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Abstract
Post-translational modification by small ubiquitin-like modifier (Sumo) regulates many cellular processes, including the adaptive response to various types of stress, referred to as the Sumo stress response (SSR). However, it remains unclear whether the SSR involves a common set of core proteins regardless of the type of stress or whether each particular type of stress induces a stress-specific SSR that targets a unique, largely nonoverlapping set of Sumo substrates. In this study, we used MS and a Gene Ontology approach to identify differentially sumoylated proteins during heat stress, hyperosmotic stress, oxidative stress, nitrogen starvation, and DNA alkylation in Saccharomyces cerevisiae cells. Our results indicate that each stress triggers a specific SSR signature centered on proteins involved in transcription, translation, and chromatin regulation. Strikingly, whereas the various stress-specific SSRs were largely nonoverlapping, all types of stress tested here resulted in desumoylation of subunits of RNA polymerase III, which correlated with a decrease in tRNA synthesis. We conclude that desumoylation and subsequent inhibition of RNA polymerase III constitutes the core of all stress-specific SSRs in yeast.
Highlights
Post-translational modification by small ubiquitin-like modifier (Sumo) regulates many cellular processes, including the adaptive response to various types of stress, referred to as the Sumo stress response (SSR)
Comparative Gene Ontology (GO) analysis of differentially sumoylated substrates revealed that proteins that were differentially sumoylated upon heat shock, hyperosmotic stress, and nitrogen starvation were mainly involved in chromatin organization, whereas DNA alkylation and oxidative stress resulted in differential sumoylation of the translation machinery (Fig. 1F)
We previously reported that Rpc82 sumoylation, but not Ret1 SUMOylation, was necessary to promote RNAPIII assembly and transcriptional activity at class III genes [23]. tRNA molecules are transcribed as precursors that undergo sequential post-transcriptional modifications to generate mature tRNAs
Summary
To better define the S. cerevisiae SSR, we performed affinity purification combined with MS to identify Sumo stress targets (SSTs), i.e. sets of differentially sumoylated proteins in various stress conditions. Comparative GO (biological process) analysis of differentially sumoylated substrates revealed that proteins that were differentially sumoylated upon heat shock, hyperosmotic stress, and nitrogen starvation were mainly involved in chromatin organization, whereas DNA alkylation and oxidative stress resulted in differential sumoylation of the translation machinery (Fig. 1F). A prominent group of differentially sumoylated proteins included transcription factors previously shown to participate in general stress responses, including Crz, Asg, and Yhb (28 –30), as well as the osmotic stressregulated transcription factor Sko1 [31] In addition to these DNA sequence-specific transcription factors, we found that several subunits of chromatin silencing and remodeling complexes are Sumo targets, such as the RSC (remodeling the structure of chromatin)–type complex, and two SWI/SNF superfamily-type complexes, Ino and Swr (Fig. 2B and Tables S1 and S2). A unique feature of the nitrogen starvation stress response was an apparent increase in sumoylation of multiple subunits of the mitochondrial respiratory chain, with the notable exception of Gcv (glycine decarboxylase), which was desumoylated (Tables S1 and S2)
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