Derivation and Application of Effective Interface Conditions for Continuum Mechanical Models of Cell Invasion through Thin Membranes

We consider a continuum mechanical model of cell invasion through thin membranes. The model consists of a transmission problem for cell volume fraction complemented with continuity of stresses and mass flux across the surfaces of the membranes. We reduce the original problem to a limiting transmission problem whereby each thin membrane is replaced by an effective interface, and we develop a formal asymptotic method that enables the derivation of a set of biophysically consistent transmission conditions to close the limiting problem. The formal results obtained are validated via numerical simulations showing that the relative error between the solutions to the original transmission problem and the solutions to the limiting problem vanishes when the thickness of the membranes tends to zero. In order to show potential applications of our effective interface conditions, we employ the limiting transmission problem to model cancer cell invasion through the basement membrane and the metastatic spread of ovarian carcinoma.

[1]  A. Katchalsky,et al.  Thermodynamic analysis of the permeability of biological membranes to non-electrolytes. , 1958, Biochimica et biophysica acta.

[2]  H. Greenspan Models for the Growth of a Solid Tumor by Diffusion , 1972 .

[3]  A. Huber,et al.  Disruption of the subendothelial basement membrane during neutrophil diapedesis in an in vitro construct of a blood vessel wall. , 1989, The Journal of clinical investigation.

[4]  Steinberg,et al.  Liquid properties of embryonic tissues: Measurement of interfacial tensions. , 1994, Physical review letters.

[5]  H M Byrne,et al.  Growth of nonnecrotic tumors in the presence and absence of inhibitors. , 1995, Mathematical biosciences.

[6]  C. Viebahn Epithelio-mesenchymal transformation during formation of the mesoderm in the mammalian embryo. , 1995, Acta anatomica.

[7]  Stephen Whitaker,et al.  Heat transfer at the boundary between a porous medium and a homogeneous fluid , 1997 .

[8]  Frédéric Valentin,et al.  Effective Boundary Conditions for Laminar Flows over Periodic Rough Boundaries , 1998 .

[9]  F. Kleinhans,et al.  Membrane permeability modeling: Kedem-Katchalsky vs a two-parameter formalism. , 1998, Cryobiology.

[10]  Stefano Lenci,et al.  Mathematical Analysis of a Bonded Joint with a Soft Thin Adhesive , 1999 .

[11]  F Reitich,et al.  Analysis of a mathematical model for the growth of tumors , 1999, Journal of mathematical biology.

[12]  H M Byrne,et al.  The influence of growth-induced stress from the surrounding medium on the development of multicell spheroids , 2001, Journal of mathematical biology.

[13]  L. Preziosi,et al.  ON THE CLOSURE OF MASS BALANCE MODELS FOR TUMOR GROWTH , 2002 .

[14]  R. Kalluri Basement membranes: structure, assembly and role in tumour angiogenesis , 2003, Nature reviews. Cancer.

[15]  R. Fässler,et al.  The role of laminin in embryonic cell polarization and tissue organization. , 2003, Developmental cell.

[16]  Jay D. Humphrey,et al.  Review Paper: Continuum biomechanics of soft biological tissues , 2003, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[17]  H. M. Byrne,et al.  Modelling the early growth of ductal carcinoma in situ of the breast , 2003, Journal of mathematical biology.

[18]  V. Cristini,et al.  Nonlinear simulation of tumor growth , 2003, Journal of mathematical biology.

[19]  H. Ammari,et al.  Reconstruction of Thin Conductivity Imperfections , 2004 .

[20]  D. McElwain,et al.  A linear-elastic model of anisotropic tumour growth , 2004, European Journal of Applied Mathematics.

[21]  D L S McElwain,et al.  A history of the study of solid tumour growth: The contribution of mathematical modelling , 2004, Bulletin of mathematical biology.

[22]  D Ambrosi,et al.  The role of stress in the growth of a multicell spheroid , 2004, Journal of mathematical biology.

[23]  G. Christofori New signals from the invasive front , 2006, Nature.

[24]  Yves Capdeboscq,et al.  Pointwise polarization tensor bounds, and applications to voltage perturbations caused by thin inhomogeneities , 2006, Asymptot. Anal..

[25]  B Ribba,et al.  A multiscale mathematical model of avascular tumor growth to investigate the therapeutic benefit of anti-invasive agents. , 2006, Journal of theoretical biology.

[26]  G. Berx,et al.  A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. , 2006, Gastroenterology.

