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Smeets, B.

Publications and source records attributed to Smeets, B..

At least 19 recordsLinked to original sources

Matrix-controlled emergence of biofilm architecture shapes antimicrobial survival

Biofilms are structured microbial communities whose extracellular matrix is widely regarded as a basis of their protection against antimicrobial compounds. Yet how matrix production by individual bacteria gives rise to collective architecture and antimicrobial protection remains poorly understood. Here, we systematically varied expression of the master biofilm regulator csgD in Salmonella enterica and found that increasing matrix production reorganizes biofilms from dense, isotropic packings into sparse, nematically aligned communities by altering cell-cell interactions. By combining experimentally measured biofilm architectures with reaction-diffusion modeling, we show that these structural changes produce distinct patterns of antimicrobial killing, ranging from preferential killing near the liquid-biofilm interface to more uniform killing throughout the community. Consequently, increasing matrix production unexpectedly reduces antimicrobial survival by shifting the biofilm into different transport regimes, while strain-specific physiological differences further modulate antimicrobial depletion. Rather than acting as a passive barrier, EPS therefore shapes antimicrobial susceptibility by reorganizing biofilm architecture and its transport properties. EPS thus provides a physical link between molecular regulation, collective architecture and antimicrobial survival, providing a quantitative framework for understanding how cellular matrix production generates emergent biofilm function.

microbiology↗

Cellular timing heterogeneity regulates phase transitions in living matter

Rigidity transitions govern tissue organization in ways reminiscent of inert materials. Yet, living tissues are composed of active units with autonomous timing mechanisms, raising the question whether microscopic cellular timing distribution influences collective mechanical states. Here we identify heterogeneity in cellular timescales as a heritable parameter, regulating rigidity transitions in embryonic tissues. Lineage tracking and quantitative mechanical analysis reveal that zebrafish morphogenesis starts with a tissue rigidity collapse occurring at maximal cell cycle length heterogeneity. This heterogeneity arises from size-dependent stochastic differences in resource allocation, with resource availability defining the cell cycle length. Such differences are inherited across generations, amplifying and structuring tissue-wide cell cycle length heterogeneity. Experiments and large-scale 3D simulations identify an optimum level of cellular timing variability at which cell-cell contact remodelling is spatially coordinated driving timely and robustly the rigidity transition. These findings demonstrate that embryos exploit microscopic temporal disorder for timing and tuning tissue morphogenesis.

biophysics↗

Modeling spheroid assembly dynamics and mechanical stress generation in magnetic-based biofabrication

Magnetic biofabrication enables rapid assembly of multicellular spheroids but still lacks a basis for predictive control over structure and mechanical environment. Here, we combine experiments and an individual spheroid-based model to study magnetic assembly of periosteum-derived spheroids. Spheroids are treated as discrete particles interacting through magnetic forces, contact mechanics, and interfacial friction, with parameters obtained from independent measurements. This model quantitatively captures assembly dynamics arising from magnetic force patterns and viscous drag with the well surface. The spatial distribution of magnetic forces, determined by magnet geometry and positioning, predicts the size and morphology of magnetic assembloids, including disk- and ring-like structures. Magnetic assembly further generates heterogeneous compressive stresses that depend on magnet geometry and spheroid number. Radial stresses arise collectively through inter-spheroid interactions, whereas vertical stresses are mainly determined by magnetic loading of individual spheroids. These results establish a minimal physical framework for magnetic biofabrication and provide a basis for predictive control of both tissue structure and mechanical microenvironment.

bioengineering↗

Integrated quantitative imaging and biomechanical modeling of early gastrulation in C. elegans

