XB-ART-59915
Elife
2023 Jul 10;12. doi: 10.7554/eLife.87181.
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From actin waves to mechanism and back: How theory aids biological understanding.
Beta C
,
Edelstein-Keshet L
,
Gov N
,
Yochelis A
.
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Actin dynamics in cell motility, division, and phagocytosis is regulated by complex factors with multiple feedback loops, often leading to emergent dynamic patterns in the form of propagating waves of actin polymerization activity that are poorly understood. Many in the actin wave community have attempted to discern the underlying mechanisms using experiments and/or mathematical models and theory. Here, we survey methods and hypotheses for actin waves based on signaling networks, mechano-chemical effects, and transport characteristics, with examples drawn from Dictyostelium discoideum, human neutrophils, Caenorhabditis elegans, and Xenopus laevis oocytes. While experimentalists focus on the details of molecular components, theorists pose a central question of universality: Are there generic, model-independent, underlying principles, or just boundless cell-specific details? We argue that mathematical methods are equally important for understanding the emergence, evolution, and persistence of actin waves and conclude with a few challenges for future studies.
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Species referenced: Xenopus laevis
GO keywords: actin polymerization or depolymerization [+]
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References [+] :
Abercrombie,
The locomotion of fibroblasts in culture. II. "RRuffling".
1970, Pubmed
Abercrombie, The locomotion of fibroblasts in culture. II. "RRuffling". 1970, Pubmed
Allard, Traveling waves in actin dynamics and cell motility. 2013, Pubmed
Alonso, Nonlinear physics of electrical wave propagation in the heart: a review. 2016, Pubmed
Alonso, Modeling random crawling, membrane deformation and intracellular polarity of motile amoeboid cells. 2018, Pubmed
Alt, Patterns of spontaneous motility in videomicrographs of human epidermal keratinocytes (HEK). 1995, Pubmed
Arai, Self-organization of the phosphatidylinositol lipids signaling system for random cell migration. 2010, Pubmed
Asano, Correlated waves of actin filaments and PIP3 in Dictyostelium cells. 2008, Pubmed
Avila Ponce de León, A phosphoinositide-based model of actin waves in frustrated phagocytosis. 2021, Pubmed
Bailey, Reverse engineering an amyloid aggregation pathway with dimensional analysis and scaling. 2011, Pubmed
Bailles, Mechanochemical Principles of Spatial and Temporal Patterns in Cells and Tissues. 2022, Pubmed
Banerjee, Spatiotemporal dynamics of membrane surface charge regulates cell polarity and migration. 2022, Pubmed
Barnhart, An adhesion-dependent switch between mechanisms that determine motile cell shape. 2011, Pubmed
Barnhart, Adhesion-Dependent Wave Generation in Crawling Cells. 2017, Pubmed
Bement, Activator-inhibitor coupling between Rho signalling and actin assembly makes the cell cortex an excitable medium. 2015, Pubmed , Xenbase
Ben Isaac, Linking actin networks and cell membrane via a reaction-diffusion-elastic description of nonlinear filopodia initiation. 2013, Pubmed
Bernitt, Dynamics of actin waves on patterned substrates: a quantitative analysis of circular dorsal ruffles. 2015, Pubmed
Bernitt, Fronts and waves of actin polymerization in a bistability-based mechanism of circular dorsal ruffles. 2017, Pubmed
Beta, Why a Large-Scale Mode Can Be Essential for Understanding Intracellular Actin Waves. 2020, Pubmed
Bhattacharya, Traveling and standing waves mediate pattern formation in cellular protrusions. 2020, Pubmed
Blanchoin, Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. 2000, Pubmed
