Bulletin of the American Physical Society
APS March Meeting 2023
Volume 68, Number 3
Las Vegas, Nevada (March 5-10)
Virtual (March 20-22); Time Zone: Pacific Time
Session M11: Biological Active Matter IIIFocus
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Sponsoring Units: DBIO Chair: Wolfgang Losert, University of Maryland College Park Room: Room 203 |
Wednesday, March 8, 2023 8:00AM - 8:36AM |
M11.00001: Configurational entropy as a driver of tissue structural heterogeneityVasudha Srivastava, Jennifer L. Hu, Sundus F. Shalabi, James C. Garbe, Boris Veytsman, Martha R.Stampfer, Matt Thomson, Greg Huber, Mark A. LaBarge, ZevJ. Gartner Invited Speaker: Zev J Gartner A hallmark of tissues is the ability of their multiple cell types to form and maintain complex structures by self-organization. While tissues have an identifiable average structure, tissues remain spatially and temporally heterogeneous, where the local arrangement of cells can deviate significantly from the population average. The fundamental sources of this heterogeneity remain unknown. We therefore reconstituted primary human mammary epithelial cells into organoids with carefully controlled composition, geometry and microenvironment as models to study the emergence of tissue heterogeneity during self-organization. At the steady state these organoids closely mimic in vivo tissue architecture, excluding luminal cells from the tissue edge while maintaining a highly heterogeneous ensemble structure centered around a reproducible mean. We demonstrate that the observed structural ensemble follows Boltzmann statistics, corresponding to the maximum entropy distribution subject to the energetic constraints derived from interfacial mechanics. We directly measure the relative entropy and mechanical energy of different tissue configurations and use a statistical mechanical framework to systematically engineer organoid ensembles by either perturbing their mechanical potential, entropy, or activity (the active "temperature" of the tissue). These experiments reveal that the configurational entropy of cell arrangements imposes a theoretical limit to structural order at the tissue level. |
Wednesday, March 8, 2023 8:36AM - 8:48AM |
M11.00002: Strain Response to Energy Consumption in Contractile Acto-Myosin Gels Francis M Cavanna, José R Alvarado Acto-myosin networks are used by living cells for essential functions such as locomotion, structural reorganization, and mechanical feedback. To accomplish these tasks these networks often adopt a disordered mesh-like structure that experiences deformation, or strain, through myosin motors consuming ATP and sliding actin filaments past each other. Previous work has measured the mechanical response of these acto-myosin networks to external stresses, however the response to myosin-driven ATPase activity remains poorly understood. What is the relationship between the energy consumed and the strain observed in these networks? We present the first direct simultaneous measurements of ATP consumption and strain in a reconstituted in-vitro acto-myosin network. This is achieved through dual-channel observation of an acto-myosin network with an NADH assay that couples ATP consumption to fluorescence output. We systematically vary myosin and crosslinking protein concentrations to determine which network conditions create an optimal strain response. Our work establishes a novel method of characterizing the mechanical response of contractile active gels to internal driving, and will allow for future studies that quantify how contractile strain measurements affect molecular motor activity through biochemical regulatory feedback. |
Wednesday, March 8, 2023 8:48AM - 9:00AM |
M11.00003: Emergent Programmable Behavior and Chaos in Dynamically Driven Active Filaments Deepak Krishnamurthy, Manu Prakash How the behavior of biological systems emerges from its constituent parts is an outstanding challenge at the intersection of physics and biology. Single cells lacking neuro-muscular systems and having a direct connection between cell behavior and underlying biochemical and physical constituents, offer a unique opportunity to mechanistically understand behavior. A remarkable example of single-celled behavior is seen in the ciliate Lacrymaria olor, which uses rapid shape changes to an active, slender protrusion, many times the cell size, to hunt for prey. Here, inspired by these extreme behaviors in L. olor, we present an active filament model wherein behavior (filament shape dynamics) is mechanistically linked to the underlying physical properties and motile ciliary dynamics of the cell. Our model captures two key features of this system - dynamic activity patterns (extension and compression cycles) and active stresses that are uniquely aligned with the filament geometry - leading to a so-called "follower force" constraint. We show that active filaments under deterministic, time-varying follower forces display rich behaviors including periodic and aperiodic shape dynamics didover long times. We further show that aperiodic dynamics are due to a transition to chaos in regions of a biologically accessible parameter space. We further find a simple recurrence map of filament shape that predicts long-term behavior shedding light on the underlying nonlinearities in the dynamics. Lastly, using these maps as a design tool we demonstrate a few examples of “programming” filament behaviors by using frequency and amplitude modulated patterns of activity. Overall our work is a first step towards mechanistically understanding behavior in cells like L. olor and also inspires programmable active matter systems using filament geometries. |
