On the Role of Curved Membrane Nanodomains and Passive and Active Skeleton Forces in the Determination of Cell Shape and Membrane Budding (original) (raw)
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On the role of membrane anisotropy and BAR proteins in the stability of tubular membrane structures
Journal of …, 2012
Recent studies have demonstrated that actin filaments are not crucial for the short-term stability of tubular membrane protrusions originating from the cell surface. It has also been demonstrated that prominin nanodomains and curvature inducing I-BAR proteins could account for the stability of the membrane protrusion. Here we constructed an axisymmetric model of a membrane protrusion that excludes actin filaments in order to investigate the contributions of prominin nanodomains (rafts) and I-BAR proteins to the membrane protrusion stability. It was demonstrated that prominin nanodomains and I-BAR proteins can stabilize the membrane protrusion only over a specific range of spontaneous curvature. On the other hand, high spontaneous curvature and/or high density of I-BAR proteins could lead to system instability and to non-uniform contraction in the radial direction of the membrane protrusion. In agreement with previous studies, it was also shown that the isotropic bending energy of lipids is not sufficient to explain the stability of the observed tubular membrane protrusion without actin filaments.
Membrane nanodomains: contribution of curvature and interaction with proteins and cytoskeleton
Essays in Biochemistry, 2015
The understanding of lipid membranes and their organization has undergone significant development with better techniques and therefore more resolved experiments. Many new factors and organizing principles have been discovered, and interplay between these factors is expected to result in rich functional behaviours. The major factors regulating the lateral membrane heterogeneity, apart from the well-studied phase separation, are cytoskeleton pinning, clustering of lipids and curvature. These factors are effective means to create membrane domains that provide rich biological functionality. We review the recent advances and concepts of membrane heterogeneity organization by curvature, cytoskeleton and clustering proteins.
Closed membrane shapes with attached BAR domains subject to external force of actin filaments
Membrane deformations induced by attached BAR superfamily domains could trigger or facilitate the growth of plasma membrane protrusions. The BAR domain family consists of BAR, F-BAR and I-BAR domains, each enforcing a different local curvature when attached to the membrane surface. Our theoretical study mainly focuses on the role of I-BAR in the membrane tubular deformations generated or stabilised by actin filaments. The influence of the area density of membrane attached BAR domains and their intrinsic curvature on the closed membrane shapes (vesicles) was investigated numerically. We derived an analytical approximative expression for the critical relative area density of BARs at which the membrane tubular protrusions on vesicles are most prominent. We have shown that the BARs with a higher intrinsic curvature induce thinner and longer cylindrical protrusions. The average orientation of the membrane attached BARs is altered when the vesicle shape is subjected to external force of growing actin rod-like structure inside a vesicle. The average orientation angle of membrane attached BARs may indicate whether the actin filaments are just stabilising the protrusion or generating it by stretching the vesicle.
Phase Transitions of the Coupled Membrane-Cytoskeleton Modify Cellular Shape
Biophysical Journal, 2007
Formation of protrusions and protein segregation on the membrane is of a great importance for the functioning of the living cell. This is most evident in recent experiments that show the effects of the mechanical properties of the surrounding substrate on cell morphology. We propose a mechanism for the formation of membrane protrusions and protein phase separation, which may lay behind this effect. In our model, the fluid cell membrane has a mobile but constant population of proteins with a convex spontaneous curvature. Our basic assumption is that these membrane proteins represent small adhesion complexes, and also include proteins that activate actin polymerization. Such a continuum model couples the membrane and protein dynamics, including cell-substrate adhesion and protrusive actin force. Linear stability analysis shows that sufficiently strong adhesion energy and actin polymerization force can bring about phase separation of the membrane protein and the appearance of protrusions. Specifically, this occurs when the spontaneous curvature and aggregation potential alone (passive system) do not cause phase separation. Finite-size patterns may appear in the regime where the spontaneous curvature energy is a strong factor. Different instability characteristics are calculated for the various regimes, and are compared to various types of observed protrusions and phase separations, both in living cells and in artificial model systems. A number of testable predictions are proposed.
The role of spontaneous curvature in the formation of cell membrane necks
Cornell University - arXiv, 2022
The mechanical effects of membrane compositional inhomogeneities are analyzed in a process analogous of neck formation in cellular membranes. We cast on the Canham-Helfrich model of fluid membranes with both the spontaneous curvature and the surface tension being non-homogeneous functions along the cell membrane. The inhomogeneous distribution is determined by the equilibrium mechanical equations, and, in order to establish the role played by the inhomogeneity, we focus on the catenoid, a surface of zero mean curvature, which can be described in terms of the catenary curve parameterized by arc length. We show that analytic solutions exist for the spontaneous curvature, as well as for both, the surface tension and the radial elastic force. An analytic expression for the constrictive force at the neck, is obtained. From the energetic analysis, it is found that, if we fix the value of the constrictive force at the neck, the set of solutions lies on two branches separated by an energetic barrier. This barrier corresponds to the energy of the maximum catenoid. If instead we fix the axial force, the solution has access to catenoid of any size.
Guided by curvature: shaping cells by coupling curved membrane proteins and cytoskeletal forces
Philosophical Transactions of the Royal Society B: Biological Sciences, 2018
Eukaryote cells have flexible membranes that allow them to have a variety of dynamical shapes. The shapes of the cells serve important biological functions, both for cells within an intact tissue, and during embryogenesis and cellular motility. How cells control their shapes and the structures that they form on their surface has been a subject of intensive biological research, exposing the building blocks that cells use to deform their membranes. These processes have also drawn the interest of theoretical physicists, aiming to develop models based on physics, chemistry and nonlinear dynamics. Such models explore quantitatively different possible mechanisms that the cells can employ to initiate the spontaneous formation of shapes and patterns on their membranes. We review here theoretical work where one such class of mechanisms was investigated: the coupling between curved membrane proteins, and the cytoskeletal forces that they recruit. Theory indicates that this coupling gives rise...
Non-axisymmetric shapes of biological membranes from locally induced curvature
2019
In various biological processes such as endocytosis and caveolae formation, the cell membrane is locally deformed into curved configurations. Previous theoretical and computational studies to understand membrane morphologies resulting from locally induced curvature are often limited to axisymmetric shapes, which severely restricts the physically admissible morphologies. Under the restriction of axisymmetry, past efforts predict that the cell membrane buds at low resting tensions and stalls at a flat pit at high resting tensions. In this work, we lift the restriction of axisymmetry by employing recent theoretical and numerical advances to understand arbitrarily curved and deforming lipid bilayers. Our non-axisymmetric morphologies reveal membrane morphologies which agree well with axisymmetric studies—however only if the resting tension of the membrane is low. When the resting tension is moderate to high, we show that (i) axisymmetric invaginations are unstable; and (ii) non-axisymme...
Journal of Biomechanics, 2010
It is indicated that nonhomogeneous lateral distribution of membrane attached and flexible rod-like proteins (MRPs) may stabilize nanotubular membrane protrusions. We have shown that curvature induced accumulation of MRPs in the nanotubular membrane protrusion and the corresponding reduction of the membrane free energy are possible if the decrease of the deviatoric free energy of MRPs in the nanotubular protrusions is large enough to overcome the increase of the free energy due to decrease of configurational entropy in the process of lateral sorting of MRPs. The decrease of isotropic curvature energy of MRPs in the region of membrane protrusion is usually not sufficient for substantial MRPs sorting and consequent stabilization of the nanotubular membrane protrusions.