Seg1 controls eisosome assembly and shape

Moreira, Karen Betancourt; Schuck, Sebastian; Schrul, Bianca; Fröhlich, Florian; Moseley, James B.; Walther, Tobias C.; Walter, Peter

doi:10.1083/jcb.201202097

Cited by 60 publications

(75 citation statements)

References 57 publications

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“…S1C,D), meaning there is no effect from pressure changes induced by the microfluidics device. Pil1 functions with the protein Sle1, which localizes to eisosomes and is required for proper eisosome assembly (Kabeche et al, 2014;Moreira et al, 2012). sle1Δ protoplasts displayed a similar defect in protoplast survival, and no additive defects were observed in pil1Δ sle1Δ double mutants (Fig.…”

Section: Resultsmentioning

confidence: 99%

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: Resultsmentioning

confidence: 99%

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

Kabeche

Howard

Moseley

2015

Journal of Cell Science

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“…In budding yeast cells, many proteins in addition to Pil1 localize at MCC/eisosomes (Fröhlich et al, 2009;Grossmann et al, 2008). By contrast, fission yeast eisosomes contain only two additional proteins: the transmembrane protein Fhn1 and the peripheral membrane protein Sle1, which are both required for proper eisosome formation in cells (Kabeche et al, 2011;Moreira et al, 2012). This suggests that fission yeast eisosomes might represent a simplified form of this prominent cellular structure.…”

Section: Introductionmentioning

confidence: 99%

A Pil1-Sle1-Syj1-Tax4 functional pathway links eisosomes with PI(4,5)P2 regulation

Kabeche

Roguev

Krogan

et al. 2014

Journal of Cell Science

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Stable compartments of the plasma membrane promote a wide range of cellular functions. In yeast cells, cytosolic structures called eisosomes generate prominent cortical invaginations of unknown function. Through a series of genetic screens in fission yeast, we found that the eisosome proteins Pil1 and Sle1 function with the synaptojanin-like lipid phosphatase Syj1 and its ligand Tax4. This genetic pathway connects eisosome function with the hydrolysis of phosphatidylinositol (4,5)-bisphosphate [PI(4,5)P 2 ] in cells. Defects in PI(4,5)P 2 regulation led to eisosome defects, and we found that the core eisosome protein Pil1 can bind to and tubulate liposomes containing PI(4,5)P 2 . Mutations in components of the Pil1-Sle1-Syj1-Tax4 pathway suppress the growth and morphology defects of TORC2 mutants, indicating that eisosome-dependent regulation of PI(4,5)P 2 feeds into signal transduction pathways. We propose that the geometry of membrane invaginations generates spatial and temporal signals for lipid-mediated signaling events in cells.

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“…The cytoplasmic protein Seg1p, reported to control the length of eisosomes in S. cerevisiae (30), is found only within the budding yeasts (Saccharomycetales); its functional homologue, the "Seg1-like" Sle1p protein in S. pombe (30), shares sequence homology only in the polybasic C-terminal region. Not surprisingly, no algal Seg1 homologues were found.…”

Section: Resultsmentioning

confidence: 99%

“…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. Caveolae, found in certain animal cell types, start out as flat, cholesterol-rich lipid rafts that are induced to form spherical invaginations via the association of accessory cholesterol-binding proteins, called caveolins, which hairpin into but do not span the plasma membrane, and the cavins, peripheral membrane proteins thought to control caveolin oligomerization.…”

Section: Discussionmentioning

confidence: 99%

“…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. The MCC protein Nce102p has also been implicated in generating curvature (5,31).…”

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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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Seg1 controls eisosome assembly and shape

Abstract: Seg1 establishes a platform for the assembly of eisosomes and is important for determining their length.

Cited by 60 publications

References 57 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

A Pil1-Sle1-Syj1-Tax4 functional pathway links eisosomes with PI(4,5)P2 regulation

Eisosome Ultrastructure and Evolution in Fungi, Microalgae, and Lichens

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