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J. Biol. Chem., Vol. 281, Issue 9, 5546-5552, March 3, 2006

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Carbon Catabolite Repression Regulates Amino Acid Permeases in Saccharomyces cerevisiae via the TOR Signaling Pathway^*

George J. Peter, Louis Düring, and Aamir Ahmed¹

From the Institute of Urology and Nephrology, University College London, 67 Riding House Street, London, W1W 7EY, United Kingdom and Carlsberg Research Laboratory, Gamle Carlsberg Vej 10, DK-2500, Copenhagen Valby, Denmark

We have identified carbon catabolite repression (CCR) as a regulator of amino acid permeases in Saccharomyces cerevisiae, elucidated the permeases regulated by CCR, and identified the mechanisms involved in amino acid permease regulation by CCR. Transport of L-arginine and L-leucine was increased by 10–25-fold in yeast grown in carbon sources alternate to glucose, indicating regulation by CCR. In wild type yeast the uptake (pmol/10⁶ cells/h), in glucose versus galactose medium, of L-[¹⁴C]arginine was (0.24 ± 0.04 versus 6.11 ± 0.42) and L-[¹⁴C]leucine was (0.30 ± 0.02 versus 3.60 ± 0.50). The increase in amino acid uptake was maintained when galactose was replaced with glycerol. Deletion of gap1 and agp1 from the wild type strain did not alter CCR induced increase in L-leucine uptake; however, deletion of further amino acid permeases reduced the increase in L-leucine uptake in the following manner: 36% (gnp1), 62% (bap2), 83% ((bap2-tat1)). Direct immunofluorescence showed large increases in the expression of Gnp1 and Bap2 proteins when grown in galactose compared with glucose medium. By extending the functional genomic approach to include major nutritional transducers of CCR in yeast, we concluded that SNF/MIG, GCN, or PSK pathways were not involved in the regulation of amino acid permeases by CCR. Strikingly, the deletion of TOR1, which regulates cellular response to changes in nitrogen availability, from the wild type strain abolished the CCR-induced amino acid uptake. Our results provide novel insights into the regulation of yeast amino acid permeases and signaling mechanisms involved in this regulation.

Received for publication, December 28, 2005

^* This work was supported by the Wellcome Trust, United Kingdom. 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.

¹ To whom correspondence should be addressed: Institute of Urology and Nephrology, University College London, 67 Riding House St., London, W1W 7EY, UK. Tel.: 44-207-679-9597; Fax: 44-207-679-9633; E-mail: aamir.ahmed{at}ucl.ac.uk.

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