Molecular Motors—Self-Organization of Cytoskeletal Network

Kishore Dutta

doi:10.4236/ym.2017.14021

Cytoplasmic self-organization established by internal lipid membranes in the interplay with either actin or microtubules

10.1101/506436 ◽

2018 ◽

Cited By ~ 1

Author(s):

Sindy K. Y. Tang ◽

Malte Renz ◽

Tom Shemesh ◽

Meghan Driscoll ◽

Jennifer Lippincott-Schwartz

Keyword(s):

Molecular Motors ◽

Lipid Membranes ◽

Lipid Membrane ◽

Protein Structures ◽

Specific Protein ◽

Self Organization ◽

Network Systems ◽

3 Dimensional ◽

Cytoskeletal Network ◽

Cytoplasmic Organization

AbstractCells harbor an intrinsic organization of their components. Specific protein structures, as the centrosome, have been described master regulators of cell organization. In the absence of these key elements, however, cytoplasmic selforganization has nevertheless been observed. Cytoplasmic self-organization was postulated to arise from the interaction of microtubules with molecular motors on lipid membrane surfaces.Here, we show that lipid membranes are capable of organizing both major cytoskeletal systems, microtubules and actin, even if one or the other cytoskeletal system is completely paralyzed. A microfluidic droplet system and Xenopus oocyte extracts enabled us to build an artificial cell and study minimal requirements for cellular self-organization. Mathematical modeling reveals the interaction of lipid membranes with any filament system through molecular motors as a universal principle of cytoplasmic self-organization. Both cytoskeletal systems form mechanisms to establish robust 2-dimensional selforganization and self-centering. Pharmacologic inhibition of the cytoskeletal network systems helps dissect specific contributions of each network in the interplay with lipid membranes with regards to 2- and 3-dimensional organization, time and length scale of cytoplasmic organization and the degree of concentration of the centered elements. While microtubules provide 3-dimensional polarity, actin filaments ensure fast and dense compaction and long-range organization.

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Self-Organization and Cooperativity of Weakly Coupled Molecular Motors under Unequal Loading

Physical Review Letters ◽

10.1103/physrevlett.102.118104 ◽

2009 ◽

Vol 102 (11) ◽

Cited By ~ 30

Author(s):

Jan Brugués ◽

Jaume Casademunt

Keyword(s):

Molecular Motors ◽

Self Organization ◽

Weakly Coupled

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Actin-microtubule dynamic composite forms responsive active matter with memory

10.1101/2022.01.10.475629 ◽

2022 ◽

Author(s):

Ondrej Kucera ◽

Jeremie Gaillard ◽

Christophe Guerin ◽

Manuel Thery ◽

Laurent Blanchoin

Keyword(s):

Molecular Motors ◽

Actin Filaments ◽

Adaptive Plasticity ◽

Self Assembling ◽

Cytoskeletal Network ◽

External Stimuli ◽

With Memory ◽

Structurally Stable ◽

Structural Memory

Active cytoskeletal materials in vitro demonstrate self-organising properties similar to those observed in their counterparts in cells. However, the search to emulate phenomena observed in the living matter has fallen short of producing a cytoskeletal network that would be structurally stable yet possessing adaptive plasticity. Here, we address this challenge by combining cytoskeletal polymers in a composite, where self-assembling microtubules and actin filaments collectively self-organise due to the activity of microtubules-percolating molecular motors. We demonstrate that microtubules spatially organise actin filaments that in turn guide microtubules. The two networks align in an ordered fashion using this feedback loop. In this composite, actin filaments can act as structural memory and, depending on the concentration of the components, microtubules either write this memory or get guided by it. The system is sensitive to external stimuli suggesting possible autoregulatory behaviour in changing mechanochemical environment. We thus establish artificial active actin-microtubule composite as a system demonstrating architectural stability and plasticity.

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A physical perspective on cytoplasmic streaming

Interface Focus ◽

10.1098/rsfs.2015.0030 ◽

2015 ◽

Vol 5 (4) ◽

pp. 20150030 ◽

Cited By ~ 57

Author(s):

Raymond E. Goldstein ◽

Jan-Willem van de Meent

Keyword(s):

Molecular Motors ◽

Cytoplasmic Streaming ◽

Aquatic Plant ◽

Broad Class ◽

Self Organization ◽

Cell Periphery ◽

Wide Range ◽

Streaming Transport ◽

Eukaryotic Organisms

Organisms show a remarkable range of sizes, yet the dimensions of a single cell rarely exceed 100 µm. While the physical and biological origins of this constraint remain poorly understood, exceptions to this rule give valuable insights. A well-known counterexample is the aquatic plant Chara , whose cells can exceed 10 cm in length and 1 mm in diameter. Two spiralling bands of molecular motors at the cell periphery drive the cellular fluid up and down at speeds up to 100 µm s −1 , motion that has been hypothesized to mitigate the slowness of metabolite transport on these scales and to aid in homeostasis. This is the most organized instance of a broad class of continuous motions known as ‘cytoplasmic streaming’, found in a wide range of eukaryotic organisms—algae, plants, amoebae, nematodes and flies—often in unusually large cells. In this overview of the physics of this phenomenon, we examine the interplay between streaming, transport and cell size and discuss the possible role of self-organization phenomena in establishing the observed patterns of streaming.