Bloomfield, Uses and abuses of macropinocytosis. 2016, Pubmed
Bolado-Carrancio, Periodic propagating waves coordinate RhoGTPase network dynamics at the leading and trailing edges during cell migration. 2020, Pubmed
Bretschneider, Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. 2004, Pubmed
Bretschneider, The three-dimensional dynamics of actin waves, a model of cytoskeletal self-organization. 2009, Pubmed
Brzeska, The association of myosin IB with actin waves in dictyostelium requires both the plasma membrane-binding site and actin-binding region in the myosin tail. 2014, Pubmed
Brzeska, Dictyostelium myosin 1F and myosin 1E inhibit actin waves in a lipid-binding-dependent and motor-independent manner. 2020, Pubmed
Buccione, Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. 2004, Pubmed
Buttenschön, Cell Repolarization: A Bifurcation Study of Spatio-Temporal Perturbations of Polar Cells. 2022, Pubmed
Byrne, Bistability in the Rac1, PAK, and RhoA Signaling Network Drives Actin Cytoskeleton Dynamics and Cell Motility Switches. 2016, Pubmed
Camley, Periodic migration in a physical model of cells on micropatterns. 2013, Pubmed
Camley, Crawling and turning in a minimal reaction-diffusion cell motility model: Coupling cell shape and biochemistry. 2017, Pubmed
Campbell, A computational model of amoeboid cell motility in the presence of obstacles. 2018, Pubmed
Cao, A minimal computational model for three-dimensional cell migration. 2019, Pubmed
Cao, Plasticity of cell migration resulting from mechanochemical coupling. 2019, Pubmed
Carlsson, Actin dynamics: from nanoscale to microscale. 2010, Pubmed
Case, Adhesive F-actin waves: a novel integrin-mediated adhesion complex coupled to ventral actin polymerization. 2011, Pubmed
Cherkashin, Discontinuously propagating waves in the bathoferroin-catalyzed Belousov-Zhabotinsky reaction incorporated into a microemulsion. 2008, Pubmed
Chhabra, The many faces of actin: matching assembly factors with cellular structures. 2007, Pubmed
Desroches, Classification of bursting patterns: A tale of two ducks. 2022, Pubmed
Devreotes, Excitable Signal Transduction Networks in Directed Cell Migration. 2017, Pubmed
Diz-Muñoz, Use the force: membrane tension as an organizer of cell shape and motility. 2013, Pubmed
Diz-Muñoz, Membrane Tension Acts Through PLD2 and mTORC2 to Limit Actin Network Assembly During Neutrophil Migration. 2016, Pubmed
Dogterom, Actin-microtubule crosstalk in cell biology. 2019, Pubmed
Dominguez, Actin structure and function. 2011, Pubmed
Doubrovinski, Cell motility resulting from spontaneous polymerization waves. 2011, Pubmed
Driscoll, Cell shape dynamics: from waves to migration. 2012, Pubmed
Driscoll, Cellular contact guidance through dynamic sensing of nanotopography. 2014, Pubmed
Driscoll, Spatiotemporal relationships between the cell shape and the actomyosin cortex of periodically protruding cells. 2015, Pubmed
Döbereiner, Lateral membrane waves constitute a universal dynamic pattern of motile cells. 2006, Pubmed
Ecke, Formins specify membrane patterns generated by propagating actin waves. 2020, Pubmed
Enculescu, Modeling of protrusion phenotypes driven by the actin-membrane interaction. 2010, Pubmed
Etienne-Manneville, Rho GTPases in cell biology. 2002, Pubmed
Fitzhugh, Impulses and Physiological States in Theoretical Models of Nerve Membrane. 1961, Pubmed
Flemming, How cortical waves drive fission of motile cells. 2020, Pubmed
Flyvbjerg, Kinetics of self-assembling microtubules: an "inverse problem" in biochemistry. 1996, Pubmed
Fukushima, Excitable dynamics of Ras triggers spontaneous symmetry breaking of PIP3 signaling in motile cells. 2019, Pubmed
Ganusov, Strong Inference in Mathematical Modeling: A Method for Robust Science in the Twenty-First Century. 2016, Pubmed
