Mechanisms of Plastic Deformation in Collagen Networks Induced by Cellular Forces

Ehsan Ban, J. Matthew Franklin, Sungmin Nam, Lucas R. Smith, Hailong Wang, Rebecca G. Wells, Ovijit Chaudhuri, Jan T. Liphardt, Vivek B. Shenoy

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

Contractile cells can reorganize fibrous extracellular matrices and form dense tracts of fibers between neighboring cells. These tracts guide the development of tubular tissue structures and provide paths for the invasion of cancer cells. Here, we studied the mechanisms of the mechanical plasticity of collagen tracts formed by contractile premalignant acinar cells and fibroblasts. Using fluorescence microscopy and second harmonic generation, we quantified the collagen densification, fiber alignment, and strains that remain within the tracts after cellular forces are abolished. We explained these observations using a theoretical fiber network model that accounts for the stretch-dependent formation of weak cross-links between nearby fibers. We tested the predictions of our model using shear rheology experiments. Both our model and rheological experiments demonstrated that increasing collagen concentration leads to substantial increases in plasticity. We also considered the effect of permanent elongation of fibers on network plasticity and derived a phase diagram that classifies the dominant mechanisms of plasticity based on the rate and magnitude of deformation and the mechanical properties of individual fibers. Plasticity is caused by the formation of new cross-links if moderate strains are applied at small rates or due to permanent fiber elongation if large strains are applied over short periods. Finally, we developed a coarse-grained model for plastic deformation of collagen networks that can be employed to simulate multicellular interactions in processes such as morphogenesis, cancer invasion, and fibrosis.

Original languageEnglish (US)
Pages (from-to)450-461
Number of pages12
JournalBiophysical Journal
Volume114
Issue number2
DOIs
StatePublished - Jan 23 2018
Externally publishedYes

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Plastics
Collagen
Rheology
Acinar Cells
Morphogenesis
Fluorescence Microscopy
Extracellular Matrix
Neoplasms
Fibrosis
Fibroblasts

ASJC Scopus subject areas

  • Biophysics

Cite this

Ban, E., Franklin, J. M., Nam, S., Smith, L. R., Wang, H., Wells, R. G., ... Shenoy, V. B. (2018). Mechanisms of Plastic Deformation in Collagen Networks Induced by Cellular Forces. Biophysical Journal, 114(2), 450-461. https://doi.org/10.1016/j.bpj.2017.11.3739

Mechanisms of Plastic Deformation in Collagen Networks Induced by Cellular Forces. / Ban, Ehsan; Franklin, J. Matthew; Nam, Sungmin; Smith, Lucas R.; Wang, Hailong; Wells, Rebecca G.; Chaudhuri, Ovijit; Liphardt, Jan T.; Shenoy, Vivek B.

In: Biophysical Journal, Vol. 114, No. 2, 23.01.2018, p. 450-461.

Research output: Contribution to journalArticle

Ban, E, Franklin, JM, Nam, S, Smith, LR, Wang, H, Wells, RG, Chaudhuri, O, Liphardt, JT & Shenoy, VB 2018, 'Mechanisms of Plastic Deformation in Collagen Networks Induced by Cellular Forces', Biophysical Journal, vol. 114, no. 2, pp. 450-461. https://doi.org/10.1016/j.bpj.2017.11.3739
Ban, Ehsan ; Franklin, J. Matthew ; Nam, Sungmin ; Smith, Lucas R. ; Wang, Hailong ; Wells, Rebecca G. ; Chaudhuri, Ovijit ; Liphardt, Jan T. ; Shenoy, Vivek B. / Mechanisms of Plastic Deformation in Collagen Networks Induced by Cellular Forces. In: Biophysical Journal. 2018 ; Vol. 114, No. 2. pp. 450-461.
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