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

2018 ◽  
Author(s):  
Haleh Alimohamadi ◽  
Ben Ovryn ◽  
Padmini Rangamani

AbstractMembrane nanotubes have been identified as dynamic structures for cells to connect over long distances. Nanotubes typically appear as thin and cylindrical tubes, but they may also have a beaded architecture along the tube. In this paper, we study the role of membrane mechanics in governing the architecture of these tubes and show that the formation of beadlike structures along the nanotubes can result from local heterogeneities in the membrane either due to protein aggregation or due to membrane composition. We present numerical results that predict how membrane properties, protein density, and local tension compete to create a phase space that governs the morphology of a nanotube. We also find that there is an energy barrier that prevents two beads from fusing. These results suggest that the membrane-protein interaction, membrane composition, and membrane tension closely govern the tube radius, number of beads, and the bead morphology.

2016 ◽  
Vol 114 (2) ◽  
pp. 328-333 ◽  
Author(s):  
Matthias Garten ◽  
Lars D. Mosgaard ◽  
Thomas Bornschlögl ◽  
Stéphane Dieudonné ◽  
Patricia Bassereau ◽  
...  

Studying how the membrane modulates ion channel and transporter activity is challenging because cells actively regulate membrane properties, whereas existing in vitro systems have limitations, such as residual solvent and unphysiologically high membrane tension. Cell-sized giant unilamellar vesicles (GUVs) would be ideal for in vitro electrophysiology, but efforts to measure the membrane current of intact GUVs have been unsuccessful. In this work, two challenges for obtaining the “whole-GUV” patch-clamp configuration were identified and resolved. First, unless the patch pipette and GUV pressures are precisely matched in the GUV-attached configuration, breaking the patch membrane also ruptures the GUV. Second, GUVs shrink irreversibly because the membrane/glass adhesion creating the high-resistance seal (>1 GΩ) continuously pulls membrane into the pipette. In contrast, for cell-derived giant plasma membrane vesicles (GPMVs), breaking the patch membrane allows the GPMV contents to passivate the pipette surface, thereby dynamically blocking membrane spreading in the whole-GMPV mode. To mimic this dynamic passivation mechanism, beta-casein was encapsulated into GUVs, yielding a stable, high-resistance, whole-GUV configuration for a range of membrane compositions. Specific membrane capacitance measurements confirmed that the membranes were truly solvent-free and that membrane tension could be controlled over a physiological range. Finally, the potential for ion transport studies was tested using the model ion channel, gramicidin, and voltage-clamp fluorometry measurements were performed with a voltage-dependent fluorophore/quencher pair. Whole-GUV patch-clamping allows ion transport and other voltage-dependent processes to be studied while controlling membrane composition, tension, and shape.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Mayte Bonilla-Quintana ◽  
Florentin Wörgötter

AbstractDendritic spines, small protrusions of the dendrites, enlarge upon LTP induction, linking morphological and functional properties. Although the role of actin in spine enlargement has been well studied, little is known about its relationship with mechanical membrane properties, such as membrane tension, which is involved in many cell processes, like exocytosis. Here, we use a 3D model of the dendritic spine to investigate how polymerization of actin filaments can effectively elevate the membrane tension to trigger exocytosis in a domain close to the tip of the spine. Moreover, we show that the same pool of actin promotes full membrane fusion after exocytosis and spine stabilization.


2017 ◽  
Vol 114 (7) ◽  
pp. E1118-E1127 ◽  
Author(s):  
Julian E. Hassinger ◽  
George Oster ◽  
David G. Drubin ◽  
Padmini Rangamani

A critical step in cellular-trafficking pathways is the budding of membranes by protein coats, which recent experiments have demonstrated can be inhibited by elevated membrane tension. The robustness of processes like clathrin-mediated endocytosis (CME) across a diverse range of organisms and mechanical environments suggests that the protein machinery in this process has evolved to take advantage of some set of physical design principles to ensure robust vesiculation against opposing forces like membrane tension. Using a theoretical model for membrane mechanics and membrane protein interaction, we have systematically investigated the influence of membrane rigidity, curvature induced by the protein coat, area covered by the protein coat, membrane tension, and force from actin polymerization on bud formation. Under low tension, the membrane smoothly evolves from a flat to budded morphology as the coat area or spontaneous curvature increases, whereas the membrane remains essentially flat at high tensions. At intermediate, physiologically relevant, tensions, the membrane undergoes a “snap-through instability” in which small changes in the coat area, spontaneous curvature or membrane tension cause the membrane to “snap” from an open, U-shape to a closed bud. This instability can be smoothed out by increasing the bending rigidity of the coat, allowing for successful budding at higher membrane tensions. Additionally, applied force from actin polymerization can bypass the instability by inducing a smooth transition from an open to a closed bud. Finally, a combination of increased coat rigidity and force from actin polymerization enables robust vesiculation even at high membrane tensions.


