Cell migration is the directed movement of cells from one location to another, a fundamental biological process essential for establishing and maintaining the organization of multicellular organisms, including roles in morphogenesis, immune responses, wound healing, and tissuehomeostasis.[1] It occurs through various motility modes, such as mesenchymal migration, which relies on strong adhesions to the extracellular matrix (ECM) and actin-driven protrusions like lamellipodia and filopodia, and amoeboid migration, characterized by weak adhesions, rapid deformation, and high-speed movement (up to 10–15 μm/min in keratocytes).[2] Collective migration, in contrast, involves coordinated groups of cells moving together while preserving cell-cell contacts via adhesions like cadherins, often featuring leader cells that guide followers through signaling and mechanical cues.[3]The process is tightly regulated by intracellular mechanisms, including cytoskeletal dynamics (e.g., actin polymerization for protrusion and myosin contraction for force generation), integrin-mediated adhesions to the ECM, and responses to environmental signals like chemoattractants, substrate stiffness, and confinement.[1] Key steps encompass cell polarization to establish front-rear asymmetry, protrusion extension, traction force application, and rear retraction, enabling adaptation to diverse microenvironments such as 2D surfaces or 3D matrices.[2] In physiological contexts, it drives embryonic development (e.g., neural crestcell dispersal), immune surveillance (e.g., leukocyte recruitment to infection sites), and tissue regeneration (e.g., epidermal sheet migration in wound closure).[4]Aberrant cell migration underlies numerous pathologies, particularly cancer, where dysregulated motility facilitates tumor invasion and metastasis, as seen in collective invasion by breast or colorectal cancer cells adapting mesenchymal or amoeboid strategies.[3] Research models, from in vitro assays like Boyden chambers to in vivo systems such as zebrafish embryos, have elucidated these dynamics, highlighting therapeutic potential in targeting migration pathways for disease intervention.[2]
Overview
Definition and basic principles
Cell migration is defined as the directed movement of individual cells or groups of cells through tissues or along substrates, a process essential for multicellular organization.[1] This motility is primarily powered by actin-myosin contractility, where actin polymerization generates protrusive forces at the cell front, and myosin-mediated contraction enables rear retraction, all modulated by environmental cues such as chemical or mechanical signals.[5] The plasma membrane plays a critical role as the interface for sensing these cues, facilitating membrane turnover and lipid flow that support protrusion formation and overall cell dynamics during migration.[6]At its core, cell migration operates on several basic principles that dictate how cells respond to their surroundings. Chemotaxis involves the directional movement of cells up or down chemical gradients, allowing navigation toward attractants like nutrients or signaling molecules.[7] Haptotaxis refers to migration guided by gradients in substrate adhesiveness, where cells preferentially move toward regions of higher adhesion ligand density via integrin-mediated interactions.[7] Durotaxis describes the response to mechanical stiffness gradients in the extracellular matrix, with cells typically migrating toward stiffer areas through mechanosensitive cytoskeletal adjustments.[8] In contrast, random migration represents undirected motility, where cells explore their environment without specific guidance, often exhibiting persistent but stochastic paths.[9]Key cellular components underpin these processes as prerequisites for effective migration. The cytoskeleton, comprising actin filaments and microtubules, provides the structural framework: actin drives protrusion and contractility, while microtubules stabilize polarity and transport organelles to the leading edge.[10]Integrins, as transmembrane receptors, link the extracellular matrix to the actincytoskeleton, enabling traction generation and signal transduction essential for adhesion dynamics.[11]Historically, observations of cell migration trace back to the mid-19th century, with Rudolf Virchow describing motile cells isolated from lymph fluid and cartilage tissue in 1863, highlighting leukocyte movement in pathological contexts.[12] A pivotal advancement occurred in 1942, when Brúnó F. Straub discovered actin as a key protein in muscle extracts, later recognized for its central role in contractile motility across cell types.[13]
Biological significance
