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Three-dimensional traction force microscopy: a new tool for quantifying cell-matrix interactions.

ABSTRACT: The interactions between biochemical processes and mechanical signaling play important roles during various cellular processes such as wound healing, embryogenesis, metastasis, and cell migration. While traditional traction force measurements have provided quantitative information about cell matrix interactions in two dimensions, recent studies have shown significant differences in the behavior and morphology of cells when placed in three-dimensional environments. Hence new quantitative experimental techniques are needed to accurately determine cell traction forces in three dimensions. Recently, two approaches both based on laser scanning confocal microscopy have emerged to address this need. This study highlights the details, implementation and advantages of such a three-dimensional imaging methodology with the capability to compute cellular traction forces dynamically during cell migration and locomotion. An application of this newly developed three-dimensional traction force microscopy (3D TFM) technique to single cell migration studies of 3T3 fibroblasts is presented to show that this methodology offers a new quantitative vantage point to investigate the three-dimensional nature of cell-ECM interactions.

SUBMITTER: Franck C

PROVIDER: S-EPMC3066163 | biostudies-literature | 2011 Mar

REPOSITORIES: biostudies-literature

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Three-dimensional traction force microscopy: a new tool for quantifying cell-matrix interactions.

Franck Christian C Maskarinec Stacey A SA Tirrell David A DA Ravichandran Guruswami G

PloS one 20110329 3

The interactions between biochemical processes and mechanical signaling play important roles during various cellular processes such as wound healing, embryogenesis, metastasis, and cell migration. While traditional traction force measurements have provided quantitative information about cell matrix interactions in two dimensions, recent studies have shown significant differences in the behavior and morphology of cells when placed in three-dimensional environments. Hence new quantitative experime ...[more]

PMID: 21468318

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Project description:Tractions exerted by cells on their surroundings play an important role in many biological processes including stem cell differentiation, tumorigenesis, cell migration, cancer metastasis, and angiogenesis. The ability to quantify these tractions is important in understanding and manipulating these processes. Three-dimensional traction force microscopy (3DTFM) provides reliable means of evaluating cellular tractions by first measuring the displacement of fluorescent beads in response to these tractions in the surrounding matrix, and then using this measurement to compute the tractions. However, most applications of 3DTFM assume that the surrounding extra-cellular matrix (ECM) is non-fibrous, despite the fact that in many natural and synthetic environments the ECM contains a significant proportion of fibrous components. Motivated by this, we develop a computational approach for determining tractions, while accounting for the fibrous nature of the ECM. In particular, we make use of a fiber-based constitutive model in which the stress contains contributions from a distribution of nonlinear elastic fibers and a hyperelastic matrix. We solve an inverse problem with the nodal values of the traction vector as unknowns, and minimize the difference between a predicted displacement field, obtained by solving the equations of equilibrium in conjunction with the fiber-based constitutive model, and the measured displacement field at the bead locations. We employ a gradient-based minimization method to solve this problem and determine the gradient efficiently by solving for the appropriate adjoint field. We apply this algorithm to problems with experimentally observed cell geometries and synthetic, albeit realistic, traction fields to gauge its sensitivity to noise, and quantify the impact of using an incorrect constitutive model: the so-called model error. We conclude that the approach is robust to noise, yielding about 10% error in tractions for 5% displacement noise. We also conclude that the impact of model error is significant, where using a nonlinear exponential hyperelastic model instead of the fiber-based model, can lead to more than 100% error in the traction field. These results underline the importance of using appropriate constitutive models in 3DTFM, especially in fibrous ECM constructs.

Dataset Information

Three-dimensional traction force microscopy: a new tool for quantifying cell-matrix interactions.

Publications

Three-dimensional traction force microscopy: a new tool for quantifying cell-matrix interactions.

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