Vgl1, a multi-KH domain protein, is a novel component of the fission yeast stress granules required for cell survival under thermal stress

Wen, Wei-Ling; Stevenson, Abigail L.; Wang, Chunyu; Chen, Hsiang-Ju; Kearsey, Stephen; Norbury, Chris J.; Watt, Stephen; Bähler, Jürg; Wang, Shao-Win

doi:10.1093/nar/gkq555

Cited by 35 publications

(58 citation statements)

References 36 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Cytoplasmic vigilin plays a key role in mRNA stabilization and positively regulates translation, notably in response to stress (17)(18)(19)46). Interestingly, we observed that CF airway neutrophils undergo marked changes in their transcriptional profile compared with CF blood neutrophils (Laval et al, manuscript in preparation), consistent with reprogramming (3,39).…”

Section: Discussionsupporting

confidence: 52%

Metabolic Adaptation of Neutrophils in Cystic Fibrosis Airways Involves Distinct Shifts in Nutrient Transporter Expression

Laval

Touhami

Herzenberg

et al. 2013

The Journal of Immunology

View full text Add to dashboard Cite

Inflammatory conditions can profoundly alter human neutrophils, a leukocyte subset generally viewed as terminally differentiated and catabolic. In cystic fibrosis (CF) patients, neutrophils recruited to CF airways show active exocytosis and sustained phosphorylation of prosurvival, metabolic pathways. Because the CF airway lumen is also characterized by high levels of free glucose and amino acids, we compared surface expression of Glut1 (glucose) and ASCT2 (neutral amino acids) transporters, as well as that of PiT1 and PiT2 (inorganic phosphate transporters), in blood and airway neutrophils, using specific retroviral envelope-derived ligands. Neither nutrient transporter expression nor glucose uptake was altered on blood neutrophils from CF patients compared with healthy controls. Notably, however, airway neutrophils of CF patients had higher levels of PiT1 and Glut1 and increased glucose uptake compared with their blood counterparts. Based on primary granule exocytosis and scatter profiles, CF airway neutrophils could be divided into two subsets, with one of the subsets characterized by more salient increases in Glut1, ASCT2, PiT1, and PiT2 expression. Moreover, in vitro exocytosis assays of blood neutrophils suggest that surface nutrient transporter expression is not directly associated with primary (or secondary) granule exocytosis. Although expression of nutrient transporters on CF blood or airway neutrophils was not altered by genotype, age, gender, or Pseudomonas aeruginosa infection, oral steroid treatment decreased Glut1 and PiT2 levels in blood neutrophils. Thus, neutrophils recruited from blood into the CF airway lumen display augmented cell surface nutrient transporter expression and glucose uptake, consistent with metabolic adaptation.

show abstract

Section: Discussionsupporting

confidence: 52%

Metabolic Adaptation of Neutrophils in Cystic Fibrosis Airways Involves Distinct Shifts in Nutrient Transporter Expression

Laval

Touhami

Herzenberg

et al. 2013

The Journal of Immunology

View full text Add to dashboard Cite

show abstract

“…Despite the fact that yeast SGs seem to contain most if not all components of mammalian SGs, unlike the situation in mammals, their formation is independent of eIF2a phosphorylation in the budding yeast (Grousl et al 2009). Similarly, observations from fission yeast (Wen et al 2010;Nilsson and Sunnerhagen 2011) and trypanosomes (Kramer et al 2008) show that assemblies of SGs in response to heat shock are also independent of phosphorylation of eIF2a. It appears that other pathways contribute to formation of SGs in several organisms.…”

Section: Introductionmentioning

confidence: 79%

“…Polyribosomes were obtained as previously described (Wen et al 2010). CHX (100 mg/mL) was added to 50 mL of cultures at an OD 600 of 0.5 grown at 30°C.…”