Cell migration plays a pivotal role in embryonic development, enabling the reorganization of tissues and formation of complex structures. During gastrulation, cells undergo coordinated migrations to form the three primary germ layers—ectoderm, mesoderm, and endoderm—which lay the foundation for organogenesis.[14] Neural crest cells, a transient multipotent population, delaminate from the neural tube and migrate extensively to contribute to diverse derivatives including peripheral neurons, craniofacial skeleton, and melanocytes. In angiogenesis, endothelial cells migrate directionally to form new vascular networks essential for oxygen and nutrient delivery during embryogenesis.[15] These processes highlight how cell migration drives morphogenetic movements critical for establishing the body plan.In immune function, cell migration facilitates rapid responses to pathogens by directing leukocytes to infection sites. Neutrophils and other leukocytes extravasate from blood vessels through diapedesis, a process involving adhesion to and transmigration across the endothelium, allowing them to infiltrate tissues and initiate inflammatory responses.[16] This recruitment is vital for containing infections and promoting clearance of debris.Cell migration maintains tissue homeostasis in adult organisms, supporting repair and renewal. In wound healing, keratinocytes migrate from the wound edges to re-epithelialize the injury site, while fibroblasts migrate into the provisional matrix to produce extracellular matrix components necessary for tissue remodeling.[17] Epithelial renewal, such as in the intestinal mucosa, relies on active migration of epithelial cells from stem cell niches toward the tissue surface, ensuring barrier integrity and turnover.[18]The mechanisms of cell migration exhibit remarkable evolutionary conservation, underscoring their fundamental importance across taxa. In the social amoebaDictyostelium discoideum, chemotaxis drives single-celled migration toward nutrients or during multicellular aggregation, sharing signaling pathways like phosphoinositide gradients with vertebrate leukocytes.[19] This conservation extends from unicellular eukaryotes to multicellular animals, reflecting an ancient adaptation for directed motility in response to environmental cues.[20]
Types of Cell Migration
Individual migration modes
Individual cell migration encompasses several distinct modes characterized by differences in cell morphology, adhesion to the extracellular matrix (ECM), and propulsion mechanisms. These modes allow cells to navigate diverse environments, from fluid-filled spaces to dense tissues, adapting to physical constraints and biochemical cues. The primary modes include amoeboid, mesenchymal, and blebbing migration, each optimized for specific contexts such as immune surveillance or tissue invasion.[21]Amoeboid migration features a rounded cell shape with minimal adhesions to the substrate, relying on high actomyosin contractility to squeeze through 3D matrices without significant ECM degradation. This mode is prevalent in leukocytes, such as neutrophils and dendritic cells, enabling rapid traversal of interstitial tissues during immune responses. Actomyosin-driven cortical tension generates intracellular pressure that propels the cell forward, often through weak, transient attachments rather than stable focal adhesions.[21]00008-2)[22]In contrast, mesenchymal migration involves an elongated, fibroblast-like morphology with strong, integrin-mediated adhesions to the ECM, coupled with proteolytic degradation of matrix barriers by matrix metalloproteinases (MMPs). This mode is typical of fibroblasts during wound healing and metastatic cancer cells invading stromal tissues, where cells extend lamellipodia or filopodia at the leading edge to probe and remodel the environment. The process requires coordinated cycles of adhesion formation, maturation, and disassembly, making it energy-intensive but effective for persistent directional movement.[21]00206-3)[23]Blebbing migration, often considered a subtype of amoeboid movement, is characterized by dynamic membrane protrusions called blebs, formed by localized rupture of the actin cortex and subsequent inflation via intracellular hydrostatic pressure. These blebs expand rapidly and retract through actin polymerization at their bases, facilitating propulsion in confined or low-adhesion settings, such as within tumor microenvironments or during embryonic development. This mode is observed in various cancer cells and amoeboid leukocytes under spatial constraints, where blebs enable cells to bypass adhesion-dependent mechanisms.[24][25][26]Key differences among these modes include migration speed and energy demands: amoeboid and blebbing cells typically achieve velocities of 10–30 μm/min, far exceeding the 0.1–1 μm/min of mesenchymal migration, due to reduced reliance on adhesion turnover and matrix remodeling. Amoeboid and blebbing modes demand less energy for adhesion but higher contractility, while mesenchymal migration invests in proteolytic and signaling pathways for sustained traction.[21][23]Environmental factors, particularly substrate dimensionality, profoundly influence mode selection and switching. On 2D surfaces, cells often default to mesenchymal migration with prominent lamellipodia, but in 3D dense ECM, mesenchymal cells can transition to faster amoeboid or blebbing modes to navigate confinement without proteolysis, as seen in tumor cells encountering high matrix density. This plasticity enhances invasion efficiency by allowing adaptation to varying mechanical barriers.00008-2)[21][27]
Collective migration
