Mouse γ-Synuclein Promoter-Mediated Gene Expression and Editing in Mammalian Retinal Ganglion Cells

J Neurosci. 2020 May 13;40(20):3896-3914. doi: 10.1523/JNEUROSCI.0102-20.2020. Epub 2020 Apr 16.

Abstract

Optic neuropathies are a group of optic nerve (ON) diseases caused by various insults including glaucoma, inflammation, ischemia, trauma, and genetic deficits, which are characterized by retinal ganglion cell (RGC) death and ON degeneration. An increasing number of genes involved in RGC intrinsic signaling have been found to be promising neural repair targets that can potentially be modulated directly by gene therapy, if we can achieve RGC specific gene targeting. To address this challenge, we first used adeno-associated virus (AAV)-mediated gene transfer to perform a low-throughput in vivo screening in both male and female mouse eyes and identified the mouse γ-synuclein (mSncg) promoter, which specifically and potently sustained transgene expression in mouse RGCs and also works in human RGCs. We further demonstrated that gene therapy that combines AAV-mSncg promoter with clustered regularly interspaced short palindromic repeats (CRISPR)/Cas9 gene editing can knock down pro-degenerative genes in RGCs and provide effective neuroprotection in optic neuropathies.SIGNIFICANCE STATEMENT Here, we present an RGC-specific promoter, mouse γ-synuclein (mSncg) promoter, and perform extensive characterization and proof-of-concept studies of mSncg promoter-mediated gene expression and clustered regularly interspaced short palindromic repeats (CRISPR)/Cas9 gene editing in RGCs in vivo To our knowledge, this is the first report demonstrating in vivo neuroprotection of injured RGCs and optic nerve (ON) by AAV-mediated CRISPR/Cas9 inhibition of genes that are critical for neurodegeneration. It represents a powerful tool to achieve RGC-specific gene modulation, and also opens up a promising gene therapy strategy for optic neuropathies, the most common form of eye diseases that cause irreversible blindness.

Keywords: AAV; CRSPR; RGC; Sncg; neuroprotection; optic nerve.

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
  • CRISPR-Cas Systems
  • Dependovirus / genetics
  • Female
  • Gene Deletion
  • Gene Expression Regulation / genetics*
  • Genetic Therapy
  • Humans
  • Induced Pluripotent Stem Cells
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Optic Nerve / pathology
  • Optic Nerve Diseases / genetics
  • Optic Nerve Diseases / therapy
  • RNA Editing / genetics*
  • Retinal Ganglion Cells / metabolism*
  • Retinal Ganglion Cells / pathology
  • Transgenes / genetics
  • gamma-Synuclein / genetics*

Substances

  • gamma-Synuclein