Influence of nucleus deformability on cell entry into cylindrical structures

The mechanical properties of cell nuclei have been demonstrated to play a fundamental role in cell movement across extracellular networks and micro-channels. In this work, we focus on a mathematical description of a cell entering a cylindrical channel composed of extracellular matrix. An energetic approach is derived in order to obtain a necessary condition for which cells enter cylindrical structures. The nucleus of the cell is treated either (i) as an elastic membrane surrounding a liquid droplet or (ii) as an incompressible elastic material with Neo-Hookean constitutive equation. The results obtained highlight the importance of the interplay between mechanical deformability of the nucleus and the capability of the cell to establish adhesive bonds and generate active forces in the cytoskeleton due to myosin action.

[1]  R. Skalak,et al.  Strain energy function of red blood cell membranes. , 1973, Biophysical journal.

[2]  W. Helfrich Elastic Properties of Lipid Bilayers: Theory and Possible Experiments , 1973, Zeitschrift fur Naturforschung. Teil C: Biochemie, Biophysik, Biologie, Virologie.

[3]  R. Skalak Modelling the mechanical behavior of red blood cells. , 1973, Biorheology.

[4]  E. Evans,et al.  New membrane concept applied to the analysis of fluid shear- and micropipette-deformed red blood cells. , 1973, Biophysical journal.

[5]  R. Waugh,et al.  Elastic area compressibility modulus of red cell membrane. , 1976, Biophysical journal.

[6]  S Chien,et al.  Theoretical and experimental studies on viscoelastic properties of erythrocyte membrane. , 1978, Biophysical journal.

[7]  R. Waugh,et al.  Thermoelasticity of red blood cell membrane. , 1979, Biophysical journal.

[8]  J. Hartwig,et al.  Distribution of actin-binding protein and myosin in polymorphonuclear leukocytes during locomotion and phagocytosis , 1981, Cell.

[9]  Report From The International Symposium (Osaka). On hemorheological approach to cardiovascular diseases , 1982 .

[10]  E Evans,et al.  Passive material behavior of granulocytes based on large deformation and recovery after deformation tests. , 1984 .

[11]  R M Nerem,et al.  The application of a homogeneous half-space model in the analysis of endothelial cell micropipette measurements. , 1988, Journal of biomechanical engineering.

[12]  E. Evans,et al.  Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. , 1989, Biophysical journal.

[13]  Edward Y Lee,et al.  Synthesis and characterization of a model extracellular matrix that induces partial regeneration of adult mammalian skin. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[14]  E. Evans,et al.  Cortical shell-liquid core model for passive flow of liquid-like spherical cells into micropipets. , 1989, Biophysical journal.

[15]  Glazier,et al.  Simulation of biological cell sorting using a two-dimensional extended Potts model. , 1992, Physical review letters.

[16]  D. Ingber,et al.  Cellular tensegrity : defining new rules of biological design that govern the cytoskeleton , 2022 .

[17]  R M Hochmuth Measuring the mechanical properties of individual human blood cells. , 1993, Journal of biomechanical engineering.

[18]  W. Saltzman,et al.  Neutrophil motility in extracellular matrix gels: mesh size and adhesion affect speed of migration. , 1997, Biophysical journal.

[19]  R. D. Wood,et al.  Nonlinear Continuum Mechanics for Finite Element Analysis , 1997 .

[20]  A. Libchaber,et al.  Elasticity and Structure of Eukaryote Chromosomes Studied by Micromanipulation and Micropipette Aspiration , 1997, The Journal of cell biology.

[21]  M. Dembo,et al.  Stresses at the cell-to-substrate interface during locomotion of fibroblasts. , 1999, Biophysical journal.

[22]  W. R. Jones,et al.  Alterations in the Young's modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. , 1999, Journal of biomechanics.

[23]  R. Hochmuth,et al.  Micropipette aspiration of living cells. , 2000, Journal of biomechanics.

[24]  H Schindler,et al.  Cadherin interaction probed by atomic force microscopy. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  P. Friedl,et al.  The biology of cell locomotion within three-dimensional extracellular matrix , 2000, Cellular and Molecular Life Sciences CMLS.

[26]  N. Caille,et al.  Contribution of the nucleus to the mechanical properties of endothelial cells. , 2002, Journal of biomechanics.

[27]  D. Ingber Tensegrity I. Cell structure and hierarchical systems biology , 2003, Journal of Cell Science.

[28]  R.M. Capito,et al.  Scaffold-based articular cartilage repair , 2003, IEEE Engineering in Medicine and Biology Magazine.

[29]  P. Friedl,et al.  Tumour-cell invasion and migration: diversity and escape mechanisms , 2003, Nature Reviews Cancer.

[30]  Z. C. Tu,et al.  A geometric theory on the elasticity of bio-membranes , 2004, cond-mat/0403309.

[31]  Yiider Tseng,et al.  Intracellular mechanics of migrating fibroblasts. , 2004, Molecular biology of the cell.

[32]  F. Marga,et al.  Multiple membrane tethers probed by atomic force microscopy. , 2005, Biophysical journal.

[33]  J. Lammerding,et al.  Mechanical properties of the cell nucleus and the effect of emerin deficiency. , 2006, Biophysical journal.

