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J. Biol. Chem., Vol. 281, Issue 48, 36632-36642, December 1, 2006

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The Transcriptional Response of the Yeast Na⁺-ATPase ENA1 Gene to Alkaline Stress Involves Three Main Signaling Pathways^*>

Maria Platara¹, Amparo Ruiz², Raquel Serrano³, Aarón Palomino⁴, Fernando Moreno, and Joaquín Ariño⁵

From the Department of Bioquímica i Biologia Molecular, Universitat Autónoma de Barcelona, Bellaterra 08193, Barcelona and the Department of Bioquímica y Biología Molecular, Universidad de Oviedo, Oviedo 33006, Spain

Adaptive response of the yeast Saccharomyces cerevisiae to environmental alkalinization results in remodeling of gene expression. A key target is the gene ENA1, encoding a Na⁺-ATPase, whose induction by alkaline pH has been shown to involve calcineurin and the Rim101/Nrg1 pathway. Previous functional analysis of the ENA1 promoter revealed a calcineurin-independent pH responsive region (ARR2, 83 nucleotides). We restrict here this response to a small (42 nucleotides) ARR2 5·-region, named MCIR (minimum calcineurin independent response), which contains a MIG element, able to bind Mig1,2 repressors. High pH-induced response driven from this region was largely abolished in snf1 cells and moderately reduced in a rim101 strain. Cells lacking Mig1 or Mig2 repressors had a near wild type response, but the double mutant presented a high level of expression upon alkaline stress. Deletion of NRG1 (but not of NRG2) resulted in increased expression. Induction from the MCIR region was marginal in a quadruple mutant lacking Nrg1,2 and Mig1,2 repressors. In vitro band shift experiments demonstrated binding of Nrg1 to the 5· end of the ARR2 region. Furthermore, we show that Nrg1 binds in vivo around the MCIR region under standard growth conditions, and that binding is largely abolished after high pH stress. Therefore, the calcineurin-independent response of the ENA1 gene is under the regulation of Rim101 (through Nrg1) and Snf1 (through Nrg1 and Mig2). Accordingly, induction by alkaline stress of the entire ENA1 promoter in a snf1 rim101 mutant in the presence of the calcineurin inhibitor FK506 is completely abolished. Thus, the transcriptional response to alkaline stress of the ENA1 gene integrates three different signaling pathways.

Received for publication, July 7, 2006 , and in revised form, September 22, 2006.

^* This work was supported in part by Grants BMC2002-04011-C05-04 and BFU2005-06388-C4-04-BMC (to J. A.) and BFU2004-02855-C0202 (to F. M.) from the Ministerio de Educación y Ciencia, Spain, and Fondo Europeo de Desarrollo Regional. 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 supplemental Table S1.

¹ Currently holds a fellowship from the Spanish Ministry of Education and Science.

² Recipient of a fellowship from the Generalitat de Catalunya, Spain.

³ Recipient of a fellowship from the Spanish Ministry of Education and Science.

⁴ Recipient of a fellowship from FICYT (Fundación para el Fomento en Asturias de la Investigación Científica Aplicada y la Tecnología).

⁵ Recipient of "Ajut de Support a les Activitats dels Grups de Recerca" Grant 2005SGR-00542, Generalitat de Catalunya. To whom correspondence should be addressed: Dept. Bioquímica i Biologia Molecular, Ed. V, Universitat Autònoma de Barcelona, Bellaterra 08193, Barcelona, Spain. Tel.: 34-93-5812182; Fax: 34-93-5812006; E-mail: Joaquin.Arino{at}uab.es.

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