scholarly journals Dynamic mechanochemical feedback between curved membranes and BAR protein self-organization

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Anabel-Lise Le Roux ◽  
Caterina Tozzi ◽  
Nikhil Walani ◽  
Xarxa Quiroga ◽  
Dobryna Zalvidea ◽  
...  
Keyword(s):  
Molecular Organization ◽  
Self Organization ◽  
Membrane Mechanics ◽  
Curvature Sensing ◽  
Cellular Processes ◽  
Mechanical Responses ◽  
Curved Membranes ◽  
Comprehensive Framework ◽  
Membrane Shape ◽  
Template Size

AbstractIn many physiological situations, BAR proteins reshape membranes with pre-existing curvature (templates), contributing to essential cellular processes. However, the mechanism and the biological implications of this reshaping process remain unclear. Here we show, both experimentally and through modelling, that BAR proteins reshape low curvature membrane templates through a mechanochemical phase transition. This phenomenon depends on initial template shape and involves the co-existence and progressive transition between distinct local states in terms of molecular organization (protein arrangement and density) and membrane shape (template size and spherical versus cylindrical curvature). Further, we demonstrate in cells that this phenomenon enables a mechanotransduction mode, in which cellular stretch leads to the mechanical formation of membrane templates, which are then reshaped into tubules by BAR proteins. Our results demonstrate the interplay between membrane mechanics and BAR protein molecular organization, integrating curvature sensing and generation in a comprehensive framework with implications for cell mechanical responses.

scholarly journals Mapping Cell Membrane Organization and Dynamics Using Soft Nano-Imprint Lithography

2019 ◽  
Author(s):  
T. Sansen ◽  
D. Sanchez-Fuentes ◽  
R. Rathar ◽  
A. Colom-Diego ◽  
F. El Alaoui ◽  
...  
Keyword(s):  
Cell Membrane ◽  
High Performance ◽  
Protein Complexes ◽  
Membrane Mechanics ◽  
Nanostructured Surfaces ◽  
Cellular Processes ◽  
State Organization ◽  
Cell Membrane Mechanics ◽  
Membrane Shape

AbstractMembrane shape is a key feature of many cellular processes, including cell differentiation, division, migration, and trafficking. The development of nanostructured surfaces allowing for the in situ manipulation of membranes in living cells is crucial to understand these processes, but this requires complicated and limited-access technologies. Here, we investigate the self-organization of cellular membranes by using a customizable and bench top method allowing to engineer 1D SiO2 nanopillar arrays of defined sizes and shapes on high-performance glass compatible with advanced microscopies. As a result of this original combination, we provide a mapping of the morphology-induced modulation of the cell membrane mechanics, dynamics and steady-state organization of key protein complexes implicated in cellular trafficking and signal transduction.

scholarly journals Dynamic Mechanochemical feedback between curved membranes and BAR protein self-organization

2020 ◽  
Author(s):  
Anabel-Lise Le Roux ◽  
Caterina Tozzi ◽  
Nikhil Walani ◽  
Xarxa Quiroga ◽  
Dobryna Zalvidea ◽  
...  
Keyword(s):  
Lipid Membranes ◽  
Mechanical Stretch ◽  
Mechanical Stimuli ◽  
Protein Orientation ◽  
Cellular Processes ◽  
Protein Membrane ◽  
Initial Membrane ◽  
Curved Membranes ◽  
Protein Response ◽  
Membrane Shape

AbstractIn many physiological situations, BAR proteins interact with, and reshape, pre-existing curved membranes, contributing to essential cellular processes. However, the non-equilibrium and timedependent process of reshaping, and its dependence on initial membrane shape, remains largely unknown. Here we explain, both experimentally and through modelling, how a BAR protein dynamically interacts with mechanically bent lipid membranes. We capture protein binding to curved membranes, and characterize a variety of dynamical reshaping events depending on membrane shape and protein arrangement. The events can be generally understood by an isotropic-to-nematic phase transition, in which low curvature templates with isotropic protein orientation progress towards highly curved lipid tubes with nematic protein arrangement. Our findings also apply in cells, where mechanical stretch triggers BAR-protein-membrane interactions that enable potential mechanotransduction mechanisms. Our results characterize and broaden the reshaping processes of BAR proteins on mechanically constrained membranes, demonstrating the interplay between membrane mechanical stimuli and BAR protein response.