Collective cell migration refers to the coordinated movement of groups of cells, such as sheets, strands, or clusters, that maintain intercellular connections while advancing as a unit. This process is distinct from individual cell motility, as the behavior of one cell influences its neighbors through physical and chemical interactions, enabling tissue-scale dynamics without complete disruption of cell-cell contacts.[28][29] Prominent examples include epithelial wound closure, where keratinocytes collectively migrate to seal gaps in the skin, and neural crest streams, where multipotent cells form elongated chains that delaminate from the neural tube and invade surrounding tissues during embryogenesis.[30][31]Key mechanisms underlying collective migration involve cadherin-mediated adherens junctions, which transmit mechanical forces across cells to synchronize protrusions and retractions. These junctions, primarily E-cadherin in epithelial contexts, couple the cytoskeletons of adjacent cells, allowing traction forces generated at the leading edge to propagate rearward and guide follower cells.[32][33] A hallmark feature is leader-follower dynamics, in which specialized leader cells at the front extend protrusions via actinpolymerization and form focal adhesions, while follower cells in the rear adopt a more passive role, relying on intercellular tugs to maintain cohesion and directionality.[34][35]Classic examples illustrate these principles in vivo. In Drosophila border cell migration, a cluster of 6-10 cells detaches from the follicular epithelium during oogenesis and invades the egg chamber as a cohesive group, guided by chemotactic signals and maintained by cadherin junctions that ensure collective polarity.[36] Similarly, vertebrate epiboly during gastrulation involves the collective spreading of a blastodermal cell sheet over the yolk, driven by radial intercalation and purse-string contractility at the margin, which expands the epithelial layer to envelop the embryo.[37][38]Biomechanically, collective migration relies on stress propagation through cell-cell contacts, where contractile forces from myosin II at junctions create anisotropic tension fields that align cell orientations and velocities across the group.[39] In stream-like formations, such as neural crest chains, velocity gradients emerge with front cells moving faster due to stronger protrusive activity, while rear cells experience drag from adhesions, resulting in a tapered speed profile that sustains stream integrity over distances exceeding 100 cell diameters.[31][40]Recent post-2020 studies have highlighted the role of YAP/TAZ signaling in collective durotaxis, where groups of mammary gland cells preferentially migrate toward softer substrates by modulating focal adhesion maturation and cytoskeletal dynamics, enabling persistent motility in mechanically heterogeneous environments. This mechanotransductive pathway integrates substrate stiffness gradients with intercellular force transmission, promoting coordinated invasion in breast tissue models.[41]
Molecular and Cellular Mechanisms
Establishment of cell polarity
Cell polarity establishment is a fundamental process in directed cell migration, where cells develop a front-rear asymmetry that defines the direction of movement. This asymmetry arises through the coordinated activation of signaling pathways that localize protrusive and contractile machinery to specific cellular regions, enabling persistent motion toward environmental cues. In migrating cells, such as fibroblasts or leukocytes, polarity is initiated by external stimuli that break the initial symmetry, leading to the recruitment of key regulatory proteins to the leading edge and suppression at the rear.00469-4)Central to this process are Rho family GTPases, which establish asymmetric signaling gradients. Cdc42 activates at the front to promote protrusion and directional sensing, while RhoA predominates at the rear to drive contractility and tail retraction. This spatial segregation is mediated by guanine nucleotide exchange factors (GEFs) and GTPase-activating proteins (GAPs) that respond to upstream signals, ensuring mutually inhibitory interactions between Cdc42 and RhoA. For instance, in migrating astrocytes, Cdc42 activation via integrins triggers polarity by orienting cytoskeletal elements toward the wound edge.00469-4)[42]The PI3K-Akt pathway further reinforces front-rear asymmetry by localizing to the leading edge, where it generates phosphatidylinositol (3,4,5)-trisphosphate (PIP3) gradients that recruit effectors for protrusion. In chemotaxing Dictyostelium cells, PI3K accumulates rapidly at the front in response to stimuli, activating Akt to stabilize polarity through downstream targets that inhibit rear signaling. This localization depends on receptor-mediated activation and is essential for maintaining the PIP3 bias, which in turn confines Akt activity to the advancing edge.00755-9)00833-5)Organelle repositioning contributes to polarity by aligning the secretory apparatus with the migration direction. The Golgi apparatus and microtubule-organizing center (MTOC) reorient toward the leading edge, facilitating targeted vesicle delivery and microtubule stabilization at the front. In migrating epithelial cells, Cdc42 coordinates this reorientation by coupling the MTOC to the actin cytoskeleton via dynein motors, positioning the Golgi between the nucleus and the direction of travel. This alignment enhances directional persistence, as seen in fibroblasts during wound healing.