Wednesday, March 8, 2023 9:00AM - 9:12AM |
M11.00004: Sensing Physical Signals with Cytoskeletal Dynamics Wolfgang Losert The dynamic assembly and disassembly of the cytoskeleton can create waves and oscillations that are critical to cell migration and other important cell behaviors. Chemical signals have been found to trigger and steer these waves, facilitating the guidance e.g. of immune cells to their target. Here we consider the role of these cytoskeletal dynamics in sensing of the physical microenvironment. We demonstrate that cytoskeletal waves are directly involved in sensing both the microscopic texture of the surrounding , and local DC electric fields. In turn, these cytoskeletal dynamics drive signaling pathways, reversing the typical hierarchy where signals drive biomechanics. |
Wednesday, March 8, 2023 9:12AM - 9:24AM |
M11.00005: Geometric trade-off between contractile force and fluid drag determines the motility of actomyosin droplets Ryota Sakamoto, Ziane Izri, Yuta Shimamoto, Makito Miyazaki, Yusuke T Maeda The actomyosin cytoskeleton, composed of actin filaments (F-actin) and myosin motors, plays pivotal roles in cellular force generation. One of the distinctive abilities of migratory cells is force transmission: intracellularly generated forces are transmitted to the external environments such as extracellular matrices, by which the cell body is propelled forward. Although much is known about biomolecules involved in cell migration, less is known about physical determinants enabling efficient force transmission. This is because the inherent complexities of cells, such as complex actin-membrane interactions, obscure the mechanical contributions of contractile actomyosin networks to force transmission. |
Wednesday, March 8, 2023 9:24AM - 9:36AM |
M11.00006: F-actin architecture governs self-organized criticality in the cytoskeleton Zachary G Sun, Michael P Murrell Self-Organized criticality (SOC) is observed across diverse natural phenomena, including earthquakes, avalanches, and landslides. Signatures of critical phenomena include fractal geometry, 1/f noise, and power-law distributed dissipative events. Recent work has suggested that living systems are poised close to critical points. For example, cells quickly change their shape, and dramatically remodel their internal organization during cell migration or cell division, suggestive of critical behavior in their internal mechanical machinery, the cell cytoskeleton. Composed of protein polymers and mechano-chemical enzymes, ‘active’ stresses are imparted by the enzymes to the polymer network, which accumulate from the molecular scale to the scale of the cell. To explore criticality in the dynamics of the cytoskeleton, we reconstruct an experimental model of the cytoskeleton in vitro, composed of purified protein polymers (F-actin) and enzymes (myosin II), whose organization and activity are controlled precisely. Upon initiation of myosin II activity within F-actin, the network becomes highly dynamic. If the F-actin network is branched, dissipative events are Levy-α distributed and exhibit 1/f noise. By contrast, if the F-actin network is bundled, dissipative events follow double exponential tails. Thus, cells can control their F-actin organization from fractal-like branches to linear bundles to control their approach to criticality, and utilize power-law dissipative events to dramatically remodel their cytoskeleton and ultimately change shape. |
Wednesday, March 8, 2023 9:36AM - 9:48AM |
M11.00007: Motor-driven advection competes with macromolecular crowding to drive spatiotemporally heterogeneous transport in cytoskeleton composites Janet Y Sheung, Jonathan Garamella, Stella Kahl, Brian Y Lee, Nadia Schwartz Bolef, Daisy H Achiriloaie, Jennifer L Ross, Ryan J McGorty, Rae M Robertson-Anderson The cytoskeleton, a far-from-equilibrium network of biofilaments and their associated proteins, facilitate life-sustaining mesoscale transport of cellular cargo through a crowded, dynamic, and viscoelastic environment. Understanding the transport of particles traversing the cytoskeleton is critical to cellular processes such as mitosis, endocytosis, migration, and regeneration. Yet, at the same time, macromolecules and particles diffusing through active, crowded, or