scholarly journals The Interplay between the Self-Organization and Curvature Sensing in Septin Assemblies

2021 ◽  
Vol 120 (3) ◽  
pp. 190a
Author(s):  
Ehssan Nazockdast ◽  
Wenzheng Shi ◽  
Kevin Cannon ◽  
Amy Gladfelter
Keyword(s):  
The Self ◽  
Self Organization ◽  
Curvature Sensing

scholarly journals Miga-mediated endoplasmic reticulum–mitochondria contact sites regulate neuronal homeostasis

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Lingna Xu ◽  
Xi Wang ◽  
Jia Zhou ◽  
Yunyi Qiu ◽  
Weina Shang ◽  
...  
Keyword(s):  
Endoplasmic Reticulum ◽  
Mammalian Cells ◽  
Mitochondrial Dynamics ◽  
Molecular Organization ◽  
Lipid Transport ◽  
Cellular Processes ◽  
Contact Sites ◽  
Neuronal Homeostasis ◽  
Higher Eukaryotes ◽  
Lateral Sclerosis

Endoplasmic reticulum (ER)–mitochondria contact sites (ERMCSs) are crucial for multiple cellular processes such as calcium signaling, lipid transport, and mitochondrial dynamics. However, the molecular organization, functions, regulation of ERMCS, and the physiological roles of altered ERMCSs are not fully understood in higher eukaryotes. We found that Miga, a mitochondrion located protein, markedly increases ERMCSs and causes severe neurodegeneration upon overexpression in fly eyes. Miga interacts with an ER protein Vap33 through its FFAT-like motif and an amyotrophic lateral sclerosis (ALS) disease related Vap33 mutation considerably reduces its interaction with Miga. Multiple serine residues inside and near the Miga FFAT motif were phosphorylated, which is required for its interaction with Vap33 and Miga-mediated ERMCS formation. The interaction between Vap33 and Miga promoted further phosphorylation of upstream serine/threonine clusters, which fine-tuned Miga activity. Protein kinases CKI and CaMKII contribute to Miga hyperphosphorylation. MIGA2, encoded by the miga mammalian ortholog, has conserved functions in mammalian cells. We propose a model that shows Miga interacts with Vap33 to mediate ERMCSs and excessive ERMCSs lead to neurodegeneration.

scholarly journals An amphipathic helix enables septins to sense micrometer-scale membrane curvature

2019 ◽  
Vol 218 (4) ◽  
pp. 1128-1137 ◽  
Author(s):  
Kevin S. Cannon ◽  
Benjamin L. Woods ◽  
John M. Crutchley ◽  
Amy S. Gladfelter
Keyword(s):  
Membrane Curvature ◽  
Amphipathic Helix ◽  
Curvature Sensing ◽  
C Terminus ◽  
Number Of Binding Sites ◽  
Curved Membranes ◽  
Necessary And Sufficient ◽  
Micrometer Scale

Cell shape is well described by membrane curvature. Septins are filament-forming, GTP-binding proteins that assemble on positive, micrometer-scale curvatures. Here, we examine the molecular basis of curvature sensing by septins. We show that differences in affinity and the number of binding sites drive curvature-specific adsorption of septins. Moreover, we find septin assembly onto curved membranes is cooperative and show that geometry influences higher-order arrangement of septin filaments. Although septins must form polymers to stay associated with membranes, septin filaments do not have to span micrometers in length to sense curvature, as we find that single-septin complexes have curvature-dependent association rates. We trace this ability to an amphipathic helix (AH) located on the C-terminus of Cdc12. The AH domain is necessary and sufficient for curvature sensing both in vitro and in vivo. These data show that curvature sensing by septins operates at much smaller length scales than the micrometer curvatures being detected.