[43]00188-1)External cues, such as chemoattractant gradients, trigger polarity via G-protein-coupled receptors (GPCRs) that activate heterotrimeric G proteins. In neutrophils, binding of formyl peptides to GPCRs initiates asymmetric Gβγ signaling, leading to front enrichment of activators like PI3K within seconds. This receptor-mediated response decodes shallow gradients (1-2% difference across the cell) to establish a single leading edge.Feedback loops amplify and stabilize these asymmetries. Positive reinforcement at the front involves Arp2/3-mediated actin nucleation, which sustains protrusion and recruits additional signaling molecules to amplify the signal. Conversely, inhibitory signals at the rear, driven by myosin II contractility, suppress ectopic protrusions and promote detachment. In motile cells like Dictyostelium, these reciprocal loops—linking actinpolymerization to PI3K activation at the front and myosin II to RhoA at the rear—ensure robust polarity. Such mechanisms are critical in immune cells, where rapid polarization enables efficient chemotaxis to infection sites.[44]Temporally, polarity establishment occurs rapidly, typically within 5-10 minutes in response to uniform chemoattractant exposure, allowing cells to break symmetry and initiate directed migration. In neutrophils, this involves sequential waves of signaling that stabilize the front within 30-90 seconds, followed by full asymmetry consolidation.[45][46]
Cytoskeletal remodeling
Cytoskeletal remodeling is essential for cell migration, involving the dynamic reorganization of actin filaments and microtubules to generate protrusive forces at the leading edge and contractile forces for rear retraction. In migrating cells, actin polymerization drives the formation of protrusions such as lamellipodia and filopodia, while microtubules provide structural support and directional cues. Non-muscle myosin II contributes to force generation, enabling the cell to propel forward against substrate resistance. These processes are powered by ATP hydrolysis, which sustains continuous cytoskeletal turnover.Actin dynamics form the core of protrusive activity during cell migration. In lamellipodia, branched actin networks are assembled by the Arp2/3 complex, which nucleates new filaments at approximately 70° angles from existing ones, creating a dendritic array that pushes the plasma membrane forward.[47] This branching is crucial for broad, sheet-like protrusions in adherent cells. In contrast, filopodia feature linear bundles of unbranched actin filaments, polymerized by formins that elongate filaments from their barbed ends without branching.[48] Actin polymerization rates in these structures typically range from 0.1 to 1 μm/s, allowing rapid extension of protrusions under physiological monomer concentrations.[49]Microtubules play a supportive role in cytoskeletal remodeling by stabilizing the leading edge and facilitating directed motility. They polymerize toward the front of the cell, where their plus ends anchor to the cortex, providing a scaffold for vesicle and organelle transport essential for protrusion maintenance.[50]Dynein motors, anchored at the cortex, pull on microtubule minus ends to orient the microtubule-organizing center toward the direction of migration, enhancing overall polarity and force transmission.[51]Myosin contractility, mediated by non-muscle myosin II, generates the traction forces necessary to counterbalance protrusive expansion and drive cell body advancement. Assemblies of myosin II minifilaments hydrolyze ATP to cross-link and slide actin filaments, producing forces in the range of 10-100 pN per focal contact, which propel the cell forward while inducing retrogradeactin flow at the leading edge.[52] This contractility ensures coordinated rearward movement of the cytoskeleton relative to the substrate.Key regulatory proteins fine-tune these dynamics. The WAVE/Scar complex activates the Arp2/3 complex at the leading edge by recruiting it to sites of Rac signaling, promoting efficient branched network formation for lamellipodial protrusion.[53] In filopodia, fascin bundles parallel actin filaments into rigid shafts, stabilizing them against disassembly and supporting sensing of the extracellular environment.[54]The energy for these remodeling events derives from ATP hydrolysis, which powers actintreadmilling—the continuous addition of ATP-actin at barbed ends and dissociation of ADP-actin from pointed ends—maintaining filament flux without net length change under steady-state conditions.[55] Recent structural insights from cryo-EM have refined our understanding of Arp2/3-mediated branching, confirming the canonical 70° branch angle in mature junctions and highlighting conformational changes upon activation.[56]
Adhesion dynamics and signaling
Cell adhesion to the extracellular matrix (ECM) during migration is primarily mediated by focal adhesions (FAs), dynamic protein complexes that assemble at integrin-based sites. Integrin clusters bind ECM ligands, recruiting talin to link integrins to the actin cytoskeleton, followed by vinculin for structural reinforcement and focal adhesion kinase (FAK) for signaling initiation.[57] This assembly begins with nascent adhesions forming small integrin clusters (<250 nm) in the lamellipodium, which mature into sliding focal complexes at the lamellipodium-lamella transition under initial tension, and further develop into stable focal adhesions anchored to stress fibers upon sustained force application.