Front-Rear Polarization by Mechanical Cues: From Single Cells to Tissues.

Directed cell migration is a complex process that involves front-rear polarization, characterized by cell adhesion and cytoskeleton-based protrusion, retraction, and contraction of either a single cell or a cell collective. Single cell polarization depends on a variety of mechanochemical signals including external adhesive cues, substrate stiffness, and confinement. In cell ensembles, coordinated polarization of migrating tissues results not only from the application of traction forces on the extracellular matrix but also from the transmission of mechanical stress through intercellular junctions. We focus here on the impact of mechanical cues on the establishment and maintenance of front-rear polarization from single cell to collective cell behaviors through local or large-scale mechanisms.

[1]  Felix Oswald,et al.  Forces Driving Epithelial Spreading in Zebrafish Gastrulation , 2012, Science.

[2]  I. Dupin,et al.  Classical cadherins control nucleus and centrosome position and cell polarity , 2009, The Journal of cell biology.

[3]  L. Addadi,et al.  Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates , 2001, Nature Cell Biology.

[4]  P. Chavrier,et al.  Collective migration of an epithelial monolayer in response to a model wound , 2007, Proceedings of the National Academy of Sciences.

[5]  Srivatsan Raghavan,et al.  Cell polarity triggered by cell-cell adhesion via E-cadherin , 2009, Journal of Cell Science.

[6]  Z. Kam,et al.  Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing , 2011, Nature Cell Biology.

[7]  G. Wayne Brodland,et al.  Forces driving epithelial wound healing , 2014, Nature Physics.

[8]  Daniel M. Suter,et al.  Transmission of growth cone traction force through apCAM–cytoskeletal linkages is regulated by Src family tyrosine kinase activity , 2001, The Journal of cell biology.

[9]  Michael P. Sheetz,et al.  Force Sensing by Mechanical Extension of the Src Family Kinase Substrate p130Cas , 2006, Cell.

[10]  A. Bershadsky,et al.  Lamellipodium extension and cadherin adhesion: two cell responses to cadherin activation relying on distinct signalling pathways , 2004, Journal of Cell Science.

[11]  Nicolas Biais,et al.  Integrin-dependent force transmission to the extracellular matrix by α-actinin triggers adhesion maturation , 2013, Proceedings of the National Academy of Sciences.

[12]  C. Lim,et al.  Adaptive rheology and ordering of cell cytoskeleton govern matrix rigidity sensing , 2015, Nature Communications.

[13]  Jie Yan,et al.  Force-dependent conformational switch of α-catenin controls vinculin binding , 2014, Nature Communications.

[14]  M. Poujade,et al.  Velocity fields in a collectively migrating epithelium. , 2010, Biophysical journal.

[15]  Gabriel Fenteany,et al.  Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets , 2000, Current Biology.

[16]  Alain Richert,et al.  Real-time single-cell response to stiffness , 2010, Proceedings of the National Academy of Sciences.

[17]  W. Nelson,et al.  Remodeling epithelial cell organization: transitions between front-rear and apical-basal polarity. , 2009, Cold Spring Harbor perspectives in biology.

[18]  U. Schwarz,et al.  Cell organization in soft media due to active mechanosensing , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Xingyu Jiang,et al.  Directing cell migration with asymmetric micropatterns. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  O. Pertz,et al.  SrGAP2-Dependent Integration of Membrane Geometry and Slit-Robo-Repulsive Cues Regulates Fibroblast Contact Inhibition of Locomotion. , 2015, Developmental cell.

[21]  M. Dembo,et al.  Cell movement is guided by the rigidity of the substrate. , 2000, Biophysical journal.

[22]  Eshel Ben-Jacob,et al.  Polarity mechanisms such as contact inhibition of locomotion regulate persistent rotational motion of mammalian cells on micropatterns , 2014, Proceedings of the National Academy of Sciences.

[23]  P. Janmey,et al.  Tissue Cells Feel and Respond to the Stiffness of Their Substrate , 2005, Science.

[24]  J. Fredberg,et al.  Collective cell guidance by cooperative intercellular forces , 2010 .

[25]  J. Fredberg,et al.  Glass-like dynamics of collective cell migration , 2011, Proceedings of the National Academy of Sciences.

[26]  Viola Vogel,et al.  Spatial distribution of cell–cell and cell–ECM adhesions regulates force balance while maintaining E-cadherin molecular tension in cell pairs , 2015, Molecular biology of the cell.

[27]  Julien Colombelli,et al.  Pulsed Forces Timed by a Ratchet-like Mechanism Drive Directed Tissue Movement during Dorsal Closure , 2009, Cell.

[28]  A. Turing.  The chemical basis of morphogenesis , 1990 .

[29]  Miguel Vicente-Manzanares,et al.  Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells , 2007, The Journal of cell biology.

[30]  G. Danuser,et al.  Substrate stiffness regulates cadherin-dependent collective migration through myosin-II contractility , 2012, The Journal of cell biology.

[31]  P. Friedl,et al.  Collective cell migration: guidance principles and hierarchies. , 2015, Trends in cell biology.