Gerhardt, Actin and PIP3 waves in giant cells reveal the inherent length scale of an excited state. 2014, Pubmed
Gerhardt, Signaling in chemotactic amoebae remains spatially confined to stimulated membrane regions. 2014, Pubmed
Gerisch, Mobile actin clusters and traveling waves in cells recovering from actin depolymerization. 2004, Pubmed
Gerisch, Self-organizing actin waves as planar phagocytic cup structures. 2009, Pubmed
Gerisch, Self-organizing actin waves that simulate phagocytic cup structures. 2010, Pubmed
Gerisch, Different modes of state transitions determine pattern in the Phosphatidylinositide-Actin system. 2011, Pubmed
Gerisch, PIP3 waves and PTEN dynamics in the emergence of cell polarity. 2012, Pubmed
Ghabache, Coupling traction force patterns and actomyosin wave dynamics reveals mechanics of cell motion. 2021, Pubmed
Giannone, Periodic lamellipodial contractions correlate with rearward actin waves. 2004, Pubmed
Giannone, Lamellipodial actin mechanically links myosin activity with adhesion-site formation. 2007, Pubmed
Glogauer, Two pathways through Cdc42 couple the N-formyl receptor to actin nucleation in permeabilized human neutrophils. 2000, Pubmed
Goryachev, How to make a static cytokinetic furrow out of traveling excitable waves. 2016, Pubmed
Gov, Guided by curvature: shaping cells by coupling curved membrane proteins and cytoskeletal forces. 2018, Pubmed
Graessl, An excitable Rho GTPase signaling network generates dynamic subcellular contraction patterns. 2017, Pubmed
Guetta-Terrier, Protrusive waves guide 3D cell migration along nanofibers. 2015, Pubmed
HODGKIN, A quantitative description of membrane current and its application to conduction and excitation in nerve. 1952, Pubmed
Hadjitheodorou, Directional reorientation of migrating neutrophils is limited by suppression of receptor input signaling at the cell rear through myosin II activity. 2021, Pubmed
Halatek, Self-organization principles of intracellular pattern formation. 2018, Pubmed
Helenius, Oscillatory Switches of Dorso-Ventral Polarity in Cells Confined between Two Surfaces. 2018, Pubmed
Hilgemann, Local PIP(2) signals: when, where, and how? 2007, Pubmed
Hodge, Regulating Rho GTPases and their regulators. 2016, Pubmed
Holmes, Regimes of wave type patterning driven by refractory actin feedback: transition from static polarization to dynamic wave behaviour. 2012, Pubmed
Holmes, An efficient, nonlinear stability analysis for detecting pattern formation in reaction diffusion systems. 2014, Pubmed
Holmes, Local perturbation analysis: a computational tool for biophysical reaction-diffusion models. 2015, Pubmed
Holmes, Analysis of a minimal Rho-GTPase circuit regulating cell shape. 2016, Pubmed
Holmes, A mathematical model of GTPase pattern formation during single-cell wound repair. 2016, Pubmed
Honda, Microtopographical guidance of macropinocytic signaling patches. 2021, Pubmed
Hoon, Functions and regulation of circular dorsal ruffles. 2012, Pubmed
Houk, Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration. 2012, Pubmed
Huang, An excitable signal integrator couples to an idling cytoskeletal oscillator to drive cell migration. 2013, Pubmed
Hörning, Three-Dimensional Cell Geometry Controls Excitable Membrane Signaling in Dictyostelium Cells. 2019, Pubmed
Imoto, Comparative mapping of crawling-cell morphodynamics in deep learning-based feature space. 2021, Pubmed
Inagaki, Actin Waves: Origin of Cell Polarization and Migration? 2017, Pubmed
Itoh, Mechanistic insights into the regulation of circular dorsal ruffle formation. 2013, Pubmed
Jasnin, The Architecture of Traveling Actin Waves Revealed by Cryo-Electron Tomography. 2019, Pubmed
Jiang, PI3K/PTEN signaling in tumorigenesis and angiogenesis. 2008, Pubmed