heterogeneous environments have been shown to exhibit widely varying and poorly understood anomalous transport properties that deviate significantly from normal Brownian diffusion. As such, dissecting the complex transport of particles through active matter that exhibits a combination of these complexities, remains a formidable challenge. Here, we investigate diffusive transport of spherical particles and DNA through in vitro motor-driven cytoskeleton composites using single particle tracking and differential dynamic microscopy. We show that myosin motors induce ballistic-like dynamics of the composites, leading entrained particles to exhibit superdiffusive, advective and Gaussian-like transport. Conversely, steric entanglements, connectivity and slow thermal relaxation of cytoskeletal filaments mediate heterogeneous, subdiffusive transport of confined particles. Additionally, we show that the topology of the DNA plays a strong role in determining the degree to which restructuring of the cytoskeleton can mediate advective transport, possibly due to a threading mechanism. |
Wednesday, March 8, 2023 9:48AM - 10:00AM |
M11.00008: Competition of convection and diffusion in the self-mixing of microtubule-kinesin active fluid with non-uniform activity: Experiment Teagan Bate, Megan Varney, Ezra Taylor, Joshua Dickie, Chih-Che Chueh, Michael M Norton, Kun-Ta Wu Active fluids have potential applications in micromixing, but little is known about the mixing kinematics of such systems with spatiotemporally-varying activity. To investigate, UV-activated caged ATP was used to activate controlled regions of microtubule-kinesin active fluid inducing a propagating active-passive interface. The mixing process of the system from non-uniform to uniform activity as the interface advanced was observed with fluorescent tracers and molecular dyes. At low Péclet numbers (diffusive transport), the active-inactive interface progressed toward the inactive area in a diffusion-like manner and at high Péclet numbers (convective transport), the active-inactive interface progressed in a superdiffusion-like manner. The results show mixing in non-uniform active fluid systems evolve from a complex interplay between the spatial distribution of ATP and its active transport. This active transport may be diffusion-like or superdiffusion-like depending on Péclet number and couples the spatiotemporal distribution of ATP and the subsequent localized active stresses of active fluid. Our work will inform the design of future microfluidic mixing applications and provide insight into intracellular mixing processes. |
Wednesday, March 8, 2023 10:00AM - 10:12AM |
M11.00009: Competition of convection and diffusion in the self-mixing of microtubule-kinesin active fluid with non-uniform activity: Simulation Joshua H Dickie, Teagan Bate, Megan Varney, Ezra Taylor, Chih-Che Chueh, Michael M Norton, Kun-Ta Wu Active fluids with spatiotemporally varying activity have potential applications to micromixing; however previously existing active fluids models are not prepared to account for spatiotemporally-varying active stresses. Our experimental work used UV-activated caged ATP to activate controlled regions of microtubule-kinesin active fluid inducing a propagating active-passive interface. Here, we recapitulate our experimental results with two models. The first model redistributes an initial ATP distribution by Fick's law and translates the ATP distribution into a velocity profile by Michaelis-Menton kinetics. This model reproduces our experimental measurements for the low-Péclet number limit within 10% error without fitting parameters. However, as the model is diffusion based, it fails to capture the convective based superdiffusive-like behaviour at high Péclet numbers. Our second model introduces a spatiotemporally varying ATP field to an existing nematohydrodynamic active fluid model and then couples the active stresses to local ATP concentrations. This model is successful in qualitatively capturing the superdiffusive-like progression of the active-inactive interface for high Peclet number (convective transport) experimental cases. Our results show that new model frameworks are necessary for capturing the behaviour of active fluid with spatiotemporally varying activity. |
Wednesday, March 8, 2023 10:12AM - 10:24AM |
M11.00010: Kinesin-driven microtubule flows drive elastic structural transitions in actin networks John P Berezney, Itamar Kolvin, Seth Fraden, Zvonimir Dogic Active materials organize not just themselves but also their environment. Here, we describe how active consituents of a cytoskeletal composite material are reorganized into a steady-state structure through the action of molecular motors. We use fast-scanning three-dimensional confocal microscopy to directly image, at the resolution of single filaments, a network of actin as it undergoes structural reorganization due to the flow of kinesin-driven microtubule bundles. We examine the connected network structure as it evolves and connect structural transitions to changes in the elasticity of the network. Such work provides a basis for understanding how active fluids can sculpt passive materials into structures inaccessible via other means of construction. |