[32]  Shereen R Kadir,et al.  Competition amongst Eph receptors regulates contact inhibition of locomotion and invasiveness in prostate cancer cells , 2010, Nature Cell Biology.

[33]  C. Waterman-Storer,et al.  Spatiotemporal Feedback between Actomyosin and Focal-Adhesion Systems Optimizes Rapid Cell Migration , 2006, Cell.

[34]  Benjamin Geiger,et al.  Dynamics and segregation of cell–matrix adhesions in cultured fibroblasts , 2000, Nature Cell Biology.

[35]  D. Discher,et al.  Optimal matrix rigidity for stress fiber polarization in stem cells. , 2010, Nature physics.

[36]  Philippe Marcq,et al.  Rigidity sensing explained by active matter theory. , 2011, Biophysical journal.

[37]  Ben Fabry,et al.  Linear and Nonlinear Rheology of Living Cells , 2011 .

[38]  Michael P. Sheetz,et al.  Stretching Single Talin Rod Molecules Activates Vinculin Binding , 2009, Science.

[39]  Chwee Teck Lim,et al.  Emerging modes of collective cell migration induced by geometrical constraints , 2012, Proceedings of the National Academy of Sciences.

[40]  P. Hersen,et al.  Strength dependence of cadherin-mediated adhesions. , 2010, Biophysical journal.

[41]  D. Weitz,et al.  Alpha-actinin binding kinetics modulate cellular dynamics and force generation , 2015, Proceedings of the National Academy of Sciences.

[42]  Brendon M. Baker,et al.  Cell-mediated fiber recruitment drives extracellular matrix mechanosensing in engineered fibrillar microenvironments , 2015, Nature materials.

[43]  Anna Haeger,et al.  Cell jamming: collective invasion of mesenchymal tumor cells imposed by tissue confinement. , 2014, Biochimica et biophysica acta.

[44]  Samantha J. Stehbens,et al.  Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. , 2005, Molecular biology of the cell.

[45]  M. Parsons,et al.  Collective Chemotaxis Requires Contact-Dependent Cell Polarity , 2010, Developmental cell.

[46]  Gary G. Borisy,et al.  Self-polarization and directional motility of cytoplasm , 1999, Current Biology.

[47]  M. Parsons,et al.  Cadherin Switch during EMT in Neural Crest Cells Leads to Contact Inhibition of Locomotion via Repolarization of Forces , 2015, Developmental cell.

[48]  Patrick W Oakes,et al.  Spatiotemporal constraints on the force-dependent growth of focal adhesions. , 2011, Biophysical journal.

[49]  Frank Jülicher,et al.  Active gel physics , 2015, Nature Physics.

[50]  Patrick W. Oakes,et al.  Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation , 2014, Nature Communications.

[51]  David A. Weitz,et al.  Physical forces during collective cell migration , 2009 .

[52]  Hannah G. Yevick,et al.  Architecture and migration of an epithelium on a cylindrical wire , 2015, Proceedings of the National Academy of Sciences.

[53]  B. Ladoux,et al.  Adhesive interactions of N-cadherin limit the recruitment of microtubules to cell–cell contacts through organization of actomyosin , 2014, Journal of Cell Science.

[54]  Chwee Teck Lim,et al.  Guidance of collective cell migration by substrate geometry. , 2013, Integrative biology : quantitative biosciences from nano to macro.

[55]  G. Borisy,et al.  Cell Migration: Integrating Signals from Front to Back , 2003, Science.

[56]  Gareth E. Jones,et al.  Cellular signaling in macrophage migration and chemotaxis , 2000, Journal of leukocyte biology.

[57]  Dylan T Burnette,et al.  Myosin II functions in actin-bundle turnover in neuronal growth cones , 2006, Nature Cell Biology.

[58]  E. M. Terentjev,et al.  Liquid Crystal Elastomers , 2003 .

[59]  Eric Theveneau,et al.  Chase-and-run between adjacent cell populations promotes directional collective migration , 2013, Nature Cell Biology.

[60]  Sanjay Kumar,et al.  Mechanics, malignancy, and metastasis: The force journey of a tumor cell , 2009, Cancer and Metastasis Reviews.

[61]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[62]  E. Grasland-Mongrain,et al.  Orientation and polarity in collectively migrating cell structures: statics and dynamics. , 2011, Biophysical journal.

[63]  S. Ramaswamy,et al.  Hydrodynamics of soft active matter , 2013 .

[64]  S. Yonemura,et al.  α-Catenin as a tension transducer that induces adherens junction development , 2010, Nature Cell Biology.

[65]  Marion Ghibaudo,et al.  Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates , 2007, Proceedings of the National Academy of Sciences.

[66]  Tom Shemesh,et al.  Cellular chirality arising from the self-organization of the actin cytoskeleton , 2015, Nature Cell Biology.

[67]  A. Buguin,et al.  Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells , 2014, Nature Cell Biology.

[68]  Hannah G. Yevick,et al.  Perfect nematic order in confined monolayers of spindle-shaped cells. , 2014, Soft matter.

