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Molecular and Cellular Biology, March 2006, p. 1731-1742, Vol. 26, No. 5
0270-7306/06/$08.00+0     doi:10.1128/MCB.26.5.1731-1742.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Autoregulation of Ribosome Biosynthesis by a Translational Response in Fission Yeast

François Bachand,1* Daniel H. Lackner,2 Jürg Bähler,2 and Pamela A. Silver3

Department of Biochemistry, Université de Sherbrooke, Sherbrooke, Québec, Canada,1 Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom,2 Department of Systems Biology, Harvard Medical School and Dana Farber Cancer Institute, Boston, Massachusetts3

Received 7 July 2005/ Returned for modification 29 August 2005/ Accepted 5 December 2005

Maintaining the appropriate balance between the small and large ribosomal subunits is critical for translation and cell growth. We previously identified the 40S ribosomal protein S2 (rpS2) as a substrate of the protein arginine methyltransferase 3 (RMT3) and reported a misregulation of the 40S/60S ratio in rmt3 deletion mutants of Schizosaccharomyces pombe. For this study, using DNA microarrays, we have investigated the genome-wide biological response of rmt3-null cells to this ribosomal subunit imbalance. Whereas little change was observed at the transcriptional level, a number of genes showed significant alterations in their polysomal-to-monosomal ratios in rmt3{Delta} mutants. Importantly, nearly all of the 40S ribosomal protein-encoding mRNAs showed increased ribosome density in rmt3 disruptants. Sucrose gradient analysis also revealed that the ribosomal subunit imbalance detected in rmt3-null cells is due to a deficit in small-subunit levels and can be rescued by rpS2 overexpression. Our results indicate that rmt3-null fission yeast compensate for the reduced levels of small ribosomal subunits by increasing the ribosome density, and likely the translation efficiency, of 40S ribosomal protein-encoding mRNAs. Our findings support the existence of autoregulatory mechanisms that control ribosome biosynthesis and translation as an important layer of gene regulation.

* Corresponding author. Mailing address: Department of Biochemistry, Université de Sherbrooke, Sherbrooke, Québec, Canada. Phone: (819) 820-6868. Fax: (819) 564-5340. E-mail: f.bachand{at}usherbrooke.ca.

Molecular and Cellular Biology, March 2006, p. 1731-1742, Vol. 26, No. 5
0022-538X/06/$08.00+0     doi:10.1128/MCB.26.5.1731-1742.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Perreault, A., Gascon, S., D'Amours, A., Aletta, J. M., Bachand, F. (2009). A Methyltransferase-independent Function for Rmt3 in Ribosomal Subunit Homeostasis. J. Biol. Chem. 284: 15026-15037 [Abstract] [Full Text]  
  • Perreault, A., Bellemer, C., Bachand, F. (2008). Nuclear export competence of pre-40S subunits in fission yeast requires the ribosomal protein Rps2. Nucleic Acids Res 36: 6132-6142 [Abstract] [Full Text]  
  • Sadaie, M., Shinmyozu, K., Nakayama, J.-i. (2008). A Conserved SET Domain Methyltransferase, Set11, Modifies Ribosomal Protein Rpl12 in Fission Yeast. J. Biol. Chem. 283: 7185-7195 [Abstract] [Full Text]  
  • Swiercz, R., Cheng, D., Kim, D., Bedford, M. T. (2007). Ribosomal Protein rpS2 Is Hypomethylated in PRMT3-deficient Mice. J. Biol. Chem. 282: 16917-16923 [Abstract] [Full Text]  
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  • Porras-Yakushi, T. R., Whitelegge, J. P., Clarke, S. (2006). A Novel SET Domain Methyltransferase in Yeast: Rkm2-DEPENDENT TRIMETHYLATION OF RIBOSOMAL PROTEIN L12ab AT LYSINE 10. J. Biol. Chem. 281: 35835-35845 [Abstract] [Full Text]  


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