The 2018 biomembrane curvature and remodeling roadmap

Bassereau, Patricia; Jin, Rui; Baumgart, Tobias; Deserno, Markus; Dimova, Rumiana; Frolov, Vadim A.; Bashkirov, Pavel V.; Grubmüller, Helmut; Jahn, Reinhard; Risselada, Herre Jelger; Johannes, Ludger; Kozlov, Michael M.; Lipowsky, Reinhard; Pucadyil, Thomas J.; Zeno, Wade F.; Stachowiak, Jeanne C.; Stamou, Dimitrios; Breuer, Artù; Lauritsen, Line; Simon, Camille; Sykes, Cécile; Voth, Gregory A.; Weikl, Thomas R.

doi:10.1088/1361-6463/aacb98

Cited by 239 publications

(201 citation statements)

References 158 publications

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“…In addition, the filamentous growth of multilamellar oleate vesicles (≈4 µm) was used to mimic the full proliferation cycle of growth and division, [71] and the chemistry was extended to other surface-active molecules beyond oleate. [76,78,79] Slow flip-flop molecules induce an increase in the membrane spontaneous curvature due to their asymmetric incorporation into the outer leaflet of the membrane, resulting in tubulation, [80][81][82] increased membrane tension, and eventually rupture. With respect to this distinction, the addition of oleate to preformed phospholipid vesicles was used in other attempts to mimic selfreproduction as an intermediate approach.…”

Section: Polymer-rich Dropletsmentioning

confidence: 99%

Directed Growth of Biomimetic Microcompartments

et al. 2019

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twilight zone), it is widely recognized that the formation of micro-and nanocompartments is an essential ingredient of all forms of life. This spatial constraint serves numerous purposes, including the segregation and protection from the environment (to allow for individuality and maintenance), the establishment of gradients (to enable and make use of outof-equilibrium conditions), and the role of 2D and 3D confinement for self-organization phenomena, all of which serve to overcome the overall "dilution problem." In order to fulfill another cornerstone of life-proliferation-compartments also need to change with time by fusion, growth, and division. In particular, the dynamic growth of compartments is an essential prerequisite for enabling selfreproduction as a fundamental life process, both in simplistic systems such as droplets or fatty acid-based vesicles, as well as for lipid vesicle compartments with membranes that resemble the biomembranes of today's cells. In this context, we argue that growth deserves more attention, not only because growth precedes division but also because of the difficulty to realize growth compared to division, especially in the case of lipid vesicles, where budding and division has been observed in response to various factors. This growth aspect has also been recognized in basic theoretical models of living systems such as Ganti's chemoton, [1,2] for which the increase of membrane area (referred to as membrane formation) was postulated to be one of three subsystems, characterizing living entities from a chemical viewpoint. The autopoietic theory was also centered on the membrane but focused on self-maintenance rather than on (self-)reproduction. [3,4] However, such a self-maintaining system could also enter a self-reproduction mode, manifested by growth, if homeostatic misbalance leads to excess membrane formation as shown in a thought experiment by Luisi. [3] In this progress report, we review the existing approaches for growth of compartments in the context of bottom-up synthetic biology and protobiology. We consider mainly micrometer-sized compartments due to their characteristic cellular dimensions; this feature also ensures that the area and curvature of the interface or the bounding membrane has less influence on the enclosed solution. Microcompartments of various origins and chemistries have been used as protocell models, and many studies have addressed growth and division simultaneously in an ambitious effort to mimic self-reproduction. Contemporary biological cells are sophisticated and highly compartmentalized. Compartmentalization is an essential principle of prebiotic life as well as a key feature in bottom-up synthetic biology research.In this review, the dynamic growth of compartments as an essential prerequisite for enabling self-reproduction as a fundamental life process is discussed. The micrometer-sized compartments are focused on due to their cellular dimensions. Two types of compartments are considered, membraneless droplets and membrane-bound microcompartments. Gr...