1The stereotyped internalization of two endodermal precursors during early Caenorhabditis elegans gastrulation enables quantitative dissection of cell ingression mechanics. Experimental work has shown that apical constriction drives Ea and Ep ingression, and several molecular features involved have been identified. Yet, no integrative mechanical analysis has assessed how these elements collectively produce the observed behavior. To address this, we combined biomechanical simulations with a comprehensive dataset of 3D-segmented cell meshes, some with cortical protein distributions, to analyze the mechanics of ingression in its in-vivo context. Our analysis shows the process starts shortly after birth of the ingressing cells. A cortical flow drives the formation of an E-cadherin-rich structure at the apical Ea-Ep interface, which contributes to localizing the buildup of apical tension. Simulations show that medioapical actomyosin contraction can reproduce the observed ingression movements and suggest force transmission to neighboring cells via a friction-based molecular clutch at the apical ring of contact. A series of concurrent cell divisions facilitates ingression, and their stereotyped planar orientation also contributes. Furthermore, we observe an embryo-wide movement of cells during gastrulation. This movement resembles a flow, suggesting that local force generation leads to global rearrangements via internal pressure changes. Finally, at the end of ingression, detailed microscopy shows that neighboring cells actively close the gastrulation cleft by forming a rosette-like configuration and extending actin-rich protrusions. In conclusion, our integrated mechanical description of gastrulation shows that successful ingression is driven by apical constriction and supported by localized friction-based force transmission, coordinated stereotyped cell divisions, and the resulting global tissue flow.

developmental biology↗

Nematic structures contribute to robust zygotic polarization in C. elegans

The C. elegans zygote is a powerful model for asymmetric cell division. Its strikingly patterned cortex features thick F-actin bundles and myosin foci, contractile nematic structures that drive characteristic surface ruffles. Early in the cell cycle, symmetry breaks near the sperm-contributed centrosomes, typically at the presumptive posterior pole, and is marked by local downregulation of contractility. This initiates a cortical flow that polarizes the cell and enables PAR proteins to establish anterior and posterior domains. While biochemical mechanisms maintaining these domains are well understood, the mechanical role of cortical architecture in polarization remains unclear. We developed a three-dimensional (3D) mechanical model of C. elegans zygote polarization that represents the actin bundles and myosin foci of the cortex as a network of stiff contractile filaments. We measured cortical flow with high spatiotemporal resolution by tracking myosin foci, and used these data alongside mechanical properties from the literature to parametrize the model. The model simulates the complete polarization process in 3D, from symmetry breaking through domain stabilization, and reproduces key cortical dynamics including flow profiles, surface ruffles, and tension anisotropy. Domain arrest near the embryo midpoint emerges from density-dependent contractility regulation, in which cortical material redistribution during flow creates a mechanical negative feedback that balances anterior and posterior tension.We find that compressive flow aligns actin bundles in the anterior domain and generates anisotropic tension perpendicular to the flow direction. Although this alignment is not essential for polarization when symmetry breaking occurs at the pole, it contributes to this process when symmetry breaking occurs laterally. In such cases, anisotropic tension from aligned bundles drives axis convergence by rotating the posterior domain towards the nearest pole. Nematic cortical structures therefore ensure robust alignment of the polarization axis. AvailabilityAll data and code required to reproduce the results are freely available at https://doi.org/10.5281/zenodo.18135771. The latest version of the software is maintained at https://bitbucket.org/pgmsembryogenesis/polarization.

developmental biology↗

Stress-dependent growth of breast cancer models emerges from a cellular volume checkpoint

Mechanoresponsive cell proliferation is a feature of growing tumours, despite the suppression of many other regulatory checkpoints in cancer, but the underlying cell-scale mechanisms driving this behaviour have not yet been established. In this study we propose a biophysical model for cell growth as governed by actively controlled osmolarity, which we integrate with a discrete particle framework to simulate growth and remodelling of breast cancer spheroids. Confinement and biomechanical feedback from the extracellular environment are analysed through a neuralnetwork-accelerated finite element solver. Combining the framework with experiments, our model reveals that stress-dependent spheroid growth can arise from a sizing checkpoint for mitosis. Under sufficient extracellular loading, cell growth is restricted by high hydrostatic forces in competition with osmotic pressure from biomolecule synthesis, which prevents cells from surpassing a critical volume. Our model provides new insight into mechanosensitive growth arrest in breast cancer, potentially serving as a computational tool for analysing growth in a wider range of normal and malignant biological tissues.

