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Molecular and Cellular Biology, September 2007, p. 5968-5985, Vol. 27, No. 17
0270-7306/07/$08.00+0     doi:10.1128/MCB.00019-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Ribosomal Protein L33 Is Required for Ribosome Biogenesis, Subunit Joining, and Repression of GCN4 Translation{triangledown} ,{dagger}

Pilar Martín-Marcos,1 Alan G. Hinnebusch,2 and Mercedes Tamame1*

Instituto de Microbiología Bioquímica, CSIC/Universidad de Salamanca, Edificio Departamental de Biología, Campus Miguel de Unamuno, 37007 Salamanca, Spain,1 Laboratory of Gene Regulation and Development, National Institute of Child Health and Human Development, Bethesda, Maryland 208922

Received 4 January 2007/ Returned for modification 8 February 2007/ Accepted 21 May 2007

We identified a mutation in the 60S ribosomal protein L33A (rpl33a-G76R) that elicits derepression of GCN4 translation (Gcd– phenotype) by allowing scanning preinitiation complexes to bypass inhibitory upstream open reading frame 4 (uORF4) independently of prior uORF1 translation and reinitiation. At 37°C, rpl33a-G76R confers defects in 60S biogenesis comparable to those produced by the deletion of RPL33A ({Delta}A). At 28°C, however, the 60S biogenesis defect is less severe in rpl33a-G76R than in {Delta}A cells, yet rpl33a-G76R confers greater derepression of GCN4 and a larger reduction in general translation. Hence, it appears that rpl33a-G76R has a stronger effect on ribosomal-subunit joining than does a comparable reduction of wild-type 60S levels conferred by {Delta}A. We suggest that rpl33a-G76R alters the 60S subunit in a way that impedes ribosomal-subunit joining and thereby allows 48S rRNA complexes to abort initiation at uORF4, resume scanning, and initiate downstream at GCN4. Because overexpressing tRNAiMet suppresses the Gcd– phenotype of rpl33a-G76R cells, dissociation of tRNAiMet from the 40S subunit may be responsible for abortive initiation at uORF4 in this mutant. We further demonstrate that rpl33a-G76R impairs the efficient processing of 35S and 27S pre-rRNAs and reduces the accumulation of all four mature rRNAs, indicating an important role for L33 in the biogenesis of both ribosomal subunits.

* Corresponding author. Mailing address: Mercedes Tamame, Instituto de Microbiología Bioquímica, CSIC/Universidad de Salamanca, Edificio Departamental de Biología, Campus Miguel de Unamuno, 37007 Salamanca, Spain. Phone: 34 923 121673. Fax: 34 923 224876. E-mail: tamame{at}usal.es

{triangledown} Published ahead of print on 4 June 2007.

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

Molecular and Cellular Biology, September 2007, p. 5968-5985, Vol. 27, No. 17
0270-7306/07/$08.00+0     doi:10.1128/MCB.00019-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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