Role of turgor pressure in endocytosis in fission yeast

Basu, Roshni; Munteanu, Emilia Laura; Chang, Fred

doi:10.1091/mbc.e13-10-0618

Cited by 112 publications

(148 citation statements)

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“…In yeast, actin polymerization is required for endocytosis under normal conditions [4, 5]. This requirement is lessened under conditions of reduced turgor pressure [6, 7] and conversely becomes more stringent when turgor pressure is increased [7]. Finally, correlative light- and electron-microscopy measurements indicate that membrane bending is always preceded by actin polymerization [8], although this finding has been disputed by electron-microscopy studies using other methods [9].…”

Section: Introductionmentioning

confidence: 99%

Actin growth profile in clathrin-mediated endocytosis

2017

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Clathrin-mediated endocytosis in yeast is driven by a protein patch containing close to 100 different types of proteins. Among the proteins are 5000-10,000 copies of polymerized actin, and successful endocytosis requires growth of the actin network. Since it is not known exactly how actin network growth drives endocytosis, we calculate the spatial distribution of actin growth required to generate the force that drives the process. First, we establish the force distribution that must be supplied by actin growth, by combining membrane-bending profiles obtained via electron microscopy with established theories of membrane mechanics. Next we determine the profile of actin growth, using a continuum mechanics approach and an iterative procedure starting with an actin growth profile obtained from a linear analysis. The profile has fairly constant growth outside a central hole of radius 45-50 nm, but very little growth in this hole. This growth profile can reproduce the required forces if the actin shear modulus exceeds 80 kPa, and the growing filaments can exert very large polymerization forces. The growth profile prediction could be tested via electron-microscopy or superresolution experiments in which the turgor pressure is suddenly turned off.

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Section: Introductionmentioning

confidence: 99%

Actin growth profile in clathrin-mediated endocytosis

2017

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“…A calculation based on the total number of type-I myosins in fission yeast (10), assuming that each one can generate 2 pN of force, suggested that they could overcome the turgor pressure, but only over a smaller region of radius 10 nm. The geometric arrangement of myosins that would supply forces with the correct orientation and distribution is also not known.…”

Section: Alternative Mechanismsmentioning

confidence: 99%

“…Recent theoretical work on CME in yeast has treated the mechanics of forces generated by actin polymerization, as well as the intrinsic curvature of the clathrin coat that accumulates on the cell membrane (5)(6)(7)(8). To date, however, it is not known how actin and other curvature-generating proteins can produce enough force to overcome the large turgor pressure in yeast (9,10). Here we explore the hypothesis that increasing the membrane permeability at the endocytic site can locally reduce the turgor pressure and thus facilitate endocytosis.…”

Section: Introductionmentioning

confidence: 99%

“…Another calculation based on membrane elasticity theory and an actin point force suggested that the required force is even larger than our estimate (5). Finally, calculations using somewhat different approaches (10) found it implausible that actin polymerization can overcome the turgor pressure. We note, however, that the insufficiency of actin polymerization forces cannot be taken as rigorously proved, because there are substantial uncertainties in all of the quantities used to estimate the slowing of polymerization.…”

Section: Introductionmentioning

confidence: 99%

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Local Turgor Pressure Reduction via Channel Clustering

Scher-Zagier

2017

Biophysical Journal

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The primary drivers of yeast endocytosis are actin polymerization and curvature-generating proteins, such as clathrin and BAR domain proteins. Previous work has indicated that these factors may not be capable of generating the forces necessary to overcome turgor pressure. Thus local reduction of the turgor pressure, via localized accumulation or activation of solute channels, might facilitate endocytosis. The possible reduction in turgor pressure was calculated numerically, by solving the diffusion equation through a Legendre polynomial expansion. It was found that for a region of increased permeability having radius 45 nm, as few as 60 channels with a spacing of 10 nm could locally decrease the turgor pressure by 50%. We identified a key dimensionless parameter, p ¼ P 1 a/D, where P 1 is the increased permeability, a is the radius of the permeable region, and D is the solute diffusion coefficient. When p > 0.44, the turgor pressure is locally reduced by >50%. An approximate analytic theory was used to generate explicit formulas for the turgor pressure reduction in terms of key parameters. These findings may also be relevant to plants, where the mechanisms that allow endocytosis to proceed despite high turgor pressure are largely unknown.

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“…6 Pa [32,33]) inside yeast cells [34]. Under such high pressure, theoretical studies suggest that the force needed to initiate membrane invagination is on the order of 3000pN [35,36] and actin polymerization is thought to provide the driving force.…”

Section: Introductionmentioning

confidence: 99%

Structural organization and energy storage in crosslinked actin-assemblies

Berro

2017

Preprint

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During clathrin-mediated endocytosis in yeast cells, short actin filaments (< 200nm) and crosslinking protein fimbrin assemble to drive the internalization of the plasma membrane. However, the organization of the actin meshwork during endocytosis remains largely unknown. In addition, only a small fraction of the force necessary to elongate and pinch off vesicles can be accounted for by actin polymerization alone. In this paper, we used mathematical modeling to study the self-organization of rigid actin filaments in the presence of elastic crosslinkers in conditions relevant to endocytosis. We found that actin filaments condense into either a disordered meshwork or an ordered bundle depending on filament length and the mechanical and kinetical properties of the crosslinkers. Our simulations also demonstrated that these nanometer-scale actin structures can store a large amount of elastic energy within the crosslinkers (up to 10kBT per crosslinker). This conversion of binding energy into elastic energy is the consequence of geometric constraints created by the helical pitch of the actin filaments, which results in frustrated configurations of crosslinkers attached to filaments. We propose that this stored elastic energy can be used at a later time in the endocytic process. As a proof of principle, we presented a simple mechanism for sustained torque production by ordered detachment of crosslinkers from a pair of parallel filaments.

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Role of turgor pressure in endocytosis in fission yeast

Cited by 112 publications

References 57 publications

Actin growth profile in clathrin-mediated endocytosis

Actin growth profile in clathrin-mediated endocytosis

Local Turgor Pressure Reduction via Channel Clustering

Structural organization and energy storage in crosslinked actin-assemblies

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