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Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón II, Piso 2. C1428EGA, Buenos Aires, Argentina
Correspondence
Susana Correa García
correa{at}qb.fcen.uba.ar
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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-aminobutyric acid (GABA) and 
-aminolaevulinic acid (ALA) permease, is well known to be regulated by the nitrogen source. Its expression levels are low in the presence of a rich nitrogen source but are higher when a poor nitrogen source is used. In addition, GABA can induce UGA4 expression when cells are grown with proline but not when they are grown with ammonium. Although vast amounts of evidence have been gathered about UGA4 regulation by nitrogen, little is known about its regulation by the carbon source. Using glucose and acetate as rich and poor carbon source respectively, this work aimed to shed light on hitherto unclear aspects of the regulation of this gene. In poor nitrogen conditions, cells grown with acetate were found to have higher UGA4 basal expression levels than those grown with glucose, and did not show UGA4 induction in response to GABA. Analysis of the expression and subcellular localization of the transcription factors that regulate UGA4 as well as partial deletions and site-directed mutations of the UGA4 promoter region suggested that there are two parallel pathways that act in regulating this gene by the carbon source. Furthermore, the results demonstrate the existence of a new factor operating in UGA4 regulation.
-aminolaevulinic acid; GABA, -aminobutyric acid; NCR, nitrogen catabolite repression; UAS, upstream activating sequence
Members of the Research Career Programme of CONICET.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) and a diverse set of developmental functions in animal cells (Kelley et al., 1993; Laverriere et al., 1994), is one of the gene families shared by S. cerevisiae and higher eukaryotes. Yeast GATA proteins Gln3, Gat1/Nil1, Dal80/Uga43 and Gzf3/Deh1 are the main regulators of nitrogen catabolism gene expression that are responsible for the phenomenon known as nitrogen catabolite repression (NCR). The expression of the UGA4 gene, which encodes the -aminobutyric acid (GABA) and -aminolaevulinic acid (ALA) permease in S. cerevisiae, depends on GABA induction and NCR (Andre et al., 1993; Bermudez Moretti et al., 1996). Induction of this permease requires at least two positive-acting proteins, the specific Uga3p factor and the pleiotropic Dal81p/Uga35p factor (Andre et al., 1995; Bricmont et al., 1991). These factors act through a 19 bp CG-rich upstream activating sequence, UASGABA. The promoter region of UGA4 also contains four adjacent repeats of the heptanucleotide 5'-CGAT(A/T)AG-3', which constitute a UASGATA element. This element can potentially confer high levels of expression in the absence of inducer. Nevertheless, the basal expression levels of the UGA4 gene in uninduced cells grown with a poor nitrogen source such as proline are low since there is a strong repression mechanism involving Dal80p/Uga43p, a pleiotropic regulatory factor (Andre et al., 1995; Bricmont et al., 1991; Cunningham et al., 1994). Gln3p, another GATA transcription factor, upregulates the expression of UGA4 in the presence of inducer by competing with Dal80p/Uga43p for binding to the UASGATA sequence (Coffman et al., 1997; Soussi-Boudekou et al., 1997). The outcome of this competition influences basal levels of transcription. The role of the other positive and negative GATA factors, Gat1 and Gzf3 respectively, in UGA4 regulation has been poorly studied.
NCR is superimposed on the above regulation: in cells grown with a rich nitrogen source such as ammonium or glutamine, Ure2p, a pre-prionic cytoplasmic protein, prevents nuclear localization of Gln3p by retaining it in the cytoplasm, consequently preventing its activity (Kulkarni et al., 2001).
Gat1 was thought to act in a way similar to Gln3, but whereas a Gln3–Ure2 complex has been isolated from cells in which NCR-sensitive transcription is repressed, a similar Gat1–Ure2 complex has not yet been reported (Tate et al., 2006).
Many reports have been published assessing the relationship between nuclear localization and phosphorylation levels of Gln3; emerging results show a lack of correlation between these parameters. However, Gln3 intracellular localization and NCR do correlate well (Tate et al., 2005). It must be noted that much less is known about Gat1 phosphorylation and localization in response to nutrient availability (Kulkarni et al., 2006).
TOR1/2 are phosphatidylinositol kinase-related proteins, which are inhibited by rapamycin and sense nutrients, specifically carbon and nitrogen quality, regulating gene expression. These kinases are, at least in part, involved in Gln3 and Gat1 phosphorylation (Bertram et al., 2002). It has been reported that the activation of Gln3 and Gat1 is not identical, that they control distinct (although overlapping) sets of genes and that low-quality carbon or nitrogen activates Gln3 or Gat1 differentially (Crespo et al., 2002; Kuruvilla et al., 2001; Shamji et al., 2000). Moreover, the phosphorylation state of Ure2, the anchor protein of the positive GATA factors in the cytoplasm when carbon and nitrogen nutrients are abundant (Beck & Hall, 1999), responds not to the nitrogen availability but rather to the carbon source (Kuruvilla et al., 2002).
