The Fibrous Character of Pericellular Matrix Mediates Cell Mechanotransduction

Overview

Journal J Mech Phys Solids

Date 2024 Apr 1

PMID 38559448

Authors

Xiangjun Peng

Yuxuan Huang

Guy M Genin

Affiliations

Soon will be listed here.

Abstract

Cells in solid tissues sense and respond to mechanical signals that are transmitted through extracellular matrix (ECM) over distances that are many times their size. This long-range force transmission is known to arise from strain-stiffening and buckling in the collagen fiber ECM network, but must also pass through the denser pericellular matrix (PCM) that cells form by secreting and compacting nearby collagen. However, the role of the PCM in the transmission of mechanical signals is still unclear. We therefore studied an idealized computational model of cells embedded within fibrous collagen ECM and PCM. Our results suggest that the smaller network pore sizes associated with PCM attenuates tension-driven collagen-fiber alignment, undermining long-range force transmission and shielding cells from mechanical stress. However, elongation of the cell body or anisotropic cell contraction can compensate for these effects to enable long distance force transmission. Results are consistent with recent experiments that highlight an effect of PCM on shielding cells from high stresses. Results have implications for the transmission of mechanical signaling in development, wound healing, and fibrosis.

References

Babaei B, Davarian A, Lee S, Pryse K, McConnaughey W, Elson E . Remodeling by fibroblasts alters the rate-dependent mechanical properties of collagen. Acta Biomater. 2016; 37:28-37. PMC: 4890571. DOI: 10.1016/j.actbio.2016.03.034. View

Liu L, Yu H, Zhao H, Wu Z, Long Y, Zhang J . Matrix-transmitted paratensile signaling enables myofibroblast-fibroblast cross talk in fibrosis expansion. Proc Natl Acad Sci U S A. 2020; 117(20):10832-10838. PMC: 7245086. DOI: 10.1073/pnas.1910650117. View

Siadat S, Ruberti J . Mechanochemistry of collagen. Acta Biomater. 2023; 163:50-62. DOI: 10.1016/j.actbio.2023.01.025. View

Cosgrove B, Mui K, Driscoll T, Caliari S, Mehta K, Assoian R . N-cadherin adhesive interactions modulate matrix mechanosensing and fate commitment of mesenchymal stem cells. Nat Mater. 2016; 15(12):1297-1306. PMC: 5121068. DOI: 10.1038/nmat4725. View

Huang G, Li F, Zhao X, Ma Y, Li Y, Lin M . Functional and Biomimetic Materials for Engineering of the Three-Dimensional Cell Microenvironment. Chem Rev. 2017; 117(20):12764-12850. PMC: 6494624. DOI: 10.1021/acs.chemrev.7b00094. View

Saraswathibhatla A, Indana D, Chaudhuri O . Cell-extracellular matrix mechanotransduction in 3D. Nat Rev Mol Cell Biol. 2023; 24(7):495-516. PMC: 10656994. DOI: 10.1038/s41580-023-00583-1. View

Fraley S, Wu P, He L, Feng Y, Krisnamurthy R, Longmore G . Three-dimensional matrix fiber alignment modulates cell migration and MT1-MMP utility by spatially and temporally directing protrusions. Sci Rep. 2015; 5:14580. PMC: 4589685. DOI: 10.1038/srep14580. View

Nerurkar N, Baker B, Sen S, Wible E, Elliott D, Mauck R . Nanofibrous biologic laminates replicate the form and function of the annulus fibrosus. Nat Mater. 2009; 8(12):986-92. PMC: 3415301. DOI: 10.1038/nmat2558. View

Ahmadzadeh H, Webster M, Behera R, Jimenez Valencia A, Wirtz D, Weeraratna A . Modeling the two-way feedback between contractility and matrix realignment reveals a nonlinear mode of cancer cell invasion. Proc Natl Acad Sci U S A. 2017; 114(9):E1617-E1626. PMC: 5338523. DOI: 10.1073/pnas.1617037114. View

10.

Long Y, Niu Y, Liang K, Du Y . Mechanical communication in fibrosis progression. Trends Cell Biol. 2021; 32(1):70-90. DOI: 10.1016/j.tcb.2021.10.002. View

11.

Lee S, Nekouzadeh A, Butler B, Pryse K, McConnaughey W, Nathan A . Physically-induced cytoskeleton remodeling of cells in three-dimensional culture. PLoS One. 2013; 7(12):e45512. PMC: 3531413. DOI: 10.1371/journal.pone.0045512. View

12.

Chen X, Chen D, Ban E, Toussaint K, Janmey P, Wells R . Glycosaminoglycans modulate long-range mechanical communication between cells in collagen networks. Proc Natl Acad Sci U S A. 2022; 119(15):e2116718119. PMC: 9169665. DOI: 10.1073/pnas.2116718119. View

13.

Liu S, Tao R, Wang M, Tian J, Genin G, Lu T . Regulation of Cell Behavior by Hydrostatic Pressure. Appl Mech Rev. 2019; 71(4):0408031-4080313. PMC: 6808007. DOI: 10.1115/1.4043947. View

14.

Vining K, Mooney D . Mechanical forces direct stem cell behaviour in development and regeneration. Nat Rev Mol Cell Biol. 2017; 18(12):728-742. PMC: 5803560. DOI: 10.1038/nrm.2017.108. View

15.

McKinney J, Willoughby K, Liang S, ELLIS E . Stretch-induced injury of cultured neuronal, glial, and endothelial cells. Effect of polyethylene glycol-conjugated superoxide dismutase. Stroke. 1996; 27(5):934-40. DOI: 10.1161/01.str.27.5.934. View

16.

Peng X, Liu Y, He W, Hoppe E, Zhou L, Xin F . Acoustic radiation force on a long cylinder, and potential sound transduction by tomato trichomes. Biophys J. 2022; 121(20):3917-3926. PMC: 9674985. DOI: 10.1016/j.bpj.2022.08.038. View

17.

Reynolds N, McEvoy E, Ghosh S, Panadero Perez J, Neu C, McGarry P . Image-derived modeling of nucleus strain amplification associated with chromatin heterogeneity. Biophys J. 2021; 120(8):1323-1332. PMC: 8105730. DOI: 10.1016/j.bpj.2021.01.040. View

18.

ELLIS E, McKinney J, Willoughby K, Liang S, Povlishock J . A new model for rapid stretch-induced injury of cells in culture: characterization of the model using astrocytes. J Neurotrauma. 1995; 12(3):325-39. DOI: 10.1089/neu.1995.12.325. View

19.

Ronan W, Deshpande V, McMeeking R, McGarry J . Cellular contractility and substrate elasticity: a numerical investigation of the actin cytoskeleton and cell adhesion. Biomech Model Mechanobiol. 2013; 13(2):417-35. DOI: 10.1007/s10237-013-0506-z. View

20.

Alisafaei F, Moheimani H, Elson E, Genin G . A nuclear basis for mechanointelligence in cells. Proc Natl Acad Sci U S A. 2023; 120(19):e2303569120. PMC: 10175757. DOI: 10.1073/pnas.2303569120. View