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J. Biol. Chem., Vol. 283, Issue 14, 8919-8929, April 4, 2008

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Tor Pathway Control of the Nitrogen-responsive DAL5 Gene Bifurcates at the Level of Gln3 and Gat1 Regulation in Saccharomyces cerevisiae^*

Isabelle Georis¹, Jennifer J. Tate², Terrance G. Cooper²³, and Evelyne Dubois¹

From the Institut de Recherches Microbiologiques J.-M. Wiame, Laboratoire de Microbiologie Université Libre de Bruxelles, B1070 Brussels, Belgium and the Department of Molecular Sciences, University of Tennessee, Memphis, Tennessee 38163

The Tor1,2 protein kinases globally influence many cellular processes including nitrogen-responsive gene expression that correlates with intracellular localization of GATA transcription activators Gln3 and Gat1/Nil1. Gln3-Myc¹³ and Gat1-Myc¹³ are restricted to the cytoplasm of cells provided with good nitrogen sources, e.g. glutamine. Following the addition of the Tor1,2 inhibitor, rapamycin, both transcription factors relocate to the nucleus. Gln3-Myc¹³ localization is highly dependent upon Ure2 and type 2A-related phosphatase, Sit4. Ure2 is required for Gln3 to be restricted to the cytoplasm of cells provided with good nitrogen sources, and Sit4 is required for its location to the nucleus following rapamycin treatment. The paucity of analogous information concerning Gat1 regulation prompted us to investigate the effects of deleting SIT4 and URE2 on Gat1-Myc¹³ localization, DNA binding, and NCR-sensitive transcription. Our data demonstrate that Tor pathway control of NCR-responsive transcription bifurcates at the regulation of Gln3 and Gat1. Gat1-Myc¹³ localization is not strongly influenced by deleting URE2, nor is its nuclear targeting following rapamycin treatment strongly dependent on Sit4. ChIP experiments demonstrated that Gat1-Myc¹³ can bind to the DAL5 promoter in the absence of Gln3. Gln3-Myc¹³, on the other hand, cannot bind to DAL5 in the absence of Gat1. We conclude that: (i) Tor pathway regulation of Gat1 differs markedly from that of Gln3, (ii) nuclear targeting of Gln3-Myc¹³ is alone insufficient for its recruitment to the DAL5 promoter, and (iii) the Tor pathway continues to play an important regulatory role in NCR-sensitive transcription even after Gln3-Myc¹³ is localized to the nucleus.

Received for publication, October 25, 2007 , and in revised form, January 15, 2008.

^* 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.

This article is dedicated to Prof. Ronald Butow of the University of Texas Southwestern Medical Center (1936–2007), who contributed so much to the field of mitochondrial retrograde regulation and its interface with nitrogen and GATA factor regulation in S. cerevisiae.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1 and S2.

¹ Supported by the Commission Communautaire Française.

² Supported by National Institutes of Health Grant GM-35642 and National Institutes of Health/National Science Foundation Grant DMS-0443901.

³ To whom correspondence should be addressed. Fax: 901-448-8462; E-mail: tcooper{at}utmem.edu.

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