Molecular motors robustly drive active gels to a critically connected state

Alvarado, José; Sheinman, Michael; Sharma, Abhinav; MacKintosh, F. C.; Koenderink, Gijsje H.

doi:10.1038/nphys2715

Cited by 205 publications

(318 citation statements)

References 58 publications

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“…As observed in other in vitro works, long actin filaments form bundled structures (37,54) or contracted networks (35,37,59) under the action of myosin II, whereas at the shorter actin filament lengths used here, they gave rise to compact, isolated asters. We find that the following parameters characterize the different static states obtained: (i) actin filament length, (ii) myosin-to-actin filament ratio, and (iii) F-actin concentration.…”

Section: Discussionmentioning

confidence: 71%

Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer

Köster

Husain

Iljazi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

137

149

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The surface of a living cell provides a platform for receptor signaling, protein sorting, transport, and endocytosis, whose regulation requires the local control of membrane organization. Previous work has revealed a role for dynamic actomyosin in membrane protein and lipid organization, suggesting that the cell surface behaves as an active composite composed of a fluid bilayer and a thin film of active actomyosin. We reconstitute an analogous system in vitro that consists of a fluid lipid bilayer coupled via membrane-associated actinbinding proteins to dynamic actin filaments and myosin motors. Upon complete consumption of ATP, this system settles into distinct phases of actin organization, namely bundled filaments, linked apolar asters, and a lattice of polar asters. These depend on actin concentration, filament length, and actin/myosin ratio. During formation of the polar aster phase, advection of the self-organizing actomyosin network drives transient clustering of actin-associated membrane components. Regeneration of ATP supports a constitutively remodeling actomyosin state, which in turn drives active fluctuations of coupled membrane components, resembling those observed at the cell surface. In a multicomponent membrane bilayer, this remodeling actomyosin layer contributes to changes in the extent and dynamics of phasesegregating domains. These results show how local membrane composition can be driven by active processes arising from actomyosin, highlighting the fundamental basis of the active composite model of the cell surface, and indicate its relevance to the study of membrane organization.T he cell surface mediates interactions between the cell and the outside world by serving as the site for signal transduction. It also facilitates the uptake and release of cargo and supports adhesion to substrates. These diverse roles require that the cell surface components involved in each function are spatially and temporally organized into domains spanning a few nanometers (nanoclusters) to several micrometers (microdomains). The cell surface itself may be considered as a fluid-lipid bilayer wherein proteins are embedded (1). In the living cell, this multicomponent system is supported by an actin cortex, composed of a branched network of actin and a collection of filaments (2-4).Current models of membrane organization fall into three categories: those invoking lipid-lipid and lipid-protein interactions in the plasma membrane [e.g., the fluid mosaic model (1, 5) and the lipid raft hypothesis (6)], or those that appeal to the membrane-associated actin cortex (e.g., the picket fence model) (7), or a combination of these (8, 9). Although these models based on thermodynamic equilibrium principles have successfully explained the organization and dynamics of a range of membrane components and molecules, there is a growing class of phenomena that appears inconsistent with chemical and thermal equilibrium, which might warrant a different explanation. These include aspects of the organization and dynamics of outer leaflet...

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Section: Discussionmentioning

confidence: 71%

Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer

Köster

Husain

Iljazi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

137

149

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“…The geometry for the simulations was an ellipse of half-axes a = 19.2 µm, b = 6.6 µm with the MTOC being 1.2 µm off the center of the ellipse in x-and in y-direction which are representative parameters for the cell geometry discussed in [206]. Figures (A-B) (simulations) are taken from [110] and figures (C-D) (experiments) from [206] have been studied in in vitro experiments [52,203,11,104]. We shall not address this large field of research in this review.…”

Section: Actin Filamentsmentioning

confidence: 99%

Intracellular transport driven by cytoskeletal motors: General mechanisms and defects

