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Vimentin is a Key Regulator of Cell Mechanosensing Through Opposite Actions on Actomyosin and Microtubule Networks

Overview
Journal Commun Biol
Specialty Biology
Date 2024 May 29
PMID 38811770
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Abstract

The cytoskeleton is a complex network of interconnected biopolymers consisting of actin filaments, microtubules, and intermediate filaments. These biopolymers work in concert to transmit cell-generated forces to the extracellular matrix required for cell motility, wound healing, and tissue maintenance. While we know cell-generated forces are driven by actomyosin contractility and balanced by microtubule network resistance, the effect of intermediate filaments on cellular forces is unclear. Using a combination of theoretical modeling and experiments, we show that vimentin intermediate filaments tune cell stress by assisting in both actomyosin-based force transmission and reinforcement of microtubule networks under compression. We show that the competition between these two opposing effects of vimentin is regulated by the microenvironment stiffness. These results reconcile seemingly contradictory results in the literature and provide a unified description of vimentin's effects on the transmission of cell contractile forces to the extracellular matrix.

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References
1.
Chang Y, Nalbant P, Birkenfeld J, Chang Z, Bokoch G . GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol Biol Cell. 2008; 19(5):2147-53. PMC: 2366883. DOI: 10.1091/mbc.e07-12-1269. View

2.
Wiche G, Winter L . Plectin isoforms as organizers of intermediate filament cytoarchitecture. Bioarchitecture. 2011; 1(1):14-20. PMC: 3158638. DOI: 10.4161/bioa.1.1.14630. View

3.
Oakes P, Banerjee S, Marchetti M, Gardel M . Geometry regulates traction stresses in adherent cells. Biophys J. 2014; 107(4):825-33. PMC: 4142236. DOI: 10.1016/j.bpj.2014.06.045. View

4.
Mitra A, Venkatachalapathy S, Ratna P, Wang Y, Jokhun D, Shivashankar G . Cell geometry dictates TNFα-induced genome response. Proc Natl Acad Sci U S A. 2017; 114(20):E3882-E3891. PMC: 5441774. DOI: 10.1073/pnas.1618007114. View

5.
Vahabikashi A, Park C, Perkumas K, Zhang Z, Deurloo E, Wu H . Probe Sensitivity to Cortical versus Intracellular Cytoskeletal Network Stiffness. Biophys J. 2019; 116(3):518-529. PMC: 6369565. DOI: 10.1016/j.bpj.2018.12.021. View