Membrane Morphologies Induced by Arc-Shaped Scaffolds Are Determined by Arc Angle and Coverage

Bonazzi, Francesco; Weikl, Thomas R.

doi:10.1016/j.bpj.2019.02.017

Cited by 23 publications

(54 citation statements)

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“…Similar pearled tubular morphologies have been experimentally and computationally observed in bilayers with isotropic spontaneous curvature caused by anchored polymers [11,86], in cells as a result of crowding of the grycocalyx [12] or by asymmetric lipid swelling due to changes in pH [87]. We note that if proteins induce anisotropic spontaneous curvature, for instance because they are elongated and adopt nematic order, experiments and molecular models suggest that one can expect tubular protein-rich protrusions of uniform radius [15,28,30] rather than pearled protrusions as we find here. We leave models capturing nematic ordering of curved proteins for future work.…”

Section: Curvature Sensing and Generation Starting From A Prolate Vessupporting

confidence: 80%

“…In doing so, we assume that proteins are isotropic, or in a regime in which entropic effects dominate over orientational order. We leave for future work a general continuum theory accounting for nematic order, pertinent for instance to elongated membrane proteins with BAR domains [15,28,30].…”

Section: Setup Kinematics and Balance Lawsmentioning

confidence: 99%

“…At the nanoscale, all-atom molecular dynamics have described curvature generation by single domains [24] and curvature maintenance by multiple proteins [25]. Reaching a micron, coarse-grained molecular dynamics simulations, treating the membrane either molecularly or as a continuum object, have followed the aggregation of multiple proteins to cooperatively form protein-rich curved domains [26][27][28][29][30]. Models treating proteins as discrete objects in a continuum membrane have examined membrane-mediated protein-protein interactions [31,32], or the spontaneous curvature induced by anchored polymers [33,34].…”

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confidence: 99%

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Out-of-equilibrium mechanochemistry and self-organization of fluid membranes interacting with curved proteins

2019

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The function of biological membranes is controlled by the interaction of the fluid lipid bilayer with various proteins, some of which induce or react to curvature. These proteins can preferentially bind or diffuse towards curved regions of the membrane, induce or stabilize membrane curvature and sequester membrane area into protein-rich curved domains. The resulting tight interplay between mechanics and chemistry is thought to control organelle morphogenesis and dynamics, including traffic, membrane mechanotransduction, or membrane area regulation and tension buffering. Despite all these processes are fundamentally dynamical, previous work has largely focused on equilibrium and a self-consistent theoretical treatment of the dynamics of curvature sensing and generation has been lacking. Here, we develop a general theoretical and computational framework based on a nonlinear Onsager's formalism of irreversible thermodynamics for the dynamics of curved proteins and membranes. We develop variants of the model, one of which accounts for membrane curving by asymmetric crowding of bulky off-membrane protein domains. As illustrated by a selection of test cases, the resulting governing equations and numerical simulations provide a foundation to understand the dynamics of curvature sensing, curvature generation, and more generally membrane curvature mechano-chemistry.To quantitatively understand these phenomena, various biophysical studies have exposed artificial lipid membranes to purified proteins in controlled conditions [14]. At high concentration, curved proteins can induce severe membrane curvature when incubated with liposomes [15], can stabilize membrane tubes [10,16], and can dynamically trigger protein-rich tubular protrusions out of tense vesicles [17][18][19]. At lower concentrations, proteins sense curvature and preferentially adsorb or migrate to favorably curved membranes, as probed in assays involving polydisperse vesicle suspensions [20], vesicles with membrane tethers [18,21] or supported lipid bilayers on wavy substrates [22]. Since protein-rich curved domains sequester apparent membrane area from the adjacent planar membrane, their formation perform work against membrane tension, and thus can be hindered if tension is large enough. This kind of mechano-chemical coupling, tested in vitro by exposing aspirated vesicles to BAR proteins [19], has physiological implications during the mechano-protection of stressed cells by the release of membrane area through disassembly of caveolae [4], or in the regulation of clathrin-mediated endocytosis by membrane tension [23].A number of theoretical and computational studies at various scales have been developed to understand the interaction between curved proteins and membranes. At the nanoscale, all-atom molecular dynamics have described curvature generation by single domains [24] and curvature maintenance by multiple proteins [25]. Reaching a micron, coarse-grained molecular dynamics simulations, treating the membrane either molecularly or as a continuum object, hav...

