Mechanical stability of membrane nanotubular protrusions influenced by attachment of flexible rod-like proteins (original) (raw)
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Dynamics of membrane nanotubes coated with I-BAR
Membrane deformation is a necessary step in a number of cellular processes such as filopodia and invadopodia formation and has been shown to involve membrane shaping proteins containing membrane binding domains from the IRSp53-MIM protein family. In reconstituted membranes the membrane shaping domains can efficiently deform negatively charged membranes into tubules without any other proteins present. Here, we show that the IM domain (also called I-BAR domain) from the protein ABBA, forms semi-flexible nanotubes protruding into Giant Unilamellar lipid Vesicles (GUVs). By simultaneous quantification of tube intensity and tubular shape we find both the diameter and stiffness of the nanotubes. I-BAR decorated tubes were quantified to have a diameter of ~50 nm and exhibit no stiffening relative to protein free tubes of the same diameter. At high protein density the tubes are immobile whereas at lower density the tubes diffuse freely on the surface of the GUV. Bleaching experiments of the fluorescently tagged I-BAR confirmed that the mobility of the tubes correlates with the mobility of the I-BAR on the GUV membrane. Finally, at low density of I-BAR the protein upconcentrates within tubes protruding into the GUVs. This implies that I-BAR exhibits strong preference for negatively curved membranes.
Spontaneous shape transformation of free-floating lipid membrane nanotubes
Soft Matter, 2013
Freely floating lipid nanotubes, up to several hundred micrometers long, were found to spontaneously contract in length, and eventually transform into stomatocyte-like structures. This transformation was largely driven by the high curvature energy. The nanotubes equilibrate their membrane leaflet areas, by folding into tubular stomatocyte-like structures without any significant volume change, but require a substantial interleaflet lipid transport rate, estimated to be as high as 0.01-0.001 s À1 . The rate of transformation was dependent on the fluorescent membrane stain used, and nanotubes labelled with a water-soluble styryl dye, FM1-43, transformed approximately five-fold faster than nanotubes labelled with the phospholipid conjugated dye Texas Red DHPE.
The transport along membrane nanotubes driven by the spontaneous curvature of membrane components
…, 2012
Intercellular membrane nanotubes (ICNs) serve as a very specific transport system between neighboring cells. The underlying mechanisms responsible for the transport of membrane components and vesicular dilations along the ICNs are not clearly understood. The present study investigated the spatial distribution of anisotropic membrane components of tubular shapes and isotropic membrane components of spherical shapes. Experimental results revealed the preferential distribution of CTB (cholera toxin B)-GM1 complexes mainly on the spherical cell membrane, and cholesterol-sphingomyelin at the membrane leading edge and ICNs. In agreement with previous studies, we here propose that the spatial distribution of CTB-GM1 complexes and cholesterol-sphingomyelin rafts were due to their isotropic and anisotropic shapes, respectively. To elucidate the relationship between a membrane component shape and its spatial distribution, a twocomponent computational model was constructed. The minimization of the membrane bending (free) energy revealed the enrichment of the anisotropic component along the ICN and the isotropic component in the parent cell membrane, which was due to the curvature mismatch between the ICN curvature and the spontaneous curvature of the isotropic component. The equations of motion, derived from the differentiation of the membrane free energy, revealed a curvature-dependent flux of the isotropic component and a curvature-dependent force exerted on a vesicular dilation along the ICN. Finally, the effects of possible changes in the orientational ordering of the anisotropic component attendant to the transport of the vesicular dilation were discussed with connection to the propagation of electrical and chemical signals.
International Journal of Molecular Sciences, 2021
Biological membranes are composed of isotropic and anisotropic curved nanodomains. Anisotropic membrane components, such as Bin/Amphiphysin/Rvs (BAR) superfamily protein domains, could trigger/facilitate the growth of membrane tubular protrusions, while isotropic curved nanodomains may induce undulated (necklace-like) membrane protrusions. We review the role of isotropic and anisotropic membrane nanodomains in stability of tubular and undulated membrane structures generated or stabilized by cyto- or membrane-skeleton. We also describe the theory of spontaneous self-assembly of isotropic curved membrane nanodomains and derive the critical concentration above which the spontaneous necklace-like membrane protrusion growth is favorable. We show that the actin cytoskeleton growth inside the vesicle or cell can change its equilibrium shape, induce higher degree of segregation of membrane nanodomains or even alter the average orientation angle of anisotropic nanodomains such as BAR domains...
Protoplasma, 2010
Membrane nanotubes are a morphologically versatile group of membrane structures (some resembling filopodia), usually connecting two closely positioned cells. In this article, we set morphological criteria that distinguish the membrane nanotubes from filopodia, as there is no specific molecular marker known to date that unequivocally differentiates between filopodia and protruding nanotubes. Membrane nanotubes have been extensively studied from the morphological point of view and the transport that can be conducted through them, but little is known about the way they connect to the adjacent cell. Our results show that the nanotubes may connect to a neighboring cell by anchoring junctions. Among cell adhesion proteins, Ncadherin, β-catenin, nectin-2, afadin and the desmosomal protein desmoplakin-2 were immune-labeled. We found that N-cadherin and β-catenin are concentrated in nanotubes, while the concentrations of other junction-involved proteins are not increased in these structures. On the basis of data from transmission electron microscopy, we propose a model of the nanotube attachment where the connection of nanotubes is stabilized by several anchoring junctions, most likely adherens junctions that are formed when the nanotube is sliding along the target cell membrane.
Blood Cells, Molecules, and Diseases, 2007
Tubular budding of the erythrocyte membrane may be induced by exogenously added substances. It is shown that tubular budding may be explained by self-assembly of anisotropic membrane nanodomains into larger domains forming nanotubular membrane protrusions. In contrast to some previously reported theories, no direct external mechanical force is needed to explain the observed tubular budding of the bilayer membrane.
Unexpected Membrane Dynamics Unveiled by Membrane Nanotube Extrusion
Biophysical Journal, 2013
In cell mechanics, distinguishing the respective roles of the plasma membrane and of the cytoskeleton is a challenge. The difference in the behavior of cellular and pure lipid membranes is usually attributed to the presence of the cytoskeleton as explored by membrane nanotube extrusion. Here we revisit this prevalent picture by unveiling unexpected force responses of plasma membrane spheres devoid of cytoskeleton and synthetic liposomes. We show that a tiny variation in the content of synthetic membranes does not affect their static mechanical properties, but is enough to reproduce the dynamic behavior of their cellular counterparts. This effect is attributed to an amplified intramembrane friction. Reconstituted actin cortices inside liposomes induce an additional, but not dominant, contribution to the effective membrane friction. Our work underlines the necessity of a careful consideration of the role of membrane proteins on cell membrane rheology in addition to the role of the cytoskeleton.
Mechanics of Microtubule-Based Membrane Extension
Physical Review Letters, 1997
We observe quasistatic deformation of lipid vesicles from within, due to the polymerization of confined microtubules. A pair of long, narrow membrane sleeves appears, sheathing the microtubule ends as they grow. Spontaneous buckling reveals that the force generated can be greater than 2 pN. The evolution of shape and magnitude of force are consistent with a simple theory for the membrane free energy. We consider a model of the force generating mechanism in which thermal fluctuations of the membrane are "rectified" by the binding of tubulin dimers to the microtubule end.