Jilkine, A comparison of mathematical models for polarization of single eukaryotic cells in response to guided cues. 2011, Pubmed
Kabsch, Structure and function of actin. 1992, Pubmed
Khamviwath, A continuum model of actin waves in Dictyostelium discoideum. 2013, Pubmed
Kholodenko, Cell-signalling dynamics in time and space. 2006, Pubmed
Killich, The locomotion, shape and pseudopodial dynamics of unstimulated Dictyostelium cells are not random. 1993, Pubmed
Knobloch, Oscillatory convection in binary mixtures. 1986, Pubmed
Knobloch, Origin of jumping oscillons in an excitable reaction-diffusion system. 2021, Pubmed
Knoch, Modeling self-organized spatio-temporal patterns of PIP₃ and PTEN during spontaneous cell polarization. 2014, Pubmed
Kobayashi, Self-organized pulse generator in a reaction-diffusion system. 1994, Pubmed
Kortholt, Highlighting the role of Ras and Rap during Dictyostelium chemotaxis. 2008, Pubmed
Kulawiak, Active poroelastic two-phase model for the motion of physarum microplasmodia. 2019, Pubmed
Kölsch, The regulation of cell motility and chemotaxis by phospholipid signaling. 2008, Pubmed
Lam Hui, Adhesion-dependent modulation of actin dynamics in Jurkat T cells. 2014, Pubmed
Landino, Rho and F-actin self-organize within an artificial cell cortex. 2021, Pubmed , Xenbase
Lange, Local Ras activation, PTEN pattern, and global actin flow in the chemotactic responses of oversized cells. 2016, Pubmed
Le Goff, Pattern Formation in Polymerizing Actin Flocks: Spirals, Spots, and Waves without Nonlinear Chemistry. 2016, Pubmed
Liu, Spots, stripes, and spiral waves in models for static and motile cells : GTPase patterns in cells. 2021, Pubmed
Lou, Myosin light chain kinase regulates cell polarization independently of membrane tension or Rho kinase. 2015, Pubmed
Lutton, Formation and closure of macropinocytic cups in Dictyostelium. 2023, Pubmed
Machacek, Morphodynamic profiling of protrusion phenotypes. 2006, Pubmed
Machesky, Signaling to actin dynamics. 1999, Pubmed
Marchesin, ARF6-JIP3/4 regulate endosomal tubules for MT1-MMP exocytosis in cancer invasion. 2015, Pubmed
Marée, Polarization and movement of keratocytes: a multiscale modelling approach. 2006, Pubmed
Marée, How cells integrate complex stimuli: the effect of feedback from phosphoinositides and cell shape on cell polarization and motility. 2012, Pubmed
Masters, F-actin waves, actin cortex disassembly and focal exocytosis driven by actin-phosphoinositide positive feedback. 2016, Pubmed
Mata, A model for intracellular actin waves explored by nonlinear local perturbation analysis. 2013, Pubmed
Meshik, Optogenetic Control of Cell Migration. 2018, Pubmed
Miao, Altering the threshold of an excitable signal transduction network changes cell migratory modes. 2017, Pubmed
Miao, Wave patterns organize cellular protrusions and control cortical dynamics. 2019, Pubmed
Michaud, Cortical excitability and cell division. 2021, Pubmed
Michaud, A versatile cortical pattern-forming circuit based on Rho, F-actin, Ect2, and RGA-3/4. 2022, Pubmed , Xenbase
Michaux, Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo. 2018, Pubmed
Millius, Neutrophils establish rapid and robust WAVE complex polarity in an actin-dependent fashion. 2009, Pubmed
Mogilner, Force generation by actin polymerization II: the elastic ratchet and tethered filaments. 2003, Pubmed
Moldenhawer, Spontaneous transitions between amoeboid and keratocyte-like modes of migration. 2022, Pubmed
Mori, Wave-pinning and cell polarity from a bistable reaction-diffusion system. 2008, Pubmed
Naoz, Cell-Substrate Patterns Driven by Curvature-Sensitive Actin Polymerization: Waves and Podosomes. 2020, Pubmed
Neilson, Chemotaxis: a feedback-based computational model robustly predicts multiple aspects of real cell behaviour. 2011, Pubmed
