mTOR signaling promotes stem cell activation via counterbalancing BMP-mediated suppression during hair regeneration

J Mol Cell Biol. 2015 Feb;7(1):62-72. doi: 10.1093/jmcb/mjv005. Epub 2015 Jan 20.

Abstract

Hair follicles (HFs) undergo cycles of degeneration (catagen), rest (telogen), and regeneration (anagen) phases. Anagen begins when the hair follicle stem cells (HFSCs) obtain sufficient activation cues to overcome suppressive signals, mainly the BMP pathway, from their niche cells. Here, we unveil that mTOR complex 1 (mTORC1) signaling is activated in HFSCs, which coincides with the HFSC activation at the telogen-to-anagen transition. By using both an inducible conditional gene targeting strategy and a pharmacological inhibition method to ablate or inhibit mTOR signaling in adult skin epithelium before anagen initiation, we demonstrate that HFs that cannot respond to mTOR signaling display significantly delayed HFSC activation and extended telogen. Unexpectedly, BMP signaling activity is dramatically prolonged in mTOR signaling-deficient HFs. Through both gain- and loss-of-function studies in vitro, we show that mTORC1 signaling negatively affects BMP signaling, which serves as a main mechanism whereby mTORC1 signaling facilitates HFSC activation. Indeed, in vivo suppression of BMP by its antagonist Noggin rescues the HFSC activation defect in mTORC1-null skin. Our findings reveal a critical role for mTOR signaling in regulating stem cell activation through counterbalancing BMP-mediated repression during hair regeneration.

Keywords: BMP; hair follicle; mTOR; skin; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Morphogenetic Proteins / antagonists & inhibitors
  • Bone Morphogenetic Proteins / metabolism*
  • Carrier Proteins / pharmacology
  • Hair
  • Hair Follicle / physiology*
  • Humans
  • Mice
  • Mice, Knockout
  • Regeneration*
  • Signal Transduction* / drug effects
  • Stem Cells / drug effects
  • Stem Cells / metabolism*
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / metabolism*

Substances

  • Bone Morphogenetic Proteins
  • Carrier Proteins
  • noggin protein
  • TOR Serine-Threonine Kinases