cancer biology↗

Rigidity transitions in a 3D active foam model of cell monolayers with frictional contact interactions

In morphogenesis and disease, biological tissues may exhibit diverse mechanical properties due to their capacity to switch between fluid-like to solid-like states through the (un)jamming transition. Here, we introduce a novel foam model to investigate how active mechanical properties and cellular interactions govern this transition in active cell monolayers. This model explicitly represents 3D cell shapes and describes cell-cell interactions via discrete interacting surfaces. Simulations reveal that cell-cell adhesive tension promotes tissue fluidization in high adhesive tissues, where it mainly promotes cell deformability, while it induces solidification in the low adhesive regime, where it prevents cell-cell debonding. Moreover, we study the dynamic role of adhesive ligand turnover through an effective intercellular friction. Through simulated shear experiments, we find that intercellular friction strongly suppresses neighbor exchanges, but does not lead to solid-like tissue properties. We discuss the implications of our results for understanding the relationship between unjamming and partial epithelial-mesenchymal transition, highlighting how differences in adhesion dynamics and intercellular friction may reconcile conflicting observations in tissue mechanics and cancer metastasis.

biophysics↗

Active foam dynamics of tissue spheroid fusion

Three-dimensional tissue spheroids are a key building block in biofabrication, yet the link between their material properties and active mechanics of individual cells is not fully understood. We study the material properties of small spheroids of human periosteum-derived cells as they effect spheroid fusion, an elementary operation for constructing large tissue structures. We use two-photon confocal microscopy to measure cell-cell tension and individual cell motility throughout fusion. Cytoskeletal inhibition through Y-27632 (ROCKi) results in more granular tissues with decreased cell rearrangements, but accelerated fusion. Further reducing cell contractility with blebbistatin and ROCKi increases tissue granularity, decreases rearrangements, and slows down fusion. In all conditions, complete fusion is associated with frequent cellular rearrangements. Using a novel computational model that represents tissue material as an active cellular foam, with cells depicted as viscous shells with interfacial tension and persistent, random motility, we construct a phase diagram of spheroid fusion in function of relative cell-cell tension and cell motility. Our results reveal a close relationship between microscopic tissue fluidity and the visco-elastic properties of spheroid fusion. Additionally, we find that cell-cell friction promotes arrested fusion by inducing jamming through a distinct physical mechanism. Combined, our findings offer a framework for understanding spheroid fusion dynamics that can aid in the robust generation of large tissue constructs for regenerative medicine.

biophysics↗

Image-based force inference by biomechanical simulation

During morphogenesis, cells precisely generate forces that drive cell shape changes and cellular motion. These forces predominantly arise from contractility of the actomyosin cortex, allowing for cortical tension, protrusion formation, and cell division. Image-based force inference can derive such forces from microscopy images, without complicated and time-consuming experimental set-ups. However, current methods do not account for common effects, such as physical confinement and local force generation. Here we propose a force-inference method based on a biophysical model of cell shape, and assess relative cellular surface tension, adhesive tension between cells, as well as cytokinesis and protrusion formation. We applied our method on fluorescent microscopy images of the early C. elegans embryo. Predictions for cell surface tension at the 7-cell stage were validated by measurements using cortical laser ablation. Our non-invasive method facilitates the accurate tracking of force generation, and offers many new perspectives for studying morphogenesis. Author summaryAn important challenge in understanding morphogenesis is to determine where forces are generated. Force generation, such as differential cortical tension, plays a key role in cellular self-organization. However, measuring these forces experimentally is a big challenge that typically requires complicated experiments and direct access to the cells being investigated. A non-invasive method, such as force inference based on cell shapes, would have important advantages. Unfortunately, current methods can only be applied in certain cases. Here, we describe a more flexible 3D force inference method, FIDES, that can account for physical confinement, cell divisions and protrusions. We applied the method to infer forces throughout early C. elegans embryogenesis. By using cortical laser ablations, we confirmed that FIDES correctly inferred cell surface tensions in a dynamic stage of the nematodes embryogenesis. Our approach offers a route to routinely infer force generation in complex movements during morphogenesis, with microscopy images of cell shapes as the sole experimental input.

