T., Rothblum, L., Hannan, K. M., McArthur, G. A., Pearson, R. B., Hannan, R. D. (2008). UBF levels determine the number of active ribosomal RNA genes in mammals. JCB 183: 1259-1274 [Abstract] [Full Text]
Rickards, B., Flint, S. J., Cole, M. D., LeRoy, G. (2007). Nucleolin Is Required for RNA Polymerase I Transcription In Vivo. Mol. Cell. Biol. 27: 937-948 [Abstract] [Full Text]
Romanova, L., Korobova, F., Noniashvilli, E., Dyban, A., Zatsepina, O. (2006). High Resolution Mapping of Ribosomal DNA in Early Mouse Embryos by Fluorescence In Situ Hybridization. Biol. Reprod. 74: 807-815 [Abstract] [Full Text]
Conconi, A., Paquette, M., Fahy, D., Bespalov, V. A., Smerdon, M. J. (2005). Repair-Independent Chromatin Assembly onto Active Ribosomal Genes in Yeast after UV Irradiation. Mol. Cell. Biol. 25: 9773-9783 [Abstract] [Full Text]
Gonzales, B., Henning, D., So, R. B., Dixon, J., Dixon, M. J., Valdez, B. C. (2005). The Treacher Collins syndrome (TCOF1) gene product is involved in pre-rRNA methylation. Hum Mol Genet 14: 2035-2043 [Abstract] [Full Text]
Mais, C., Wright, J. E., Prieto, J.-L., Raggett, S. L., McStay, B. (2005). UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery. Genes Dev. 19: 50-64 [Abstract] [Full Text]
Leung, A. K. L., Gerlich, D., Miller, G., Lyon, C., Lam, Y. W., Lleres, D., Daigle, N., Zomerdijk, J., Ellenberg, J., Lamond, A. I. (2004). Quantitative kinetic analysis of nucleolar breakdown and reassembly during mitosis in live human cells. JCB 166: 787-800 [Abstract] [Full Text]
Halkidou, K., Logan, I. R., Cook, S., Neal, D. E., Robson, C. N. (2004). Putative involvement of the histone acetyltransferase Tip60 in ribosomal gene transcription. Nucleic Acids Res 32: 1654-1665 [Abstract] [Full Text]
Mi, Y., Thomas, S. D., Xu, X., Casson, L. K., Miller, D. M., Bates, P. J. (2003). Apoptosis in Leukemia Cells Is Accompanied by Alterations in the Levels and Localization of Nucleolin. J. Biol. Chem. 278: 8572-8579 [Abstract] [Full Text]
Okuwaki, M., Tsujimoto, M., Nagata, K. (2002). The RNA Binding Activity of a Ribosome Biogenesis Factor, Nucleophosmin/B23, Is Modulated by Phosphorylation with a Cell Cycle-dependent Kinase and by Association with Its Subtype. Mol. Biol. Cell 13: 2016-2030 [Abstract] [Full Text]
O'Sullivan, A. C., Sullivan, G. J., McStay, B. (2002). UBF Binding In Vivo Is Not Restricted to Regulatory Sequences within the Vertebrate Ribosomal DNA Repeat. Mol. Cell. Biol. 22: 657-658 [Abstract] [Full Text]
Fair, T., Hyttel, P., Lonergan, P., Boland, M. P. (2001). Immunolocalization of Nucleolar Proteins During Bovine Oocyte Growth, Meiotic Maturation, and Fertilization. Biol. Reprod. 64: 1516-1525 [Abstract] [Full Text]
Mais, C, Scheer, U (2001). Molecular architecture of the amplified nucleoli of Xenopus oocytes. J. Cell Sci. 114: 709-718 [Abstract]
Zhai, W., Comai, L. (2000). Repression of RNA Polymerase I Transcription by the Tumor Suppressor p53. Mol. Cell. Biol. 20: 5930-5938 [Abstract] [Full Text]
Dundr, M., Misteli, T., Olson, M. O.J. (2000). The Dynamics of Postmitotic Reassembly of the Nucleolus. JCB 150: 433-446 [Abstract] [Full Text]
Spencer, C. A., Kruhlak, M. J., Jenkins, H. L., Sun, X., Bazett-Jones, D. P. (2000). Mitotic Transcription Repression in Vivo in the Absence of Nucleosomal Chromatin Condensation. JCB 150: 13-26 [Abstract] [Full Text]
Sirri, V., Roussel, P., Hernandez-Verdun, D. (2000). In Vivo Release of Mitotic Silencing of Ribosomal Gene Transcription Does Not Give Rise to Precursor Ribosomal RNA Processing. JCB 148: 259-270 [Abstract] [Full Text]
