mRNA decay is regulated via sequestration of the conserved 5′-3′ exoribonuclease Xrn1 at eisosome in yeast

Vaškovičová, Katarína; Awadová, Thuraya; Veselá, Petra; Balážová, Mária; Opekarová, Miroslava; Malínský, J

doi:10.1016/j.ejcb.2017.05.001

Cited by 20 publications

(21 citation statements)

References 44 publications

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“…Eisosomes also seem important in nitrogen stress-induced yeast filamentation, as Pun1, a protein essential to this process, is a Sur7-like component of EMCs (50). Last, the main mRNA decay enzyme, exoribonuclease Xrn1, is reported to accumulate in EMCs specifically after glucose (Glu) exhaustion, and this accumulation negatively regulates the activity of the enzyme during the stationary phase (51,52). Two other EMC-resident proteins, Fmp45 and Pst2, are essential for recovery from the stationary phase (53).…”

Section: Discussionmentioning

confidence: 99%

Conformation-dependent partitioning of yeast nutrient transporters into starvation-protective membrane domains

Gournas

Gkionis

Carquin

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

160

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The eukaryotic plasma membrane is compartmentalized into domains enriched in specific lipids and proteins. However, our understanding of the molecular bases and biological roles of this partitioning remains incomplete. The best-studied domain in yeast is the membrane compartment containing the arginine permease Can1 (MCC) and later found to cluster additional transporters. MCCs correspond to static, furrow-like invaginations of the plasma membrane and associate with subcortical structures named "eisosomes" that include upstream regulators of the target of rapamycin complex 2 (TORC2) in the sensing of sphingolipids and membrane stress. However, how and why Can1 and other nutrient transporters preferentially segregate in MCCs remains unknown. In this study we report that the clustering of Can1 in MCCs is dictated by its conformation, requires proper sphingolipid biosynthesis, and controls its ubiquitin-dependent endocytosis. In the substrate-free outward-open conformation, Can1 accumulates in MCCs in a manner dependent on sustained biogenesis of complex sphingolipids. An arginine transport-elicited shift to an inward-facing conformation promotes its cell-surface dissipation and makes it accessible to the ubiquitylation machinery triggering its endocytosis. We further show that under starvation conditions MCCs increase in number and size, this being dependent on the BAR domain-containing Lsp1 eisosome component. This expansion of MCCs provides protection for nutrient transporters from bulk endocytosis occurring in parallel with autophagy upon TORC1 inhibition. Our study reveals nutrient-regulated protection from endocytosis as an important role for protein partitioning into membrane domains.

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Section: Discussionmentioning

confidence: 99%

Conformation-dependent partitioning of yeast nutrient transporters into starvation-protective membrane domains

Gournas

Gkionis

Carquin

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

160

View full text Add to dashboard Cite

show abstract

“…The Nce102 and Slm1/2 proteins can move out of these domains in response to sphingolipid levels [ 21 ]. The Xrn1 exonuclease resides in eisosomes until altered nutrient conditions permit its migration to the cytoplasm where it can promote the degradation of mRNAs at P bodies [ 36 , 63 ].…”

Section: Mcc/eisosome Function In Cell Wall Synthesis and Morphogementioning

confidence: 99%

MCC/Eisosomes Regulate Cell Wall Synthesis and Stress Responses in Fungi

Foderaro

Douglas

Konopka

2017

JoF

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The fungal plasma membrane is critical for cell wall synthesis and other important processes including nutrient uptake, secretion, endocytosis, morphogenesis, and response to stress. To coordinate these diverse functions, the plasma membrane is organized into specialized compartments that vary in size, stability, and composition. One recently identified domain known as the Membrane Compartment of Can1 (MCC)/eisosome is distinctive in that it corresponds to a furrow-like invagination in the plasma membrane. MCC/eisosomes have been shown to be formed by the Bin/Amphiphysin/Rvs (BAR) domain proteins Lsp1 and Pil1 in a range of fungi. MCC/eisosome domains influence multiple cellular functions; but a very pronounced defect in cell wall synthesis has been observed for mutants with defects in MCC/eisosomes in some yeast species. For example, Candida albicans MCC/eisosome mutants display abnormal spatial regulation of cell wall synthesis, including large invaginations and altered chemical composition of the walls. Recent studies indicate that MCC/eisosomes affect cell wall synthesis in part by regulating the levels of the key regulatory lipid phosphatidylinositol 4,5-bisphosphate (PI4,5P2) in the plasma membrane. One general way MCC/eisosomes function is by acting as protected islands in the plasma membrane, since these domains are very stable. They also act as scaffolds to recruit >20 proteins. Genetic studies aimed at defining the function of the MCC/eisosome proteins have identified important roles in resistance to stress, such as resistance to oxidative stress mediated by the flavodoxin-like proteins Pst1, Pst2, Pst3 and Ycp4. Thus, MCC/eisosomes play multiple roles in plasma membrane organization that protect fungal cells from the environment.

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“…Furthermore, there are numerous examples of the stabilisation (or destabilisation) of lncRNA transcript classes under specific conditions, such as meiosis, respiration or sporulation [ 26 – 29 ], carbon source [ 14 , 30 ], metal abundance [ 31 ], and osmotic stress [ 32 ]. It was recently shown that the 5′–3′ exonuclease Xrn1p is localised to eisosomes when glucose is scarce but relocalises to the cytoplasm when glucose is present, where it degrades lncRNAs called XUTs and modulates lncRNA regulation of gene expression [ 33 ]. Whether this phenomenon constitutes primary regulation or merely “fine-tuning” of gene expression remains to be determined.…”

Section: Important Messages or Random Spam?mentioning

confidence: 99%

Long Noncoding RNAs in Yeast Cells and Differentiated Subpopulations of Yeast Colonies and Biofilms

Wilkinson

Váchová

Hlaváček

et al. 2018

Oxidative Medicine and Cellular Longevity

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We summarize current knowledge regarding regulatory functions of long noncoding RNAs (lncRNAs) in yeast, with emphasis on lncRNAs identified recently in yeast colonies and biofilms. Potential regulatory functions of these lncRNAs in differentiated cells of domesticated colonies adapted to plentiful conditions versus yeast colony biofilms are discussed. We show that specific cell types differ in their complements of lncRNA, that this complement changes over time in differentiating upper cells, and that these lncRNAs target diverse functional categories of genes in different cell subpopulations and specific colony types.

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mRNA decay is regulated via sequestration of the conserved 5′-3′ exoribonuclease Xrn1 at eisosome in yeast

Cited by 20 publications

References 44 publications

Conformation-dependent partitioning of yeast nutrient transporters into starvation-protective membrane domains

Conformation-dependent partitioning of yeast nutrient transporters into starvation-protective membrane domains

MCC/Eisosomes Regulate Cell Wall Synthesis and Stress Responses in Fungi

Long Noncoding RNAs in Yeast Cells and Differentiated Subpopulations of Yeast Colonies and Biofilms

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