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Theriot, J. A.

Publications and source records attributed to Theriot, J. A..

At least 19 recordsLinked to original sources

Dynamics of ML-based Morphological Features Indicate a Shear Stress-Dependent Bifurcation of hiPSC-Derived Endothelial Cell States

Cell states are increasingly conceptualized as attractors of high-dimensional dynamical systems, yet quantitative approaches for integrating phenotypic information into this framework remain limited. Here, we take an image-based approach that combines unsupervised machine learning (ML) with timelapse imaging to extract and characterize the temporal dynamics of morphological features. Using a cell line with endogenously tagged VE-cadherin, we acquired brightfield and fluorescence timelapse images of human induced pluripotent stem cell-derived endothelial cell (hiPSC-EC) monolayers, which adopt distinct phenotypes at two different magnitudes of shear stress in terms of their morphology, behavior, and VE-cadherin organization. To quantify these phenotypic cell states without segmentation, we trained a diffusion autoencoder to predict VE-cadherin signal from brightfield images. We identified interpretable ML-based features representing cell orientation, elongation, and local density. Treating these variables as dimensions of a morphological state space, we estimated a data-driven vector field and found that the two observed phenotypic cell states correspond to stable fixed points of the inferred dynamical system. Mapping measured cell migration coherence onto this space further distinguished the states. Imaging cells across intermediate shear stresses revealed a regime of bistability in which both states coexist, indicating that the shear-stress-dependent transition between endothelial cell states occurs as a bifurcation of the inferred dynamical system. Finally, we applied this method to study an N-terminal truncation of VE-cadherin, finding that mutated cells preserve alignment and coherent migration, but exhibit altered morphology and increased migration speed. This work demonstrates the applicability of a dynamical systems approach to quantitatively characterize morphological aspects of cell state from interpretable ML-based features.

biophysics↗

Intracellular pH dynamics promotes zebrafish larval tail regeneration

Intracellular pH (pHi) dynamics regulates numerous cell behaviors, including migration and proliferation. While these functions are well-established in cell lines, the role of pHi changes in vivo is less well understood. We generated a transgenic zebrafish line expressing a fluorescent ratiometric pHi biosensor and identified functional changes in pHi during zebrafish larval tail regeneration. We found that tail amputation led to a transient decrease in pHi, followed by a prolonged increase in pHi above pre-amputation values. Moreover, we showed that pharmacologically inhibiting Na+/H+ exchanger (NHE) activity or decreasing extracellular pH attenuated the post-amputation increase in pHi, reduced subsequent cell proliferation, and impaired tail regeneration. We further found that inhibiting NHE activity post-amputation led to elevated inflammation, disrupted myeloid cell behavior, decreased reactive oxygen species, and increased glycogen synthase kinase-3 (GSK3) activity. Finally, we showed that the regeneration defects in larvae with disrupted pHi were partially rescued by the GSK3 inhibitor BIO. Our data reveal a previously unrecognized role for pHi dynamics in coordinating tissue behaviors in vivo and enabling zebrafish larval tail regeneration.

developmental biology↗

Protein diffusion controls how single cells respond to electric fields

Cells sense and respond to electric fields, using these fields as a guidance cue in wound healing and development. This sensing is done by redistribution of charged membrane proteins on the cells surface ("sensors") via electrophoresis and electroosmotic flow. If membrane proteins have to physically rearrange on the cells surface, how quickly can a cell respond to an applied signal? What limits the cells ability to respond? Are galvanotaxing cells, like chemotaxing cells, limited by stochasticity from the finite number of molecules? Here, we develop a model for the response dynamics of galvanotaxing cells and show that, for weak enough field strengths, two relevant timescales emerge: the time for the cells sensors to rearrange, which depends on their diffusion across the cell, and the time for the cells orientation to respond to an applied field, which may be very different. We fit this model to experimental measurements on the recently-identified sensor galvanin (TMEM154) in neutrophil-like HL-60 cells, finding that given the dynamics of a cell responding to an applied field, we can predict the dynamics of the cell after the field is turned off. This fit constrains the noise of the galvanotaxis process, demonstrating that HL-60 is not limited by the stochasticity of finite sensor number. Our model also allows us to explain the effect of media viscosity on cell dynamics, and predict how cells respond to pulsed DC fields. These results place constraints on the ability to guide cells with pulsed fields, predicting that a field on half of the time is no better than a field that is always on with half the magnitude.

