Non-equilibrium cytoquake dynamics in cytoskeletal remodeling and stabilization

Alencar, Adriano M.; Ferraz, Mariana Sacrini Ayres; Park, Chan Young; Millet, Emil; Trepat, Xavier; Fredberg, Jeffrey J.; Butler, James P.

doi:10.1039/c6sm01041e

Cited by 19 publications

(23 citation statements)

References 37 publications

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“…These cellular-level forces arise from the collective nonequilibrium activity of molecular motors interacting with the actin filament scaffold, enabling dynamic, driven-dissipative cytoskeletal remodeling ( 6 – 8 ). Recent experimental efforts have uncovered a remarkable phenomenon exhibited by cytoskeletal networks in vivo: These networks undergo large, sudden structural rearrangements significantly more frequently than predicted by a Gaussian distribution ( 9 , 10 ). Heavy-tailed distributions of event sizes are well known in seismology, where the Gutenberg–Richter law describes the power-law relationship between the energy released by an earthquake and such an earthquake’s frequency ( 11 , 12 ).…”

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confidence: 99%

“…The physics underlying cytoquakes is not well understood, as current explanations based on experimental data are mostly speculative and rely on qualitative comparisons to systems amenable to computational study, which similarly exhibit nonexponential relaxation, such as jammed granular packings and spin glasses ( 9 , 10 , 14 , 15 ). In particular, it is not known whether large cytoskeletal displacements actually arise from an avalanche-like process of slow energy storage and fast, large events of energy release.…”

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confidence: 99%

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Understanding cytoskeletal avalanches using mechanical stability analysis

Floyd

Levine

Jarzynski

et al. 2021

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

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Eukaryotic cells are mechanically supported by a polymer network called the cytoskeleton, which consumes chemical energy to dynamically remodel its structure. Recent experiments in vivo have revealed that this remodeling occasionally happens through anomalously large displacements, reminiscent of earthquakes or avalanches. These cytoskeletal avalanches might indicate that the cytoskeleton’s structural response to a changing cellular environment is highly sensitive, and they are therefore of significant biological interest. However, the physics underlying “cytoquakes” is poorly understood. Here, we use agent-based simulations of cytoskeletal self-organization to study fluctuations in the network’s mechanical energy. We robustly observe non-Gaussian statistics and asymmetrically large rates of energy release compared to accumulation in a minimal cytoskeletal model. The large events of energy release are found to correlate with large, collective displacements of the cytoskeletal filaments. We also find that the changes in the localization of tension and the projections of the network motion onto the vibrational normal modes are asymmetrically distributed for energy release and accumulation. These results imply an avalanche-like process of slow energy storage punctuated by fast, large events of energy release involving a collective network rearrangement. We further show that mechanical instability precedes cytoquake occurrence through a machine-learning model that dynamically forecasts cytoquakes using the vibrational spectrum as input. Our results provide a connection between the cytoquake phenomenon and the network’s mechanical energy and can help guide future investigations of the cytoskeleton’s structural susceptibility.

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confidence: 99%

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Understanding cytoskeletal avalanches using mechanical stability analysis

Floyd

Levine

Jarzynski

et al. 2021

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

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“…The mechanical behavior of soft materials, especially when they interface with fluids, is a recurrent question in biology and medicine, 21 attracting researchers from different fields. However, in any field, 22,23 the Young-Laplace equation is recognized as perhaps the most classical observation.…”

Section: Review On the Properties Of Nasal Polyposis Fluid Dynamics Amentioning

confidence: 99%

Nasal Polyposis: More than a Chronic Inflammatory Disorder—A Disease of Mechanical Dysfunction—The São Paulo Position

Pezato

Voegels²,

Pignatari

et al. 2019

Int Arch Otorhinolaryngol

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Introduction The importance of our study lies in the fact that we have demonstrated the occurrence of mechanical dysfunction within polypoid tissues, which promotes the development of polyps in the nasal cavity. Objective To change the paradigm of nasal polyposis (NP). In this new conception, the chronic nasal inflammatory process that occurs in response to allergies, to pollution, to changes in the epithelial barrier, or to other factors is merely the trigger of the development of the disease in individuals with a genetic predisposition to an abnormal tissue remodeling process, which leads to a derangement of the mechanical properties of the nasal mucosa and, consequently, allows it to grow unchecked. Data Synthesis We propose a fundamentally new approach to intervening in the pathological process of NP, addressing biomechanical properties, fluid dynamics, and the concept of surface tension. Conclusion The incorporation of biomechanical knowledge into our understanding of NP provides a new perspective to help elucidate the physiology and the pathology of nasal polyps, and new avenues for the treatment and cure of NP.

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“…In this microenvironment, mechanical properties can act in direct combination with cell signaling and biochemical regulation in these cellular processes [21,22]. The dynamics of these forces at this interface effects mechanical changes in the extracellular matrix which influences cell morphology, the amount and strength of focal adhesions, and cytoskeletal arrangement [23][24][25]. Thus, an enhanced understanding and quantification of cell/extracellular matrix interactions and regulation within three-dimensional environments becomes important [26].…”

Section: Introductionmentioning

confidence: 99%