[34]  Yiider Tseng,et al.  Single-molecule analysis of cadherin-mediated cell-cell adhesion , 2006, Journal of Cell Science.

[35]  Kuo-Kang Liu,et al.  Deformation behaviour of soft particles: a review , 2006 .

[36]  M. Stack,et al.  Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion , 2007, Nature Cell Biology.

[37]  Z. Ou-Yang,et al.  Elastic theory of low-dimensional continua and its applications in bio- and nano-structures (vol 5, pg 422, 2008) , 2007, 0706.0001.

[38]  Jeen-Shang Lin,et al.  Cell traction force and measurement methods , 2007, Biomechanics and modeling in mechanobiology.

[39]  Luigi Preziosi,et al.  Modeling cell movement in anisotropic and heterogeneous network tissues , 2007, Networks Heterog. Media.

[40]  Ashkan Vaziri,et al.  Mechanics and deformation of the nucleus in micropipette aspiration experiment. , 2007, Journal of biomechanics.

[41]  Erik Sahai,et al.  Illuminating the metastatic process , 2007, Nature Reviews Cancer.

[42]  Peter Friedl,et al.  Proteolytic interstitial cell migration: a five-step process , 2009, Cancer and Metastasis Reviews.

[43]  Peter Friedl,et al.  Interstitial leukocyte migration and immune function , 2008, Nature Immunology.

[44]  M. Sixt,et al.  Rapid leukocyte migration by integrin-independent flowing and squeezing , 2008, Nature.

[45]  Christopher Beadle,et al.  The role of myosin II in glioma invasion of the brain. , 2008, Molecular biology of the cell.

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

[47]  Douglas A Lauffenburger,et al.  Microarchitecture of three-dimensional scaffolds influences cell migration behavior via junction interactions. , 2008, Biophysical journal.

[48]  Luigi Preziosi,et al.  Review: Rheological properties of biological materials , 2009 .

[49]  Stefan Schinkinger,et al.  The regulatory role of cell mechanics for migration of differentiating myeloid cells , 2009, Proceedings of the National Academy of Sciences.

[50]  Stephen J. Weiss,et al.  Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited , 2009, The Journal of cell biology.

[51]  K. Painter Modelling cell migration strategies in the extracellular matrix , 2009, Journal of mathematical biology.

[52]  J. Joanny,et al.  Pushing off the walls: a mechanism of cell motility in confinement. , 2009, Physical review letters.

[53]  C. Verdier,et al.  Traction patterns of tumor cells , 2009, Journal of mathematical biology.

[54]  Jacco van Rheenen,et al.  Collagen-based cell migration models in vitro and in vivo. , 2009, Seminars in cell & developmental biology.

[55]  Wesley R. Legant,et al.  Measurement of mechanical tractions exerted by cells in three-dimensional matrices , 2010, Nature Methods.

[56]  M. Sixt,et al.  Mechanisms of force generation and force transmission during interstitial leukocyte migration , 2010, EMBO reports.

[57]  Aymen Laadhari,et al.  On the equilibrium equation for a generalized biological membrane energy by using a shape optimization approach , 2010 .

[58]  H. Frieboes,et al.  Nonlinear modelling of cancer: bridging the gap between cells and tumours , 2010, Nonlinearity.

[59]  Jochen Guck,et al.  Critical review: cellular mechanobiology and amoeboid migration. , 2010, Integrative biology : quantitative biosciences from nano to macro.

[60]  Claudio G. Rolli,et al.  Impact of Tumor Cell Cytoskeleton Organization on Invasiveness and Migration: A Microchannel-Based Approach , 2010, PloS one.

[61]  Jan Lammerding,et al.  Nuclear mechanics during cell migration. , 2011, Current opinion in cell biology.

[62]  G. Gerlitz,et al.  The role of chromatin structure in cell migration. , 2011, Trends in cell biology.

[63]  P. Friedl,et al.  Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. , 2011, Trends in cell biology.

[64]  L. Preziosi,et al.  Mechanics of tumor growth: Multiphase models, adhesion, and evolving configurations , 2011 .

[65]  L. Preziosi,et al.  Mechanical aspects of tumour growth: Multiphase modelling, adhesion, and evolving natural configurations , 2011 .

[66]  Frank Janssens,et al.  Surface Area and Curvature of the General Ellipsoid , 2011, 1104.5145.

[67]  Sylvain Gabriele,et al.  Spatial coordination between cell and nuclear shape within micropatterned endothelial cells , 2012, Nature Communications.

[68]  L. Preziosi,et al.  A numerical method for the inverse problem of cell traction in 3D , 2012 .

[69]  L. Preziosi,et al.  Modeling the influence of nucleus elasticity on cell invasion in fiber networks and microchannels. , 2013, Journal of theoretical biology.

[70]  Luigi Preziosi,et al.  Time‐dependent traction force microscopy for cancer cells as a measure of invasiveness , 2013, Cytoskeleton.

[71]  L. Preziosi,et al.  A Cellular Potts Model simulating cell migration on and in matrix environments. , 2012, Mathematical biosciences and engineering : MBE.