[27]  Patrick Joly,et al.  Matching of Asymptotic Expansions for Wave Propagation in Media with Thin Slots I: The Asymptotic Expansion , 2006, Multiscale Model. Simul..

[28]  M. Quinn,et al.  Epithelial–mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: An exception to the norm , 2007, Journal of cellular physiology.

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

[30]  Andrew J Link,et al.  A proximal activator of transcription in epithelial-mesenchymal transition. , 2007, The Journal of clinical investigation.

[31]  Willi Jäger,et al.  Effective Transmission Conditions for Reaction-Diffusion Processes in Domains Separated by an Interface , 2007, SIAM J. Math. Anal..

[32]  Houssem Haddar,et al.  GENERALIZED IMPEDANCE BOUNDARY CONDITIONS FOR SCATTERING PROBLEMS FROM STRONGLY ABSORBING OBSTACLES: THE CASE OF MAXWELL'S EQUATIONS , 2008 .

[33]  S. Weiss,et al.  Breaching the basement membrane: who, when and how? , 2008, Trends in cell biology.

[34]  Luigi Preziosi,et al.  Multiphase and Multiscale Trends in Cancer Modelling , 2009 .

[35]  H. Ford,et al.  Epithelial-Mesenchymal Transition in Cancer: Parallels Between Normal Development and Tumor Progression , 2010, Journal of Mammary Gland Biology and Neoplasia.

[36]  D. Radisky,et al.  Microenvironmental Influences that Drive Progression from Benign Breast Disease to Invasive Breast Cancer , 2010, Journal of Mammary Gland Biology and Neoplasia.

[37]  Luigi Preziosi,et al.  Individual Cell-Based Model for In-Vitro Mesothelial Invasion of Ovarian Cancer , 2010 .

[38]  Frank Jülicher,et al.  Fluidization of tissues by cell division and apoptosis , 2010, Proceedings of the National Academy of Sciences.

[39]  E. Lengyel Ovarian cancer development and metastasis. , 2010, The American journal of pathology.

[40]  Gyan Bhanot,et al.  A 2D mechanistic model of breast ductal carcinoma in situ (DCIS) morphology and progression. , 2010, Journal of theoretical biology.

[41]  R. Natalini,et al.  A spatial model of cellular molecular trafficking including active transport along microtubules. , 2010, Journal of theoretical biology.

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

[43]  Frank Jülicher,et al.  Cell Flow Reorients the Axis of Planar Polarity in the Wing Epithelium of Drosophila , 2010, Cell.

[44]  M. Neuss-Radu,et al.  Multiscale analysis and simulation of a reaction–diffusion problem with transmission conditions , 2010 .

[45]  Michael Sixt,et al.  Breaching multiple barriers: leukocyte motility through venular walls and the interstitium , 2010, Nature Reviews Molecular Cell Biology.

[46]  Olga Ilina,et al.  Two-photon laser-generated microtracks in 3D collagen lattices: principles of MMP-dependent and -independent collective cancer cell invasion , 2011, Physical biology.

[47]  Erik S. Welf,et al.  Signaling pathways that control cell migration: models and analysis , 2011, Wiley interdisciplinary reviews. Systems biology and medicine.

[48]  Elliott J. Hagedorn,et al.  Cell invasion through basement membrane: the anchor cell breaches the barrier. , 2011, Current opinion in cell biology.

[49]  W. Burns,et al.  Neuroendocrine Pancreatic Tumors: Guidelines for Management and Update , 2012, Current Treatment Options in Oncology.

[50]  Hans G Othmer,et al.  The role of the microenvironment in tumor growth and invasion. , 2011, Progress in biophysics and molecular biology.

[51]  P. Friedl,et al.  Classifying collective cancer cell invasion , 2012, Nature Cell Biology.

[52]  C. Poignard Boundary layer correctors and generalized polarization tensor for periodic rough thin layers. A review for the conductivity problem , 2012 .

[53]  Houssem Haddar,et al.  Approximate models for wave propagation across thin periodic interfaces , 2012 .

[54]  Gaudenz Danuser,et al.  Mathematical modeling of eukaryotic cell migration: insights beyond experiments. , 2013, Annual review of cell and developmental biology.

[55]  A. A. Moussa,et al.  Asymptotic study of thin elastic layer , 2013 .