bioinformatics↗

Spatial distribution of bacteria and extracellular polymeric substances impacts nanoparticle penetration in biofilms

Extracellular polymeric substances (EPS) in bacterial biofilms complicate treatment by inactivating drugs and slowing down diffusion. Through enhanced penetration and resistance to degradation in bacterial biofilms, nanoparticle (NP) carriers can help improve biofilm treatment. However, the way in which biofilm architecture influences the diffusive properties and penetration of NPs in biofilms is still poorly understood. In this work, we combined single particle tracking (SPT) and confocal laser scanning microscopy (CLSM) in Salmonella biofilms with simulations of a Brownian dynamics model to quantify how macro- (spatial organization of the bacteria) and micro- (EPS dependent) structure of the biofilm affects NP penetration. In CLSM images we observed immobilization of NPs in the EPS, which allows shielding of bacteria from the NPs, an effect that was more pronounced in dispersed biofilms, grown in nutrient-rich conditions, than in compacted biofilms, grown in nutrient-poor conditions. SPT experiments revealed anomalous diffusion, with an increased probability for small displacements near clusters of bacteria. Simulations of a Brownian dynamics model revealed that EPS reinforces shielding by affecting the pore structure of the biofilm. Finally, in virtual biofilms with varying spatial distribution of bacteria, we found that even for the same number of bacteria, dispersed biofilm structures provide more shielding than biofilms organized in dense, compacted clusters, even when accounting for decreased NP diffusivity.

microbiology↗

Stability of asymmetric cell division under confinement: A deformable cell model of cytokinesis applied to C. elegans development

Cell division during early embryogenesis has been linked to key morphogenic events such as embryo symmetry breaking and tissue patterning. It is thought that boundary conditions together with cell intrinsic cues act as a mechanical "mold", guiding cell division to ensure these events are more robust. We present a novel computational mechanical model of cytokinesis, the final phase of cell division, to investigate how cell division is affected by mechanical and geometrical boundary conditions. The model reproduces experimentally observed furrow dynamics and predicts the volume ratio of daughter cells in asymmetric cell divisions based on the position and orientation of the mitotic spindle. We show that the orientation of confinement relative to the division axis modulates the volume ratio in asymmetric cell division and quantified the mechanical contribution of cortex mechanics, relative to the mechanical properties of the furrow ring. We apply this model to early C. elegans development, which proceeds within the confines of an eggshell, and simulate the formation of the three body axes via sequential (a)symmetric divisions up until the six cell stage. We demonstrate that spindle position and orientation alone can be used to predict the volume ratio of daughter cells during the cleavage phase of development. However, for compression perturbed egg geometries, the model predicts that the change in confinement alone is insufficient to explain experimentally observed differences in cell volume, inferring an unmodeled underlying spindle positioning mechanism. Finally, the model predicts that confinement stabilizes asymmetric cell divisions against bubble-instabilities, which can arise due to elevated mitotic cortical tension. Author summaryA crucial morphogenic step during early embryonic development is symmetry breaking in the embryo. For C. elegans the formation of the three body axes can be traced back to the six cell stage, where tissue-topology is the result of symmetric and asymmetric divisions. How cell mechanical boundary conditions and cell intrinsic cues influence this process of symmetry breaking is still an open question, as currently, a quantitative mechanical description of cytokinesis in complex architectures is lacking. We developed a simple mechanical model of cell division, incorporated in an existing mechanical cortex model, to simulate cytokinesis in geometrically confined environments. Our approach was able to both capture furrow ring dynamics and predict the volume ratio of daughter cells accurately. By simulating early C. elegans development with different geometrical boundary conditions, we were able to trace back the origin of volume discrepancies between the experimental setups to a quantifiable shift in spindle positioning during cytokinesis. Finally, we showed how embryo confinement partially stabilizes bubble-instabilities that arise during asymmetric cell division during the early cleavage phase.