Wednesday, March 8, 2023 10:24AM - 10:36AM |
M11.00011: Extensile to contractile transition in active networks of microtubule and molecular motors Guillaume Duclos, Bibi Najma, Peter J Foster, Aparna Baskaran Active materials are far-from-equilibrium materials composed of energy-consuming building blocks. They self-organize into spontaneously moving structures larger than their microscopic components, where material-scale mechanics emerge from non-equilibrium interactions between active units. Rationalizing why active materials self-organize into various far-from-equilibrium states often relies on determining what symmetries are conserved or broken at the mesoscopic scale. However, coarse-graining the microscopic interactions is often challenging, in particular for living systems and biomimetic active matter where molecular interactions are either unknown, non-linear, or too complex to be reduced to a single physical mechanism. Here, we investigate the microscopic origin of the extensile to contractile transition in active gels composed of microtubule bundles and multivalent clusters of kinesin-1 motors. We combined bulk assays, single microtubule experiments, and theory to explain why decreasing ATP concentration or increasing motor concentration leads in extensile gels leads to the formation of contractile asters. Our results suggest that competition between nematic alignment and polar sorting by molecular motors controls the extensile-to-contractile transition. |
Wednesday, March 8, 2023 10:36AM - 10:48AM |
M11.00012: Toward Rational Design of Biotic-Abiotic Machines Jonathan A Michel, Michael J Rust, Jennifer L Ross, Megan T Valentine, Rae M Robertson-Anderson, Timothy J Atherton, Moumita Das We describe ongoing efforts to model the dynamics of light-actuated soft machines consisting of a reconstituted active biopolymer network tethered to passive soft supports. Force generation in organisms often features an actively driven polymer network, such as the actomyosin cortex, anchored to structural proteins. The modern availability of purified cytoskeletal proteins and click chemistry allow the creation of devices that mimic the generation and transmission of force in living tissues. We consider an active gel made of actin crosslinked and driven by myosin II minifilaments, bound to PEG-DA hydrogel slabs using the biotin-streptavidin system. Owing to the rich design space of such a device, a high-throughput method for anticipating the behavior of a system with given gel moduli, actin concentration, degree of crosslinking, and motor activity is highly desirable. Our method couples an agent-based model of an active actomyosin network to a finite element-based description of a passive gel and uses Langevin dynamics to simulate the behavior of this composite system. We will discuss the utility of this technique in identifying rational design principles for soft actuators powered by chemical potential energy. |
Wednesday, March 8, 2023 10:48AM - 11:00AM |
M11.00013: Extracting Active Fluctuating forces from Fluctuating motions of an active particle in viscoelastic medium a quadratic confinement Simin Xia, Chong Shen, H Daniel Ou-Yang Fluctuating motions of active Brownian particles are produced by a combination of active and passive forces, however, active forces, carrying the origin and the mechanisms of how they are generated, are difficult to separate from the Brownian motion. Extracting the active forces from the fluctuating motions of an active particle is nontrivial because the motions produced by the two different randomly fluctuating forces are convoluted. However, if the active Brownian particle in aqueous is confined in a quadratic potential, the position histogram of the pure active fluctuation can be extracted from known histograms of the total fluctuating position and that of the Brownian fluctuations by deconvolution. Whether and how deconvolution can work for active particle motions in viscoelastic media is of current interest. This study uses 1064nm and 980nm wavelength lasers to create an optical trap and to serve as a tracking beam, respectively. Motions of active particles, i.e., electrophoresis-driven Janus particles, embedded in a PEG-based hydrogel in an optical trap are measured by the tracking laser beam. Langevin equation-based numerical simulations are conducted to recreate the motion of the active particles in viscoelastic media for comparing with the experimental results. Mean square displacements, power spectral densities, and particle position histograms of the same experimental data are analyzed for comparing the limitations of each analytical method. |
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