scholarly journals Bioelectrical understanding and engineering of cell biology

2020 ◽  
Vol 17 (166) ◽  
pp. 20200013 ◽  
Author(s):  
Zoe Schofield ◽  
Gabriel N. Meloni ◽  
Peter Tran ◽  
Christian Zerfass ◽  
Giovanni Sena ◽  
...  
Keyword(s):  
Systems Biology ◽  
Cell Biology ◽  
Genetic Basis ◽  
Control Cell ◽  
Status Quo ◽  
Cell Behaviour ◽  
Cellular Processes ◽  
Mechanical Responses ◽  
Predictive Understanding ◽  
Biology Research

The last five decades of molecular and systems biology research have provided unprecedented insights into the molecular and genetic basis of many cellular processes. Despite these insights, however, it is arguable that there is still only limited predictive understanding of cell behaviours. In particular, the basis of heterogeneity in single-cell behaviour and the initiation of many different metabolic, transcriptional or mechanical responses to environmental stimuli remain largely unexplained. To go beyond the status quo , the understanding of cell behaviours emerging from molecular genetics must be complemented with physical and physiological ones, focusing on the intracellular and extracellular conditions within and around cells. Here, we argue that such a combination of genetics, physics and physiology can be grounded on a bioelectrical conceptualization of cells. We motivate the reasoning behind such a proposal and describe examples where a bioelectrical view has been shown to, or can, provide predictive biological understanding. In addition, we discuss how this view opens up novel ways to control cell behaviours by electrical and electrochemical means, setting the stage for the emergence of bioelectrical engineering.

scholarly journals Pattern formation in reaction–diffusion system on membrane with mechanochemical feedback

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Naoki Tamemoto ◽  
Hiroshi Noguchi
Keyword(s):  
Pattern Formation ◽  
Plasma Membranes ◽  
Reaction Diffusion ◽  
Living Cells ◽  
Nonequilibrium Dynamics ◽  
Membrane Deformation ◽  
Brusselator Model ◽  
Diffusion Dynamics ◽  
Curved Membranes ◽  
Membrane Shape

Abstract Shapes of biological membranes are dynamically regulated in living cells. Although membrane shape deformation by proteins at thermal equilibrium has been extensively studied, nonequilibrium dynamics have been much less explored. Recently, chemical reaction propagation has been experimentally observed in plasma membranes. Thus, it is important to understand how the reaction–diffusion dynamics are modified on deformable curved membranes. Here, we investigated nonequilibrium pattern formation on vesicles induced by mechanochemical feedback between membrane deformation and chemical reactions, using dynamically triangulated membrane simulations combined with the Brusselator model. We found that membrane deformation changes stable patterns relative to those that occur on a non-deformable curved surface, as determined by linear stability analysis. We further found that budding and multi-spindle shapes are induced by Turing patterns, and we also observed the transition from oscillation patterns to stable spot patterns. Our results demonstrate the importance of mechanochemical feedback in pattern formation on deforming membranes.

scholarly journals Self-Organization and Information Processing: From Basic Enzymatic Activities to Complex Adaptive Cellular Behavior

2021 ◽  
Vol 12 ◽  
Author(s):  
Ildefonso M. De la Fuente ◽  
Luis Martínez ◽  
Jose Carrasco-Pujante ◽  
Maria Fedetz ◽  
José I. López ◽  
...  
Keyword(s):  
Information Processing ◽  
Metabolic Networks ◽  
Effective Connectivity ◽  
Molecular Organization ◽  
Regulatory Control ◽  
Self Organization ◽  
Enzymatic Reactions ◽  
Dynamic Architecture ◽  
Complex Adaptive ◽  
Quantitative Analyses

