Axin2 marks quiescent hair follicle bulge stem cells that are maintained by autocrine Wnt/β-catenin signaling

Proc Natl Acad Sci U S A. 2016 Mar 15;113(11):E1498-505. doi: 10.1073/pnas.1601599113. Epub 2016 Feb 22.

Abstract

How stem cells maintain their identity and potency as tissues change during growth is not well understood. In mammalian hair, it is unclear how hair follicle stem cells can enter an extended period of quiescence during the resting phase but retain stem cell potential and be subsequently activated for growth. Here, we use lineage tracing and gene expression mapping to show that the Wnt target gene Axin2 is constantly expressed throughout the hair cycle quiescent phase in outer bulge stem cells that produce their own Wnt signals. Ablating Wnt signaling in the bulge cells causes them to lose their stem cell potency to contribute to hair growth and undergo premature differentiation instead. Bulge cells express secreted Wnt inhibitors, including Dickkopf (Dkk) and secreted frizzled-related protein 1 (Sfrp1). However, the Dickkopf 3 (Dkk3) protein becomes localized to the Wnt-inactive inner bulge that contains differentiated cells. We find that Axin2 expression remains confined to the outer bulge, whereas Dkk3 continues to be localized to the inner bulge during the hair cycle growth phase. Our data suggest that autocrine Wnt signaling in the outer bulge maintains stem cell potency throughout hair cycle quiescence and growth, whereas paracrine Wnt inhibition of inner bulge cells reinforces differentiation.

Keywords: Wnt signaling; hair follicle; homeostasis; regeneration; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Autocrine Communication
  • Axin Protein / genetics
  • Axin Protein / metabolism*
  • Gene Expression Regulation
  • Hair Follicle / cytology*
  • Hair Follicle / metabolism
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice, Mutant Strains
  • Mice, Transgenic
  • Stem Cells / cytology
  • Stem Cells / metabolism*
  • Wnt Proteins / genetics
  • Wnt Proteins / metabolism
  • Wnt Signaling Pathway / physiology*
  • beta Catenin / genetics
  • beta Catenin / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Axin Protein
  • Axin2 protein, mouse
  • CTNNB1 protein, mouse
  • Dkk3 protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Sfrp1 protein, mouse
  • Wnt Proteins
  • beta Catenin