Closed membrane shapes with attached BAR domains subject to external force of actin filaments

Mesarec, Luka; Góźdź, Wojciech T.; Iglič, Veronika Kralj; Kralj, Samo; Iglič, Aleš

doi:10.1016/j.colsurfb.2016.01.010

Cited by 37 publications

(85 citation statements)

References 71 publications

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“…Given the computational cost of resolving many I-BAR domains at a finer resolution, the current model parameterization also does not take into account direct interactions between neighboring I-BAR domains (except excluded volume), and therefore, high density conditions are outside of the scope of this model. We also note that axial aggregates are in contrast to previous computational studies of I-BAR domains (14,15) that show perpendicular aggregates inside of membrane tubules, but these previous studies used models unlike the models presented here. Among the several differences including membrane representation and protein-membrane interactions, the CG I-BAR model used in this work reproduces the properties of a single, isolated, and atomically resolved I-BAR domain, which flattens when bound to the membrane and is outside the curvature ranges previously studied.…”

Section: I-bar Domains Form Axial Aggregates At Low Coveragecontrasting

confidence: 82%

“…I-BAR domains have been the subject of several computational and theoretical studies (13)(14)(15)(16)(17), with varying degrees of accuracy. I-BAR domain-mediated membrane remodeling spans many length scales, from nanometer-scale local interactions between individual I-BAR domains and lipid headgroups to the micron-scale deformations collectively induced by many I-BAR domains.…”

Section: Introductionmentioning

confidence: 99%

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Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes

Jarin

Tsai

Davtyan

et al. 2019

Biophysical Journal

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Protein-mediated membrane remodeling is a ubiquitous and critical process for proper cellular function. Inverse Bin/Amphiphysin/Rvs (I-BAR) domains drive local membrane deformation as a precursor to large-scale membrane remodeling. We employ a multiscale approach to provide the molecular mechanism of unusual I-BAR domain-driven membrane remodeling at a low protein surface concentration with near-atomistic detail. We generate a bottom-up coarse-grained model that demonstrates similar membrane-bound I-BAR domain aggregation behavior as our recent Mesoscopic Membrane with Explicit Proteins model. Together, these models bridge several length scales and reveal an aggregation behavior of I-BAR domains. We find that at low surface coverage (i.e., low bound protein density), I-BAR domains form transient, tip-to-tip strings on periodic flat membrane sheets. Inside of lipid bilayer tubules, we find linear aggregates parallel to the axis of the tubule. Finally, we find that I-BAR domains form tip-to-tip aggregates around the edges of membrane domes. These results are supported by in vitro experiments showing low curvature bulges surrounded by I-BAR domains on giant unilamellar vesicles. Overall, our models reveal new I-BAR domain aggregation behavior in membrane tubules and on the surface of vesicles at low surface concentration that add insight into how I-BAR domain proteins may contribute to certain aspects of membrane remodeling in cells.

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Section: I-bar Domains Form Axial Aggregates At Low Coveragecontrasting

confidence: 82%

Section: Introductionmentioning

confidence: 99%

Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes

Jarin

Tsai

Davtyan

et al. 2019

Biophysical Journal

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“…These results disfavor mechanisms where the mechanosensor restricting Rac activation responds directly to membrane tension, suggesting that tension sensors such as stretch-activated ion channels (e.g., Piezo (Cox et al, 2016;Shi et al, 2018)), cannot be the sole class of mechanosensors mediating neutrophil long-range inhibition. Given that osmotically-induced swelling/shrinking leads to changes in membrane geometry (Cheung et al, 1982;Ting-Beall et al, 1993), mechanosensors responding to changes in membrane shape, using curvature-sensitive membrane binders like BAR proteins (Mesarec et al, 2016;Mim and Unger, 2012), are likely to be involved. An analogous mechanism operates in budding yeast where the highly-conserved mTORC2 signaling pathway is engaged by proteins sensing changes in plasma membrane geometry (Berchtold et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Cell confinement reveals a branched-actin independent circuit for neutrophil polarity