Evidence indicates that not only nitrogen but also carbon nutrient quality controls the expression of some NCR genes (Shamji et al., 2000) and that Gln3 and Gat1 localization and/or phosphorylation depend on the quality of the available carbon and/or nitrogen source (Bertram et al., 2002; Crespo et al., 2002; Kulkarni et al., 2006; Tate et al., 2005).
Since the UGA4 gene is tightly regulated and some of the transcription factors participating in its regulation (i.e. Gln3 and Gat1) have been linked to NCR gene expression in response to the quality of the carbon source, the aim of our work was to get further insights into the regulation of this gene by the carbon source. We analysed the expression of UGA4 and the role of the GATA factors and the target DNA sequences on the UGA4 promoter involved in the regulation of the UGA4 gene.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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1278b, were 23344c (MAT
ura3), 30505b (MAT ura3 gln3
), 30078c (MAT ura3 uga43), CD17 (MAT ura3 uga35), 26790a (MAT ura3 uga3), 34411c (MATa ura3 nil1° (KanR) gln3°) and 32164b (MAT ura3 nil1° (KanR)). These strains were kindly provided by Professor S. Vissers (Université Libre de Bruxelles, Belgium). Cells were grown in minimal medium containing 0.17 % Difco yeast nitrogen base (YNB without amino acids and ammonium sulfate) with 2 % glucose or 2 % potassium acetate as carbon source, and 10 mM proline or 10 mM ammonium sulfate as nitrogen source. Yeast strains were transformed using the methodology described by Gietz & Woods (2002).
Construction of fusion plasmids.
All procedures for manipulating DNA were standard ones (Sambrook et al., 1997). 5'-Regulatory regions and part of the coding regions of the UGA4 (–583 to +15, with respect to the ATG initiation codon), UGA43 (–848 to +48), GZF3 (–790 to +21), GLN3 (–826 to +44), GAT1 (–787 to +48), UGA35 (–393 to +51) and UGA3 (–261 to +24) genes were fused in-frame to the lacZ gene lacking its first seven codons, in the plasmid YEP357 (Myers et al., 1986). This plasmid carries the URA3 selectable marker complementing the uracil auxotrophy of the yeast strains used. DNA fragments were generated by PCR amplification using 1278b genomic DNA as template. Primers used in these constructions are listed in Table 1. All fusion plasmids were verified by DNA sequence analysis. Escherichia coli DH5 was used to amplify and maintain the plasmids.
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(i.e. without the UASGATA sequence) and UAS (i.e. without the UASGATA and UASGABA sequences) (see Table 1
and Fig. 5) fused to the lacZ reporter gene were also generated using the strategy described above.
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. Briefly, two PCRs, using primers mut1 and F-UGA4 or primers mut2 and R-UGA4 and the fusion plasmid carrying UGA4-lacZ as template, were performed. Primers mut1 and mut2 (Table 1) contain the specific pre-determined mutation (Fig. 5a), located in a central segment. After the two products were combined, denatured and allowed to reanneal, the DNA polymerase extended the 3' end of heteroduplexes with recessed 3' ends. Thereafter, a full-length product (UASGABAmut) with the introduced mutation in a central segment was amplified by PCR using the outer primers F-UGA4 and R-UGA4 and then it was fused to the lacZ gene in YEP357.
-Galactosidase assays.
Cells were grown on the indicated media to OD570 0.5–0.9, then harvested and transferred to the same fresh medium with or without 0.1 mM GABA. An aliquot (10 ml) of each culture was collected by centrifugation after 2 h incubation at 30 °C and resuspended in 2 ml buffer Z (Miller, 1972). -Galactosidase activity measured according to Miller (1972) was expressed as Miller units. Results are shown as mean±standard deviation of duplicates within a representative assay. At least duplicate assays for each of two independent transformants were performed. The deviation of these values from the mean was less than 15 %.
Fluorescence microscopy.