Héliot, L., Mongelard, F., Klein, C., O'Donohue, M.-F., Chassery, J.-M., Robert-Nicoud, M., Usson, Y. (2000). Nonrandom Distribution of Metaphase AgNOR Staining Patterns on Human Acrocentric Chromosomes. J. Histochem. Cytochem. 48: 13-20 [Abstract] [Full Text]
Srivastava, M., Pollard, H. B. (1999). Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J. 13: 1911-1922 [Abstract] [Full Text]
Sirri, V, Roussel, P, Hernandez-Verdun, D (1999). The mitotically phosphorylated form of the transcription termination factor TTF-1 is associated with the repressed rDNA transcription machinery. J. Cell Sci. 112: 3259-3268 [Abstract]
Panse, S., Masson, C, Heliot, L, Chassery, J., Junera, H., Hernandez-Verdun, D (1999). 3-D organization of ribosomal transcription units after DRB inhibition of RNA polymerase II transcription. J. Cell Sci. 112: 2145-2154 [Abstract]
Ginisty, H, Sicard, H, Roger, B, Bouvet, P (1999). Structure and functions of nucleolin. J. Cell Sci. 112: 761-772 [Abstract]
Piñol-Roma, S. (1999). Association of Nonribosomal Nucleolar Proteins in Ribonucleoprotein Complexes during Interphase and Mitosis. Mol. Biol. Cell 10: 77-90 [Abstract] [Full Text]
Klein, C., Cheutin, T., O'Donohue, M.-F., Rothblum, L., Kaplan, H., Beorchia, A., Lucas, L., Héliot, L., Ploton, D. (1998). The Three-dimensional Study of Chromosomes and Upstream Binding Factor-immunolabeled Nucleolar Organizer Regions Demonstrates Their Nonrandom Spatial Arrangement during Mitosis. Mol. Biol. Cell 9: 3147-3159 [Abstract] [Full Text]
Dundr, M., Olson, M. O.J. (1998). Partially Processed pre-rRNA Is Preserved in Association with Processing Components in Nucleolus-derived Foci during Mitosis. Mol. Biol. Cell 9: 2407-2422 [Abstract] [Full Text]
Fomproix, N, Gebrane-Younes, J, Hernandez-Verdun, D (1998). Effects of anti-fibrillarin antibodies on building of functional nucleoli at the end of mitosis. J. Cell Sci. 111: 359-372 [Abstract]
Heliot, L., Kaplan, H., Lucas, L., Klein, C., Beorchia, A., Doco-Fenzy, M., Menager, M., Thiry, M., O'Donohue, M.-F., Ploton, D. (1997). Electron Tomography of Metaphase Nucleolar Organizer Regions: Evidence for a Twisted-Loop Organization. Mol. Biol. Cell 8: 2199-2216 [Abstract] [Full Text]
Gebrane-Younes, J, Fomproix, N, Hernandez-Verdun, D (1997). When rDNA transcription is arrested during mitosis, UBF is still associated with non-condensed rDNA. J. Cell Sci. 110: 2429-2440 [Abstract]
Bell, P, Mais, C, McStay, B, Scheer, U (1997). Association of the nucleolar transcription factor UBF with the transcriptionally inactive rRNA genes of pronuclei and early Xenopus embryos. J. Cell Sci. 110: 2053-2063 [Abstract]
Bell, P, Scheer, U (1997). Prenucleolar bodies contain coilin and are assembled in Xenopus egg extract depleted of specific nucleolar proteins and U3 RNA. J. Cell Sci. 110: 43-54 [Abstract]
Segil, N, Guermah, M, Hoffmann, A, Roeder, R G, Heintz, N (1996). Mitotic regulation of TFIID: inhibition of activator-dependent transcription and changes in subcellular localization.. Genes Dev. 10: 2389-2400 [Abstract]
Beven, A., Lee, R, Razaz, M, Leader, D., Brown, J., Shaw, P. (1996). The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs. J. Cell Sci. 109: 1241-1251 [Abstract]
Junera, H., Masson, C, Geraud, G, Hernandez-Verdun, D (1995). The three-dimensional organization of ribosomal genes and the architecture of the nucleoli vary with G1, S and G2 phases. J. Cell Sci. 108: 3427-3441 [Abstract]