Fractal heterogeneity in minimal matrix models of scars modulates stiff-niche stem-cell responses via nuclear exit of a mechanorepressor

P. C.Dave P. Dingal, Andrew M. Bradshaw, Sangkyun Cho, Matthew Raab, Amnon Buxboim, Joe Swift, Dennis E. Discher

Research output: Contribution to journalArticlepeer-review

Abstract

Scarring is a long-lasting problem in higher animals, and reductionist approaches could aid in developing treatments. Here, we show that copolymerization of collagen I with polyacrylamide produces minimal matrix models of scars (MMMS), in which fractal-fibre bundles segregate heterogeneously to the hydrogel subsurface. Matrix stiffens locally - as in scars - while allowing separate control over adhesive-ligand density. The MMMS elicits scar-like phenotypes from mesenchymal stem cells (MSCs): cells spread and polarize quickly, increasing nucleoskeletal lamin-A yet expressing the â scar markerâ €™ smooth muscle actin (SMA) more slowly. Surprisingly, expression responses to MMMS exhibit less cell-to-cell noise than homogeneously stiff gels. Such differences from bulk-average responses arise because a strong SMA repressor, NKX2.5, slowly exits the nucleus on rigid matrices. NKX2.5 overexpression overrides rigid phenotypes, inhibiting SMA and cell spreading, whereas cytoplasm-localized NKX2.5 mutants degrade in well-spread cells. MSCs thus form a â mechanical memoryâ €™ of rigidity by progressively suppressing NKX2.5, thereby elevating SMA in a scar-like state.

Original languageEnglish
Pages (from-to)951-960
Number of pages10
JournalNature Materials
Volume14
Issue number9
DOIs
StatePublished - 21 Sep 2015
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • General Chemistry
  • General Materials Science
  • Condensed Matter Physics
  • Mechanics of Materials
  • Mechanical Engineering

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