biophysics↗

Permissive aggregative group formation favors coexistence in yeast

In Saccharomyces cerevisiae, the FLO1 gene encodes flocculins that lead to formation of multicellular flocs, that offer protection to the constituent cells. Flo1p was found to preferentially bind to fellow cooperators compared to defectors lacking FLO1 expression, resulting in enrichment of cooperators within the flocs. Given this dual function in cooperation and kin recognition, FLO1 has been termed a green beard gene. Because of the heterophilic nature of Flo1p binding however, we hypothesize that kin recognition is permissive and depends on the relative stability of FLO1+/flo1- versus FLO1+/FLO1+ bonds, which itself can be dependent on environmental conditions and intrinsic cell properties. We combine single cell measurements of adhesion strengths, individual cell-based simulations of cluster formation and evolution, and in vitro flocculation experiments to study the impact of relative bond stability on defector exclusion as well as benefit and stability of cooperation. We hereto vary the relative bond stability by changing the shear flow rate and the inherent bond strength. We identify a marked trade-off between both aspects of the green beard mechanism, with reduced relative bond stability leading to increased kin recognition, but at the expense of decreased cluster sizes and benefit of cooperation. Most notably, we show that the selection of FLO1 cooperators is negative-frequency dependent, which we directly attribute to the permissive character of the Flo1p bond. Taking into account the costs associated to FLO1 expression, this asymmetric selection results in a broad range of ecological conditions where coexistence between cooperators and defectors is stable. Although the kin recognition aspect of the FLO1 green beard gene is thus limited and condition dependent, the negative-frequency dependency of selection can conserve the diversity of flocculent and non-flocculent phenotypes ensuring flexibility towards variable selective pressures.

evolutionary biology↗

Human pluripotent stem cell-derived kidney organoids for personalized congenital and idiopathic nephrotic syndrome modeling

Nephrotic syndrome (NS) is characterized by severe proteinuria as a consequence of kidney glomerular injury due to podocyte damage. In vitro models mimicking in vivo podocyte characteristics are a prerequisite to resolve NS pathogenesis. Here, we report human induced pluripotent stem cell derived kidney organoids containing a podocyte population that heads towards adult podocytes and were superior compared to 2D counterparts, based on scRNA sequencing, super-resolution imaging and electron microscopy. In this study, these next-generation podocytes in kidney organoids enabled personalized idiopathic nephrotic syndrome modeling as shown by activated slit diaphragm signaling and podocyte injury following protamine sulfate treatment and exposure to NS plasma containing pathogenic permeability factors. Organoids cultured from cells of a patient with heterozygous NPHS2 mutations showed poor NPHS2 expression and aberrant NPHS1 localization, which was reversible after genetic correction. Repaired organoids displayed increased VEGFA pathway activity and transcription factor activity known to be essential for podocyte physiology, as shown by RNA sequencing. This study shows that organoids are the preferred model of choice to study idiopathic and congenital podocytopathies. Summary StatementKidney organoid podocytes allow personalized nephrotic sydrome modeling,

molecular biology↗

Activity-induced fluidization of arrested coalescence in fusion of cellular aggregates