cell biology↗

Listeria monocytogenes cell-to-cell spread bypasses nutrient limitation for replicating intracellular bacteria

Listeria monocytogenes is an intracellular bacterial pathogen that obtains nutrients from the mammalian host cell to fuel its replication in cytosol. Sparse infection of epithelial monolayers by L. monocytogenes results in the formation of distinct infectious foci, where each focus originates from the initial infection of a single host cell followed by multiple rounds of active bacterial cell-to-cell spread into neighboring host cells in the monolayer. We used time-lapse microscopy to measure changes in bacterial growth rate in individual foci over time and found that intracellular bacteria initially replicate exponentially, but then bacterial growth rate slows later in infection, particularly in the center of the infectious focus. We found that the intracellular replication rate of L. monocytogenes is measurably decreased by limiting host cell glucose availability, by decreasing the rate of intracellular bacterial oligopeptide import, and, most interestingly, by alterations in host cell junctional proteins that limit bacterial spread into neighboring cells without directly affecting bacterial growth or metabolism. By measuring the carrying capacity of individual host cells, we found that the nutritional density of cytoplasm is comparable to rich medium. Taken together, our results indicate that the rate of intracellular L. monocytogenes replication is governed by a balance of the rate of nutrient depletion by the bacteria, the rate of nutrient replenishment by the metabolically active host cells, and the rate of bacterial cell-to-cell spread which enables the bacteria to seek out "greener pastures" before nutrient availability in a single host cell becomes limiting. SIGNIFICANCEListeria monocytogenes is a foodborne pathogen that is capable of facultative intracellular growth in a wide variety of mammalian cell types. It uses actin-based motility to spread directly from the cytoplasm of one infected host cell into another. After initially infecting cells in the small intestine, L. monocytogenes can circulate inside of infected macrophages, and subsequently spread to cells of distal organs, where it can cause spontaneous abortions in pregnant women and meningitis in immunocompromised individuals. In addition to facilitating body-wide dissemination, the actin-based cell-to-cell spread of L. monocytogenes contributes to the ability of the pathogen to evade the cell-mediated arm of the immune system. In this work, we find that cell-to-cell spread also benefits the bacteria in a third way, by enabling the bacteria to overcome the nutrient limitation they would face if they remained confined to a single host cell, such that they never enter stationary phase.

microbiology↗

Galvanin is an electric-field sensor for directed cell migration

Directed cell migration of immune and epithelial cells is critical for their rapid response to tissue injury or infection. Endogenous electric fields generated by disruption of the transepithelial potential across the skin have been postulated to play an important role in guiding cells to wound sites, though how individual cells sense these tissue-scale physical cues remains largely unknown. We have identified Galvanin (TMEM154), a previously uncharacterized single-pass transmembrane protein, as being required for electric-field-guided migration of individual rapidly moving cells. Galvanin functions in both immune and epithelial cell types. Upon exposure of cells to an electric field, Galvanin rapidly relocalizes to the anodal side of a cell, and the net charge on its extracellular domain is necessary and sufficient to drive this spatial relocalization. Furthermore, expression of Galvanin is sufficient to confer electric field-guided migration on otherwise non-responsive epithelial cells. In human neutrophils, we show that Galvanin relocalization is immediately followed by changes in the spatial pattern of cellular protrusion and retraction. The strong directional response of these cells is lost upon truncation of Galvanins intracellular domain, suggesting that Galvanin acts as a direct sensor of the electric field, transducing spatial information about a cells electrical environment to the intracellular migratory apparatus. This sensor relocalization mechanism of cell steering defines a new paradigm for directed cell migration.

cell biology↗

A human induced pluripotent stem (hiPS) cell model for the holistic study of epithelial to mesenchymal transitions (EMTs)

The epithelial to mesenchymal transition (EMT) is a widely studied but poorly defined state change due to the variety of ways in which it has been characterized in cells. There is a need for reproducible cell model systems that enable the integration and comparison of different types of measured observations of cells across many distinct cellular contexts. We present human induced pluripotent stem (hiPS) cells as such a model system by demonstrating its utility through a comparative analysis of hiPS cell-EMT in 2D and 3D cell culture geometries. We developed live-imaging-based assays to directly compare examples of changes in cell function (via migration timing), molecular components (via expression of marker proteins), organization (via reorganization of cell junctions), and environment (via dynamics of basement membrane) in the same experimental system. The EMT-related changes we measured occurred earlier in 2D colonies than in 3D lumenoids, likely due to differences in the basement membrane environments associated with 2D vs. 3D initial hiPS cell culture geometries. We have made the 449 60-hour-long 3D time-lapse movies and the associated tools used for analysis and visualization open-source and easily accessible as a resource for future work in this field.