[58]FA signaling integrates mechanical cues with biochemical pathways to drive migration. Upon integrin engagement, FAK undergoes autophosphorylation at Tyr397, recruiting and activating Src kinase, which in turn phosphorylates FAK at additional sites to form a complex that stimulates the ERK/MAPK cascade, promoting gene expression changes and cytoskeletal reorganization essential for motility.[59] Phosphoinositides such as phosphatidylinositol 4,5-bisphosphate (PIP2) and phosphatidylinositol 3,4,5-trisphosphate (PIP3) localize to FAs, with PIP2 levels rising during assembly to recruit effectors like talin and FAK, while PIP3 supports broader signaling; these lipids facilitate FA maturation and turnover to sustain directed movement.[60]FA dynamics involve rapid assembly and disassembly to enable protrusion and retraction. Nascent adhesions form within seconds of integrin binding, while mature FAs disassemble over minutes, allowing net forward translocation.[61] In the molecular clutch model, retrograde actin flow engages adhesions like a clutch: at low loads, linkages slip, permitting actin polymerization to drive protrusion without traction; at higher loads, clutches grip the ECM, transmitting force for cell advancement, with slippage dominating at the cell rear to facilitate disassembly.[62]Interactions with specific ECM components modulate adhesion strength. The α5β1 integrin binds fibronectin with high affinity (Kd ≈ 1.5–1.7 nM), enabling stable anchorage, whereas collagen engagement via other integrins like α2β1 supports diverse migratory contexts.[63]Growth factors such as epidermal growth factor (EGF) fine-tune adhesion dynamics to optimize migration. EGF enhances directional persistence by stabilizing lamellipodial protrusions and modulating adhesion strength, reducing detachment rates on fibronectin substrates to balance speed and directionality.[64] These adhesion processes interface briefly with cytoskeletal elements, where talin and vinculin transmit signals to actin networks for coordinated force generation.[57]
Theoretical Models of Motility
Cytoskeletal protrusion model
The cytoskeletal protrusion model posits that cell migration is primarily driven by the polymerization of actin filaments at the leading edge, generating protrusive forces that push the plasma membrane forward. In this framework, actin monomers (G-actin) assemble into filamentous actin (F-actin) networks, particularly in structures like lamellipodia, creating a polymerizing front that advances the cell edge against mechanical resistance. This model emphasizes the role of directed actin assembly and disassembly, known as treadmilling, where polymerization at the barbed (plus) ends near the membrane exceeds depolymerization at the pointed (minus) ends, resulting in net forward protrusion. Originally conceptualized for bacterial motility, it was adapted to eukaryotic cell migration, highlighting how thermal fluctuations enable filament growth despite spatial constraints imposed by the membrane.A key quantitative aspect of the model is the protrusion velocity, derived from the balance of polymerization and depolymerization fluxes. The net velocity v is given byv = (J_{\text{polymer}} - J_{\text{depolymer}}) \cdot \delta,where J_{\text{polymer}} is the flux of actin subunits adding to the filament barbed end (typically k_{\text{on}} \cdot C, with k_{\text{on}} the on-rate constant and C the free G-actin concentration), J_{\text{depolymer}} is the flux from the pointed end (k_{\text{off}}), and \delta is the size of an actin subunit, approximately 2.7 nm. This equation captures how the steady-state treadmilling rate translates into membrane advancement, with protrusion stalling when loads equal the polymerization force, estimated at 1-10 pN per filament.Central components include the Brownian ratchet mechanism, which rectifies thermal Brownian motion to prevent backward diffusion of the membrane and allow continuous subunit addition by transiently separating the filament tip from the membrane barrier. Complementing this, the elastic clutch hypothesis describes how linkage proteins (e.g., ENA/VASP family members) transmit polymerization-generated forces to the substrate via adhesions, with clutch slippage under high loads enabling adaptive force distribution across the actin network. These elements ensure efficient force generation, with polymerization rates of 1-10 subunits per second per filament supporting observed protrusion speeds of 0.1-1 μm/min in motile cells.The model predicts that protrusion speed inversely correlates with mechanical load, such as viscous drag from the extracellular medium, where drag force scales as F_{\text{drag}} \approx \eta v, with \eta as viscosity; higher loads reduce effective polymerization by compressing the ratchet space, leading to slower migration. Experimental perturbations, like increasing actinmonomer availability, enhance velocity until saturation, aligning with the flux-based formulation.Despite its explanatory power, the model is most applicable to two-dimensional lamellipodial protrusion in adherent cells on flat substrates, where branched actin networks dominate. It applies less effectively to three-dimensional environments or bleb-based migration, where hydrostatic pressure or cortical actomyosin contractility play larger roles in force balance. Updates in the 2000s refined it to incorporate multi-filament interactions and load-dependent kinetics, but it remains a foundational framework for polymerization-centric motility.