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Section: Curvature Sensing and Generation Starting From A Prolate Vessupporting

confidence: 80%

Section: Setup Kinematics and Balance Lawsmentioning

confidence: 99%

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confidence: 99%

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Out-of-equilibrium mechanochemistry and self-organization of fluid membranes interacting with curved proteins

2019

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“…To understand the physical mechanisms underlying our observations, we developed a theoretical framework considering the dynamics of lipid tubes and buds with low coverage (since protein is injected once structures are formed) and low curvature (since the structures are made markedly thinner by Amphiphysin) upon exposure to BAR proteins. Theoretically, various computational studies using coarse-grained simulations of elongated and curved objects moving on a deformable membrane have suggested the self-organization of regions with high anisotropic (cylindrical) curvature with high-protein coverage and strong nematic order 18,19,20 . None of these works, however, predicted or observed the tube-sphere complexes that appear in our experiments (Fig.…”

Section: Mainmentioning

confidence: 99%

Dynamic Mechanochemical feedback between curved membranes and BAR protein self-organization

Roux

Tozzi

Walani

et al. 2020

Preprint

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In many physiological situations, BAR proteins interact with, and reshape, pre-existing curved membranes, contributing to essential cellular processes. However, the non-equilibrium and timedependent process of reshaping, and its dependence on initial membrane shape, remains largely unknown. Here we explain, both experimentally and through modelling, how a BAR protein dynamically interacts with mechanically bent lipid membranes. We capture protein binding to curved membranes, and characterize a variety of dynamical reshaping events depending on membrane shape and protein arrangement. The events can be generally understood by an isotropic-to-nematic phase transition, in which low curvature templates with isotropic protein orientation progress towards highly curved lipid tubes with nematic protein arrangement. Our findings also apply in cells, where mechanical stretch triggers BAR-protein-membrane interactions that enable potential mechanotransduction mechanisms. Our results characterize and broaden the reshaping processes of BAR proteins on mechanically constrained membranes, demonstrating the interplay between membrane mechanical stimuli and BAR protein response.

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“…The formation of the clathrin coated pits can be assisted by curved proteins like BAR, which bind to the membrane surface inducing membrane curvature [77]. Simulations in which the BAR protein is described as a collection of beads arranged into a curved rigid body have demonstrated how membrane morphologies depend on the density and geometrical properties of the arc-shaped proteins [58,78,79], see Fig. 3.…”

Section: Remodelling Of Lipid Membranesmentioning

confidence: 99%

Minimal coarse-grained models for molecular self-organisation in biology

Hafner

Krausser

Šarić

2019

Current Opinion in Structural Biology

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The molecular machinery of life is largely created via self-organisation of individual molecules into functional assemblies. Minimal coarse-grained models, where a whole macromolecule is represented by a small number of particles, can be of great value in identifying the main driving forces behind self-organisation in cell biology. Such models can incorporate data from both molecular and continuum scales, and their results can be directly compared to experiments. Here we review the state of the art of models for studying the formation and biological function of macromolecular assemblies in cells. We outline the key ingredients of each model and their main findings. We illustrate the contribution of this class of simulations to identifying the physical mechanisms behind life and diseases, and discuss their future developments. IntroductionSelf-assembly of individual molecules into large-scale functional structures generates the molecular machinery of life [1]. Such processes underlie the formation of cell membranes, protein filaments and networks, and drive the formation of three-dimensional genome structures. Many of these assemblies, such as protein filaments and lattices, also function as efficient nanomachines that enable cells to sense, move, divide, and transport materials in and out of the cell [2]. To sustain life, the formation of macromolecular assemblies needs to *

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Membrane Morphologies Induced by Arc-Shaped Scaffolds Are Determined by Arc Angle and Coverage

Cited by 23 publications

References 58 publications

Out-of-equilibrium mechanochemistry and self-organization of fluid membranes interacting with curved proteins

Out-of-equilibrium mechanochemistry and self-organization of fluid membranes interacting with curved proteins

Dynamic Mechanochemical feedback between curved membranes and BAR protein self-organization

Minimal coarse-grained models for molecular self-organisation in biology

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