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Section: Polymer-rich Dropletsmentioning

confidence: 99%

Directed Growth of Biomimetic Microcompartments

et al. 2019

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“…Lipid bilayers are present both in the plasma membrane and in intracellular organelles [1] and have an extremely heterogeneous composition [2]. They consist of many different types of lipids, integral, and peripheral membrane proteins [3], all of which are important in cellular function [4]. One of the classic features of cellular membranes is their ability to bend out of plane and this has been the focus of many studies, both theoretical and experimental, over the past five decades [5,6,7,8,9].…”

Section: Introductionmentioning

confidence: 99%

Transport Phenomena in Fluid Films with Curvature Elasticity

Mahapatra

Saintillan

Rangamani

2020

Preprint

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Cellular membranes are elastic lipid bilayers that contain a variety of proteins, including ion channels, receptors, and scaffolding proteins. These proteins are known to diffuse in the plane of the membrane and to influence the bending of the membrane. Experiments have shown that lipid flow in the plane of the membrane is closely coupled with the diffusion of proteins. Thus there is a need for a comprehensive framework that accounts for the interplay between these processes. Here, we present a theory for the coupled in-plane viscous flow of lipids, diffusion of transmembrane proteins, and curvature elastic deformation of lipid bilayers. The proteins in the membrane are modeled such that they influence membrane bending by inducing a spontaneous curvature. We formulate the free energy of the membrane with a Helfrich-like curvature elastic energy density function modified to account for the chemical potential energy of proteins. We derive the conservation laws and equations of motion for this system. Finally, we present results from dimensional analysis and numerical simulations and demonstrate the effect of coupled transport processes in governing the dynamics of membrane bending and protein diffusion.

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“…Finally, we aimed to clarify the molecular mechanism driving the deformation of the membrane induced by M1. Several mechanisms for the induction of membrane curvature driven by (non trans-membrane) proteins were described, including: membrane insertion, protein crowding and scaffolding (47,48). In order to distinguish among these possibilities, we observed M1-GUV interaction in conditions in which M1 could bind to the membrane but protein multimerization was hindered (i.e.…”

Section: Discussionmentioning

confidence: 99%

Influenza A matrix protein M1 is sufficient to induce lipid membrane deformation

Dahmani

Ludwig

Chiantia

2019

Preprint

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The matrix protein M1 of the Influenza A virus is considered to mediate viral assembly and budding at the plasma membrane (PM) of infected cells. In order for a new viral particle to form, the PM lipid bilayer has to bend into a vesicle towards the extracellular side. Studies in cellular models have proposed that different viral proteins might be responsible for inducing membrane curvature in this context (including M1), but a clear consensus has not been reached. In this study, we use a combination of fluorescence microscopy, cryogenic transmission electron microscopy (cryo-TEM), cryo-electron tomography (cryo-ET) and scanning fluorescence correlation spectroscopy (sFCS) to investigate M1-induced membrane deformation in biophysical models of the PM. Our results indicate that M1 is indeed capable to cause membrane curvature in lipid bilayers containing negatively-charged lipids, in the absence of other viral components. Furthermore, we prove that simple protein binding is not sufficient to induce membrane restructuring. Rather, it appears that stable M1-M1 interactions and multimer formation are required in order to alter the bilayer threedimensional structure, through the formation of a protein scaffold. Finally, our results suggest that, in a physiological context, M1-induced membrane deformation might be modulated by the initial bilayer curvature and the lateral organization of membrane components (i.e. the presence of lipid domains). FIGURE 4: M1 layer interacting with the membrane is stable even after lipid removal. A-B: LSM confocal image of a typical GUV composed of DOPC:cholesterol:DOPS 50:20:30, after incubation with 5 µM M1-Alexa488 (green channel, panel A). The lipid bilayer is visualized via the addition of 0.05 mol% Rhodamine-DOPE (red channel, panel B). C-D: LSM confocal image of a typical GUV after treatment for 5 min with detergent (e.g. Triton X-100 1.7 mM). Panel C represent the signal from M1-Alexa488. Panel D represents the signal from Rhodamine-DOPE. The excitation laser power used to acquire the image shown in panel D was ~10 times higher than the power used to acquire the image shown in panel B. GUVs contained 150 mM sucrose in their lumen and were suspended in a phosphate buffered protein solution (pH 7.4) with similar osmolarity (see Materials and Methods). Scale bars are 5 µM. Images were acquired at 23°C.

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The 2018 biomembrane curvature and remodeling roadmap

Cited by 239 publications

References 158 publications

Directed Growth of Biomimetic Microcompartments

Directed Growth of Biomimetic Microcompartments

Transport Phenomena in Fluid Films with Curvature Elasticity

Influenza A matrix protein M1 is sufficient to induce lipid membrane deformation

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