Membrane flow and traction models
The membrane flow model posits that cell migration arises from retrograde flow of the plasma membrane originating at the leading edge, which is subsequently recycled through endocytosis primarily at the cell rear. This flow is driven by cortical tension generated by actomyosin contractility, creating a continuous circulation of membrane material that propels the cell forward without requiring strong substrate adhesions. Experimental evidence from photobleaching studies in Dictyostelium discoideum supports this "fountain flow" mechanism, where membrane components move rearward at speeds correlating with migration velocity, with a half-life of approximately 60 seconds in fast-moving cells.[6]Endocytosis at the rear, an energy-dependent process inhibited by metabolic blockers like sodium azide, ensures membrane balance and sustains the flow.[6]In contrast, the traction model emphasizes myosin-generated contractile forces pulling on substrate adhesions to achieve net cell displacement. Non-muscle myosin II assembles at adhesions, generating rearward tension that detaches the cell body and advances the leading edge relative to the substrate. Traction force microscopy measurements reveal typical stress magnitudes of around 50 pN/μm² in migrating epithelial cells on compliant substrates, highlighting the scale of these forces in mesenchymal migration.[65] This model underscores how clutch-like engagement of adhesions modulates force transmission, with myosin activity directly linking contractility to propulsion.[66]A unifying framework in these models describes net cell velocity as the difference between protrusion velocity and retrograde flow velocity:v_{\text{net}} = v_{\text{protrusion}} - v_{\text{retrograde}}Here, v_{\text{retrograde}} represents the backward actin-membrane flow, given by v_{\text{retrograde}} = F_{\text{clutch}} / \beta, where F_{\text{clutch}} is the force transmitted through adhesion clutches and \beta is the viscous drag coefficient opposing flow.[66] This equation captures how effective clutch engagement reduces retrograde flow, enhancing forward migration.Hybrid models integrate membrane flow with cytoskeletal protrusions, simulating scenarios where both mechanisms coexist for adaptive motility. Recent biophysical simulations demonstrate that in amoeboid cells, membrane flow dominates propulsion, particularly in low-adhesion environments, optimizing speed and efficiency over pure protrusion-based modes. These integrations reveal an optimal hybrid regime for transitioning between migration modes. Such models notably explain bleb-based amoeboid migration, where adhesion-independent propulsion relies on cortical flow and transient bleb expansion driven by intracellular pressure, as observed in RhoA-activated leukocytes.[67]
Recent theoretical advances
Post-2020 developments have expanded these frameworks to include novel force-generation mechanisms. The osmotic engine model proposes that ion and water fluxes, mediated by channels like NHE-1 and aquaporins, create osmotic pressure gradients that drive protrusion and migration, particularly in confined or 3D environments; this synergizes with actin-based motility, as disrupting polymerization halves speeds in breast cancer cells.[68] Similarly, the nuclear piston mechanism posits that the nucleus acts as a piston, generating hydrostatic pressure (~2400 Pa at the front versus ~900 Pa at the rear) to expand lobopodia in mesenchymal-like migration. Hybrid models further integrate blebbing with adhesions, explaining rapid transitions in cancer cells within collagen matrices, with theoretical predictions matching observed physiological speeds up to 2025.[68]
Experimental Approaches
In vitro migration assays
In vitro migration assays provide controlled environments to quantify cell movement under defined conditions, enabling the study of chemotaxis, haptotaxis, and durotaxis without the complexities of living tissues. These assays typically involve two-dimensional or three-dimensional substrates that mimic aspects of the extracellular matrix (ECM), allowing researchers to manipulate variables such as chemoattractant gradients and substrate properties. Common setups include transwell systems and scratch assays, which facilitate high-throughput screening and precise measurement of migratory behaviors.The Boyden chamber assay, first described in 1962, consists of two compartments separated by a porous membrane, where cells in the upper chamber migrate toward a chemoattractant in the lower chamber, assessing directed motility or chemotaxis.[69] Modern adaptations, known as Transwell assays, use inserts with polycarbonate membranes featuring pore sizes of 3-8 μm, suitable for various cell types such as leukocytes (3 μm pores) or epithelial cells (8 μm pores).[70] To evaluate invasion, the membrane is coated with Matrigel, a basement membrane matrix that requires cells to degrade and traverse the ECM-like barrier, quantifying metastatic potential through cell counts on the underside of the membrane after a fixed incubation period.[71]The wound healing assay, also called the scratch assay, involves creating an artificial gap in a confluent monolayer of cells using a pipette tip or stamp, followed by monitoring collective migration to close the wound via time-lapse microscopy.[72] This method assesses both individual and coordinated cell movements in a two-dimensional setting, with wound closure rates calculated as the reduction in gap area over time, typically over 12-48 hours depending on cell type.[73]Key metrics in these assays include persistence length, which measures directionality as the average distance a cell travels in a straight path before changing direction, reflecting the stability of migratory polarity.[74] Another fundamental metric is mean squared displacement (MSD), defined for two-dimensional diffusive motion as\text{MSD} = 4Dt,where D is the diffusion coefficient and t is time, providing insight into random versus directed motility by analyzing trajectory deviations from Brownian motion.[75]These assays offer advantages such as high throughput, with Transwell formats supporting parallel testing of multiple conditions in 96-well plates, and precise control over environmental cues like linear chemoattractant gradients generated via microfluidic devices.[76] Microfluidics enable stable, tunable gradients over micrometer scales, improving reproducibility compared to diffusion-based systems.[77]Recent advances include organ-on-chip models, which integrate three-dimensional ECM hydrogels with tunable stiffness (e.g., 0.1-50 kPa) to simulate tissue mechanics, allowing real-time observation of cell migration in vascularized or tumor-like environments.