Graziano¹,

Town²,

Nagy³

et al. 2018

Preprint

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Migratory cells use distinct motility modes to navigate different microenvironments, but it is unclear whether these modes rely on the same core set of polarity components. To investigate this, we disrupted Arp2/3 and WAVE complex, which assemble branched actin networks that are essential for neutrophil polarity and motility in standard adherent conditions. Surprisingly, confinement rescues polarity and movement of neutrophils lacking these components, revealing a processive bleb-based protrusion program that is mechanistically distinct from the branched actin-based protrusion program but shares some of the same core components and underlying molecular logic. We further find that the restriction of protrusion growth to one site does not always respond to membrane tension directly, as previously thought, but may rely on closely linked properties such as local membrane curvature. Our work reveals a hidden circuit for neutrophil polarity and indicates that cells have distinct molecular mechanisms for polarization that dominate in different microenvironments.to produce a single protrusion ( Fig. 1A) (Diz-Muñoz et al., 2016;Houk et al., 2012;Keren et al., 2008;Sens and Plastino, 2015).While actin polymerization serves as a key ingredient in generating the positive and negative feedback loops that give rise to polarity, we lack an understanding of how specific types of actin networks provide each kind of feedback. Immune cells assemble multiple actin networks at different subcellular locations that carry out distinct functions to support migration: Arp2/3dependent assembly of branched actin networks at the leading edge contributes to cell guidance/steering and protrusion extension, while actomyosin bundles near the trailing edge provide contractile force to lift the cell rear and squeeze the cell body forward (Lämmermann and Germain, 2014;Moreau et al., 2018). Along with these functional differences, the types of actin networks immune cells and other migratory cells employ for migration vary with microenvironment (Lämmermann and Germain, 2014;Paluch et al., 2016). The role of actin dynamics in migration is complex and likely depends on the type of actin network, its subcellular location, and the extracellular environment. Existing tools to probe the role of actin networks in both the positive and negative feedback loops needed for polarity are fairly crude and have largely been based on pharmacological perturbations that target all actin polymer (Diz-Muñoz et al., 2016;Huang et al., 2013;Inoue and Meyer, 2008;Sasaki et al., 2007;Wang et al., 2002;Weiner et al., 2007;Yang et al., 2016). More surgical experiments are needed to clarify how different subcellular actin networks contribute to polarity generation under different environmental conditions. Figure 1. WAVE complex is required for neutrophil polarity and motility.A) Polarity generation depends on fast-acting, short-range positive feedback and slower-acting, long-range negative feedback. Actin assembly participates in both types of feedback, with its role in negat...

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“…-We assume that the transmembrane proteins are rotationally symmetric. Therefore we ignore the influence of anisotropic membrane inclusions such as BIN-Amphiphysin-Rvs (BAR) domain proteins [41,40,66]. -We do not consider the role of forces applied by actin-mediated nanotube formation [40], so that we can focus only on membrane nanotube deformation due to membrane-protein interactions [67][68][69].…”

Section: Assumptionsmentioning

confidence: 99%

“…Recently, a series of elegant modeling studies have proposed the idea that curved proteins and cytoskeletal proteins can induce protrusions along the membrane [39][40][41][42][43]. Separately, experiments are beginning to demonstrate that (a) the composition of a membrane nanotube is not homogeneous [44]; (b) tension due to adhesion of rolling neutrophils can lead to tether formation [44]; and (c) spontaneous curvature along a nanotube can lead to the formation of bead like structures [44-47, 17, 20].…”

Section: Introductionmentioning

confidence: 99%

Modeling membrane nanotube morphology: the role of heterogeneity in composition and material properties

Alimohamadi

Ovryn

Rangamani

2018

Preprint

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Membrane nanotubes have been identified as a dynamic way for cells to connect and interact over long distances. These long and thin membranous protrusions have been shown to serve as conduits for the transport of proteins, organelles, viral particles, and mRNA. Nanotubes typically appear as thin and cylindrical tubes, but they can also have a beads-on-a-string architecture. Here, we study the role of membrane mechanics in governing the architecture of these tubes and show that the formation of a bead-like structure along the nanotube can result from a local heterogeneity in the membrane due to protein aggregation or due to membrane composition. We present numerical results that predict how membrane properties, protein density, and tension compete to create a phase space that governs the morphology of a nanotube. We also find that the stability of multiple beads is regulated by an energy barrier that prevents two beads from fusing. These results suggest that the membrane-protein interaction, protein aggregation, and membrane tension closely regulate the tube radius, number of beads, and the bead morphology.

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Closed membrane shapes with attached BAR domains subject to external force of actin filaments

Cited by 37 publications

References 71 publications

Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes

Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes

Cell confinement reveals a branched-actin independent circuit for neutrophil polarity

Modeling membrane nanotube morphology: the role of heterogeneity in composition and material properties

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