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Molecular and Cellular Biology, July 2006, p. 5131-5145, Vol. 26, No. 13
0270-7306/06/$08.00+0     doi:10.1128/MCB.02227-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Potential Roles for Ubiquitin and the Proteasome during Ribosome Biogenesis{ddagger}

Diana A. Stavreva,1,{dagger} Miyuki Kawasaki,3,{dagger} Miroslav Dundr,1,§ Karel Koberna,2,¶ Waltraud G. Müller,1 Teruko Tsujimura-Takahashi,3 Wataru Komatsu,3 Toshiya Hayano,3 Toshiaki Isobe,3 Ivan Raska,2 Tom Misteli,1 Nobuhiro Takahashi,3 and James G. McNally1*

Laboratory of Receptor Biology and Gene Expression, Center for Cancer Research, National Cancer Institute, Bethesda, Maryland 20892,1 Institute of Cellular Biology and Pathology, First Faculty of Medicine, Charles University in Prague, and Institute of Physiology, Academy of Sciences of the Czech Republic, Albertov 4, 128 00 Prague 2, Czech Republic,2 Department of Applied Biological Science and Department of Biotechnology, United Graduate School of Agriculture, Tokyo University of Agriculture and Technology, and Integrated Proteomics System Project, Pioneer Research on Genome the Frontier, Ministry of Education, Culture, Sports, Science, and Technology of Japan, 3-5-8 Saiwai-cho, Fuchu-shi, Tokyo 183-8509, Japan3

Received 18 November 2005/ Returned for modification 23 December 2005/ Accepted 17 March 2006

We have investigated the possible involvement of the ubiquitin-proteasome system (UPS) in ribosome biogenesis. We find by immunofluorescence that ubiquitin is present within nucleoli and also demonstrate by immunoprecipitation that complexes associated with pre-rRNA processing factors are ubiquitinated. Using short proteasome inhibition treatments, we show by fluorescence microscopy that nucleolar morphology is disrupted for some but not all factors involved in ribosome biogenesis. Interference with proteasome degradation also induces the accumulation of 90S preribosomes, alters the dynamic properties of a number of processing factors, slows the release of mature rRNA from the nucleolus, and leads to the depletion of 18S and 28S rRNAs. Together, these results suggest that the UPS is probably involved at many steps during ribosome biogenesis, including the maturation of the 90S preribosome.

* Corresponding author. Mailing address for James G. McNally: Laboratory of Receptor Biology and Gene Expression, 41 Library Dr., National Cancer Institute, Bethesda, MD 20892. Phone: (301) 402-0209. Fax: (301) 496-4951. E-mail: mcnallyj{at}exchange.nih.gov. Mailing address for Nobuhiro Takahashi: Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu-shi, Tokyo 183-8509, Japan. Phone and fax: 81-042-367-5709. E-mail: ntakahas{at}cc.tuat.ac.jp.

{ddagger} Supplemental material for this article may be found at http://mcb.asm.org/.

{dagger} D.A.S. and M.K. contributed equally to this study.

§ Present address: Department of Cell Biology and Anatomy, Rosalin Franklin University of Medicine and Science, 3333 Green Bay Road, North Chicago, IL 60064.

Present address: Department of Cell Biology, Institute of Experimental Medicine, Videnska 1083, Prague 4, Czech Republic.

Molecular and Cellular Biology, July 2006, p. 5131-5145, Vol. 26, No. 13
0270-7306/06/$08.00+0     doi:10.1128/MCB.02227-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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