Fiber alignment in 3D collagen networks as a biophysical marker for cell contractility
Cells cultured in 3D fibrous biopolymer matrices exert traction forces on their environment that induce deformations and remodeling of the fiber network. By measuring these deformations, the traction forces can be reconstructed if the mechanical properties of the matrix and the force-free matrix con...
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| Published in | Matrix biology Vol. 124; pp. 39 - 48 |
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| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
01.12.2023
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Cells cultured in 3D fibrous biopolymer matrices exert traction forces on their environment that induce deformations and remodeling of the fiber network. By measuring these deformations, the traction forces can be reconstructed if the mechanical properties of the matrix and the force-free matrix configuration are known. These requirements limit the applicability of traction force reconstruction in practice. In this study, we test whether force-induced matrix remodeling can instead be used as a proxy for cellular traction forces. We measure the traction forces of hepatic stellate cells and different glioblastoma cell lines and quantify matrix remodeling by measuring the fiber orientation and fiber density around these cells. In agreement with simulated fiber networks, we demonstrate that changes in local fiber orientation and density are directly related to cell forces. By resolving Rho-kinase (ROCK) inhibitor-induced changes of traction forces, fiber alignment, and fiber density in hepatic stellate cells, we show that the method is suitable for drug screening assays. We conclude that differences in local fiber orientation and density, which are easily measurable, can be used as a qualitative proxy for changes in traction forces. The method is available as an open-source Python package with a graphical user interface. |
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| AbstractList | Cells cultured in 3D fibrous biopolymer matrices exert traction forces on their environment that induce deformations and remodeling of the fiber network. By measuring these deformations, the traction forces can be reconstructed if the mechanical properties of the matrix and the force-free matrix configuration are known. These requirements limit the applicability of traction force reconstruction in practice. In this study, we test whether force-induced matrix remodeling can instead be used as a proxy for cellular traction forces. We measure the traction forces of hepatic stellate cells and different glioblastoma cell lines and quantify matrix remodeling by measuring the fiber orientation and fiber density around these cells. In agreement with simulated fiber networks, we demonstrate that changes in local fiber orientation and density are directly related to cell forces. By resolving Rho-kinase (ROCK) inhibitor-induced changes of traction forces, fiber alignment, and fiber density in hepatic stellate cells, we show that the method is suitable for drug screening assays. We conclude that differences in local fiber orientation and density, which are easily measurable, can be used as a qualitative proxy for changes in traction forces. The method is available as an open-source Python package with a graphical user interface.Cells cultured in 3D fibrous biopolymer matrices exert traction forces on their environment that induce deformations and remodeling of the fiber network. By measuring these deformations, the traction forces can be reconstructed if the mechanical properties of the matrix and the force-free matrix configuration are known. These requirements limit the applicability of traction force reconstruction in practice. In this study, we test whether force-induced matrix remodeling can instead be used as a proxy for cellular traction forces. We measure the traction forces of hepatic stellate cells and different glioblastoma cell lines and quantify matrix remodeling by measuring the fiber orientation and fiber density around these cells. In agreement with simulated fiber networks, we demonstrate that changes in local fiber orientation and density are directly related to cell forces. By resolving Rho-kinase (ROCK) inhibitor-induced changes of traction forces, fiber alignment, and fiber density in hepatic stellate cells, we show that the method is suitable for drug screening assays. We conclude that differences in local fiber orientation and density, which are easily measurable, can be used as a qualitative proxy for changes in traction forces. The method is available as an open-source Python package with a graphical user interface. Cells cultured in 3D fibrous biopolymer matrices exert traction forces on their environment that induce deformations and remodeling of the fiber network. By measuring these deformations, the traction forces can be reconstructed if the mechanical properties of the matrix and the force-free matrix configuration are known. These requirements limit the applicability of traction force reconstruction in practice. In this study, we test whether force-induced matrix remodeling can instead be used as a proxy for cellular traction forces. We measure the traction forces of hepatic stellate cells and different glioblastoma cell lines and quantify matrix remodeling by measuring the fiber orientation and fiber density around these cells. In agreement with simulated fiber networks, we demonstrate that changes in local fiber orientation and density are directly related to cell forces. By resolving Rho-kinase (ROCK) inhibitor-induced changes of traction forces, fiber alignment, and fiber density in hepatic stellate cells, we show that the method is suitable for drug screening assays. We conclude that differences in local fiber orientation and density, which are easily measurable, can be used as a qualitative proxy for changes in traction forces. The method is available as an open-source Python package with a graphical user interface. Cells cultured in 3D fibrous biopolymer matrices exert traction forces on their environment that induce deformations and remodeling of the fiber network. By measuring these deformations, the traction forces can be reconstructed if the mechanical properties of the matrix and the force-free matrix configuration are known. These requirements severely limit the applicability of traction force reconstruction in practice. In this study, we test whether force-induced matrix remodeling can instead be used as a proxy for cellular traction forces. We measure the traction forces of hepatic stellate cells and different glioblastoma cell lines and quantify matrix remodeling by measuring the fiber orientation and fiber density around these cells. In agreement with simulated fiber networks, we demonstrate that changes in local fiber orientation and density are directly related to cell forces. By resolving Rho-kinase (ROCK) Inhibitor-induced changes of traction forces and fiber alignment and density in hepatic stellate cells, we show that the method is suitable for drug screening assays. We conclude that differences in local fiber orientation and density, which are easily measurable, can be used as a qualitative proxy for changes in traction forces. The method is available as an open-source Python package with a graphical user interface. |
