Actin cable distribution and dynamics arising from cross-linking, motor pulling, and filament turnover

Tang, Haosu; Laporte, Damien; Vavylonis, Dimitrios

doi:10.1091/mbc.e14-05-0965

Cited by 31 publications

(57 citation statements)

References 69 publications

(103 reference statements)

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“…Briefly, glycan strands are modeled as semi-flexible filaments consisting of beads connected with springs, while peptide bridges are modeled as springs connecting glycan beads (Figure 3C) (Laporte et al, 2012; Tang et al, 2014; Huang et al, 2008). Typical length of inserted glycan polymer is ∼1 μm (∼1/3 cell circumference) (Hayhurst et al, 2008) and in our model the peptide bridges between newly inserted glycan strands are in a relaxed state.…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Cell-wall remodeling drives engulfment during Bacillus subtilis sporulation

Ojkic

López‐Garrido

Pogliano

et al. 2016

eLife

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When starved, the Gram-positive bacterium Bacillus subtilis forms durable spores for survival. Sporulation initiates with an asymmetric cell division, creating a large mother cell and a small forespore. Subsequently, the mother cell membrane engulfs the forespore in a phagocytosis-like process. However, the force generation mechanism for forward membrane movement remains unknown. Here, we show that membrane migration is driven by cell wall remodeling at the leading edge of the engulfing membrane, with peptidoglycan synthesis and degradation mediated by penicillin binding proteins in the forespore and a cell wall degradation protein complex in the mother cell. We propose a simple model for engulfment in which the junction between the septum and the lateral cell wall moves around the forespore by a mechanism resembling the ‘template model’. Hence, we establish a biophysical mechanism for the creation of a force for engulfment based on the coordination between cell wall synthesis and degradation.DOI: http://dx.doi.org/10.7554/eLife.18657.001

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Section: Resultsmentioning

confidence: 99%

“…Inserted glycans are equilibriated using Langevin dynamics in 3D (Laporte et al, 2012; Tang et al, 2014; Ojkic et al, 2014). The Langevin dynamic equation of the

i^{th}

glycan bead at position

𝐫_{i}

is given by:

ζ_{i} \frac{d {bold𝐫}_{i}}{d t} = {bold𝐅}_{i}^{spr} + {bold𝐅}_{i}^{bend} + {bold𝐅}_{i}^{pep} + {bold𝐅}_{i}^{stoch} + {bold𝐅}_{i}^{Δ p} + {bold𝐅}_{i}^{wall},

…”

Section: Image Analysismentioning

confidence: 99%

Cell-wall remodeling drives engulfment during Bacillus subtilis sporulation

Ojkic

López‐Garrido

Pogliano

et al. 2016

eLife

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“…Actin filaments are simulated using a coarse-grained bead-spring model [Nédélec and Foethke 2007; Tang et al 2014] (Figure 1B). One bead represents a segment of the helical actin filament.…”

Section: Model and Methodsmentioning

confidence: 99%

“…We conclude this paper with a comparison to previous 3D models of actin cable and contractile ring formation in fission yeast [Bidone et al 2014; Tang et al 2014]. In comparison to those models, the present work includes two important changes: 1) we include explicit severing of filaments into smaller fragments while in the earlier studies turnover was simulated as whole filament removal, and 2) cross-linking interactions have an explicit orientation dependence.…”

Section: Introductionmentioning

confidence: 98%

Computational model of polarized actin cables and cytokinetic actin ring formation in budding yeast

2015

Self Cite

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The budding yeast actin cables and contractile ring are important for polarized growth and division, revealing basic aspects of cytoskeletal function. To study these formin-nucleated structures, we built a 3D computational model with actin filaments represented as beads connected by springs. Polymerization by formins at the bud tip and bud neck, crosslinking, severing, and myosin pulling, are included. Parameter values were estimated from prior experiments. The model generates actin cable structures and dynamics similar to those of wild type and formin deletion mutant cells. Simulations with increased polymerization rate result in long, wavy cables. Simulated pulling by type V myosin stretches actin cables. Increasing the affinity of actin filaments for the bud neck together with reduced myosin V pulling promotes the formation of a bundle of antiparallel filaments at the bud neck, which we suggest as a model for the assembly of actin filaments to the contractile ring.

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“…In actin cables and the contractile ring, formin-nucleated actin filaments are crosslinked into long bundles with a length on the order of microns [3][4][5]. Computational models of these actin structures typically treat actin filaments as semi-flexible polymers that are connected by rigid segments [6][7][8][9]. In contrast, the organization of the actin network in actin patches formed during clathrinmediated endocytosis is drastically different from that in actin cables or the contractile ring.…”

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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Actin cable distribution and dynamics arising from cross-linking, motor pulling, and filament turnover

Cited by 31 publications

References 69 publications

Cell-wall remodeling drives engulfment during Bacillus subtilis sporulation

Cell-wall remodeling drives engulfment during Bacillus subtilis sporulation

Computational model of polarized actin cables and cytokinetic actin ring formation in budding yeast

Structural organization and energy storage in crosslinked actin-assemblies

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