Mmp14-dependent remodeling of the pericellular-dermal collagen interface governs fibroblast survival

J Cell Biol. 2024 Sep 2;223(9):e202312091. doi: 10.1083/jcb.202312091. Epub 2024 Jul 11.

Abstract

Dermal fibroblasts deposit type I collagen, the dominant extracellular matrix molecule found in skin, during early postnatal development. Coincident with this biosynthetic program, fibroblasts proteolytically remodel pericellular collagen fibrils by mobilizing the membrane-anchored matrix metalloproteinase, Mmp14. Unexpectedly, dermal fibroblasts in Mmp14-/- mice commit to a large-scale apoptotic program that leaves skin tissues replete with dying cells. A requirement for Mmp14 in dermal fibroblast survival is recapitulated in vitro when cells are embedded within, but not cultured atop, three-dimensional hydrogels of crosslinked type I collagen. In the absence of Mmp14-dependent pericellular proteolysis, dermal fibroblasts fail to trigger β1 integrin activation and instead actuate a TGF-β1/phospho-JNK stress response that leads to apoptotic cell death in vitro as well as in vivo. Taken together, these studies identify Mmp14 as a requisite cell survival factor that maintains dermal fibroblast viability in postnatal dermal tissues.

MeSH terms

  • Animals
  • Apoptosis*
  • Cell Survival*
  • Cells, Cultured
  • Collagen Type I / genetics
  • Collagen Type I / metabolism
  • Dermis / cytology
  • Dermis / metabolism
  • Extracellular Matrix / metabolism
  • Fibroblasts* / metabolism
  • Integrin beta1 / genetics
  • Integrin beta1 / metabolism
  • Matrix Metalloproteinase 14* / genetics
  • Matrix Metalloproteinase 14* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Skin / metabolism
  • Transforming Growth Factor beta1 / metabolism

Substances

  • Matrix Metalloproteinase 14
  • Mmp14 protein, mouse
  • Collagen Type I
  • Integrin beta1
  • Transforming Growth Factor beta1