Microscopic biophysical model of self-organization in tissue due to feedback between cell- and macroscopic-scale forces

We develop a microscopic biophysical model for self-organization and reshaping of artificial tissue, that is codriven by microscopic active forces between cells and an extracellular matrix (ECM), and macroscopic forces that develop within the tissue, finding close agreement with experiment. Microsco...

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Main Authors: J. P. Hague, P. W. Mieczkowski, C. O'Rourke, A. J. Loughlin, J. B. Phillips
Format: Article
Language:English
Published: American Physical Society 2020-11-01
Series:Physical Review Research
Online Access:http://doi.org/10.1103/PhysRevResearch.2.043217
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author J. P. Hague
P. W. Mieczkowski
C. O'Rourke
A. J. Loughlin
J. B. Phillips
author_facet J. P. Hague
P. W. Mieczkowski
C. O'Rourke
A. J. Loughlin
J. B. Phillips
author_sort J. P. Hague
collection DOAJ
description We develop a microscopic biophysical model for self-organization and reshaping of artificial tissue, that is codriven by microscopic active forces between cells and an extracellular matrix (ECM), and macroscopic forces that develop within the tissue, finding close agreement with experiment. Microscopic active forces are stimulated by μm-scale interactions between cells and the ECM within which they exist, and when large numbers of cells act together these forces drive, and are affected by, macroscopic-scale self-organization and reshaping of tissues in a feedback loop. To understand this loop, there is a need to (1) construct microscopic biophysical models that can simulate these processes for the very large number of cells found in tissues, (2) validate and calibrate those models against experimental data, and (3) understand the active feedback between cells and the extracellular matrix, and its relationship to macroscopic self-organization and reshaping of tissue. Our microscopic biophysical model consists of a contractile network representing the ECM, that interacts with a large number of cells via dipole forces, to describe macroscopic self-organization and reshaping of tissue. We solve the model using simulated annealing, finding close agreement with experiments on artificial neural tissue. We discuss the calibration of model parameters. We conclude that feedback between microscopic cell-ECM dipole interactions and tissue-scale forces is a key factor in driving macroscopic self-organization and reshaping of tissue. We discuss the application of the biophysical model to the simulation and rational design of artificial tissues.
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spelling doaj.art-e53505b5184c40b7a136d0a45f39b6452024-04-12T17:03:45ZengAmerican Physical SocietyPhysical Review Research2643-15642020-11-012404321710.1103/PhysRevResearch.2.043217Microscopic biophysical model of self-organization in tissue due to feedback between cell- and macroscopic-scale forcesJ. P. HagueP. W. MieczkowskiC. O'RourkeA. J. LoughlinJ. B. PhillipsWe develop a microscopic biophysical model for self-organization and reshaping of artificial tissue, that is codriven by microscopic active forces between cells and an extracellular matrix (ECM), and macroscopic forces that develop within the tissue, finding close agreement with experiment. Microscopic active forces are stimulated by μm-scale interactions between cells and the ECM within which they exist, and when large numbers of cells act together these forces drive, and are affected by, macroscopic-scale self-organization and reshaping of tissues in a feedback loop. To understand this loop, there is a need to (1) construct microscopic biophysical models that can simulate these processes for the very large number of cells found in tissues, (2) validate and calibrate those models against experimental data, and (3) understand the active feedback between cells and the extracellular matrix, and its relationship to macroscopic self-organization and reshaping of tissue. Our microscopic biophysical model consists of a contractile network representing the ECM, that interacts with a large number of cells via dipole forces, to describe macroscopic self-organization and reshaping of tissue. We solve the model using simulated annealing, finding close agreement with experiments on artificial neural tissue. We discuss the calibration of model parameters. We conclude that feedback between microscopic cell-ECM dipole interactions and tissue-scale forces is a key factor in driving macroscopic self-organization and reshaping of tissue. We discuss the application of the biophysical model to the simulation and rational design of artificial tissues.http://doi.org/10.1103/PhysRevResearch.2.043217
spellingShingle J. P. Hague
P. W. Mieczkowski
C. O'Rourke
A. J. Loughlin
J. B. Phillips
Microscopic biophysical model of self-organization in tissue due to feedback between cell- and macroscopic-scale forces
Physical Review Research
title Microscopic biophysical model of self-organization in tissue due to feedback between cell- and macroscopic-scale forces
title_full Microscopic biophysical model of self-organization in tissue due to feedback between cell- and macroscopic-scale forces
title_fullStr Microscopic biophysical model of self-organization in tissue due to feedback between cell- and macroscopic-scale forces
title_full_unstemmed Microscopic biophysical model of self-organization in tissue due to feedback between cell- and macroscopic-scale forces
title_short Microscopic biophysical model of self-organization in tissue due to feedback between cell- and macroscopic-scale forces
title_sort microscopic biophysical model of self organization in tissue due to feedback between cell and macroscopic scale forces
url http://doi.org/10.1103/PhysRevResearch.2.043217
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