At long time scales, tissue spheroids may flow or appear solid depending on their capacity to reorganize their internal structure. Understanding the relationship between intrinsic mechanical properties at the single cell level, and the tissue spheroids dynamics at the long-time scale is key for artificial tissue constructs, which are assembled from multiple tissue spheroids that over time fuse to form coherent structures. The dynamics of this fusion process are frequently analyzed in the framework of liquid theory, wherein the time scale of coalescence of two droplets is governed by its radius, viscosity and surface tension. In this work, we extend this framework to glassy or jammed cell behavior which can be observed in spheroid fusion. Using simulations of an individual-cell based model, we demonstrate how the spheroid fusion process can be steered from liquid to arrested by varying active cell motility and repulsive energy as established by cortical tension. The divergence of visco-elastic relaxation times indicates glassy relaxation near the transition towards arrested coalescence. Finally, we investigate the role of cell growth in spheroid fusion dynamics. We show that the presence of cell division introduces plasticity in the material and thereby increases coalescence during fusion.

biophysics↗

Tfam knockdown results in reduction of mtDNA copy number, OXPHOS deficiency and abnormalities in zebrafish embryos

High mitochondrial DNA (mtDNA) copy numbers are essential for oogenesis and embryogenesis and correlate with fertility of oocytes and viability of embryos. To understand the pathology and mechanisms associated with low mtDNA copy numbers, we knocked down mitochondrial transcription factor A (Tfam), a regulator of mtDNA replication, during early zebrafish development. Reduction of Tfam using a splice-modifying morpholino (MO) resulted in a 42%{+/-}4% decrease in mtDNA copy number in embryos at 4 days post fertilization. Morphant embryos displayed abnormal development of the eye, brain, heart and muscle, as well as a 50%{+/-}11% decrease in ATP production. Transcriptome analysis revealed a decrease in protein-encoding transcripts from the heavy strand of the mtDNA. In addition, various RNA translation pathways were increased, indicating an upregulation of nuclear and mitochondria-related translation. The developmental defects observed were supported by a decreased expression of pathways related to eye development and haematopoiesis. The increase in mRNA translation might serve as a compensation mechanism, but appears insufficient during prolonged periods of mtDNA depletion, highlighting the importance of high mtDNA copy numbers for early development in zebrafish. SUMMARY STATEMENTThe first tuneable zebrafish model used to characterize the effect of a reduced mtDNA copy number and resulting OXPHOS deficiency on zebrafish embryonic development.

developmental biology↗

Intercellular adhesion stiffness moderates cell decoupling on stiff substrates

The interplay between cell-cell and cell-substrate interactions is complex yet necessary for the formation and well-functioning of tissues. The same mechanosensing mechanisms used by the cell to sense its extracellular matrix, also play a role in intercellular interactions. We used the discrete element method to develop a computational model of a deformable cell that includes subcellular components responsible for mechanosensing. We modeled a cell pair in 3D on a patterned substrate, a simple laboratory setup to study intercellular interactions. We explicitly modeled focal adhesions between the cells and the substrate, and adherens junctions between cells. These mechanosensing adhesions matured; their disassembly rate was dictated by the force they carry. We also modeled stress fibers which bind the discrete adhesions and contract. The mechanosensing fibers strengthened upon stalling and exerted higher forces. Traction exerted on the substrate was used to generate maps displaying the magnitude of the tractions along the cell-substrate interface. Simulated traction maps are compared to experimental maps obtained via traction force microscopy. The model recreates the dependence on substrate stiffness of the tractions spatial distribution across the cell-substrate interface, the contractile moment of the cell pair, the intercellular force, and the number of focal adhesions. It also recreates the phenomenon of cell decoupling, in which cells exert forces separately when substrate stiffness increases. More importantly, the model provides viable molecular explanations for decoupling. It shows that the implemented mechanosensing mechanisms are responsible for competition between different fiber-adhesion configurations present in the cell pair. The point at which an increasing substrate stiffness becomes as high as that of the cell-cell interface is the tipping point at which configurations that favor cell-substrate adhesion dominate over those favoring cell-cell adhesion. This competition is responsible for decoupling. Additionally, we learn that extent of decoupling is modulated by adherens junction maturation.\n\nStatement of SignificanceCells are sensitive to mechanical factors of their extracellular matrix while simultaneously in contact with other cells. This creates complex intercellular interactions that depend on substrate stiffness and play a role in processes such as development and diseases like cardiac arrhythmia, asthma, and cancer. The simplest cell collective system in vitro is a cell pair on a patterned substrate. We developed a computational model of this system which explains the role of molecular adhesions and contractile fibers in the dynamics of cell-cell interactions on substrates with different stiffness. It is one of the first models of a deformable cell collective based on mechanical principles. It recreates cellular decoupling, a phenomenon in which cells exert forces separately, when substrate stiffness increases.

