Reorganization of budding yeast cytoplasm upon energy depletion

Marini, Guendalina; Nüske, Elisabeth; Leng, Weihua; Alberti, Simon; Pigino, Gaia

doi:10.1091/mbc.e20-02-0125

Cited by 42 publications

(38 citation statements)

References 79 publications

(117 reference statements)

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“…In the presence of a crowding agent, assemblies already formed at pH 6.5 as opposed to a pH 6.25 in the absence of crowder. In agreement with this, a related study found that glucose starvation and energy depletion also increase molecular crowding conditions inside cells (Marini et al, 2020). To investigate whether changes in crowding conditions alone are sufficient to induce eIF2B assembly in cells, we exposed cells to different osmotic stress conditions.…”

Section: Eif2b Assembly Involves Bundling Into Filamentssupporting

confidence: 62%

“…We found that mutations in Gcn3 and Gcd1 drastically altered eIF2B filament formation, which indicates that these subunits are involved in stacking. This hypothesis is further supported by (i) the crystal structure of eIF2B from S chizosaccharomyces pombe , which shows that eIF2B dimerizes via its alpha subunit (Gcn3) ( Kashiwagi et al, 2016 ), (ii) work on human eIF2B and the regulatory subcomplex of S. cerevisiae eIF2B where a similar interaction of eIF2B- α was proposed ( Bogorad et al, 2014 ; Wortham et al, 2014 ), (iii) a study by Gordiyenko et al who proposed dimerization of S. cerevisiae eIF2B pentamers via Gcd1 and Gcd6 ⎯ the catalytical subcomplex ( Gordiyenko et al, 2014 ), and (iv) data from Marini et al, who performed a comparison between the Cryo-EM structure of the eIF2B decamer and the in situ tomographic reconstruction of the eIF2B filament, which suggests a decamer-to-decamer interaction through the Gcd6 subunit ( Marini et al, 2020 ). Altogether, this suggests that eIF2B stacking occurs via dimerization of the regulatory subcomplex on one side and the catalytic subcomplex on the other side.…”

Section: Discussionmentioning

confidence: 99%

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Filament formation by the translation factor eIF2B regulates protein synthesis in starved cells

et al. 2020

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Cells exposed to starvation have to adjust their metabolism to conserve energy and protect themselves. Protein synthesis is one of the major energy-consuming processes and as such has to be tightly controlled. Many mechanistic details about how starved cells regulate the process of protein synthesis are still unknown. Here, we report that the essential translation initiation factor eIF2B forms filaments in starved budding yeast cells. We demonstrate that filamentation is triggered by starvation-induced acidification of the cytosol, which is caused by an influx of protons from the extracellular environment. We show that filament assembly by eIF2B is necessary for rapid and efficient downregulation of translation. Importantly, this mechanism does not require the kinase Gcn2. Furthermore, analysis of sitespecific variants suggests that eIF2B assembly results in enzymatically inactive filaments that promote stress survival and fast recovery of cells from starvation. We propose that translation regulation through filament assembly is an efficient mechanism that allows yeast cells to adapt to fluctuating environments.

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Section: Eif2b Assembly Involves Bundling Into Filamentssupporting

confidence: 62%

Section: Discussionmentioning

confidence: 99%

Filament formation by the translation factor eIF2B regulates protein synthesis in starved cells

et al. 2020

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“…As a result, stationary cells have more LDs than log-phase, dividing cells. A recent report showed that the number of LDs increased even when yeast cells were given a short period of glucose starvation by replacing glucose with a non-hydrolysable glucose analogue [32].…”

Section: Discussionmentioning

confidence: 99%

Membrane and lipid metabolism plays an important role in desiccation resistance in the yeast Saccharomyces cerevisiae

Ren

Brenner

Boothby

et al. 2020

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Background: Anhydrobiotes, such as the yeast Saccharomyces cerevisiae , are capable of surviving almost total loss of water. Desiccation tolerance requires an interplay of multiple events, including preserving the protein function and membrane integrity, preventing and mitigating oxidative stress, maintaining certain level of energy required for cellular activities in the desiccated state. Many of these crucial processes can be controlled and modulated at the level of organelle morphology and dynamics. However, little is understood about what organelle perturbations manifest in desiccation-sensitive cells as a consequence of drying or how this differs from organelle biology in desiccation-tolerant organisms undergoing anhydrobiosis. Results: In this study, electron and optical microscopy was used to examine the dynamic changes of yeast cells during the desiccation process. Dramatic structural changes were observed during the desiccation process, including the diminishing of vacuoles, and increase and then decrease of lipid droplets as well as a decrease in mitochondria and mitochondrial cristae and an increase of ER membrane, which is likely caused by ER stress and unfolded protein response. The survival rate was significantly decreased in mutants that are defective in lipid droplet biosynthesis, or cells treated with cerulenin, an inhibitor of fatty acid synthesis. Conclusion: Our study suggests that the metabolism of lipid droplets and membrane may play an important role in yeast desiccation tolerance by providing cells with energy and possibly metabolic water. Additionally, the decrease in mitochondria and cristae coupled with an initial increase and then drop in lipid droplets number is indicative of a cellular response to reduce the production of reactive oxygen species.

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“…As a result, stationary cells have more LDs than log-phase dividing cells. A recent report showed that the number of LDs increased even when yeast cells were given a short period of glucose starvation by replacing glucose with a non-hydrolysable glucose analogue [43]. At stationary phase, fatty acids are released slowly from triglycerides and degraded via β-oxidation, to provide energy necessary for cellular maintenance [38].…”

Section: Discussionmentioning

confidence: 99%

Membrane and lipid metabolism plays an important role in desiccation resistance in the yeast Saccharomyces cerevisiae

Ren

Brenner

Boothby

et al. 2020

Preprint

View full text Add to dashboard Cite

BackgroundAnhydrobiotes, such as the yeast Saccharomyces cerevisiae, are capable of surviving almost total loss of water. Desiccation tolerance requires an interplay of multiple events, including preserving the protein function and membrane integrity, preventing and mitigating oxidative stress, maintaining certain level of energy required for cellular activities in the desiccated state. Many of these crucial processes can be controlled and modulated at the level of organelle morphology and dynamics. However, little is understood about what organelle perturbations manifest in desiccation-sensitive cells as a consequence of drying or how this differs from organelle biology in desiccation-tolerant organisms undergoing anhydrobiosis.ResultsIn this study, electron and optical microscopy was used to examine the dynamic changes of yeast cells during the desiccation process. Dramatic structural changes were observed during the desiccation process, including the diminishing of vacuoles, decrease of lipid droplets, decrease in mitochondrial cristae and increase of ER membrane, which is likely caused by ER stress and unfolded protein response. The survival rate was significantly decreased in mutants that are defective in lipid droplet biosynthesis, or cells treated with cerulenin, an inhibitor of fatty acid synthesis.ConclusionOur study suggests that the metabolism of lipid droplets and membrane may play an important role in yeast desiccation tolerance by providing cells with energy and possibly metabolic water. Additionally, the decrease in mitochondrial cristae coupled with a decrease in lipid droplets is indicative of a cellular response to reduce the production of reactive oxygen species.

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Reorganization of budding yeast cytoplasm upon energy depletion

Cited by 42 publications

References 79 publications

Filament formation by the translation factor eIF2B regulates protein synthesis in starved cells

Filament formation by the translation factor eIF2B regulates protein synthesis in starved cells

Membrane and lipid metabolism plays an important role in desiccation resistance in the yeast Saccharomyces cerevisiae

Membrane and lipid metabolism plays an important role in desiccation resistance in the yeast Saccharomyces cerevisiae

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