Reprogramming to recover youthful epigenetic information and restore vision

Nature. 2020 Dec;588(7836):124-129. doi: 10.1038/s41586-020-2975-4. Epub 2020 Dec 2.

Abstract

Ageing is a degenerative process that leads to tissue dysfunction and death. A proposed cause of ageing is the accumulation of epigenetic noise that disrupts gene expression patterns, leading to decreases in tissue function and regenerative capacity1-3. Changes to DNA methylation patterns over time form the basis of ageing clocks4, but whether older individuals retain the information needed to restore these patterns-and, if so, whether this could improve tissue function-is not known. Over time, the central nervous system (CNS) loses function and regenerative capacity5-7. Using the eye as a model CNS tissue, here we show that ectopic expression of Oct4 (also known as Pou5f1), Sox2 and Klf4 genes (OSK) in mouse retinal ganglion cells restores youthful DNA methylation patterns and transcriptomes, promotes axon regeneration after injury, and reverses vision loss in a mouse model of glaucoma and in aged mice. The beneficial effects of OSK-induced reprogramming in axon regeneration and vision require the DNA demethylases TET1 and TET2. These data indicate that mammalian tissues retain a record of youthful epigenetic information-encoded in part by DNA methylation-that can be accessed to improve tissue function and promote regeneration in vivo.

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

  • Aging / genetics*
  • Aging / physiology
  • Animals
  • Axons / physiology
  • Cell Line, Tumor
  • Cell Survival
  • Cellular Reprogramming / genetics*
  • DNA Methylation*
  • DNA-Binding Proteins / genetics
  • Dependovirus / genetics
  • Dioxygenases
  • Disease Models, Animal
  • Epigenesis, Genetic*
  • Eye* / cytology
  • Eye* / innervation
  • Eye* / pathology
  • Female
  • Genetic Vectors / genetics
  • Glaucoma / genetics
  • Glaucoma / pathology
  • Humans
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors / genetics
  • Mice
  • Mice, Inbred C57BL
  • Nerve Regeneration / genetics*
  • Octamer Transcription Factor-3 / genetics
  • Optic Nerve Injuries / genetics
  • Proto-Oncogene Proteins / genetics
  • Retinal Ganglion Cells / cytology
  • SOXB1 Transcription Factors / genetics
  • Transcriptome / genetics
  • Vision, Ocular / genetics*
  • Vision, Ocular / physiology*

Substances

  • DNA-Binding Proteins
  • KLF4 protein, human
  • Klf4 protein, mouse
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors
  • Octamer Transcription Factor-3
  • Pou5f1 protein, mouse
  • Proto-Oncogene Proteins
  • SOXB1 Transcription Factors
  • Sox2 protein, mouse
  • TET1 protein, mouse
  • Dioxygenases
  • Tet2 protein, mouse