2020 ◽  
Author(s):  
Mayte Bonilla-Quintana ◽  
Florentin Wörgötter

AbstractDendritic spines, small protrusions of the dendrites, enlarge upon LTP induction, linking morphological and functional properties. Although the role of actin in spine enlargement has been well studied, little is known about its relationship with mechanical membrane properties, such as membrane tension, which is involved in many cell processes, like exocytosis. Here, we use a 3D model of the dendritic spine to investigate how polymerization of actin filaments can effectively elevate the membrane tension to trigger exocytosis in a domain close to the tip of the spine. Moreover, we show that the same pool of actin promotes full membrane fusion after exocytosis and spine stabilization.


2017 ◽  
Author(s):  
Hao Wu ◽  
Marco Avila Ponce de León ◽  
Hans G. Othmer

AbstractRecent research has shown that motile cells can adapt their mode of propulsion to the mechanical properties of the environment in which they find themselves – crawling in some environments while swimming in others. The latter can involve movement by blebbing or other cyclic shape changes, and both highly-simplified and more realistic models of these modes have been studied previously. Herein we study swimming that is driven by membrane tension gradients that arise from flows in the actin cortex underlying the membrane, and does not involve imposed cyclic shape changes. Such gradients can lead to a number of different characteristic cell shapes, and our first objective is to understand how different distributions of membrane tension influence the shape of cells in a quiescent fluid. We then analyze the effects of spatial variation in other membrane properties, and how they interact with tension gradients to determine the shape. We also study the effect of fluid-cell interactions and show how tension leads to cell movement, how the balance between tension gradients and a variable bending modulus determine the shape and direction of movement, and how the efficiency of movement depends on the properties of the fluid and the distribution of tension and bending modulus in the membrane.Dedicated to the memory of Karl P. Hadeler, a pioneer in the field of Mathematical Biology and a friend and mentor to many.


2017 ◽  
Vol 63 ◽  
pp. 60-65 ◽  
Author(s):  
Vaddi Damodara Reddy ◽  
Pannuru Padmavathi ◽  
Saradamma Bulle ◽  
Ananda Vardhan Hebbani ◽  
Shakeela Begum Marthadu ◽  
...  

2022 ◽  
Author(s):  
Viola Introini ◽  
Alejandro Marin-Menendez ◽  
Guilherme Nettesheim ◽  
Yen-Chun Lin ◽  
Silvia N Kariuki ◽  
...  

Malaria parasites such as Plasmodium falciparum have exerted formidable selective pressures on the human genome. Of the human genetic variants associated with malaria protection, beta thalassaemia (a haemoglobinopathy) was the earliest to be associated with malaria prevalence. However, the malaria protective properties of beta thalassaemic erythrocytes remain unclear. Here we studied the mechanics and surface protein expression of beta thalassaemia heterozygous erythrocytes, measured their susceptibility to P. falciparum invasion, and calculated the energy required for merozoites to invade them. We found invasion-relevant differences in beta thalassaemic cells versus matched controls, specifically: elevated membrane tension, reduced bending modulus, and higher levels of expression of the major invasion receptor basigin. However, these differences acted in opposition to each other with respect to their likely impact on invasion, and overall we did not observe beta thalassaemic cells to have lower P. falciparum invasion efficiency for any of the strains tested.


2014 ◽  
Author(s):  
Erin C. McKiernan

Motor activity, like that producing locomotion, is generated by networks of neurons. At the last output level of these networks are the motor neurons, which send signals to the muscles, causing them to contract. Current research in motor control is focused on finding out how motor neurons contribute to shaping the timing of motor behaviors. Are motor neurons just passive relayers of the signals they receive? Or, do motor neurons shape the signals before passing them on to the muscles, thereby influencing the timing of the behavior? It is now well accepted that motor neurons have active, intrinsic membrane properties - there are ion channels in the cell membrane that allow motor neurons to respond to input in non-linear and diverse ways. However, few direct tests of the role of motor neuron intrinsic properties in shaping motor behavior have been carried out, and many questions remain about the role of specific ion channel genes in motor neuron function. In this study, two potassium channel transgenes were expressed in Drosophila larvae, causing motor neurons to fire at lower levels of current stimulation and at higher frequencies, thereby increasing excitability. Mosaic animals were created in which some identified motor neurons expressed the transgenes while others did not. Motor output underlying crawling was compared in muscles innervated by control and experimental neurons in the same animals. Counterintuitively, no effect of the transgenic manipulation on motor output was seen. Future experiments are outlined to determine how the larval nervous system produces normal motor output in the face of altered motor neuron excitability.


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