cell biology↗

4D hybrid model interrogates agent-level rules and parameters driving hiPS cell colony dynamics

Iterating between data-driven research and generative computational models is a powerful approach for emulating biological systems, testing hypotheses, and gaining a deeper understanding of these systems. We developed a hybrid agent-based model (ABM) that integrates a Cellular Potts Model (CPM) designed to investigate cell shape and colony dynamics in human induced pluripotent stem cell (hiPS cell) colonies. This model aimed to first mimic and then explore the dynamics observed in real-world hiPS cell cultures. Initial outputs showed great potential, seeming to mimic small colony behaviors relatively well. However, longer simulations and quantitative comparisons revealed limitations, particularly with the CPM component, which lacked long-range interactions that might be necessary for accurate simulations. This challenge led us to thoroughly examine the hybrid models potential and limitations, providing insights and recommendations for systems where cell-wide mechanics play significant roles. The CPM supports 2D and 3D cell shapes using a Monte Carlo algorithm to prevent cell fragmentation. Basic "out of the box" CPM Hamiltonian terms of volume and adhesion were insufficient to match live cell imaging of hiPS cell cultures. Adding substrate adhesion resulted in flatter colonies, highlighting the need to consider environmental context in modeling. High-throughput parameter sweeps identified regimes that produced consistent simulated shapes and demonstrated the impact of specific model decisions on emergent dynamics. Full-scale simulations showed that while certain agent rules could form a hiPS cell monolayer in 3D, they could not maintain it over time. Our study underscores that "out of the box" 3D CPMs, which do not natively incorporate long-range cell mechanics like elasticity, may be insufficient for accurately simulating hiPS cell and colony dynamics. To address this limitation, future work could add mechanical constraints to the CPM Hamiltonian or integrate global agent rules. Alternatively, replacing the CPM with a methodology that directly represents cell mechanics might be necessary. Documenting and sharing our model development process fosters open team science and supports the broader research community in developing computational models of complex biological systems.

systems biology↗

Interpretable representation learning for 3D multi-piece intracellular structures using point clouds

A key challenge in understanding subcellular organization is quantifying interpretable measurements of intracellular structures with complex multi-piece morphologies in an objective, robust and generalizable manner. Here we introduce a morphology-appropriate representation learning framework that uses 3D rotation invariant autoencoders and point clouds. This framework is used to learn representations of complex multi-piece morphologies that are independent of orientation, compact, and easy to interpret. We apply our framework to intracellular structures with punctate morphologies (e.g. DNA replication foci) and polymorphic morphologies (e.g. nucleoli). We systematically compare our framework to image-based autoencoders across several intracellular structure datasets, including a synthetic dataset with pre-defined rules of organization. We explore the trade-offs in the performance of different models by performing multi-metric benchmarking across efficiency, generative capability, and representation expressivity metrics. We find that our framework, which embraces the underlying morphology of multi-piece structures, facilitates the unsupervised discovery of sub-clusters for each structure. We show how our approach can also be applied to phenotypic profiling using a dataset of nucleolar images following drug perturbations. We implement and provide all representation learning models using CytoDL, a python package for flexible and configurable deep learning experiments.

cell biology↗

Colony context and size-dependent compensation mechanisms give rise to variations in nuclear growth trajectories

To investigate the fundamental question of how cellular variations arise across spatiotemporal scales in a population of identical healthy cells, we focused on nuclear growth in hiPS cell colonies as a model system. We generated a 3D timelapse dataset of thousands of nuclei over multiple days, and developed open-source tools for image and data analysis and an interactive timelapse viewer for exploring quantitative features of nuclear size and shape. We performed a data-driven analysis of nuclear growth variations across timescales. We found that individual nuclear volume growth trajectories arise from short timescale variations attributable to their spatiotemporal context within the colony. We identified a strikingly time-invariant volume compensation relationship between nuclear growth duration and starting volume across the population. Notably, we discovered that inheritance plays a crucial role in determining these two key nuclear growth features while other growth features are determined by their spatiotemporal context and are not inherited.

cell biology↗

Topographical analysis of immune cell interactions reveals a biomechanical signature for immune cytolysis