23344c cells transformed with the plasmid pRR482 (kindly provided by Dr T. Cooper, University of Tennessee, Memphis, USA), containing the full-length coding sequence of Gln3 fused to GFP under the GAL1 promoter, were grown on a plate of ammonium-glucose medium. Cells were picked from the plate, transferred to fresh liquid medium containing 4 % galactose and 10 mM proline as the nitrogen source and incubated for 30 min. Then cells were collected, washed and transferred again to the indicated fresh medium. After a 90 min incubation, cells from a 5 ml culture were fixed with 70 % ethanol in 50 mM Tris/HCl pH 7.5. After 1 h of incubation, an overnight RNase treatment was performed and nuclei were stained with a 50 µg ml–1 propidium iodide solution in PBS. Analysis was carried out by using a laser-scanning confocal microscope (Fluoview FV300 BS61; Olympus). Images were acquired simultaneously into acquisition channels with the FLUOVIEW FV300 (version 3.3) acquisition/analyser program. Photographs were imported to Adobe Photoshop 8.0 for image management.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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-Galactosidase activity was measured in wild-type cells (strain 23344c) transformed with a plasmid carrying the 5'-regulatory region and part of the coding region of UGA4 fused in-frame to lacZ (YEP357 UGA4 : : lacZ) grown with different nitrogen and carbon sources. Both basal and GABA-induced UGA4 expression were analysed. When glucose, a glycolytic substrate, was used in the presence of the poor nitrogen source proline, the basal expression level was low and significant GABA induction was detected, whereas in the presence of ammonium, a rich nitrogen source, both basal and GABA-induced levels were repressed (Fig. 1). These were the expected results since UGA4 is an inducible gene and it is subject to NCR (Talibi et al., 1995). When the carbon source was acetate, a gluconeogenic substrate, basal expression levels in cells grown in derepressed conditions (i.e. proline as nitrogen source) were higher than those observed in cells from glucose-proline medium and there was no significant GABA induction. NCR was still observed when acetate was the carbon source. These results show that UGA4 is not only regulated by the nitrogen source, as has been extensively described, but also by the carbon source.
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Firstly, the expression of the four GATA factors in wild-type cells grown with either glucose or acetate was determined using -galactosidase assays. These experiments were performed using proline as the nitrogen source since expression values obtained with ammonium were too low to detect any differences (data not shown). A high expression of UGA43 and a low expression of GZF3 were observed and they did not vary with the carbon source (Table 2). Thus, changes in expression of the negative GATA factors do not explain the observed variation in UGA4 expression.
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) and GLN3 expression (compare Fig. 1 and Table 2).
It has been extensively described that UGA4 expression is, at least in part, the result of the competition between positive and negative GATA factors for the binding to the UASGATA element (Andre et al., 1995; Cunningham et al., 1994). Gat1 and Gzf3 regulate UGA4 expression in the presence of a preferred nitrogen source (Coffman et al., 1997; Soussi-Boudekou et al., 1997) while Gln3 and Uga43 are the main GATA factors acting on the UASGATA element of the UGA4 promoter in our experimental conditions, i.e. proline-glucose medium. To determine if the absence of GABA induction of UGA4 gene in cells grown on acetate is due to a strong binding of the repressor Uga43 to UASGATA, UGA4 expression was measured in cells deficient in this negative factor. As expected, UGA4 levels were high in uga43 cells grown on glucose even in the absence of GABA; however, in uga43 cells grown on acetate, values were similar to those obtained in wild-type cells (Table 3). These data clearly show that the effect of carbon source on UGA4 does not depend on Uga43.
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). As expected, in wild-type cells grown on glucose, Gln3 was mainly observed in the nucleus. In acetate-grown cells, GFP fluorescence was preferentially seen in the nucleus, although some fluorescence was detected in the cytoplasm. In cells incubated in glucose or acetate the protein Gln3-GFP was overexpressed. As expression of this fusion protein is driven by GAL1, when cells were transferred to glucose the shut-off of the promoter was probably much more drastic than in acetate. In this case, the amount of Gln3-GFP in acetate-grown cells would be higher than in glucose-grown cells. In any case, since the fluorescence was mainly observed in the nucleus, the absence of induction of UGA4 gene in acetate medium can not be attributed to the absence of Gln3 in the nucleus. Although the Gln3 localization patterns were slightly different, the observation of a large number of cells from independent experiments, where several Gln3-GFP expression levels were assayed, led us to the belief that carbon source may regulate Gln3 intracellular localization.
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strain irrespective of the carbon source, whereas the deletion of GAT1 did not seem to affect UGA4 expression (Fig. 3a, b). Interestingly, in the double mutant gln3 gat1 the expression levels of UGA4 were similar to those observed in wild-type cells. This apparent discrepancy was explained by analysing the expression of each negative GATA factor in these strains (Fig. 4a–d). The data show that in gln3 cells there was significant expression of the negative factor UGA43 while in gln3 gat1 cells almost no expression of both negative factors was observed, allowing the recovery of UGA4 expression levels. In other words, the absence of the two activators is compensated by the simultaneous absence of the two repressors. It must be noted that in the double mutant strain (gln3 gat1), when both positive GATA factors were absent and the expression of the negative ones was negligible, the expression profiles of UGA4 were significantly different depending on the carbon source: UGA4 levels were lower, and no GABA induction was observed, in cells from acetate compared to those from glucose (Fig. 3).
