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J. Biol. Chem., Vol. 278, Issue 46, 45882-45887, November 14, 2003

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ATO3 Encoding a Putative Outward Ammonium Transporter Is an RTG-independent Retrograde Responsive Gene Regulated by GCN4 and the Ssy1-Ptr3-Ssy5 Amino Acid Sensor System^*

Nicoletta Guaragnella and Ronald A. Butow

From the Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9148

Respiratory deficient yeast cells such as ^o petites activate an inter-organelle signaling pathway called retrograde regulation. This results in changes in the expression of a subset of nuclear genes leading to major reconfigurations of metabolism that enable cells to adapt to the respiratory deficient state. Previous studies have focused on the role of three positive regulatory factors in the retrograde pathway, Rtg1p, Rtg2p, and Rtg3p, which are essential for both basal and elevated expressions of some, but not all, retrograde responsive genes. Here we characterize the retrograde regulation of one of those genes, ATO3, whose elevated expression in ^o petites is largely independent of RTG gene function. ATO3 encodes a member of the YaaH family of proteins that is a putative outward ammonium transporter. We show that Ato3p-green fluorescent protein is preferentially localized to the plasma membrane of mother cells. ^o petites express more Ato3p-green fluorescent protein in their plasma membrane than do ⁺ cells, consistent with the elevated level of ATO3 transcripts in ^o cells. We find that ATO3 expression has two levels of control, both of which are connected to amino acid sensing and regulation. The first involves GCN4, which is required for the bulk of ATO3 expression. The second involves the Ssy1-Ptr3-Ssy5 amino acid sensor system, which is preferentially required for elevated ATO3 expression in ^o cells. We propose that ATO3 is induced in ^o cells to eliminate the excess ammonia that arises because of a potential defect in ammonia assimilation in those cells.

Received for publication, August 21, 2003 , and in revised form, September 5, 2003.

^* This work was supported by National Institutes of Health Grant GM 22525 and The Robert A. Welch Foundation Grant I-0642. 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.

To whom correspondence should be addressed: Dept. of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390-9148; Tel.: 214-648-1465; Fax: 214-648-1488; E-mail: ronald.butow{at}utsouthwestern.edu.

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