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J. Biol. Chem., Vol. 283, Issue 42, 28670-28679, October 17, 2008

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Whi3, a Developmental Regulator of Budding Yeast, Binds a Large Set of mRNAs Functionally Related to the Endoplasmic Reticulum^*

From the Departament de Ciències Mèdiques Bàsiques, Institut de Recerca Biomèdica de Lleida, Universitat de Lleida, Montserrat Roig 2, 25008 Lleida, Catalonia, Spain

Whi3 is an RNA-binding protein associated with the endoplasmic reticulum (ER) that binds the CLN3 mRNA and plays a key role in the efficient retention of cyclin Cln3 at the ER. In the present work, we have identified new Whi3-associated mRNAs by a genomic approach. A large and significant number of these Whi3 targets encode for membrane and exocytic proteins involved in processes such as transport and cell wall biogenesis. Consistent with the genomic data, we have observed that cell wall integrity is compromised in Whi3-deficient cells and found strong genetic interactions between WHI3 and the cell integrity pathway. Whi3-associated mRNAs are enriched in clusters of the tetranucleotide GCAU, and mutation of the GCAU clusters in the CLN3 mRNA caused a reduction in its association to Whi3, suggesting that these sequences may act as cis-determinants for binding. Our data suggest that Whi3 is involved in the regulation and/or localization of a large subset of mRNAs functionally related to the ER and, since it is important for different molecular processes such as cytoplasmic retention or exocytic traffic of proteins, we propose that Whi3 is a general modulator of protein fate in budding yeast.

Received for publication, June 17, 2008 , and in revised form, July 28, 2008.

The microarray data have been deposited in the ArrayExpress data base with accession number E-MEXP-1734.

^* This work was funded by grants from the Ministry of Education and Science of Spain (Consolider-Ingenio 2010), the Fundació La Caixa, and the European Union (Fondos FEDER). 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 a supplemental table with nine worksheets.

This article was selected as a Paper of the Week.

¹ These authors contributed equally to this work.

² N. C. and F. F. are researchers of the Ramón y Cajal program.

³ Present address, Department of Molecular Genetics and Microbiology, The State University of New York (SUNY), Stony Brook, NY 11794-5222.

⁴ To whom correspondence should be addressed: Dept. Ciències Mèdiques Bàsiques, Facultat de Medicina, Universitat de Lleida, Montserrat Roig 2, 25008 Lleida, Catalunya, Spain, Tel.: 34-973702411; Fax: 34-973702426. E-mail: eloi.gari{at}cmb.udl.cat.

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