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A gelation transition enables the self-organization of bipolar metaphase spindles

10.1101/2021.01.15.426844 ◽

2021 ◽

Author(s):

Benjamin A. Dalton ◽

David Oriola ◽

Franziska Decker ◽

Frank Jülicher ◽

Jan Brugués

Keyword(s):

Molecular Motors ◽

Mitotic Spindle ◽

Large Scale ◽

Relaxation Times ◽

Network Connectivity ◽

The Self ◽

Self Organization ◽

Bipolar Structure ◽

Microtubule Polarity ◽

Microtubule Transport

The mitotic spindle is a highly dynamic bipolar structure that emerges from the self-organization of microtubules, molecular motors, and other proteins. Sustained motor-driven poleward flows of short dynamic microtubules play a key role in the bipolar organization of spindles. However, it is not understood how the local activity of motor proteins generates these large-scale coherent poleward flows. Here, we combine experiments and simulations to show that a gelation transition enables long-ranged microtubule transport causing spindles to self-organize into two oppositely polarized microtubule gels. Laser ablation experiments reveal that local active stresses generated at the spindle midplane propagate through the structure thereby driving global coherent microtubule flows. Simulations show that microtubule gels undergoing rapid turnover can exhibit long stress relaxation times, in agreement with the long-ranged flows observed in experiments. Finally, we show that either disrupting such flows or decreasing the network connectivity can lead to a microtubule polarity reversal in spindles both in the simulations and in the experiments. Thus, we uncover an unexpected connection between spindle rheology and architecture in spindle self-organization.

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A model for the self-organization of microtubules driven by molecular motors

The European Physical Journal B ◽

10.1007/s100510051150 ◽

2000 ◽

Vol 15 (3) ◽

pp. 483-492 ◽

Cited By ~ 19

Author(s):

B. Bassetti ◽

M. Cosentino Lagomarsino ◽

P. Jona

Keyword(s):

Molecular Motors ◽

The Self ◽

Self Organization

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Filamentous active matter: Band formation, bending, buckling, and defects

Science Advances ◽

10.1126/sciadv.aaw9975 ◽

2020 ◽

Vol 6 (30) ◽

pp. eaaw9975 ◽

Cited By ~ 1

Author(s):

Gerard A. Vliegenthart ◽

Arvind Ravichandran ◽

Marisol Ripoll ◽

Thorsten Auth ◽

Gerhard Gompper

Keyword(s):

Molecular Motors ◽

Persistence Length ◽

Topological Defects ◽

Domain Size ◽

Self Organization ◽

Design Strategies ◽

Band Formation ◽

Microscopic Interactions ◽

Large Length ◽

Microscopy Techniques

Motor proteins drive persistent motion and self-organization of cytoskeletal filaments. However, state-of-the-art microscopy techniques and continuum modeling approaches focus on large length and time scales. Here, we perform component-based computer simulations of polar filaments and molecular motors linking microscopic interactions and activity to self-organization and dynamics from the filament level up to the mesoscopic domain level. Dynamic filament cross-linking and sliding and excluded-volume interactions promote formation of bundles at small densities and of active polar nematics at high densities. A buckling-type instability sets the size of polar domains and the density of topological defects. We predict a universal scaling of the active diffusion coefficient and the domain size with activity, and its dependence on parameters like motor concentration and filament persistence length. Our results provide a microscopic understanding of cytoplasmic streaming in cells and help to develop design strategies for novel engineered active materials.

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Filament Rigidity and Connectivity Tune the Deformation Modes of Active Biopolymer Networks

10.1101/141796 ◽

2017 ◽

Cited By ~ 1

Author(s):

Samantha Stam ◽

Simon L. Freedman ◽

Shiladitya Banerjee ◽

Kimberly L. Weirich ◽

Aaron R. Dinner ◽

...

Keyword(s):

Molecular Motors ◽

The Self ◽

Self Organization ◽

Cross Linking ◽

Physical Parameters ◽

Active Materials ◽

Wide Range ◽

Filament Bundles ◽

Deformation Modes ◽

Insight Into

ABSTRACTMolecular motors embedded within collections of actin and microtubule filaments underlie the dynamic behaviors of cytoskeletal assemblies. Understanding the physics of such motor-filament materials is critical to developing a physical model of the cytoskeleton and the design of biomimetic active materials. Here, we demonstrate through experiments and simulations that the rigidity and connectivity of filaments in active biopolymer networks regulates the anisotropy and the length scale of the underlying deformations, yielding materials with varying contractility. Semi-flexible filaments that can be compressed and bent by motor stresses undergo deformations that are predominantly biaxial. By contrast, rigid filament bundles contract via actomyosin sliding deformations that are predominantly uniaxial. Networks dominated by filament buckling are robustly contractile under a wide range of connectivities, while networks dominated by actomyosin sliding can be tuned from contractile to extensile through reduced connectivity via cross-linking. These results identify physical parameters that control the forces generated within motor-filament arrays, and provide insight into the self-organization and mechanics of cytoskeletal assemblies.

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