The Balance between Actomyosin Contractility and Microtubule Polymerization Regulates Hierarchical Protrusions That Govern Efficient Fibroblast-Collagen Interactions

Delaram Shakiba, Farid Alisafaei, Alireza Savadipour, Roger A. Rowe, Zhangao Liu, Kenneth M. Pryse, Vivek B. Shenoy, Elliot L. Elson, Guy M. Genin

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Fibroblasts undergo a critical transformation from an initially inactive state to a morphologically different and contractile state after several hours of being embedded within a physiologically relevant three-dimensional (3D) fibrous collagen-based extracellular matrix (ECM). However, little is known about the critical mechanisms by which fibroblasts adapt themselves and their microenvironment in the earliest stage of cell-matrix interaction. Here, we identified the mechanisms by which fibroblasts interact with their 3D collagen fibrous matrices in the early stages of cell-matrix interaction and showed that fibroblasts use energetically efficient hierarchical micro/nano-scaled protrusions in these stages as the primary means for the transformation and adaptation. We found that actomyosin contractility in these protrusions in the early stages of cell-matrix interaction restricts the growth of microtubules by applying compressive forces on them. Our results show that actomyosin contractility and microtubules work in concert in the early stages of cell-matrix interaction to adapt fibroblasts and their microenvironment to one another. These early stage interactions result in responses to disruption of the microtubule network and/or actomyosin contractility that are opposite to well-known responses to late-stage disruption and reveal insight into the ways that cells adapt themselves and their ECM recursively.

Original languageEnglish
Pages (from-to)7868-7879
Number of pages12
JournalACS nano
Volume14
Issue number7
DOIs
StatePublished - Jul 28 2020

Keywords

  • cell protrusion
  • cell−matrix early interaction
  • collagen remodeling
  • dendritic morphology
  • fibrous traction force microscopy

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