| Author | Görlach, Ekkehard Strick, Reiner Gerum, Richard Strissel, Pamela L Malandrino, Andrea Moravec, Ivana Mark, Christoph Bauer, Andreas Budday, Silvia O'Neill, Geraldine M Grundy, Thomas J Fabry, Ben Böhringer, David Bischof, Lars Rausch, Martin Mak, Michael Kah, Delf |
| AuthorAffiliation | 4 Department of Mechanical Engineering, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany 8 Department of Physics and Astronomy, York University, Toronto, Canada 1 Department of Physics, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany 2 Novartis Institutes for BioMedical Research, Basel, Switzerland 5 Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany 6 Department of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany 7 Department of Materials Science and Engineering, Universitat Politècnica de Catalunya, Barcelona, Spain 3 Children’s Cancer Research Unit, The Children’s Hospital at Westmead, University of Sydney, Australia 9 Department of Biomedical Engineering, Yale University, New Haven, USA |
| AuthorAffiliation_xml | – sequence: 0 name: 6 Department of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 0 name: 7 Department of Materials Science and Engineering, Universitat Politècnica de Catalunya, Barcelona, Spain – sequence: 0 name: 8 Department of Physics and Astronomy, York University, Toronto, Canada – sequence: 0 name: 1 Department of Physics, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 0 name: 2 Novartis Institutes for BioMedical Research, Basel, Switzerland – sequence: 0 name: 3 Children’s Cancer Research Unit, The Children’s Hospital at Westmead, University of Sydney, Australia – sequence: 0 name: 4 Department of Mechanical Engineering, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 0 name: 5 Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 0 name: 9 Department of Biomedical Engineering, Yale University, New Haven, USA |
| Author_xml | – sequence: 1 givenname: David surname: Böhringer fullname: Böhringer, David email: david.boehringer@fau.de organization: Department of Physics, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; Novartis Institutes for BioMedical Research, Basel, Switzerland. Electronic address: david.boehringer@fau.de – sequence: 2 givenname: Andreas surname: Bauer fullname: Bauer, Andreas organization: Department of Physics, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 3 givenname: Ivana surname: Moravec fullname: Moravec, Ivana organization: Novartis Institutes for BioMedical Research, Basel, Switzerland – sequence: 4 givenname: Lars surname: Bischof fullname: Bischof, Lars organization: Department of Physics, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 5 givenname: Delf surname: Kah fullname: Kah, Delf organization: Department of Physics, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 6 givenname: Christoph surname: Mark fullname: Mark, Christoph organization: Department of Physics, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 7 givenname: Thomas J surname: Grundy fullname: Grundy, Thomas J organization: Children's Cancer Research Unit, The Children's Hospital at Westmead, University of Sydney, Australia – sequence: 8 givenname: Ekkehard surname: Görlach fullname: Görlach, Ekkehard organization: Novartis Institutes for BioMedical Research, Basel, Switzerland – sequence: 9 givenname: Geraldine M surname: O'Neill fullname: O'Neill, Geraldine M organization: Children's Cancer Research Unit, The Children's Hospital at Westmead, University of Sydney, Australia – sequence: 10 givenname: Silvia surname: Budday fullname: Budday, Silvia organization: Department of Mechanical Engineering, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 11 givenname: Pamela L surname: Strissel fullname: Strissel, Pamela L organization: Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; Department of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 12 givenname: Reiner surname: Strick fullname: Strick, Reiner organization: Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany – sequence: 13 givenname: Andrea surname: Malandrino fullname: Malandrino, Andrea organization: Department of Materials Science and Engineering, Universitat Politécnica de Catalunya, Barcelona, Spain – sequence: 14 givenname: Richard surname: Gerum fullname: Gerum, Richard organization: Department of Physics, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; Department of Physics and Astronomy, York University, Toronto, Canada – sequence: 15 givenname: Michael surname: Mak fullname: Mak, Michael email: michael.mak@yale.edu organization: Department of Biomedical Engineering, Yale University, New Haven, USA. Electronic address: michael.mak@yale.edu – sequence: 16 givenname: Martin surname: Rausch fullname: Rausch, Martin organization: Novartis Institutes for BioMedical Research, Basel, Switzerland – sequence: 17 givenname: Ben surname: Fabry fullname: Fabry, Ben email: ben.fabry@fau.de organization: Department of Physics, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany. Electronic address: ben.fabry@fau.de |
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| CitedBy_id | crossref_primary_10_1016_j_isci_2024_109950 crossref_primary_10_1016_j_ceb_2024_102341 crossref_primary_10_1016_j_actbio_2024_03_028 crossref_primary_10_3390_ijms25116198 |
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| Keywords | Fiber Orientation Biopolymer Networks Mechanobiology Traction Force Microscopy |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contribution. AB, DB, MR, EG and BF developed the analysis method. AB, RG and DB developed the fiber analysis software. MM performed the fiber network simulations. IM, LB and DB and performed HSC single cell experiments. AM conducted fibrin experiments. CM, GO and TG conducted and analyzed the glioblastoma traction force experiments. SB and DB conducted the rheological measurements. RS and PS established the primary CAF cell lines. DB conducted spheroid experiments. DB conducted the data analysis. DB and DK created figures and tables. BF and DB wrote the manuscript. |
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