bioengineering↗

Compaction dynamics during progenitor cell self-assembly reveal granular mechanics

We study the self-assembly dynamics of human progenitor cells in agarose micro-wells that are used for production of chondrogenic organoids. Using image analysis on time-lapse microscopy, we estimate the aggregate area in function of time for a large number of aggregates. In control conditions, the aggregate radius follows an exponential relaxation that is consistent with the dewetting dynamics of a liquid film. Introducing Y-27632 Rho kinase inhibitor, the compatibility with the liquid model is lost, and slowed down relaxation dynamics are observed. We demonstrate that these aggregates behave as granular piles undergoing compaction, with a density relaxation that follows a stretched exponential. Using simulations with an individual cell-based model, we construct a phase diagram of cell aggregates that suggests that the aggregate in presence of Rho kinase inhibitor approaches the glass transition.

biophysics↗

The role of actin protrusion dynamics in cell migration through a degradable viscoelastic extracellular matrix: Insights from a computational model

Actin protrusion dynamics plays an important role in the regulation of three-dimensional (3D) cell migration. Cells form protrusions that adhere to the surrounding extracellular matrix (ECM), mechanically probe the ECM and contract in order to displace the cell body. This results in cell migration that can be directed by the mechanical anisotropy of the ECM. However, the subcellular processes that regulate protrusion dynamics in 3D cell migration are difficult to investigate experimentally and therefore not well understood. Here, we present a computational model of cell migration through a degradable viscoelastic ECM. The cell is modeled as an active deformable object that captures the viscoelastic behavior of the actin cortex and the subcellular processes underlying 3D cell migration. The ECM is regarded as a viscoelastic material, with or without anisotropy due to fibrillar strain stiffening, and modeled by means of the meshless Lagrangian smoothed particle hydrodynamics (SPH) method. ECM degradation is captured by local fluidization of the material and permits cell migration through the ECM. We demonstrate that changes in ECM stiffness and cell strength affect cell migration and are accompanied by changes in number, lifetime and length of protrusions. Interestingly, directly changing the total protrusion number or the average lifetime or length of protrusions does not affect cell migration. A stochastic variability in protrusion lifetime proves to be enough to explain differences in cell migration velocity. Force-dependent adhesion disassembly does not result in faster migration, but can make migration more efficient. We also demonstrate that when a number of simultaneous protrusions is enforced, the optimal number of simultaneous protrusions is one or two, depending on ECM anisotropy. Together, the model provides non-trivial new insights in the role of protrusions in 3D cell migration and can be a valuable contribution to increase the understanding of 3D cell migration mechanics.\n\nAuthor summaryThe ability of cells to migrate through a tissue in the human body is vital for many processes such as tissue development, growth and regeneration. At the same time, abnormal cell migration is also playing an important role in many diseases such as cancer. If we want to be able to explain the origin of these abnormalities and develop new treatment strategies, we have to understand how cells are able to regulate their migration. Since it is challenging to investigate cell migration through a biological tissue in experiments, computational modeling can provide a valuable contribution. We have developed a computational model of cell migration through a deformable and degradable material that describes both mechanics of the cell and the surrounding material and subcellular processes underlying cell migration. This model captures the formation of long and thin protrusions that adhere to the surrounding material and that pull the cell forward. It provides new non-trivial insights in the role of these protrusions in cell migration and the regulation of protrusion dynamics by cell strength and anisotropic mechanical properties of the surrounding material. Therefore, we believe that this model can be a valuable tool to further improve the understanding of cell migration.

bioengineering↗