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Molecular and Cellular Biology, October 2007, p. 6581-6592, Vol. 27, No. 19
0270-7306/07/$08.00+0     doi:10.1128/MCB.00668-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Cytoplasmic Recycling of 60S Preribosomal Factors Depends on the AAA Protein Drg1 ^,

Brigitte Pertschy,^1,, Cosmin Saveanu,^2, Gertrude Zisser,¹ Alice Lebreton,^2,¶ Martin Tengg,¹ Alain Jacquier,² Eva Liebminger,¹ Berthold Nobis,¹ Lisa Kappel,¹ Ida van der Klei,³ Gregor Högenauer,¹ Micheline Fromont-Racine,^2* and Helmut Bergler^1*

Institut für Molekulare Biowissenschaften, Karl-Franzens Universität Graz, Universitätsplatz 2, A-8010 Graz, Austria,¹ Unité de Génétique des Interactions Macromoléculaires, URA 2171-CNRS Département Génomes et Génétique, Batiment Fernbach, Institut Pasteur, 25, rue du Dr. Roux, F-75724 Paris cedex 15, France,² Laboratory of Eukaryotic Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands³

Received 17 April 2007/ Returned for modification 7 May 2007/ Accepted 13 July 2007

Allelic forms of DRG1/AFG2 confer resistance to the drug diazaborine, an inhibitor of ribosome biogenesis in Saccharomyces cerevisiae. Our results show that the AAA-ATPase Drg1 is essential for 60S maturation and associates with 60S precursor particles in the cytoplasm. Functional inactivation of Drg1 leads to an increased cytoplasmic localization of shuttling pre-60S maturation factors like Rlp24, Arx1, and Tif6. Surprisingly, Nog1, a nuclear pre-60S factor, was also relocalized to the cytoplasm under these conditions, suggesting that it is a previously unsuspected shuttling preribosomal factor that is exported with the precursor particles and very rapidly reimported. Proteins that became cytoplasmic under drg1 mutant conditions were blocked on pre-60S particles at a step that precedes the association of Rei1, a later-acting preribosomal factor. A similar cytoplasmic accumulation of Nog1 and Rlp24 in pre-60S-bound form could be seen after overexpression of a dominant-negative Drg1 variant mutated in the D2 ATPase domain. We conclude that the ATPase activity of Drg1 is required for the release of shuttling proteins from the pre-60S particles shortly after their nuclear export. This early cytoplasmic release reaction defines a novel step in eukaryotic ribosome maturation.

Published ahead of print on 23 July 2007.

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

Present address: Biochemie-Zentrum Heidelberg (BZH), Universität Heidelberg, Im Neuenheimer Feld 328, D-69120 Heidelberg, Germany.

These authors contributed equally.

^¶ Present address: Centre de Génétique Moléculaire, CNRS-UPR2167, Avenue de la Terrasse, 91190 Gif sur Yvette, France.

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• Lebreton, A., Rousselle, J.-C., Lenormand, P., Namane, A., Jacquier, A., Fromont-Racine, M., Saveanu, C. (2008). 60S ribosomal subunit assembly dynamics defined by semi-quantitative mass spectrometry of purified complexes. Nucleic Acids Res 36: 4988-4999 [Abstract] [Full Text]  
• Kressler, D., Roser, D., Pertschy, B., Hurt, E. (2008). The AAA ATPase Rix7 powers progression of ribosome biogenesis by stripping Nsa1 from pre-60S particles. J. Cell Biol. 181: 935-944 [Abstract] [Full Text]