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Published online
doi:10.1083/jcb.200805146
The Journal of Cell Biology, Vol. 183, No. 7, 1259-1274
The Rockefeller University Press, 0021-9525 $30.00
© Sanij et al.
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Article

UBF levels determine the number of active ribosomal RNA genes in mammals



Elaine Sanij1, Gretchen Poortinga1, Kerith Sharkey1, Sandy Hung1, Timothy P. Holloway1, Jaclyn Quin1, Elysia Robb1, Lee H. Wong3, Walter G. Thomas4, Victor Stefanovsky5, Tom Moss5, Lawrence Rothblum6, Katherine M. Hannan1, Grant A. McArthur1,2,7, Richard B. Pearson1,8, and Ross D. Hannan1,8

1 Research Division and 2 Division of Haematology and Medical Oncology, Peter MacCallum Cancer Centre, East Melbourne, Victoria 3002, Australia
3 Murdoch Childrens Research Institute, Royal Children's Hospital, Parkville, Victoria 3010, Australia
4 School of Biomedical Sciences, University of Queensland, St. Lucia, Queensland 4072, Australia
5 Cancer Research Centre, Laval University, Hôtel-Dieu de Québec, Québec G1R 2J6, Canada
6 Department of Cell Biology, University of Oklahoma Medical College, Oklahoma City, OK 73104
7 Department of Medicine, St. Vincent's Hospital and 8 Department of Biochemistry and Molecular Biology, University of Melbourne, Melbourne, Victoria 3010, Australia

Correspondence to Ross D. Hannan: ross.hannan{at}petermac.org

In mammals, the mechanisms regulating the number of active copies of the ~200 ribosomal RNA (rRNA) genes transcribed by RNA polymerase I are unclear. We demonstrate that depletion of the transcription factor upstream binding factor (UBF) leads to the stable and reversible methylation-independent silencing of rRNA genes by promoting histone H1–induced assembly of transcriptionally inactive chromatin. Chromatin remodeling is abrogated by the mutation of an extracellular signal-regulated kinase site within the high mobility group box 1 domain of UBF1, which is required for its ability to bend and loop DNA in vitro. Surprisingly, rRNA gene silencing does not reduce net rRNA synthesis as transcription from remaining active genes is increased. We also show that the active rRNA gene pool is not static but decreases during differentiation, correlating with diminished UBF expression. Thus, UBF1 levels regulate active rRNA gene chromatin during growth and differentiation.

E. Robb's present address is Mental Health Research Institute, Parkville, Victoria 3052, Australia.

Abbreviations used in this paper: AgNOR, argyrophilic NOR; ChIP, chromatin immunoprecipitation; ETS, external transcribed spacer; GAPDH, glyceraldehyde 3-phosphate dehydrogenase; HMG, high mobility group; IGS, intergenic spacer; MeDIP, methylated DNA immunoprecipitation; MEF, mouse embryonic fibroblast; MPRO, murine promyelocytic; MSCV, murine stem cell virus; NOR, nucleolar organizing region; NoRC, nucleolar remodeling complex; Pol I, polymerase I; pRT, pRevTRE; qChIP, quantitative ChIP; qRT-PCR, quantitative real-time PCR; r-chromatin, ribosomal gene chromatin; rDNA, ribosomal DNA; rRNA, ribosomal RNA; rUBF, rattus UBF; shRNA, short hairpin RNA; shRNAmir, shRNA–micro RNA; SS, serum starvation; UBF, upstream binding factor; UCE, upstream control element.

© 2008 Sanij et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.jcb.org/misc/terms.shtml). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).


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