In vivo imaging and analysis
In vivo imaging techniques enable the observation of cell migration within living organisms, providing insights into physiological contexts that in vitro assays cannot replicate. Two-photon microscopy, which uses near-infrared light to excite fluorophores, facilitates deep tissue imaging by reducing scattering and phototoxicity compared to single-photon methods, allowing visualization up to several hundred micrometers in depth. This approach has been instrumental in tracking immune cell dynamics and tumor cell movements in intact tissues. Intravital imaging windows, such as cranial or abdominal chambers implanted in mice, further enhance access to internal sites like brain tumors or mammary glands, enabling repeated, longitudinal monitoring of tumor cell invasion and metastasis without disrupting the native microenvironment. For instance, these windows have revealed how cancer cells navigate through stromal barriers in real time during orthotopic pancreatic tumor progression.Despite these advances, in vivo imaging faces significant challenges, including tissue opacity from light scattering in dense structures like skin or brain, which limits penetration depth, and motion artifacts from breathing or heartbeat that blur dynamic processes. Typical resolutions achieve approximately 1 μm laterally and 2-3 μm axially, sufficient for single-cell tracking but constraining subcellular details in deeper layers. To mitigate these, stabilized mounts and adaptive optics are employed, though they cannot fully eliminate physiological movements in non-anesthetized models.Analysis of in vivo migration data relies on computational tools to extract quantitative metrics from complex, noisy datasets. Particle image velocimetry (PIV) processes time-lapse images to compute velocity fields and trajectories of individual or collective cell movements, revealing patterns like swirling flows in epithelial sheets during zebrafish lateral line primordium migration. Segmentation algorithms, often based on deep learning networks like U-Net, delineate cell boundaries in phase-contrast or fluorescence images, enabling the quantification of collective flows and neighbor interactions in dense tissues. For assessing cell-cell interactions, correlation spectroscopy techniques, such as spatiotemporal image correlation spectroscopy (STICS), measure flux rates and co-diffusion of molecules between migrating cells, providing rates of adhesive or signaling exchanges during epithelial wound closure.Key insights from these methods highlight the dynamic regulation of migration in development. Real-time imaging in zebrafish has shown that neural crest cells establish polarity through planar cell polarity (PCP) signaling, with asymmetric localization of proteins like Prickle1 directing oriented migration along axon tracts. These approaches underscore the interplay between individual polarity and collective coordination in vivo.
