A role for eisosomes in maintenance of plasma membrane phosphoinositide levels

Fröhlich, Florian; Christiano, Romain; Olson, Daniel K.; Alcázar-Román, Abel R.; DeCamilli, Pietro; Walther, Tobias C.

doi:10.1091/mbc.e13-11-0639

Cited by 45 publications

(69 citation statements)

References 46 publications

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“…The primary component of yeast eisosomes is the BAR domain protein Pil1, which directly binds lipids at the membrane to generate invaginations (Kabeche et al, 2011(Kabeche et al, , 2014Karotki et al, 2011;Moreira et al, 2009;Olivera-Couto et al, 2011;Stradalova et al, 2009;Ziółkowska et al, 2011). Recent studies have linked eisosome function with the control of signaling pathways (Berchtold et al, 2012;Frohlich et al, 2014;Kabeche et al, 2014), but we noted that their architecture possesses the capacity to act as a membrane reservoir. Here, we devised a singlecell assay to observe rapid expansion of the yeast plasma membrane in the absence of a cell wall and found that eisosomes display properties that suggest they act as membrane reservoirs that are required for increases in cell surface area.…”

Section: Introductionmentioning

confidence: 84%

Eisosomes provide membrane reservoirs for rapid expansion of the yeast plasma membrane

Kabeche

Howard

Moseley

2015

Journal of Cell Science

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Cell surface area rapidly increases during mechanical and hypoosmotic stresses. Such expansion of the plasma membrane requires 'membrane reservoirs' that provide surface area and buffer membrane tension, but the sources of this membrane remain poorly understood. In principle, the flattening of invaginations and buds within the plasma membrane could provide this additional surface area, as recently shown for caveolae in animal cells. Here, we used microfluidics to study the rapid expansion of the yeast plasma membrane in protoplasts, which lack the rigid cell wall. To survive hypoosmotic stress, yeast cell protoplasts required eisosomes, protein-based structures that generate long invaginations at the plasma membrane. Both budding yeast and fission yeast protoplasts lacking eisosomes were unable to expand like wild-type protoplasts during hypoosmotic stress, and subsequently lysed. By performing quantitative fluorescence microscopy on single protoplasts, we also found that eisosomes disassembled as surface area increased. During this process, invaginations generated by eisosomes at the plasma membrane became flattened, as visualized by scanning electron microscopy. We propose that eisosomes serve as tensiondependent membrane reservoirs for expansion of yeast cells in an analogous manner to caveolae in animal cells.

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Section: Introductionmentioning

confidence: 84%

Eisosomes provide membrane reservoirs for rapid expansion of the yeast plasma membrane

Kabeche

Howard

Moseley

2015

Journal of Cell Science

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“…PI(4,5)P 2 Is Important for Cell Integrity Pathway ActivationEisosomes function with the lipid phosphatase synaptojanin to down-regulate PI(4,5)P 2 levels in both budding yeast and fission yeast (8,10). We hypothesized that eisosomes control the cell integrity pathway through their role in PI(4,5)P 2 hydrolysis.…”

Section: Eisosome Mutants Suppress Torc2 Mutations Through Cellmentioning

confidence: 99%

“…Genetic screens in fission yeast demonstrated that eisosome proteins function with Syj1, a synaptojanin protein that hydrolyzes PI(4,5)P 2 , 2 and its putative ligand Tax4 (8). Furthermore, budding yeast eisosomes were shown to recruit synaptojanin to the plasma membrane, and eisosome mutants exhibited elevated levels of PI(4,5)P 2 (10). These studies have provided a framework to understand how eisosomes, which bind tightly to lipids at the plasma membrane, contribute to PI(4,5)P 2 hydrolysis with specific synaptojanin isoforms.…”

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confidence: 94%

Eisosomes Regulate Phosphatidylinositol 4,5-Bisphosphate (PI(4,5)P2) Cortical Clusters and Mitogen-activated Protein (MAP) Kinase Signaling upon Osmotic Stress

Kabeche

Madrid

Cansado

et al. 2015

Journal of Biological Chemistry

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Background: Eisosomes are protein-based structures of unknown function at the plasma membrane of yeast cells. Results: Eisosomes are shown to organize lipid domains that promote signal transduction during environmental stress. Conclusion: Environmental stress induces clustering of signal transduction lipids and proteins. Significance: A new mechanism to relay extracellular cues for intracellular responses is provided.