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Effect of transcription factors acting through the UASGABA element in the UGA4 promoter
The transcription factors Uga3 and Uga35 regulate UGA4 expression, acting through the UASGABA element. Thus, the expression of these factors in wild-type cells was analysed in order to establish their involvement in UGA4 regulation by carbon source. UGA35 levels did not vary and were very low on both carbon sources (less than 25 Miller units) whereas UGA3 levels in glucose medium were three times higher than those measured in acetate medium (160 Miller units in glucose and 53 Miller units in acetate).
Results of UGA4 expression in strains deficient in UGA35 and UGA3 were not reproducible although always low. It must be noted that these strains do not grow well in minimal media. Thus, the involvement of Uga3 in the effect of the carbon source on UGA4 gene (i.e. GABA induction in glucose but not in acetate) could not be determined by this methodology.
Role of the UAS elements in the response of UGA4 to carbon source
In order to establish the DNA sequences participating in carbon regulation of UGA4, modifications in the promoter were introduced and cloned upstream of lacZ. Expression driven by a 5' deletion of the UGA4 promoter lacking the UASGATA element in wild-type cells was lower than when the whole promoter was used but the effect of the carbon source remained unchanged (Fig. 5a, b, c). These results indicate that other elements besides GATA participate in this regulation. No differences between wild-type cells grown with glucose or acetate were observed in lacZ expression driven by a 5' deletion of the UGA4 promoter lacking both UASGATA and UASGABA elements (Fig. 5a, b, d). Taken together these results indicate that the UGA4 DNA sequence –406 to –385 is involved in carbon regulation. Expression levels driven by UASGABAmut were high with both glucose and acetate, indicating that this element is responsible for carbon regulation (Fig. 5a, b, e). Moreover, a repressor seems to be acting on the native UASGABA element (compare Fig. 5b, e).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Kuruvilla et al. (2002), dissecting glucose signalling in yeast, found a set of genes regulated by carbon source but UGA4 was not one of them. Moreover, this research group postulated that carbon and nitrogen quality signal preferentially through the multiprocessing Tor proteins to Gat1 and Gln3, respectively (Kuruvilla et al., 2001). Our results do not agree with these findings since the activity of Gat1 on UGA4 does not seem to depend on the carbon source, wheras Gln3 activity is clearly regulated by carbon quality.
We found that in the presence of the rich carbon source glucose UGA4 expression is low and a significant increase of this expression is observed when the inducer GABA is added. In contrast, UGA4 expression in cells grown on the non-fermentable carbon source acetate is higher than that observed in glucose-grown cells and it is not dependent on the presence of GABA. We conclude that the expression of the GATA factor Gln3 is also modulated by the carbon source. Moreover, the slight changes in the subcellular localization patterns observed suggest that Gln3 activity could be also regulated by carbon source at this level. Thus, UGA4 expression must be affected by the different patterns of Gln3 expression and it probably responds to changes in Gln3 localization too. However, there is another pathway participating in the regulation of UGA4 by carbon source since in the absence of the four GATA factors or in the absence of the UASGATA element, UGA4 still responds to the carbon source. Our results also show that the UASGABA element is the target of factors acting in response to the quality of the carbon source since expression driven by the promoter with a mutated UASGABA becomes independent of the carbon source. Moreover, results using this mutated promoter clearly show that there is a negative factor acting on UASGABA and its activity depends on the carbon source. It is known that, to be effective, UASGABA requires two positive-acting proteins, namely pathway-specific Uga3p and pleiotropic Uga35p (Dal81p/DurLp) (Talibi et al., 1995). Thus two possibilities may arise in the light of this new evidence. The first one is that Uga3 and/or Uga35 may have a negative influence on UGA4 transcription. Our results argue against a direct negative function of these factors since UGA4 expression levels detected in cells deficient in Uga3 or Uga35, although not reproducible, were always lower than those in wild-type cells. The second possibility would be the action, not yet described, of another transcription factor on UASGABA. Even though the participation of Leu3 in UGA4 transcription has not been reported, its consensus site for the binding to DNA overlaps the UASGABA element, suggesting that this factor may be the negative factor operating in UGA4 regulation. Moreover, Boer et al. (2005) recently reported the impact of the LEU3 deletion on transcriptional regulation of nitrogen metabolism in cells under different growth conditions; they found an increase in UGA4 and UGA3 transcription. The results presented in this work and preliminary results recently obtained in our laboratory together with data from Boer et al. (2005) support our present hypothesis which is that the interaction of Uga3 and Uga35 with others factors (protein or effector molecules) results in the formation of a repressor complex that acts on UASGABA in a way that depends on the carbon source.
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ACKNOWLEDGEMENTS |
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Edited by: D. Burke
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 31 May 2007;
revised 3 July 2007;
accepted 16 July 2007.
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