One of the main aims of current biology is to understand the origin of the molecular organization that underlies the complex dynamic architecture of cellular life. Here, we present an overview of the main sources of biomolecular order and complexity spanning from the most elementary levels of molecular activity to the emergence of cellular systemic behaviors. First, we have addressed the dissipative self-organization, the principal source of molecular order in the cell. Intensive studies over the last four decades have demonstrated that self-organization is central to understand enzyme activity under cellular conditions, functional coordination between enzymatic reactions, the emergence of dissipative metabolic networks (DMN), and molecular rhythms. The second fundamental source of order is molecular information processing. Studies on effective connectivity based on transfer entropy (TE) have made possible the quantification in bits of biomolecular information flows in DMN. This information processing enables efficient self-regulatory control of metabolism. As a consequence of both main sources of order, systemic functional structures emerge in the cell; in fact, quantitative analyses with DMN have revealed that the basic units of life display a global enzymatic structure that seems to be an essential characteristic of the systemic functional metabolism. This global metabolic structure has been verified experimentally in both prokaryotic and eukaryotic cells. Here, we also discuss how the study of systemic DMN, using Artificial Intelligence and advanced tools of Statistic Mechanics, has shown the emergence of Hopfield-like dynamics characterized by exhibiting associative memory. We have recently confirmed this thesis by testing associative conditioning behavior in individual amoeba cells. In these Pavlovian-like experiments, several hundreds of cells could learn new systemic migratory behaviors and remember them over long periods relative to their cell cycle, forgetting them later. Such associative process seems to correspond to an epigenetic memory. The cellular capacity of learning new adaptive systemic behaviors represents a fundamental evolutionary mechanism for cell adaptation.

scholarly journals Active contraction of microtubule networks

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Peter J Foster ◽  
Sebastian Fürthauer ◽  
Michael J Shelley ◽  
Daniel J Needleman
Keyword(s):  
Large Scale ◽  
Quantitative Agreement ◽  
Self Organization ◽  
Cellular Processes ◽  
Network Geometry ◽  
Initial Network ◽  
Fluid Theory ◽  
Scale Structures ◽  
Density Inhomogeneities ◽  
Microtubule Networks

Many cellular processes are driven by cytoskeletal assemblies. It remains unclear how cytoskeletal filaments and motor proteins organize into cellular scale structures and how molecular properties of cytoskeletal components affect the large-scale behaviors of these systems. Here, we investigate the self-organization of stabilized microtubules in Xenopus oocyte extracts and find that they can form macroscopic networks that spontaneously contract. We propose that these contractions are driven by the clustering of microtubule minus ends by dynein. Based on this idea, we construct an active fluid theory of network contractions, which predicts a dependence of the timescale of contraction on initial network geometry, a development of density inhomogeneities during contraction, a constant final network density, and a strong influence of dynein inhibition on the rate of contraction, all in quantitative agreement with experiments. These results demonstrate that the motor-driven clustering of filament ends is a generic mechanism leading to contraction.

scholarly journals From cartoons to quantitative models in Golgi transport

2020 ◽  
Author(s):  
D. Nicolas Quiros ◽  
Luis S. Mayorga
Keyword(s):  
Golgi Apparatus ◽  
Mathematical Models ◽  
Chemical Reactions ◽  
Molecular Interactions ◽  
Cell Biology ◽  
Lipid Transport ◽  
Self Organization ◽  
Agent Based ◽  
Cellular Processes ◽  
Golgi Transport

ABSTRACTCell biology is evolving to become a more formal and quantitative science. In particular, several mathematical models have been proposed to address Golgi self-organization and protein and lipid transport. However, most scientific articles about the Golgi apparatus are still using static cartoons to represent their findings that miss the dynamism of this organelle. In this report, we show that schematic drawings of Golgi trafficking can be easily translated into an Agent-Based Model (ABM) using the Repast platform. The simulations generate an active interplay among cisternae and vesicles rendering quantitative predictions about Golgi stability and transport of soluble and membrane-associated cargoes. The models can incorporate complex networks of molecular interactions and chemical reactions by association with COPASI, a software that handles Ordinary Differential Equations. The strategy described provides a simple, flexible, and multiscale support to analyze Golgi transport. The simulations can be used to address issues directly linked to the mechanism of transport or as a way to incorporate the complexity of trafficking to other cellular processes that occur in dynamic organelles.

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