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“…One possibility is that striation variability may reflect a switch in "levels of engagement" between the eisosomal lipids and their underlying organizing systems. If this is the case, the variability could be a morphological reflection of (some of) the signal transduction properties attributed to eisosomes (19,20,22). Walther and colleagues (30,83) have suggested analogies between eisosomes and caveolae.…”

Section: Discussionmentioning

confidence: 99%

“…These observations were brought together by Strádalová et al (5), who showed that the membrane compartment occupied by Can1p (MCC) localized to the invaginations seen with freeze fracture EM, and by Karotki et al (6), who showed that Pil1p localizes to the cytoplasmic surfaces of these invaginations. Additional proteins also associate with these punctate domains, in some cases in a transient fashion (17), and the MCC component is reportedly enriched in ergosterol (18) and influenced by phosphoinositide (6,19,20) and sphingolipid (14,17,(21)(22)(23)(24) levels. Hence, the current yeast model (25,26) proposes that Pil1p and Lsp1p, which contain membrane curvatureinducing BAR domains (6,27,28), together with Seg1p (29,30), form a submembrane complex (6) reportedly influenced by Pil1p phosphorylation (25); this complex then either creates or associates with the MCC domains, presumably inducing an inward curvature.…”

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confidence: 99%

Eisosome Ultrastructure and Evolution in Fungi, Microalgae, and Lichens

et al. 2015

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Eisosomes are among the few remaining eukaryotic cellular differentations that lack a defined function(s). These trough-shaped invaginations of the plasma membrane have largely been studied in Saccharomyces cerevisiae, in which their associated proteins, including two BAR domain proteins, have been identified, and homologues have been found throughout the fungal radiation. Using quick-freeze deep-etch electron microscopy to generate high-resolution replicas of membrane fracture faces without the use of chemical fixation, we report that eisosomes are also present in a subset of red and green microalgae as well as in the cysts of the ciliate Euplotes. Eisosome assembly is closely correlated with both the presence and the nature of cell walls. Microalgal eisosomes vary extensively in topology and internal organization. Unlike fungi, their convex fracture faces can carry lineagespecific arrays of intramembranous particles, and their concave fracture faces usually display fine striations, also seen in fungi, that are pitched at lineage-specific angles and, in some cases, adopt a broad-banded patterning. The conserved genes that encode fungal eisosome-associated proteins are not found in sequenced algal genomes, but we identified genes encoding two algal lineage-specific families of predicted BAR domain proteins, called Green-BAR and Red-BAR, that are candidate eisosome organizers. We propose a model for eisosome formation wherein (i) positively charged recognition patches first establish contact with target membrane regions and (ii) a (partial) unwinding of the coiled-coil conformation of the BAR domains then allows interactions between the hydrophobic faces of their amphipathic helices and the lipid phase of the inner membrane leaflet, generating the striated patterns.

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A role for eisosomes in maintenance of plasma membrane phosphoinositide levels

Cited by 45 publications

References 46 publications

Eisosomes provide membrane reservoirs for rapid expansion of the yeast plasma membrane

Eisosomes provide membrane reservoirs for rapid expansion of the yeast plasma membrane

Eisosomes Regulate Phosphatidylinositol 4,5-Bisphosphate (PI(4,5)P2) Cortical Clusters and Mitogen-activated Protein (MAP) Kinase Signaling upon Osmotic Stress

Eisosome Ultrastructure and Evolution in Fungi, Microalgae, and Lichens

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