2015

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Cells are the elementary units of living organisms, which are able to carry out many vital functions. These functions rely on active processes on a microscopic scale. Therefore, they are strongly out-of-equilibrium systems, which are driven by continuous energy supply. The tasks that have to be performed in order to maintain the cell alive require transportation of various ingredients, some being small, others being large. Intracellular transport processes are able to induce concentration gradients and to carry objects to specific targets. These processes cannot be carried out only by diffusion, as cells may be crowded, and quite elongated on molecular scales. Therefore active transport has to be organized.The cytoskeleton, which is composed of three types of filaments (microtubules, actin and intermediate filaments), determines the shape of the cell, and plays a role in cell motion. It also serves as a road network for a special kind of vehicles, namely the cytoskeletal motors. These molecules can attach to a cytoskeletal filament, perform directed motion, possibly carrying along some cargo, and then detach.It is a central issue to understand how intracellular transport driven by molecular motors is regulated. The interest for this type of question was enhanced when it was discovered that intracellular transport breakdown is one of the signatures of some neuronal diseases like the Alzheimer.We give a survey of the current knowledge on microtubule based intracellular transport. Our review includes on the one hand an overview of biological facts, obtained from experiments, and on the other hand a presentation of some modeling attempts based on cellular automata. We present some background knowledge on the original and variants of the TASEP (Totally Asymmetric Simple Exclusion Process), before turning to more application oriented models. After addressing microtubule based transport in general, with a focus on in vitro experiments, and on cooperative effects in the transportation of large cargos by multiple motors, we concentrate on axonal transport, because of its relevance for neuronal diseases. Some important characteristics of axonal transport is that it takes place in a confined environment; Besides several types of motors are involved, that move in opposite directions. It is a challenge to understand how this bidirectional transport is organized. We review several features that could contribute to the efficiency of bidirectional transport in the axon, including in particular the role of motor-motor interactions and of the dynamics of the underlying microtubule network. Finally, we also discuss some open questions that may be relevant for future research in this field.

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“…Myosin motors pull the filaments together, thereby exerting contractile forces on the network [5]. The resulting crosslinker unbinding and actin filament movement fundamentally alter the underlying actin network (see supplementary movies in [10]). …”

Section: Experimental Findingsmentioning

confidence: 99%

“…In their experiments, Alvarado et al [10] prepared a quasi-two dimensional network of actin filaments, about 2.5 × 2.5mm 2 in size, which are connected by fascin crosslinkers, illustrated schematically in Fig. 1.…”

Section: Experimental Findingsmentioning

confidence: 99%

“…An actomyosin network consists of an actin polymer network connected by crosslinker proteins and motor protein myosins that generate internal stresses on the network. A recent discovery shows that for a range of experimental parameters, actomyosin networks contract to clusters with a power-law size distribution [Alvarado J. et al (2013) Nature Physics 9 591]. Here, we argue that actomyosin networks can exhibit robust critical signature without fine-tuning because the dynamics of the system can be mapped onto a modified version of percolation with trapping (PT), which is known to show critical behaviour belonging to the static percolation universality class without the need of fine-tuning of a control parameter.…”

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confidence: 99%

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Percolation mechanism drives actin gels to the critically connected state

Lee

Pruessner

2016

Phys. Rev. E

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Cell motility and tissue morphogenesis depend crucially on the dynamic remodelling of actomyosin networks. An actomyosin network consists of an actin polymer network connected by crosslinker proteins and motor protein myosins that generate internal stresses on the network. A recent discovery shows that for a range of experimental parameters, actomyosin networks contract to clusters with a power-law size distribution [Alvarado J. et al. (2013) Nature Physics 9 591]. Here, we argue that actomyosin networks can exhibit robust critical signature without fine-tuning because the dynamics of the system can be mapped onto a modified version of percolation with trapping (PT), which is known to show critical behaviour belonging to the static percolation universality class without the need of fine-tuning of a control parameter. We further employ our PT model to generate experimentally testable predictions.

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Molecular motors robustly drive active gels to a critically connected state

Cited by 205 publications

References 58 publications

Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer

Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer

Intracellular transport driven by cytoskeletal motors: General mechanisms and defects

Percolation mechanism drives actin gels to the critically connected state

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