Newby, Quasi-steady state reduction of molecular motor-based models of directed intermittent search. 2010, Pubmed
Nishikawa, Excitable signal transduction induces both spontaneous and directional cell asymmetries in the phosphatidylinositol lipid signaling system for eukaryotic chemotaxis. 2014, Pubmed
Nobes, Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. 1995, Pubmed
Nonaka, A multiphysical model of cell migration integrating reaction-diffusion, membrane and cytoskeleton. 2011, Pubmed
O'Neill, Subcellular optogenetic inhibition of G proteins generates signaling gradients and cell migration. 2014, Pubmed
O'Neill, Subcellular optogenetic activation of Cdc42 controls local and distal signaling to drive immune cell migration. 2016, Pubmed
Orth, Get off my back! Rapid receptor internalization through circular dorsal ruffles. 2006, Pubmed
Pal, The excitable signal transduction networks: movers and shapers of eukaryotic cell migration. 2019, Pubmed
Peleg, Propagating cell-membrane waves driven by curved activators of actin polymerization. 2011, Pubmed
Plazen, Excitable dynamics in a molecularly-explicit model of cell motility: Mixed-mode oscillations and beyond. 2023, Pubmed
Plazen, Polarity and mixed-mode oscillations may underlie different patterns of cellular migration. 2023, Pubmed
Povarova, The Role of Liquid-Liquid Phase Separation in Actin Polymerization. 2023, Pubmed
Radszuweit, Intracellular mechanochemical waves in an active poroelastic model. 2013, Pubmed
Ruthel, Actin-dependent anterograde movement of growth-cone-like structures along growing hippocampal axons: a novel form of axonal transport? 1998, Pubmed
Ryan, Excitable actin dynamics in lamellipodial protrusion and retraction. 2012, Pubmed
Ryan, A review of models of fluctuating protrusion and retraction patterns at the leading edge of motile cells. 2012, Pubmed
Saito, Three-dimensional morphodynamic simulations of macropinocytic cups. 2021, Pubmed
Schroth-Diez, Propagating waves separate two states of actin organization in living cells. 2009, Pubmed
Sept, Modeling large-scale dynamic processes in the cell: polarization, waves, and division. 2014, Pubmed
Shao, Computational model for cell morphodynamics. 2010, Pubmed
Shi, Interaction of motility, directional sensing, and polarity modules recreates the behaviors of chemotaxing cells. 2013, Pubmed
Shibata, Modeling the self-organized phosphatidylinositol lipid signaling system in chemotactic cells using quantitative image analysis. 2012, Pubmed
Shibata, Intracellular encoding of spatiotemporal guidance cues in a self-organizing signaling system for chemotaxis in Dictyostelium cells. 2013, Pubmed
Shlomovitz, Membrane waves driven by actin and Myosin. 2007, Pubmed
Spiering, Dynamics of the Rho-family small GTPases in actin regulation and motility. 2011, Pubmed
Staddon, Pulsatile contractions and pattern formation in excitable actomyosin cortex. 2022, Pubmed
Stankevicins, Deterministic actin waves as generators of cell polarization cues. 2020, Pubmed
Stich, Self-organized pacemakers and bistability of pulses in an excitable medium. 2009, Pubmed
Sun, Asymmetric nanotopography biases cytoskeletal dynamics and promotes unidirectional cell guidance. 2015, Pubmed
Svitkina, Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. 1999, Pubmed , Xenbase
Swanson, Shaping cups into phagosomes and macropinosomes. 2008, Pubmed
Swider, Cell cycle and developmental control of cortical excitability in Xenopus laevis. 2022, Pubmed , Xenbase
Tamemoto, Pattern formation in reaction-diffusion system on membrane with mechanochemical feedback. 2020, Pubmed
Tamemoto, Reaction-diffusion waves coupled with membrane curvature. 2021, Pubmed
Taniguchi, Phase geometries of two-dimensional excitable waves govern self-organized morphodynamics of amoeboid cells. 2013, Pubmed