Immune cells live intensely physical lifestyles characterized by structural plasticity, mechanosensitivity, and force exertion. Whether specific immune functions require stereotyped patterns of mechanical output, however, is largely unknown. To address this question, we used super-resolution traction force microscopy to compare cytotoxic T cell immune synapses with contacts formed by other T cell subsets and macrophages. T cell synapses were globally and locally protrusive, which was fundamentally different from the coupled pinching and pulling of macrophage phagocytosis. By spectrally decomposing the force exertion patterns of each cell type, we associated cytotoxicity with compressive strength, local protrusiveness, and the induction of complex, asymmetric interfacial topographies. These features were further validated as cytotoxic drivers by genetic disruption of cytoskeletal regulators, direct imaging of synaptic secretory events, and in silico analysis of interfacial distortion. We conclude that T cell-mediated killing and, by implication, other effector responses are supported by specialized patterns of efferent force.

immunology↗

Mapping variation in the morphological landscape of human cells with optical pooled CRISPRi screening

The contributions of individual genes to cell-scale morphology and cytoskeletal organization are challenging to define due to the wide intercellular variation of these complex phenotypes. We leveraged the controlled nature of image-based pooled screening to assess the impact of CRISPRi knockdown of 366 genes on cell and nuclear morphology in human U2OS osteosarcoma cells. Screen scale-up was facilitated by a new, efficient barcode readout method that successfully genotyped 85% of cells. Phenotype analysis using a deep learning algorithm, the {beta}-variational autoencoder, produced a feature embedding space distinct from one derived from conventional morphological profiling, but detected similar gene hits while requiring minimal design decisions. We found 45 gene hits and visualized their effect by rationally constrained sampling of cells along the direction of phenotypic shift. By relating these phenotypic shifts to each other, we construct a quantitative and interpretable space of morphological variation in human cells.

cell biology↗

Cell migration CRISPRi screens in human neutrophils reveal regulators of context-dependent migration and differentiation state

Neutrophils are the most abundant leukocyte in humans and provide a critical early line of defense as part of our innate immune system. Their exquisite sensitivity to chemical gradients and ability to rapidly migrate make them especially suited to protect against infection. However, their terminal differentiation status and short lifetime (on the order of days) have hindered their study. Furthermore, while modern CRISPR-based gene perturbation strategies now allow comprehensive, genome-scale screens in human cells, their application to complex and dynamic processes like cell migration remain limited. Using HL-60 cells, a leukemia cell line that can be differentiated into neutrophil-like cells, we have developed multiple cell migration screen strategies that provide comprehensive, genome-wide discovery of molecular factors that are critical for directed (chemotaxis), undirected (chemokinesis), and 3D amoeboid cell migration in these fast-moving cells. Combining these assays with additional, pooled, genome-wide CRISPR interference dropout screens of cell proliferation and neutrophil differentiation, we have identified a comprehensive set of genes that are important across the processes of cellular growth, differentiation, and migration. This combined dataset highlights a particular reliance upon mTORC1 signaling that alters neutrophil lifetime, migration phenotype, and sensitivity to chemotactic cues. Across our cell migration screens, we identified several hundred genes important for migration including those with specific roles only in particular migratory contexts. This genome-wide screening strategy, therefore, provides an invaluable approach to the study of neutrophils and provides a resource that will inform future studies of cell migration in these and other rapidly migrating cells.

cell biology↗

Cell surface receptors TREM2, CD14 and integrin αMβ2 drive sinking engulfment in phosphatidylserine-mediated phagocytosis

Macrophages phagocytose and thereby eliminate a wide array of extracellular threats, ranging from antibody-coated bacteria to apoptotic cells. Precision modulation of phagocytosis has emerged as a therapeutic strategy across a range of diseases, but is limited by our incomplete understanding of how macrophages recognize, engulf, and respond to different phagocytic targets. Here, we undertook a systematic investigation of the morphological, biophysical and regulatory differences between two major types of phagocytosis: an immunostimulatory form of phagocytosis triggered by antibody-coated targets and an immunosuppressive form triggered by phosphatidylserine (PS)-coated targets. We confirmed classic observations that antibody-mediated phagocytosis involves the extension of thin actin-rich protrusions around the target, but find that PS-mediated phagocytosis involves an unexpected combination of filopodial probing, piecemeal phagocytosis and a distinct sinking mechanism of uptake. Using a genome-wide screening approach, we identified genes specifically required for each form of phagocytosis, including actin regulators, cell surface receptors and intracellular signaling molecules. Three cell surface receptors - TREM2, CD14 and integrin M{beta}2 - were revealed as essential for PS-mediated uptake. Strikingly, each receptor exhibited a distinct pattern of localization at the plasma membrane and contributed uniquely to the organization of the PS-dependent phagocytic cup. Overall, this work reveals divergent genetic requirements for the morphologically and mechanically distinct forms of PS-mediated and antibody-mediated phagocytosis, thereby informing therapeutic strategies for substrate-specific phagocytosis modulation.