Pathological Dysregulation
Role in cancer progression
Cell migration plays a pivotal role in cancer progression by enabling the dissemination of tumor cells from the primary site to distant organs, a process central to metastasis. During epithelial-mesenchymal transition (EMT), transcription factors such as Snail and Twist reprogram epithelial cancer cells into a mesenchymal state, enhancing their migratory and invasive capabilities. Snail overexpression in carcinoma cells induces EMT, leading to loss of cell-cell adhesion and increased motility essential for tumor invasion. Similarly, Twist drives EMT in breast cancer cells, promoting their detachment from the primary tumor and subsequent migration to metastatic sites. This mesenchymal mode, characterized by elongated morphology and upregulated motility genes, facilitates cancer cell invasion through tissue barriers.[78][79]Invasion mechanisms in cancer rely on proteolytic remodeling of the extracellular matrix (ECM) and specialized structures like invadopodia. Matrix metalloproteinases (MMPs), particularly MMP-2 and MMP-9, degrade ECM components such as collagen and laminin, creating paths for tumor cell advancement and promoting invasion. These enzymes are upregulated in metastatic cancers, where they facilitate tissue remodeling and angiogenesis to support migratory spread. Invadopodia, actin-rich protrusions enriched with cortactin, enable localized ECM degradation and are critical for cancer cell penetration into surrounding stroma. Cortactin phosphorylation at invadopodia regulates their maturation and turnover, directly enhancing invasive migration in breast and other carcinomas. In hypoxic tumor microenvironments, common in solid cancers, breast cancer cells exhibit significantly enhanced migration rates, with motility increasing up to several-fold compared to normoxic conditions, driven by pathways like HIF-1α and PERK signaling.[80][81][82]The metastatic cascade involves sequential steps where dysregulated cell migration drives tumor spread: local invasion, intravasation into blood or lymphatic vessels, survival during circulation as circulating tumor cells, extravasation into distant tissues, and colonization to form secondary tumors. Metastasis is the primary cause of cancer mortality, accounting for an estimated 70-90% of cancer-related deaths, though recent studies suggest around 70% for solid tumors, as primary tumors are often treatable but metastases resist therapy and lead to organ failure.[83] Aberrant migration during intravasation and extravasation is particularly rate-limiting, with invadopodia aiding endothelial breaching. Therapeutic strategies targeting these migratory events have included MMP inhibitors like marimastat, a broad-spectrum blocker of MMP-2 and MMP-9, which showed preclinical promise but failed in Phase III trials in the early 2000s due to musculoskeletal toxicity and lack of efficacy in cancers like pancreatic and lung. Emerging approaches as of 2025 include CAR-T cell therapies engineered to enhance infiltration and target solid tumors, with designs incorporating chemokine receptors like CXCR3 to improve trafficking and potentially disrupt metastatic migration dynamics in preclinical models.[84][85][86][87]
Involvement in immune responses and inflammation
Cell migration plays a central role in immune responses by enabling leukocytes to extravasate from the bloodstream into inflamed tissues, where they combat pathogens and facilitate tissue repair. This process begins with leukocyte rolling along the vascular endothelium, mediated by selectins such as P-selectin and E-selectin expressed on activated endothelial cells, which bind to carbohydrate ligands on leukocytes like sialyl Lewis X, allowing initial tethering and slowing of rolling leukocytes.[88] Firm arrest follows, driven by the activation of leukocyte integrins such as LFA-1 (αLβ2) and Mac-1 (αMβ2), which transition to a high-affinity state in response to chemokine signaling and bind tightly to endothelial ligands ICAM-1 and ICAM-2, halting the rolling leukocytes.[89] Transmigration, or diapedesis, then occurs primarily through paracellular routes, facilitated by homophilic interactions of PECAM-1 (CD31) between leukocytes and endothelial junctions, enabling leukocytes to cross the endothelial barrier and enter the subendothelial space.[90]Chemokine gradients are essential for directing leukocyte migration to sites of inflammation. For instance, CXCL8 (also known as IL-8) forms gradients that potently attract neutrophils via CXCR1 and CXCR2 receptors, promoting their chemotaxis to infection or injury sites.[91] Similarly, dendritic cells rely on CCR7 expression to sense CCL19 and CCL21 gradients in lymphatic vessels, enabling their homing to draining lymph nodes for antigen presentation and T cell priming.[92] These gradients ensure precise recruitment, with neutrophils often exhibiting amoeboid migration modes to rapidly navigate through inflamed tissues.[93]In the resolution phase of inflammation, cell migration contributes to tissue homeostasis by clearing apoptotic cells and dampening recruitment. Macrophages perform efferocytosis, phagocytosing apoptotic neutrophils and other dying cells, which prevents secondary necrosis and promotes the release of anti-inflammatory mediators to resolve inflammation.[94]Anti-inflammatory signals, such as TGF-β, further halt excessive leukocyte migration by suppressing chemokine production and integrin activation in immune cells, thereby limiting ongoing recruitment and facilitating return to steady-state conditions.[95]Dysregulated cell migration underlies chronic inflammatory conditions, including atherosclerosis, where excessive monocyterecruitment into arterial walls drives plaque formation. Monocytes, attracted by chemokines like CCL2, extravasate and differentiate into macrophages that accumulate lipids, exacerbating inflammation and lesion progression.[96] In wound healing, 2022 studies highlighted neutrophil swarming, a collectivemigration behavior where neutrophils rapidly converge on injury sites in relay waves, amplifying recruitment but self-limiting to prevent tissue damage.[93]Neutrophils in inflamed tissues typically migrate at speeds of 10-20 μm/min, allowing swift responses while resolution mechanisms ensure controlled dispersal.[97]