[56]  Patrick Joly,et al.  EFFECTIVE TRANSMISSION CONDITIONS FOR THIN-LAYER TRANSMISSION PROBLEMS IN ELASTODYNAMICS. THE CASE OF A PLANAR LAYER MODEL , 2013 .

[57]  Multicellular aggregates: a model system for tissue rheology , 2013, The European physical journal. E, Soft matter.

[58]  Guojun Sheng,et al.  EMT in developmental morphogenesis. , 2013, Cancer letters.

[59]  Hans G Othmer,et al.  A Hybrid Model of Tumor–Stromal Interactions in Breast Cancer , 2013, Bulletin of Mathematical Biology.

[60]  B. Perthame,et al.  Composite waves for a cell population system modeling tumor growth and invasion , 2013, Chinese Annals of Mathematics, Series B.

[61]  Clair Poignard,et al.  Asymptotic expansion of steady-state potential in a high contrast medium with a thin resistive layer , 2013, Appl. Math. Comput..

[62]  Robert M. Hoffman,et al.  Physical limits of cell migration: Control by ECM space and nuclear deformation and tuning by proteolysis and traction force , 2013, The Journal of cell biology.

[63]  Roberto Natalini,et al.  A spatial physiological model for p53 intracellular dynamics. , 2013, Journal of theoretical biology.

[64]  Elliott J. Hagedorn,et al.  Traversing the basement membrane in vivo: A diversity of strategies , 2014, The Journal of cell biology.

[65]  C. Giverso,et al.  Influence of nucleus deformability on cell entry into cylindrical structures , 2013, Biomechanics and Modeling in Mechanobiology.

[66]  J. Clairambault,et al.  The dynamics of p53 in single cells: physiologically based ODE and reaction–diffusion PDE models , 2014, Physical biology.

[67]  A. Vorotnikov,et al.  Chemotactic signaling in mesenchymal cells compared to amoeboid cells , 2014, Genes & diseases.

[68]  Guy Z. Ramon,et al.  The effective flux through a thin-film composite membrane , 2015 .

[69]  Luigi Preziosi,et al.  A multiphase model of tumour segregation in situ by a heterogeneous extracellular matrix , 2015 .

[70]  Keijo Mattila,et al.  Diffusion through thin membranes: Modeling across scales. , 2016, Physical review. E.

[71]  R. S. Zola,et al.  Anomalous diffusion and transport in heterogeneous systems separated by a membrane , 2016, Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[72]  Nick Jagiella,et al.  Inferring Growth Control Mechanisms in Growing Multi-cellular Spheroids of NSCLC Cells from Spatial-Temporal Image Data , 2016, PLoS Comput. Biol..

[73]  Jean-Jacques Marigo,et al.  Two-scale homogenization to determine effective parameters of thin metallic-structured films , 2016, Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[74]  Giuseppe Geymonat,et al.  Asymptotic Analysis of a Linear Isotropic Elastic Composite Reinforced by a Thin Layer of Periodically Distributed Isotropic Parallel Stiff Fibres , 2016 .

[75]  C. Giverso,et al.  On the morphological stability of multicellular tumour spheroids growing in porous media , 2016, The European physical journal. E, Soft matter.

[76]  F. Caubet,et al.  New Transmission Condition Accounting For Diffusion Anisotropy In Thin Layers Applied To Diffusion MRI , 2017 .

[77]  C. Poignard,et al.  Tumor growth model of ductal carcinoma: from in situ phase to stroma invasion. , 2017, Journal of theoretical biology.

[78]  Stefano Berrone,et al.  Flow simulations in porous media with immersed intersecting fractures , 2017, J. Comput. Phys..

[79]  Alexis Auvray,et al.  Asymptotic expansions and effective boundary conditions: a short review for smooth and nonsmooth geometries with thin layers , 2018 .

[80]  C. Giverso,et al.  How Nucleus Mechanics and ECM Microstructure Influence the Invasion of Single Cells and Multicellular Aggregates , 2017, Bulletin of Mathematical Biology.

[81]  Peter Knabner,et al.  Effective interface conditions for processes through thin heterogeneous layers with nonlinear transmission at the microscopic bulk-layer interface , 2018, Networks Heterog. Media.

[82]  Adrian Moure,et al.  Three-dimensional simulation of obstacle-mediated chemotaxis , 2018, Biomechanics and modeling in mechanobiology.

[83]  C. Giverso,et al.  Influence of the mechanical properties of the necrotic core on the growth and remodelling of tumour spheroids , 2019, International Journal of Non-Linear Mechanics.