Fibers in the Extracellular Matrix Enable Long-Range Stress Transmission between Cells

Cells can sense, signal, and organize via mechanical forces. The ability of cells to mechanically sense and respond to the presence of other cells over relatively long distances (e.g., ∼100 μm, or ∼10 cell-diameters) across extracellular matrix (ECM) has been attributed to the strain-hardening behav...

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Bibliographic Details
Published in:Biophysical journal 2013-04, Vol.104 (7), p.1410-1418
Main Authors: Ma, Xiaoyue, Schickel, Maureen E., Stevenson, Mark D., Sarang-Sieminski, Alisha L., Gooch, Keith J., Ghadiali, Samir N., Hart, Richard T.
Format: Article
Language:English
Subjects:
Animals
Biomechanical Phenomena
Biophysics
Cell Biophysics
Cells
collagen
Collagen - metabolism
extracellular matrix
Extracellular Matrix - metabolism
Fibers
Finite Element Analysis
gels
Mice
microscopy
Microscopy, Confocal
NIH 3T3 Cells
reflectance
Signal transduction
Strain hardening
Stress analysis
Stress, Mechanical
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Summary:Cells can sense, signal, and organize via mechanical forces. The ability of cells to mechanically sense and respond to the presence of other cells over relatively long distances (e.g., ∼100 μm, or ∼10 cell-diameters) across extracellular matrix (ECM) has been attributed to the strain-hardening behavior of the ECM. In this study, we explore an alternative hypothesis: the fibrous nature of the ECM makes long-range stress transmission possible and provides an important mechanism for long-range cell-cell mechanical signaling. To test this hypothesis, confocal reflectance microscopy was used to develop image-based finite-element models of stress transmission within fibroblast-seeded collagen gels. Models that account for the gel’s fibrous nature were compared with homogenous linear-elastic and strain-hardening models to investigate the mechanisms of stress propagation. Experimentally, cells were observed to compact the collagen gel and align collagen fibers between neighboring cells within 24 h. Finite-element analysis revealed that stresses generated by a centripetally contracting cell boundary are concentrated in the relatively stiff ECM fibers and are propagated farther in a fibrous matrix as compared to homogeneous linear elastic or strain-hardening materials. These results support the hypothesis that ECM fibers, especially aligned ones, play an important role in long-range stress transmission.
ISSN:0006-3495
1542-0086
DOI:10.1016/j.bpj.2013.02.017