Tarama, Mechanochemical subcellular-element model of crawling cells. 2022, Pubmed
Tomba, Geometrical Determinants of Neuronal Actin Waves. 2017, Pubmed
Toriyama, Shootin1: A protein involved in the organization of an asymmetric signal for neuronal polarization. 2006, Pubmed
Tran, Bifurcation and chaos in a model of cardiac early afterdepolarizations. 2009, Pubmed
Tyson, Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. 2003, Pubmed
Van Keymeulen, To stabilize neutrophil polarity, PIP3 and Cdc42 augment RhoA activity at the back as well as signals at the front. 2006, Pubmed
Vanderlei, A computational model of cell polarization and motility coupling mechanics and biochemistry. 2011, Pubmed
Veksler, Calcium-actin waves and oscillations of cellular membranes. 2009, Pubmed
Veltman, A plasma membrane template for macropinocytic cups. 2016, Pubmed
Verkhovsky, The mechanisms of spatial and temporal patterning of cell-edge dynamics. 2015, Pubmed
Vicker, Reaction-diffusion waves of actin filament polymerization/depolymerization in Dictyostelium pseudopodium extension and cell locomotion. 2000, Pubmed
Vicker, F-actin assembly in Dictyostelium cell locomotion and shape oscillations propagates as a self-organized reaction-diffusion wave. 2002, Pubmed
Vicker, Eukaryotic cell locomotion depends on the propagation of self-organized reaction-diffusion waves and oscillations of actin filament assembly. 2002, Pubmed
Villar-Sepúlveda, conditions for Turing and wave instabilities in reaction-diffusion systems. 2023, Pubmed
Wasnik, Modeling the dynamics of dendritic actin waves in living cells. 2014, Pubmed
Watanabe, p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. 1997, Pubmed
Weiner, An actin-based wave generator organizes cell motility. 2007, Pubmed
Welch, Cellular control of actin nucleation. 2002, Pubmed
Whitelam, Transformation from spots to waves in a model of actin pattern formation. 2009, Pubmed
Winans, Waves of actin and microtubule polymerization drive microtubule-based transport and neurite growth before single axon formation. 2016, Pubmed
Wu, Calcium oscillations-coupled conversion of actin travelling waves to standing oscillations. 2013, Pubmed
Wu, Membrane shape-mediated wave propagation of cortical protein dynamics. 2018, Pubmed
Wu, Mechanobiology in cortical waves and oscillations. 2021, Pubmed
Xiong, Cells navigate with a local-excitation, global-inhibition-biased excitable network. 2010, Pubmed
Xiong, Frequency and amplitude control of cortical oscillations by phosphoinositide waves. 2016, Pubmed
Yang, Jumping solitary waves in an autonomous reaction-diffusion system with subcritical wave instability. 2006, Pubmed
Yang, Cortical waves mediate the cellular response to electric fields. 2022, Pubmed
Yao, Modulating RhoA effectors induces transitions to oscillatory and more wavelike RhoA dynamics in Caenorhabditis elegans zygotes. 2022, Pubmed
Yochelis, Generation of finite wave trains in excitable media. 2008, Pubmed
Yochelis, Origin of finite pulse trains: Homoclinic snaking in excitable media. 2015, Pubmed
Yochelis, Excitable solitons: Annihilation, crossover, and nucleation of pulses in mass-conserving activator-inhibitor media. 2020, Pubmed
Yochelis, Versatile Patterns in the Actin Cortex of Motile Cells: Self-Organized Pulses Can Coexist with Macropinocytic Ring-Shaped Waves. 2022, Pubmed
Zeng, Investigating circular dorsal ruffles through varying substrate stiffness and mathematical modeling. 2011, Pubmed
Zhan, An Excitable Ras/PI3K/ERK Signaling Network Controls Migration and Oncogenic Transformation in Epithelial Cells. 2020, Pubmed
Zmurchok, Coupling mechanical tension and GTPase signaling to generate cell and tissue dynamics. 2018, Pubmed