[69]  Pascal Silberzan,et al.  Is the mechanical activity of epithelial cells controlled by deformations or forces? , 2005, Biophysical journal.

[70]  J. Joanny,et al.  Generic phase diagram of active polar films. , 2006, Physical review letters.

[71]  K. Alitalo,et al.  VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia , 2003, The Journal of cell biology.

[72]  Gaudenz Danuser,et al.  Fluctuations of intracellular forces during cell protrusion , 2008, Nature Cell Biology.

[73]  Manuel Théry,et al.  Cell distribution of stress fibres in response to the geometry of the adhesive environment. , 2006, Cell motility and the cytoskeleton.

[74]  J. Fredberg,et al.  Mechanical waves during tissue expansion , 2012, Nature Physics.

[75]  D. Discher,et al.  Crawling from soft to stiff matrix polarizes the cytoskeleton and phosphoregulates myosin-II heavy chain , 2012, The Journal of cell biology.

[76]  Florian Rehfeldt,et al.  Hyaluronic acid matrices show matrix stiffness in 2D and 3D dictates cytoskeletal order and myosin-II phosphorylation within stem cells. , 2012, Integrative biology : quantitative biosciences from nano to macro.

[77]  H. Guillou,et al.  Spatial organization of the extracellular matrix regulates cell–cell junction positioning , 2012, Proceedings of the National Academy of Sciences.

[78]  Ning Wang,et al.  Local VE-cadherin mechanotransduction triggers long-ranged remodeling of endothelial monolayers , 2015, Journal of Cell Science.

[79]  Peer Bork,et al.  Luminal signalling links cell communication to tissue architecture during organogenesis , 2014, Nature.

[80]  D. Gilmour,et al.  Quantitative cell polarity imaging defines leader-to-follower transitions during collective migration and the key role of microtubule-dependent adherens junction formation , 2014, Development.

[81]  Chwee Teck Lim,et al.  Epithelial bridges maintain tissue integrity during collective cell migration. , 2014, Nature materials.

[82]  Sergey V. Plotnikov,et al.  Force Fluctuations within Focal Adhesions Mediate ECM-Rigidity Sensing to Guide Directed Cell Migration , 2012, Cell.

[83]  B. Grzybowski,et al.  Microtubule guidance tested through controlled cell geometry , 2012, Journal of Cell Science.

[84]  M. Gardel,et al.  Regulation of cell motile behavior by crosstalk between cadherin- and integrin-mediated adhesions , 2010, Proceedings of the National Academy of Sciences.

[85]  Integrins and cadherins join forces to form adhesive networks , 2011, Journal of Cell Science.

[86]  J. Klarlund.  Dual modes of motility at the leading edge of migrating epithelial cell sheets , 2012, Proceedings of the National Academy of Sciences.

[87]  J. Fredberg,et al.  Cell migration driven by cooperative substrate deformation patterns. , 2010, Physical review letters.

[88]  Marco Antunes,et al.  Coordinated waves of actomyosin flow and apical cell constriction immediately after wounding , 2013, The Journal of cell biology.

[89]  Léa Trichet,et al.  Evidence of a large-scale mechanosensing mechanism for cellular adaptation to substrate stiffness , 2012, Proceedings of the National Academy of Sciences.

[90]  F. Raynaud,et al.  Minimal model for spontaneous cell polarization and edge activity in oscillating, rotating and migrating cells , 2016, Nature Physics.

[91]  D. Leckband,et al.  N-cadherin regulates spatially polarized signals through distinct p120ctn and β-catenin-dependent signaling pathways , 2013, Nature Communications.

[92]  E. Rosten,et al.  Emergence of embryonic pattern through contact inhibition of locomotion , 2012, Development.

[93]  M. Abercrombie,et al.  Observations on the social behaviour of cells in tissue culture. I. Speed of movement of chick heart fibroblasts in relation to their mutual contacts. , 1953, Experimental cell research.

[94]  M. Sheetz,et al.  Talin depletion reveals independence of initial cell spreading from integrin activation and traction , 2008, Nature Cell Biology.

[95]  Paul Martin,et al.  Actin cables and epidermal movement in embryonic wound healing , 1992, Nature.

[96]  A. Kabla,et al.  Gap geometry dictates epithelial closure efficiency , 2015, Nature Communications.

[97]  A. Mogilner,et al.  Protrusive waves guide 3D cell migration along nanofibers , 2015, The Journal of cell biology.

[98]  J. Rädler,et al.  Phenomenological approaches to collective behavior in epithelial cell migration. , 2015, Biochimica et biophysica acta.

[99]  Joachim P. Spatz,et al.  A molecular mechanotransduction pathway regulates collective migration of epithelial cells , 2015, Nature Cell Biology.

[100]  M. Miodownik,et al.  Inter-Cellular Forces Orchestrate Contact Inhibition of Locomotion , 2015, Cell.

[101]  M. Takeichi,et al.  Emerging roles of protocadherins: from self‐avoidance to enhancement of motility , 2015, Journal of Cell Science.