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J. Biol. Chem., Vol. 283, Issue 26, 17908-17918, June 27, 2008

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Comprehensive Transcriptional Analysis of the Oxidative Response in Yeast^*

María Micaela Molina-Navarro¹, Laia Castells-Roca¹, Gemma Bellí, José García-Martínez, Julia Marín-Navarro^¶, Joaquín Moreno^¶, José E. Pérez-Ortín^¶2, and Enrique Herrero²³

From the Departament de Ciències Mèdiques Bàsiques and IRBLleida, Universitat de Lleida, Montserrat Roig 2, 25008-Lleida and the Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Biológicas and ^¶Sección de Chips de DNA-Servicio Central de Ayuda a la Investigación Experimental, Universitat de València, 46100-Burjassot Valencia, Spain

The oxidative stress response in Saccharomyces cerevisiae has been analyzed by parallel determination of mRNA levels and transcription rates for the entire genome. A mathematical algorithm has been adapted for a dynamic situation such as the response to stress, to calculate theoretical mRNA decay rates from the experimental data. Yeast genes have been grouped into 25 clusters according to mRNA level and transcription rate kinetics, and average mRNA decay rates have been calculated for each cluster. In most of the genes, changes in one or both experimentally determined parameters occur during the stress response. 24% of the genes are transcriptionally induced without an increase in mRNA levels. The lack of parallelism between the evolution of the mRNA amount and transcription rate predicts changes in mRNA stability during stress. Genes for ribosomal proteins and rRNA processing enzymes are abundant among those whose mRNAs are predicted to destabilize. The number of genes whose mRNAs are predicted to stabilize is lower, although some protein folding or proteasomal genes are among the latter. We have confirmed the mathematical predictions for several genes pertaining to different clusters by experimentally determining mRNA decay rates using the regulatable tetO promoter in transcriptional expression conditions not affected by the oxidative stress. This study indicates that the oxidative stress response in yeast cells is not only conditioned by gene transcription but also by the mRNA decay dynamics and that this complex response may be particularly relevant to explain the temporary down-regulation of protein synthesis occurring during stress.

Received for publication, January 11, 2008 , and in revised form, March 19, 2008.

^* This work was supported by Grants BFU2004-03167 and CSD2007-0020 (from the Ministerio de Educación y Ciencia) and 2005SGR-00677 (from the Generalitat de Catalunya) (to E. H.) and BFU2006-15446-CO3-02 and BFU2007-67575-CO3-01/BMC (from the Ministerio de Educación y Ciencia) (to J. E. P.-O.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains seven supplemental tables.

This article was selected as a Paper of the Week.

¹ Both authors contributed equally to the paper.

² Both authors contributed equally to the senior authorship of this work.

³ To whom correspondence should be addressed. Tel.: 34-973-702409; Fax: 34-973-702426; E-mail: enric.herrero{at}cmb.udl.cat.

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