cell biology↗

Confined keratocytes mimic in vivo migration and reveal volume-speed relationship

Fish basal epidermal cells, known as keratocytes, are well-suited for cell migration studies. In vitro, isolated keratocytes adopt a stereotyped shape with a large fan-shaped lamellipodium and a nearly spherical cell body. However, in their native in vivo environment, these cells adopt a significantly different shape during their rapid migration towards wounds. Within the epidermis, keratocytes experience 2D confinement between the outer epidermal cell layer and the basement membrane; these two deformable surfaces constrain keratocyte cell bodies to be flatter in vivo than in isolation. In vivo keratocytes also exhibit a relative elongation of the front-to-back axis and substantially more lamellipodial ruffling, as compared to isolated cells. We have explored the effects of 2D confinement, separated from other in vivo environmental cues, by overlaying isolated cells with an agarose hydrogel with occasional spacers, or with a ceiling made of PDMS elastomer. Under these conditions, isolated keratocytes more closely resemble the in vivo migratory shape phenotype, displaying a flatter apical-basal axis and a longer front-to-back axis than unconfined keratocytes. We propose that 2D confinement contributes to multiple dimensions of in vivo keratocyte shape determination. Further analysis demonstrates that confinement causes a synchronous 20% decrease in both cell speed and volume. Interestingly, we were able to replicate the 20% decrease in speed using a sorbitol hypertonic shock to shrink the cell volume, which did not affect other aspects of cell shape. Collectively, our results suggest that environmentally imposed changes in cell volume may influence cell migration speed, potentially by perturbing physical properties of the cytoplasm.

cell biology↗

Post-injury hydraulic fracturing drives fissure formation in the zebrafish basal epidermal cell layer

The skin epithelium acts as the barrier between an organisms internal and external environments. In zebrafish and other freshwater organisms, this barrier function requires withstanding a large osmotic pressure differential. Wounds breach this epithelium, causing a large disruption to the tissue microenvironment due to the mixing of isotonic interstitial fluid with the external hypotonic fresh water. Here we show that, following acute injury, the larval zebrafish epidermis undergoes a dramatic fissuring process that resembles hydraulic fracturing, driven by the influx of external fluid. The fissuring starts in the basal epidermal layer nearest to the wound, and then propagates at a constant rate through the tissue spanning over one hundred micrometers; during this process the outermost superficial epidermal layer remains intact. Fissuring is completely inhibited when larvae are wounded in an isotonic external media, suggesting that osmotic pressure gradients drive fissure. Additionally, fissuring partially depends on myosin II activity, as its inhibition reduces fissure propagation away from the wound. During and after fissuring, the basal layer forms large macropinosomes (with cross-sectional areas ranging from 1-10 {micro}m2), presumably to clear the excess fluid. We conclude that excess external fluid entry through the wound and subsequent closure of the wound through actomyosin purse string contraction in the superficial cell layer causes fluid pressure buildup in the extracellular space of the zebrafish epidermis. This excess fluid pressure causes tissue to fissure, and eventually the fluid is cleared through macropinocytosis.

cell biology↗

Vast heterogeneity in cytoplasmic diffusion rates revealed by nanorheology and Doppelgänger simulations

