Binding of anisotropic curvature-inducing proteins onto membrane tubes

Noguchi, Hiroshi; Tozzi, Caterina; Arroyo, Marino

doi:10.1039/d2sm00274d

Cited by 14 publications

(22 citation statements)

References 72 publications

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“…The binding and unbinding of these anisotropic curvature inducing proteins is curvature dependent. 9,20,64 The accumulation of these protein dimers and the interaction between their curvature sensing and curvature generation abilities also depends on their adsorption, diffusion, and aggregation in the plane of the membrane. 65 Such processes have been studied using molecular dynamics simulations 18,19 and a continuum description of these process that couples the underlying thermodynamics 66,67 coupled with membrane deformation would be necessary to avoid the model simplifications.…”

Section: Discussionmentioning

confidence: 99%

“…From a theoretical standpoint, the mechanism of tube formation has been studied quite extensively using continuum mechanics and molecular dynamics simulations. [18][19][20] Our focus here is on continuum models where the Helfrich energy 21 is used to capture the bending energy of the membrane and a spontaneous curvature is used to capture asymmetries between the two leaflets. When an isotropic spontaneous curvature is used in the Helfrich energy, spheres and pearls emerge as energy-minimizing shapes because the minimum energy state of these geometries is such that both principal curvatures have the same value.…”

Section: Introductionmentioning

confidence: 99%

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Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Mahapatra

Rangamani

2023

Soft Matter

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Mahapatra

Rangamani

2023

Soft Matter

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“…We note that our present work has a number of simplifications particularly with respect to the protein coat. The binding and unbinding of these anisotropic curvature inducing proteins is curvature dependent ( 8, 19, 58 ). The accumulation of these protein dimers and the interaction between their curvature sensing and curvature generation abilities also depends on their adsorption, diffusion, and aggregation in the plane of the membrane ( 59 ).…”

Section: Discussionmentioning

confidence: 99%

“…From a theoretical standpoint, the mechanism of tube formation has been studied quite extensively using continuum mechanics and molecular dynamics simulations (17)(18)(19). Our focus here is on continuum models where the Helfrich energy (20) is used to capture the bending energy of the membrane and a spontaneous curvature is used to capture asymmetries between the two leaflets.…”

Section: Introductionmentioning

confidence: 99%

Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Mahapatra

Rangamani

2022

Preprint

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Plasma membrane tubes are ubiquitous in cellular membranes and in the membranes of intracellular organelles. They play crucial roles in trafficking, ion transport, and cellular motility. The formation of plasma membrane tubes can be due to localized forces acting on the membrane or by curvature-induced by membrane-bound proteins. Here, we present a mathematical framework to model cylindrical tubular protrusions formed by proteins that induce anisotropic spontaneous curvature. Our analysis revealed that the tube radius depends on an effective tension that includes contributions from the bare membrane tension and the protein-induced curvature. We also found that the length of the tube undergoes an abrupt transition from a short, dome-shaped membrane to a long cylinder and this transition is characteristic of a snapthrough instability. Finally, we show that the snapthrough instability depends on the different parameters including coat area, bending modulus, and extent of protein-induced curvature. Our findings have implications for tube formation due to BAR-domain proteins in processes such as endocytosis, t-tubule formation in myocytes, and cristae formation in mitochondria.1Significance StatementCylindrical tubes are ubiquitous on cellular membranes and many studies have focused on how forces can give rise to tubes. How do curvature-inducing proteins, in the absence of forces, form cylindrical tubes on lipid bilayers? The answer to this question relies on minimizing the bending energy of the membrane to accommodate two different principal curvatures such that a cylindrical shape is an energy minimizer. Here, we build on previous works to develop such a model and show that the formation of an elongated cylindrical tube is accompanied by a snapthrough transition in the bending energy. Furthermore, we identify how this transition depends on different membrane properties, providing a landscape for comparing with different experimental observations. These findings have implications for our understanding how tubes forms in different cellular processes including trafficking, mitochondrial inner membrane cristae formation, and T-tubule formation in myocytes.

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“…The aim of this study is to clarify the collective effects of the anisotropic curvature-inducing domains and anchored polymer chains. Previously, we have simulated anisotropic curvature-inducing proteins using a meshless membrane method [37][38][39][40][41][42][43][44][45]. The assembly of crescent rods induces tubulation from a flat membrane [40,43], and the protein chirality enhances this ability [44].…”

Section: Introductionmentioning

confidence: 99%

Membrane shape deformation induced by curvature-inducing proteins consisting of chiral crescent binding and intrinsically disordered domains

Noguchi

2022

Preprint

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Curvature-inducing proteins containing a Bin/Amphiphysin/Rvs (BAR) domain often have intrinsically disordered domains. Recent experiments have shown that these disordered chains enhance curvature sensing and generation. Here, we report on the modification of protein-membrane interactions by disordered chains using meshless membrane simulations. The protein and bound membrane are modeled together as a chiral crescent protein rod with two excluded-volume chains. As the chain length increases, the repulsion between them reduces the cluster size of the proteins. It induces spindle-shaped vesicles and a transition between arc-shaped and circular protein assemblies in a disk-shaped vesicle. For flat membranes, an intermediate chain length induces many tubules owing to the repulsion between the protein assemblies, whereas longer chains promote perpendicular elongation of tubules. Moreover, protein rods with zero rod curvature and sufficiently long chains stabilize the spherical buds. For proteins with a negative rod curvature, an intermediate chain length induces a rugged membrane with branched protein assemblies, whereas longer chains induce the formation of tubules with periodic concave-ring structures.

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Binding of anisotropic curvature-inducing proteins onto membrane tubes

Abstract: Bin/Amphiphysin/Rvs superfamily proteins and other curvature-inducing proteins have anisotropic shapes and anisotropically bend biomembrane. Here, we report how the anisotropic proteins bind the membrane tube and are orientationally ordered using...

Cited by 14 publications

References 72 publications

Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Membrane shape deformation induced by curvature-inducing proteins consisting of chiral crescent binding and intrinsically disordered domains

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