Tethering Cells via Enzymatic Oxidative Crosslinking Enables Mechanotransduction in Non-Cell-Adhesive Materials

Adv Mater. 2021 Oct;33(42):e2102660. doi: 10.1002/adma.202102660. Epub 2021 Sep 3.

Abstract

Cell-matrix interactions govern cell behavior and tissue function by facilitating transduction of biomechanical cues. Engineered tissues often incorporate these interactions by employing cell-adhesive materials. However, using constitutively active cell-adhesive materials impedes control over cell fate and elicits inflammatory responses upon implantation. Here, an alternative cell-material interaction strategy that provides mechanotransducive properties via discrete inducible on-cell crosslinking (DOCKING) of materials, including those that are inherently non-cell-adhesive, is introduced. Specifically, tyramine-functionalized materials are tethered to tyrosines that are naturally present in extracellular protein domains via enzyme-mediated oxidative crosslinking. Temporal control over the stiffness of on-cell tethered 3D microniches reveals that DOCKING uniquely enables lineage programming of stem cells by targeting adhesome-related mechanotransduction pathways acting independently of cell volume changes and spreading. In short, DOCKING represents a bioinspired and cytocompatible cell-tethering strategy that offers new routes to study and engineer cell-material interactions, thereby advancing applications ranging from drug delivery, to cell-based therapy, and cultured meat.

Keywords: adhesomes; biomechanics; cell volume; inflammation; lineage commitment; single-cell analysis; stem cell microniches.

MeSH terms

  • Animals
  • Biocompatible Materials / chemistry*
  • Biocompatible Materials / metabolism
  • Biocompatible Materials / pharmacology
  • Cell Adhesion / drug effects
  • Cell Differentiation / drug effects
  • Cell Lineage
  • Dextrans / chemistry
  • Horseradish Peroxidase / metabolism
  • Humans
  • Hydrogels / chemistry
  • Integrins / metabolism
  • Mechanotransduction, Cellular* / drug effects
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Oligopeptides / chemistry
  • Oxidation-Reduction
  • Tyramine / chemistry

Substances

  • Biocompatible Materials
  • Dextrans
  • Hydrogels
  • Integrins
  • Oligopeptides
  • arginyl-glycyl-aspartic acid
  • Horseradish Peroxidase
  • Tyramine