The cytoplasm is a complex, crowded, actively-driven environment whose biophysical characteristics modulate critical cellular processes such as cytoskeletal dynamics, phase separation, and stem-cell fate. Little is known about the variance in these cytoplasmic properties. Here, we employed particle-tracking nanorheology on genetically encoded multimeric 40-nm nanoparticles (GEMs) to measure diffusion within the cytoplasm of the fission yeast Schizosaccharomyces pombe. We found that the apparent diffusion coefficients of individual GEM particles varied over a 400-fold range, while the differences in average particle diffusivity among individual cells spanned a 10-fold range. To determine the origin of this heterogeneity, we developed a Doppelganger Simulation approach that uses stochastic simulations of GEM diffusion that replicate the experimental statistics on a particle-by-particle basis, such that each experimental track and cell had a one-to-one correspondence with their simulated counterpart. These simulations showed that the large intra- and inter-cellular variations in diffusivity could not be explained by experimental variability but could only be reproduced with stochastic models that assume a wide intra- and inter-cellular variation in cytoplasmic viscosity. The simulation combining intra- and inter-cellular variation in viscosity also predicted weak non-ergodicity in GEM diffusion, consistent with the experimental data. To probe the origin of this variation, we found that the variance in GEM diffusivity was largely independent of factors such as temperature, cytoskeletal effects, cell cycle stage and spatial locations, but was magnified by hyperosmotic shocks. Taken together, our results provide a striking demonstration that the cytoplasm is not "well-mixed" but represents a highly heterogeneous environment in which subcellular components at the 40-nm sizescale experience dramatically different effective viscosities within an individual cell, as well as in different cells in a genetically identical population. These findings carry significant implications for the origins and regulation of biological noise at cellular and subcellular levels. SignificanceBiophysical properties of the cytoplasm influence many cellular processes, from differentiation to cytoskeletal dynamics, yet little is known about how tightly cells control these properties. We developed a combined experimental and computational approach to analyze cytoplasmic heterogeneity through the lens of diffusion. We find that the apparent cytoplasmic viscosity varies tremendously - over 100-fold within any individual cell, and over 10-fold among individual cells when comparing averages of all particles measured for each cell. The variance was largely independent of temperature, the cytoskeleton, cell cycle stage, and localization, but was magnified under hyperosmotic shock. This suggests that cytoplasmic heterogeneity contributes substantially to biological variability within and between cells, and has significant implications for any cellular process that depends on diffusion. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=156 SRC="FIGDIR/small/491518v3_ufig1.gif" ALT="Figure 1"> View larger version (42K): org.highwire.dtl.DTLVardef@a6faeforg.highwire.dtl.DTLVardef@a49dc4org.highwire.dtl.DTLVardef@171d62borg.highwire.dtl.DTLVardef@a3c7bf_HPS_FORMAT_FIGEXP M_FIG C_FIG

cell biology↗

Listeria monocytogenes Co-opts Caveolin-Mediated E-cadherin Trafficking and Macropinocytosis for Epithelial Cell-to-Cell Spread

Listeria monocytogenes is an intracellular bacterial pathogen that spreads directly between adjacent host cells without exposure to the extracellular space. Recent studies have identified several host cell factors that promote L. monocytogenes cell-to-cell spread in epithelial monolayers, but details of the mechanism remain unclear. We find that the adherens junction protein, E-cadherin, promotes L. monocytogenes cell-to-cell spread at the recipient side of cell contacts. In particular, two point mutations in E-cadherins cytoplasmic domain that prevent its ubiquitination hinder bacterial cell-to-cell spread efficiency without reducing the extent of contact between neighboring cells. As ubiquitination induces E-cadherin endocytosis, we hypothesize that E-cadherin promotes protrusion engulfment, where donor cell protrusions containing L. monocytogenes are taken up by the recipient cell concurrently with E-cadherin internalization. In support of this hypothesis, we show that inhibiting caveolin-mediated membrane trafficking reduces L. monocytogenes cell-to-cell spread only under conditions where E-cadherin can be ubiquitinated. Additionally, we demonstrate that macropinocytosis also contributes to dissemination of L. monocytogenes through an epithelial monolayer.

microbiology↗

Mechanical competition promotes selective listening to receptor inputs to resolve directional dilemmas in neutrophil migration

As neutrophils navigate complex environments to reach sites of infection, they may encounter obstacles that force them to split their front into multiple leading edges, raising the question of how the cell selects which front to maintain and which front(s) to abandon. Here we challenge chemotaxing HL60 neutrophil-like cells with symmetric bifurcating microfluidic channels, enabling us to probe the cell-intrinsic properties of their decision-making process. Using supervised statistical learning, we demonstrate that cells commit to one leading edge late in the decision- making process, rather than amplifying early pre-existing asymmetries. Furthermore, we use optogenetic tools to show that receptor inputs only bias the decision similarly late, once mechanical stretching begins to weaken each front. Finally, optogenetic attempts to reverse cell decisions reveal that, once an edge begins retracting, it commits to this fate, with the kinase ROCK limiting its sensitivity to inputs until the retraction is complete. Collectively our results suggest a "selective listening" model in which both actively protruding cell fronts and actively retracting cell rears have strong commitment to their current migratory program.

cell biology↗