Section: Polyribosome Profile Analysismentioning

confidence: 99%

See 1 more Smart Citation

Analysis of stress granule assembly in Schizosaccharomyces pombe

Wang¹,

Wen²,

Nilsson³

et al. 2012

RNA

View full text Add to dashboard Cite

Stress granules (SGs) are cytoplasmic aggregates of RNA and proteins in eukaryotic cells that are rapidly induced in response to environmental stress, but are not seen in cells growing under favorable conditions. SGs have been primarily studied in mammalian cells. The existence of SGs in the fission yeast and the distantly related budding yeast was demonstrated only recently. In both species, they contain many orthologs of the proteins seen in mammalian SGs. In this study, we have characterized these proteins and determined their involvement in the assembly of fission yeast SGs, in particular, the homolog of human G3BP proteins. G3BP interacts with the deubiquitinating protease USP10 and plays an important role in the assembly of SGs. We have also identified Ubp3, an ortholog of USP10, as an interaction partner of the fission yeast G3BP-like protein Nxt3 and required for its stability. Under thermal stress, like their human orthologs, both Nxt3 and Ubp3 rapidly relocalize to cytoplasmic foci that contain the SG marker poly(A)-binding protein Pabp. However, in contrast to G3BP1 and USP10, neither deletion nor overexpression of nxt3 + or ubp3 + affected the assembly of fission yeast SGs as judged by the relocalization of Pabp. Similar results were observed in mutants defective in orthologs of SG components that are known to affect SG assembly in human and in budding yeast, such as ataxia-2 and TIA-like proteins. Together, our data indicate that despite similar protein compositions, the underlying molecular mechanisms for the assembly of SGs could be distinct between species.

show abstract

“…Conditions for growth, maintenance, and genetic manipulation of fission yeast were as described previously (10). A complete list of the strains used in this study is given in Table S1 in the supplemental material.…”

Section: Methodsmentioning

confidence: 99%

Pdc1 Functions in the Assembly of P Bodies in Schizosaccharomyces pombe

Wang

Chen

Wang

2013

Molecular and Cellular Biology

View full text Add to dashboard Cite

P bodies are cytoplasmic RNA granules containing the Dcp1-Dcp2 decapping enzymes where mRNA decay can occur. Here, we describe the characterization of P bodies in the fission yeast Schizosaccharomyces pombe. Most information on the property and function of P bodies stems from studies in the distantly related budding yeast Saccharomyces cerevisiae, and Edc3 was identified as a scaffold protein required for P-body assembly. However, we found that, unlike in S. cerevisiae, fission yeast Edc3 was dispensable for P-body formation. Pdc1, a novel partner of the fission yeast decapping enzyme, with a limited similarity to plant Edc4/Varicose that is required for the assembly of P bodies, was identified (tandem affinity purification-matrix-assisted laser desorption ionization tandem mass spectrometry [TAP-MALDI MS/MS]). Pdc1 interacts with Dcp2 through its C terminus and contains a coiled-coil region for self-interaction to mediate P-body formation. In line with the model that Pdc1 cross-bridges different proteins, additional interactions can be demonstrated with components such as Edc3 and Ste13. Although Pdc1 is not required for the interaction between Dcp1 and Dcp2, our data suggest that Pdc1 acts as a functional homologue of Edc4, a third component of the decapping enzymes that is thought to be absent from fungi. Together, these results highlight the diverse Pbody protein compositions between different species and might help to provide insight into their evolutionary paths. C ytoplasmic processing bodies (P bodies) are dynamic RNA protein aggregates that play critical roles in mRNA degradation, nonsense-mediated mRNA decay, translational repression, and RNA-mediated gene silencing (reviewed in reference 1). Because several components of P bodies, such as the decapping enzyme and its coactivators, are found in both yeast and mammalian cells, it is believed that P bodies are evolutionarily conserved among eukaryotes. However, a detailed study of P bodies in the fission yeast has not yet been described.The decapping of mRNAs, which occurs inside P bodies, represents a critical step in mRNA turnover and is therefore tightly regulated. The decapping enzyme Dcp2 requires additional proteins for full activity and/or stability. These proteins are generally termed decapping coactivators (or enhancers of decapping [EDCs]) although they may activate decapping by different mechanisms (2). In Saccharomyces cerevisiae, proteins that activate decapping include Dcp1, enhancer of decapping 1 to 3 (Edc1-3), the heptameric Lsm1-7 complex, DEXH/D-box RNA helicase 1 (Dhh1; RCK/p54 in mammals), and Pat1 (3). Dcp1 interacts directly with Dcp2 and is required for decapping in vivo (4). All of these proteins colocalize to P bodies.In human cells, the interaction between Dcp1 and Dcp2 appears to be mediated by the decapping activator Edc4 (also known as Ge-1 or Hedls, for human enhancer of decapping large subunit) (5, 6). Edc4, Dcp1, and Dcp2 are part of a multimeric protein complex, which also includes Edc3 and RCK/p54 (5). Similarly, Arabid...

show abstract

Vgl1, a multi-KH domain protein, is a novel component of the fission yeast stress granules required for cell survival under thermal stress

Cited by 35 publications

References 36 publications

Metabolic Adaptation of Neutrophils in Cystic Fibrosis Airways Involves Distinct Shifts in Nutrient Transporter Expression

Metabolic Adaptation of Neutrophils in Cystic Fibrosis Airways Involves Distinct Shifts in Nutrient Transporter Expression

Analysis of stress granule assembly in Schizosaccharomyces pombe

Pdc1 Functions in the Assembly of P Bodies in Schizosaccharomyces pombe

Contact Info

Product

Resources

About