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Vesicular Trafficking Systems Impact TORC1-Controlled Transcriptional Programs in Saccharomyces cerevisiae.

ABSTRACT: The Target of Rapamycin Complex I (TORC1) orchestrates global reprogramming of transcriptional programs in response to myriad environmental conditions, yet, despite the commonality of the TORC1 complex components, different TORC1-inhibitory conditions do not elicit a uniform transcriptional response. In Saccharomyces cerevisiae, TORC1 regulates the expression of nitrogen catabolite repressed (NCR) genes by controlling the nuclear translocation of the NCR transactivator Gln3. Moreover, Golgi-to-endosome trafficking was shown to be required for nuclear translocation of Gln3 upon a shift from rich medium to the poor nitrogen source proline, but not upon rapamycin treatment. Here, we employed microarray profiling to survey the full impact of the vesicular trafficking system on yeast TORC1-orchestrated transcriptional programs. In addition to the NCR genes, we found that ribosomal protein, ribosome biogenesis, phosphate-responsive, and sulfur-containing amino acid metabolism genes are perturbed by disruption of Golgi-to-endosome trafficking following a nutritional shift from rich to poor nitrogen source medium, but not upon rapamycin treatment. Similar to Gln3, defects in Golgi-to-endosome trafficking significantly delayed cytoplasmic-nuclear translocation of Sfp1, but did not detectably affect the cytoplasmic-nuclear or nuclear-cytoplasmic translocation of Met4, which are the transactivators of these genes. Thus, Golgi-to-endosome trafficking defects perturb TORC1 transcriptional programs via multiple mechanisms. Our findings further delineate the downstream transcriptional responses of TORC1 inhibition by rapamycin compared with a nitrogen quality downshift. Given the conservation of both TORC1 and endomembrane networks throughout eukaryotes, our findings may also have implications for TORC1-mediated responses to nutritional cues in mammals and other eukaryotes.

SUBMITTER: Kingsbury JM

PROVIDER: S-EPMC4777127 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Vesicular Trafficking Systems Impact TORC1-Controlled Transcriptional Programs in Saccharomyces cerevisiae.

Kingsbury Joanne M JM Cardenas Maria E ME

G3 (Bethesda, Md.) 20160106 3

The Target of Rapamycin Complex I (TORC1) orchestrates global reprogramming of transcriptional programs in response to myriad environmental conditions, yet, despite the commonality of the TORC1 complex components, different TORC1-inhibitory conditions do not elicit a uniform transcriptional response. In Saccharomyces cerevisiae, TORC1 regulates the expression of nitrogen catabolite repressed (NCR) genes by controlling the nuclear translocation of the NCR transactivator Gln3. Moreover, Golgi-to-e ...[more]

PMID: 26739646

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Project description:The ability to survive stress conditions is important for every living cell. Some stresses can affect not only current cell well-being, but may have far-reaching consequences. Uncurbed oxidative stress can cause DNA damage and the decrease in cell survival and/or increase in mutation rate. Some substances generating oxidative damage in the cell act mainly on DNA. Radiomimetic zeocin is a chemoenzyme that causes oxidative damage in DNA, inducing predominantly single or double strand breaks. Such lesions can subsequently lead to chromosomal rearrangements in genomic DNA, especially in diploid cells in which each sequence has its duplicate in the homologous chromosome. In a global screen for mutants oversensitive to zeocin, we selected 136 genes whose deletion causes the decrease in survival of diploid Saccharomyces cerevisiae cells exposed to this compound. The screen revealed numerous genes connected with stress response, including response to DNA damage stimulus; DNA repair genes, especially connected with homologous recombination and telomere maintenance; genes involved in cell cycle progression, chiefly in control of cell divisions checkpoints, both meiotic and mitotic; and genes involved in remodeling of chromatin. Notably, our screen also demonstrated the involvement of vesicular trafficking system in cell protection against DNA damage. Presented data imply vesicular system in various pathways of cell protection from zeocin-dependent damage, including the role in detoxification and probably more direct role in genome maintenance processes. We show, that cells with vesicular trafficking dysfunction are unable to repair zeocin induced damage, accumulate Rad52 foci and frequently possess an atypical DNA content. Therefore, we postulate that functional vesicular trafficking is crucial for sustaining integral genome. We believe that numerous new genes implicated in genome maintenance after genotoxic oxidative stress, together with newly discovered vesicular trafficking link to genome integrity, will help revealing novel molecular processes involved in the genome stability of diploid cells.

Dataset Information

Vesicular Trafficking Systems Impact TORC1-Controlled Transcriptional Programs in Saccharomyces cerevisiae.

Publications

Vesicular Trafficking Systems Impact TORC1-Controlled Transcriptional Programs in Saccharomyces cerevisiae.

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