Sox2 haploinsufficiency primes regeneration and Wnt responsiveness in the mouse cochlea

J Clin Invest. 2018 Apr 2;128(4):1641-1656. doi: 10.1172/JCI97248. Epub 2018 Mar 19.

Abstract

During development, Sox2 is indispensable for cell division and differentiation, yet its roles in regenerating tissues are less clear. Here, we used combinations of transgenic mouse models to reveal that Sox2 haploinsufficiency (Sox2haplo) increases rather than impairs cochlear regeneration in vivo. Sox2haplo cochleae had delayed terminal mitosis and ectopic sensory cells, yet normal auditory function. Sox2haplo amplified and expanded domains of damage-induced Atoh1+ transitional cell formation in neonatal cochlea. Wnt activation via β-catenin stabilization (β-cateninGOF) alone failed to induce proliferation or transitional cell formation. By contrast, β-cateninGOF caused proliferation when either Sox2haplo or damage was present, and transitional cell formation when both were present in neonatal, but not mature, cochlea. Mechanistically, Sox2haplo or damaged neonatal cochleae showed lower levels of Sox2 and Hes5, but not of Wnt target genes. Together, our study unveils an interplay between Sox2 and damage in directing tissue regeneration and Wnt responsiveness and thus provides a foundation for potential combinatorial therapies aimed at stimulating mammalian cochlear regeneration to reverse hearing loss in humans.

Keywords: Cell Biology; Mouse models; Mouse stem cells; Neurodegeneration; Neuroscience.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cochlea / physiology*
  • Haploinsufficiency*
  • Hearing Loss / genetics
  • Hearing Loss / metabolism
  • Hearing Loss / pathology
  • Hearing Loss / therapy
  • Humans
  • Mice
  • Mice, Transgenic
  • Regeneration*
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • SOXB1 Transcription Factors / genetics
  • SOXB1 Transcription Factors / metabolism*
  • Wnt Proteins / genetics
  • Wnt Signaling Pathway*

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Hes5 protein, mouse
  • Repressor Proteins
  • SOXB1 Transcription Factors
  • Sox2 protein, mouse
  • Wnt Proteins